Genetic association suggests that SMOC1 mediates between prenatal sex hormones and digit ratio

Human Genetics

Volumn 132, Issue 4, 2013, Pages 415-421

  Lawrance Owen, Adam J ^a   Bargary, Gary ^a,b   Bosten, Jenny M ^a   Goodbourn, Patrick T ^a   Hogg, Ruth E ^a,c   Mollon, J D ^a  

^a UK   (United Kingdom)

^b CITY UNIVERSITY   (United Kingdom)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM BINDING PROTEIN; SECRETED MODULAR CALCIUM BINDING PROTEIN 1; SEX HORMONE; UNCLASSIFIED DRUG;

ADULT; ALLELE; ARTICLE; CHROMOSOME 14; FINGER; GENETIC ASSOCIATION; GENETIC TRAIT; GENETIC VARIABILITY; GENOTYPE; HUMAN; META ANALYSIS; NORMAL HUMAN; PRENATAL PERIOD; PRIORITY JOURNAL; PROSTATE; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; FEMALE; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; GONADAL STEROID HORMONES; HUMANS; MALE; OSTEONECTIN; PROSTATE;

EID: 84876464803     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-012-1259-y     Document Type: Article

References (65)

1. Abouzeid H, Boisset G, Favez T, Youssef M, Marzouk I, Shakankiry N, Bayoumi N, Descombes P, Agosti C, Munier FL, Schorderet DF (2011) Mutations in the SPARC-related modular calcium-binding protein 1 gene, SMOC1, cause Waardenburg anophthalmia syndrome. Am J Hum Genet 88:92-98. doi: 10.1016/j.ajhg.2010.12.002
2. Abramovich DR (1974) Human sexual differentiation - in utero influences. J Obstet Gynaecol Br Commonw 81:448-453
3. Allaway HC, Bloski TG, Pierson RA, Lujan ME (2009) Digit ratios (2D:4D) determined by computer-assisted analysis are more reliable than those using physical measurements, photocopies, and printed scans. Am J Hum Biol 21:365-370. doi: 10.1002/ajhb.20892
4. Bang AK, Carlsen E, Holm M, Petersen JH, Skakkebaek NE, Jørgensen N (2005) A study of finger lengths, semen quality and sex hormones in 360 young men from the general Danish population. Hum Reprod 20:3109-3113. doi: 10.1093/humrep/dei170
5. Berenbaum SA, Bryk KK, Nowak N, Quigley CA, Moffat S (2009) Fingers as a marker of prenatal androgen exposure. Endocrinology 150:5119-5124. doi: 10.1210/en.2009-0774
6. Boruk M (1998) AF-2-Dependent potentiation of CCAAT enhancer binding protein-mediated transcriptional activation by glucocorticoid receptor. Mol Endocrinol 12:1749-1763. doi: 10.1210/me.12.11.1749
7. Bradshaw AD (2012) Diverse biological functions of the SPARC family of proteins. Int J Biochem Cell Biol 44:480-488. doi: 10.1016/j.biocel.2011.12.021
8. Brown WM, Hines M, Fane BA, Breedlove SM (2002) Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Horm Behav 42:380-386
9. Burley NT, Foster VS (2004) Digit ratio varies with sex, egg order and strength of mate preference in zebra finches. Proc R Soc B 271:239-244
10. Choi Y-A, Lim J, Kim KM, Acharya B, Cho J-Y, Bae Y-C, Shin H-I, Kim S-Y, Park EK (2010) Secretome analysis of human BMSCs and identification of SMOC1 as an important ECM protein in osteoblast differentiation. J Proteome Res 9:2946-2956. doi: 10.1021/pr901110q
11. Choi IH, Kim KH, Jung H, Yoon SJ, Kim SW, Kim TB (2011) Second to fourth digit ratio: a predictor of adult penile length. Asian J Androl 13:710-714. doi: 10.1038/aja.2011.75
12. Coates JM, Gurnell M, Rustichini A (2009) Second-to-fourth digit ratio predicts success among high-frequency financial traders. Proc Natl Acad Sci USA 106:623-628. doi: 10.1073/pnas.0810907106
13. Coleman IM, Kiefer JA, Brown LG, Pitts TE, Nelson PS, Brubaker KD, Vessella RL, Corey E (2006) Inhibition of androgen-independent prostate cancer by estrogenic compounds is associated with increased expression of immune-related genes. Neoplasia 8:862-878. doi: 10.1593/neo.06328
14. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigó R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775-1789. doi: 10.1101/gr.132159.111
15. Ecker A (1875) Einige Bemerkungen über einen schwankenden Charakter in der Hand des Menschen. Archiv für Anthroplogie 8:67-74
16. Fink B, Manning JT, Neave N, Tan U (2004) Second to fourth digit ratio and hand skill in Austrian children. Biol Psychol 67:375-384. doi: 10.1016/j.biopsycho.2004.03.012
17. Fink B, Grammer K, Mitteroecker P, Gunz P, Schaefer K, Bookstein FL, Manning JT (2005) Second to fourth digit ratio and face shape. Proc R Soc B 272:1995-2001
18. Fink B, Manning JT, Neave N (2006) The 2nd-4th digit ratio (2D:4D) and neck circumference: implications for risk factors in coronary heart disease. Int J Obes 30:711-714. doi: 10.1038/sj.ijo.0803154
19. Forstmeier W, Mueller JC, Kempenaers B (2010) A polymorphism in the oestrogen receptor gene explains covariance between digit ratio and mating behaviour. Proc R Soc B 277:3353-3361. doi: 10.1098/rspb.2010.1007
20. Genomes Project Consortium (2010) A map of human genome variation from population-scale sequencing. Nature 467:1061-1073. doi: 10.1038/nature09534
21. Goodbourn PT, Bosten JM, Hogg RE, Bargary G, Lawrance-Owen AJ, Mollon JD (2012) Do different 'magnocellular tasks' probe the same neural substrate? Proc R Soc B 279:4263-4271. doi: 10.1098/rspb.2012.1430
22. Grimbos T, Dawood K, Burriss RP, Zucker KJ, Puts DA (2010) Sexual orientation and the second to fourth finger length ratio: a meta-analysis in men and women. Behav Neurosci 124:278-287. doi: 10.1037/a0018764
23. Hönekopp J (2011) Relationships between digit ratio 2D:4D and self-reported aggression and risk taking in an online study. Pers Individ Dif 51:77-80. doi: 10.1016/j.paid.2011.03.010
24. Hönekopp J (2012) Digit ratio 2D:4D in relation to autism spectrum disorders, empathizing, and systemizing: a quantitative review. Autism Res 5:221-230. doi: 10.1002/aur.1230
25. Hönekopp J, Schuster M (2010) A meta-analysis on 2D:4D and athletic prowess: substantial relationships but neither hand out-predicts the other. Pers Individ Dif 48:4-10. doi: 10.1016/j.paid.2009.08.009
26. Howie BN, Donnelly P, Marchini J (2009) A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet 5:e1000529. doi: 10.1371/journal.pgen.1000529
27. Howie B, Marchini J, Stephens M (2011) Genotype imputation with thousands of genomes. G3 (Bethesda) 1:457-470. doi: 10.1534/g3.111.001198
28. Jung H, Kim KH, Yoon SJ, Kim TB (2010) Second to fourth digit ratio: a predictor of prostate-specific antigen level and the presence of prostate cancer. BJU Int 107:591-596. doi: 10.1111/j.1464-410X.2010.09490.x
29. Kimura S, Schaumann BA, Plato CC, Kitagawa T (1990) Embryological development and prevalence of digital flexion creases. Anat Rec 226:249-257. doi: 10.1002/ar.1092260214
30. Klump KL, Gobrogge KL, Perkins PS, Thorne D, Sisk CL, Breedlove SM (2006) Preliminary evidence that gonadal hormones organize and activate disordered eating. Psychol Med 36:539-546. doi: 10.1017/S0033291705006653
31. Kondo T, Zákány J, Innis JW, Duboule D (1997) Of fingers, toes and penises. Nature 390:29. doi: 10.1038/36234
32. Kornhuber J, Erhard G, Lenz B, Kraus T, Sperling W, Bayerlein K, Biermann T, Stoessel C (2011) Low digit ratio 2D:4D in alcohol dependent patients. PLoS One 6:e19332. doi: 10.1371/journal.pone.0019332
33. Love HD, Booton SE, Boone BE, Breyer JP, Koyama T, Revelo MP, Shappell SB, Smith JR, Hayward SW (2009) Androgen regulated genes in human prostate xenografts in mice: relation to BPH and prostate cancer. PLoS One 4:e8384. doi: 10.1371/journal.pone.0008384
34. Lutchmaya S, Baron-Cohen S, Raggatt P, Knickmeyer R, Manning JT (2004) 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum Dev 77:23-28. doi: 10.1016/j.earlhumdev.2003.12.002
35. MacLusky N, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211:1294-1302. doi: 10.1126/science.6163211
36. Malas MA, Dogan S, Evcil EH, Desdicioglu K (2006) Fetal development of the hand, digits and digit ratio (2D:4D). Early Hum Dev 82:469-475. doi: 10.1016/j.earlhumdev.2005.12.002
37. Manning JT, Fink B (2011) Is low digit ratio linked with late menarche? Evidence from the BBC internet study. Am J Hum Biol 23:527-533. doi: 10.1002/ajhb.21186
38. Manning JT, Leinster SJ (2001) re: The ratio of 2nd to 4th digit length and age at presentation of breast cancer: a link with prenatal oestrogen? Breast 10:355-357. doi: 10.1054/brst.2001.0284
39. Manning JT, Scutt D, Wilson J, Lewis-Jones DI (1998) The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Hum Reprod 13:3000-3004
40. Manning JT, Stewart A, Bundred PE, Trivers RL (2004) Sex and ethnic differences in 2nd to 4th digit ratio of children. Early Hum Dev 80:161-168. doi: 10.1016/j.earlhumdev.2004.06.004
41. Martel MM, Gobrogge KL, Breedlove SM, Nigg JT (2008) Masculinized finger-length ratios of boys, but not girls, are associated with attention-deficit/hyperactivity disorder. Behav Neurosci 122:273-281. doi: 10.1037/0735-7044.122.2.273
42. McIntyre MH (2006) The use of digit ratios as markers for perinatal androgen action. Reprod Biol Endocrinol 4:10. doi: 10.1186/1477-7827-4-10
43. McIntyre MH, Ellison PT, Lieberman DE, Demerath E, Towne B (2005) The development of sex differences in digital formula from infancy in the Fels Longitudinal Study. Proc R Soc B 272:1473-1479. doi: 10.1098/rspb.2005.3100
44. Medland SE, Loehlin JC (2008) Multivariate genetic analyses of the 2D:4D ratio: examining the effects of hand and measurement technique in data from 757 twin families. Twin Res Hum Genet 11:335-341. doi: 10.1375/twin.11.3.335
45. Medland SE, Zayats T, Glaser B, Nyholt DR, Gordon SD, Wright MJ, Montgomery GW, Campbell MJ, Henders AK, Timpson NJ, Peltonen L, Wolke D, Ring SM, Deloukas P, Martin NG, Smith GD, Evans DM (2010) A variant in LIN28B is associated with 2D:4D finger-length ratio, a putative retrospective biomarker of prenatal testosterone exposure. Am J Hum Genet 86:519-525. doi: 10.1016/j.ajhg.2010.02.017
46. Nelson E, Rolian C, Cashmore L, Shultz S (2011) Digit ratios predict polygyny in early apes, Ardipithecus, Neanderthals and early modern humans but not in Australopithecus. Proc R Soc B 278:1556-1563
47. Okada I, Hamanoue H, Terada K, Tohma T, Megarbane A, Chouery E, Abou-Ghoch J, Jalkh N, Cogulu O, Ozkinay F, Horie K, Takeda J, Furuichi T, Ikegawa S, Nishiyama K, Miyatake S, Nishimura A, Mizuguchi T, Niikawa N, Hirahara F, Kaname T, Yoshiura K-I, Tsurusaki Y, Doi H, Miyake N, Furukawa T, Matsumoto N, Saitsu H (2011) SMOC1 is essential for ocular and limb development in humans and mice. Am J Hum Genet 88:30-41. doi: 10.1016/j.ajhg.2010.11.012
48. Okten A, Kalyoncu M, Yariş N (2002) The ratio of second- and fourth-digit lengths and congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Early Hum Dev 70:47-54
49. Pazin DE, Albrecht KH (2009) Developmental expression of Smoc1 and Smoc2 suggests potential roles in fetal gonad and reproductive tract differentiation. Dev Dyn 238:2877-2890. doi: 10.1002/dvdy.22124
50. Peters M, Manning JT, Reimers S (2007) The effects of sex, sexual orientation, and digit ratio (2D:4D) on mental rotation performance. Arch Sex Behav 36:251-260. doi: 10.1007/s10508-006-9166-8
51. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904-909. doi: 10.1038/ng1847
52. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559-575. doi: 10.1086/519795
53. Rahman AA, Lophatananon A, Stewart-Brown S, Harriss D, Anderson J, Parker T, Easton D, Kote-Jarai Z, Pocock R, Dearnaley D, Guy M, O'Brien L, Wilkinson RA, Hall AL, Sawyer E, Page E, Liu J-F, Eeles RA, Muir K (2011) Hand pattern indicates prostate cancer risk. Br J Cancer 104:175-177. doi: 10.1038/sj.bjc.6605986
54. Rainger J, van Beusekom E, Ramsay JK, McKie L, Al-Gazali L, Pallotta R, Saponari A, Branney P, Fisher M, Morrison H, Bicknell L, Gautier P, Perry P, Sokhi K, Sexton D, Bardakjian TM, Schneider AS, Elcioglu N, Ozkinay F, Koenig R, Megarbane A, Semerci CN, Khan A, Zafar S, Hennekam R, Sousa SB, Ramos L, Garavelli L, Furga AS, Wischmeijer A, Jackson IJ, Gillessen-Kaesbach G, Brunner HG, Wieczorek D, van Bokhoven H, Fitzpatrick DR, Mégarbané A (2011) Loss of the BMP antagonist, SMOC-1, causes Ophthalmo-acromelic (Waardenburg Anophthalmia) syndrome in humans and mice. PLoS Genet 7:e1002114. doi: 10.1371/journal.pgen.1002114
55. Schaeffer EM, Marchionni L, Huang Z, Simons B, Blackman A, Yu W, Parmigiani G, Berman DM (2008) Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene 27:7180-7191. doi: 10.1038/onc.2008.327
56. Stein B, Yang MX (1995) Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Mol Cell Biol 15:4971-4979
57. Stevenson JC, Everson PM, Williams DC, Hipskind G, Grimes M, Mahoney ER (2007) Attention deficit/hyperactivity disorder (ADHD) symptoms and digit ratios in a college sample. Am J Hum Biol 19:41-50. doi: 10.1002/ajhb.20571
58. Stricker S, Mundlos S (2011) Mechanisms of digit formation: human malformation syndromes tell the story. Dev Dyn 240:990-1004. doi: 10.1002/dvdy.22565
59. Talarovicová A, Krsková L, Blazeková J (2009) Testosterone enhancement during pregnancy influences the 2D:4D ratio and open field motor activity of rat siblings in adulthood. Horm Behav 55:235-239. doi: 10.1016/j.yhbeh.2008.10.010
60. Thomas JT, Canelos P, Luyten FP, Moos M (2009) Xenopus SMOC-1 Inhibits bone morphogenetic protein signaling downstream of receptor binding and is essential for postgastrulation development in Xenopus. J Biol Chem 284:18994-19005. doi: 10.1074/jbc.M807759200
61. Vannahme C, Smyth N, Miosge N, Gösling S, Frie C, Paulsson M, Maurer P, Hartmann U (2002) Characterization of SMOC-1, a novel modular calcium-binding protein in basement membranes. J Biol Chem 277:37977-37986. doi: 10.1074/jbc.M203830200
62. Wilson GD (1983) Finger-length as an index of assertiveness in women. Pers Individ Dif 4:111-112. doi: 10.1016/0191-8869(83)90061-2
63. Yuan X, Lu ML, Li T, Balk SP (2001) SRY interacts with and negatively regulates androgen receptor transcriptional activity. J Biol Chem 276:46647-46654. doi: 10.1074/jbc.M108404200
64. Zhang W, Robertson J, Doherty S, Liu JJ, Maciewicz RA, Muir KR, Doherty M (2008) Index to ring finger length ratio and the risk of osteoarthritis. Arthritis Rheum 58:137-144. doi: 10.1002/art.23237
65. Zheng Z, Cohn MJ (2011) Developmental basis of sexually dimorphic digit ratios. Proc Natl Acad Sci USA 108:16289-16294. doi: 10.1073/pnas.1108312108