Comprehensive characterization of MHC class II haplotypes in Mauritian cynomolgus macaques

Immunogenetics

Volumn 59, Issue 6, 2007, Pages 449-462

  O'Connor, Shelby L ^a   Blasky, Alex J ^b   Pendley, Chad J ^b   Becker, Ericka A ^b   Wiseman, Roger W ^b   Karl, Julie A ^a   Hughes, Austin L ^c   O'Connor, David H ^a,b,d  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d NONE   (United States)

Author keywords

Immunogenetics; Macaca fascicularis; MHC

Indexed keywords

COMPLEMENTARY DNA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TETRAMER;

ALLELE; ARTICLE; CD4+ T LYMPHOCYTE; CELL LINE; DNA SEQUENCE; GENE EXPRESSION; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC TRAIT; GENETIC VARIABILITY; HAPLOTYPE; MACACA; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMATE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; GENES, MHC CLASS II; HAPLOTYPES; HUMANS; MACACA FASCICULARIS; MOLECULAR SEQUENCE DATA; PHYLOGENY; VARIATION (GENETICS);

CERCOPITHECIDAE; MACACA; MACACA FASCICULARIS; MACACA MULATTA; PRIMATES;

EID: 34247575203     PISSN: 00937711     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00251-007-0209-7     Document Type: Article

References (93)

1. Allen TM, Mothe BR, Sidney J, Jing P, Dzuris JL, Liebl ME, Vogel TU, O'Connor DH, Wang X, Wussow MC, Thomson JA, Altman JD, Watkins DI, Sette A (2001) CD8(+) lymphocytes from simian immunodeficiency virus-infected rhesus macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule mamu-A*01: implications for vaccine design and testing. J Virol 75:738-749
2. Allen TM, Sidney J, del Guercio MF, Glickman RL, Lensmeyer GL, Wiebe DA, DeMars R, Pauza CD, Johnson RP, Sette A, Watkins DI (1998) Characterization of the peptide binding motif of a rhesus MHC class I molecule (Mamu-A*01) that binds an immunodominant CTL epitope from simian immunodeficiency virus. J Immunol 160:6062-6071
3. Allen TM, Vogel TU, Fuller DH, Mothe BR, Steffen S, Boyson JE, Shipley T, Fuller J, Hanke T, Sette A, Altman JD, Moss B, McMichael AJ, Watkins DI (2000) Induction of AIDS virusspecific CTL activity in fresh, unstimulated peripheral blood lymphocytes from rhesus macaques vaccinated with a DNA prime/modified vaccinia virus Ankara boost regimen. J Immunol 164:4968-4978
4. Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, Bell JI, McMichael AJ, Davis MM (1996) Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94-96
5. Auffray C, Lillie JW, Arnot D, Grossberger D, Kappes D, Strominger JL (1984) Isotypic and allotypic variation of human class II histocompatibility antigen alpha-chain genes. Nature 308:327-333
6. Bakker NP, van Erck MG, Otting N, Lardy NM, Noort RC, 't Hart BA, Jonker M, Bontrop RE (1992) Resistance to collageninduced arthritis in a nonhuman primate species maps to the major histocompatibility complex class I region. J Exp Med 175:933-937
7. Blancher A, Tisseyre P, Dutaur M, Apoil PA, Maurer C, Quesniaux V, Raulf F, Bigaud M, Abbal M (2006) Study of cynomolgus monkey (Macaca fascicularis) MhcDRB (Mafa-DRB) polymorphism in two populations. Immunogenetics 58:269-282
8. Bontrop RE (2001) Non-human primates: essential partners in biomedical research. Immunol Rev 183:5-9
9. Bontrop RE (2006) Comparative genetics of MHC polymorphisms in different primate species: duplications and deletions. Hum Immunol 67:388-397
10. Bontrop RE, Watkins DI (2005) MHC polymorphism: AIDS susceptibility in non-human primates. Trends Immunol 26:227-233
11. Bontrop RE, Otting N, de Groot NG, Doxiadis GG (1999) Major histocompatibility complex class II polymorphisms in primates. Immunol Rev 167:339-350
12. Bosinger SE, Hosiawa KA, Cameron MJ, Persad D, Ran L, Xu L, Boulassel MR, Parenteau M, Fournier J, Rud EW, Kelvin DJ (2004) Gene expression profiling of host response in models of acute HIV infection. J Immunol 173:6858-6863
13. Carrington M, Bontrop RE (2002) Effects of MHC class I on HIV/SIV disease in primates. Aids 16(Suppl 4):S105-S114
14. Christ R, Hunsmann G, Sauermann U (1994) PCR-RFLP-based DQA1 typing of rhesus monkeys: sequence analysis of a new allele. Tissue Antigens 44:241-247
15. Das HK, Lawrance SK, Weissman SM (1983) Structure and nucleotide sequence of the heavy chain gene of HLA-DR. Proc Natl Acad Sci USA 80:3543-3547
16. Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE (2004) Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14:1501-1515
17. de Groot N, Doxiadis GG, De Groot NG, Otting N, Heijmans C, Rouweler AJ, Bontrop RE (2004) Genetic makeup of the DR region in rhesus macaques: gene content, transcripts, and pseudogenes. J Immunol 172:6152-6157
18. de Groot NG, Otting N, Doxiadis GG, Antunes SM, Bontrop RE (1998) Characterisation of four non-human primate Mhc-DQB1 alleles. Tissue Antigens 52:497-499
19. DeMars R, Chang CC, Shaw S, Reitnauer PJ, Sondel PM (1984) Homozygous deletions that simultaneously eliminate expressions of class I and class II antigens of EBV-transformed B-lymphoblastoid cells. I. Reduced proliferative responses of autologous and allogeneic T cells to mutant cells that have decreased expression of class II antigens. Hum Immunol 11:77-97
20. Dittmer U, Feldmann G, Sauermann U, Spirng M, Uberla K, Stahl-Hennig C, Hunsmann G (1998) Specificity of helper T-cells generated from macaques infected with attenuated simian immunodeficiency virus. J Gen Virol 79:1801-1807
21. Doxiadis GG, Otting N, de Groot NG, Bontrop RE (2001) Differential evolutionary MHC class II strategies in humans and rhesus macaques: relevance for biomedical studies. Immunol Rev 183:76-85
22. Doxiadis GG, Otting N, De Groot NG, De Groot N, Rouweler AJ, Noort R, Verschoor EJ, Bontjer I, Bontrop RE (2003) Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics 55:540-551
23. Doxiadis GG, Rouweler AJ, de Groot NG, Louwerse A, Otting N, Verschoor EJ, Bontrop RE (2006) Extensive sharing of MHC class II alleles between rhesus and cynomolgus macaques. Immunogenetics 58:259-268
24. Dzuris JL, Sidney J, Horton H, Correa R, Carter D, Chesnut RW, Watkins DI, Sette A (2001) Molecular determinants of peptide binding to two common rhesus macaque major histocompatibility complex class II molecules. J Virol 75:10958-10968
25. Erlich H, Lee JS, Petersen JW, Bugawan T, DeMars R (1986) Molecular analysis of HLA class I and class II antigen loss mutants reveals a homozygous deletion of the DR, DQ, and part of the DP region: implications for class II gene order. Hum Immunol 16:205-219
26. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791
27. Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, Stohr K, Osterhaus AD (2003) Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423:240
28. Gaur LK, Nepom GT (1996) Ancestral major histocompatibility complex DRB genes beget conserved patterns of localized polymorphisms. Proc Natl Acad Sci USA 93:5380-5383
29. Gyllensten U, Bergstrom T, Josefsson A, Sundvall M, Erlich HA (1996) Rapid allelic diversification and intensified selection at antigen recognition sites of the MHC class II DPB1 locus during hominoid evolution. Tissue Antigens 47:212-221
30. Hale DA, Dhanireddy K, Bruno D, Kirk AD (2005) Induction of transplantation tolerance in non-human primate preclinical models. Philos Trans R Soc Lond B Biol Sci 360:1723-1737
31. Hatta Y, Kanai T, Matsumoto Y, Kyuwa S, Hayasaka I, Yoshikawa Y (2002) Analysis of cDNA coding MHC class II beta chain of the chimpanzee (Pan troglodytes). Exp Anim 51:133-142
32. Haveman LM, Bierings M, Legger E, Klein MR, de Jager W, Otten HG, Albani S, Kuis W, Sette A, Prakken BJ (2006) Novel pan-DR-binding T cell epitopes of adenovirus induce pro-inflammatory cytokines and chemokines in healthy donors. Int Immunol 18:1521-1529
33. Hu SL (2005) Non-human primate models for AIDS vaccine research. Curr Drug Targets Infect Disord 5:193-201
34. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86:958-962
35. Jahrling PB, Hensley LE, Martinez MJ, Leduc JW, Rubins KH, Relman DA, Huggins JW (2004) Exploring the potential of variola virus infection of cynomolgus macaques as a model for human smallpox. Proc Natl Acad Sci USA 101:15196-15200
36. Jonker M, Ringers J, Kuhn EM, 't Hart B, Foulkes R (2004) Treatment with anti-MHC-class-II antibody postpones kidney allograft rejection in primates but increases the risk of CMV activation. Am J Transplant 4:1756-1761
37. Kaufmann DE, Bailey PM, Sidney J, Wagner B, Norris PJ, Johnston MN, Cosimi LA, Addo MM, Lichterfeld M, Altfeld M, Frahm N, Brander C, Sette A, Walker BD, Rosenberg ES (2004) Comprehensive analysis of human immunodeficiency virus type 1-specific CD4 responses reveals marked immunodominance of gag and nef and the presence of broadly recognized peptides. J Virol 78:4463-4477
38. Kenter M, Otting N, Anholts J, Leunissen J, Jonker M, Bontrop RE (1992) Evolutionary relationships among the primate Mhc-DQA1 and DQA2 alleles. Immunogenetics 36:71-78
39. Knapp LA, Lehmann E, Piekarczyk MS, Urvater JA, Watkins DI (1997) A high frequency of Mamu-A*01 in the rhesus macaque detected by polymerase chain reaction with sequence-specific primers and direct sequencing. Tissue Antigens 50:657-661
40. Krebs KC, Jin Z, Rudersdorf R, Hughes AL, O'Connor DH (2005) Unusually high frequency MHC class I alleles in Mauritian origin cynomolgus macaques. J Immunol 175:5230-5239
41. Kuiken T, Rimmelzwaan GF, Van Amerongen G, Osterhaus AD (2003) Pathology of human influenza A (H5N1) virus infection in cynomolgus macaques (Macaca fascicularis). Vet Pathol 40:304-310
42. Kuroda MJ, Schmitz JE, Lekutis C, Nickerson CE, Lifton MA, Franchini G, Harouse JM, Cheng-Mayer C, Letvin NL (2000) Human immunodeficiency virus type 1 envelope epitope-specific CD4(+) T lymphocytes in simian/human immunodeficiency virus-infected and vaccinated rhesus monkeys detected using a peptide-major histocompatibility complex class II tetramer. J Virol 74:8751-8756
43. Kuroda MJ, Schmitz JE, Barouch DH, Craiu A, Allen TM, Sette A, Watkins DI, Forman MA, Letvin NL (1998) Analysis of Gagspecific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J Exp Med 187:1373-1381
44. Kwok WW, Ptacek NA, Liu AW, Buckner JH (2002) Use of class II tetramers for identification of CD4+ T cells. J Immunol Methods 268:71-81
45. Lawler JV, Endy TP, Hensley LE, Garrison A, Fritz EA, Lesar M, Baric RS, Kulesh DA, Norwood DA, Wasieloski LP, Ulrich MP, Slezak TR, Vitalis E, Huggins JW, Jahrling PB, Paragas J (2006) Cynomolgus macaque as an animal model for severe acute respiratory syndrome. PLoS Med 3:677-686
46. Lawler SH, Sussman RW, Taylor LL (1995) Mitochondrial DNA of the Mauritian macaques (Macaca fascicularis): an example of the founder effect. Am J Phys Anthropol 96:133-141
47. Lekutis C, Letvin NL (1995) Biochemical and molecular characterization of rhesus monkey major histocompatibility complex class II DR. Hum Immunol 43:72-80
48. Lekutis C, Letvin NL (1997) HIV-1 envelope-specific CD4+ T helper cells from simian/human immunodeficiency virus-infected rhesus monkeys recognize epitopes restricted by MHC class II DRB1*0406 and DRB*W201 molecules. J Immunol 159:2049-2057
49. Leuchte N, Berry N, Kohler B, Almond N, LeGrand R, Thorstensson R, Titti F, Sauermann U (2004) MhcDRB-sequences from cynomolgus macaques (Macaca fascicularis) of different origin. Tissue Antigens 63:529-537
50. Loffredo JT, Rakasz EG, Giraldo JP, Spencer SP, Grafton KK, Martin SR, Napoe G, Yant LJ, Wilson NA, Watkins DI (2005) Tat(28-35)SL8-specific CD8+ T lymphocytes are more effective than Gag(181-189)CM9-specific CD8+ T lymphocytes at suppressing simian immunodeficiency virus replication in a functional in vitro assay. J Virol 79:14986-14991
51. Mills KH, Barnard AL, Williams M, Page M, Ling C, Stott EJ, Silvera P, Taffs F, Kingsman AS, Adams SE et al (1991) Vaccineinduced CD4+ T cells against the simian immunodeficiency virus gag protein. Epitope specificity and relevance to protective immunity. J Immunol 147:3560-3567
52. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418-426
53. Norris PJ, Moffett HF, Yang OO, Kaufmann DE, Clark MJ, Addo MM, Rosenberg ES (2004) Beyond help: direct effector functions of human immunodeficiency virus type 1-specific CD4(+) T cells. J Virol 78:8844-8851
54. O'Connor DH, Mothe BR, Weinfurter JT, Fuenger S, Rehrauer WM, Jing P, Rudersdorf RR, Liebl ME, Krebs K, Vasquez J, Dodds E, Loffredo J, Martin S, McDermott AB, Allen TM, Wang C, Doxiadis GG, Montefiori DC, Hughes A, Burton DR, Allison DB, Wolinsky SM, Bontrop R, Picker LJ, Watkins DI (2003) Major histocompatibility complex class I alleles associated with slow simian immunodeficiency virus disease progression bind epitopes recognized by dominant acute-phase cytotoxic-T-lymphocyte responses. J Virol 77:9029-9040
55. Ogg GS, McMichael AJ (1998) HLA-peptide tetrameric complexes. Curr Opin Immunol 10:393-396
56. Otting N, de Groot NG, Doxiadis GG, Bontrop RE (2002) Extensive Mhc-DQB variation in humans and non-human primate species. Immunogenetics 54:230-239
57. Otting N, de Groot NG, Noort MC, Doxiadis GG, Bontrop RE (2000) Allelic diversity of Mhc-DRB alleles in rhesus macaques. Tissue Antigens 56:58-68
58. Otting N, Doxiadis GG, Versluis L, de Groot NG, Anholts J, Verduin W, Rozemuller E, Claas F, Tilanus MG, Bontrop RE (1998) Characterization and distribution of Mhc-DPB1 alleles in chimpanzee and rhesus macaque populations. Hum Immunol 59:656-664
59. Otting N, Kenter M, van Weeren P, Jonker M, Bontrop RE (1992) Mhc-DQB repertoire variation in hominoid and Old World primate species. J Immunol 149:461-470
60. Patterson JL, Carrion RJ (2005) Demand for nonhuman primate resources in the age of biodefense. ILAR J 46:15-22
61. Penedo MC, Bontrop RE, Heijmans CM, Otting N, Noort R, Rouweler AJ, de Groot N, de Groot NG, Ward T, Doxiadis GG (2005) Microsatellite typing of the rhesus macaque MHC region. Immunogenetics 57:198-209
62. Pitcher CJ, Quittner C, Peterson DM, Connors M, Koup RA, Maino VC, Picker LJ (1999) HIV-1-specific CD4+ T cells are detectable in most individuals with active HIV-1 infection, but decline with prolonged viral suppression. Nat Med 5:518-525
63. Reimann KA, Parker RA, Seaman MS, Beaudry K, Beddall M, Peterson L, Williams KC, Veazey RS, Montefiori DC, Mascola JR, Nabel GJ, Letvin NL (2005) Pathogenicity of simian-human immunodeficiency virus SHIV-89.6P and SIVmac is attenuated in cynomolgus macaques and associated with early T-lymphocyte responses. J Virol 79:8878-8885
64. Rimmelzwaan GF, Kuiken T, van Amerongen G, Bestebroer TM, Fouchier RA, Osterhaus AD (2001) Pathogenesis of influenza A (H5N1) virus infection in a primate model. J Virol 75:6687-6691
65. Robinson J, Waller MJ, Parham P, de Groot N, Bontrop R, Kennedy LJ, Stoehr P, Marsh SG (2003) IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic Acids Res 31:311-314
66. Rosenberg ES, Billingsley JM, Caliendo AM, Boswell SL, Sax PE, Kalams SA, Walker BD (1997) Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278:1447-1450
67. Rowe T, Gao G, Hogan RJ, Crystal RG, Voss TG, Grant RL, Bell P, Kobinger GP, Wivel NA, Wilson JM (2004) Macaque model for severe acute respiratory syndrome. J Virol 78:11401-11404
68. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
69. Sano K, Shiina T, Kohara S, Yanagiya K, Hosomichi K, Shimizu S, Anzai T, Watanabe A, Ogasawara K, Torii R, Kulski JK, Inoko H (2006) Novel cynomolgus macaque MHC-DPB1 polymorphisms in three South-East Asian populations. Tissue Antigens 67:2 97-306
70. Sarkar S, Kalia V, Murphey-Corb M, Montelaro RC (2002) Detailed analysis of CD4+ Th responses to envelope and Gag proteins of simian immunodeficiency virus reveals an exclusion of broadly reactive Th epitopes from the glycosylated regions of envelope. J Immunol 168:4001-4011
71. Satta Y, O'hUigin C, Takahata N, Klein J (1993) The synonymous substitution rate of the major histocompatibility complex loci in primates. Proc Natl Acad Sci USA 90:7480-7484
72. Shimizu Y, DeMars R (1989) Production of human cells expressing individual transferred HLA-A,-B,-C genes using an HLA-A,-B,-C null human cell line. J Immunol 142:3320-3328
73. Slierendregt BL, Hall M, 't Hart B, Otting N, Anholts J, Verduin W, Claas F, Jonker M, Lanchbury JS, Bontrop RE (1995a) Identification of an Mhc-DPB1 allele involved in susceptibility to experimental autoimmune encephalomyelitis in rhesus macaques. Int Immunol 7:1671-1679
74. Slierendregt BL, Otting N, Kenter M, Bontrop RE (1995b) Allelic diversity at the Mhc-DP locus in rhesus macaques (Macaca mulatta). Immunogenetics 41:29-37
75. Slierendregt BL, van Noort JT, Bakas RM, Otting N, Jonker M, Bontrop RE (1992) Evolutionary stability of transpecies major histocompatibility complex class II DRB lineages in humans and rhesus monkeys. Hum Immunol 35:29-39
76. Sullivan NJ, Geisbert TW, Geisbert JB, Xu L, Yang ZY, Roederer M, Koup RA, Jahrling PB, Nabel GJ (2003) Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. Nature 424:681-684
77. Sussman R, Tattersall I (1986) Distribution, abundance, and putative ecological strategy of Macaca fascicularis on the island of Mauritius, Southwestern Indian Ocean. Folia Primatol 46:28-43
78. Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967-978
79. Takezaki N, Rzhetsky A, Nei M (1995) Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol 12:823-833
80. Rhesus Macaque Genome Sequencing and Analysis Consortium (2007) The rhesus macaque genome sequence informs biomedical and evolutionary analyses. Science (in press)
81. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882
82. Todd JA, Bell JI, McDevitt HO (1987) HLA-DQ beta gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature 329:599-604
83. Tosi AJ, Coke CS (2007) Comparative phylogenetics offer new insights into the biogeographic history of Macaca fascicularis and the origin of the Mauritian macaques. Mol Phylogenet Evol 42(2):498-504
84. Tosi AJ, Morales JC, Melnick DJ (2002) Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra. Int J Primatol 23:161-178
85. Tosi AJ, Morales JC, Melnick DJ (2003) Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution Int J Org Evolution 57:1419-1435
86. Vigon N, Sauermann U (2002) Sequence-based typing techniques for rhesus macaque MhcMamu-DQB1 allow the identification of more than 35 alleles. Tissue Antigens 59:88-94
87. Wake CT (1986) Molecular biology of the HLA class I and class II genes. Mol Biol Med 3:1-11
88. Walsh GP, Tan EV, dela Cruz EC, Abalos RM, Villahermosa LG, Young LJ, Cellona RV, Nazareno JB, Horwitz MA (1996) The Philippine cynomolgus monkey (Macaca fasicularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med 2:430-436
89. Wiseman RW, Wojcechowskyj JA, Greene JM, Blasky AJ, Gopon T, Soma T, Friedrich TC, O'Connor SL, O'Connor DH (2007) Simian immunodeficiency virus SIVmac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius. J Virol 81:349-361
90. Yant LJ, Friedrich TC, Johnson RC, May GE, Maness NJ, Enz AM, Lifson JD, O'connor DH, Carrington M, Watkins DI (2006) The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 80:5074-5077
91. Yoo TJ, Kim SY, Stuart JM, Floyd RA, Olson GA, Cremer MA, Kang AH (1988) Induction of arthritis in monkeys by immunization with type II collagen. J Exp Med 168:777-782
92. Yoshioka T, Ageyama N, Shibata H, Yasu T, Misawa Y, Takeuchi K, Matsui K, Yamamoto K, Terao K, Shimada K, Ikeda U, Ozawa K, Hanazono Y (2005) Repair of infarcted myocardium mediated by transplanted bone marrow-derived CD34+ stem cells in a nonhuman primate model. Stem Cells 23:355-364
93. Zhu ZF, Vincek V, Figueroa F, Schonbach C, Klein J (1991) Mhc-DRB genes of the pigtail macaque (Macaca nemestrina): implications for the evolution of human DRB genes. Mol Biol Evol 8:563-578