Environmental Physiology of Livestock (Collier/Environmental Physiology of Livestock) || Regulation of Acclimation to Environmental Stress

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BLBS093-c04 Collier October 29, 2011 10:11 Trim: 244mm×172mm

Chapter 4

Regulation of Acclimation toEnvironmental StressKajal Sankar Roy and Robert J. Collier

What Is Acclimation?

A variety of environmental factors such as ambient temperature, solar radiation, relativehumidity, and wind speed are known to have direct and indirect effects on domestic animals(Collier et al., 1982, 2004, 2005). The direct effects involve impacts of the environment onthermoregulation, the endocrine system, metabolism, production, and reproduction. Indirecteffects include impacts of the environment on food and water availability, pest and pathogenpopulations, and resistance of the immune system to immunologic challenges. Animals havedeveloped coping mechanisms to minimize the impact of these environmental stressors on theirbiological systems. These responses are broadly described as acclimation, acclimatization, andadaptation. Acclimation is the coordinated phenotypic response developed by the animalto a specific stressor in the environment (Fregley, 1996), while acclimatization refers tothe coordinated response to several individual stressors simultaneously (e.g., temperature,humidity, and photoperiod; Bligh, 1976). In general, there is hardly ever a case in the naturalenvironment where only one environmental variable changes. Thus, in the vast majority ofcases the animal is undergoing acclimatization to the changing environment. Acclimation andacclimatization involve phenotypic and not genotypic change, and the acclimation responseswill decay if the stress is removed. The overall impact of acclimation and acclimatization is toimprove the fitness of the animal in the environment. In many cases the acclimation response isinduced by sudden environmental change. In other examples the acclimation response is drivenby changes in photoperiod or other environmental cues such as the lunar cycle, which permit theanimal to “anticipate” the coming change in the environment leading to seasonal acclimationadjustments in insulation (coat thickness, fat deposition), feed intake, or reproductive activityin advance of the actual environmental change. However, in every case, the process is drivenby the endocrine system and is “homeorhetic.” Homeorhesis is defined as the “coordination of

Environmental Physiology of Livestock, First Edition. Edited by R. J. Collier and J. L Collier.C© 2012 John Wiley & Sons, Inc. Published 2012 by John Wiley & Sons, Inc.

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50 Environmental Physiology of Livestock

metabolism to support a specific physiologic state” (Bauman and Currie, 1984). In this casethe specific physiologic state is the “acclimatized animal.”

Adaptation: Bos indicus versus Bos taurus

If environmental stressors are present for prolonged periods of time (e.g., years) the metabolicand physiologic adjustment can become “fixed genetically” and we refer to this state as the“adapted” state of animal. Examples are Bos indicus breeds of cattle, which have evolved underconditions of high temperature and humidity and display a number of genetic differences thatendow them with improved thermotolerance, compared to Bos taurus breeds of cattle, whichevolved under temperate weather conditions.

Bos indicus cattle have greater thermoregulatory capability than Bos taurus. As pointedout by Hansen (2004), Bos indicus cattle produce less heat, have increased capacity to loseheat toward the environment, or a combination of both. This suggests that low metabolic ratesresulting from reduced growth rates and milk yields of many Indicus breeds constitute a majorcontributing factor to thermotolerance. The basal metabolic rate of B. indicus is in fact lowerthan that for B. taurus (Finch, 1985). The physiological and cellular basis for this differencehas not been identified. One possibility for improved heat loss in B. indicus is that the density ofarteriovenous anastomoses is higher in B. indicus. Since these structures have lower resistanceto flow than vascular passages involving capillary networks, they facilitate increased bloodflow to the skin during heat stress (Hales et al., 1978).

The vascularity and degree of insulation of the skin and quality of the hair coat (hair andskin coat color, thickness and density of hair fibers) also contribute to the effectiveness ofheat loss in cattle (Gebremedhin et al., 2008, 2010). All of these are affected by breed andcontribute to well-known genotype × environment effects.

The actual rate of heat loss via sweating depends not only upon the extrusion of water at theskin surface but also upon the evaporation of that water. It has been observed that evaporativeheat loss rates were less affected by humidity for Indicus cows than for Holstein and BrownSwiss cows. For example, studies showed that the sweating rate in Indicus cattle exposedto heat stress was unaffected by humidity of the surrounding air while the sweating rate ofShorthorn cattle was reduced as humidity increased (Finch, 1985). This result was interpretedas reflecting the greater trapping of humidified air in the dense hair coat of the Shorthorns.There is no evidence that respiratory capacity for heat loss is superior for Indicus cattle. Theproportion of evaporative heat lost via respiration was roughly similar for Indicus, Holstein,Jersey, and Brown Swiss (Kibler and Brody, 1952). During heat stress, evaporative heat loss viarespiration rate can be greater for European breeds and this occurrence also probably reflectsthe greater engagement of heat loss mechanisms for the less-adapted breeds.

There is a general belief that the appendages of B. indicus cattle contribute to their superiorthermoregulatory ability, as the appendages increase the surface area per unit body weight ascompared to B. taurus. The actual importance of these anatomical features is not likely to becrucial for thermoregulation because surgical removal of the dewlap or hump of Red Sindhibulls did not have a measurable impact on thermoregulatory ability (McDowell et al., 1958).Additionally, differences in regulation of rectal temperature in response to heat stress wereobserved between Jersey and Red Sindhi × Jersey even though surface area per unit bodyweight or metabolic body weight was similar between the two genotypes.

Heat stress has less severe effects on semen quality of Indicus bulls than it does on bulls ofEuropean breeds, and this phenomenon reflects not only adaptations that affect whole-body

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Regulation of Acclimation to Environmental Stress 51

thermoregulation but also specific adaptations that enhance the local cooling of blood enteringthe testis. A study by Brito et al. (2004) demonstrated that the anatomical features of thetesticular thermoregulatory system differed between Nelore, crossbred (5/8 or 5/16 Charolais ×Zebu) and Angus bulls. For example, the ratio of testicular artery length to testicular volumewas greatest for Nelore bulls, intermediate for crossbred bulls, and least for Angus bulls. Inaddition, the testicular artery wall thickness and the distance between arterial–venous bloodin the testicular vascular cone were least in Nelore, intermediate in crossbreds, and greatestin Angus. These anatomical differences were related to differences in testicular intra-arterialtemperature, which was lowest in Nelore, intermediate in crossbreds, and highest in Angus(Brito et al., 2004).

When animals are adapted the physiologic differences between them and non-adaptedanimals do not disappear when the environment changes. This is not the case in acclimationwhere differences do disappear if the stress is removed. However, it is becoming clear that thesame systems that are involved in acclimatization are the systems that endow animals withthermotolerance or adaptation to heat. Therefore, obtaining a better understanding of the genenetworks involved in response to environmental stress will also lead us to those pathwayswhich offer promise to improve thermotolerance.

Acclimatization requires several days to weeks to fully develop, there is a hormonal linkbetween the central nervous system and the effector cell types involved, and the effect ofthe hormonal change is to alter the responsiveness of the effector cells to environmentalchange (Bligh, 1976). These key features are hallmarks of a homeorhetic process in whichmetabolism of multiple tissues and organs is coordinated to support the new acclimatizedstate as contrasted to a homeostatic process (Bauman and Currie, 1984; Collier et al., 2004),and where regulation is occurring around a set point. We then need to consider the stages ofacclimation, the hormones that are driving acclimation, and what changes are occurring ineffector tissues to accomplish development of the acclimatized state.

What Are the Stages of Acclimation?

Acclimatization is generally considered to occur in two stages: acute or short term and chronicor long term (Johnson and Vanjonack, 1976; Horowitz, 2002; Garrett et al., 2009). Theacute phase includes a shock response at the cellular level (Carper et al., 1987; Sonna,2002) and homeostatic endocrine, physiological, and metabolic responses at the systemiclevel. The chronic or long-term phase results in acclimation to the stressor and involves thereprogramming of gene expression and metabolism (Horowitz, 2002; Collier et al., 2006).

In agricultural animals there is generally a loss in productivity as animals progress throughthe acute phase and some or even all of this productivity is restored as animals undergoacclimation to the stress.

What Is Involved in the Systemic Response?

The systemic response to environmental stress is driven by two systems: (1) the central nervoussystem (CNS) and (2) peripheral nervous system and endocrine components (Charmandariet al., 2005). The central component is comprised of nuclei in the hypothalamus and thebrainstem, which release corticotropin-releasing hormone (CRH) and arginine vasopressin(AVP). The peripheral components of the stress system include the pituitary-adrenal axis,

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the efferent sympathetic-adrenomedullary system, and components of the parasympatheticsystem (Habib et al., 2001). However, relative to environmental stress and acclimation, theinitial phases of the response involve receptor systems at the periphery that drive autonomicand endocrine responses to the changing environment (e.g., skin thermoreceptors andphotoreceptors in the retina).

Sweating and panting are two of the primary autonomic responses exhibited by animalsunder heat stress. Sweating results in increased evaporative heat loss from the skin surface,whereas in panting, sensible heat from the body core is used to heat the water vapor and expelheat in the form of vaporized moisture from the lungs. However, these responses are likelydriven more by surface temperatures than core body temperatures. As shown in Figures 4.1and 4.2, evaporative heat loss from skin and the respiratory tract is highly correlated with skintemperature. In fact, skin temperature is more highly correlated with these parameters thancore temperature suggesting that thermal receptors in the skin initiate the autonomic systemicresponse to thermal stress. Another potential route of information flow from the surface to thewhole system would be via secreted heat shock protein (HSP) released from skin epitheliumduring heat stress, which would act as an alarm system to assist in mobilizing the acute responseto thermal shock. An examination of the relationship between skin temperature and expressionof the gene for inducible heat shock protein 70 (see Fig. 4.3) revealed that gene expression isincreased several-fold as skin temperature approaches 35◦C, which is below body temperaturebut represents the upper limit of the thermoneutral zone of cattle. Berman (2005) estimated thatthe stress response system in cattle would be activated at effective temperatures at and above35◦C. Previously, it has been demonstrated that evaporative heat loss and rectal temperaturerise dramatically above an effective environmental temperature of 35◦C (see figs. 4.1 and 4.2;Collier et al., 2008). It is now apparent that the heat shock response in bovine skin epithelialtissue is activated at effective environmental temperature of 35◦C as well. Activation of theheat shock response in cells in many cases leads to secretions of HSPs into the extracellularspace and plasma (Ireland et al., 2007).

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Figure 4.1. Correlation of left side surface temperature and respiration rate in Holstein cows in asemi-arid environment.

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y = 1.1665x2 – 64.166x + 894.35R2 = 0.4348

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Figure 4.2. Relationship between infrared coat surface temperature and evaporative heat loss (EVHL)in Holstein dairy cows. Open circles and regression correlation (R2 = 0.4348) denote EVHL below35◦C. Closed circles and regression correlation (R2 = 0.0358) denote EVHL above 35◦C. Slopes of tworegressions differ, P < 0.001.

Figure 4.3. Relationship between skin temperature and fold increases in heat shock protein 70 geneexpression in cattle skin.

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Recently, secreted heat shock protein was identified in plasma of cattle. Kristenson andcolleagues (2004) in Australia have demonstrated that secreted HSP concentrations rise inplasma when the effective environmental temperature exceeds 35◦C (Gaughan and Bonner,2009). Thus, activation of the heat shock response in cells also leads to secretion of HSPs intothe extracellular space and plasma (Ireland et al., 2007). It has been hypothesized that secretedheat shock protein acts as an alarm signal for the immune system and several measures ofinnate immunity are increased following increases in secreted heat shock protein in blood(Fleshner and Johnson, 2005). Secreted heat shock protein has also been shown to improvesurvival of neural cells subjected to environmental and metabolic stressors (Tytell, 2005;Guzhova et al., 2001).

Thus, the acute response in cattle is initially driven by thermal receptors in skin thatactivate the CNS and subsequently, the endocrine system and the peripheral components of theautonomic system. This response is augmented by secreted HSPs that rapidly rise in plasmaand are believed to provide protective effects to a variety of cell types as well as activatingthe innate immune system. At a skin surface temperature of 35◦C the respiration rate of cattlewill reach or exceed half maximal which is about 60 to 70 breaths per minute (see Fig. 4.1).At this point, the animal is entering the acute phase of the stress response.

During the acute phase there is rapid decline in productivity of domestic animals and thisis especially true in high producing dairy cows. The decline in productivity begins on the daythe stress is initiated but is not maximal until 48 hours following the initiation of the stress(Collier et al., 1981). This suggests there are intermediate events between the rise in bodytemperature and the reduction in milk yield. Rhoads et al. (2009) demonstrated that reducedfeed intake only accounted for 40% of the decline in milk yield and that other factors werelikely involved in the rapid decline in production to severe heat stress. They postulated thatreduced glucose availability could potentially reduce lactose synthesis rates and contribute tothe reduced milk volume. Silanikove et al. (2009) reported that acute heat stress reduced milksecretion in lactating cows by up-regulating the activity of a milk-borne negative feedbackregulatory system, specifically an n-terminal fragment of �-casein. They also reported thatthis fragment has an inhibitory activity on the mammary epithelial cell potassium channel.Identification of the exact mechanisms by which milk yield is reduced in response to heatstress offers potential in improving productivity of animals in warm climates.

After five to seven days of continuous stress, animals enter the chronic “acclimation” phaseof the stress response. During this phase there is a reprogramming of metabolism resulting inaltered responses to homeostatic signals. The overall impact of these changes is a reduction inthe impact of the stress on the animal. The transition of animals from the acute to the chronicphase of the stress response has been extensively studied in laboratory models by Horowitzand coworkers (Horowitz, 2002; Horowitz et al., 2004; Maloyan et al., 2005; Horowitz, 2007).These changes are driven by the endocrine system and result in global changes in geneexpression as well as post-translational alterations in protein function. Hormones that havebeen identified as being homeorhetic regulators are also linked to acclimation responsesto thermal stress and changes in photoperiod related to season. These hormones includesomatotropin, prolactin, thyroid hormones, glucocorticoids, and mineralocorticoids. Severalof these hormones are known to contribute to regulation of HSP gene expression, as noted inTable 4.1. The changes that occur at the cellular level and provide improved cytoprotection aredescribed in the section on the cellular response to heat stress.

At the systemic level, metabolism is coordinated to support a new physiological state. Someof the changes that occur include a lowering of the threshold for vasodilation and evaporative

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Table 4.1. Partial list of hormones affecting heat shock protein (HSP) gene expression or protein activity

Hormone Effect Reference

ACTH Stimulates HSP production Blake et al. 1991,1994Insulin Stimulates HSP gene in cardiac tissue Li et al. 2006IGF-1 Increased HSPs in epidermis of IGF

transgenic miceShen et al. 2007

Prolactin Stimulates HSP-60 in rodent luteal cells Stocco et al. 2001Growth Hormone Stimulates HSP in whole blood of Sea

BreamDeane & Woo 2005

Glucocorticoids Increases cytosol HSPs and HSP geneexpression

Vijayan et al. 2003

Melatonin Increases HSP gene expression inpancreatic AR42J cells

Bonior et al. 2005

Leptin Down regulates HSP-70 in chicken liverand hypothalamus

Figueiredo et al. 2006

Vasopressin Stimulates HSP in renal tubular cells Xu et al. 1996Catecholamines Stimulates HSP in Brown Adipose tissue Matz et al. 1996Prostaglandin A Increased expression of HSP in bovine Collier et al. 2007

Mammary epithelial cells & human K562 Amici et al. 1992Cells and human monocytes Elia et al. 1999

Estrogensa & Androgens Increased HSP gene expression in humanneurons

Zhang et al. 2004

Adapted from Collier et al. (2008).

cooling (Roberts et al., 1977), reduced metabolic rate, increased resistance to thermal injury,and improved cardiac performance (Horowitz, 2002). Endocrine changes occurring with ac-climation to heat stress in cattle include increased plasma prolactin, reduced glucocorticoid,somatotropin, and thyroxine concentrations, and in pregnant cattle endocrine changes led toincreased progesterone concentrations and decreased estrone sulfate concentrations (Collieret al., 2004). Somatotropin is a homeorhetic regulator and has been shown to be beneficialin improving evaporative heat loss and thermal balance in cattle during summer heat stress(Manalu et al., 1991). Despite large reductions in feed intake and energy balance during heatstress there appears to be a tighter coupling of the somatotropin-IGF axis during summer,resulting in higher IGF concentrations during summer months compared to winter months andonly slight decreases in plasma IGF to severe heat stress even when somatotropin concentra-tions are reduced (Collier et al., 2008; Rhoads et al., 2009). This fact reinforces the importanceof somatotropin in dealing with environmental stress (Collier et al., 2005). Additionally, thesomatotropin response to GRF is not affected by severe heat stress (Rhoads et al., 2009). Theseasonal variation in coupling of the growth hormone-IGF axis is also associated with effectsof increased photoperiod on growth rate and milk yield in cattle (Collier et al., 2006).

Cellular Heat Shock Responses

Heat tolerance at the cellular level is directly related to the ability of the cell to maintainelevated levels of heat shock proteins (HSPs). As stated by Horowitz and Assadi (2010), “Ahallmark of the acclimation process is the enhancement of cytoprotective networks – that ofthe heat shock proteins, anti-oxidative and apoptotic – and the stabilization of the HypoxiaInducible Factor (I�), the master regulator of oxygen homeostasis.”

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a

d e f

b c

Figure 4.4. Regression of ductal structures in response to 24 hours of heat stress; samples representthree separate cultures in which control samples (a, b, c) were cultured at 37◦C but were otherwise treatedidentical to the thermal stress (42◦C) samples (d, e, f).

The heat shock response of bovine embryos and mammary epithelial cells to heat stress hasbeen described (Edwards et al., 1997; Jousan and Hansen, 2004; Collier et al., 2006, 2008).The dramatic effect of heat shock on mammary epithelial cell growth and structure is shownin Figure 4.4. Heat shock acutely down-regulates DNA synthesis and adversely affects theability of cells to maintain their cytoskeleton, leading to a collapse of cell structure.

The transcriptome profile of heat-shocked bovine mammary epithelial cells indicated down-regulation of genes involved in cell structure, DNA synthesis, cell division, metabolism,biosynthesis, and intracellular transport, while genes associated with cellular and proteinrepair and degradation were up-regulated. The up-regulation of the heat shock family ofproteins during thermal stress is characterized in Figure 4.5 which displays the pattern ofHSP-70 gene expression during thermal shock. Also apparent in Figure 4.5 is the drop inexpression of HSP-70 message after four hours at 42◦C. At the cellular level, loss of HSPexpression coincides with loss of thermotolerance and initiation of apoptosis. The heat shockresponse is induced by accumulation of misfolded proteins in the cytoplasm and is mediatedby heat shock transcription factors (HSF; Voellmy and Boellmann, 2007). There are fourforms of HSF but HSF-1 is considered to be the primary transcription factor involved in theheat shock response (Akerfelt et al., 2007). Regulation of HSF-1 activity has been reportedto be largely controlled post-translationally and not at the level of synthesis/degradation ofthe transcription factor (Voellmy and Boellmann, 2007). Once activated, the HSF-1 monomertrimerizes with other HSF-1 molecules, which is essential for DNA binding (Sarge et al.,

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Figure 4.5. Effect of thermal stress (42◦C) on Heat Shock Protein 70 gene expression in culturedbovine mammary epithelial cells.

1993). The activated complex can then enter the nucleus and initiate transcription of heatshock proteins.

Thermal acclimation and thermal adaptation are associated with increased basal levels ofHSPs (Carpar et al., 1987; Kregel, 1992; Maloyan et al., 1999). Thermal acclimation andcyclopentenone prostaglandins have been shown to increase the DNA-binding activity ofHSF-1 leading to increased HSP gene transcription (Amici et al., 1992; Straus and Glass,2001; Ianaro et al., 2003; Buckley and Hofmann, 2002). Several investigators have shown thatheat acclimation also provides cross-tolerance against other types of stress such as hypoxia,ischemia, acidosis, and energy depletion (Horowitz, 2002; Kregel et al., 2002), and that HSF-1is involved in this process. Although there is little evidence for endocrine regulation of HSF-1gene expression activity there is substantial evidence that expression of heat shock proteinsand other cytoprotective proteins are modulated by the endocrine system. A partial list ofhormones affecting heat shock protein gene expression is shown in Table 4.1.

The separate evolution of Bos taurus, Bos indicus, and Sanga cattle has resulted in differinggenotypes of Bos indicus and Sanga cattle that confer improved thermotolerance comparedto Bos taurus cattle in both beef and dairy populations (Paula-Lopes et al., 2003; Hansen,2004). In addition, large genotype × environment interactions in dairy cattle for milk yield(Ceron-Munoz et al., 2004; Ravagnolo et al., 2000; Bohmanova et al., 2006) for Holsteincattle indicate that there is considerable opportunity to improve thermal resistance and per-formance in dairy cattle. These differences include thermoregulatory capability, feed intakeand production responses, and cellular differences in heat shock responses (Hansen, 2004;Collier et al., 2008).

There are genetic differences in cellular resistance to elevated temperature in cattle. Itis possible that the same gene or genes conferring cellular thermotolerance are present inIndicus, Senepol, and Romosinuano, especially because of the contribution of B. indicusgenotypes to these two other breeds (Magee et al., 2002). An alternative explanation is that

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distinct thermotolerance genes are present in the different genotypes. Identification of thegenes conferring cellular thermotolerance offers the possibility of transferring these genes toheat-sensitive breeds to improve reproduction and other physiological systems compromised byhyperthermia. Little is known regarding the molecular basis for the improved cellular resistanceto elevated temperature in thermotolerant cattle. There were no detectable differences betweenIndicus, Senepol, and Angus in the amount of heat shock protein 70 (HSP-70) in heat-shockedlymphocytes (Kamwanja et al., 1994) although the tendency for lower cellular concentrationof HSPs in Brahman and Senepol may indicate that protein denaturation in response toelevated temperature (one of the signals for HSP-70 synthesis; Shamovsky and Nudler, 2008).The capacity for transcription in response to elevated temperature seems to be importantfor expression of genetic differences because there were no differences between Indicus andHolstein embryos in resistance to elevated temperature at the two-cell stage, a time whenthe embryonic genome is largely inactive (Hansen, 2004). Also, in vitro effects of elevatedtemperature on spermatozoa were similar for Indicus, Indicus-influenced breeds, Angus, andHolstein (Block et al., 2002).

The cellular thermotolerance of crossbred embryos is dependent upon the genotype of theoocyte and not the spermatozoa. Embryos produced by insemination of Brahman oocytes withAngus spermatozoa were more thermotolerant than embryos produced by insemination ofHolstein oocytes with Angus semen (Block et al., 2002). In contrast, there were no differencesin thermotolerance between Indicus × Holstein embryos and Angus × Holstein embryos.These results indicate that either genes conferring thermotolerance are paternally imprinted(only the maternal allele is expressed) or thermotolerance in embryos depends upon somegenetically controlled factor produced in the oocyte. Regulation of body temperature is themost critical factor for genetic differences in reproductive function during heat stress sincethe depression in fertility per unit increase in body temperature is the same for B. indicus ×B. taurus crossbred cows as for Hereford × Shorthorn cows (Hansen, 2004).

New genomics tools are also beginning to provide information on specific gene networksassociated with thermotolerance. Lillehammer et al. (2009) identified single nucleotide poly-morphisms (SNPs) that were associated with gene × environment interactions for productiontraits in cattle. Hayes et al. (2009) also reported on a genome-wide association study aimedat identifying differences related to adaptation to environmental change. It is envisioned thatin the not too distant future use of SNP markers will lead to greater progress in improvingthermotolerance of high producing dairy breeds.

Conclusion

Acclimation is a homeorhetic process driven by the endocrine system, which enables animalsto respond to a stress. The resulting cellular, metabolic and systemic changes associated withacclimation reduce the impact of the stress on the animal and allow it to function moreeffectively in the stressful environment. These changes are lost if the stress is removed sothe process is not based on changes in the genome. However, if the stressful environment isnot removed over successive generations these changes will become “genetically fixed” andare referred to as adaptations. A better understanding of genetic differences between adaptedanimals will contribute useful information on the genes associated with acclimation. Likewise,study of gene expression changes during acclimation will assist in identifying genes associatedwith improved thermotolerance.

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References

Akerfelt, M, D Trouillet, V Mezger, and L Sistonen. 2007. Heat shock factors at a crossroadbetween stress and development. Ann NY Acad Sci. 1113:15–27.

Amici, C, L Sistonene, M Gabriella Santoro, and RI Morimoto. 1992. Antiproliferativeprostaglandins activate heat shock transcription factor. Proc Natl Acad Sci. 89:6227–6231.

Bauman, DE, and WB Currie, 1980. Partitioning of nutrients during pregnancy and lac-tation: A review of mechanisms involving homeostasis and homeorhesis. J Dairy Sci.63(9):1514–1529.

Berman, A. 2005. Estimates of heat stress relief needs for Holstein dairy cows. J Anim Sci.1377–1384.

Blake, MJ, R Udelsman, GJ Feulner, DD Norton, and NJ Holbrook. 1991. Stress-induced heatshock protein 70 expression in adrenal cortex: An adrenocorticotropic hormone-sensitive,age-dependent response. Proc Natl Acad Sci. 88:9873–9877.

Blake, MJ, AR Buckley, KP LaVoi, and T Bartlett. 1994. Neural and endocrine mechanisms ofcocaine-induced 70k-Da heat shock protein expression in aorta and adrenal gland. J Phar-macol Exper Ther. 268:522–529.

Bligh, J. 1976. Introduction to acclimatory adaptation-including notes on terminology. In:J Bligh, JL Cloudsley-Thompson, and AG Macdonald, editors. Environmental Physiologyof Animals. New York: John Wiley and Sons. p.219–229.

Block, J, CC Chase, and PJ Hansen. 2002. Inheritence of resistance of bovine preimplantationembryos to heat shock: Relative importance of the maternal versus paternal contribution.Mol Reprod Dev. 63:32–37.

Bohmanova, J, I Misztal, S Tsuruta, HD Norman, and TJ Lawlor. 2006. Short Communication:Genotype by environment interaction due to heat stress. J Dairy Sci. 91:840–846.

Bonior, J, J Jaworek, SJ Konturek, and WW Pawlik. 2005. Increase of heat shock protein geneexpression by melatonin in AR42J cells. J Physiol and Pharmacol. 56:471–481.

Brito, LF, AE Silva, RT Barbosa, and JP Kastelic. 2004. Testicular thermoregulation in Bosindicus, crossbred and Bos taurus bulls: relationship with scrotal, testicular vascular cone andtesticular morphology and effects on semen quality and sperm production. Theriogenology.15:511–528.

Buckley, BA, and GE Hofmann. 2002. Thermal acclimation changes DNA-binding activityof heat shock factor 1 (HSF1) in the goby Gillichthys mirabilis: implications for plasticityin the heat-shock response in natural populations. J Exper Bio. 205:3231–3240.

Carper, SW, JJ Duffy, and EW Gerner. 1987. Perspectives in Cancer: Heat Shock Proteins inThermotolerance and Other Cellular Processes. Canc Res. 47:5249–5255.

Ceron-Munoz M, H Tonhati, CN Costa, D Rojas-Sarmiento, and DM Echeverri. 2004. Factorsthat cause genotype by environment interaction and use of a multiple-trait herd-clustermodel for milk yield of Holstein cattle from Brazil and Colombia. J Dairy Sci. 87:2687–92.

Charmandari, E, C Tsigos, and G Chrousos. 2005. Endocrinology of the stress response. AnnuRev Physiol. 67:259–284.

Collier, R J, RM Eley, AK Sharma, RM Pereira, and DE Buffington. 1981. Shade managementin subtropical environment for milk yield and composition in Holstein and Jersey cows.J Dairy Sci. 64:844–849.

Collier, RJ, DK Beede, WW Thatcher, LA Israel, and CJ Wilcox. 1982. Influences of environ-ment and its modification on dairy animal health and production. J Dairy Sci. 65:2213–2227.

P1: SFK/UKS P2: SFK



Collier, RJ, LH Baumgard, AL Lock, and D Bauman. 2005. Physiological Limitations, NutrientPartitioning. In: R Sylvester-Bradley, and J Wiseman, editors. Yields of Farmed Species:Constraints and Opportunities in the 21st Century. p.351–377.

Collier, RJ, GE Dahl, and MJ VanBaale. 2006. Major advances associated with environmentaleffects on dairy cattle. J Dairy Sci Centenial Issue. 89:1244–1253.

Collier, JL, MB Abdallah, LL Hernandez, JV Norgaard, and RJ Collier. 2007. ProstaglandinsA1 (PGA1) and E1 (PGE1) alter heat shock protein 70 (HSP-70) gene expression in bovinemammary epithelial cells (BMEC). J Dairy Sci. 90:Suppl 1. p.62

Collier, RJ, JL Collier, RP Rhoads, and LH Baumgard. 2008. Invited review: Genes involvedin the bovine heat stress response. J Dairy Sci. 91(2):445–454.

Collier, RJ, MA Miller, CL McLaughlin, HD Johnson, and CA Baile. 2008. Effects of recom-binant bovine somatotropin (rbST) and season on plasma and milk insulin-like growthfactors I (IGF-I) and II (IGF-II) in lactating dairy cows. Dome Anim Endocrin. 35:16–23.

Collier, RJ, CM Stiening, BC Pollard, MJ VanBaale, LH Baumgard, PC Gentry, and PMCoussens. 2006. Use of gene expression microarrays for evaluating environmental stresstolerance at the cellular level in cattle. J Anim Sci. 84(E. Suppl.):E1–E13.

Deane, EE, and NY Woo. 2005. Growth hormone increases hsc70/hsp70 expression andprotects against apoptosis in whole blood preparations from silver sea bream. Ann NYAcad Sci. 1040:288–292.

Edwards, JL, AD Ealy, VH Monterroso, and PJ Hansen. 1997. Ontogeny of temperature-regulated heat shock protein 70 synthesis in preimplantation bovine embryos. Mol ReprodDev. 48:25–33.

Elia, G, B Polla, A Rossi, and MG Santoro. 1999. Induction of ferritin and heat shock proteinsby prostaglandin A1 in human monocytes. Eur J Biochem. 264:736–745.

Figueiredo, D, A Gertler, G Cabello, E Decuypere, J Buyse, and S Dridi. 2007. Leptin downreg-ulates heat shock protein-70 (HSP-70) gene expression in chicken liver and hypothalamus.Cell Tiss Res. 329(1):91–101.

Finch, VA. 1985. Comparison of non-evaporative heat transfer in different cattle breeds. AustJ Agric Res. 36:497–508.

Fleshner, M, and JD Johnson. 2005. Endogenous extra-cellular heat shock protein 72: Releas-ing signal(s) and function. Int J Hyperthermia. 21:457–471.

Fregley, MJ. 1996. Adaptations: Some general characteristics. In: MJ Fregley and CM Blatteis,editors. Handbook of Physiology, Section 4: Environmental Physiology. Vol I. Oxford:Oxford University Press. p.3–15.

Garrett, AT, NG Goosens, NG Rehrer, MJ Patterson, and JD Cotter. 2009. Induction and decayof short-term heat acclimation. Eur J Appl Physiol. 107:659–670.

Gaughan JB, and S Bonner. 2009. HSP 70 expression in cattle exposed to hot climaticconditions. In: Proceedings 4th International Congress on Stress Responses in Biology andMedicine, Sapporo Japan. p.231.

Gebremedhin, KG, PE Hillman, CN Lee, RJ Collier, ST Willard, J Arthington, andTM Brown-Brandl. 2008. Sweating rates of dairy cows and beef heifers in hot conditions.Trans ASABE. 51:1693–1697.

Gebremedhin, KG, CN Lee, PE Hillman, and RJ Collier. 2010. Physiological responses ofdairy cows during extended solar exposure. Trans ASABE. 53:239–247.

Guzhova, I, K Kislyakova, O Moskaliova, I Fridlanskaya, M Tytell, M Cheetham, andB Margulis. 2001. In vitro studies show that HSP70 can be released by glia and thatexogenous Hsp70 can enhance neuronal stress tolerance. Brain Res. 914:66–73.

P1: SFK/UKS P2: SFK



Habib, KE, PW Gold, and GP Chrousos. 2001. Neuroendocrinology of stress. EndocrinolMetab Clin North Am. 30:695–728.

Hales, JR, AA Fawcett, JW Bennett, and AD Needham. 1978. Thermal control of bloodflow through capillaries and arteriovenous anastomoses in skin of sheep. Pflugers Arch.378:55–63.

Hansen, PJ. 2004. Physiological and cellular adaptations of zebu cattle to thermal stress. AnimReprod Sci. 82-83:349–360.

Horowitz, M. 2002. From molecular and cellular to integrative heat defense during exposureto chronic heat. Comp Biochem Physiol A. Mol Integr Physiol. 131(3):475–483.

Horowitz, M. 2007. Heat acclimation and cross-tolerance against novel stressors: genomic-physiological linkage. Prog Brain Res. 162:373–392.

Horowitz, M, and H Assadi. 2010. Heat acclimation-mediated cross-tolerance in cardiopro-tection: Do HSP70 and HIF-1a play a role? Ann N Y Acad Sci. (1188):199–206.

Horowitz, M, L Eli-Berchoer, I Wapinski, N Friedman, and E Kodesh. 2004. Stress-relatedgenomic responses during the course of heat acclimation and its association with ischemic-reperfusion cross-tolerance. J Appl Physiol. 97:1496–1507.

Horowitz, M, and SD Robinson. 2007. Heat shock proteins and the heat shock responseduring hyperthermia and its modulation by altered physiological conditions. Prog BrainRes. 162:433–436.

Ianaro, A, A Ialenti, P Maffia, P Di Meglio, M Di Rosa, and MG Santoro. 2003. Anti-Inflammatory activity of 15-Deoxy-D12,14-PGJ2 and 2-Cyclopenten-1-one: Role of the heatshock response. Mol Pharmacol. (64):85–93.

Ireland, HE, F Leoni, O Altaie, CS Birch, RC Coleman, C Hunter-Lavin, and JHH Williams.2007. Measuring the secretion of heat shock proteins from cells. Methods. 43(176):183.

Johnson, HD, and WJ Vanjonack. 1976. Effects of environmental and other stressors on bloodhormone patterns in lactating animals. J Dairy Sci. 59:1603–1617.

Jousan, FD, and PJ Hansen. 2004. Insulin-like growth factor-I as a survival factor forthe bovine preimplantation embryo exposed to heat shock. Biol Reprod. 71(5):1665–1670.

Kamwanja, LA, CC Chase, JA Gutierrez, V Guerriero, TA Olson, and AC Hammond. 1994.Responses of bovine lymphocytes to heat shock as modified by breed and antioxidant status.J Anim Sci. 72:438–444.

Kibler, HH, and S Brody. 1952. Environmental physiology with special reference to domesticanimals XIX. Relative efficiency of surface evaporative, respiratory evaporative and non-evaporative cooling in relation to heat production in Jersey, Holstein, Brown Swiss andBrahman cattle, 5◦ to 105◦F. Mo Res. Bull 497.

Kregel, KC. 2002. Molecular biology of thermoregulation Invited Review: Heat shock pro-teins: modifying factors in physiological stress responses and acquired thermotolerance.J Appl Physiol. 92:2177–2186.

Kristenson, TN, P Lovendahl, P Berg, and V Loeschcke. 2004. HSP72 is present in plasmafrom Holstein-Friesian dairy cattle, and the concentration level is repeatable across daysand age classes. Cell Stress Chaperones. 9:143–149.

Li, G, IS Ali, and RW Currie. 2006. Insulin induces myocardial protection and HSP70localization to plasma membranes in rat hearts. Am J Physiol Heart Circ Physiol.291:H1709–H1721.

Lillehammer, M, BJ Hayes, THE Meuwissen, and ME Goddard. 2009. Gene by environ-ment interactions for production traits in Australian dairy cattle. J. Dairy Sci. 92:4008–4017.

P1: SFK/UKS P2: SFK



Magee, DA, C Meghen, S Harrison, CS Troy, T Cymbron, C Gaillard, A Morrow, JC Maillard,and DG Bradley. 2002. A partial African ancestry for the creole cattle populations of theCaribbean. J Hered. 93:429–432.

Maloyan, A, A Palmon, and M Horowitz. 1999. Heat acclimation increases basal HSP72 leveland alters its produciton dynamics during heat stress. Am J Physiol Regul Integr CompPhysiol. 276:R1506–R1515.

Maloyan, A, L Eli-Berchoer, GL Semenza, G Gerstenblith, MD Stern, and M Horowitz. 2005.HIF-1a-targeted pathways are activated by heat acclimation and contribute to acclimation-ischemic cross-tolerance in the heat. Physiol Genomics. 23:79–88.

Manalu, W, HD Johnson, R Li, BA Becker, and RJ Collier. 1991. Assessment of thermal statusof somatotropin-injected lactating Holstein cows maintained under controlled-laboratorythermoneutral, hot and cold environments. J Nutr. 121:2006–2019.

Matz, JM, KP LaVoi, and MJ Blake. 1996. Adrenergic regulation of the heat shock responsein brown adipose tissue. J Pharmacol Exp Ther. 277:1751–1758.

McDowell, RE. 1958. Physiological approaches to animal climatology. J Hered. 49:52–61.Paula-Lopes, FF, CC Chase, Jr, YM Al-Katanani, CE Krininger III, RM Rivera, S Tekin,

AC Majewski, OM Ocon, TA Olson, and PJ Hansen. 2003. Genetic divergence in cellularresistance to heat shock in cattle: differences between breeds developed in temperate ver-sus hot climates in responses of preimplantation embryos, reproductive tract tissues andlymphocytes to increased culture temperatures. Reproduction. 125:285–294.

Ravagnolo, O, I Misztal, and G Hoogenboom. 2000. Genetic component of heat stress in dairycattle, development of heat index function. J Dairy Sci. 83:2120–2125.

Rhoads, ML, RP Rhoads, MJ VanBaale, RJ Collier, SR Sanders, WJ Weber, BA Crooker,and LH Baumgard. 2009. Effects of heat stress and plane of nutrition on lactating holsteincows: I. Production, metabolism, and aspects of circulating somatotropin. J Dairy Sci.92:1986–1997.

Roberts, MF, CB Wenger, JAJ Stolwijk, and ER Nadel. 1977. Skin blood flow and sweatingchanges following exercise training and heat acclimatization. J Appl Physiol. 43:133–137.

Sarge, KD, SP Murphy, RI, and RI Morimoto. 1993. Activation of heat shock gene transcriptionby heat shock factor 1 involves oligomerization,acquisition of DNA-binding activity, andnuclear localization and can occur in the absence of stress. Mol Cell Biol. 13:1392–1407.

Shamovsky, I, and E Nudler. 2008. New insights into the mechanism of heat shock responseactivation. Cell Mol Life Sci. 65:855–861.

Shen, J, PK Riggs, SC Hensley, LJ Schroeder, AR Traner, KJ Kochan, MD Person, andJ DiGiovanni. 2007. Differential expression of multiple anti-apoptotic proteins in epidermisof IGF-1 transgenic mice as revealed by 2-dimensional gel electrophoresis/mass spectrom-etry analysis. Molec Carcinogenesis. 46:331–340.

Silanikove, N, F Shapiro, and D Shinder. 2009. Acute heat stress brings down milk secretionin dairy cows by up-regulating the activity of the milk-borne negative feedback regulatorysystem. BMC Physiology. 9(13).

Sonna, LA, J Fujita, SL Gaffin, and CM Lilly. 2002. Molecular Biology of ThermoregulationInvited Review: Effects of heat and cold stress on mammalian gene expression. J ApplPhysiol. 92:1725–1742.

Stocco, C, E Callegari, and G Gibori. 2001. Opposite effect of prolactin and prostaglandin F2�

on the expression of luteal genes as revealed by rat cDNA expression array. Endocrinology.142:4158–4161.

Straus, DS, and CK Glass. 2001. Cyclopentenone prostaglandins: New insights on biologicalactivities and cellular targets. Med Res Rev. (3):185–210.

P1: SFK/UKS P2: SFK



Tytell, M. 2005. Release of heat shock proteins (HSPs) and the effects of extracellular Hspson neural cells and tissues. Int J Hyperthermia. 21:445–455.

Vijayan, MM, S Raptis, and R Sathiyaa. 2003. Cortisol treatment affects glucocorticoid recep-tor and glucocorticoid responsive genes in the liver of rainbow trout. Gen Comp Endocrinol.132:256–263.

Voellmy, R, and F Boellmann. 2007. Chaperone Regulation of the Heat Shock Protein Re-sponse. In: P Csermely and L Vigh, editors. Molecular Aspects of the Stress Response:Chaperones, Membranes and Networks. Landes Bioscience and Springer Science. p.89–99.

Xu, Q, L Ganju, TW Fawcett, and NJ Holbrook. 1996. Vasopressin-induced heat shock proteinexpression in renal tubular cells. Lab Invest. 74:178–187.

Zhang, Y, N Champagne, LK Beitel, CG Goodyer, M Trifiro, and A LeBlanc. 2004. Estrogenand androgen protection of human neurons against intracellular Amyloid ß1-42 toxicitythrough heat shock protein 70. J Neurosci. 24:5315–5321.

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Environmental Physiology of Livestock (Collier/Environmental Physiology of Livestock) || Regulation of Acclimation to Environmental Stress