Gene-gene interaction between RBMS3 and ZNF516 influences bone mineral density

Journal of Bone and Mineral Research

Volumn 28, Issue 4, 2013, Pages 828-837

  Yang, Tie Lin ^a   Guo, Yan ^a   Li, Jian ^b   Zhang, Lei ^c   Shen, Hui ^b   Li, Siyang M ^d   Li, Siyuan K ^d   Tian, Qing ^b   Liu, Yong Jun ^b   Papasian, Christopher J ^d   Deng, Hong Wen ^a,b,c  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b TULANE UNIVERSITY   (United States)

^c UNIVERSITY OF SHANGHAI FOR SCIENCE AND TECHNOLOGY   (China)

^d UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

Author keywords

association; BMD; interaction; osteoporosis

Indexed keywords

ADULT; AFRICAN AMERICAN; ARTICLE; BONE DENSITY; CAUCASIAN; CONTROLLED STUDY; FEMALE; GENE; GENE INTERACTION; HIP; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; OSTEOPOROSIS; RBMS3 GENE; SCORING SYSTEM; SINGLE NUCLEOTIDE POLYMORPHISM; ZNF516 GENE; EPISTASIS; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MIDDLE AGED; PHYSIOLOGY; REPRODUCIBILITY;

DNA BINDING PROTEIN; RBMS3 PROTEIN, HUMAN; RNA BINDING PROTEIN; TRANSACTIVATOR PROTEIN; ZNF516 PROTEIN, HUMAN;

BONE DENSITY; DNA-BINDING PROTEINS; EPISTASIS, GENETIC; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HIP; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; RNA-BINDING PROTEINS; TRANS-ACTIVATORS;

EID: 84875316537     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1788     Document Type: Article

References (47)

1. Ray NF, Chan JK, Thamer M, Melton LJ 3rd., Medical expenditures for the treatment of osteoporotic fractures in the United States in 1995: report from the National Osteoporosis Foundation. J Bone Miner Res. 1997; 12 (1): 24-35.
2. Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P, Eisman JA, Fujiwara S, Kroger H, Mellstrom D, Meunier PJ, Melton LJ 3rd, O'Neill T, Pols H, Reeve J, Silman A, Tenenhouse A., Predictive value of BMD for hip and other fractures. J Bone Miner Res. 2005; 20 (7): 1185-94.
3. Cummings SR, Melton LJ., Epidemiology and outcomes of osteoporotic fractures. Lancet. 2002; 359 (9319): 1761-7.
4. Eisman JA., Genetics of osteoporosis. Endocr Rev. 1999; 20 (6): 788-04.
5. Slemenda CW, Christian JC, Williams CJ, Norton JA, Johnston CC Jr., Genetic determinants of bone mass in adult women: a reevaluation of the twin model and the potential importance of gene interaction on heritability estimates. J Bone Miner Res. 1991; 6 (6): 561-7.
6. Nair RP, Duffin KC, Helms C, Ding J, Stuart PE, Goldgar D, Gudjonsson JE, Li Y, Tejasvi T, Feng BJ, Ruether A, Schreiber S, Weichenthal M, Gladman D, Rahman P, Schrodi SJ, Prahalad S, Guthery SL, Fischer J, Liao W, Kwok PY, Menter A, Lathrop GM, Wise CA, Begovich AB, Voorhees JJ, Elder JT, Krueger GG, Bowcock AM, Abecasis GR., Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat Genet. 2009; 41 (2): 199-204.
7. Styrkarsdottir U, Halldorsson BV, Gretarsdottir S, Gudbjartsson DF, Walters GB, Ingvarsson T, Jonsdottir T, Saemundsdottir J, Center JR, Nguyen TV, Bagger Y, Gulcher JR, Eisman JA, Christiansen C, Sigurdsson G, Kong A, Thorsteinsdottir U, Stefansson K., Multiple genetic loci for bone mineral density and fractures. N Engl J Med. 2008; 358 (22): 2355-65.
8. Styrkarsdottir U, Halldorsson BV, Gretarsdottir S, Gudbjartsson DF, Walters GB, Ingvarsson T, Jonsdottir T, Saemundsdottir J, Snorradottir S, Center JR, Nguyen TV, Alexandersen P, Gulcher JR, Eisman JA, Christiansen C, Sigurdsson G, Kong A, Thorsteinsdottir U, Stefansson K., New sequence variants associated with bone mineral density. Nat Genet. 2009; 41 (1): 15-7.
9. Richards JB, Rivadeneira F, Inouye M, Pastinen TM, Soranzo N, Wilson SG, Andrew T, Falchi M, Gwilliam R, Ahmadi KR, Valdes AM, Arp P, Whittaker P, Verlaan DJ, Jhamai M, Kumanduri V, Moorhouse M, van Meurs JB, Hofman A, Pols HA, Hart D, Zhai G, Kato BS, Mullin BH, Zhang F, Deloukas P, Uitterlinden AG, Spector TD., Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study. Lancet. 2008; 371 (9623): 1505-12.
10. Guo Y, Zhang LS, Yang TL, Tian Q, Xiong DH, Pei YF, Deng HW., IL21R and PTH may underlie variation of femoral neck bone mineral density as revealed by a genome-wide association study. J Bone Miner Res. 2010; 25 (5): 1042-8.
11. Guo Y, Tan LJ, Lei SF, Yang TL, Chen XD, Zhang F, Chen Y, Pan F, Yan H, Liu X, Tian Q, Zhang ZX, Zhou Q, Qiu C, Dong SS, Xu XH, Guo YF, Zhu XZ, Liu SL, Wang XL, Li X, Luo Y, Zhang LS, Li M, Wang JT, Wen T, Drees B, Hamilton J, Papasian CJ, Recker RR, Song XP, Cheng J, Deng HW., Genome-wide association study identifies ALDH7A1 as a novel susceptibility gene for osteoporosis. PLoS Genet. 2010; 6 (1): e1000806.
12. Estrada K, Styrkarsdottir U, Evangelou E, Hsu YH, Duncan EL, Ntzani EE, Oei L, Albagha OM, Amin N, Kemp JP, Koller DL, Li G, Liu CT, Minster RL, Moayyeri A, Vandenput L, Willner D, Xiao SM, Yerges-Armstrong LM, Zheng HF, Alonso N, Eriksson J, Kammerer CM, Kaptoge SK, Leo PJ, Thorleifsson G, Wilson SG, Wilson JF, Aalto V, Alen M, Aragaki AK, Aspelund T, Center JR, Dailiana Z, Duggan DJ, Garcia M, Garcia-Giralt N, Giroux S, Hallmans G, Hocking LJ, Husted LB, Jameson KA, Khusainova R, Kim GS, Kooperberg C, Koromila T, Kruk M, Laaksonen M, Lacroix AZ, Lee SH, Leung PC, Lewis JR, Masi L, Mencej-Bedrac S, Nguyen TV, Nogues X, Patel MS, Prezelj J, Rose LM, Scollen S, Siggeirsdottir K, Smith AV, Svensson O, Trompet S, Trummer O, van Schoor NM, Woo J, Zhu K, Balcells S, Brandi ML, Buckley BM, Cheng S, Christiansen C, Cooper C, Dedoussis G, Ford I, Frost M, Goltzman D, González-Macías J, Kähönen M, Karlsson M, Khusnutdinova E, Koh JM, Kollia P, Langdahl BL, Leslie WD, Lips P, Ljunggren Ö, Lorenc RS, Marc J, Mellström D, Obermayer-Pietsch B, Olmos JM, Pettersson-Kymmer U, Reid DM, Riancho JA, Ridker PM, Rousseau F, Slagboom PE, Tang NL, Urreizti R, Van Hul W, Viikari J, Zarrabeitia MT, Aulchenko YS, Castano-Betancourt M, Grundberg E, Herrera L, Ingvarsson T, Johannsdottir H, Kwan T, Li R, Luben R, Medina-Gõmez C, Palsson ST, Reppe S, Rotter JI, Sigurdsson G, van Meurs JB, Verlaan D, Williams FM, Wood AR, Zhou Y, Gautvik KM, Pastinen T, Raychaudhuri S, Cauley JA, Chasman DI, Clark GR, Cummings SR, Danoy P, Dennison EM, Eastell R, Eisman JA, Gudnason V, Hofman A, Jackson RD, Jones G, Jukema JW, Khaw KT, Lehtimäki T, Liu Y, Lorentzon M, McCloskey E, Mitchell BD, Nandakumar K, Nicholson GC, Oostra BA, Peacock M, Pols HA, Prince RL, Raitakari O, Reid IR, Robbins J, Sambrook PN, Sham PC, Shuldiner AR, Tylavsky FA, van Duijn CM, Wareham NJ, Cupples LA, Econs MJ, Evans DM, Harris TB, Kung AW, Psaty BM, Reeve J, Spector TD, Streeten EA, Zillikens MC, Thorsteinsdottir U, Ohlsson C, Karasik D, Richards JB, Brown MA, Stefansson K, Uitterlinden AG, Ralston SH, Ioannidis JP, Kiel DP, Rivadeneira F., Genome-wide meta-analysis identifies 56 bone mineral density loci and reveals 14 loci associated with risk of fracture. Nat Genet. 2012; 44 (5): 491-501.
13. Rivadeneira F, Styrkarsdottir U, Estrada K, Halldorsson BV, Hsu YH, Richards JB, Zillikens MC, Kavvoura FK, Amin N, Aulchenko YS, Cupples LA, Deloukas P, Demissie S, Grundberg E, Hofman A, Kong A, Karasik D, van Meurs JB, Oostra B, Pastinen T, Pols HA, Sigurdsson G, Soranzo N, Thorleifsson G, Thorsteinsdottir U, Williams FM, Wilson SG, Zhou Y, Ralston SH, van Duijn CM, Spector T, Kiel DP, Stefansson K, Ioannidis JP, Uitterlinden AG., Twenty bone-mineral-density loci identified by large-scale meta-analysis of genome-wide association studies. Nat Genet. 2009; 41 (11): 1199-206.
14. Cordell HJ., Detecting gene-gene interactions that underlie human diseases. Nat Rev Genet. 2009; 10 (6): 392-404.
15. Murcray CE, Lewinger JP, Gauderman WJ., Gene-environment interaction in genome-wide association studies. Am J Epidemiol. 2009; 169 (2): 219-26.
16. Marchini J, Donnelly P, Cardon LR., Genome-wide strategies for detecting multiple loci that influence complex diseases. Nat Genet. 2005; 37 (4): 413-7.
17. Evans DM, Marchini J, Morris AP, Cardon LR., Two-stage two-locus models in genome-wide association. PLoS Genet. 2006; 2 (9): e157.
18. Deng HW, Mahaney MC, Williams JT, Li J, Conway T, Davies KM, Li JL, Deng H, Recker RR., Relevance of the genes for bone mass variation to susceptibility to osteoporotic fractures and its implications to gene search for complex human diseases. Genet Epidemiol. 2002; 22 (1): 12-25.
19. Glastre C, Braillon P, David L, Cochat P, Meunier PJ, Delmas PD., Measurement of bone mineral content of the lumbar spine by dual energy x-ray absorptiometry in normal children: correlations with growth parameters. J Clin Endocrinol Metab. 1990; 70 (5): 1330-3.
20. Cupples LA, Arruda HT, Benjamin EJ, D'Agostino RB Sr, Demissie S, DeStefano AL, Dupuis J, Falls KM, Fox CS, Gottlieb DJ, Govindaraju DR, Guo CY, Heard-Costa NL, Hwang SJ, Kathiresan S, Kiel DP, Laramie JM, Larson MG, Levy D, Liu CY, Lunetta KL, Mailman MD, Manning AK, Meigs JB, Murabito JM, Newton-Cheh C, O'Connor GT, O'Donnell CJ, Pandey M, Seshadri S, Vasan RS, Wang ZY, Wilk JB, Wolf PA, Yang Q, Atwood LD., The Framingham Heart Study 100K SNP genome-wide association study resource: overview of 17 phenotype working group reports. BMC Med Genet. 2007; 8 (Suppl 1): S1.
21. Hannan MT, Felson DT, Anderson JJ., Bone mineral density in elderly men and women: results from the Framingham osteoporosis study. J Bone Miner Res. 1992; 7 (5): 547-53.
22. Design of the Women's Health Initiative clinical trial and observational study. The Women's Health Initiative Study Group. Control Clin Trials. 1998; 19 (1): 61-109.
23. Langer RD, White E, Lewis CE, Kotchen JM, Hendrix SL, Trevisan M., The Women's Health Initiative Observational Study: baseline characteristics of participants and reliability of baseline measures. Ann Epidemiol. 2003; 13 (9 Suppl): S107-21.
24. Liu YJ, Liu XG, Wang L, Dina C, Yan H, Liu JF, Levy S, Papasian CJ, Drees BM, Hamilton JJ, Meyre D, Delplanque J, Pei YF, Zhang L, Recker RR, Froguel P, Deng HW., Genome-wide association scans identified CTNNBL1 as a novel gene for obesity. Hum Mol Genet. 2008; 17 (12): 1803-13.
25. Marchini J, Howie B, Myers S, McVean G, Donnelly P., A new multipoint method for genome-wide association studies by imputation of genotypes. Nat Genet. 2007; 39 (7): 906-13.
26. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D., Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet. 2006; 38 (8): 904-9.
27. Hsu YH, Zillikens MC, Wilson SG, Farber CR, Demissie S, Soranzo N, Bianchi EN, Grundberg E, Liang L, Richards JB, Estrada K, Zhou Y, van Nas A, Moffatt MF, Zhai G, Hofman A, van Meurs JB, Pols HA, Price RI, Nilsson O, Pastinen T, Cupples LA, Lusis AJ, Schadt EE, Ferrari S, Uitterlinden AG, Rivadeneira F, Spector TD, Karasik D, Kiel DP., An integration of genome-wide association study and gene expression profiling to prioritize the discovery of novel susceptibility Loci for osteoporosis-related traits. PLoS Genet. 2010; 6 (6): e1000977.
28. Kooperberg C, Leblanc M., Increasing the power of identifying gene x gene interactions in genome-wide association studies. Genet Epidemiol. 2008; 32 (3): 255-63.
29. 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 (3): 559-75.
30. Perez A, Ulla M, Garcia B, Lavezzo M, Elias E, Binci M, Rivoira M, Centeno V, Alisio A, de Talamoni NT., Genotypes and clinical aspects associated with bone mineral density in Argentine postmenopausal women. J Bone Miner Metab. 2008; 26 (4): 358-65.
31. Colin EM, Uitterlinden AG, Meurs JB, Bergink AP, van de Klift M, Fang Y, Arp PP, Hofman A, van Leeuwen JP, Pols HA., Interaction between vitamin D receptor genotype and estrogen receptor alpha genotype influences vertebral fracture risk. J Clin Endocrinol Metab. 2003; 88 (8): 3777-84.
32. Bustamante M, Nogues X, Enjuanes A, Elosua R, Garcia-Giralt N, Perez-Edo L, Caceres E, Carreras R, Mellibovsky L, Balcells S, Diez-Perez A, Grinberg D., COL1A1, ESR1, VDR and TGFB1 polymorphisms and haplotypes in relation to BMD in Spanish postmenopausal women. Osteoporos Int. 2007; 18 (2): 235-43.
33. Xiong DH, Shen H, Zhao LJ, Xiao P, Yang TL, Guo Y, Wang W, Guo YF, Liu YJ, Recker RR, Deng HW., Robust and comprehensive analysis of 20 osteoporosis candidate genes by very high-density single-nucleotide polymorphism screen among 405 white nuclear families identified significant association and gene-gene interaction. J Bone Miner Res. 2006; 21 (11): 1678-95.
34. Choi JY, Shin A, Park SK, Chung HW, Cho SI, Shin CS, Kim H, Lee KM, Lee KH, Kang C, Cho DY, Kang D., Genetic polymorphisms of OPG, RANK, and ESR1 and bone mineral density in Korean postmenopausal women. Calcif Tissue Int. 2005; 77 (3): 152-9.
35. Kim JG, Kim JH, Kim JY, Ku SY, Jee BC, Suh CS, Kim SH, Choi YM., Association between osteoprotegerin (OPG), receptor activator of nuclear factor-kappaB (RANK), and RANK ligand (RANKL) gene polymorphisms and circulating OPG, soluble RANKL levels, and bone mineral density in Korean postmenopausal women. Menopause. 2007; 14 (5): 913-8.
36. Kumar J, Swanberg M, McGuigan F, Callreus M, Gerdhem P, Akesson K., LRP4 association to bone properties and fracture and interaction with genes in the Wnt- and BMP signaling pathways. Bone. 2011; 49 (3): 343-8.
37. Xing L, He GP, Chen YM, Su YX., Interaction of interleukin-6 and estrogen receptor gene polymorphisms on bone mass accrual in Chinese adolescent girls. J Bone Miner Metab. 2008; 26 (5): 493-8.
38. Rivadeneira F, van Meurs JB, Kant J, Zillikens MC, Stolk L, Beck TJ, Arp P, Schuit SC, Hofman A, Houwing-Duistermaat JJ, van Duijn CM, van Leeuwen JP, Pols HA, Uitterlinden AG., Estrogen receptor beta (ESR2) polymorphisms in interaction with estrogen receptor alpha (ESR1) and insulin-like growth factor I (IGF1) variants influence the risk of fracture in postmenopausal women. J Bone Miner Res. 2006; 21 (9): 1443-56.
39. Pineda B, Tarin JJ, Hermenegildo C, Laporta P, Cano A, Garcia-Perez MA., Gene-gene interaction between CD40 and CD40L reduces bone mineral density and increases osteoporosis risk in women. Osteoporos Int. 2011; 22 (5): 1451-8.
40. Zupan J, Mencej-Bedrac S, Jurkovic-Mlakar S, Prezelj J, Marc J., Gene-gene interactions in RANK/RANKL/OPG system influence bone mineral density in postmenopausal women. J Steroid Biochem Mol Biol. 2010; 118 (1-2): 102-6.
41. Hsu YH, Niu T, Terwedow HA, Xu X, Feng Y, Li Z, Brain JD, Rosen CJ, Laird N., Variation in genes involved in the RANKL/RANK/OPG bone remodeling pathway are associated with bone mineral density at different skeletal sites in men. Hum Genet. 2006; 118 (5): 568-77.
42. Penkov D, Ni R, Else C, Pinol-Roma S, Ramirez F, Tanaka S., Cloning of a human gene closely related to the genes coding for the c-myc single-strand binding proteins. Gene. 2000; 243 (1-2): 27-36.
43. Fritz D, Stefanovic B., RNA-binding protein RBMS3 is expressed in activated hepatic stellate cells and liver fibrosis and increases expression of transcription factor Prx1. J Mol Biol. 2007; 371 (3): 585-95.
44. Kiel DP, Demissie S, Dupuis J, Lunetta KL, Murabito JM, Karasik D., Genome-wide association with bone mass and geometry in the Framingham Heart Study. BMC Med Genet. 2007; 8 Suppl 1: S14.
45. Zuk O, Hechter E, Sunyaev SR, Lander ES., The mystery of missing heritability: Genetic interactions create phantom heritability. Proc Natl Acad Sci U S A. 2012; 109 (4): 1193-8.
46. Duncan EL, Danoy P, Kemp JP, Leo PJ, McCloskey E, Nicholson GC, Eastell R, Prince RL, Eisman JA, Jones G, Sambrook PN, Reid IR, Dennison EM, Wark J, Richards JB, Uitterlinden AG, Spector TD, Esapa C, Cox RD, Brown SD, Thakker RV, Addison KA, Bradbury LA, Center JR, Cooper C, Cremin C, Estrada K, Felsenberg D, Gluer CC, Hadler J, Henry MJ, Hofman A, Kotowicz MA, Makovey J, Nguyen SC, Nguyen TV, Pasco JA, Pryce K, Reid DM, Rivadeneira F, Roux C, Stefansson K, Styrkarsdottir U, Thorleifsson G, Tichawangana R, Evans DM, Brown MA., Genome-wide association study using extreme truncate selection identifies novel genes affecting bone mineral density and fracture risk. PLoS Genet. 2011; 7 (4): e1001372.
47. Kung AW, Xiao SM, Cherny S, Li GH, Gao Y, Tso G, Lau KS, Luk KD, Liu JM, Cui B, Zhang MJ, Zhang ZL, He JW, Yue H, Xia WB, Luo LM, He SL, Kiel DP, Karasik D, Hsu YH, Cupples LA, Demissie S, Styrkarsdottir U, Halldorsson BV, Sigurdsson G, Thorsteinsdottir U, Stefansson K, Richards JB, Zhai G, Soranzo N, Valdes A, Spector TD, Sham PC., Association of JAG1 with bone mineral density and osteoporotic fractures: a genome-wide association study and follow-up replication studies. Am J Hum Genet. 2010; 86 (2): 229-39.