Increased heterozygosity for MHC class II lineages in newborn males

Genes and Immunity

Volumn 3, Issue 5, 2002, Pages 263-269

  Dorak, M T ^a,c   Lawson, T ^a   Machulla, H K G ^b   Mills, K I ^a   Burnett, A K ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b MARTIN LUTHER UNIVERSITÄT HALLE WITTENBERG   (Germany)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Gender effect; HLA DRB lineages; Homozygosity; MHC; Prenatal selection

Indexed keywords

DNA; HLA ANTIGEN; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; HLA DRB3; HLA DRB4; HLA DRB5; HLA-DRB1 ANTIGEN; HLA-DRB3; HLA-DRB4; HLA-DRB5;

ANTIGEN SPECIFICITY; ARTICLE; CORRELATION ANALYSIS; DEER; DELIVERY; DNA SEQUENCE; FEMALE; FERTILIZATION; FUNGAL GENETICS; GAMETE; GENE LOCUS; GENETIC CODE; GENETIC COMPATIBILITY; GENETIC SELECTION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HETEROZYGOSITY; HUMAN; HYPOTHESIS; INVERTEBRATE; MACACA; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOUSE; NEWBORN; NONHUMAN; PHYLOGENY; PLANT GENETICS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGENY; RAT; REPRODUCTIVE SUCCESS; SELECTIVE ABORTION; SEX DIFFERENCE; SEX RATIO; ALLELE; ANIMAL; COMPARATIVE STUDY; GENE; GENE FREQUENCY; GENETICS; HETEROZYGOTE; HISTOCOMPATIBILITY TEST; SEXUAL DEVELOPMENT;

ANIMALIA; CERVIDAE; FUNGI; INVERTEBRATA; MACACA; VERTEBRATA;

ALLELES; ANIMALS; FEMALE; GENE FREQUENCY; GENES, MHC CLASS II; GENOTYPE; HAPLOTYPES; HETEROZYGOTE; HISTOCOMPATIBILITY TESTING; HLA-DR ANTIGENS; HUMANS; INFANT, NEWBORN; MALE; POLYMERASE CHAIN REACTION; SEX CHARACTERISTICS;

EID: 0036691785     PISSN: 14664879     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.gene.6363862     Document Type: Article

References (75)

1. Marshall DL, Folsom MW. Mate choice in plants: an anatomical to population perspective. Annu Rev Ecol Syst 1991; 22: 37-63.
2. Kao TH, McCubbin AG. How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc Natl Acad Sci USA 1996; 93: 12059-12065.
3. Willson MF. Sexual selection in plants and animals. Trends Ecol Evol 1990; 5: 210-214.
4. Kronstad JW, Staben C. Mating type in filamentous fungi. Annu Rev Genet 1997; 31: 245-276.
5. Grosberg RK. The evolution of allorecognition specificity in clonal invertebrates. Q Rev Biol 1988; 63: 377-412.
6. Burnet FM. "Self-recognition" in colonial marine forms and flowering plants in relation to the evolution of immunity. Nature 1971; 232: 230-235.
7. Jones JS, Partridge L. Tissue rejection: the price for sexual acceptance. Nature 1983; 304: 484-485.
8. Alberts SC, Ober C. Genetic variability of the MHC: a review of non-pathogen-mediated selective mechanisms. Yearbook Phys Anthropol 1993; 36: 71-89.
9. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK. The nature of selection on the major histocompatibility complex. Crit Rev Immunol 1997; 17: 179-224.
10. Penn DJ, Ports WK. The evolution of mating preferences and major histocompatibility complex genes. Am Nat 1999; 153: 145-164.
11. Tregenza T, Wedell N. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 2000; 9: 1013-1027.
12. The MHC sequencing consortium. Complete sequence and gene map of a human major histocompatibility complex. Nature 1999; 401: 921-923.
13. Potts WK, Wakeland EK. Evolution of diversity at the major histocompatibility complex. Trends Ecol Evol 1990; 5: 181-187.
14. Little AM, Parham P. Polymorphism and evolution of HLA class I and II genes and molecules. Rev Immunogenet 1999; 1: 105-123.
15. Kasahara M, Klein D, Vincek V, Sarapata DE, Klein J. Comparative anatomy of the primate major histocompatibility complex DR subregion: evidence for combinations of DRB genes conserved across species. Genomics 1992; 14: 340-349.
16. Trowsdale J. "Both man & bird & beast": comparative organization of MHC genes. Immunogenetics 1995; 41: 1-17.
17. Andersson G, Andersson L, Larhammar D, Rask L, Sigurdardottir S. Simplifying genetic locus assignment of HLA-DRB genes. Immunol Today 1994; 15: 58-61.
18. Satta Y, Mayer WE, Klein J. HLA-DRB intron 1 sequences: implications for the evolution of HLA-DRB genes and haplotypes. Hum Immunol 1996; 51: 1-12.
19. Satta Y, O'Huigin C, Takahata N, Klein J. Intensity of natural selection at the major histocompatibility complex loci. Proc Natl Acad Sci USA 1994; 91: 7184-7188.
20. Black FL, Hedrick PW. Strong balancing selection at HLA loci: evidence from segregation in South Amerindian families. Proc Natl Acad Sci USA 1997; 94: 12452-12456.
21. Hedrick PW. Balancing selection and MHC. Genetica 1999; 104: 207-214.
22. Edwards SV, Hedrick PW. Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 1998; 13: 305-311.
23. Richman AD. Evolution of balanced genetic polymorphism. Mol Ecol 2000; 9: 1953-1963.
24. Thursz MR, Thomas HC, Greenwood BM, Hill AV. Heterozygote advantage for HLA class-II type in hepatitis B virus infection. Nat Genet 1997; 17: 11-12 (letter).
25. Carrington M, Nelson GW, Martin MP et al. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 1999; 283: 1748-1752.
26. Jeffery KJ, Siddiqui AA, Bunce M et al. The influence of HLA class I alleles and heterozygosity on the outcome of human T cell lymphotropic virus type I infection. J Immunol 2000; 165: 7278-7284.
27. Dorak MT, Lawson T, Machulla HKG, Darke C, Mills Kl, Burnett AK. Unravelling an HLA-DR association in childhood acute lymphoblastic leukemia. Blood 1999; 94: 694-700.
28. Dorak MT. A search for a leukaemia susceptibility gene in the HLA complex. PhD Dissertation. The University of Wales College of Medicine, UK, 2000.
29. Kaye SA, Robison LL, Smithson WA, Gunderson P, King FL, Neglia JP. Maternal reproductive history and birth characteristics in childhood acute lymphoblastic leukemia. Cancer 1991; 68: 1351-1355.
30. Yeazel MW, Buckley JD, Woods WG, Ruccione K, Robison LL. History of maternal fetal loss and increased risk of childhood acute leukemia at an early age. A report from the Childrens Cancer Group. Cancer 1995; 75: 1718-1727.
31. Klein J, Gutknecht J, Fischer N. The major histocompatibility complex and human evolution. Trends Genet 1990; 6: 7-11.
32. Ayala FJ, Escalante A, O'hUigin C, Klein J. Molecular genetics of speciation and human origins. Proc Natl Acad Sci USA 1994; 91: 6787-6794.
33. Zeh JA, Zeh DW. The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc Lond B Biol Sci 1997; 264: 69-75.
34. Jennions MD, Petrie M. Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 2000; 75: 21-64.
35. Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer SR, van den Bussche RA. Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus Virginianus): evidence for good-genes advertisement. Evolution 2001; 55: 616-625.
36. Wakeland EK, Boehme S, She JX et al. Ancestral polymorphisms of MHC class II genes: divergent allele advantage. Immunol Res 1990; 9: 115-122.
37. Flaherty L. Major histocompatibility complex polymorphism: a nonimmune theory for selection. Hum Immunol 1988; 21: 3-13.
38. Sette A, Sidney J. HLA supertypes and supermotifs: a functional perspective on HLA polymorphism. Curr Opin Immunol 1998; 10: 478-482.
39. Bell Jl, Denney Jr, D, Foster L, Belt T, Todd JA, McDevitt HO. Allelic variation in the DR subregion of the human major histocompatibility complex. Proc Natl Acad Sci USA 1987; 84: 6234-6238.
40. Gorski J, Rollini P, Mach B. Structural comparison of the genes of two HLA-DR supertypic groups: the loci encoding DRw52 and DRw53 are not truly allelic. Immunogenetics 1987; 25: 897-402.
41. Palm J. Association of maternal genotype and excess heterozygosity for Ag-B histocompatibility antigens among male rats. Transplant Proc 1969; 1: 82-84.
42. Palm J. Maternal-fetal interactions and histocompatibility antigen polymorphisms. Transplant Proc 1970; 2: 162-173.
43. Palm J. Maternal-fetal histoincompatibility in rats: an escape from adversity. Cancer Res 1974; 34: 2061-2065.
44. Hamilton MS, Hellstrom I. Selection for histoincompatible progeny in mice. Biol Reprod 1978; 19: 267-270.
45. Hull P. Maternal-foetal incompatibility associated with the H-3 locus in the mouse. Heredity 1969; 24: 203-209.
46. Bechtol KB. Lethality of heterozygotes between t-haplotype complementation groups of mouse: sex-related effect on lethality of t6/tw5 heterozygotes. Genet Res 1982; 39: 79-84.
47. King TR. Partial complementation by murine t haplotypes: deficit of males among t6/tw5 double heterozygotes and correlation with transmission-ratio distortion. Genet Res 1991; 57: 55-59.
48. Wedekind C, Chapuisat M, Macas E, Rulicke T. Non-random fertilization in mice correlates with the MHC and something else. Heredity 1996; 77: 400-409.
49. Crew FA. The sex ratio. Am Nat 1937; 71: 529-559.
50. McMillen MM. Differential mortality by sex in fetal and neonatal deaths. Science 1979; 204: 89-91.
51. Kellokumpu-Lehtinen P, Pelliniemi LJ. Sex ratio in human conceptuses. Obstet Gynecol 1984; 64: 220-222.
52. Byrne J, Warburton D. Male excess among anatomically normal fetuses in spontaneous abortions. Am J Med Genet 1987; 26: 605-611.
53. Roberts CJ, Lowe CR. Where have all the conceptions gone? Lancet 1975; 1: 498-499.
54. Drife JO. What proportion of pregnancies are spontaneously aborted? Br Med J 1983; 286: 294.
55. Diamond JM. Causes of death before birth. Nature 1987; 329: 487-488.
56. Kirby DR. The egg and immunology. Proc Roy Soc Med 1970; 63: 59-61.
57. Amos DB. HL-A, fertility and natural selection. Acta Endocrinol Suppl (Copenhagen) 1975; 194: 318-335.
58. Brown JL. Some paradoxical goals of cells and organisms: the role of the MHC. In: Pfaff DW (ed). Ethical Questions in Brain and Behavior: Problems and Opportunities, Springer-Verlag: New York, 1983, pp 111-124.
59. Mori T, Guo MW, Sato E, Baba T, Takasaki S, Mori E. Molecular and immunological approaches to mammalian fertilization. Am J Reprod Immunol 2000; 47: 139-158.
60. Grob B, Knapp LA, Martin RD, Anzenberger G. The major histocompatibility complex and mate choice: inbreeding avoidance and selection of good genes. Exp Clin Immunogenet 1998; 15: 119-129.
61. Landry C, Garant D, Duchesne P, Bernatchez L. The good genes as heterozygosity: MHC and mate choice in Atlantic salmon (Salmo salar). Proc R Soc Lond B Biol Sci 2001; 268: 1279-1285.
62. Wedekind C, Seebeck T, Bettens F, Paepke AJ. MHC-dependent mate preferences in humans. Proc R Soc Lond B Biol Sci 1995; 260: 245-249.
63. Ober C, Weitkamp LR, Cox N, Dytch H, Kostyu DD, Elias S. HLA and mate choice in humans. Am J Hum Genet 1997; 61: 497-504.
64. Hedrick PW, Black FL. HLA and mate selection: no evidence in South Amerindians. Am J Hum Genet 1997; 61: 505-511.
65. Michie D, Anderson NF. A strong selective effect associated with a histocompatibility gene in the rat. Ann New York Acad Sci 1966; 129: 88-93.
66. Brown JL. A theory of mate choice based on heterozygosity. Behav Ecol 1997; 8: 60-65.
67. Brown JL. The new heterozygosity theory of mate choice and the MHC. Genetica 1998; 104: 215-221.
68. Wedekind C, Furi S. Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc R Soc Lond B Biol Sci 1997; 264: 1471-1479.
69. von Schantz T, Wittzell H, Goransson G, Grahn M, Persson K. MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc R Soc Lond B Biol Sci 1996; 263: 265-271.
70. Sauermann U, Nurnberg P, Bercovitch FB et al. Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques. Hum Genet 2001; 108: 249-254.
71. Yuhki N, O'Brien SJ. DNA variation of the mammalian major histocompatibility complex reflects genomic diversity and population history. Proc Natl Acad Sci USA 1990; 87: 836-840.
72. Wright S. Variability Within and Among Natural Populations. University of Chicago Press: Chicago, 1978.
73. Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978; 89: 583-590.
74. Yeh FC, Yang, R-C, Boyle TBJ, Ye Z-H, Mao JX. POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada, 1997.
75. Daly LE, Bourke GJ. Interpretation and Uses of Medical Statistics. 5th edition. Blackwell Scientific Publications: Oxford, 2000.