Genetic variation in the odorant receptors family 13 and the mhc loci influence mate selection in a multiple sclerosis dataset

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Khankhanian, Pouya ^a   Gourraud, Pierre Antoine ^a   Caillier, Stacy J ^a   Santaniello, Adam ^a   Hauser, Stephen L ^a   Baranzini, Sergio E ^a   Oksenberg, Jorge R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA DQA1 ANTIGEN; HLA DQB1 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; HLA ANTIGEN;

ADULT; ARTICLE; CAUCASIAN; CHROMOSOME 6P; CHROMOSOME 9; CONTROLLED STUDY; FEMALE; GENE LOCUS; GENETIC VARIABILITY; HAPLOTYPE MAP; HEREDITY; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; MAJOR CLINICAL STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MATE CHOICE; MULTIPLE SCLEROSIS; OLFACTORY RECEPTOR; POPULATION GENETICS; SEQUENCE HOMOLOGY; AGED; ALLELE; BASE PAIRING; GENETIC DATABASE; GENETIC PREDISPOSITION; GENETIC RECOMBINATION; GENETICS; HETEROZYGOTE; HOMOZYGOTE; HUMAN GENOME; MARRIAGE; PARENT; PHYLOGENY; REPRODUCIBILITY; SINGLE NUCLEOTIDE POLYMORPHISM; SPOUSE;

VERTEBRATA;

AGED; ALLELES; BASE PAIRING; CHROMOSOMES, HUMAN, PAIR 9; DATABASES, GENETIC; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GENETICS, POPULATION; GENOME, HUMAN; HETEROZYGOTE; HLA ANTIGENS; HOMOZYGOTE; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MARRIAGE; MULTIPLE SCLEROSIS; PARENTS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, ODORANT; RECOMBINATION, GENETIC; REPRODUCIBILITY OF RESULTS; SPOUSES;

EID: 78149241644     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-626     Document Type: Article

References (70)

1. Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Sollecito SV. Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 2003, 12:3077-3083. 10.1046/j.1365-294X.2003.01968.x, 14629387.
2. Knapp LA, Robson J, Waterhouse JS. Olfactory signals and the MHC: a review and a case study in Lemur catta. Am J Primatol 2006, 68:568-584. 10.1002/ajp.20253, 16715507.
3. OlsEn KH, Grahn M, Lohm J, Langefors A. MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim Behav 1998, 56:319-327. 10.1006/anbe.1998.0837, 9787022.
4. Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H. Major histocompatibility complex and mate choice in sand lizards. Proc Biol Sci 2003, 270(Suppl 2):S254-256. 10.1098/rsbl.2003.0079, 1809963, 14667398.
5. Yamazaki K, Beauchamp GK, Kupniewski D, Bard J, Thomas L, Boyse EA. Familial imprinting determines H-2 selective mating preferences. Science 1988, 240:1331-1332. 10.1126/science.3375818, 3375818.
6. Yamazaki K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, Abbott J, Boyse J, Zayas ZA, Thomas L. Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 1976, 144:1324-1335. 10.1084/jem.144.5.1324, 2190468, 1032893.
7. Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, Goedert JJ, Kaslow R, Buchbinder S, Hoots K, O'Brien SJ. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 1999, 283:1748-1752. 10.1126/science.283.5408.1748, 10073943.
8. McMichael AJ, Phillips RE. Escape of human immunodeficiency virus from immune control. Annu Rev Immunol 1997, 15:271-296. 10.1146/annurev.immunol.15.1.271, 9143689.
9. Penn DJ, Damjanovich K, Potts WK. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci USA 2002, 99:11260-11264. 10.1073/pnas.162006499, 123244, 12177415.
10. Penn DJ, Potts WK. The Evolution of Mating Preferences and Major Histocompatibility Complex Genes. The American Naturalist, 1999 - UChicago Press 1999,
11. Havlicek J, Roberts SC. MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 2009, 34:497-512. 10.1016/j.psyneuen.2008.10.007, 19054623.
12. Beauchamp GK, Yamazaki K. HLA and mate selection in humans: commentary. Am J Hum Genet 1997, 61:494-496. 10.1086/515521, 1715952, 9326313.
13. Chaix R, Cao C, Donnelly P. Is mate choice in humans MHC-dependent?. PLoS Genet 2008, 4:e1000184. 10.1371/journal.pgen.1000184, 2519788, 18787687.
14. Derti A, Cenik C, Kraft P, Roth F. Absence of Evidence for MHC-Dependent Mate Selection within HapMap Populations. PLoS Genet 2010, 6. 10.1371/journal.pgen.1000925, 2861700, 20442868.
15. 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. 10.1159/000019063, 9813409.
16. Jordan WC, Bruford MW. New perspectives on mate choice and the MHC. Heredity 1998, 81(Pt 3):239-245. 10.1038/sj.hdy.6884280, 9800367.
17. Roberts SC, Little AC. Good genes, complementary genes and human mate preferences. Genetica 2008, 134:31-43. 10.1007/s10709-008-9254-x, 18327646.
18. Yamazaki K, Beauchamp GK. Genetic basis for MHC-dependent mate choice. Adv Genet 2007, 59:129-145. full_text, 17888797.
19. Ober C, Weitkamp LR, Cox N, Dytch H, Kostyu D, Elias S. HLA and mate choice in humans. Am J Hum Genet 1997, 61:497-504. 10.1086/515511, 1715964, 9326314.
20. Hedrick PW, Black FL. HLA and mate selection: no evidence in South Amerindians. Am J Hum Genet 1997, 61:505-511. 10.1086/515519, 1715963, 9326315.
21. Giphart MJ, D'Amaro J. HLA and reproduction?. J Immunogenet 1983, 10:25-29. 10.1111/j.1744-313X.1983.tb01013.x, 6841981.
22. Ihara Y, Aoki K, Tokunaga K, Takahashi K, Juji T. HLA and Human Mate Choice: Tests on Japanese Couples. Anthropological Science 2000, 108:199-214.
23. Nordlander C, Hammarstrom L, Lindblom B, Smith CI. No role of HLA in mate selection. Immunogenetics 1983, 18:429-431. 10.1007/BF00372474, 6579022.
24. Sans M, Alvarez I, Callegari-Jacques SM, Salzano FM. Genetic similarity and mate selection in Uruguay. J Biosoc Sci 1994, 26:285-289. 10.1017/S0021932000021374, 7929477.
25. Jin K, Speed TP, Thomson G. Tests of random mating for a highly polymorphic locus: application to HLA data. Biometrics 1995, 51:1064-1076. 10.2307/2533005, 7548691.
26. Rosenberg LT, Cooperman D, Payne R. HLA and mate selection. Immunogenetics 1983, 17:89-93. 10.1007/BF00364292, 6826211.
27. Coetzee V, Barrett L, Greeff JM, Henzi SP, Perrett DI, Wadee AA. Common HLA alleles associated with health, but not with facial attractiveness. PLoS One 2007, 2:e640. 10.1371/journal.pone.0000640, 1919430, 17653267.
28. Lie HC, Rhodes G, Simmons LW. Genetic diversity revealed in human faces. Evolution 2008, 62:2473-2486. 10.1111/j.1558-5646.2008.00478.x, 18691260.
29. Roberts SC, Little AC, Gosling LM, Jones BC, Perrett DI, Carter V, Petrie M. MHC-assortative facial preferences in humans. Biol Lett 2005, 1:400-403. 10.1098/rsbl.2005.0343, 1626373, 17148217.
30. Roberts SC, Little AC, Gosling LM, Perrett DI, Carter V, Jones BC, Penton-Voak IS, Petrie M. MHC-heterozygosity and human facial attractiveness. Evol Hum Behav 2005, 26:213-226.
31. Thornhill R, Gangestad S, Miller R, Scheyd G, McCollough J, Franklin M. Major histocompatibility complex genes, symmetry, and body scent attractiveness in men and women. Behav Ecol 2003, 14:668-678.
32. Jacob S, McClintock MK, Zelano B, Ober C. Paternally inherited HLA alleles are associated with women's choice of male odor. Nat Genet 2002, 30:175-179. 10.1038/ng830, 11799397.
33. Roberts SC, Gosling LM, Carter V, Petrie M. MHC-correlated odour preferences in humans and the use of oral contraceptives. Proc Biol Sci 2008, 275:2715-2722. 10.1098/rspb.2008.0825, 2605820, 18700206.
34. Santos PS, Schinemann JA, Gabardo J, Bicalho Mda G. New evidence that the MHC influences odor perception in humans: a study with 58 Southern Brazilian students. Horm Behav 2005, 47:384-388. 10.1016/j.yhbeh.2004.11.005, 15777804.
35. Wedekind C, Furi S. Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity?. Proc Biol Sci 1997, 264:1471-1479. 10.1098/rspb.1997.0204, 1688704, 9364787.
36. Wedekind C, Seebeck T, Bettens F, Paepke AJ. MHC-dependent mate preferences in humans. Proc Biol Sci 1995, 260:245-249. 10.1098/rspb.1995.0087, 7630893.
37. IMSGC IMSGC Risk alleles for multiple sclerosis identified by a genomewide study. N Engl J Med 2007, 357:851-862. 10.1056/NEJMoa073493, 17660530, IMSGC IMSGC.
38. Benjamini YHY. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 1995, 57:289-300.
39. Rioux JD, Goyette P, Vyse TJ, Hammarstrom L, Fernando MMA, Green T, De Jager PL, Foisy S, Wang J, de Bakker PIW, Leslie S, McVean G, Padyukov L, Alfredsson L, Annese V, Hafler DA, Pan-Hammarstrom Q, Pirskanen R, Sawcer SJ, Compston AD, Cree BAC, Mirel DB, Daly MJ, Behrens TW, Klareskog L, Gregersen PK, Oksenberg JR, Hauser SL. International MHC and Autoimmunity Genetics Network (IMAGEN) Mapping of Multiple Susceptibility Variants Within the MHC Region for Seven Immune-Mediated Diseases. Proc Natl Acad Sci USA 2009, International MHC and Autoimmunity Genetics Network (IMAGEN).
40. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007, 81:559-575. 10.1086/519795, 1950838, 17701901.
41. Potts WK, Wakeland EK. Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends Genet 1993, 9:408-412. 10.1016/0168-9525(93)90103-O, 8122307.
42. Potts WK. Wisdom through immunogenetics. Nat Genet 2002, 30:130-131. 10.1038/ng0202-130, 11818954.
43. Murphy MR, Schneider GE. Olfactory bulb removal eliminates mating behavior in the male golden hamster. Science 1970, 167:302-304. 10.1126/science.167.3916.302, 5409714.
44. Gosling LM, Roberts SC. Scent-Marking by Male Mammals: Cheat-Proof Signals to Competitors and Mates. Advances in the Study of Behavior 2001 - Academic Press Limited 2001,
45. Sherborne AL, Thom MD, Paterson S, Jury F, Ollier WE, Stockley P, Beynon RJ, Hurst JL. The genetic basis of inbreeding avoidance in house mice. Curr Biol 2007, 17:2061-2066. 10.1016/j.cub.2007.10.041, 2148465, 17997307.
46. Yamaguchi M, Yamazaki K, Beauchamp GK, Bard J, Thomas L, Boyse EA. Distinctive urinary odors governed by the major histocompatibility locus of the mouse. Proc Natl Acad Sci USA 1981, 78:5817-5820. 10.1073/pnas.78.9.5817, 348873, 6946517.
47. Yeo TW, De Jager PL, Gregory SG, Barcellos LF, Walton A, Goris A, Fenoglio C, Ban M, Taylor CJ, Goodman RS, Walsh E, Wolfish CS, Horton R, Traherne J, Beck S, Trowsdale J, Caillier SJ, Ivinson AJ, Green T, Pobywajlo S, Lander ES, Pericak-Vance MA, Haines JL, Daly MJ, Oksenberg JR, Hauser SL, Compston A, Hafler DA, Rioux JD, Sawcer S. A second major histocompatibility complex susceptibility locus for multiple sclerosis. Ann Neurol 2007, 61:228-236. 10.1002/ana.21063, 2737610, 17252545.
48. Bagert BA. Epstein-Barr virus in multiple sclerosis. Curr Neurol Neurosci Rep 2009, 9:405-410. 10.1007/s11910-009-0059-9, 19664371.
49. Cullen M, Perfetto SP, Klitz W, Nelson G, Carrington M. High-resolution patterns of meiotic recombination across the human major histocompatibility complex. Am J Hum Genet 2002, 71:759-776. 10.1086/342973, 378534, 12297984.
50. Gandelman R, Zarrow MX, Denenberg VH, Myers M. Olfactory bulb removal eliminates maternal behavior in the mouse. Science 1971, 171:210-211. 10.1126/science.171.3967.210, 5540330.
51. Rowe FA, Edwards DA. Olfactory bulb removal: influences on the mating behavior of male mice. Physiol Behav 1972, 8:37-41. 10.1016/0031-9384(72)90127-8, 4665330.
52. Herz RSEDC. Differential use of sensory information in sexual behavior as a function of gender. Hum Nat 1997, 8:275-289.
53. Wedekind C. The MHC and body odors: arbitrary effects caused by shifts of mean pleasantness. Nat Genet 2002, 31:237. author reply 237, 10.1038/ng0702-237a, 12089519.
54. Chen D, Haviland-Jones J. Rapid mood change and human odors. Physiol Behav 1999, 68:241-250. 10.1016/S0031-9384(99)00147-X, 10627087.
55. Havlicek J, Saxton TK, Roberts SC, Jozifkova E, Lhota S, Valentova J, Flegr J. He sees, she smells? Male and female reports of sensory reliance in mate choice and non-mate-choice contexts. Pers Individ Diff 2008, 45:565-570.
56. Jacob S, Kinnunen LH, Metz J, Cooper M, McClintock MK. Sustained human chemosignal unconsciously alters brain function. Neuroreport 2001, 12:2391-2394. 10.1097/00001756-200108080-00021, 11496116.
57. Saxton TK, Lyndon A, Little AC, Roberts SC. Evidence that androstadienone, a putative human chemosignal, modulates women's attributions of men's attractiveness. Horm Behav 2008, 54:597-601. 10.1016/j.yhbeh.2008.06.001, 18601928.
58. Malnic B, Godfrey PA, Buck LB. The human olfactory receptor gene family. Proc Natl Acad Sci USA 2004, 101:2584-2589. 10.1073/pnas.0307882100, 356993, 14983052.
59. Kleinjan DA, Lettice LA. Long-range gene control and genetic disease. Adv Genet 2008, 61:339-388. full_text, 18282513.
60. Kleinjan DA, van Heyningen V. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am J Hum Genet 2005, 76:8-32. 10.1086/426833, 1196435, 15549674.
61. Lettice LA, Horikoshi T, Heaney SJ, van Baren MJ, van der Linde HC, Breedveld GJ, Joosse M, Akarsu N, Oostra BA, Endo N, Shibata M, Suzuki M, Takahashi E, Shinka T, Nakahori Y, Ayusawa D, Nakabayashi K, Scherer SW, Heutink P, Hill RE, Noji S. Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Proc Natl Acad Sci USA 2002, 99:7548-7553. 10.1073/pnas.112212199, 124279, 12032320.
62. Nobrega MA, Ovcharenko I, Afzal V, Rubin EM. Scanning human gene deserts for long-range enhancers. Science 2003, 302:413. 10.1126/science.1088328, 14563999.
63. Pfeifer D, Kist R, Dewar K, Devon K, Lander ES, Birren B, Korniszewski L, Back E, Scherer G. Campomelic dysplasia translocation breakpoints are scattered over 1 Mb proximal to SOX9: evidence for an extended control region. Am J Hum Genet 1999, 65:111-124. 10.1086/302455, 1378081, 10364523.
64. Wunderle VM, Critcher R, Hastie N, Goodfellow PN, Schedl A. Deletion of long-range regulatory elements upstream of SOX9 causes campomelic dysplasia. Proc Natl Acad Sci USA 1998, 95:10649-10654. 10.1073/pnas.95.18.10649, 27949, 9724758.
65. Rousset F. Inbreeding and relatedness coefficients: what do they measure?. Heredity 2002, 88:371-380. 10.1038/sj.hdy.6800065, 11986874.
66. Fisher R. Combining independent tests of significance. American Statistician 1948, 2:30.
67. Sebro R, Hoffman TJ, Lange C, Rogus JJ, Risch NJ. Testing for non-random mating: evidence for ancestry-related assortative mating in the Framingham heart study. Genet Epidemiol 2010,
68. Murtagh F. Multidimensional Clustering Algorithms. COMPSTAT Lectures 4 Wuerzburg: Physica-Verlag 1985,
69. Leslie S, Donnelly P, McVean G. A statistical method for predicting classical HLA alleles from SNP data. Am J Hum Genet 2008, 82:48-56. 10.1016/j.ajhg.2007.09.001, 2253983, 18179884.
70. de Bakker PI, McVean G, Sabeti PC, Miretti MM, Green T, Marchini J, Ke X, Monsuur AJ, Whittaker P, Delgado M, Morrison J, Richardson A, Walsh EC, Gao X, Galver L, Hart J, Hafler DA, Pericak-Vance M, Todd JA, Daly MJ, Trowsdale J, Wijmenga C, Vyse TJ, Beck S, Murray SS, Carrington M, Gregory S, Deloukas P, Rioux JD. A high-resolution HLA and SNP haplotype map for disease association studies in the extended human MHC. Nat Genet 2006, 38:1166-1172. 10.1038/ng1885, 2670196, 16998491.