Chromosome Y genetic variants: Impact in animal models and on human disease

Physiological Genomics

Volumn 47, Issue 11, 2015, Pages 525-537

  Prokop, J W ^a   Deschepper, C F ^b  

^a HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

Chromosome Y; Consomic strains; Human disease; Mouse; Phenotypic traits; Rat; Sex differences

Indexed keywords

CARDIOVASCULAR DISEASE; CELL FUNCTION; CHROMOSOME SUBSTITUTION STRAIN; EXPERIMENTAL MODEL; GENE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; NEOPLASM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STABILITY; REVIEW; TESTIS; Y CHROMOSOME; Y CHROMOSOME GENE; ANIMAL; ANIMAL MODEL; CHROMATIN ASSEMBLY AND DISASSEMBLY; FEMALE; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETIC VARIATION; MALE; MOUSE; PHYSIOLOGY;

SEX HORMONE;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENETIC VARIATION; GONADAL STEROID HORMONES; HAPLOTYPES; HUMANS; MALE; MICE; MODELS, ANIMAL; PHENOTYPE; Y CHROMOSOME;

EID: 84946057375     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00074.2015     Document Type: Review

References (138)

1. Aitken RJ, Marshall Graves JA. The future of sex. Nature 415: 963, 2002.
2. Albers HE. Gonadal hormones organize and modulate the circadian system of the rat. Am J Physiol Regul Integr Comp Physiol 241: R62-R66, 1981.
3. Araujo FC, Milsted A, Watanabe IKM, Puerto HLD, Santos RAS, Lazar J, Reis FM, Prokop JW. Similarities and differences of X and Y chromosome homologous genes, SRY and SOX3, in regulating the renin-angiotensin system promoters. Physiol Genomics 47: 177-186, 2015.
4. Arnold AP. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav 55: 570-578, 2009.
5. Arnold AP. The end of gonad-centric sex determination in mammals. Trends Genet 28: 55-61, 2012.
6. Arnold AP, Chen X. What does the “four core genotypes” mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol 30: 1-9, 2009.
7. Ayyanathan K, Lechner MS, Bell P, Maul GG, Schultz DC, Yamada Y, Tanaka K, Torigoe K, Rauscher FJ. Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev 17: 1855-1869, 2003.
8. Bachtrog D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14: 113-124, 2013.
9. Beatty WW, Powley TL, Keesey RE. Effects of neonatal testosterone injection and hormone replacement in adulthood on body weight and body fat in female rats. Physiol Behav 5: 1093-1098, 1970.
10. Bellott DW, Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Cho TJ, Koutseva N, Zaghlul S, Graves T, Rock S, Kremitzki C, Fulton RS, Dugan S, Ding Y, Morton D, Khan Z, Lewis L, Buhay C, Wang Q, Watt J, Holder M, Lee S, Nazareth L, Rozen S, Muzny DM, Warren WC, Gibbs RA, Wilson RK, Page DC. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508: 494-499, 2014.
11. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci USA 107: 3394-3399, 2010.
12. Bishop CE, Boursot P, Baron B, Bonhomme F, Hatat D. Most classical Mus musculus domesticus laboratory mouse strains carry a Mus musculus musculus Y chromosome. Nature 315: 70-72, 1985.
13. Bloomer LDS, Nelson CP, Eales J, Denniff M, Christofidou P, Debiec R, Moore J, Cardiogenics Consortium, Zukowska-Szczechowska E, Goodall AH, Thompson J, Samani NJ, Charchar FJ, Tomaszewski M. Male-specific region of the Y chromosome and cardiovascular risk phylogenetic analysis and gene expression studies. Arterioscler Thromb Vasc Biol 33: 1722-1727, 2013.
14. Botbol M, Roubertoux PL, Carlier M, Trabado S, Brailly-Tabard S, Perez-Diaz F, Bonnot O, Bronsard G, Tordjman S. Modulation of brain β-endorphin concentration by the specific part of the Y chromosome in mice. PLoS One 6: e16704, 2011.
15. Bullejos M, Sánchez A, Burgos M, Jiménez R, Díaz De La Guardia R. Multiple mono- and polymorphic Y-linked copies of the SRY HMGbox in microtidae. Cytogenet Cell Genet 86: 46-50, 1999.
16. Burgoyne PS, Thornhill AR, Boudrean SK, Darling SM, Bishop CE, Evans EP, Capel B, Mittwoch U. The genetic basis of XX-XY differences present before gonadal sex differentiation in the mouse. Philos Trans R Soc Lond B Biol Sci 350: 253-261, 1995.
17. Case LK, Toussaint L, Moussawi M, Roberts B, Saligrama N, Brossay L, Huber SA, Teuscher C. Chromosome Y regulates survival following murine coxsackievirus b3 infection. G3 (Bethesda) 2: 115-121, 2012.
18. Case LK, Wall EH, Dragon JA, Saligrama N, Krementsov DN, Moussawi M, Zachary JF, Huber SA, Blankenhorn EP, Teuscher C. The Y chromosome as a regulatory element shaping immune cell transcriptomes and susceptibility to autoimmune disease. Genome Res 23: 1474-1485, 2013.
19. Case LK, Wall EH, Osmanski EE, Dragon JA, Saligrama N, Zachary JF, Lemos B, Blankenhorn EP, Teuscher C. Copy number variation in Y chromosome multicopy genes is linked to a paternal parent-of-origin effect on CNS autoimmune disease in female offspring. Genome Biol 16: 28, 2015.
20. Charchar FJ, Bloomer LDS, Barnes TA, Cowley MJ, Nelson CP, Wang Y, Denniff M, Debiec R, Christofidou P, Nankervis S, Dominiczak AF, Bani-Mustafa A, Balmforth AJ, Hall AS, Erdmann J, Cambien F, Deloukas P, Hengstenberg C, Packard C, Schunkert H, Ouwehand WH, Ford I, Goodall AH, Jobling MA, Samani NJ, Tomaszewski M. Inheritance of coronary artery disease in men: an analysis of the role of the Y chromosome. Lancet 379: 915-922, 2012.
21. Charchar FJ, Tomaszewski M, Lacka B, Zakrzewski J, Zukowska- Szczechowska E, Grzeszczak W, Dominiczak AF. Association of the human Y chromosome with cholesterol levels in the general population. Arterioscler Thromb Vasc Biol 24: 308-312, 2004.
22. Charchar FJ, Tomaszewski M, Padmanabhan S, Lacka B, Upton MN, Inglis GC, Anderson NH, McConnachie A, Zukowska-Szczechowska E, Grzeszczak W, Connell JMC, Watt GCM, Dominiczak AF. The Y chromosome effect on blood pressure in two European populations. Hypertension 39: 353-356, 2002.
23. Chen W, Yang CC, Tsai RY, Liao CY, Yen YT, Hung CL, Chen KF, Tsai SJ, Zouboulis CC. Expression of sex-determining genes in the scalp of men with androgenetic alopecia. Dermatology (Basel) 214: 199-204, 2007.
24. Christine Knickmeyer R, Baron-Cohen S. Fetal testosterone and sex differences. Early Hum Dev 82: 755-760, 2006.
25. Collignon J, Sockanathan S, Hacker A, Cohen-Tannoudji M, Norris D, Rastan S, Stevanovic M, Goodfellow PN, Lovell-Badge R. A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122: 509-520, 1996.
26. Corbier P, Edwards DA, Roffi J. The neonatal testosterone surge: a comparative study. Arch Int Physiol Biochim Biophys 100: 127-131, 1992.
27. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grützner F, Kaessmann H. Origins and functional evolution of Y chromosomes across mammals. Nature 508: 488-493, 2014.
28. Csernus V. Production of sexual steroids in rats during pre- and early postnatal life. Exp Clin Endocrinol 88: 1-5, 1986.
29. Dai Y, Ngo D, Jacob J, Forman LW, Faller DV. Prohibitin and the SWI/SNF ATPase subunit BRG1 are required for effective androgen antagonist-mediated transcriptional repression of androgen receptor-regulated genes. Carcinogenesis 29: 1725-1733, 2008.
30. Davidson AO, Schork N, Jaques BC, Kelman AW, Sutcliffe RG, Reid JL, Dominiczak AF. Blood pressure in genetically hypertensive rats. Influence of the Y chromosome. Hypertension 26: 452-459, 1995.
31. Demissie M, Lazic M, Foecking EM, Aird F, Dunaif A, Levine JE. Transient prenatal androgen exposure produces metabolic syndrome in adult female rats. Am J Physiol Endocrinol Metab 295: E262-E268, 2008.
32. Dewing P, Chiang CWK, Sinchak K, Sim H, Fernagut PO, Kelly S, Chesselet MF, Micevych PE, Albrecht KH, Harley VR, Vilain E. Direct regulation of adult brain function by the male-specific factor SRY. Curr Biol 16: 415-420, 2006.
33. Dewing P, Shi T, Horvath S, Vilain E. Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Mol Brain Res 118: 82-90, 2003.
34. Dumanski JP, Rasi C, Lönn M, Davies H, Ingelsson M, Giedraitis V, Lannfelt L, Magnusson PKE, Lindgren CM, Morris AP, Cesarini D, Johannesson M, Tiensuu Janson E, Lind L, Pedersen NL, Ingelsson E, Forsberg LA. Mutagenesis. Smoking is associated with mosaic loss of chromosome Y. Science 347: 81-83, 2015.
35. Ellis JA, Stebbing M, Harrap SB. Association of the human Y chromosome with high blood pressure in the general population. Hypertension 36: 731-733, 2000.
36. Ely D, Boehme S, Dunphy G, Hart M, Chiarappa F, Miller B, Martins AS, Turner M, Milsted A. The Sry3 Y chromosome locus elevates blood pressure and renin-angiotensin system indexes. Gend Med 8: 126-138, 2011.
37. Ely DL, Falvo J, Dunphy G, Caplea A, Salisbury R, Turner M. The spontaneously hypertensive rat Y chromosome produces an early testosterone rise in normotensive rats. J Hypertens 12: 769-774, 1994.
38. Ely DL, Salisbury R, Hadi D, Turner M, Johnson ML. Androgen receptor and the testes influence hypertension in a hybrid rat model. Hypertension 17: 1104-1110, 1991.
39. Ely DL, Turner ME. Hypertension in the spontaneously hypertensive rat is linked to the Y chromosome. Hypertension 16: 277-281, 1990.
40. Ely D, Milsted A, Dunphy G, Boehme S, Dunmire J, Hart M, Toot J, Martins A, Turner M. Delivery of sry1, but not sry2, to the kidney increases blood pressure and sns indices in normotensive wky rats. BMC Physiol 9: 10, 2009.
41. Ewis AA, Lee J, Naroda T, Sano T, Kagawa S, Iwamoto T, Shinka T, Shinohara Y, Ishikawa M, Baba Y, Nakahori Y. Prostate cancer incidence varies among males from different Y-chromosome lineages. Prostate Cancer Prostatic Dis 9: 303-309, 2006.
42. Ferguson-Smith MA, Bavington LD. Natural selection for genetic variants in sport: the role of Y chromosome genes in elite female athletes with 46,XY DSD. Sports Med 44: 1629-1634, 2014.
43. Flister MJ, Prokop JW, Lazar J, Shimoyama M, Dwinell M, Geurts A. 2015 guidelines for establishing genetically modified rat models for cardiovascular research. J Cardiovasc Transl Res 8: 269-277, 2015.
44. Forsberg LA, Rasi C, Malmqvist N, Davies H, Pasupulati S, Pakalapati G, Sandgren J, de Ståhl TD, Zaghlool A, Giedraitis V, Lannfelt L, Score J, Cross NCP, Absher D, Janson ET, Lindgren CM, Morris AP, Ingelsson E, Lind L, Dumanski JP. Mosaic loss of chromosome Y in peripheral blood is associated with shorter survival and higher risk of cancer. Nat Genet 46: 624-628, 2014.
45. Graves JAM. Sex chromosome specialization and degeneration in mammals. Cell 124: 901-914, 2006.
46. Hallast P, Batini C, Zadik D, Maisano Delser P, Wetton JH, Arroyo- Pardo E, Cavalleri GL, de Knijff P, Destro Bisol G, Dupuy BM, Eriksen HA, Jorde LB, King TE, Larmuseau MH, López de Munain A, López-Parra AM, Loutradis A, Milasin J, Novelletto A, Pamjav H, Sajantila A, Schempp W, Sears M, Tolun A, Tyler-Smith C, Van Geystelen A, Watkins S, Winney B, Jobling MA. The Y-chromosome tree bursts into leaf: 13,000 high-confidence SNPs covering the majority of known clades. Mol Biol Evol 32: 661-673, 2015.
47. Helgason A, Einarsson AW, Guðmundsdóttir VB, Sigurðsson Á, Gunnarsdóttir ED, Jagadeesan A, Ebenesersdóttir SS, Kong A, Stefánsson K. The Y-chromosome point mutation rate in humans. Nat Genet 47: 453-457, 2015.
48. Hensbroek RA, Sluyter F, Guillot PV, Van Oortmerssen GA, Crusio WE. Y chromosomal effects on hippocampal mossy fiber distributions in mice selected for aggression. Brain Res 682: 203-206, 1995.
49. Iyengar S, Farnham PJ. KAP1 protein: an enigmatic master regulator of the genome. J Biol Chem 286: 26267-26276, 2011.
50. Ji H, Zheng W, Wu X, Liu J, Ecelbarger CM, Watkins R, Arnold AP, Sandberg K. Sex chromosome effects unmasked in angiotensin II-induced. Hypertension 55: 1275-1282, 2010.
51. Jobling MA, Tyler-Smith C. The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet 4: 598-612, 2003.
52. Jutley JK, Stewart AD. Genetic analysis of the Y-chromosome of the mouse: evidence for two loci affecting androgen metabolism. Genet Res 47: 29-34, 1986.
53. Karmin M, Saag L, Vicente M, Wilson Sayres MA, Järve M, Talas UG, Rootsi S, Ilumäe AM, Mägi R, Mitt M, Pagani L, Puurand T, Faltyskova Z, Clemente F, Cardona A, Metspalu E, Sahakyan H, Yunusbayev B, Hudjashov G, DeGiorgio M, Loogväli EL, Eichstaedt C, Eelmets M, Chaubey G, Tambets K, Litvinov S, Mormina M, Xue Y, Ayub Q, Zoraqi G, Korneliussen TS, Akhatova F, Lachance J, Tishkoff S, Momynaliev K, Ricaut FX, Kusuma P, Razafindrazaka H, Pierron D, Cox MP, Sultana GNN, Willerslev R, Muller C, Westaway M, Lambert D, Skaro V, Kovacˇevic L, Turdikulova S, Dalimova D, Khusainova R, Trofimova N, Akhmetova V, Khidiyatova I, Lichman DV, Isakova J, Pocheshkhova E, Sabitov Z, Barashkov NA, Nymadawa P, Mihailov E, Seng JWT, Evseeva I, Migliano AB, Abdullah S, Andriadze G, Primorac D, Atramentova L, Utevska O, Yepiskoposyan L, Marjanovic D, Kushniarevich A, Behar DM, Gilissen C, Vissers L, Veltman JA, Balanovska E, Derenko M, Malyarchuk B, Metspalu A, Fedorova S, Eriksson A, Manica A, Mendez FL, Karafet TM, Veeramah KR, Bradman N, Hammer MF, Osipova LP, Balanovsky O, Khusnutdinova EK, Johnsen K, Remm M, Thomas MG, Tyler-Smith C, Underhill PA, Willerslev E, Nielsen R, Metspalu M, Villems R, Kivisild T. A recent bottleneck of Y chromosome diversity coincides with a global change in culture. Genome Res 25: 459-466, 2015.
54. Khosravi P, Gazestani VH, Asgari Y, Law B, Sadeghi M, Goliaei B. Network-based approach reveals Y chromosome influences prostate cancer susceptibility. Comput Biol Med 54: 24-31, 2014.
55. Kido T, Lau YFC. Roles of the Y chromosome genes in human cancers. Asian J Androl 17: 373-380. 2015.
56. Kostrzewa G, Broda G, Konarzewska M, Krajewki P, Płoski R. Genetic polymorphism of human Y chromosome and risk factors for cardiovascular diseases: a study in WOBASZ cohort. PLoS One 8: e68155, 2013.
57. Kren V, Qi N, Krenova D, Zidek V, Sladká M, Jáchymová M, Míková B, Horky K, Bonne A, Van Lith HA, Van Zutphen BF, Lau YF, Pravenec M, St Lezin E. Y-chromosome transfer induces changes in blood pressure and blood lipids in SHR. Hypertension 37: 1147-1152, 2001.
58. Lahn BT, Page DC. Functional coherence of the human Y chromosome. Science 278: 675-680, 1997.
59. Lahn BT, Page DC. Retroposition of autosomal mRNA yielded testisspecific gene family on human Y chromosome. Nat Genet 21: 429-433, 1999.
60. Lahn BT, Page DC. Four evolutionary strata on the human X chromosome. Science 286: 964-967, 1999.
61. Lee S, Lee JW, Lee SK. UTX, a histone H3-lysine 27 demethylase, acts as a critical switch to activate the cardiac developmental program. Dev Cell 22: 25-37, 2012.
62. Lemos B, Branco AT, Hartl DL. Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict. Proc Natl Acad Sci USA 107: 15826-15831, 2010.
63. Li J, Fu J, Toumazou C, Yoon HG, Wong J. A role of the aminoterminal (N) and carboxyl-terminal (C) interaction in binding of androgen receptor to chromatin. Mol Endocrinol 20: 776-785, 2006.
64. Li Y, Kido T, Garcia-Barcelo MM, Tam PKH, Tabatabai ZL, Lau YFC. SRY interference of normal regulation of the RET gene suggests a potential role of the Y-chromosome gene in sexual dimorphism in Hirschsprung disease. Hum Mol Genet 24: 685-697, 2015.
65. Link JC, Chen X, Arnold AP, Reue K. Metabolic impact of sex chromosomes. Adipocyte 2: 74-79, 2013.
66. Llamas B, Verdugo RA, Churchill GA, Deschepper CF. Chromosome Y variants from different inbred mouse strains are linked to differences in the morphologic and molecular responses of cardiac cells to postpubertal testosterone. BMC Genom 10: 150, 2009.
67. Luczak ED, Leinwand LA. Sex-based cardiac physiology. Annu Rev Physiol 71: 1-18, 2009.
68. Lundrigan BL, Tucker PK. Evidence for multiple functional copies of the male sex-determining locus, Sry, in African murine rodents. J Mol Evol 45: 60-65, 1997.
69. Maric C. Sex differences in cardiovascular disease and hypertension: involvement of the renin-angiotensin system. Hypertension 46: 475-476, 2005.
70. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA, Ko MSH, Niwa H. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 9: 625-635, 2007.
71. Mattson DL, Dwinell MR, Greene AS, Kwitek AE, Roman RJ, Cowley AW, Jacob HJ. Chromosomal mapping of the genetic basis of hypertension and renal disease in FHH rats. Am J Physiol Renal Physiol 293: F1905-F1914, 2007.
72. Mattson DL, Dwinell MR, Greene AS, Kwitek AE, Roman RJ, Jacob HJ, Cowley AW. Chromosome substitution reveals the genetic basis of Dahl salt-sensitive hypertension and renal disease. Am J Physiol Renal Physiol 295: F837-F842, 2008.
73. Milsted A, Underwood AC, Dunmire J, DelPuerto HL, Martins AS, Ely DL, Turner ME. Regulation of multiple renin-angiotensin system genes by Sry. J Hypertens 28: 59-64, 2010.
74. Monahan EJ, Maxson SC. Y chromosome, urinary chemosignals, and an agonistic behavior (offense) of mice. Physiol Behav 64: 123-132, 1998.
75. Mukherjee A, Dass G, Mohanarao GJ, Katneni VK, Banerjee D, Das TK, Gohain M, Chakrabarty AK, Datta TK, De S. Copy number differences of Y chromosomal genes between superior and inferior quality semen producing crossbred (Bos taurus × Bos indicus) bulls. Anim Biotechnol 26: 65-72, 2015.
76. Nada SE, Thompson RC, Padmanabhan V. Developmental programming: differential effects of prenatal testosterone excess on insulin target tissues. Endocrinology 151: 5165-5173, 2010.
77. Nadeau JH, Singer JB, Matin A, Lander ES. Analysing complex genetic traits with chromosome substitution strains. Nat Genet 24: 221-225, 2000.
78. Nagamine CM, Nishioka Y, Moriwaki K, Boursot P, Bonhomme F, Lau YF. The musculus-type Y chromosome of the laboratory mouse is of Asian origin. Mamm Genome 3: 84-91, 1992.
79. Nilsson C, Niklasson M, Eriksson E, Björntorp P, Holmäng A. Imprinting of female offspring with testosterone results in insulin resistance and changes in body fat distribution at adult age in rats. J Clin Invest 101: 74-78, 1998.
80. Ober C, Loisel DA, Gilad Y. Sex-specific genetic architecture of human disease. Nat Rev Genet 9: 911-922, 2008.
81. Oh HJ, Li Y, Lau YFC. Sry associates with the heterochromatin protein 1 complex by interacting with a KRAB domain protein. Biol Reprod 72: 407-415, 2005.
82. Ostrer H. Invited review: sex-based differences in gene expression. J Appl Physiol 91: 2384-2388, 2001.
83. Van Oven M, Van Geystelen A, Kayser M, Decorte R, Larmuseau MH. Seeing the wood for the trees: a minimal reference phylogeny for the human Y chromosome. Hum Mutat 35: 187-191, 2014.
84. Pearks Wilkerson AJ, Raudsepp T, Graves T, Albracht D, Warren W, Chowdhary BP, Skow LC, Murphy WJ. Gene discovery and comparative analysis of X-degenerate genes from the domestic cat Y chromosome. Genomics 92: 329-338, 2008.
85. Peng H, Begg GE, Schultz DC, Friedman JR, Jensen DE, Speicher DW, Rauscher FJ 3rd. Reconstitution of the KRAB-KAP-1 repressor complex: a model system for defining the molecular anatomy of RING-B box-coiled-coil domain-mediated protein-protein interactions. J Mol Biol 295: 1139-1162, 2000.
86. Peng H, Ivanov AV, Oh HJ, Lau YFC, Rauscher FJ. Epigenetic gene silencing by the sry protein is mediated by a KRAB-O protein that recruits the KAP1 co-repressor machinery. J Biol Chem 284: 35670-35680, 2009.
87. Polanco JC, Koopman P. Sry and the hesitant beginnings of male development. Dev Biol 302: 13-24, 2007.
88. Polanco JC, Wilhelm D, Mizusaki H, Jackson A, Browne C, Davidson T, Harley V, Sinclair A, Koopman P. Functional analysis of the SRY-KRAB interaction in mouse sex determination. Biol Cell 101: 55, 2009.
89. Praktiknjo SD, Llamas B, Scott-Boyer MP, Picard S, Robert F, Langlais D, Haibe-Kains B, Faubert D, Silversides DW, Deschepper CF. Novel effects of chromosome Y on cardiac regulation, chromatin remodeling, and neonatal programming in male mice. Endocrinology 154: 4746-4756, 2013.
90. Premi S, Srivastava J, Chandy SP, Ahmad J, Ali S. Tandem duplication and copy number polymorphism of the SRY gene in patients with sex chromosome anomalies and males exposed to natural background radiation. Mol Hum Reprod 12: 113-121, 2006.
91. Premi S, Srivastava J, Panneer G, Ali S. Startling mosaicism of the Y-chromosome and tandem duplication of the SRY and DAZ genes in patients with Turner syndrome. PLoS One 3: e3796-e3806, 2008.
92. Prokop JW, Leeper TC, Duan ZH, Milsted A. Amino acid function and docking site prediction through combining disease variants, structure alignments, sequence alignments, and molecular dynamics: a study of the HMG domain. BMC Bioinformat 13, Suppl 2: S3, 2012.
93. Prokop JW, Rauscher FJ, Peng H, Liu Y, Araujo FC, Watanabe I, Reis FM, Milsted A. MAS promoter regulation: a role for Sry and tyrosine nitration of the KRAB domain of ZNF274 as a feedback mechanism. Clin Sci 126: 727-738, 2014.
94. Prokop JW, Underwood AC, Turner ME, Miller N, Pietrzak D, Scott S, Smith C, Milsted A. Analysis of Sry duplications on the Rattus norvegicus Y-chromosome. BMC Genom 14: 792, 2013.
95. Prokop JW, Watanabe IKM, Turner ME, Underwood AC, Martins AS, Milsted A. From rat to human: regulation of renin-angiotensin system genes by sry. Int J Hypertens 2012: 724240, 2012.
96. Ralf A, van Oven M, Zhong K, Kayser M. Simultaneous analysis of hundreds of Y-chromosomal SNPs for high-resolution paternal lineage classification using targeted semiconductor sequencing. Hum Mutat 36: 151-159, 2015.
97. Reckelhoff JF. Gender differences in the regulation of blood pressure. Hypertension 37: 1199-1208, 2001.
98. Reckelhoff JF, Zhang H, Srivastava K, Granger JP. Gender differences in hypertension in spontaneously hypertensive rats: role of androgens and androgen receptor. Hypertension 34: 920-923, 1999.
99. Robinson DP, Huber SA, Moussawi M, Roberts B, Teuscher C, Watkins R, Arnold AP, Klein SL. Sex chromosome complement contributes to sex differences in coxsackievirus B3 but not influenza A virus pathogenesis. Biol Sex Diff 2: 8, 2011.
100. Rodríguez S, Chen X, Miller GJ, Day INM. Non-recombining chromosome Y haplogroups and centromeric HindIII RFLP in relation to blood pressure in 2,743 middle-aged Caucasian men from the UK. Hum Genet 116: 311-318, 2005.
101. Roland AV, Nunemaker CS, Keller SR, Moenter SM. Prenatal androgen exposure programs metabolic dysfunction in female mice. J Endocrinol 207: 213-223, 2010.
102. Ronen D, Benvenisty N. Sex-dependent gene expression in human pluripotent stem cells. Cell Rep 8: 923-932, 2014.
103. Ross JL, Tartaglia N, Merry DE, Dalva M, Zinn AR. Behavioral phenotypes in males with XYY and possible role of increased NLGN4Y expression in autism features. Genes Brain Behav 14: 137-144, 2015.
104. Rosser ZH, Balaresque P, Jobling MA. Gene conversion between the X chromosome and the male-specific region of the Y chromosome at a translocation hotspot. Am J Hum Genet 85: 130-134, 2009.
105. Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Page DC. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423: 873-876, 2003.
106. Russo P, Siani A, Miller MA, Karanam S, Esposito T, Gianfrancesco F, Barba G, Lauria F, Strazzullo P, Cappuccio FP. Genetic variants of Y chromosome are associated with a protective lipid profile in black men. Arterioscler Thromb Vasc Biol 28: 1569-1574, 2008.
107. Russo P, Venezia A, Lauria F, Strazzullo P, Cappuccio FP, Iacoviello L, Barba G, Siani A. HindIII(+/-) polymorphism of the y chromosome, blood pressure, and serum lipids: no evidence of association in three white populations*. Am J Hypertens 19: 331-338, 2006.
108. Vom Saal FS. Prenatal exposure to androgen influences morphology and aggressive behavior of male and female mice. Horm Behav 12: 1-11, 1979.
109. Secombe J, Eisenman RN. The function and regulation of the JARID1 family of histone H3 lysine 4 demethylases: the Myc connection. Cell Cycle 6: 1324-1328, 2007.
110. Selmanoff MK, Jumonville JE, Maxson SC, Ginsburg BE. Evidence for a Y chromosomal contribution to an aggressive phenotype in inbred mice. Nature 253: 529-530, 1975.
111. Sezgin E, Lind JM, Shrestha S, Hendrickson S, Goedert JJ, Donfield S, Kirk GD, Phair JP, Troyer JL, O’Brien SJ, Smith MW. Association of Y chromosome haplogroup I with HIV progression, and HAART outcome. Hum Genet 125: 281-294, 2009.
112. Sharpe RM. Pathways of endocrine disruption during male sexual differentiation and masculinisation. Best Pract Res Clin Endocrinol Metab 20: 91-110, 2006.
113. Shpargel KB, Sengoku T, Yokoyama S, Magnuson T. UTX and UTY demonstrate histone demethylase-independent function in mouse embryonic development. PLoS Genet 8: e1002964, 2012.
114. Shrenker P, Maxson SC. The Y chromosomes of DBA/1Bg and DBA/2Bg compared for effects on intermale aggression. Behav Genet 12: 429-434, 1982.
115. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou SF, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang SP, Waterston RH, Wilson RK, Rozen S, Page DC. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423: 825-837, 2003.
116. Smith-Bouvier DL, Divekar AA, Sasidhar M, Du S, Tiwari-Woodruff SK, King JK, Arnold AP, Singh RR, Voskuhl RR. A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med 205: 1099-1108, 2008.
117. Soh YQS, Alföldi J, Pyntikova T, Brown LG, Graves T, Minx PJ, Fulton RS, Kremitzki C, Koutseva N, Mueller JL, Rozen S, Hughes JF, Owens E, Womack JE, Murphy WJ, Cao Q, de Jong P, Warren WC, Wilson RK, Skaletsky H, Page DC. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 159: 800-813, 2014.
118. Strahorn P, Graham D, Charchar FJ, Sattar N, McBride MW, Dominiczak AF. Genetic determinants of metabolic syndrome components in the stroke-prone spontaneously hypertensive rat. J Hypertens 23: 2179-2186, 2005.
119. Suto J. Y chromosome of the inbred mouse KK/Ta strain is associated with reduced body size in Y-consomic strains. BMC Res Notes 6: 64, 2013.
120. Suto J, Satou K. Effect of the Y chromosome on plasma high-density lipoprotein-cholesterol levels in Y-chromosome-consomic mouse strains. BMC Res Notes 7: 393, 2014.
121. Tordjman S, Roubertoux PL, Carlier M, Moutier R, Anderson G, Launay M, Degrelle H. Linkage between brain serotonin concentration and the sex-specific part of the Y-chromosome in mice. Neurosci Lett 183: 190-192, 1995.
122. Trombetta B, Cruciani F, Sellitto D, Scozzari R. A new topology of the human Y chromosome haplogroup E1b1 (E-P2) revealed through the use of newly characterized binary polymorphisms. PLoS One 6: e16073, 2011.
123. Trombetta B, Sellitto D, Scozzari R, Cruciani F. Inter- and intraspecies phylogenetic analyses reveal extensive X-Y gene conversion in the evolution of gametologous sequences of human sex chromosomes. Mol Biol Evol 31: 2108-2123, 2014.
124. Turner ME, Ely D, Prokop J, Milsted A. Sry, more than testis determination? Am J Physiol Regul Integr Comp Physiol 301: R561-R571, 2011.
125. Turner ME, Farkas J, Dunmire J, Ely D, Milsted A. Which Sry locus is the hypertensive Y chromosome locus? Hypertension 53: 430-435, 2008.
126. Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson Å, Kampf C, Sjöstedt E, Asplund A, Olsson I, Edlund K, Lundberg E, Navani S, Szigyarto CAK, Odeberg J, Djureinovic D, Takanen JO, Hober S, Alm T, Edqvist PH, Berling H, Tegel H, Mulder J, Rockberg J, Nilsson P, Schwenk JM, Hamsten M, von Feilitzen K, Forsberg M, Persson L, Johansson F, Zwahlen M, von Heijne G, Nielsen J, Pontén F. Proteomics. Tissue-based map of the human proteome. Science 347: 1260419, 2015.
127. Veitia RA. FOXL2 versus SOX9: a lifelong “battle of the sexes.” Bioessays 32: 375-380, 2010.
128. Vijayakumar S, Garcia D, Hensel CH, Banerjee M, Bracht T, Xiang R, Kagan J, Naylor SL. The human Y chromosome suppresses the tumorigenicity of PC-3, a human prostate cancer cell line, in athymic nude mice. Genes Chromosomes Cancer 44: 365-372, 2005.
129. Waxman DJ, Holloway MG. Sex differences in the expression of hepatic drug metabolizing enzymes. Mol Pharmacol 76: 215-228, 2009.
130. Whitacre CC. Sex differences in autoimmune disease. Nat Immunol 2: 777-780, 2001.
131. Willuweit S, Roewer L. The new Y chromosome haplotype reference database. Forensic Sci Int Genet 15: 43-48, 2015.
132. Wilson CA, Davies DC. The control of sexual differentiation of the reproductive system and brain. Reproduction 133: 331-359, 2007.
133. Xu J, Deng X, Watkins R, Disteche CM. Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons. J Neurosci 28: 4521-4527, 2008.
134. Yamazaki K, Beauchamp GK, Matsuzaki O, Bard J, Thomas L, Boyse EA. Participation of the murine X and Y chromosomes in genetically determined chemosensory identity. Proc Natl Acad Sci USA 83: 4438-4440, 1986.
135. Yuan X, Lu ML, Li T, Balk SP. SRY interacts with and negatively regulates androgen receptor transcriptional activity. J Biol Chem 276: 46647-46654, 2001.
136. Zhao D, McBride D, Nandi S, McQueen HA, McGrew MJ, Hocking PM, Lewis PD, Sang HM, Clinton M. Somatic sex identity is cell autonomous in the chicken. Nature 464: 237-242, 2010.
137. Zhou J, Sackton TB, Martinsen L, Lemos B, Eickbush TH, Hartl DL. Y chromosome mediates ribosomal DNA silencing and modulates the chromatin state in Drosophila. Proc Natl Acad Sci USA 109: 9941-9946, 2012.
138. Zuloaga DG, McGivern RF, Handa RJ. Organizational influence of the postnatal testosterone surge on the circadian rhythm of core body temperature of adult male rats. Brain Res 1268: 68-75, 2009.