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Marcus Palatnik Laboratorio de Pesquisa, Servico de Hemoterapia, Hospital Universitario, Universidade Federal do Rio De Janeiro, 3~ andar, Ave. Brg. Trompowski, s/n, 21941 Ilha do Governador, Rio de Janeiro, R j , Brazil Arthur W. Rowe The Laboratory of Cryobiology, The New York Blood Center, 310 East 67 Street, New York, NY 10021, U.S.A. Received 7 January 1983 and accepted 7 November 1983 Keywords: Duffy and Duffy-related antigens, primate serology, human antigens in apes and monkeys. Duffy and Duffy-related Human Antigens in Primates Duffy-related Fy3, Fy5, and Fs antigens on red cells of various species of primates were characterized and compared to the findings of others. While most species appear to be monomorphic for the Fy b and Fy3 antigens, Macaca mulatta, Macaca fascicularis, and Pan troglodytes are polymorphic for Fy b with the gene frequencies ranging for b~v b from 0'72 to 0.80 and fur Fy from 0"20 to 0"28. It may be postulated that Fy:3 and Fy(a-b-) could constitute the oldest phenotypes common to several species in primate evolution, while Fy5 and Fy ~ appear to be more recent antigens particular to the gorilla and human lineages respectively. 1. Introduction Numerous studies of antigens related to human blood groups in non-human primates have yielded significant information about their serological and genetic relationship. Studies of ABO blood groups in primates, particularly anthropoid apes, have helped to clarify the fundamental problem of the relationship of the H substance to the A and B group substance. According to Wiener, H is not a precursor of A and B as proposed by Watkins & Morgan (Race & Sanger, 1975) but the A-B genes act in parallel attaching appropriate determinant groups on the same macromolecule on the red cell surface (Socha & Moor-Jankowski, 1979). The Rh and MN locus in primates has been studied by Wiener's school in a comprehensive series of papers allowing for a rather complete evolutionary picture of this locus (see Moor-Jankowski & Wiener, 1968; Ruffi~ & Socha, 1980; Ruffi~ et al., 1982). The expression of human T-cell-like antigen determinants on anthropoid ape cells also constitutes evidence for a relatively recent common ancestor for chimpanzees, gorillas and man. Moreover, the high degree of conservation of T-cell subset antigen determinants suggests that these molecules may have been important in conferring a selective evolutionary advantage (Haynes et al., 1982). Interest in Duffy-related antigens on primate red cells has recently been revived because of observations that some Duffy phenotypes may be important in resistance to infection by Plasmodium vivax (Mason et al., 1977a; Miller et al., 1977). After studying a weak antibody (anti-Fs) found in the serum of a Brazilian Mulatto woman that reacted preferentially against Fy (a-b-) red cells (Palatnik et al., 1982), we have looked for the presence of the respective antigen along primate phylogeny. We report here studies on the Duffy-related antigens, Fy3 and Fy5, as well as Fs, of various species of primates and compare our findings with those in the literature about the Duffy system in primates, including man. Journal of Human Evolution (1984) /{3, 173-179 0047-2484/84/020173 + 07 $03.00/0 1984 Academic Press Inc. (London) Limited

Duffy and duffy-related human antigens in primates

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Marcus Palatnik Laboratorio de Pesquisa, Servico de Hemoterapia, Hospital Universitario, Universidade Federal do Rio De

Janeiro, 3 ~ andar, Ave. Brg. Trompowski, s/n, 21941 Ilha do Governador, Rio de Janeiro, R j , Brazil

Arthur W. Rowe

The Laboratory of Cryobiology, The New York Blood Center, 310 East 67 Street, New York, N Y 10021, U.S.A.

Received 7 January 1983 and accepted 7 November 1983

Keywords: Duffy and Duffy-related antigens, primate serology, human antigens in apes and monkeys.

Duffy and Duffy-related Human Antigens in Primates

Duffy-related Fy3, Fy5, and Fs antigens on red cells of various species of primates were characterized and compared to the findings of others. While most species appear to be monomorphic for the Fy b and Fy3 antigens, Macaca mulatta, Macaca fascicularis, and Pan troglodytes are polymorphic for Fy b with the gene frequencies ranging for b~v b from 0'72 to 0.80 and fur Fy from 0"20 to 0"28.

It may be postulated that Fy:3 and F y ( a - b - ) could constitute the oldest phenotypes common to several species in primate evolution, while Fy5 and Fy ~ appear to be more recent antigens particular to the gorilla and human lineages respectively.

1. Introduction

Numerous studies of antigens related to human blood groups in non-human primates have yielded significant information about their serological and genetic relationship. Studies of ABO blood groups in primates, particularly anthropoid apes, have helped to clarify the fundamental problem of the relationship of the H substance to the A and B group substance. According to Wiener, H is not a precursor of A and B as proposed by Watkins & Morgan (Race & Sanger, 1975) but the A-B genes act in parallel attaching appropriate determinant groups on the same macromolecule on the red cell surface (Socha & Moor-Jankowski, 1979).

The Rh and MN locus in primates has been studied by Wiener's school in a comprehensive series of papers allowing for a rather complete evolutionary picture of this locus (see Moor-Jankowski & Wiener, 1968; Ruffi~ & Socha, 1980; Ruffi~ et al., 1982).

The expression of human T-cell-like antigen determinants on anthropoid ape cells also constitutes evidence for a relatively recent common ancestor for chimpanzees, gorillas and man. Moreover, the high degree of conservation of T-cell subset antigen determinants suggests that these molecules may have been important in conferring a selective evolutionary advantage (Haynes et al., 1982).

Interest in Duffy-related antigens on primate red cells has recently been revived because of observations that some Duffy phenotypes may be important in resistance to infection by Plasmodium vivax (Mason et al., 1977a; Miller et al., 1977).

After studying a weak antibody (anti-Fs) found in the serum of a Brazilian Mulatto woman that reacted preferentially against Fy ( a - b - ) red cells (Palatnik et al., 1982), we have looked for the presence of the respective antigen along primate phylogeny.

We report here studies on the Duffy-related antigens, Fy3 and Fy5, as well as Fs, of various species of primates and compare our findings with those in the literature about the Duffy system in primates, including man.

Journal of Human Evolution (1984) /{3, 173-179

0047-2484/84/020173 + 07 $03.00/0 �9 1984 Academic Press Inc. (London) Limited

174 M. P A L A T N I K AND A. W . R O W E

2 . M a t e r i a l s and M e t h o d s

Red-cell samples, from various pr imate species were obtained from our collection at the New York Blood Center. All red cells studied had been previously frozen and s t o r e d a t - 1 9 6 ~ in liquid nitrogen (Rowe & Allen, 1965; Rowe et al., 1972). Using the ether technique (Rubin, 1963) as modified by Marsh (Miller, 1977), eluates were obtained from human red cells of appropr ia te Duffy blood groups, previously incubated with anti-Fy3, anti-Fy5, and anti-Fs sera.

The conventional nomenclature for the Duffy system was used: (a) For the genes, Fy ~, Fy b, Fy x, Fy 3, Fy 4, Fy 5, Fs; (b) For the antigens, Fy a, Fy b, Fy x, Fy3, Fy4, Fy5, Fs; (c) A positive phenotype is indicated by Fy (a+) , Fy (b+) , Fy:3, Fy:4, Fy:5, Fs (+) ; (d) A negative phenotype is indicated by F y ( a - ) , F y ( b - ) , F y : - 3 , F y : - 4 , F y : - 5 ,

Fs(-). All agglutination tests were done by the antiglobulin method (using commercial rabbit

polyspecific an t ihuman globulin serum), incubat ing equal volumes of eluate and red cell suspension for 1 h at 37 ~ Results of all tests were read and scored by macroscopic reading.

3. R e s u l t s

In order to compare the findings in non-human primates with those in man, human Duffy blood groups in Caucasoids and Negroids are presented in Table 1. Five Duffy phenotypes may be characterized in Caucasoids and Negroids by means o fan t i -Fy a and anti-Fy b sera (Table 1). Their frequencies vary in relation to race so that F y ( a - b - ) type is of a high incidence in Negroids and extremely rare in Causasoids; the FyxFy x genotype, which produces weak Fy b antigen, has not been reported in Negroes.

The Fy3 antigen is present in cells having either the Fy ~ or the Fy b antigens and lacking, therefore, in all the F y ( a - b - ) cells studied so far. The Fy4 antigen is present in all Negroid F y ( a - b - ) erythrocytes and in some Negroid F y ( a + b - ) and F y ( a - b + ) cells, but lacking in Negroid F y ( a + b + ) and in all Caucasoid red cells. The Fs antigen is also possibly related to the Duffy system because it is present in 80% of F y ( a - b - ) cells and in about 15% of the other phenotypes from both Caucasoid and Negroid cells. Fy5 parallels the reactions of Fy3 but has some impor tant differences because it is present in the extremely rare Caucasoid F y ( a - b - ) red cells while it is absent in all Negroid F y ( a - b - ) cells. The most important

Table 1 The Duffy and Duffy-related antigens in several human red cells

Duffyphenotype, Fy ~ Fy b Fy3 Fy4 Fy5 Fs Common Rh C. N. C. N. C. N. C. N. C. N. C. N.

Fy(a+b-) + + - - + + - + + + + o r - + o r - Fy(a-b+) - - + + + + - + + + + o r - + o r - Fy(a+b+) + + + + + + - - + + + o r - + o r - Fy(a-b-) . . . . . . unk. + + - + most + FyxFy x - weak weak unk. weak +

C. = Caucasoid; N. = Negroid. + = presence; - = absence. unk. = unknown.

PRIMATE DUFFY BLOOD G R o u P s 175

characteristic of Fy5 is that it is absent when Duffy (Fy a and Fy b) or Rh antigens are also absent.

Duffy and Duffy-related antigens were ~/isO found on red cells of various primate species and thes'e observations are presented in Table 2 which is based on our own findings about the, Fy3, Fy5 and Fs anfigerrs, as well as those of others about Fy a, Fy b and Fy3 antigens.

The Fy3 anttgen is found in most of the primate species including prosimians while the Fy5 appear~just in the gorilla as a "new" evolutionary character. The Fy a antigen cannot be detected in the primates studied so far, man being the only exception. Some rhesus monk~eys have the Fs antigen and some others do not. The same situation~holds for the gorillas, therefore, Fy3 seems to be the most ancient while Fy5, Fy a and Fs appear to be the most i~ecent of the Duffy-related mutations in the evolution of primates.

The serological relationship among Fy% Fy b afltigens and Fy3 seen in human beings (Tabl e 1) cloes not hold in prosimians and New World monkeys since several species with F y ( a - b - ) cells proved to be Fy:3. The first examples o f F y ( a - b + ) Fy:3 and F y ( a - b - ) F y : - 3 cells in primates were observed in chimpanzees.

Red ceil samples from nonprimates, prosimians and New World monkeys appear to be F y ( a ~ b - ) . In the Old World monkeys, however, some animals, e.g. the patas, guenon, stump-tailed and pig-tailed monkeys are F y ( a - b + ) while others, e.g. the cynomolgus and rhesus show two phenotypes, F y ( a - b + ) and F y ( a - b - ) , the former being in higher proportion. Most of the Great Apes are F y ( a - b + ) with the exceptionofone chimpanzee which was found to be F y ( a - b - ) (Table 2).

Pan troglodytes, Macaca fascicularis and Macaca mulatta are within the same range of variation for the gene frequencies, f y b from 0"72 to 0"80 and Fy from 0-20 to 0'28 (Table 3).

4. Discussion

Blood grouping reagentS of human origin cannot be used for tests on red cells of apes and monkeys without previous elimination of hetero-agglutinins directed against red cells of most simian species. This can be achieved by various methods and among others, for example, by first sensitizing human red cells with the human sera and then recovering the specific antibodies by elution as has been done by us. The antibodies eluted in this way are free ofhetero-agglutinins and could be used as specific reagents for testing ape and monkey red cells (Moor-Jankowski & Wiener, 1969; Marsh, 1975).

Fy3, Fy, Fy• Fy b There is no instance of primate Fy(h+) cells giving an F y : - 3 reaction; and this supports the hypothesis that Fy3 is a precursor of the Duffy antigens, as has been suggested by Albrey et al. (1971). However, the phenotype F y ( a - b - ) Fy:3 of the red cells of douroucoli and rhesus monkeys may result either from the lack of expression of the f y b gene in these taxa or these two antigens expressing themselves an erratic distribution similar to those of heterophile antigens which cut across the taxonomic lines as described for instance by Wiener et al. (1965) for the I and i antigens. Obviously, the absence of a factor in such a small sample of animals should have a different weight than its presence. Moreover, Stong & Stone (1980) consider that i f F y ( a - b - ) phenotype exists in rhesus monkeys, it must be relatively rare and thus it seems likely that the Fy b determinant is detectable with most but not all anti-Fy b sera.

Some prosimians (bush baby and slow loris) and chimpanzees appear to be F y ( a - b - )

1 7 6

T a b l e 2

M. P A L A T N I K A N D A. W . R O W E

D u f f y a n d D u f f y - r e l a t e d a n t i g e n s i n v a r i o u s s p e c i e s o f p r i m a t e s

No, of C o m m o n n a m e Spec ies Fy a Fy b Fy3 Fy5 Fs a n i m a l s R e f e r e n c e *

Great Apes Gor i l l a Gorilla gorilla gorilla _ + w + 1 ( 1 )

Gorilla.gorilla beringei + + - 1 (6) . . . . . . + + + 1 (6)

C h i m p a n z e e Pan troglodytes - + + 11 (1) . . . . - - - 1 ( 1 )

. . . . - + 17 ( 2 )

. . . . - - 5 ( 6 )

G i b b o n Hylobates agilis + - 1 (6) . . . . - + l ( 2 )

Old World monkeys K r a , C y n o m o l g u s Macacafaseicularis - + 4 (2)

. . . . - + 3 5 ( 5 )

. . . . _ _ + w 3 ( 4 )

- + w + - - - 2 ( 1 ) , ( 6 )

R h e s u s Macaca mulatta _ - + w 4 (4) . . . . - + 3 3 ( 2 )

. . . . - + 4 0 ( 5 )

. . . . - - + 2 ( 1 )

. . . . + - - 2 ( 6 )

+ - + 1 ( 6 )

S t u m p - t a i l e d Macaca arctoides - + 11 (5) P ig - t a i l ed Macaca nemestrina - + 8 (5) B a b o o n Papio sp. + - 1 (6) Pa t a s Erythrocebuspatas - + 3 (2) G u e n o n Cercopithecus aethiops - + 3 (2)

New World monkeys Squ i r r e l C a p u c h i n Douroco l i

M a r m o s e t

Prosimians B u s h b a b y

S low loris

C o m m o n t ree s h r e w

Non-primates H o r s e , sheep , etc. S h e e p

Saimiri sciureus - - 2 (2) Cebus apdla - - 8 (2) Aotus trivirgatus - - 4 (2)

. . . . _ - + w 3 ( 4 )

_ + w S o m e (3)

Saguinis sp. - - + 2 ( 1 ) Saguinisgeoffroyi - - 1 (2) Saguinis mystax - - 4 (2)

Galago crassicaudatus - - - 1 (1) . . . . - - 3 ( 2 )

Nyctieebus coucang . . . . . 2 (1), (6) . . . . - - 1 ( 2 )

Tupaia glis _ - + w - 1 ( 1 ), (6)

Tupaiasp. _ - + w - 1 (1), (6)

1 2 ( 2 )

I ( 6 )

w = w e a k . * (1) M a r s h (1975); (2) M a s o n et al. (1977a) ; (3) M a s o n et al. (19771)); (4) T i p p e t t & G a v i n (1979); (5) S t o n g & S tone (1980); (6) P r e s e n t p a p e r . W h e n r e f e r ences (1), (6) a re i n d i c a t e d , s a m p l e s f r o m the s a m e a n i m a l s w e r e s t u d i e d for Fy% Fy b a n d Fy3 a n t i g e n s (1) a n d for Fy3, Fy5 a n d Fs a n t i g e n s (6).

P R I M A T E D U F F Y B L O O D G R O U P S 177

F y : - 3 similar to the human phenotype. Thus, these cells are similar to negroid cells of the Fy Fy genotype.

Some weak reactivity in tests with eluates and absorption-elution methods is described for Fy b in the gorilla and cynomolgus (Marsh, 1975) and for Fy3 in the tree shrew (Marsh 1975) and in rhesus, kra and douroucoli by absorption methods (Tippett & Gavin, 1979). Similarity of the weak Fy b to the human Fy x reactions is reflected not only by the serological score of agglutination but also in the capacity of monkey cells for absorbing and releasing the anti-Fy b antibody. I t could be, therefore, that the Fy x may be reflecting the presence of a regulator gene which suppresses the expression of Fy b and Fy s structural genes (Buchanan et al., 1976). In view of the fact, however, that only single representative species were tested in which weak or doubtful reactions were obtained that could not be checked on larger animals, the question of the presence o f F y • in primate animals remains open.

F•5 The Fy5 antigen was detected on red cells of two highland gorillas but was absent in all five chimpanzees and in the seven New World and Old World monkeys and prosimians.

Fy5 is detected on gorilla but not on chimpanzee cells although both species have the homologues of human Rho and hr ' factors. This may suggest a different pathway for the Fy5 synthesis in non-hominid primates than in man. On the other hand, cells from New and Old World monkeys, including rhesus, do not react with any human Rh-Hr antisera (Moor-Janowski & Wiener, 1968). This could explain negative reaction for the Fy5 antigen if one postulates that in these taxa Fy5 is produced by the same pathway as was described for humans by Colledge et al. (1973), i.e. by interaction of the Duffy and Rh genes. However, the absence of simultaneous and parallel testing with the entire set of Duffy reagents on the one hand and the very small number of representatives of some species on the other hand make the theoretical discussion concerning the evolutionary pathways of the Duffy system highly speculative.

Our results herein described and data from the literature for the Duffy antigens suggest, as has been postulated by Ruffi4 (1973) for the ABO blood groups, that the serological phenotype in primates do not follow the zoological classification; on the contrary, they seem to be at random.

As no studies were yet made on the inheritance of the Duffy factors and the genetics of some human factors such as Fy3, Fy5, and Fs, remains to be established, we cannot

Table 3 Approximate gene frequencies of Duffy antigens in primates

Number of Phenotypes Gene frequencies Species animals Fy(a-b+) Fy(a-b-) Fy Fy b

Pan troglodytes 29 28 1 0'20 0.80 Macacafascicularis 42 39 3 0"26 0.74 Macaca mulatta 79 73 6 0'28 0'72

Gene frequencies were estimated by solving the quadratic equation:

FY b = -2Fy+ V'(2/a~v) 2 + 4Fy(a-b+) ;/~v = V'Fy(a-b-"i, 2

where Fy(a-b+) and Fy(a-b-) are phenotype frequencies (Race & Sanger, 1975). Fy a = 0"00 in the three species and F y b -{- Fy = 1.

178 M. PALATNIK AND A. W. ROWE

apply rigorously for the Dully system the concept of"pal~o-sequences"--(a fraction of a blood group system common to several species in a phylogenetic tree) and "n~o- sfiquences"--(fractions particular to each line) as defined by Ruffi~ (1976) and expanded by Ruffi~ and Socha (1980) for other blood group systems studied in large numbers of animals in which the genetics of the serological characters appear to be firmly established. In any case, it may be postulated that Fy:3 and F y ( a - b - ) could constitute the oldest phenotypes common to several species in primate evolution while Fy5 and Fy a appear to be antigens particular to the gorilla and man lines respectively.

Allowing for the small number of animals studied, most of the species appear to be monomorphic of the Fy b or the Fy3 antigens, although three species, rhesus, crab-eating macaque, and chimpanzee, appear to be polymorphic for Fy b.

The antiquity or persistence of some blood group factors in primate phylogeny supports Ohno's concept (Ohno, 1975) that the original linkage groups of a common ancestor might have been conserved to a surprising degree; and therefore, man might owe his success in part to a relatively rigid conservation of an original linkage group.

Partial financial aid for this work was received from the Conselho Nacional de Desenvolvimento Cientffico e Tecnoldgico (CNPq), Programa Integrado de Gen~tica and Conselho de Ensino para Graduados (CEPG), Universidade Federal do Rio de Janeiro, Brazil.

A Travel Grant from CNPq and financial aid from Centro de Hematologia Santa Catarina, Rio deJaneiro, were received by one of us (M. P.). We are grateful to the staffof the Immunohematology Laboratory and to Purita Tarusan and Annamarie Khan of the Cryobiology Laboratory of the New York Blood Center for their expertise and generous help. Dr Wladyslaw W. Socha (LEMSIP, NYU School of Medicine) has critically revised the manuscript and through a stimulating discussion kindly helped to improve upon the last version of this paper. We gratefully acknowledge the critical comments and suggestions of Mr W. Laurence Marsh (Immunohematology Laboratory, NYBC).

R e f e r e n c e s

Albrey, J. A., Vincent, E. E. R., Hutchinson, J., Marsh, W. L., Allen, F. H., Gavin,J. & Sanger, R. (1971). A new antibody, anti-Fy3 in the Duffy blood group system. Vox Sanguinis 20, 29-35.

Buchanan, D. I., Sinclair, M., Sanger, R., Gavin, J. & Teesdale, P. (1976). An Alberta Cree Indian with a rare Duffy antibody, anti-Fy3. Vox Sanguinis 30, 114-121.

Colledge, K. I., Pezzulich, M. & Marsh, W. L. (1973). Anti-Fy5, an antibody disclosing a probable association between the Rhesus and Duffy blood group genes. Vox Sanguinis 24, 193-199.

Haynes, B. F., Dowell, B. L., Hensley, L. L., Gore, I. & Metzgar, R. S. (1982). Human T cell antigen expression by primate T cell. Science 215, 298-300.

Marsh, W. L. (1975). Present status of the Duffy blood group system. Critical Reviews in Clinical Laboratory Sciences March, 387-412.

Mason, S. J., Miller, L. H., Shiroishi, T., Dvorak, J. A. & McGinnis, M. H. (1977a). The Duffy blood group determinants: Their role in the susceptibility of human and animal erythrocytes to Plasmodium knowlesi malaria. British Medical Journal 36, 327-335.

Mason, S. J., Miller, L. H., Shiroishi, T., McGinnis, M. H., Dvorak, J. A. & Whitehouse, W. C. (1977b). Unpublished data cited in Miller et al. (1977).

Miller, L. H., Mason, S. J., Dvorak, J. A., Shiroishi, T. & McGinnis, M. H. (1977). Erythrocyte receptors for malarial merozoites and the Duffy blood group system. In Human Blood Groups, 5th International Convocation on Immunology, Buffalo, NY 1976. Basel: Karger, pp. 394-400.

PRIMATE DUFFY BLOOD GROUPS 179

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