A prospective study of androgen levels, hormone-related genes and risk of rheumatoid arthritis

Arthritis Research and Therapy

Volumn 11, Issue 3, 2009, Pages

  Karlson, Elizabeth W ^a   Chibnik, Lori B ^a   McGrath, Monica ^a   Chang, Shun Chiao ^b   Keenan, Brendan T ^a   Costenbader, Karen H ^a   Fraser, Patricia A ^c,d   Tworoger, Shelley ^a,b   Hankinson, Susan E ^a,b   Lee, I Min ^a,b   Buring, Julie ^a,b,e   De Vivo, Immaculata ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c CENTER FOR BLOOD RESEARCH   (United States)

^d GENZYME CORPORATION   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; AROMATASE; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR 2; PRASTERONE SULFATE; PROGESTERONE RECEPTOR; RHEUMATOID FACTOR; SEX HORMONE BINDING GLOBULIN; STEROID HORMONE; TESTOSTERONE; UNCLASSIFIED DRUG;

ADULT; AGED; ANDROGEN BLOOD LEVEL; ARTICLE; CASE CONTROL STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HORMONE BLOOD LEVEL; HUMAN; MAJOR CLINICAL STUDY; MUTATIONAL ANALYSIS; PATHOGENESIS; PROSPECTIVE STUDY; RHEUMATOID ARTHRITIS; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; TRINUCLEOTIDE REPEAT; WOMEN'S HEALTH; BLOOD; CLINICAL TRIAL; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED CLINICAL TRIAL; DOUBLE BLIND PROCEDURE; FOLLOW UP; GENETICS; MALE; MIDDLE AGED; PILOT STUDY; RANDOMIZED CONTROLLED TRIAL; RISK FACTOR;

ADULT; AGED; ANDROGENS; ARTHRITIS, RHEUMATOID; CASE-CONTROL STUDIES; COHORT STUDIES; DOUBLE-BLIND METHOD; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; PILOT PROJECTS; POLYMORPHISM, GENETIC; PROSPECTIVE STUDIES; RECEPTORS, ANDROGEN; RISK FACTORS;

EID: 67650666445     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2742     Document Type: Article

References (70)

1. Linos A Worthington JW O'Fallon WM Kurland LT The epidemiology of rheumatoid arthritis in Rochester, Minnesota: A study of incidence, prevalence, and mortality Am J Epidemiol 1980, 111:87-98. 7352462
2. Symmons DP Barrett EM Bankhead CR Scott DG Silman AJ The incidence of rheumatoid arthritis in the United Kingdom: Results from the Norfolk Arthritis Register Br J Rheumatol 1994, 33:735-739. 10.1093/rheumatology/ 33.8.735 8055200
3. Cutolo M Capellino S Sulli A Serioli B Secchi ME Villaggio B Straub RH Estrogens and autoimmune diseases Ann N Y Acad Sci 2006, 1089:538-547. 10.1196/annals.1386.043 17261796
4. Masi AT Aldag JC Chatterton RT Sex hormones and risks of rheumatoid arthritis and developmental or environmental influences Ann N Y Acad Sci 2006, 1069:223-235. 10.1196/annals.1351.020 16855149
5. Davidson JM Chen JJ Crapo L Gray GD Greenleaf WJ Catania JA Hormonal changes and sexual function in aging men J Clin Endocrinol Metab 1983, 57:71-77. 6602143
6. Sambrook PN Eisman JA Champion GD Pocock NA Sex hormone status and osteoporosis in postmenopausal women with rheumatoid arthritis Arthritis Rheum 1988, 31:973-978. 10.1002/art.1780310805 2970263
7. Spector TD Perry LA Tubb G Silman AJ Huskisson EC Low free testosterone levels in rheumatoid arthritis Ann Rheum Dis 1988, 47:65-68. 1003446 3345107 10.1136/ard.47.1.65
8. Cutolo M Balleari E Giusti M Monachesi M Accardo S Sex hormone status of male patients with rheumatoid arthritis: Evidence of low serum concentrations of testosterone at baseline and after human chorionic gonadotropin stimulation Arthritis Rheum 1988, 31:1314-1317. 10.1002/ art.1780311015 3140823
9. Gagnerault MC Touraine P Savino W Kelly PA Dardenne M Expression of prolactin receptors in murine lymphoid cells in normal and autoimmune situations J Immunol 1993, 150:5673-5681. 8515082
10. Masi AT Feigenbaum SL Chatterton RT Hormonal and pregnancy relationships to rheumatoid arthritis: Convergent effects with immunologic and microvascular systems Semin Arthritis Rheum 1995, 25:1-27. 10.1016/ S0049-0172(95)80014-X 8525387
11. Gordon D Beastall GH Thomson JA Sturrock RD Prolonged hypogonadism in male patients with rheumatoid arthritis during flares in disease activity Br J Rheumatol 1988, 27:440-444. 10.1093/rheumatology/27.6.440 3144408
12. Deighton CM Watson MJ Walker DJ Sex hormones in postmenopausal HLA-identical rheumatoid arthritis discordant sibling pairs J Rheumatol 1992, 19:1663-1667. 1491383
13. Cutolo M Accardo S Villaggio B Barone A Sulli A Coviello DA Carabbio C Felli L Miceli D Farruggio R Carruba G Castagnetta L Androgen and estrogen receptors are present in primary cultures of human synovial macrophages J Clin Endocrinol Metab 1996, 81:820-827. 10.1210/ jc.81.2.820 8636310
14. Castagnetta LA Carruba G Granata OM Stefano R Miele M Schmidt M Cutolo M Straub RH Increased estrogen formation and estrogen to androgen ratio in the synovial fluid of patients with rheumatoid arthritis J Rheumatol 2003, 30:2597-2605. 14719200
15. Booji A Biewenga-Booji CM Huber-Bruning O Cornelis C Jacobs JW Bijlsma JW Androgens as adjuvant treatment in postmenopausal female patients with rheumatoid arthritis Ann Rheum Dis 1996, 55:811-815. 1010316 8976637 10.1136/ard.55.11.811
16. Cutolo M Balleari E Giusti M Intra E Accardo S Androgen replacement therapy in male patients with rheumatoid arthritis Arthritis Rheum 1991, 34:1-5. 10.1002/art.1780340102 1824615
17. Masi AT Bijlsma JW Chikanza IC Pitzalis C Cutolo M Neuroendocrine, immunologic, and microvascular systems interactions in rheumatoid arthritis: Physiopathogenetic and therapeutic perspectives [review, 115 refs] Semin Arthritis Rheum 1999, 29:65-81. 10.1016/ S0049-0172(99)80039-0 10553979
18. Heikkila R Aho K Heliovaara M Knekt P Reunanen A Aromaa A Leino A Palosuo T Serum androgen-anabolic hormones and the risk of rheumatoid arthritis Ann Rheum Dis 1998, 57:281-285. 1752601 9741311 10.1136/ ard.57.5.281
19. Bellido T Jilka RL Boyce BF Girasole G Broxmeyer H Dalrymple SA Murray R Manolagas SC Regulation of interleukin-6, osteoclastogenesis, and bone mass by androgens. The role of the androgen receptor J Clin Invest 1995, 95:2886-2895. 295976 7769130 10.1172/JCI117995
20. Cutolo M Sulli A Villaggio B Seriolo B Accardo S Relations between steroid hormones and cytokines in rheumatoid arthritis and systemic lupus erythematosus [review, 67 refs] Ann Rheum Dis 1998, 57:573-577. 1752484 9893566 10.1136/ard.57.10.573
21. Dalal M Kim S Voskuhl RR Testosterone therapy ameliorates experimental autoimmune encephalomyelitis and induces a T helper 2 bias in the autoantigen-specific T lymphocyte response J Immunol 1997, 159:3-6. 9200430
22. Giltay EJ Fonk JC Von B Drexhage HA Schalkwijk C Gooren LJ In vivo effects of sex steroids on lymphocyte responsiveness and immunoglobulin levels in humans J Clin Endocrinol Metab 2000, 85:1648-1657. 10.1210/ jc.85.4.1648 10770211
23. Morita Y Yamamura M Nishida K Harada S Okamoto H Inoue H Ohmoto Y Modlin RL Makino H Expression of interleukin-12 in synovial tissue from patients with rheumatoid arthritis Arthritis Rheum 1998, 41:306-314. 10.1002/1529-0131(199802)41:2<306::AID-ART15>3.0.CO;2-4 9485089
24. Suzuki T Suzuki N Engleman EG Mizushima Y Sakane T Low serum levels of dehydroepiandrosterone may cause deficient IL-2 production by lymphocytes in patients with systemic lupus erythematosus (SLE) Clin Exp Immunol 1995, 99:251-255. 1534288 7851019
25. Feldmann M Brennan FM Maini RN Role of cytokines in rheumatoid arthritis [review, 226 refs] Annu Rev Immunol 1996, 14:397-440. 10.1146/ annurev.immunol.14.1.397 8717520
26. Silman A Kay A Brennan P Timing of pregnancy in relation to the onset of rheumatoid arthritis Arthritis Rheum 1992, 35:152-155. 10.1002/ art.1780350205 1734904
27. Quigley CA De Bellis A Marschke KB el-Awady MK Wilson EM French FS Androgen receptor defects: Historical, clinical, and molecular perspectives Endocr Rev 1995, 16:271-321. 7671849
28. Chamberlain NL Driver ED Miesfeld RL The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function Nucl Acids Res 1994, 22:3181-3186. 310294 8065934 10.1093/nar/22.15.3181
29. Tut TG Ghadessy FJ Trifiro MA Pinsky L Yong EL Long polyglutamine tracts in the androgen receptor are associated with reduced trans-activation, impaired sperm production, and male infertility J Clin Endocrinol Metab 1997, 82:3777-3782. 10.1210/jc.82.11.3777 9360540
30. Westberg L Baghaei F Rosmond R Hellstrand M Landen M Jansson M Holm G Bjorntorp P Eriksson E Polymorphisms of the androgen receptor gene and the estrogen receptor beta gene are associated with androgen levels in women J Clin Endocrinol Metab 2001, 86:2562-2568. 10.1210/jc.86.6.2562 11397855
31. + T lymphocytes in normal and rheumatoid synovium Arthritis Rheum 1993, 36:1087-1097. 10.1002/art.1780360809 8343185
32. Rousseau-Merck MF Misrahi M Loosfelt H Milgrom E Berger R Localization of the human progesterone receptor gene to chromosome 11q22-q23 Hum Genet 1987, 77:280-282. 3679212 10.1007/BF00284486
33. Horwitz KB Alexander PS In situ photolinked nuclear progesterone receptors of human breast cancer cells: Subunit molecular weights after transformation and translocation Endocrinology 1983, 113:2195-2201. 6685620
34. Wei LL Miner R Evidence for the existence of a third progesterone receptor protein in human breast cancer cell line T47D Cancer Res 1994, 54:340-343. 8275464
35. Ito A Imada K Sato T Kubo T Matsushima K Mori Y Suppression of interleukin 8 production by progesterone in rabbit uterine cervix Biochem J 1994, 301(Pt 1):183-186. 1137159 8037668
36. De Vivo I Hankinson SE Colditz GA Hunter DJ The progesterone receptor Val660 → Leu polymorphism and breast cancer risk Breast Cancer Res 2004, 6:R636-R639. 1064075 15535845 10.1186/bcr928
37. Le Bail J Liagre B Vergne P Bertin P Beneytout J Habrioux G Aromatase in synovial cells from postmenopausal women Steroids 2001, 66:749-757. 10.1016/S0039-128X(01)00104-0 11522337
38. Macdiarmid F Wang D Duncan LJ Purohit A Ghilchick MW Reed MJ Stimulation of aromatase activity in breast fibroblasts by tumor necrosis factor alpha Mol Cell Endocrinol 1994, 106:17-21. 10.1016/0303-7207(94)90181-3 7895904
39. Purohit A Ghilchik MW Duncan L Wang DY Singh A Walker MM Reed MJ Aromatase activity and interleukin-6 production by normal and malignant breast tissues J Clin Endocrinol Metab 1995, 80:3052-3058. 10.1210/ jc.80.10.3052 7559896
40. Haiman CA Stram DO Pike MC Kolonel LN Burtt NP Altshuler D Hirschhorn J Henderson BE A comprehensive haplotype analysis of CYP19 and breast cancer risk: The Multiethnic Cohort Hum Mol Genet 2003, 12:2679-2692. 10.1093/hmg/ddg294 12944421
41. Ridker PM Cook NR Lee IM Gordon D Gaziano JM Manson JE Hennekens CH Buring JE A randomized trial of low-dose aspirin in the primary prevention of cardiovascular disease in women N Engl J Med 2005, 352:1293-1304. 10.1056/NEJMoa050613 15753114
42. Lee IM Cook NR Gaziano JM Gordon D Ridker PM Manson JE Hennekens CH Buring JE Vitamin E in the primary prevention of cardiovascular disease and cancer: The WomeA's Health Study: a randomized controlled trial JAMA 2005, 294:56-65. 10.1001/jama.294.1.56 15998891
43. Cook NR Lee IM Gaziano JM Gordon D Ridker PM Manson JE Hennekens CH Buring JE Low-dose aspirin in the primary prevention of cancer: The Women's Health Study: A randomized controlled trial JAMA 2005, 294:47-55. 10.1001/jama.294.1.47 15998890
44. Costenbader KH Feskanich D Mandl LA Karlson EW Smoking intensity, duration, and cessation, and the risk of rheumatoid arthritis in women Am J Med 2006, 119:503-511. 10.1016/j.amjmed.2005.09.053 16750964
45. Karlson EW Sanchez-Guerrero J Wright EA Lew RA Daltroy LH Katz JN Liang MH A connective tissue disease screening questionnaire for population studies Ann Epidemiol 1995, 5:297-302. 10.1016/1047-2797(94)00096-C 8520712
46. Arnett FC Edworthy SM Bloch DA McShane DJ Fries JF Cooper NS Healey LA Kaplan SR Liang MH Luthra HS The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis Arthritis Rheum 1988, 31:315-324. 10.1002/art.1780310302 3358796
47. Hankinson SE Colditz GA Hunter DJ Manson JE Willett WC Stampfer MJ Longcope C Speizer FE Reproductive factors and family history of breast cancer in relation to plasma estrogen and prolactin levels in postmenopausal women in the Nurses' Health Study (United States) Cancer Causes Control 1995, 6:217-224. 10.1007/BF00051793 7612801
48. Wilke TJ Utley DJ Total testosterone, free-androgen index, calculated free testosterone, and free testosterone by analog RIA compared in hirsute women and in otherwise-normal women with altered binding of sex-hormone-binding globulin Clin Chem 1987, 33:1372-1375. 3608155
49. Cox DG Blanche H Pearce CL Calle EE Colditz GA Pike MC Albanes D Allen NE Amiano P Berglund G Boeing H Buring J Burtt N Canzian F Chanock S Clavel-Chapelon F Feigelson HS Freedman M Haiman CA Hankinson SE Henderson BE Hoover R Hunter DJ Kaaks R Kolonel L Kraft P LeMarchand L Lund E Palli D Peeters PH et al A comprehensive analysis of the androgen receptor gene and risk of breast cancer: Results from the National Cancer Institute Breast and Prostate Cancer Cohort Consortium (BPC3) Breast Cancer Res 2006, 8:R54. 1779488 16987421 10.1186/bcr1602
50. Cox DG Bretsky P Kraft P Pharoah P Albanes D Altshuler D Amiano P Berglund G Boeing H Buring J Burtt N Calle EE Canzian F Chanock S Clavel-Chapelon F Colditz GA Feigelson HS Haiman CA Hankinson SE Hirschhorn J Henderson BE Hoover R Hunter DJ Kaaks R Kolonel L LeMarchand L Lund E Palli D Peeters PH Pike MC et al Haplotypes of the estrogen receptor beta gene and breast cancer risk Int J Cancer 2008, 122:387-392. 10.1002/ijc.23127 17935138
51. Haiman CA Dossus L Setiawan VW Stram DO Dunning AM Thomas G Thun MJ Albanes D Altshuler D Ardanaz E Boeing H Buring J Burtt N Calle EE Chanock S Clavel-Chapelon F Colditz GA Cox DG Feigelson HS Hankinson SE Hayes RB Henderson BE Hirschhorn JN Hoover R Hunter DJ Kaaks R Kolonel LN Le Marchand L Lenner P Lund E et al Genetic variation at the CYP19A1 locus predicts circulating estrogen levels but not breast cancer risk in postmenopausal women Cancer Res 2007, 67:1893-1897. 10.1158/ 0008-5472.CAN-06-4123 17325027
52. National Center for Biotechnology Information database of single nucleotide polymorphisms http://www.ncbi.nlm.nih.gov/projects/SNP/
53. McGrath M Lee IM Hankinson SE Kraft P Hunter DJ Buring J De Vivo I Androgen receptor polymorphisms and endometrial cancer risk Int J Cancer 2006, 118:1261-1268. 10.1002/ijc.21436 16161040
54. De Vivo I Huggins GS Hankinson SE Lescault PJ Boezen M Colditz GA Hunter DJ A functional polymorphism in the promoter of the progesterone receptor gene associated with endometrial cancer risk Proc Natl Acad Sci USA 2002, 99:12263-12268. 129433 12218173 10.1073/pnas.192172299
55. De Vivo I Hankinson SE Colditz GA Hunter DJ A functional polymorphism in the progesterone receptor gene is associated with an increase in breast cancer risk Cancer Res 2003, 63:5236-5238. 14500352
56. Karlson EW Mandl LA Hankinson SE Grodstein F Do breast-feeding and other reproductive factors influence future risk of rheumatoid arthritis? Results from the Nurses' Health Study Arthritis Rheum 2004, 50:3458-3467. 10.1002/art.20621 15529351
57. DerSimonian R Laird N Meta-analysis in clinical trials Control Clin Trials 1986, 7:177-188. 10.1016/0197-2456(86)90046-2 3802833
58. Kawasaki T Ushiyama T Ueyama H Inoue K Mori K Ohkubo I Hukuda S Polymorphic CAG repeats of the androgen receptor gene and rheumatoid arthritis Ann Rheum Dis 1999, 58:500-502. 1752923 10419869 10.1136/ ard.58.8.500
59. Lo SF Huang CM Tsai CH Chen WC Lai CC Tsai Y Tsai FJ Androgen receptor gene polymorphism and rheumatoid arthritis in Taiwan Clin Exp Rheumatol 2006, 24:209-210. 16762161
60. Yu SF Cheng TT Hsu YH Lai HM Chen YC Chiu CK Lin KM Chang C Chen CJ Kang HY Association of tri-nucleotide (CAG and GGC) repeat polymorphism of androgen receptor gene in Taiwanese women with refractory or remission rheumatoid arthritis Clin Rheumatol 2007, 26:2051-2058. 10.1007/ s10067-007-0616-z 17431729
61. Takagi H Ishiguro N Iwata H Kanamono T Genetic association between rheumatoid arthritis and estrogen receptor microsatellite polymorphism J Rheumatol 2000, 27:1638-1642. 10914844
62. Ushiyama T Mori K Inoue K Huang J Nishioka J Hukuda S Association of oestrogen receptor gene polymorphisms with age at onset of rheumatoid arthritis Ann Rheum Dis 1999, 58:7-10. 1752749 10343533 10.1136/ ard.58.1.7
63. John S Myerscough A Eyre S Roby P Hajeer A Silman AJ Ollier WE Worthington J Linkage of a marker in intron D of the estrogen synthase locus to rheumatoid arthritis Arthritis Rheum 1999, 42:1617-1620. 10.1002/1529-0131(199908)42:8<1617::AID-ANR8>3.0.CO;2-N 10446859
64. Raychaudhuri S Remmers EF Lee AT Hackett R Guiducci C Burtt NP Gianniny L Korman BD Padyukov L Kurreeman FA Chang M Catanese JJ Ding B Wong S Helm-van Mil van der AH Neale BM Coblyn J Cui J Tak PP Wolbink GJ Crusius JB Horst-Bruinsma van der IE Criswell LA Amos CI Seldin MF Kastner DL Ardlie KG Alfredsson L Costenbader KH Altshuler D et al Common variants at CD40 and other loci confer risk of rheumatoid arthritis Nat Genet 2008, 40:1216-1223. 10.1038/ng.233 18794853
65. Wellcome Trust Case Control Consortium Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls Nature 2007, 447:661-678. 10.1038/nature05911 17554300
66. Hankinson SE Manson JE Spiegelman D Willett WC Longcope C Speizer FE Reproducibility of plasma hormone levels in postmenopausal women over a 2-3-year period Cancer Epidemiol Biomarkers Prev 1995, 4:649-654. 8547832
67. Hunter DJ Kraft P Jacobs KB Cox DG Yeager M Hankinson SE Wacholder S Wang Z Welch R Hutchinson A Wang J Yu K Chatterjee N Orr N Willett WC Colditz GA Ziegler RG Berg CD Buys SS McCarty CA Feigelson HS Calle EE Thun MJ Hayes RB Tucker M Gerhard DS Fraumeni JF Jr Hoover RN Thomas G Chanock SJ A genome-wide association study identifies alleles in FGFR2 associated with risk of sporadic postmenopausal breast cancer Nat Genet 2007, 39:870-874. 10.1038/ng2075 17529973
68. Plenge RM Seielstad M Padyukov L Lee AT Remmers EF Ding B Liew A Khalili H Chandrasekaran A Davies LR Li W Tan AK Bonnard C Ong RT Thalamuthu A Pettersson S Liu C Tian C Chen WV Carulli JP Beckman EM Altshuler D Alfredsson L Criswell LA Amos CI Seldin MF Kastner DL Klareskog L Gregersen PK TRAF1-C5 as a risk locus for rheumatoid arthritis - a genomewide study N Engl J Med 2007, 357:1199-209. 2636867 17804836 10.1056/NEJMoa073491
69. Remmers EF Plenge RM Lee AT Graham RR Hom G Behrens TW de Bakker PI Le JM Lee HS Batliwalla F Li W Masters SL Booty MG Carulli JP Padyukov L Alfredsson L Klareskog L Chen WV Amos CI Criswell LA Seldin MF Kastner DL Gregersen PK STAT4 and the risk of rheumatoid arthritis and systemic lupus erythematosus N Engl J Med 2007, 357:977-986. 2630215 17804842 10.1056/NEJMoa073003
70. Plenge RM Cotsapas C Davies L Price AL de Bakker PI Maller J Pe'er I Burtt NP Blumenstiel B DeFelice M Parkin M Barry R Winslow W Healy C Graham RR Neale BM Izmailova E Roubenoff R Parker AN Glass R Karlson EW Maher N Hafler DA Lee DM Seldin MF Remmers EF Lee AT Padyukov L Alfredsson L Coblyn J et al Two independent alleles at 6q23 associated with risk of rheumatoid arthritis Nat Genet 2007, 39:1477-1482. 2652744 17982456 10.1038/ng.2007.27