27
THE ROLE OF SUBSTANCE P IN EARLY EXPERIMENTAL PARKINSON’S DISEASE EMMA THORNTON B.HlthSc (Hons) Discipline of Pathology, School of Medical Sciences The University of Adelaide November 2008 A thesis submitted to the University of Adelaide in partial fulfilment of the requirements for the degree of Doctor of Philosophy

THE R SUBSTANCE P IN EARLY EXPERIMENTAL · 411 Benolieil R, Tanaka M, Caudle RM, Iadarola MJ (2000) Co-localization of N-methyl-D-aspartate receptors and substance P (neurokinin-1)

  • Upload
    others

  • View
    1

  • Download
    0

Embed Size (px)

Citation preview

THE ROLE OF SUBSTANCE P IN EARLY EXPERIMENTAL

PARKINSON’S DISEASE

EMMA THORNTON

B.HlthSc (Hons)

Discipline of Pathology, School of Medical Sciences

The University of Adelaide

November 2008

A thesis submitted to the University of Adelaide in partial fulfilment of the requirements

for the degree of Doctor of Philosophy

410

REFERENCES

Aizman O, Brismar H, Uhlen P, Zettergren E, Levey AI, Forssberg H, Greengard P, Aperia A (2000) Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat Neurosci 3:226-230.

Alves G, Forsaa EB, Pedersen KF, Gjerstad MD, Larsen JP (2008) Epidemiology of

Parkinson’s disease. J Neurol 255(Suppl 5):18-32. Alves RV, Campos MM, Santos ARS, Calixto JB (1999) Receptor subtypes involved in

tachykinin-mediated edema formation. Peptides 20:921-927. Aosaki T, Kawaguchi Y (1996) Actions of substance P on rat neostriatal neurons in vitro.

J Neurosci 16:5141-5153. Arai H, Furuya T, Mizuno Y, Mochizuki H (2006) Inflammation and infection in

Parkinson's disease Histol Histopathol 21: 673-678. Arinami T, Li L, Mitsushio H, Itokawa M, Hmamguchi H, Toru M (1996) An

insertion/deletion polymorphism in the angiotensin- converting enzyme gene is associates with both brain substance P content and affective disorders. Biol Psychiatry 40:1122-1127.

Bailey CP, Maubach KA, Jones RS (2004) Neurokinin-1 receptors in the rat nucleus

tractus solitarius: pre- and postsynaptic modulation of glutamate and GABA release. Neuroscience 127:467-479.

Bannon MJ, Elliot PJ, Bunney EB (1987) Striatal tachykinin biosynthesis: regulation of

mRNA and peptide levels by dopamine agonists and antagonists. Molecular Brain Research 3:31-37.

Bannon MJ, Brownschidle LA, Tian Y, Whitty CJ, Poosch MS, D’sa C, Moody CA

(1995) Neurokinin-3 receptors modulate dopamine cell function and alter the effects of 6-hydroxydopamine. Brain Res 695:19-24.

Barker R (1991) Substance P and Neurodegenerative disorders. A speculative review.

Neuropeptides 20:73-78. Beal MF (1998). Excitotoxicity and nitric oxide in Parkinson's disease pathogenesis. Ann

Neurol 44: S110-4. Beal MF (1992) Mechanisms of excitotoxicity in neurologic diseases. Faseb J 6:3338-

3344. Bell MI, Richardson PJ, Lee K (1998) Characterization of the mechanism of action of

tachykinins in rat striatal cholinergic interneurons. Neuroscience 87:649-658. Bennett MC (2005) The role of alpha-synuclein in neurodegenerative diseases. Pharmacol

Ther 105:311-331.

411

Benolieil R, Tanaka M, Caudle RM, Iadarola MJ (2000) Co-localization of N-methyl-D-aspartate receptors and substance P (neurokinin-1) recpetors in rat spinal cord. Neurosci Lett 291:61-64.

Berretta N, Freestone PS, Guatteo E, Castro DD, Geracitano R, Bernardi G, Mercuri NB,

Lipski J (2005) Acute Effects of 6-Hydroxydopamine on Dopaminergic Neurons of the Rat Substantia Nigra Pars Compacta In Vitro. Neurotoxicology.

Betarbet R, Sherer TB, Greenamyre JT (2005) Ubiquitin-proteasome system and

Parkinson's diseases. Exp Neurol 191 Suppl 1:S17-27. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT

(2000) Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nature Neuroscience 3:1301-1306.

Bianchi LM, Gray NA (2002) EphB receptors influence growth of ephrin-B1-positive

statoacoustic nerve fibers. Eur J Neurosci 16:1499-1506. Bishop C, Walker PD (2004) Intranigral antagonism of neurokinin 1 and 3 receptors

reduces intrastriatal dopamine D1 receptor-stimulated locomotion in the rat. Brain Res 1023:126-133.

Blanchet F, Gauchy C, Perez S, Soubrie P, Glowinski J, Kemel ML (2000) Control by

GABA and tachykinins of the evoked release of acetylcholine in striatal compartments under different modalities of NMDA receptor stimulation. Brain Res 853:142-150.

Blandini F, Armentero MT, Martignoni E (2008) The 6-hydroxydopamine model: News

from the past. Parkinsonism Relat Disord. Block ML, Li G, Qin L, Wu X, Pei Z, Wang T, wilso0n B, Yang J, Hong JS (2006)

Potent regulation of microglia derived oxidative stress and dopaminergic survival: substance P vs dynorphin. faseb J 20:251-258.

Blum D, Torch S, Lambeng N, Nissou M, Benabid AL, Sadoul R, Verna JM (2001)

Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog Neurobiol 65:135-172.

Boix F, Mattioli R, Adams F, Huston JP, Schwarting RK (1992) Effects of substance P on

extracellular dopamine in neostriatum and nucleus accumbens. Eur J Pharmacol 216:103-107.

Bowery N, Enna SJ, Olsen RW (2004) Six decades of GABA. Biochem Pharmacol

68:1477-1478. Bowery NG, Bettler B, Froestl W, Gallagher JP, Marshall F, Raiteri M, Bonner TI, Enna

SJ (2002) International Union of Pharmacology. XXXIII. Mammalian gamma-aminobutyric acid(B) receptors: structure and function. Pharmacol Rev 54:247-264.

412

Brahmachari S, Fung YK, Pahan K (2006) Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci 26:4930-4939.

Branchi I, D'Andrea I, Armida M, Cassano T, Pezzola A, Potenza RL, Morgese MG,

Popoli P, Alleva E (2008) Nonmotor symptoms in Parkinson's disease: investigating early-phase onset of behavioral dysfunction in the 6-hydroxydopamine-lesioned rat model. J Neurosci Res 86:2050-2061.

Bredesen DE, Rao RV, Mehlen P (2006) Cell death in the nervous system. Nature

443:796-802. Buck SH, Burks TF (1986) The neuropharmacology of capsaicin: review of some recent

observations. Pharmacol Rev 38:179-226. Burke RE, Kholodilov NG (1998) Programmed cell death: does it play a role in

Parkinson's disease? Ann Neurol 44:S126-133. Burkitt HG, Young B, Heath JW (1993) Wheater's Functional Histology: A Text and

Colour Atlas, Third edition Edition: Churchill Livingstone. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G (2000) Acetylcholine-

mediated modulation of striatal function. Trends Neurosci 23:120-126. Calvo N, Reiriz J, Perez-Navarro E, Alberch J (1996) Tachykinins protect cholinergic

neurons from quinolinic acid excitotoxicity in striatal cultures. Brain Res 740:323-328.

Canals S, Casarejos MJ, de Bernardo S, Rodriguez-Martin E, Mena MA (2001)

Glutathione depletion switches nitric oxide neurotrophic effects to cell death in midbrain cultures: implications for Parkinson's disease. J Neurochem 79:1183-1195.

Carson MJ, Thrash JC, Walters B (2006) The cellular response in neuroinflammation:

The role of leukocytes, microglia and astrocytes in neuronal death and survival. Clinical Neuroscience Research 6:237-245.

Castro-Obregon S, Del Rio G, Chen SF, Swanson RA, Frankowski H, Rao RV, Stoka V,

Vesce S, Nicholls DG, Bredesen DE (2002) A ligand-receptor pair that triggers a non-apoptotic form of programmed cell death. Cell Death Differ 9:807-817.

Castro-Obregon S, Rao RV, del Rio G, Chen SF, Poksay KS, Rabizadeh S, Vesce S,

Zhang XK, Swanson RA, Bredesen DE (2004) Alternative, nonapoptotic programmed cell death: mediation by arrestin 2, ERK2, and Nur77. J Biol Chem 279:17543-17553.

Cenci MA, Lindgren HS (2007) Advances in understanding L-DOPA-induced dyskinesia. Curr Opin Neurobiol 17:665-671.

Cernak I, Chapman SM, Hamlin GP, Vink R (2002) Temporal characterisation of pro-

and anti-apoptotic mechanisms following diffuse traumatic brain injury in rats. J Clin Neurosci 9:565-572.

413

Chahl LA (2006) Tachykinins and neuropsychiatric disorders. Curr Drug Targets 7:993-1003.

Chan DK, Cordato D, Karr M, Ong B, Lei H, Liu J, Hung WT (2005) Prevalence of

Parkinson's disease in Sydney. Acta Neurol Scand 111:7-11. Chassain C, Bielicki G, Donnat J-P, Renou J-P, Eschalier A, Durif F (2005) Cerebral

Glutamate metabolism in Parkinson’s disease: an in vivo dynamic 13C NMS study in the rat. Exp Neurol 191:276-284.

Chauhan VS, Sterka DG, Jr., Gray DL, Bost KL, Marriott I (2008) Neurogenic

exacerbation of microglial and astrocyte responses to Neisseria meningitidis and Borrelia burgdorferi. J Immunol 180:8241-8249.

Chen H, Zhang SM, Hernan MA, Schwarzschild MA, Willett WC, Colditz GA, Speizer

FE, Ascherio A (2003) Nonsteroidal anti-inflammatory drugs and the risk of Parkinson disease. Arch Neurol 60:1059-1064.

Chen L-W, Yung KKL, Chan YS (2004) Neurokinin peptides and neurokinin receptors as

potential therapeutic intervention targets of basal ganglia in the prevention and treatment of Parkinson’s disease. Current Drug Targets 5:1-10.

Chen Q, Veenman CL, Reiner A (1996) Cellular expression of ionotropic glutamate

receptor subunits on specific striatal neuron types and its implication for striatal vulnerability in glutamate receptor-mediated excitotoxicity. Neuroscience 73:715-731.

Ciicchetti F, Brownell AL, Williams K, Chen YI, Livini E, Isacson O (2002

Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging Eur J Neurosci 15:991-998.

Clarke CE (2004a) Neuroprotection and pharmacotherapy for motor symptoms in

Parkinson's disease. Lancet Neurol 3:466-474. Clarke CE (2004b) A "cure" for Parkinson's disease: can neuroprotection be proven with

current trial designs? Mov Disord 19:491-498. Contreras-Vidal JL, Stelmach GE (1996) Mini Review: Effects of Parkinsonism on motor

control. Life Sciences 58:165-176. Cordato DJ, Schwartz R, Abbott E, Saunders R, Morfis L (2006) A comparison of health-

care costs involved in treating people with and without Parkinson's disease in Southern Sydney, New South Wales, Australia. J Clin Neurosci 13:655-658.

Cortright DN, Szallasi A (2004) Biochemical pharmacology of the vanilloid receptor

TRPV1. An update. Eur J Biochem 271:1814-1819.

414

Cotran RS, Kumar V, Collins T (1999) Cellular pathology I: Cell injury and cell death. In: Robbins pathologic basis of disease, Sixth Edition Edition (Cotran RS, Kumar V, Collins T, eds), pp 1-30. Philadelphia: W.B Saunders Company.

Cummings JL (2004) Dementia with lewy bodies: molecular pathogenesis and

implications for classification. J Geriatr Psychiatry Neurol 17:112-119. Daenen EW, Van der Heyden JA, Kruse CG, Wolterink G, Van Ree JM (2001)

Adaptation and habituation to an open field and responses to various stressful events in animals with neonatal lesions in the amygdala or ventral hippocampus. Brain Res 918:153-165.

Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron

39:889-909. De Ceballos ML, Lopez-Lozano JJ (1999) Subgroups of parkinsonian patients

differentiated by peptidergic immunostaining of caudate nucleus biopsies. Peptides 20:249-257.

de Garavilla L, Vergnolle N, Young SH, Ennes H, Steinhoff M, Ossovskaya VS,

D'Andrea MR, Mayer EA, Wallace JL, Hollenberg MD, Andrade-Gordon P, Bunnett NW (2001) Agonists of proteinase-activated receptor 1 induce plasma extravasation by a neurogenic mechanism. Br J Pharmacol 133:975-987.

de Lago E, de Miguel R, Lastres-Becker I, Ramos JA, Fernandez-Ruiz J (2004)

Involvement of vanilloid-like receptors in the effects of anandamide on motor behavior and nigrostriatal dopaminergic activity: in vivo and in vitro evidence. Brain Res 1007:152-159.

del Rio G, Castro-Obregon S, Rao R, Ellerby HM, Bredesen DE (2001) APAP, a

sequence-pattern recognition approach identifies substance P as a potential apoptotic peptide. FEBS Lett 494:213-219.

Depino AM, Earl C, Kaczmarczyk E, Ferrari C, Besedovsky H, del Rey A, Pitossi FJ,

Oertel WH (2003) Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur J Neurosci 18:2731-2742.

Desai BS, Monahan AJ, Carvey PM, Hendey B (2007) Blood-brain barrier pathology in

Alzheimer's and Parkinson's disease: implications for drug therapy. Cell Transplant 16:285-299.

Deumens R, Blokland A, Prickaerts J (2002) Modeling Parkinson's disease in rats: an

evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp Neurol 175:303-317. Di Cara B, Samuel D, Salin P, Kerkerian-Le Goff L, Daszuta A (2003) Serotonergic

regulation of the GABAergic transmission in the rat basal ganglia. Synapse 50:144-150.

415

Dodel RC, Du Y, Bales KR, Ling Z, Carvey PM, Paul SM (1999) Caspase-3-like proteases and 6-hydroxydopamine induced neuronal cell death. Brain Res Mol Brain Res 64:141-148.

Donkin JJ, Turner RJ, Hassan I, Vink R (2007) Substance P in traumatic brain injury.

Prog Brain Res 161:97-109. Dray A (1992) Neuropharmacological mechanisms of capsaicin and related substances.

Biochem Pharmacol 44:611-615. Duzzioni M, Calixto AV, Duarte FS, De Lima TC (2008) Modulation of anxiety in rats

evaluated in the elevated T-maze: evidence of the relationship between substance P and diazepam. Behav Brain Res 187:140-145.

Ebner K, Singewald N (2006) The role of substance P in stress and anxiety responses.

Amino Acids 31:251-272. Elliot WH, Elliot DC (1997) Enzymatic protective mechanisms in the body. In:

Biochemistry and Molecular Biology, First edition Edition (Elliot WH, Elliot DC, eds), pp 213-222. Oxford: Oxford University.

Eriksen JL, Wszolek Z, Petrucelli L (2005) Molecular pathogenesis of Parkinson disease.

Arch Neurol 62:353-357. Esposito E, Di Matteo V, Benigno A, Pierucci M, Crescimanno G, Di Giovanni G (2007)

Non-steroidal anti-inflammatory drugs in Parkinson's disease. Exp Neurol 205:295-312.

Fahn S, Sulzer D (2004) Neurodegeneration and Neuroprotection in Parkinson Disease.

Neurorx 1:139-154. Fedorow H, Tribl F, Halliday G, Gerlach M, Riederer P, Double KL (2005)

Neuromelanin in human dopamine neurons: comparison with peripheral melanins and relevance to Parkinson's disease. Prog Neurobiol 75:109-124.

Fernandez A, de Ceballos ML, Jenner P, Marsden CD (1994) Neurotensin, substance P,

delta and mu opioid receptors are decreased in basal ganglia of Parkinson's disease patients. Neuroscience 61:73-79.

Ferro MM, Bellissimo MI, Anselmo-Franci JA, Angellucci ME, Canteras NS, Da Cunha

C (2005) Comparison of bilaterally 6-OHDA- and MPTP-lesioned rats as models of the early phase of Parkinson's disease: histological, neurochemical, motor and memory alterations. J Neurosci Methods 148:78-87.

Foda MA, Marmarou A (1994) A new model of diffuse brain injury in rats. Part II:

Morphological characterization. J Neurosurg 80:301-313. Fornaguera J, Schwarting RK (1999) Early behavioral changes after nigro-striatal system

damage can serve as predictors of striatal dopamine depletion. Prog Neuropsychopharmacol Biol Psychiatry 23:1353-1368.

416

Fornaguera J, Carey RJ, Huston JP, Schwarting RK (1994) Behavioral asymmetries and recovery in rats with different degrees of unilateral striatal dopamine depletion. Brain Res 664:178-188.

Gahwiler BH (1981) Organotypic monolayer cultures of nervous tissue. J Neurosci

Methods 4:329-342. Gahwiler BH (1988) Organotypic cultures of neural tissue. Trends Neurosci 11:484-489. Gahwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM (1997)

Organotypic slice cultures: a technique has come of age. Trends Neurosci 20:471-477.

Gai WP, Halliday GM, Blumbergs PC, Geffen LB, Blessing WW (1991) Substance P-

containing neurons in the mesopontine tegmentum are severely affected in Parkinson's disease. Brain 114 ( Pt 5):2253-2267.

Galarraga E, Hernandez-Lopez S, Tapia D, Reyes A, Bargas J (1999) Action of substance

P (neurokinin-1) receptor activation on rat neostriatal projection neurons. Synapse 33:26-35.

Gao HM, Jiang J, Wilson B, Zhang W, Hong JS, Lui B (2002) Microglial activation-

mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 81:1285-1297.

Garside S, Furtado JC, Mazurek MF (1996) Dopamine-glutamate interactions in the

striatum: behaviourally relevant modification of excitotoxicity by dopamine receptor-mediated mechanisms. Neuroscience 75:1065-1074.

Gasbarri A, Sulli A, Packard MG (1997) The dopaminergic mesencephalic projections to

the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21:1-22.

Gavioli EC, Canteras NS, De Lima TCM (2002) The role of lateral septal NK1 receptors

in mediating anxiogenic effects induced by intracerebroventricular injection of substance P. Beh Brain Res 134:411-415.

Gerard NP, Garraway LA, Eddy J, R.L., Shows TB, Iijima H, Paquet J-L, Gerard C

(1991) Human substance P receptor(NK-1): Organisation of the gene, chromosome localization, and functional expression of cDNA clones. Biochemistry 30:10640-10646.

Girault JA, Greengard P (2004) The neurobiology of dopamine signalling. Arch Neurol

61:641-644. Godinez-Hernandez D, Gallardo-Oritz IA, Lopez-Sanchez S, Villalobos-Molina R (2006)

Captopril therapy decreases both expression and function of alpha-adrenoreceptors in pre-hypertensive rat aorta. Auton Autocoid Pharmacol 26:21-29.

417

Golembiowska K, Konieczny J, Ossowska K, Wolfforth S (2002) The role of striatal metabotropic glutamate receptors in degeneration of dopamine neurons: review article. Amino Acids 23: 199-205.

Gomez-Urquijo SM, Hokfelt T, Ubink R, Lubec G, Herrera-Marschitz M (1999)

Neurocircuitries of the basal ganglia studied in organotypic cultures: focus on tyrosine hydroxylase, nitric oxide synthase and neuropeptide immunocytochemistry. Neuroscience 94:1133-1151.

Graybiel AM (1990) Neurotransmitters and neuromodulators in the basal ganglia. TINS

13:244-254. Greenfields S (1992) Greenfield's Pathology, 5th Edidition Edition. New York: Oxford

University Press. Gu B, Zhang YD, Hu G (2003) A unilateral 6-hydroxydopamine lesion decreases the

expression of metabotropic glutamate receptors in rat substantia nigra. Neurosci Lett 351:186-190.

Guix FX, Uribesalgo I, Coma M, Munoz FJ (2005) The physiology and pathophysiology

of nitric oxide in the brain. Prog Neurobiol. Guttman M, Kish SJ, Furukawa Y (2003) Current concepts in the diagnosis and

management of Parkinson's disease. Cmaj 168:293-301. Haber S, Gdowski M (2004) The Basal Ganglia. In: The Human Nervous System Second

edition Edition (Paxinos G, Mai J, eds), pp 677-738. California: Elsevier Academic Press.

Hail N, Jr., Lotan R (2002) Examining the role of mitochondrial respiration in vanilloid-

induced apoptosis. J Natl Cancer Inst 94:1281-1292. Hamm RJ, Pike BR, O'Dell DM, Lyeth BG, Jenkins LW (1994) The rotarod test: an

evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J Neurotrauma 11:187-196.

Harrison S, Geppetti P (2001) Review: Substance P. The International Journal of

Biochemistry & Cell Biology 33:555-576. Hasenohrl RU, De Souza-Silva MA, Nikolaus S, Tomaz C, Brandao ML, Schwarting

RKW, Huston JP (2000) Substance P and its role in neural mechanisms governing learning, anxiety and functional recovery. Neuropeptides 34:272-280.

Hauber W (1998) Involvement of basal ganglia transmitter systems in movement

initiation. Prog Neurobiol 56:507-540. He Y, Appel S, Le W (2001) minocycline inhibits microglial activation and protects

nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res 909:187-193.

418

Heikkila RE, Sonsalla PK (1992) The MPTP-treated mouse as a model of Parkinsonism: how good is it? Neurochem Int 20 Suppl:299S-303S.

Helke CJ, DiMicco JA, Jacobowitz DM, Kopin IJ (1981) Effect of capsaicin

administration to neonatal rats on the substance P content of discrete CNS regions. Brain Res 222:428-431.

Helke CJ, Krause JE, Mantyh PW, Couture R, Bannon MJ (1990) Diversity in

mammalian tachykinin peptidergic neurons: multiple peptides, receptors, and regulatory mechanisms. Faseb J 4:1606-1615.

Hely MA, Fung VS, Morris JG (2000) Treatment of Parkinson's disease. J Clin Neurosci

7:484-494. Henry B, Duty S, Fox SH, Crossman AR, Brotchie JM (2003) Increased striatal pre-

proenkephalin B expression is associated with dyskinesia in Parkinson’s disease. Exp Neurol 183:458-468.

Henze C, Earl C, Sautter J, Schmidt N, Themann C, Hartmann A, Oertel WH (2005)

Reactive oxidative and nitrogen species in the nigrostriatal system following striatal 6-hydroxydopamine lesion in rats. Brain Res 1052:97-104.

Herrera-Marschitz M, Kohlhauser C, Gomez-Urquijo S, Ubink R, Goiny M, Hokfelt T

(2000) Excitatory amino acids, monoamine, and nitric oxide synthase systems in organotypic cultures: biochemical and immunohistochemical analysis. Amino Acids 19:33-43.

Herrero M-T, Augood SJ, Hirsch EC, Javoy-Agid F, Luquin MR, Agid Y, Obeso JA,

Emson PC (1995) Effects of L-DOPA on preproenkephalin and preprotachykinin gene expression in the MPTP-treated monkey striatum. Neurosci 68:1189-1198.

Hersch SM, Gutekunst CA, Rees HD, Heilman CJ, Levey AI (1994) Distribution of m1-

m4 muscarinic receptor proteins in the rat striatum: light and electron microscopic immunocytochemistry using subtype-specific antibodies. J Neurosci 14:3351-3363.

Hilker R, Portman AT, Voges J, Staal MJ, Burghaus L, van Laar T, Koulousakis A,

Maguire RP, Pruim J, de Jong BM, Herholz K, Sturm V, Heiss WD, Leenders KL (2005) Disease progression continues in patients with advanced Parkinson's disease and effective subthalamic nucleus stimulation. J Neurol Neurosurg Psychiatry 76:1217-1221.

Hirsch EC (2000) Glial cells and Parkinson's disease. J Neurol 247 Suppl 2:II58-62. Hirsch EC, Hunot S, Damier P, Faucheux B (1998) Glial cells and inflammation in

Parkinson's disease: a role in neurodegeneration? Ann Neurol 44:S115-120. Hokfelt T, Pernow B, Wahren J (2001) Substance P: a pioneer amongst neuropeptides. J

of Internal Medicine 249:27-40.

419

Hokfelt T, Broberger C, Xu Z-QD, Sergeyev V, Ubink R, Diez M (2000) Neuropeptides- an overview. Neuropharmacology 39:1337-1356.

Holmes C, El-Oki M, Williams AL, Cunningham C, wilcockson D, Perry VH (2003)

systemic infection, interleukin-1beta and cognitive decline in Alzheimer's disease. J Neurol Neurosurg Psychiatry 74:788-789.

Holzer P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings:

involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24:739-768.

Holzer P (1991) Capsaicin: cellular targets, mechanisms of action, and selectivity for thin

sensory neurons. Pharmacol Rev 43:143-201. Hoyle CH (1998) Neuropeptide families: evolutionary perspectives. Regul Pept 73:1-33. Hu DE, Easton AS, Fraser PA (2005) TRPV1 activation results in disruption of the blood-

brain barrier in the rat. Br J Pharmacol 146:576-584. Huang SM, Bisogno T, Trevisani M, Al-Hayani A, De Petrocellis L, Fezza F, Tognetto

M, Petros TJ, Krey JF, Chu CJ, Miller JD, Davies SN, Geppetti P, Walker JM, Di Marzo V (2002) An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc Natl Acad Sci U S A 99:8400-8405.

Hudson JL, van Horne CG, Stromberg I, Brock S, Clayton J, Masserano J, Hoffer BJ,

Gerhardt GA (1993) Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats. Brain Res 626:167-174.

Humpel C, Saria A (1993) Intranigral injection of selective neurokinin-1 and neurokinin-

3 but not neurokinin-2 receptor agonists biphasically modulate striatal dopamine metabolism but not striatal preprotachykinin-A mRNA in the rat. Neurosci Lett 157:223-226.

Hunot S, Brugg B, Ricard D, Michel PP, Muriel MP, Ruberg M, Faucheux BA, Agid Y,

Hirsch EC (1997) Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with Parkinson disease. Proc Natl Acad Sci U S A 94:7531-7536.

Hunot S, Dugas N, Faucheux B, Hartmann A, Tardieu M, Debre P, Agid Y, Dugas B,

Hirsch EC (1999) FcepsilonRII/CD23 is expressed in Parkinson's disease and induces, in vitro, production of nitric oxide and tumour necrosis factor-alpha in glial cells. J Neurosci 19:3440-3447.

Ichitani Y, Okamura H, Nakahara D, Nagatsu I, Ibata Y (1994) Biochemical and

immunocytochemical changes induced by intrastriatal 6-hydroxydopamine injection in the rat nigrostriatal dopamine neuron system: evidence for cell death in the substantia nigra. Exp Neurol 130:269-278.

420

Improto G, Broccardo M (2006) Tachykinins: role in human gastrointestinal tract physiology and pathology. Curr Drug Targets 7:1021-1029.

Ivinskis A (1970) A study of validity of open-field measures. Australian Journal of

Psychology 22:175-183. Jenkins TA, Wong JY, Howells DW, Mendelsohn FA, Chai SY (1999) The effect of

chronic angiotensin-converting enzyme inhibition on striatal dopamine content in the MPTP-treated mouse. J Neurochem 73:214-219.

Jenkins TA, Mendelsohn FA, Chai SY (1997) Angiotensin-converting enzyme modulates

dopamine turnover in the striatum. J Neurochem 68: 1304-1311. Jenner P, Olanow CW (1998) Understanding cell death in Parkinson's disease. Ann

Neurol 44:S72-84. Joos GF, Germonpre PR, Pauwels RA (2000) Role of tachykinins in asthma. Allergy

55:321-327. Kaasinen V, Rinne JO (2002) Functional imaging studies of dopamine system and

cognition in normal aging and Parkinson's disease. Neurosci Biobehav Rev 26:785-793.

Kang BN, Jeong KS, Park SJ, Kim ST, Kim TH, Kim H, Rhy SY (2001) Regulation of

apoptosis by somatostatin and substance P in peritoneal macrophages. Regul.2 Pept 101:43-49.

Kang SJ, Wang S, Hara H, Peterson EP, Namura S, Amin-Hanjani S, Huang Z,

Srinivasan A, Tomaselli KJ, Thornberry NA, Moskowitz MA, Yuan J (2000) Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J Cell Biol 149:613-622.

Kannurpatti SS, Sanganahalli BG, Mishra S, Joshi PG, Joshi NB (2004) Glutamate-

induced differential mitochondrial response in young and adult rats. Neurochem Int 44:361-369.

Kashiba H, Ueda Y, Senba E (1997) Systemic capsaicin in the adult rat differentially

affects gene expression for neuropeptides and neurotrophin receptors in primary sensory neurons. Neuroscience 76:299-312.

Katsuki H, Okawara M, Shibata H, Kume T, Akaike A (2006) Nitric oxide-producing

microglia mediate thrombin-induced degeneration of dopaminergic neurons in rat midbrain slice culture. J Neurochem 97:1232-1242.

Katz J, Nielsen KM, Soghomonian JJ (2005) Comparative effects of acute or chronic

administration of levodopa to 6-hydroxydopamine-lesioned rats on the expression of glutamic acid decarboxylase in the neostriatum and GABAA receptors subunits in the substantia nigra, pars reticulata. Neuroscience 132:833-842.

421

Kemel ML, Perez S, Godeheu G, Soubrie P, Glowinski J (2002) Facilitation by endogenous tachykinins of the NMDA-evoked release of acetylcholine after acute and chronic suppression of dopaminergic transmission in the matrix of the rat striatum. J Neurosci 22:1929-1936.

Khawaja AM, Rogers DF (1996) Tachykinins: receptor to effector. Int J Biochem Cell

Biol 28:721-738. Kim NG, Lee H, Son E, Kwon OY, Park JY, Park JH, Cho GJ, Choi WS, Suk K (2003)

Hypoxic induction of caspase-11/caspase-1/interleukin-1beta in brain microglia. Brain Res Mol Brain Res 114:107-114.

Kim SR, Lee DY, Chung ES, Oh UT, Kim SU, Jin BK (2005) Transient receptor

potential vanilloid subtype 1 mediates cell death of mesencephalic dopaminergic neurons in vivo and in vitro. J Neurosci 25:662-671.

Kirik D, Rosenblad C, Bjorklund A (1998) Characterization of behavioral and

neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp Neurol 152:259-277.

Kombian SB, Ananthalakshmi KVV, Parvathy SS, Matowe WC (2003) Substance P

depresses excitatory synaptic transmission in the nucleus accumbens through dopaminergic and purinergic mechanisms. J Neurophysiol 89:728-737.

Kopin IJ, Burns SR, Chiueh CC, Markey SP (1986) MPTP-induced Parkinsonian

syndromes in humans and animals. In: Alzheimer's and Parkinson's Diseases: Strategies for research and development (Fisher A, Hanin I, Lachman C, eds), pp 519-530. New YorkLondon: Plenum Press.

Kortekaas R, Leenders KL, van Oostrom JC, Vaalburg W, Bart J, Willemsen AT,

Hendrikse NH (2005) Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann Neurol 57:176-179.

Kramer BC, Mytilineou C (2004) Alterations in the cellular distribution of bcl-2, bcl-x

and bax in the adult rat substantia nigra following striatal 6-hydroxydopamine lesions. J Neurocytol 33:213-223.

Krasnova IN, Bychkov ER, Lioudyno VI, Zubareva OE, Dambinova SA (2000)

Intracerebroventricular administration of Substance P increases dopamine content in the brain of 6-hydroxydopamine-lesioned rats. Neurosci 95:113-117.

Kress GJ, Reynolds IJ (2003) A characterisation of dopaminergic neurodegeneration in

organotypic cultures. Ann NY Acad Sci 991:304-306. Kurosaki R, Muramatsu Y, Kato H, Watanabe Y, Imai Y, Itoyama Y, Araki T (2005)

Effect of angiotensin-converting enzyme inhibitor perindopril on interneurons in MPTP-treated mice. Eur Neuropsychopharmacol 15:57-67.

422

Lapointe N, St-Hilaire M, Martinoli MG, Blanchet J, Gould P, Rouillard C, Cicchetti F (2004) Rotenone induces non-specific central nervous system and systemic toxicity. Faseb J 18:717-719.

Lee CS, Sauer H, Bjorklund A (1996) Dopaminergic neuronal degeneration and motor

impairments following axon terminal lesion by intrastriatal 6-hydroxydopamine in the rat. Neuroscience 72:641-653.

Lee J, Di Marzo V, Brotchie JM (2006) A role for vanilloid receptor 1 (TRPV1) and

endocannabinnoid signalling in the regulation of spontaneous and L-DOPA induced locomotion in normal and reserpine-treated rats. Neuropharmacology 51:557-565.

Leeman SE, Ferguson SL (2000) Substance P: an historical perspective. Neuropeptides

34:249-254. Lembeck F, Donnerer J, Tsuchiya M, Nagahisa A (1992) The non-peptide tachykinin

antagonist, CP-96, 345, is a potent inhibitor of neurogenic inflammation. Br J Pharmacol 105:527-530.

Lev N, Melamed E, Offen D (2003) Apoptosis and Parkinson's disease. Prog

Neuropsychopharmacol Biol Psychiatry 27:245-250. Lever IJ, Grant AD, Pezet S, Gerard NP, Brain SD, Malcangio M (2003) Basal and

activity-induced release of substance P from primary afferent fibers in NK1 receptor knockout mice: evidence for negative feedback. Neuropharmacology 45:1101-1110.

Levesque M, Wallman MJ, Parent R, Sik A, Parent A (2007) Neurokinin-1 and

neurokinin-3 receptors in primate substantia nigra. Neurosci Res 57:362-371. Levy G, Louis ED, Cote L, Perez M, Mejia-Santana H, Andrews H, Harris J, Waters C,

Ford B, Frucht S, Fahn S, Marder K (2005) Contribution of aging to the severity of different motor signs in Parkinson’s disease. Arch Neurol 62:467-472.

Li Y, Chopp M, Chen J, Wang L, Gautam SC, Xu YX, Zhang Z (2000) Intrastriatal

transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab 20:1311-1319.

Liang Q, Liou AK, Ding Y, Cao G, Xiao X, Perez RG, Chen J (2004) 6-

Hydroxydopamine induces dopaminergic cell degeneration via a caspase-9-mediated apoptotic pathway that is attenuated by caspase-9dn expression. J Neurosci Res 77:747-761.

Liu B, Hong JS (2003) Role of microglia in inflammation-mediated neurodegenerative

diseases: mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther 304:1-7.

Liu B, Gao HM, Hong JS (2003) Parkinson's disease and exposure to infectious agents

and pesticides and the occurrence of brain injuries: role of neuroinflammation. Environ Health Perspect 111:1065-1073.

423

Loonam TM, Noailles PA, Yu J, Zhu JP, Angulo JA (2003) Substance P and cholecystokinin regulate neurochemical responses to cocaine and methamphetamine in the striatum. Life Sci 73:737-739.

Lopez-Real A, Rey P, Soto-Otero R, Mendez-Alvarez E, Labandeira-Garcia JL (2005)

Angiotensin-converting enzyme inhibition reduces oxidative stress and protects dopaminergic neurons in a 6-hydroxydopamine rat model of Parkinsonism. J Neurosci Res 81:865-873.

Luquin MR, Saldise L, Guillen J, Belzunegui S, San Sebastian W, Izal A, Garrido P,

Vazquez M (2006) Does increased excitatory drive from the subthalamic nucleus contribute to dopaminergic neuronal death in Parkinson's disease? Exp Neurol 201:407-415.

Macho A, Blazquez MV, Navas P, Munoz E (1998) Induction of apoptosis by vanilloid

compounds does not require de novo gene transcription and activator protein 1 activity. Cell Growth Differ 9:277-286.

Macho A, Calzado MA, Munoz-Blanco J, Gomez-Diaz C, Gajate C, Mollinedo F, Navas

P, Munoz E (1999) Selective induction of apoptosis by capsaicin in transformed cells: the role of reactive oxygen species and calcium. Cell Death Differ 6:155-165.

Maggi CA (1995) The mammalian tachykinin receptors. Gen Pharmac 26:911-944. Malcangio M, Bowery NG (1999) Peptide autoreceptors: does an autoreceptor exist for

substance P. TiPS 20:405-407. Mantyh PW, Johnson DJ, Boehmer CG, Catton MD, Vinters HV, Maggio JE, Too HP,

Vigna SR (1989) Substance P receptor binding sites are expressed by glia in vivo after neuronal injury. Proc Natl Acad Sci U S A 86:5193-5197.

Marey-Semper I, Gelman M, Levi-Strauss M (1995) A selective toxicity toward cultured

mesencephalic dopaminergic neurons is induced by the synergistic effects of energetic metabolism impairment and NMDA receptor activation. J Neurosci 15:5912-5918.

Marinelli S, Di Marzo V, Berretta N, Matias I, Maccarrone M, Bernardi G, Mercuri NB

(2003) Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J Neurosci 23:3136-3144.

Marsden CD, Olanow CW (1998) The causes of Parkinson's disease are being unravelled

and rational neuroprotective therapy is close to reality. Ann Neurol 44:S189-196. Marti M, Manzalini M, Fantin M, Bianchi C, Della Corte L, Morari M (2005) Striatal

glutamate release evoked in vivo by NMDA is dependent upon ongoing neuronal activity in the substantia nigra, endogenous striatal substance P and dopamine. J Neurochem 93:195-205.

424

Martorana A, Fusco FR, D'Angelo V, Sancesario G, Bernardi G (2003) Enkephalin, neurotensin, and substance P immunoreactive neurones of the rat GP following 6-hydroxydopamine lesions of the substantia nigra. Exp Neurol 183:311-319.

Maubach KA, Martin K, Smith DW, Hewson L, Frankshun RA, Harrison T, Seabrook

GR (2001) Substance P stimulates inhibitory synaptic transmission in the guinea pig basolateral amygdala in vitro. Neuropharmacology 40:806-817.

Mauborgne A, Javoy-Agid F, Legrand JC, Agid Y, Cesselin F (1983) Decrease of

substance P-like immunoreactivity in the substantia nigra and pallidum of parkinsonian brains. Brain Res 268:167-170.

McGeer PL, McGeer EG (2008) Glial reactions in Parkinson's disease. Mov Disord

23:474-483. McIntosh TK, Vink R, Noble L, Yamakami I, Fernyak S, Soares H, Faden AL (1989)

Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28:233-244.

Melani A, Pantoni L, Corsi C, Bianchi L, Monopoli A, Bertorelli R, Pepeu G, Pedata F

(1999) Striatal outflow of adenosine, excitatory amino acids, gamma-aminobutyric acid, and taurine in awake freely moving rats after middle cerebral artery occlusion: correlations with neurological deficit and histopathological damage. Stroke 30:2448-2454; discussion 2455.

Mena MA, Pardo B, Casarejos MJ, Fahn S, Garcia de Yebenes J (1992) Neurotoxicity of

levodopa on catecholamine-rich neurons. Mov Disord 7:23-31. Meredith GE, Halliday GM, Totterdell S (2004) A critical review of the development and

importance of proteinaceous aggregates in animal models of Parkinson's disease: new insights into Lewy body formation. Parkinsonism Relat Disord 10:191-202.

Mezey E, Toth ZE, Cortright DN, Arzubi MK, Krause JE, Elde R, Guo A, Blumberg PM,

Szallasi A (2000) Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc Natl Acad Sci U S A 97:3655-3660.

Michael-Titus AT, Fernandes K, Setty H, Whelpton R (2002) In vivo metabolism and

clearance of substance P and co-expressed tachykinins in rat striatum. Neurosci 110:277-286.

Miyazaki I, Asanuma M (2008) Dopaminergic neuron-specific oxidative stress caused by

dopamine itself. Acta Med Okayama 62:141-150. Mladenovic A, Perovic M, Raicevic N, Kanazir S, Rakic L, Ruzdijic S (2004) 6-

Hydroxydopamine increases the level of TNFalpha and bax mRNA in the striatum and induces apoptosis of dopaminergic neurons in hemiparkinsonian rats. Brain Res 996:237-245.

425

Mochizuki H, Goto K, Mori H, Mizuno Y (1996) Histochemical detection of apoptosis in Parkinson's disease. J Neurol Sci 137:120-123.

Modo M, Stroemer RP, Tang E, Veizovic T, Sowniski P, Hodges H (2000) Neurological

sequelae and long-term behavioural assessment of rats with transient middle cerebral artery occlusion. J Neurosci Methods 104:99-109.

Mokry J (1995) Experimental models and behavioural tests used in the study of

Parkinson's disease. Physiol Res 44:143-150. Monahan AJ, Warren M, Carvey PM (2008) Neuroinflammation and peripheral immune

infiltration in Parkinson's disease: an autoimmune hypothesis. Cell Transplant 17:363-372.

Morari M, Marti M, Sbrenna S, Fuxe K, Bianchi C, Beani L (1998) Reciprocal dopamine-

glutamate modulation of release in the basal ganglia. Neurochem Int 33:383-397. Mosley RL, Benner EJ, Kadiu I, Thomas M, Boska MD, Hasan K, Laurie C, Gendelman

HE (2006) Neuroinflammation, Oxidative Stress and the Pathogenesis of Parkinson's Disease. Clin Neurosci Res 6:261-281.

Munoz A, Rey P, Guerra MJ, Mendez-Alvarez E, Soto-Otero R, Labandeira-Garcia JL

(2006) Reduction of dopaminergic degeneration and oxidative stress by inhibition of angiotensin converting enzyme in a MPTP model of parkinsonism. Neuropharmacology 51:112-120.

Napier TC, Mitrovic I, Churchill L, Klitenick MA, Lu XY, Kalivas PW (1995) Substance

P in the ventral pallidum: projection from the ventral striatum, and electrophysiological and behavioral consequences of pallidal substance P. Neuroscience 69:59-70.

Nikolaus S, Huston JP, Hasenohrl RU (1999) Reinforcing effects of neurokinin substance

P in the ventral pallidum: mediation by the tachykinin NK1 receptor. Eur J Pharmacol 370:93-99.

Nikolaus S, Huston JP, Korber B, Thiel C, Schwarting RKW (1997) Pretreatment with

neurokinin substance P but not with cholecystokinin-8S can alleviate functional deficits of partial nigrostriatal 6-hydoxydopamine lesion. Peptides 18:1161-1168.

Nimmo AJ, Cernak I, Heath DL, Hu X, Bennett CJ, Vink R (2004) Neurogenic

inflammation is associated with development of edema and functional deficits following traumatic brain injury in rats. Neuropeptides 38:40-47.

Nisbet AP, Foster OJ, Kingsbury A, Eve DJ, Daniel SE, Marsden CD, Lees AJ (1995)

Preproenkephalin and preprotachykinin messenger RNA expression in normal human basal ganglia and in Parkinson's disease. Neuroscience 66:361-376.

426

Ogura T, Ogata M, Akita H, Jitsuki S, Akiba L, Noda K, Hoka S, Saji M (2005) Impaired acquisition of skilled behavior in rotarod task by moderate depletion of striatal dopamine in a pre-symptomatic stage model of Parkinson's disease. Neurosci Res 51:299-308.

Olanow CW, Tatton WG (1999) Etiology and pathogenesis of Parkinson's disease. Annu

Rev Neurosci 22:123-144. Olanow CW, Agid Y, Mizuno Y, Albanese A, Bonucelli U, Damier P, De Yebenes J,

Gershanik O, Guttman M, Grandas F, Hallet M, Hornykiewicz O, Jenner P, Katzenschlager R, Langston WJ, LeWitt P, Melamed E, Mena MA, Michel PP, Mytilineou C, Obeso JA, Poewe W, Quinn N, Raisman-Vozari R, Rajput AH, Rascol O, Sampaio C, Stocchi F (2004) Levodopa in the treatment of Parkinson's disease: current controversies. Movement Disorders 19:997-1005.

Olsson M, Nikkhah G, Bentlage C, Bjorklund A (1995) Forelimb akinesia in the rat

Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 15:3863-3875.

Orosz D, Bennett JP, Jr. (1990) Baseline and apomorphine-induced extracellular levels of

nigral substance P are increased in an animal model of Parkinson's disease. Eur J Pharmacol 182:509-514.

Orth M, Tabrizi SJ (2003) Models of Parkinson's disease. Mov Disord 18:729-737. Otsuka M, Yoshioka K (1993) Neurotransmitter functions of mammalian tachykinins.

Physiol Rev 73:229-308. Parent A (1990) Extrinsic connections of the basal ganglia. TINS 13:254-258. Parkinson's Organisation of South Australia Australia (2005) Parkinson's Disease Fact

Sheets. Parkinson's Organisation of South Australia, Adelaide. Paxinos G, Watson C (1998) The Rat Brain Stereotaxic Coordinates, 4th Edition Edition.

San Diego: Academis Press. Pegorini S, Braida D, Verzoni C, Guerini-Rocco C, Consalez GG, Croci L, Sala M (2005)

Capsaicin exhibits neuroprotective effects in a model of transient global cerebral ischemia in Mongolian gerbils. Br J Pharmacol 144:727-735.

Perez-Otano I, Mandelzys A, Morgan JI (1998) MPTP-Parkinsonism is accompanied by

persistent expression of a �-FosB-like protein in dopaminergic pathways. Mol Brain

Res 53:41-52. Perry VH (2004) The influence on systemic inflammation on inflammation in the brain:

implications for neurodegenerative disease. Brain Behav Immun 18:407-413. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD (2006) Blood-brain barrier:

structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 1:223-236.

427

Petroske E, Meredith GE, Callen S, Totterdell S, Lau YS (2001) Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience 106:589-601.

Pezze MA, Feldon J (2004) Mesolimbic dopaminergic pathways in fear conditioning.

Prog Neurobiol 74:301-320. Pisani A, Bonsi P, Centonze D, Gubellini P, Bernardi G, Calabresi P (2003) Targeting

striatal cholinergic interneurons in Parkinson's disease: focus on metabotropic glutamate receptors. Neuropharmacology 45:45-56.

Polvishock JT, Hayes RL, Michel ME, McIntosh TK (1994) Workshop on animal models

of traumatic brain injury. J Neurotrauma 11:723-732. Powers KM, Kay DM, Factor SA, Zabetian CP, Higgins DS, Samii A, Nutt JG, Griffith

A, Leis B, Roberts JW, Martinez ED, Montimurro JS, Checkoway H, Payami H (2008) Combined effects of smoking, coffee, and NSAIDs on Parkinson's disease risk. Mov Disord 23:88-95.

Prensa L, Parent A (2001) The nigrostriatal pathway in the rat: A single-axon study of the

relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247-7260.

Prensa L, Cossette M, Parent A (2000) Dopaminergic innervation of human basal ganglia.

J Chem Neuroanat 20:207-213. Przedborski S, Vila M, Jackson-Lewis V (2003) Neurodegeneration: what is it and where

are we? J Clin Invest 111:3-10. Przedborski S, Tieu K, Perier C, Vila M (2004) MPTP as a mitochondrial neurotoxic

model of Parkinson’s disease. Journal of Bioenergetics and Biomembranes 36:375-379.

Przedborski S, Levivier M, Jiang H, Ferreira M, Jackson-Lewis V, Donaldson D,

Togasaki DM (1995) Dose-dependent lesions of the dopaminergic nigrostriatal pathway induced by intrastriatal injection of 6-hydroxydopamine. Neuroscience 67:631-647.

Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT (2007)

Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453-462.

Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW (1999)

Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 30:77-105.

Ramaker C, Marinus J, Stiggelbout AM, Van Hilten BJ (2002) Systematic evaluation of

rating scales for impairment and disability in Parkinson's disease. Mov Disord 17:867-876.

428

Rasley A, Bost KL, Olson JK, Miller SD, Marriott I (2002) Expression of functional NK-1 receptors in murine microglia. Glia 37:258-267.

Reale M, Iarlori C, Thomas A, Gambi D, Perfetti B, Di Nicola M, Onofrj M (2008)

Peripheral cytokines profile in Parkinson's disease. Brain Behav Immun. Reardon KA, Mendelsohn FA, Chai SY, Horne MK (2000) The angiotensin converting

enzyme (ACE) inhibitor, perindopril, modifies the clinical features of Parkinson's disease. Aust N Z J Med 30:48-53.

Rego AC, Oliveira CR (2003) Mitochondrial dysfunction and reactive oxygen species in

excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases. Neurochem Res 28:1563-1574.

Reid MS, Herrera-Marschitz M, Hokfelt T, Lindefors N, Persson H, Ungerstedt U

(1990a) Striatonigral GABA, dynorphin, substance P and neurokinin A modulation of nigrostriatal dopamine release: evidence for direct regulatory mechanisms. Exp Brain Res 82:293-303.

Reid MS, Herrera-Marschitz M, Hokfelt T, Ohlin M, Valentino KL, Ungerstedt U

(1990b) Effects of intranigral substance P and neurokinin A on striatal dopamine release--I. Interactions with substance P antagonists. Neuroscience 36:643-658.

Ribeiro-da-Silva A, Hokfelt T (2000) Neuroanatomical localisation of Substance P in the

CNS and sensory neurons. Neuropeptides 34:256-271. Richardson MD, Balius AM, Yamaguchi K, Freilich ER, Barak LS, Kwatra MM (2003)

Human substance P receptor lacking the C-terminal domain remains competent to desensitize and internalize. J Neurochem 84:854-863.

Rock RB, Peterson PK (2006) Microglia as a pharmacological target in infectious and

inflammatory diseases of the brain. J Neuroimmune Pharmacol 1:117-126. Rodrigues RW, Gomide VC, Chadi G (2004) Astroglial and microglial activation in the

wistar rat ventral tegmental area after a single striatal injection of 6-hydroxydopamine. Int J Neurosci 114:197-216.

Rodrigues RWP, Gomide VC, Chadi G (2001) Astroglial and microglial reaction after

partial nigrostriatal degeneration induced by the striatal injection of different doses of 6-hydroxydopamine. International Journal of Neuroscience 109:91-126.

Rodriguez M, Alvarez-Erviti L, Blesa FJ, Rodriguez-Oroz MC, Arina A, Melero I,

Ramos LI, Obeso JA (2007) Bone-marrow-derived cell differentiation into microglia: a study in a progressive mouse model of Parkinson's disease. Neurobiol Dis 28:316-325.

Rodriguez MC, Obeso JA, Olanow CW (1998) Subthalamic nucleus-mediated

excitotoxicity in Parkinson's disease: a target for neuroprotection. Ann Neurol 44:S175-188.

429

Rodriguez-Pallares J, Parga JA, Munoz A, Rey P, Guerra MJ, Labandeira-Garcia JL (2007) Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine-induced degeneration of dopaminergic neurons. J Neurochem.

Rodriguez-Pallares J, quinoz CR, Parga JA, Guerra MJ, Labandeira-Garcia JL (2004)

Angiotensin II increases differentiation of dopaminergic neurons from mesencephalic precursor via angiotensin type 2 receptors. Eur J Neurosci 20:1489-1498.

Rouse ST, Marino MJ, Bradley SR, Awad H, Wittmann M, Conn PJ (2000) Distribution

and roles of metabotropic glutamate receptors in the basal ganglia motor circuit: implications for treatment of Parkinson's disease and related disorders. Pharmacol Ther 88:427-435.

Rozas G, Labandeira Garcia JL (1997) Drug-free evaluation of rat models of

parkinsonism and nigral grafts using a new automated rotarod test. Brain Res 749:188-199.

Rozas G, Guerra MJ, Labandeira-Garcia JL (1997) An automated rotarod method for

quantitative drug-free evaluation of overall motor deficits in rat models of parkinsonism. Brain Res Brain Res Protoc 2:75-84.

Saka E, Iadarola M, Fitzgerald DJ, Graybiel AM (2002) Local circuit neurons in the

striatum regulate neural and behavioral responses to dopaminergic stimulation. Proc Natl Acad Sci U S A 99:9004-9009.

Salamone JD, Correa M, Mingote SM, Weber SM (2005) Beyond the reward hypothesis:

alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5:34-41. Sanberg PR, Emerich DF, Aebischer P, Amisetti SM, Ouellette W, Koutouzis TK, Cahill

DW, Norman AB (1993) Substance P containing polymer implants protect against striatal excitotoxicity. Brain Res 628:327-329.

Saria A (1999) The tachykinin NK1 receptor in the brain: pharmacology and putative

functions. Eur J of Pharmacol 375:51-60. Sawada H, Kawamura T, Shimohama S, Akaike A, Kimura J (1996) Different

mechanisms of glutamate-induced neuronal death between dopaminergic and non-dopaminergic neurons in rat mesencephalic culture. J Neurosci Res 43:503-510.

Schallert T, Upchurch M, Lobaugh N, Farrar SB, Spirduso WW, Gilliam P, Vaughn D,

Wilcox RE (1982) Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage. Pharmacol Biochem Behav 16:455-462.

Schapira AH, Olanow CW (2004) Neuroprotection in Parkinson disease: mysteries,

myths, and misconceptions. Jama 291:358-364.

430

Schatz DS, Kaufmann WA, Saria A, Humpel C (1999) Dopamine neurons in a simple GDNF-treated meso-striatal organotypic co-culture model. Exp Brain Res 127:270-278.

Schauvliege R, Vanrobaeys J, Schotte P, Beyaert R (2002) Caspase-11 gene expression in

response to lipopolysaccharide and interferon-gamma requires nuclear factor-kappa �

and signal transducer and activation of transcription (STAT)1. J Biol Chem 277: 41624-41630.

Schmidt N, Ferger B (2001) Neurochemical findings in the MPTP model of Parkinson's

disease. J Neural Transm 108:1263-1282. Schober A (2004) Classic toxin-induced animal models of Parkinson's disease: 6-OHDA

and MPTP. Cell Tissue Res 318:215-224. Schor NF (1988) Inactivation of mammalian brain glutamine synthetase by oxygen

radicals. Brain Res 456:17-21. Schwarting RK, Huston JP (1996) Unilateral 6-hydroxydopamine lesions of meso-striatal

dopamine neurons and their physiological sequelae. Prog Neurobiol 49:215-266. Serra MC, Bazzoni F, della Bianco V, Greskowiak M, Rossi F (1998) Activation of

human neutrophils by substance P. Effect on oxidative metabolism, exocytosis, cytosolic Ca2+ concentration and inositol phosphate formation. J Immunol 141:2119-2124.

Sethi KD (2002) Clinical aspects of Parkinson disease. Curr Opin Neurol 15:457-460. Severini C, Improta G, Falconieri-Erspamer G, Salvadori S, Erspamer V (2002) The

tachykinin peptide family. Pharmacol Rev 54:385-322. Seybold VS, McCarson KE, Mermelstein PG, Groth RD, Abrahams LG (2003)

Calcitonin gene-related peptide regulates expression of neurokinin1 receptors by rat spinal neurons. J Neurosci 23:1816-1824.

Sherer TB, Betarbet R, Kim J-H, Greenamyre JT (2003a) Selective microglial activation

in the rat rotenone model of Parkinson’s disease. Neurosci Lett 341:87-90. Sherer TB, Kim J-H, Betarbet R, Greenamyre JT (2003b) Subcutaneous rotenone

exposure causes highly selective dopaminergic degeneration and �-synuclein

aggregation. Exp Neurol 179:9-16. Sherer TB, Betarbet R, Testa CM, Boo Seo B, Richardson JR, Kim J-H, Miller GW, Yagi

T, Matsuno-Yagi A, Greenamyre JT (2003c) Mechanisms of toxicity in rotenone models of Parkinson’s disease. J Neurosci 23:10756-10764.

Shimizu K, Matsubara K, Ohtaki K, Shiono H (2003) Paraquat leads to dopaminergic

neural vulnerability in organotypic midbrain culture. Neurosci Res 46:523-532.

431

Shin CY, Shin J, Kim BM, Wang MH, Jang JH, Surh YJ, Oh U (2003) Essential role of mitochondrial permeability transition in vanilloid receptor 1-dependent cell death of sensory neurons. Mol Cell Neurosci 24:57-68.

Shults CW (2004) Mitochondrial dysfunction and possible treatments in Parkinson's

disease-a review. Mitochondrion 4:641-648. Sil'kis IG (2002) A possible mechanism for the dopamine-evoked synergistic

disinhibition of thalamic neurons via the "direct" and "indirect" pathways in the basal ganglia. Neurosci Behav Physiol 32:205-212.

Silkis I (2001) The cortico-basal ganglia-thalamocortical circuit with synaptic plasticity.

II. Mechanism of synergistic modulation of thalamic activity via the direct and indirect pathways through the basal ganglia. Biosystems 59:7-14.

Sivam SP (1991) Dopamine dependent decrease in enkephalin and substance P levels in

basal ganglia regions of postmortem Parkinsonian brains. Neuropeptides 18:201-207. Skidgel RA, Erdos EG (2004) Angiotensin converting enzyme (ACE) and neprilysin

hydrolyze neuropeptides: a brief history, the beginning and follow-ups to early studies. Peptides 25:521-525.

Snell RS (1997) The Basal Nuclei (Basal Ganglia) and their Connections. In: Clinical

Neuroanatomy for Medical Students, Fourth Edition Edition (Palumbo R, ed), pp 306-316. Philadelphia: Lippincott-Raven.

Soto-Otero R, Mendez-Alvarez E, Hermida-Ameijeiras A, Munoz-Patino AM,

Labandeira-Garcia JL (2000) Autoxidation and neurotoxicity of 6-hydroxydopamine in the presence of some antioxidants: potential implication in relation to the pathogenesis of Parkinson's disease. J Neurochem 74:1605-1612.

Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, Zigmond MJ, eds (2003)

Fundamental Neuroscience, Second Edition Edition: Academic Press. Stavrovskaya IG, Kristal BS (2005) The powerhouse takes control of the cell: Is the

mitochondrial permeability transition a viable therapeutic target against neuronal dysfunction and death? Free Radical Biology & Medicine 38:687-697.

Steenland HW, Ko SW, Wu LJ, Zhuo M (2006) Hot receptors in the brain. Mol Pain

2:34. Steiner H, Gerfen CR (1998) Role of dynorphin and enkephalin in the regulation of

striatal output pathways and behavior. Exp Brain Res 123:60-76. Steiner H, Gerfen CR (1999) Enkephalin regulates acute D2 dopamine receptor

antagonist-induced immediate-early gene expression in striatal neurons. Neuroscience 88:795-810.

Stocchi F, Brusa L (2000) Cognition and emotion in different stages and subtypes of

Parkinson's disease. J Neurol 247 Suppl 2:II114-121.

432

Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.

Streit WJ, Mrak RE, Griffin WS (2004) Microglia and neuroinflammation: a pathological

perspective. J Neuroinflammation 1:14. Strittmatter SM, Lo MMS, Javitch JA, Snyder SH (1984) Autoradiographic visualization

of angiotensin-converting enzyme in rat brain with [3H]captopril: localization to a striatonigral pathway. Proc Natl Acad Sci USA 81:1599-1603.

Sutoo D, Yabe K, Akiyama K (1999) Quantitative imaging of substance P in the human

brain using a brain mapping analyzer. Neurosci Res 35:339-346. Szallasi A, Blumberg PM (1999) Vanilloid (Capsaicin) receptors and mechanisms.

Pharmacol Rev 51:159-212. Szolcsanyi J (2004) Forty years in capsaicin research for sensory pharmacology and

physiology. Neuropeptides 38:377-384. Takagi S, Hayakawa N, Kimoto H, Kato H, Araki T (2007) Damage to oligodendrocytes

in the striatum after MPTP neurotoxicity in mice. J Neural Transm 114:1553-1557. Teismann P, Schulz JB (2004) Cellular pathology of Parkinson's disease: astrocytes,

microglia and inflammation. Cell Tissue Res 318: 149-161. Tenovuo O, Rinne UK, Viljanen MK (1984) Substance P immunoreactivity in the post-

mortem parkinsonian brain. Brain Res 303:113-116. Testa CM, Sherer TB, Greenamyre JT (2005) Rotenone induces oxidative stress and

dopaminergic neuron damage in organotypic substantia nigra cultures. Brain Res Mol Brain Res 134:109-118.

Thomas DM, Kuhn DM (2005) Attenuated microglial activation mediates tolerance to the

neurotoxic effects of methamphetamine. J Neurochem 92:790-797. Tillerson JL, Caudle WM, Reveron ME, Miller GW (2003) Exercise induces behavioural

recovery and attenuates neurochemical deficits in rodent models of Parkinson's disease. Neurosci 119:899-911.

Tominaga M, Tominaga T (2005) Structure and function of TRPV1. Pflugers Arch

451:143-150. Torreilles F, Salman-Tabcheh S, Guerin M, Torreilles J (1999) Neurodegenerative

disorders: the role of peroxynitrite. Brain Res Brain Res Rev 30:153-163. Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM

(2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135:162-168.

433

Turner R, Vink R (2007) Inhibition of neurogenic inflammation as a novel treatment for ischemic stroke. Drug News Perspect 20:221-226.

Turner RJ, Blumbergs PC, Sims NR, Helps SC, Rodgers KM, Vink R (2006) Increased

substance P immunoreactivity and edema formation following reversible ischemic stroke. Acta Neurochir Suppl 96:263-266.

Ukai M, Mori E, Kameyama T (1995) Effects of centrally administered neuropeptides on

discriminative stimulus properties of cocaine in the rat. Pharmacol Biochem Behav 51:705-708.

Ungerstedt U (1968) 6-hydroxy-dopamine induced degeneration of central monoamine

neurons. Eur J Pharmacol 5:107-110. Ungerstedt U, Arbuthnott GW (1970) Quantitative recording of rotational behavior in rats

after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 24:485-493.

van den Buuse M, Zheng TW, Wlaker LL, Denton DA (2005) Angiotensin-converting

enzyme (ACE) interacts with dopaminergic mechanisms in the brain to modulate prepulse inhibition in mice. Neurosci Lett 380:6-11.

van der Stelt M, Di Marzo V (2003) The endocannabinoid system in the basal ganglia and

in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur J Pharmacol 480:133-150.

Varshavskaya VM, Ivanova ON, Yakimovskii AF (2004) Motor behavior in rats after

separate and combined administration of GABAergic agents into the neostriatum. Neurosci Behav Physiol 34:293-298.

Velazquez RA, McCarson KE, Cai Y, Kovacs KJ, Shi Q, Evensjo M, Larson AA (2002)

Upregulation of neurokinin-1 receptor expression in rat spinal cord by an N-terminal metabolite of substance P. Eur J Neurosci 16:229-241.

Vernon AC, Palmer S, Dalta KP, Zbarsky V, Croucher MJ, Dexter DT (2005)

Neuroprotective effects of metabotropic glutamate receptor ligands in a 6-hydroxydopamine rodent model of Parkinson's disease. European Journal of Neuroscience 22:1799-1806.

Vila M, Vukosavic S, Jackson-Lewis V, Neystat M, Jakowec M, Przedborski S (2000)

Alpha-synuclein up-regulation in substantia nigra dopaminergic neurons following administration of the parkinsonian toxin MPTP. J Neurochem 74:721-729.

Vink R, Donkin JJ, Cruz MI, Nimmo AJ, Cernak I (2004) A substance P antagonist

increases brain intracellular free magnesium concentration after diffuse traumatic brain injury in rats. J Am Coll Nutr 23:538S-540S.

Vink R, Young A, Bennett CJ, Hu X, Connor CO, Cernak I, Nimmo AJ (2003)

Neuropeptide release influences brain edema formation after diffuse traumatic brain injury. Acta Neurochir Suppl 86:257-260.

434

Wade TV, Schneider JS (2001) Expression of striatal preprotachykinin mRNA in symptomatic and asymptomatic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-exposed monkeys is related to parkinsonian motor signs. J Neurosci 21:4901-4907.

Wallace BA, Ashkan K, Heise CE, Foote KD, Torres N, Mitofanis J, Benabid AL (2007)

Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP treated monkeys. Brain 130:2129-2145.

Walsh RN, Cummins RA (1976) The open-field test: A critical review. Psychological

Bulletin 83:482-504. Wardas J, Peitraszek M, Wolfarth S, Ossowska K (2003) The role of metabotropic

glutamate receptors in regulation of striatal proenkephalin expression: Implications for the therapy of Parkinson’s disease. Neurosci 122:747-756.

Wenk GL, Rance NE, Mobley SL (1995) Effects of excitatory amino acid lesions upon

neurokinin B and acetylcholine neurons in the nucleus basalis of the rat. Brain Res 679:8-14.

Westerink B (1979) The effects of drugs on dopamine biosynthesis and metabolism in the

brain. In: The Neurobiology of Dopamine (Horn A, Korf J, Westerink B, eds), pp 256-285. London: Academic Press.

Woie K, Koller ME, Heyeraas KJ, Reed RK (1993) Neurogenic inflammation in rat

trachea is accompanied by increased negativity of interstitial fluid pressure. Circ Res 73:839-845.

Wojtera M, Sikorska B, Sobow T, Liberski PP (2005) Microglial cells in

neurodegenerative disorders. Folia Neuropathol 43:311-321. Wolters EC (2001) Intrinsic and extrinsic psychosis in Parkinson's disease. J Neurol 248

Suppl 3:III22-27. Wong CG, Bottiglieri T, Snead OC, 3rd (2003) GABA, gamma-hydroxybutyric acid, and

neurological disease. Ann Neurol 54 Suppl 6:S3-12. Yelnik J (2002) Functional anatomy of the basal ganglia. Mov Disord 17 Suppl 3:S15-21. Yip J, Chahl LA (2000) Localization of tachykinin receptors and fos-like

immunoreactivity induced by substance P in guinea pig brain. Clinical and Experimental Pharmacology and Physiology 27:943-946.

Yu J, Cadet JL, Angulo JA (2002) Neurokinin-1 (NK-1) receptor antagonists abrogate

methamphetamine-induced striatal dopaminergic neurotoxicity in the murine brain. J Neurochem 83:613-622.

Yuan H, Sarre S, Ebinger G, Michotte Y (2004) Neuroprotective and neurotrophic effect

of apomorphine in the striatal 6-OHDA-lesion rat model of Parkinson's disease. Brain Res 1026:95-107.

435

Yuan H, Sarre S, Ebinger G, Michotte Y (2005) Histological, behavioural and neurochemical evaluation of medial forebrain bundle and striatal 6-OHDA lesions as rat models of Parkinson's disease. J Neurosci Methods 144:35-45.

Zecca L, Wilms H, Geick S, Claasen JH, Brandenburg LO, Holzknecht C, Panizza ML,

Zucca FA, Deuschl G, Sievers J, Lucius R (2008) Human neuromelanin induces neuroinflammation and neurodegeneration in the rat substantia nigra: implications for Parkinson's disease. Acta Neuropathol 116:47-55.

Zgaljardic DJ, Foldi NS, Borod JC (2004) Cognitive and behavioral dysfunction in

Parkinson's disease: neurochemical and clinicopathological contributions. J Neural Transm 111:1287-1301.

Zhang X, Xie W, Qu S, Pan T, Wang X, Le W (2005) Neuroprotection by iron chelator

against proteasome inhibitor-induced nigral degeneration. Biochem Biophys Res Commun 333:544-549.

Ziv I, Zilkha-Falb R, Offen D, Shirvan A, Barzilai A, Melamed E (1997) Levodopa

induces apoptosis in cultured neuronal cells--a possible accelerator of nigrostriatal degeneration in Parkinson's disease? Mov Disord 12:17-23.