The landscape of sex-differential transcriptome and its consequent selection in human adults

BMC Biology

Volumn 15, Issue 1, 2017, Pages

  Gershoni, Moran ^a   Pietrokovski, Shmuel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Sex differential expression; Sex differential selection; Sexual dimorphism

Indexed keywords

TRANSCRIPTOME;

ADULT; AGED; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETICS; HUMAN; MALE; MIDDLE AGED; OPEN READING FRAME; POPULATION GENETICS; SEXUAL DEVELOPMENT; YOUNG ADULT;

ADULT; AGED; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS, POPULATION; HUMANS; MALE; MIDDLE AGED; OPEN READING FRAMES; SELECTION, GENETIC; SEX CHARACTERISTICS; TRANSCRIPTOME; YOUNG ADULT;

EID: 85011883695     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-017-0352-z     Document Type: Article

References (65)

1. Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman T-L, Hahn MW, Kitano J, Mayrose I, Ming R. Sex determination: why so many ways of doing it? PLoS Biol. 2014;12:e1001899.
2. McClellan HL, Miller SJ, Hartmann PE. Evolution of lactation: nutrition v. protection with special reference to five mammalian species. Nutr Res Rev. 2008;21:97-116.
3. McClellan J, King M-C. Genetic heterogeneity in human disease. Cell. 2010;141:210-7.
4. Connallon T. The geography of sex-specific selection, local adaptation, and sexual dimorphism. Evolution. 2015;69:2333-44.
5. Deaner RO, Shepherd SV, Platt ML. Familiarity accentuates gaze cuing in women but not men. Biol Lett. 2007;3:65-8.
6. Goldstein JM, Holsen L, Handa R, Tobet S. Fetal hormonal programming of sex differences in depression: linking women's mental health with sex differences in the brain across the lifespan. Front Neurosci. 2014;8:247.
7. Giedd JN, Castellanos FX, Rajapakse JC, Vaituzis AC, Rapoport JL. Sexual dimorphism of the developing human brain. Prog Neuro-Psychopharmacol Biol Psychiatry. 1997;21:1185-201.
8. Collaer ML, Hines M. Human behavioral sex differences: a role for gonadal hormones during early development? Psychol Bull. 1995;118:55.
9. Waldron I. Sex differences in human mortality: the role of genetic factors. Soc Sci Med. 1983;17:321-33.
10. Subbaraman M, Goldman-Mellor S, Anderson E, LeWinn K, Saxton K, Shumway M, Catalano R. An exploration of secondary sex ratios among women diagnosed with anxiety disorders. Human Reprod. 2010;25:2084-91.
11. Pulido MR, Rabanal-Ruiz Y, Almabouada F, Díaz-Ruiz A, Burrell MA, Vázquez MJ, Castaño JP, Kineman RD, Luque RM, Diéguez C. Nutritional, hormonal, and depot-dependent regulation of the expression of the small GTPase Rab18 in rodent adipose tissue. J Mol Endocrinol. 2013;50:19-29.
12. Link JC, Chen X, Arnold AP, Reue K. Metabolic impact of sex chromosomes. Adipocyte. 2013;2:74-9.
13. Bartley EJ, Fillingim RB. Sex differences in pain: a brief review of clinical and experimental findings. Br J Anaesth. 2013;111:52-8.
14. Courtright SH, McCormick BW, Postlethwaite BE, Reeves CJ, Mount MK. A meta-analysis of sex differences in physical ability: revised estimates and strategies for reducing differences in selection contexts. J Appl Psychol. 2013;98:623.
15. Tseng LA, Delmonico MJ, Visser M, Boudreau RM, Goodpaster BH, Schwartz AV, Simonsick EM, Satterfield S, Harris T, Newman AB. Body composition explains sex differential in physical performance among older adults. J Gerontol Ser A Biol Med Sci. 2014;69:93-100.
16. Dimas AS, Nica AC, Montgomery SB, Stranger BE, Raj T, Buil A, Giger T, Lappalainen T, Gutierrez-Arcelus M, McCarthy MI. Sex-biased genetic effects on gene regulation in humans. Genome Res. 2012;22:2368-75.
17. Rawlik K, Canela-Xandri O, Tenesa A. Evidence for sex-specific genetic architectures across a spectrum of human complex traits. Genome Biol. 2016;17:166.
18. Gilks WP, Abbott JK, Morrow EH. Sex differences in disease genetics: evidence, evolution, and detection. Trends Genet. 2014;30:453-63.
19. Sandberg K, Verbalis JG. Sex and the basic scientist: is it time to embrace Title IX? Biol Sex Differ. 2013;4:13.
20. Fisher RA. The genetical theory of natural selection: a complete variorum edition. Oxford: Oxford University Press; 1930.
21. Connallon T, Clark AG. The resolution of sexual antagonism by gene duplication. Genetics. 2011;187:919-37.
22. Frank SA, Hurst LD. Mitochondria and male disease. Nature. 1996;383:224.
23. Morrow EH, Connallon T. Implications of sexspecific selection for the genetic basis of disease. Evol Appl. 2013;6:1208-17.
24. Gershoni M, Pietrokovski S. Reduced selection and accumulation of deleterious mutations in genes exclusively expressed in men. Nat Commun. 2014;5:4438.
25. Innocenti P, Morrow EH. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol. 2010;8:e1000335.
26. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A. 2004;101:6062-7.
27. Ardlie KG, Deluca DS, Segrè AV, Sullivan TJ, Young TR, Gelfand ET, Trowbridge CA, Maller JB, Tukiainen T, Lek M. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science. 2015;348:648-60.
28. Melé M, Ferreira PG, Reverter F, DeLuca DS, Monlong J, Sammeth M, Young TR, Goldmann JM, Pervouchine DD, Sullivan TJ. The human transcriptome across tissues and individuals. Science. 2015;348:660-5.
29. Mank JE. The transcriptional architecture of phenotypic dimorphism. Nature Ecology & Evolution. 2017;1:0006.
30. Carithers LJ, Ardlie K, Barcus M, Branton PA, Britton A, Buia SA, Compton CC, DeLuca DS, Peter-Demchok J, Gelfand ET. A novel approach to high-quality postmortem tissue procurement: The GTEx Project. Biopreservation Biobanking. 2015;13:311-9.
31. Tarazona S, Furió-Tarí P, Turrà D, Di Pietro A, Nueda MJ, Ferrer A, Conesa A. Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package. Nucleic Acids Res. 2015;43:e140.
32. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A. Differential expression in RNA-seq: a matter of depth. Genome Res. 2011;21:2213-23.
33. Mangs HA, Morris BJ. The human pseudoautosomal region (PAR): origin, function and future. Curr Genomics. 2007;8:129-36.
34. Suzuki R, Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006;22:1540-2.
35. Fuchs SB-A, Lieder I, Stelzer G, Mazor Y, Buzhor E, Kaplan S, Bogoch Y, Plaschkes I, Shitrit A, Rappaport N. GeneAnalytics: an integrative gene set analysis tool for next generation sequencing, RNAseq and microarray data. OMICS. 2016;20:139-51.
36. Holditch SJ, Schreiber CA, Burnett JC, Ikeda Y. Arterial remodeling in B-type natriuretic peptide knock-out females. Sci Rep. 2016;6:25623.
37. Wang TJ, Larson MG, Levy D, Leip EP, Benjamin EJ, Wilson PW, Sutherland P, Omland T, Vasan RS. Impact of age and sex on plasma natriuretic peptide levels in healthy adults. Am J Cardiol. 2002;90:254-8.
38. Clark BC, Collier SR, Manini TM, Ploutz-Snyder LL. Sex differences in muscle fatigability and activation patterns of the human quadriceps femoris. Eur J Appl Physiol. 2005;94:196-206.
39. Russ DW, Kent-Braun JA. Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. J Appl Physiol. 2003;94:2414-22.
40. Ellegren H, Parsch J. The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet. 2007;8:689-98.
41. 1000 Genomes Project Consortium, Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, Gibbs RA, Hurles ME, McVean GA. A map of human genome variation from population-scale sequencing. Nature. 2010;467:1061-73.
42. Kryazhimskiy S, Plotkin JB. The population genetics of dN/dS. PLoS Genet. 2008;4:e1000304.
43. Ostrow SL, Barshir R, DeGregori J, Yeger-Lotem E, Hershberg R. Cancer evolution is associated with pervasive positive selection on globally expressed genes. PLoS Genet. 2014;10:e1004239.
44. Tennessen JA, Bigham AW, O'Connor TD, Fu W, Kenny EE, Gravel S, McGee S, Do R, Liu X, Jun G, et al. Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science. 2012;337:64-9.
45. Wu R, Lin M. Functional mapping - how to map and study the genetic architecture of dynamic complex traits. Nat Rev Genet. 2006;7:229-37.
46. de Moura Souza A, Sichieri R. Association between serum TSH concentration within the normal range and adiposity: a review. Eur J Endocrinol. 2011;165:11-5.
47. Skorupskaite K, George JT, Anderson RA. The kisspeptin-GnRH pathway in human reproductive health and disease. Hum Reprod Update. 2014;20:485-500.
48. Guengerich FP, Waterman MR, Egli M. Recent structural insights into cytochrome P450 function. Trends Pharmacol Sci. 2016;37:625-40.
49. Lamba V, Lamba J, Yasuda K, Strom S, Davila J, Hancock ML, Fackenthal JD, Rogan PK, Ring B, Wrighton SA. Hepatic CYP2B6 expression: gender and ethnic differences and relationship to CYP2B6 genotype and CAR (constitutive androstane receptor) expression. J Pharmacol Exp Ther. 2003;307:906-22.
50. Xiong Q, Jiao Y, Hasty KA, Canale ST, Stuart JM, Beamer WG, Deng H-W, Baylink D, Gu W. Quantitative trait loci, genes, and polymorphisms that regulate bone mineral density in mouse. Genomics. 2009;93:401-14.
51. Brain S, Williams T, Tippins J, Morris H, MacIntyre I. Calcitonin gene-related peptide is a potent vasodilator. Nature. 1985;313:54-6.
52. Gangula PR, Zhao H, Supowit SC, Wimalawansa SJ, Dipette DJ, Westlund KN, Gagel RF, Yallampalli C. Increased blood pressure in α-calcitonin gene-related peptide/calcitonin gene knockout mice. Hypertension. 2000;35:470-5.
53. Bateman AJ. Intra-sexual selection in Drosophila. Heredity. 1948;2:349-68.
54. Cerase A, Pintacuda G, Tattermusch A, Avner P. Xist localization and function: new insights from multiple levels. Genome Biol. 2015;16:1.
55. Kassam I, Lloyd-Jones L, Holloway A, Small KS, Zeng B, Bakshi A, Metspalu A, Gibson G, Spector TD, Esko T. Autosomal genetic control of human gene expression does not differ across the sexes. Genome Biol. 2016;17:248.
56. Chen C-Y, Lopes-Ramos CM, Kuijjer ML, Paulson JN, Sonawane AR, Fagny M, Platig J, Glass K, Quackenbush J, DeMeo DL. Sexual dimorphism in gene expression and regulatory networks across human tissues. bioRxiv 2016. Epub ahead of print. doi:10.1101/082289.
57. Herrero J, Muffato M, Beal K, Fitzgerald S, Gordon L, Pignatelli M, Vilella AJ, Searle SM, Amode R, Brent S. Ensembl comparative genomics resources. Database. 2016;2016:bav096.
58. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38:e164.
59. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc. 2009;4:1073-81.
60. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7:248-9.
61. Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E, Fennell T, O'Donnell-Luria AH, Ware JS, Hill AJ, Cummings BB, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016;536:285-91.
62. Efron B, Tibshirani R, Storey JD, Tusher V. Empirical Bayes analysis of a microarray experiment. J Am Stat Assoc. 2001;96:1151-60.
63. Ferin M, Jewelewicz R. The menstrual cycle: physiology, reproductive disorders, and infertility. New York: Oxford University Press; 1993.
64. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1.
65. Kaufman L, Rousseeuw PJ. Finding groups in data: an introduction to cluster analysis, vol. 344. Hoboken, New Jersey: John Wiley & Sons; 2009.