Polymorphisms of the peroxisome proliferator-activated receptor γ (PPARγ) gene are associated with osteoporosis

Osteoporosis International

Volumn 22, Issue 10, 2011, Pages 2655-2666

  Harslof T ^a   Tofteng, C L ^b   Husted, L B ^a   Nyegaard, M ^a,c   Borglum A ^a,c   Carstens, M ^a   Stenkjaer L ^a   Brixen, K ^d   Eiken, P ^e   Jensen, J E B ^b   Mosekilde, L ^a   Rejnmark, L ^a   Langdahl, B L ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b HVIDOVRE HOSPITAL   (Denmark)

^c AARHUS UNIVERSITY   (Denmark)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

^e HILLERØD HOSPITAL   (Denmark)

Author keywords

Fractures; Gene environment interaction; Genetics; Osteoporosis

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ADULT; ALLELE; ARTICLE; BODY WEIGHT; BONE DENSITY; COHORT ANALYSIS; CONTROLLED STUDY; DENMARK; DIET; ENVIRONMENTAL FACTOR; FEMALE; FRACTURE; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; HAPLOTYPE; HETEROZYGOTE; HIP; HORMONAL THERAPY; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MENOPAUSE; OSTEOPOROSIS; POPULATION BASED CASE CONTROL STUDY; PRIORITY JOURNAL; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; VERTEBRA FRACTURE;

ADULT; AGED; BODY WEIGHT; BONE DENSITY; CASE-CONTROL STUDIES; DIET; FEMALE; HAPLOTYPES; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; OSTEOPOROSIS; OSTEOPOROTIC FRACTURES; POLYMORPHISM, SINGLE NUCLEOTIDE; PPAR GAMMA; RISK FACTORS; SPINAL FRACTURES;

EID: 80755167696     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-010-1491-z     Document Type: Article

References (45)

1. Pocock NA, Eisman JA, Yeates MG, Sambrook PN, Eberl S (1986) Physical fitness is a major determinant of femoral neck and lumbar spine bone mineral density. J Clin Invest 78:618-621
2. Hermann AP, Brot C, Gram J, Kolthoff N, Mosekilde L (2000) Premenopausal smoking and bone density in 2015 perimenopausal women. J Bone Miner Res 15:780-787
3. Huuskonen J, Vaisanen SB, Kroger H, Jurvelin C, Bouchard C, Alhava E, Rauramaa R (2000) Determinants of bone mineral density in middle aged men: a population-based study. Osteoporos Int 11:702-708
4. Slemenda CW, Christian JC, Williams CJ, Norton JA, Johnston CC 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
5. Hunter D, De Lange M, Snieder H, MacGregor AJ, Swaminathan R, Thakker RV, Spector TD (2001) Genetic contribution to bone metabolism, calcium excretion, and vitamin D and parathyroid hormone regulation. J Bone Miner Res 16:371-378
6. 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 (2008) Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study. Lancet 371:1505-1512
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 (2008) Multiple genetic loci for bone mineral density and fractures. N Engl J Med 358:2355-2365
8. Ali AA, Weinstein RS, Stewart SA, Parfitt AM, Manolagas SC, Jilka RL (2005) Rosiglitazone causes bone loss in mice by suppressing osteoblast differentiation and bone formation. Endocrinology 146:1226-1235
9. Fajas L, Fruchart JC, Auwerx J (1998) PPARgamma3 mRNA: a distinct PPARgamma mRNA subtype transcribed from an independent promoter. FEBS Lett 438:55-60
10. Fajas L, Auboeuf D, Raspe E, Schoonjans K, Lefebvre AM, Saladin R, Najib J, Laville M, Fruchart JC, Deeb S, Vidal-Puig A, Flier J, Briggs MR, Staels B, Vidal H, Auwerx J (1997) The organization, promoter analysis, and expression of the human PPARgamma gene. J Biol Chem 272:18779-18789
11. Tontonoz P, Hu E, Graves RA, Budavari AI, Spiegelman BM (1994) mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev 8:1224-1234
12. Kliewer SA, Sundseth SS, Jones SA, Brown PJ, Wisely GB, Koble CS, Devchand P, Wahli W, Willson TM, Lenhard JM, Lehmann JM (1997) Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proc Natl Acad Sci USA 94:4318-4323
13. Forman BM, Tontonoz P, Chen J, Brun RP, Spiegelman BM, Evans RM (1995) 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell 83:803-812
14. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA (1995) An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem 270:12953-12956
15. Meunier P, Aaron J, Edouard C, Vignon G (1971) Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80:147-154
16. Rzonca SO, Suva LJ, Gaddy D, Montague DC, Lecka-Czernik B (2004) Bone is a target for the antidiabetic compound rosiglitazone. Endocrinology 145(1):401
17. Soroceanu MA, Miao D, Bai XY, Su H, Goltzman D, Karaplis AC (2004) Rosiglitazone impacts negatively on bone by promoting osteoblast/osteocyte apoptosis. J Endocrinol 183(1):203-216
18. Ogawa S, Urano T, Hosoi T, Miyao M, Hoshino S, Fujita M, Shiraki M, Orimo H, Ouchi Y, Inoue S (1999) Association of bone mineral density with a polymorphism of the peroxisome proliferator-activated receptor gamma gene: PPARgamma expression in osteoblasts. Biochem Biophys Res Commun 260:122-126
19. Kiel DP, Ferrari S, Cupples LA, Karasik D, Dupuis J, Rosen CJ, Imamovic A, Demissie S (2005) Polymorphisms in the PPARg gene influence bone density in humans. J Bone Miner Res 20:S234 (Ref Type: Abstract)
20. Mosekilde L, Hermann AP, Beck-Nielsen H, Charles P, Nielsen SP, Sorensen OH (1999) The Danish Osteoporosis Prevention Study (DOPS): project design and inclusion of 2000 normal perimenopausal women. Maturitas 31:207-219
21. Genant HK, Grampp S, Gluer CC, Faulkner KG, Jergas M, Engelke K, Hagiwara S, Van Kuijk C (1994) Universal standardization for dual x-ray absorptiometry: patient and phantom cross-calibration results [see comments]. J Bone Miner Res 9:1503-1514
22. Abrahamsen B, Gram J, Hansen TB, Beck-Nielsen H (1995) Cross calibration of QDR-2000 and QDR-1000 dual-energy X-ray densitometers for bone mineral and soft-tissue measurements. Bone 16:385-390
23. McCloskey EV, Spector TD, Eyres KS, Fern ED, O'Rourke N, Vasikaran S, Kanis JA (1993) The assessment of vertebral deformity: a method for use in population studies and clinical trials. Osteoporos Int 3:138-147
24. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV, Ignatieva EV, Ananko EA, Podkolodnaya OA, Kolpakov FA, Podkolodny NL, Kolchanov NA (1998) Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 26:362-367
25. Meirhaeghe A, Fajas L, Gouilleux F, Cottel D, Helbecque N, Auwerx J, Amouyel P (2003) A functional polymorphism in a STAT5B site of the human PPAR gamma 3 gene promoter affects height and lipid metabolism in a French population. Arterioscler Thromb Vasc Biol 23:289-294
26. Wei Q, Jacobs DR Jr, Schreiner PJ, Siscovick DS, Steffes MW, Fornage M (2006) Patterns of association between PPARgamma genetic variation and indices of adiposity and insulin action in African-Americans and whites: the CARDIA study. J Mol Med 84:955-965
27. Meirhaeghe A, Tanck MW, Fajas L, Janot C, Helbecque N, Cottel D, Auwerx J, Amouyel P, Dallongeville J (2005) Study of a new PPARgamma2 promoter polymorphism and haplotype analysis in a French population. Mol Genet Metab 85:140-148
28. Wolford JK, Yeatts KA, Dhanjal SK, Black MH, Xiang AH, Buchanan TA, Watanabe RM (2005) Sequence variation in PPARG may underlie differential response to troglitazone. Diabetes 54:3319-3325
29. Muller YL, Bogardus C, Beamer BA, Shuldiner AR, Baier LJ (2003) A functional variant in the peroxisome proliferatoractivated receptor gamma2 promoter is associated with predictors of obesity and type 2 diabetes in Pima Indians. Diabetes 52:1864-1871
30. Meirhaeghe A, Cottel D, Amouyel P, Dallongeville J (2005) Association between peroxisome proliferator-activated receptor gamma haplotypes and the metabolic syndrome in French men and women. Diabetes 54:3043-3048
31. Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215
32. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2):263-265
33. Comings DE, MacMurray JP (2000) Molecular heterosis: a review. Mol Genet Metab 71:19-31
34. Altshuler D, Hirschhorn JN, Klannemark M, Lindgren CM, Vohl MC, Nemesh J, Lane CR, Schaffner SF, Bolk S, Brewer C, Tuomi T, Gaudet D, Hudson TJ, Daly M, Groop L, Lander ES (2000) The common PPARgamma Pro12Ala polymorphism is associated with decreased risk of type 2 diabetes. Nat Genet 26:76-80
35. Deeb SS, Fajas L, Nemoto M, Pihlajamaki J, Mykkanen L, Kuusisto J, Laakso M, Fujimoto W, Auwerx J (1998) A Pro12Ala substitution in PPARgamma2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nat Genet 20:284-287
36. Yamauchi T, Kamon J, Waki H, Murakami K, Motojima K, Komeda K, Ide T, Kubota N, Terauchi Y, Tobe K, Miki H, Tsuchida A, Akanuma Y, Nagai R, Kimura S, Kadowaki T (2001) The mechanisms by which both heterozygous peroxisome proliferator-activated receptor gamma (PPARgamma) deficiency and PPARgamma agonist improve insulin resistance. J Biol Chem 276:41245-41254
37. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G (2000) Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100:197-207
38. Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD, Liao EY (2006) Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res 21:1648-1656
39. Tavares V, Hirata RD, Rodrigues AC, Monte O, Salles JE, Scallissi N, Speranza AC, Gomes S, Hirata MH (2005) Effect of the peroxisome proliferator-activated receptor-gamma C161T polymorphism on lipid profile in Brazilian patients with Type 2 diabetes mellitus. J Endocrinol Invest 28:129-136
40. Wan J, Xiong S, Chao S, Xiao J, Ma Y, Wang J, Roy S (2010) PPARgamma gene C161T substitution alters lipid profile in Chinese patients with coronaryarterydisease and type 2 diabetes mellitus. Cardiovasc Diabetol 9:13
41. Rhee EJ, Oh KW, Lee WY, Kim SY, Oh ES, Baek KH, Kang MI, Kim SW (2005) The effects of C161?T polymorphisms in exon 6 of peroxisome proliferator- activated receptor-gamma gene on bone mineral metabolism and serum osteoprotegerin levels in healthy middle-aged women. Am J Obstet Gynecol 192:1087-1093
42. Spiteller G (2001) Peroxidation of linoleic acid and its relation to aging and age dependent diseases. Mech Ageing Dev 122:617-657
43. Hattersley AT, McCarthy MI (2005) What makes a good genetic association study? Lancet 366:1315-1323
44. Bielohuby M, Matsuura M, Herbach N, Kienzle E, Slawik M, Hoeflich A, Bidlingmaier M (2009) Short term exposure to low-carbohydrate/high fat diets induces low bone mineral density and reduces bone formation in rats. J Bone Miner Res 25:275-284
45. Heikkinen S, Argmann C, Feige JN, Koutnikova H, Champy MF, li-Youcef N, Schadt EE, Laakso M, Auwerx J (2009) The Pro12Ala PPARgamma2 variant determines metabolism at the gene-environment interface. Cell Metab 9:88-98