Genotypes and haplotypes of the estrogen receptor genes, but not the retinoblastoma-interacting zinc finger protein 1 gene, are associated with osteoporosis

Calcified Tissue International

Volumn 87, Issue 1, 2010, Pages 25-35

  Harslof T ^a   Husted, L B ^a   Carstens, M ^a   Stenkjaer L ^a   Langdahl, B L ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Osteoporosis: Fractures; Osteoporosis: Genetic association; Osteoporosis: Genetic polymorphism; Osteoporosis: Pathogenesis; Phytoestrogens; Steroid hormones: Estrogens

Indexed keywords

CYSTEINE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLYCINE; RETINOBLASTOMA INTERACTING ZINC FINGER PROTEIN 1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA, HUMAN; RETINOBLASTOMA PROTEIN;

ADULT; AGED; ALLELE; ARTICLE; BONE DENSITY; CONTROLLED STUDY; FEMALE; FRAGILITY FRACTURE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; LUMBAR SPINE; MAJOR CLINICAL STUDY; MALE; OSTEOPOROSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; RECEPTOR GENE; RISK REDUCTION; SEX DIFFERENCE; VERTEBRA FRACTURE; CASE CONTROL STUDY; COMPLICATION; FRACTURE; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; LUMBAR VERTEBRA; MIDDLE AGED; POSTMENOPAUSE OSTEOPOROSIS; RISK;

ADULT; AGED; ALLELES; BONE DENSITY; CASE-CONTROL STUDIES; ESTROGEN RECEPTOR ALPHA; FEMALE; FRACTURES, BONE; GENOTYPE; HAPLOTYPES; HUMANS; LUMBAR VERTEBRAE; MALE; MIDDLE AGED; OSTEOPOROSIS; OSTEOPOROSIS, POSTMENOPAUSAL; POLYMORPHISM, GENETIC; RECEPTORS, ESTROGEN; RETINOBLASTOMA PROTEIN; RISK; ZINC FINGERS;

EID: 77953869175     PISSN: 0171967X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00223-010-9375-y     Document Type: Article

References (50)

1. EF Eriksen SF Hodgson R Eastell SL Cedel WM O'Fallon BL Riggs 1990 Cancellous bone remodeling in type I (postmenopausal) osteoporosis: quantitative assessment of rates of formation, resorption, and bone loss at tissue and cellular levels J Bone Miner Res 5 311 319 10.1002/jbmr.5650050402 1:STN:280:DyaK3c3mtFGhtQ%3D%3D 2343771
2. JA Kanis FA Pitt 1992 Epidemiology of osteoporosis Bone 13 suppl 1 S7 S15 10.1016/S8756-3282(09)80004-5 1581122
3. SR Cummings WS Browner D Bauer K Stone K Ensrud S Jamal B Ettinger 1998 Endogenous hormones and the risk of hip and vertebral fractures among older women. Study of Osteoporotic Fractures Research Group N Engl J Med 339 733 738 10.1056/NEJM199809103391104 1:CAS:528:DyaK1cXmt1Khurg%3D 9731089 (Pubitemid 28417356)
4. B Ettinger A Pressman P Sklarin DC Bauer JA Cauley SR Cummings 1998 Associations between low levels of serum estradiol, bone density, and fractures among elderly women: The study of osteoporotic fractures J Clin Endocrinol Metab 83 2239 2243 10.1210/jc.83.7.2239 1:CAS:528:DyaK1cXksVSjtb4%3D 9661589 (Pubitemid 28503008)
5. K Stone DC Bauer DM Black P Sklarin KE Ensrud SR Cummings 1998 Hormonal predictors of bone loss in elderly women: a prospective study. The Study of Osteoporotic Fractures Research Group J Bone Miner Res 13 1167 1174 10.1359/jbmr.1998.13.7.1167 1:CAS:528:DyaK1cXks1arsrs%3D 9661081 (Pubitemid 28311785)
6. D Mellstrom L Vandenput H Mallmin AH Holmberg M Lorentzon A Oden H Johansson ES Orwoll F Labrie MK Karlsson O Ljunggren C Ohlsson 2008 Older men with low serum estradiol and high serum SHBG have an increased risk of fractures J Bone Miner Res 23 1552 1560 10.1359/jbmr.080518 18518773
7. NK Shevde JW Pike 1996 Estrogen modulates the recruitment of myelopoietic cell progenitors in rat through a stromal cell-independent mechanism involving apoptosis Blood 87 2683 2692 1:CAS:528:DyaK28XhvFeltrg%3D 8639884
8. H Mano T Yuasa T Kameda K Miyazawa Y Nakamaru M Shiokawa Y Mori T Yamada K Miyata H Shindo H Azuma Y Hakeda M Kumegawa 1996 Mammalian mature osteoclasts as estrogen target cells Biochem Biophys Res Commun 223 637 642 10.1006/bbrc.1996.0947 1:CAS:528:DyaK28XjvFCrur4%3D 8687448 (Pubitemid 26246125)
9. M Ponglikitmongkol S Green P Chambon 1988 Genomic organization of the human oestrogen receptor gene EMBO J 7 3385 3388 1:CAS:528:DyaL1MXitVCk 3145193
10. E Enmark M Pelto-Huikko K Grandien S Lagercrantz J Lagercrantz G Fried M Nordenskjold JA Gustafsson 1997 Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern J Clin Endocrinol Metab 82 4258 4265 10.1210/jc.82.12.4258 1:CAS:528:DyaK2sXnvFyrtL0%3D 9398750
11. T Carling KC Kim XH Yang J Gu XK Zhang S Huang 2004 A histone methyltransferase is required for maximal response to female sex hormones Mol Cell Biol 24 7032 7042 10.1128/MCB.24.16.7032-7042.2004 1:CAS:528: DC%2BD2cXmtlOjtro%3D 15282304 (Pubitemid 39014431)
12. MK Lindberg S Moverare S Skrtic H Gao K hlman-Wright JA Gustafsson C Ohlsson 2003 Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice Mol Endocrinol 17 203 208 10.1210/me.2002-0206 1:CAS:528:DC%2BD3sXhtFantbw%3D 12554748 (Pubitemid 36187395)
13. MM Liu C Albanese CM Anderson K Hilty P Webb RM Uht RH Price Jr RG Pestell PJ Kushner 2002 Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression J Biol Chem 277 24353 24360 10.1074/jbc.M201829200 1:CAS:528:DC%2BD38XltlOhsLk%3D 11986316 (Pubitemid 34951956)
14. CW Slemenda JC Christian CJ Williams JA Norton CC Johnston Jr 1991 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 6 561 567 10.1002/jbmr.5650060606 1:STN:280: DyaK3MzmtFyrtA%3D%3D 1887818
15. P Kannus M Palvanen J Kaprio J Parkkari M Koskenvuo 1999 Genetic factors and osteoporotic fractures in elderly people: prospective 25 year follow up of a nationwide cohort of elderly Finnish twins BMJ 319 1334 1337 1:STN:280:DC%2BD3c%2FjsFamsw%3D%3D 10567136
16. JB Richards F Rivadeneira M Inouye TM Pastinen N Soranzo SG Wilson T Andrew M Falchi R Gwilliam KR Ahmadi AM Valdes P Arp P Whittaker DJ Verlaan M Jhamai V Kumanduri M Moorhouse JB van Meurs A Hofman HA Pols D Hart G Zhai BS Kato BH Mullin F Zhang P Deloukas AG Uitterlinden TD Spector 2008 Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study Lancet 371 1505 1512 10.1016/S0140-6736(08)60599-1 1:CAS:528: DC%2BD1cXlsFGisr0%3D 18455228
17. U Styrkarsdottir BV Halldorsson S Gretarsdottir DF Gudbjartsson GB Walters T Ingvarsson T Jonsdottir J Saemundsdottir JR Center TV Nguyen Y Bagger JR Gulcher JA Eisman C Christiansen G Sigurdsson A Kong U Thorsteinsdottir K Stefansson 2008 Multiple genetic loci for bone mineral density and fractures N Engl J Med 358 2355 2365 10.1056/NEJMoa0801197 1:CAS:528:DC%2BD1cXmsVKgtb4%3D 18445777 (Pubitemid 351749159)
18. BL Langdahl SH Ralston SF Grant EF Eriksen 1998 An Sp1 binding site polymorphism in the COLIA1 gene predicts osteoporotic fractures in both men and women J Bone Miner Res 13 1384 1389 10.1359/jbmr.1998.13.9.1384 1:CAS:528:DyaK1cXmtVeqs7c%3D 9738510 (Pubitemid 28418904)
19. AG Uitterlinden HA Pols H Burger Q Huang PL van Daele CM Van Duijn A Hofman JC Birkenhager JP van Leeuwen 1996 A large-scale population-based study of the association of vitamin D receptor gene polymorphisms with bone mineral density J Bone Miner Res 11 1241 1248 10.1002/jbmr.5650110908 1:CAS:528:DyaK28Xls1ChtLw%3D 8864898
20. BL Langdahl JY Knudsen HK Jensen N Gregersen EF Eriksen 1997 A sequence variation: 713-8delC in the transforming growth factor-beta 1 gene has higher prevalence in osteoporotic women than in normal women and is associated with very low bone mass in osteoporotic women and increased bone turnover in both osteoporotic and normal women Bone 20 289 294 10.1016/S8756-3282(96)00363-8 1:CAS:528:DyaK2sXit12qsb0%3D 9071481 (Pubitemid 27141842)
21. SL Ferrari S Deutsch U Choudhury T Chevalley JP Bonjour ET Dermitzakis R Rizzoli SE Antonarakis 2004 Polymorphisms in the low-density lipoprotein receptor-related protein 5 (LRP5) gene are associated with variation in vertebral bone mass, vertebral bone size, and stature in whites Am J Hum Genet 74 866 875 10.1086/420771 1:CAS:528:DC%2BD2cXjvVeis7k%3D 15077203 (Pubitemid 38568961)
22. F Rivadeneira U Styrkarsdottir K Estrada BV Halldorsson YH Hsu JB Richards MC Zillikens FK Kavvoura N Amin YS Aulchenko LA Cupples P Deloukas S Demissie E Grundberg A Hofman A Kong D Karasik JB van Meurs B Oostra T Pastinen HA Pols G Sigurdsson N Soranzo G Thorleifsson U Thorsteinsdottir FM Williams SG Wilson Y Zhou SH Ralston CM Van Duijn T Spector DP Kiel K Stefansson JP Ioannidis AG Uitterlinden 2009 Twenty bone-mineral-density loci identified by large-scale meta-analysis of genome-wide association studies Nat Genet 41 1199 1206 10.1038/ng.446 1:CAS:528:DC%2BD1MXht1Wgsb7L 19801982
23. BL Langdahl E Lokke M Carstens LL Stenkjaer EF Eriksen 2000 A TA repeat polymorphism in the estrogen receptor gene is associated with osteoporotic fractures but polymorphisms in the first exon and intron are not J Bone Miner Res 15 2222 2230 10.1359/jbmr.2000.15.11.2222 1:CAS:528:DC%2BD3cXnvVKltLo%3D 11092403
24. OM Albagha FE McGuigan DM Reid SH Ralston 2001 Estrogen receptor alpha gene polymorphisms and bone mineral density: haplotype analysis in women from the United Kingdom J Bone Miner Res 16 128 134 10.1359/jbmr.2001.16.1.128 1:CAS:528:DC%2BD3MXitlChug%3D%3D 11149476
25. JP Ioannidis I Stavrou TA Trikalinos C Zois ML Brandi L Gennari O Albagha SH Ralston A Tsatsoulis 2002 Association of polymorphisms of the estrogen receptor alpha gene with bone mineral density and fracture risk in women: a meta-analysis J Bone Miner Res 17 2048 2060 10.1359/jbmr.2002.17.11.2048 1:CAS:528:DC%2BD38Xoslems7Y%3D 12412813
26. van Meurs JB, Schuit SC, Weel AE, van der KM, Bergink AP, Arp PP, Colin EM, Fang Y, Hofman A, Van Duijn CM, van Leeuwen JP, Pols HA, Uitterlinden AG (2003) Association of 5' estrogen receptor alpha gene polymorphisms with bone mineral density, vertebral bone area and fracture risk. Hum Mol Genet 12:1745-1754
27. JP Ioannidis SH Ralston ST Bennett ML Brandi D Grinberg FB Karassa B Langdahl JB van Meurs L Mosekilde S Scollen OM Albagha M Bustamante AH Carey AM Dunning A Enjuanes JP van Leeuwen C Mavilia L Masi FE McGuigan X Nogues HA Pols DM Reid SC Schuit RE Sherlock AG Uitterlinden 2004 Differential genetic effects of ESR1 gene polymorphisms on osteoporosis outcomes JAMA 292 2105 2114 10.1001/jama.292.17.2105 1:CAS:528:DC%2BD2cXpsVeku7g%3D 15523071 (Pubitemid 39435101)
28. AM Shearman D Karasik KM Gruenthal S Demissie LA Cupples DE Housman DP Kiel 2004 Estrogen receptor beta polymorphisms are associated with bone mass in women and men: the Framingham Study J Bone Miner Res 19 773 781 10.1359/JBMR.0301258 1:CAS:528:DC%2BD2cXktFGks78%3D 15068501 (Pubitemid 41094389)
29. F Rivadeneira JB van Meurs J Kant MC Zillikens L Stolk TJ Beck P Arp SC Schuit A Hofman JJ Houwing-Duistermaat CM Van Duijn JP van Leeuwen HA Pols AG Uitterlinden 2006 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 21 1443 1456 10.1359/jbmr.060605 1:CAS:528:DC%2BD28XhtVSrtrrI 16939403 (Pubitemid 44300051)
30. B Arko J Prezelj R Komel A Kocijancic J Marc 2002 No major effect of estrogen receptor beta gene RsaI polymorphism on bone mineral density and response to alendronate therapy in postmenopausal osteoporosis J Steroid Biochem Mol Biol 81 147 152 10.1016/S0960-0760(02)00061-4 1:CAS:528: DC%2BD38Xls1WhsrY%3D 12137804 (Pubitemid 34876406)
31. S Ichikawa DL Koller M Peacock ML Johnson D Lai SL Hui CC Johnston TM Foroud MJ Econs 2005 Polymorphisms in the estrogen receptor beta (ESR2) gene are associated with bone mineral density in Caucasian men and women J Clin Endocrinol Metab 90 5921 5927 10.1210/jc.2004-2253 1:CAS:528:DC%2BD2MXht1alt7jJ 16118344 (Pubitemid 41606506)
32. Z Efstathiadou G Koukoulis N Stakias A Challa E Zintzaras A Tsatsoulis 2006 Correlation of estrogen receptor beta gene polymorphisms with spinal bone mineral density in peri-and post-menopausal Greek women Maturitas 53 380 385 10.1016/j.maturitas.2005.07.005 1:CAS:528:DC%2BD28XitVaqsbY%3D 16125346
33. E Grundberg T Carling H Brandstrom S Huang EL Ribom O Ljunggren H Mallmin A Kindmark 2004 A deletion polymorphism in the RIZ gene, a female sex steroid hormone receptor coactivator, exhibits decreased response to estrogen in vitro and associates with low bone mineral density in young Swedish women J Clin Endocrinol Metab 89 6173 6178 10.1210/jc.2004-0403 1:CAS:528: DC%2BD2cXhtFSit7%2FF 15579774 (Pubitemid 39628430)
34. EV McCloskey TD Spector KS Eyres ED Fern N O'Rourke S Vasikaran JA Kanis 1993 The assessment of vertebral deformity: a method for use in population studies and clinical trials Osteoporos Int 3 138 147 10.1007/BF01623275 1:STN:280:DyaK3s3ksVGgsA%3D%3D 8481590
35. HK Genant S Grampp CC Gluer KG Faulkner M Jergas K Engelke S Hagiwara C Van Kuijk 1994 Universal standardization for dual X-ray absorptiometry: patient and phantom cross-calibration results J Bone Miner Res 9 1503 1514 10.1002/jbmr.5650091002 1:STN:280:DyaK2M7hslGmsA%3D%3D 7817795
36. LM Kunkel KD Smith SH Boyer DS Borgaonkar SS Wachtel OJ Miller WR Breg HW Jones Jr JM Rary 1977 Analysis of human Y-chromosome-specific reiterated DNA in chromosome variants Proc Natl Acad Sci USA 74 1245 1249 10.1073/pnas.74.3.1245 1:CAS:528:DyaE2sXhsFeitbY%3D 265567
37. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005;21:263-265
38. C Herold T Becker 2009 Genetic association analysis with FAMHAP: a major program update Bioinformatics 25 134 136 10.1093/bioinformatics/btn581 1:CAS:528:DC%2BD1MXmvFWg 19015131
39. Silvestri S, Thomsen AB, Gozzini A, Bagger Y, Christiansen C, Brandi ML (2006) Estrogen receptor alpha and beta polymorphisms: is there an association with bone mineral density, plasma lipids, and response to postmenopausal hormone therapy? Menopause 13:451-461
40. JT Wang Y Guo TL Yang XH Xu SS Dong M Li TQ Li Y Chen HW Deng 2008 Polymorphisms in the estrogen receptor genes are associated with hip fractures in Chinese Bone 43 910 914 10.1016/j.bone.2008.07.001 1:CAS:528: DC%2BD1cXht1ejtLnF 18678289
41. JP Ioannidis MY Ng PC Sham E Zintzaras CM Lewis HW Deng MJ Econs D Karasik M Devoto CM Kammerer T Spector T Andrew LA Cupples EL Duncan T Foroud DP Kiel D Koller B Langdahl BD Mitchell M Peacock R Recker H Shen K Sol-Church LD Spotila AG Uitterlinden SG Wilson AW Kung SH Ralston 2007 Meta-analysis of genome-wide scans provides evidence for sex-and site-specific regulation of bone mass J Bone Miner Res 22 173 183 10.1359/jbmr.060806 1:CAS:528: DC%2BD2sXhvFCgsrg%3D 17228994 (Pubitemid 46167787)
42. C Meier TV Nguyen DJ Handelsman C Schindler MM Kushnir AL Rockwood AW Meikle JR Center JA Eisman MJ Seibel 2008 Endogenous sex hormones and incident fracture risk in older men: the Dubbo Osteoporosis Epidemiology Study Arch Intern Med 168 47 54 10.1001/archinternmed.2007.2 1:CAS:528:DC%2BD1cXhslSntb0%3D 18195195
43. E Grundberg K Akesson A Kindmark P Gerdhem A Holmberg D Mellstrom O Ljunggren E Orwoll H Mallmin C Ohlsson H Brandstrom 2007 The impact of estradiol on bone mineral density is modulated by the specific estrogen receptor-alpha cofactor retinoblastoma-interacting zinc finger protein-1 insertion/deletion polymorphism J Clin Endocrinol Metab 92 2300 2306 10.1210/jc.2006-1572 1:CAS:528:DC%2BD2sXmslOgsL4%3D 17356055 (Pubitemid 46997137)
44. Z Kaminsky SC Wang A Petronis 2006 Complex disease, gender and epigenetics Ann Med 38 530 544 10.1080/07853890600989211 1:CAS:528: DC%2BD2sXitV2mtLY%3D 17438668 (Pubitemid 46292018)
45. OM Albagha U Pettersson A Stewart FE McGuigan HM MacDonald DM Reid SH Ralston 2005 Association of oestrogen receptor alpha gene polymorphisms with postmenopausal bone loss, bone mass, and quantitative ultrasound properties of bone J Med Genet 42 240 246 10.1136/jmg.2004.023895 1:CAS:528: DC%2BD2MXjtVertr4%3D 15744038 (Pubitemid 40380305)
46. FJ Moron N Mendoza F Vazquez E Molero F Quereda A Salinas J Fontes T Martinez-Astorquiza R Sanchez-Borrego A Ruiz 2006 Multilocus analysis of estrogen-related genes in Spanish postmenopausal women suggests an interactive role of ESR1, ESR2 and NRIP1 genes in the pathogenesis of osteoporosis Bone 39 213 221 10.1016/j.bone.2005.12.079 1:CAS:528:DC%2BD28Xls1ejtrw%3D 16530497 (Pubitemid 43853079)
47. Massart F, Marini F, Bianchi G, Minisola S, Luisetto G, Pirazzoli A, Salvi S, Micheli D, Masi L, Brandi ML (2009) Age-specific effects of estrogen receptors' polymorphisms on the bone traits in healthy fertile women: the BONTURNO study. Reprod Biol Endocrinol 7:32
48. JK Scariano SG Simplicio GD Montoya PJ Garry RN Baumgartner 2004 Estrogen receptor beta dinucleotide (CA) repeat polymorphism is significantly associated with bone mineral density in postmenopausal women Calcif Tissue Int 74 501 508 10.1007/s00223-003-0170-x 1:CAS:528:DC%2BD2cXks1Kmsbk%3D 15354857 (Pubitemid 38780285)
49. L Geng Z Yao H Yang J Luo L Han Q Lu 2007 Association of CA repeat polymorphism in estrogen receptor beta gene with postmenopausal osteoporosis in Chinese J Genet Genomics 34 868 876 10.1016/S1673-8527(07)60098-8 1:CAS:528:DC%2BD2sXht1alu7nM 17945165 (Pubitemid 47562330)
50. L Stolk JB van Meurs PP Arp A Hofman HA Pols AG Uitterlinden 2008 The RIZ Pro704 insertion-deletion polymorphism, bone mineral density and fracture risk: the Rotterdam study Bone 42 286 293 10.1016/j.bone.2007.10.008 1:CAS:528:DC%2BD1cXls1egsg%3D%3D 18037365