Sex hormones and their receptors in bone homeostasis: Insights from genetically modified mouse models

Osteoporosis International

Volumn 21, Issue 3, 2010, Pages 365-372

  Vico, L ^a   Vanacker, J M ^b  

^a UNIVERSITÉ JEAN MONNET   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Androgen; Androgen receptor; Aromatase; Estrogen; Estrogen receptors; Mice model

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; AROMATASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; SOMATOMEDIN C; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR SP1;

APOPTOSIS; BIOMECHANICS; BONE DENSITY; BONE GROWTH; BONE METABOLISM; CELL DIFFERENTIATION; CORTICAL BONE; EXPERIMENTAL MODEL; GENE DELETION; GENETIC MODEL; GENOTYPE; HORMONE ACTION; HUMAN; KNOCKOUT MOUSE; MECHANOTRANSDUCTION; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCYTE; OSTEOLYSIS; PERIOSTEUM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SEX DIFFERENCE; SKELETON; TRABECULAR BONE;

ANIMALS; BONE AND BONES; FEMALE; GONADAL STEROID HORMONES; HOMEOSTASIS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 76549107195     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-009-0963-5     Document Type: Review

References (65)

1. S Khosla S Amin E Orwoll 2008 Osteoporosis in men Endocr Rev 29 441 464 10.1210/er.2008-0002 1:CAS:528:DC%2BD1cXosVCqu7g%3D 18451258 (Pubitemid 351831508)
2. EP Smith J Boyd GR Frank H Takahashi RM Cohen B Specker TC Williams DB Lubahn KS Korach 1994 Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man N Engl J Med 331 1056 1061 10.1056/ NEJM199410203311604 1:CAS:528:DyaK2MXitFWjt78%3D 8090165 (Pubitemid 24317698)
3. C Carani K Qin M Simoni M Faustini-Fustini S Serpente J Boyd KS Korach ER Simpson 1997 Effect of testosterone and estradiol in a man with aromatase deficiency N Engl J Med 337 91 95 10.1056/NEJM199707103370204 1:CAS:528:DyaK2sXkvVCrsr4%3D 9211678 (Pubitemid 27284394)
4. JP Bilezikian A Morishima J Bell MM Grumbach 1998 Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency N Engl J Med 339 599 603 10.1056/NEJM199808273390905 1:STN:280:DyaK1cznt1Cmsw%3D%3D 9718379 (Pubitemid 28385657)
5. SC Manolagas S Kousteni RL Jilka 2002 Sex steroids and bone Recent Prog Horm Res 57 385 409 10.1210/rp.57.1.385 1:CAS:528:DC%2BD38Xjt1WqtLc%3D 12017554 (Pubitemid 35051830)
6. Y Onoe C Miyaura H Ohta S Nozawa T Suda 1997 Expression of estrogen receptor beta in rat bone Endocrinol 138 4509 4512 10.1210/en.138.10.4509 1:CAS:528:DyaK2sXmsVahsbk%3D (Pubitemid 27408505)
7. S Bord A Horner Beavan J Compston 2001 Estrogen receptors alpha and beta are differentially expressed in developing human bone J Clin Endocrinol Metab 86 2309 2314 10.1210/jc.86.5.2309 1:CAS:528:DC%2BD3MXjs1Omur0%3D 11344243 (Pubitemid 32472956)
8. UI Mödder A Sanyal AE Kearns JD Sibonga E Nishihara J Xu BW O'Malley EL Ritman BL Riggs TC Spelsberg S Khosla 2004 Effects of loss of steroid receptor coactivator-1 on the skeletal response to estrogen in mice Endocrinol 145 913 921 10.1210/en.2003-1089 (Pubitemid 38183835)
9. M Almeida L Han M Martin-Millan LI Plotkin SA Stewart PK Roberson S Kousteni CA O'Brien T Bellido AM Parfitt RS Weinstein RL Jilka SC Manolagas 2007 Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids J Biol Chem 282 27285 27297 10.1074/jbc.M702810200 1:CAS:528:DC%2BD2sXhtVWjsLfF 17623659 (Pubitemid 47501960)
10. JF Couse SW Curtis TF Washburn J Lindzey TS Golding DB Lubahn O Smithies KS Korach 1995 Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene Mol Endocrinol 9 1441 1454 10.1210/me.9.11.1441 1:CAS:528:DyaK2MXptV2hur0%3D 8584021
11. G Flouriot H Brand S Denger R Metivier M Kos G Reid V Sonntag-Buck F Gannon 2000 Identification of a new isoform of the human estrogen receptor-alpha (hER-alpha) that is encoded by distinct transcripts and that is able to repress hER-alpha activation function 1 EMBO J 19 4688 4700 10.1093/emboj/19.17.4688 1:CAS:528:DC%2BD3cXmslGrsr4%3D 10970861
12. NA Sims S Dupont A Krust P Clement-Lacroix D Minet M Resche-Rigon M Gaillard-Kelly R Baron 2002 Deletion of estrogen receptors reveals a regulatory role for estrogen receptors-beta in bone remodeling in females but not in males Bone 30 18 25 10.1016/S8756-3282(01)00643-3 1:CAS:528:DC%2BD38XktFeruw%3D%3D 11792560 (Pubitemid 34044296)
13. S Dupont A Krust A Gansmuller A Dierich P Chambon M Mark 2000 Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes Development 127 4277 4291 1:CAS:528:DC%2BD3cXotVWisbY%3D 10976058
14. MK Lindberg SL Alatalo JM Halleen S Mohan JA Gustafsson C Ohlsson 2001 Estrogen receptor specificity in the regulation of the skeleton in female mice J Endocrinol 171 229 236 10.1677/joe.0.1710229 1:CAS:528:DC%2BD3MXosV2htrY%3D 11691642 (Pubitemid 33061699)
15. SH Windahl O Vidal G Andersson JA Gustafsson C Ohlsson 1999 Increased cortical bone mineral content but unchanged trabecular bone mineral density in female ERbeta(-/-) mice J Clin Invest 104 895 901 10.1172/JCI6730 1:CAS:528:DyaK1MXmsVClsbw%3D 10510330
16. HZ Ke TA Brown H Qi DT Crawford HA Simmons DN Petersen MR Allen JD McNeish DD Thompson 2002 The role of estrogen receptor-beta, in the early age-related bone gain and later age-related bone loss in female mice J Musculoskelet Neuronal Interact 2 479 488 1:CAS:528:DC%2BD38XnvVSrsrw%3D 15758417
17. SH Windahl K Hollberg O Vidal JA Gustafsson C Ohlsson G Andersson 2001 Female estrogen receptor beta-/- mice are partially protected against age-related trabecular bone loss J Bone Miner Res 16 1388 1398 10.1359/jbmr.2001.16.8.1388 1:CAS:528:DC%2BD3MXmtVOht7c%3D 11499861
18. MK Lindberg S Movérare S Skrtic H Gao K Dahlman-Wright JA Gustafsson C Ohlsson 2003 Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "yin 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)
19. V Parikka Z Peng T Hentunen J Risteli T Elo HK Vaananen P Harkonen 2005 Estrogen responsiveness of bone formation in vitro and altered bone phenotype in aged estrogen receptor-alpha-deficient male and female mice Eur J Endocrinol 152 301 314 10.1530/eje.1.01832 1:CAS:528:DC%2BD2MXit1Wht7g%3D 15745940 (Pubitemid 40309579)
20. KE McDougall MJ Perry RL Gibson JM Bright SM Colley JB Hodgin O Smithies JH Tobias 2002 Estrogen-induced osteogenesis in intact female mice lacking ER Am J Physiol Endocrinol Metab 283 E817 E823 1:CAS:528:DC%2BD38XotV2qsrg%3D 12217900
21. O Vidal MK Lindberg K Hollberg DJ Baylink G Andersson DB Lubahn S Mohan JA Gustafsson C Ohlsson 2000 Estrogen receptor specificity in the regulation of skeletal growth and maturation in male mice Proc Natl Acad Sci U S A 97 5474 5479 10.1073/pnas.97.10.5474 1:CAS:528:DC%2BD3cXjsVWmsrk%3D 10805804 (Pubitemid 30313743)
22. NA Sims P Clement-Lacroix D Minet C Fraslon-Vanhulle M Gaillard-Kelly M Resche-Rigon R Baron 2003 A functional androgen receptor is not sufficient to allow estradiol to protect bone after gonadectomy in estradiol receptor-deficient mice J Clin Invest 111 1319 1327 1:CAS:528: DC%2BD3sXjsFCrsr0%3D 12727923
23. JH Krege JB Hodgin JF Couse E Enmark M Warner JF Mahler M Sar KS Korach JA Gustafsson O Smithies 1998 Generation and reproductive phenotypes of mice lacking estrogen receptor β Proc Natl Acad Sci U S A 95 15677 15682 10.1073/pnas.95.26.15677 1:CAS:528:DyaK1MXhvFeiuw%3D%3D 9861029 (Pubitemid 29018759)
24. Z Weihua S Saji S Makinen G Cheng EV Jensen M Warner JA Gustafsson 2000 Estrogen receptor (ER) β, a modulator of ERα in the uterus Proc Natl Acad Sci U S A 97 5936 5941 10.1073/pnas.97.11.5936 1:STN:280: DC%2BD3c3otl2huw%3D%3D 10823946 (Pubitemid 30367502)
25. NN Yang M Venugopalan S Hardikar A Glasebrook 1996 Identification of an estrogen response element activated by metabolites of 17-estradiol and raloxifene Science 273 1222 1225 10.1126/science.273.5279.1222 1:CAS:528:DyaK28Xltlajsr8%3D 8703055
26. Y Umayahara R Kawamori H Watada E Imano N Iwama T Morishima Y Yamasaki Y Kajimoto T Kamada 1994 Estrogen regulation of the insulin-like growth factor I gene transcription involves an AP-1 enhancer J Biol Chem 269 16433 16441 1:CAS:528:DyaK2cXkt1ymsLg%3D 8206951
27. S Kousteni T Bellido LI Plotkin CA O'Brien DL Bodenner L Han K Han GB DiGregorio JA Katznellenbogen BS Katznellenbogen PK Roberson RS Weinstein RL Jilka SC Manolagas 2001 Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity Cell 104 1 20 10.1016/S0092-8674(01)00185-4 (Pubitemid 32144966)
28. UE Mårtensson SA Salehi S Windahl MF Gomez K Swärd J Daszkiewicz-Nilsson A Wendt N Andersson P Hellstrand PO Grände C Owman CJ Rosen ML Adamo I Lundquist P Rorsman BO Nilsson C Ohlsson B Olde LM Leeb-Lundberg 2009 Deletion of the G protein-coupled receptor 30 impairs glucose tolerance, reduces bone growth, increases blood pressure, and eliminates estradiol-stimulated insulin release in female mice Endocrinol 150 687 698 10.1210/en.2008-0623
29. SH Windahl N Andersson AS Chagin UE Mårtensson H Carlsten B Olde C Swanson S Movérare-Skrtic L Sävendahl MK Lagerquist LM Leeb-Lundberg C Ohlsson 2009 The role of the G protein-coupled receptor GPR30 in the effects of estrogen in ovariectomized mice Am J Physiol Endocrinol Metab 296 E490 E496 10.1152/ajpendo.90691.2008 1:CAS:528:DC%2BD1MXjtFGrt7w%3D 19088255
30. MZ Cheng SCF Rawlinson AA Pitsillides G Zaman S Mohan DJ Baylink LE Lanyon 2002 Human osteoblasts' proliferative responses to strain and 17-estradiol are mediated by the estrogen receptor and the receptor for insulin-like growth factor I J Bone Miner Res 17 593 602 10.1359/jbmr.2002.17.4. 593 1:CAS:528:DC%2BD38XislCkurc%3D 11924572
31. G Zaman MZ Cheng HL Jessop R White LE Lanyon 2000 Mechanical strain activates estrogen response elements in bone cells Bone 27 233 239 10.1016/S8756-3282(00)00324-0 1:CAS:528:DC%2BD3cXltVGqsbk%3D 10913916 (Pubitemid 30458816)
32. JI Aguirre LI Plotkin AR Gortazar MM Millan CA O'Brien SC Manolagas T Bellido 2007 A novel ligand-independent function of the estrogen receptor is essential for osteocyte and osteoblast mechanotransduction J Biol Chem 282 25501 25508 10.1074/jbc.M702231200 1:CAS:528:DC%2BD2sXpsFWltr8%3D 17609204 (Pubitemid 47372838)
33. M Jakacka M Ito F Martinson T Ishikawa EJ Lee JL Jameson 2002 An estrogen receptor (ER) alpha deoxyribonucleic acid-binding domain knock-in mutation provides evidence for nonclassical ER pathway signaling in vivo Mol Endocrinol 16 2188 2201 10.1210/me.2001-0174 1:CAS:528:DC%2BD38XnsFKmurk%3D 12351685 (Pubitemid 35155533)
34. FA Syed UI Modder DG Fraser TC Spelsberg CJ Rosen A Krust P Chambon JL Jameson S Khosla 2005 Skeletal effects of estrogen are mediated by opposing actions of classical and nonclassical estrogen receptor pathways J Bone Miner Res 20 1992 2001 10.1359/JBMR.050713 1:CAS:528:DC%2BD2MXht1amt7bM 16234973 (Pubitemid 41532785)
35. FA Syed DG Fraser TC Spelsberg CJ Rosen A Krust P Chambon JL Jameson S Khosla 2007 Effects of loss of classical estrogen response element signaling on bone in male mice Endocrinol 148 1902 1910 10.1210/en.2006-1165 1:CAS:528:DC%2BD2sXjvVOhtbs%3D (Pubitemid 46457128)
36. EF Eriksen DS Colvard NJ Berg ML Graham KG Mann TC Spelsberg BL Riggs 1988 Evidence of estrogen receptors in normal human osteoblast-like cells Science 241 84 86 10.1126/science.3388021 1:CAS:528:DyaL1cXks1Oitr8%3D 3388021
37. O Vidal LG Kindblom C Ohlsson 1999 Expression and localization of estrogen receptor-beta in murine and human bone J Bone Miner Res 14 923 929 10.1359/jbmr.1999.14.6.923 1:CAS:528:DyaK1MXjvFKqtbk%3D 10352100 (Pubitemid 29262886)
38. IP Braidman L Hainey G Batra PL Selby PT Saunders JA Hoyland 2001 Localization of estrogen receptor beta protein expression in adult human bone J Bone Miner Res 16 214 220 10.1359/jbmr.2001.16.2.214 1:CAS:528: DC%2BD3MXptlOrtA%3D%3D 11204421
39. T Nakamura Y Imai T Matsumoto S Sato K Takeuchi K Igarashi Y Harada Y Azuma A Krust Y Yamamoto H Nishina S Takeda H Takayanagi D Metzger J Kanno K Takaoka TJ Martin P Chambon S Kato 2007 Estrogen prevents bone loss via estrogen receptor a and induction of Fas ligand in osteoclasts Cell 130 811 823 10.1016/j.cell.2007.07.025 1:CAS:528:DC%2BD2sXhtV2ntL%2FI 17803905 (Pubitemid 47332572)
40. T Kameda H Mano T Yuasa Y Mori K Miyazawa M Shiokawa Y Nakamaru E Hiroi K Hiura A Kameda NN Yang Y Hakeda M Kumegawa 1997 Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts J Exp Med 186 489 495 10.1084/jem.186.4.489 1:CAS:528:DyaK2sXlsFWmtb8%3D 9254647 (Pubitemid 27360793)
41. SA Krum GA Miranda-Carboni PV Hauschka JS Carroll TF Lane LP Freedman M Brown 2008 Estrogen protects bone by inducing Fas ligand in osteoblasts to regulated osteoclast survival EMBO J 27 535 545 10.1038/sj.emboj.7601984 1:CAS:528:DC%2BD1cXhs1KgtLs%3D 18219273 (Pubitemid 351225684)
42. CR Fisher KH Graves AF Parlow ER Simpson 1998 Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene Proc Natl Acad Sci U S A 95 6965 6970 10.1073/pnas.95.12.6965 1:CAS:528:DyaK1cXjslyms7w%3D 9618522 (Pubitemid 28278090)
43. OK Oz JE Zerwekh C Fisher K Graves L Nanu R Millsaps ER Simpson 2000 Bone has a sexually dimorphic response to aromatase deficiency J Bone Miner Res 15 507 514 10.1359/jbmr.2000.15.3.507 1:CAS:528:DC%2BD3cXitFaktrY%3D 10750565
44. C Miyaura K Toda M Inada T Ohshiba C Matsumoto T Okada M Ito Y Shizuta A Ito 2001 Sex- and age-related response to aromatase deficiency in bone Biochem Biophys Res Commun 280 1062 1068 10.1006/bbrc.2001.4246 1:CAS:528: DC%2BD3MXnvFOjsQ%3D%3D 11162635 (Pubitemid 32924448)
45. MEE Jones KJ McInnes WC Boon ER Simpson 2007 Estrogen and adiposity - Utilizing models of aromatase deficiency to explore the relationship J Steroid Biochem Mol Biol 106 3 7 10.1016/j.jsbmb.2007.05.029 1:CAS:528: DC%2BD2sXhtVWitbjF 17643292 (Pubitemid 47362638)
46. Y Onoe C Miyaura M Ito H Ohta S Nozawa T Suda 2000 Comparative effects of estrogen and raloxifene on B-lymphopoiesis and bone loss induced by sex steroid deficiency in mice J Bone Miner Res 15 541 549 10.1359/jbmr.2000.15.3.541 1:CAS:528:DC%2BD3cXitFakt78%3D 10750569
47. S Moverare K Venken AL Eriksson N Andersson S Skrtic J Wergedal S Mohan P Salmon R Bouillon JA Gustafsson D Vanderschueren C Ohlsson 2003 Differential effects on bone of estrogen receptor alpha and androgen receptor activation in orchidectomized adult male mice Proc Natl Acad Sci U S A 100 13573 13578 10.1073/pnas.2233084100 1:CAS:528:DC%2BD3sXptFOitL8%3D 14573701 Erratum in: Proc Natl Acad Sci U S A. 2006 103:8298 (Pubitemid 37448563)
48. H Kawano T Sato T Yamada T Matsumoto K Sekine T Watanabe T Nakamura T Fukuba K Yoshimura T Yoshizawa K Aihara Y Yamamoto Y Nakamichi D Metzger P Chambon K Nakamura H Kawaguchi S Kato 2003 Suppressive function of androgen receptor in bone resorption Proc Natl Acad Sci U S A 100 9416 9421 10.1073/pnas.1533500100 1:CAS:528:DC%2BD3sXmtlyktbo%3D 12872002 (Pubitemid 37033943)
49. K Venken K De Gendt S Boonen J Ophoff R Bouillon JV Swinnen G Verhoeven D Vanderschueren 2006 Relative impact of androgen and estrogen receptor activation in the effects of androgens on trabecular and cortical bone in growing male mice: a study in the androgen receptor knockout mouse model J Bone Miner Res 21 576 585 10.1359/jbmr.060103 1:CAS:528:DC%2BD28Xkt1Kqs7w%3D 16598378
50. F Callewaert K Venken J Ophoff K De Gendt A Torcasio GH van Lenthe H van Oosterwyck S Boonen R Bouillon G Verhoeven D Vanderschueren 2009 Differential regulation of bone and body composition in male mice with combined inactivation of androgen and estrogen receptor-a FASEB J. 23 232 240 10.1096/fj.08-113456 1:CAS:528:DC%2BD1MXlsVOksQ%3D%3D 18809737
51. S Khosla LJ Melton 3rd BL Riggs 2002 Clinical review 144: estrogen and the male skeleton J Clin Endocrinol Metab 87 1443 1450 10.1210/jc.87.4.1443 1:CAS:528:DC%2BD38XivFKlsbw%3D 11932262 (Pubitemid 34615219)
52. AS Chagin L Savendahl 2007 Oestrogen receptors and linear bone growth Acta Paediatrica 96 1275 1279 10.1111/j.1651-2227.2007.00415.x 17718780 (Pubitemid 47300692)
53. JF Nelson LS Felicio HH Osterburg CE Finch 1992 Differential contributions of ovarian and extraovarian factors to age-related reductions in plasma estradiol and progesterone during the estrous cycle of C57BL/6 J mice Endocrinol 130 805 810 10.1210/en.130.2.805 1:CAS:528:DyaK38XpvFGqsg%3D%3D
54. K Albertsson-Wikland S Rosberg B Lannering L Dunkel G Selstam E Norjavaara 1997 Twenty-four-hour profiles of luteinizing hormone, follicle-stimulating hormone, testosterone, and estradiol levels: a semilongitudinal study throughout puberty in healthy boys J Clin Endocrinol Metab 82 541 549 10.1210/jc.82.2.541 1:CAS:528:DyaK2sXhtVWku7Y%3D 9024251 (Pubitemid 27068626)
55. E Norjavaara C Ankarberg K Albertsson-Wikland 1996 Diurnal rhythm of 17 beta-estradiol secretion throughout pubertal development in healthy girls: evaluation by a sensitive radioimmunoassay J Clin Endocrinol Metab 81 4095 4102 10.1210/jc.81.11.4095 1:CAS:528:DyaK28XntVCrsb0%3D 8923866 (Pubitemid 26380423)
56. A Chagin M Nilsson K Dahlman Wright L Savendahl 2006 Remaining estrogenic activity in the man with mutated estrogen receptor alpha Horm Res 65 Suppl 4 28
57. JM Hall JF Couse KS Korach 2001 The multifaceted mechanisms of estradiol and estrogen receptor signaling J Biol Chem 276 36869 36872 10.1074/jbc. R100029200 1:CAS:528:DC%2BD3MXns1eltr4%3D 11459850
58. KC Lee H Jessop R Suswillo G Zaman LE Lanyon 2004 The adaptive response of bone to mechanical loading in female transgenic mice is deficient in the absence of oestrogen receptor-alpha and -beta J Endocrinol 182 193 201 10.1677/joe.0.1820193 1:CAS:528:DC%2BD2cXntFOgt7s%3D 15283680 (Pubitemid 39199003)
59. LK Saxon CH Turner 2005 Estrogen receptor β: the anti-mechanostat? Bone 36 185 192 10.1016/j.bone.2004.08.003 1:CAS:528:DC%2BD2MXhslWks70%3D 15780944 (Pubitemid 40283575)
60. S Khosla UI Moedder FA Syed 2005 Letter to the editor Bone 38 289 289 10.1016/j.bone.2005.08.001 16137932
61. R Bouillon M Bex D Vanderschueren S Boonen 2004 Estrogens are essential for male pubertal periosteal bone expansion J Clin Endocrinol Metab 89 6025 6029 10.1210/jc.2004-0602 1:CAS:528:DC%2BD2cXhtFSitrfF 15579754 (Pubitemid 39628410)
62. D Vanderschueren K Venken J Ophoff R Bouillon S Boonen 2006 Clinical review: sex steroids and the periosteum-reconsidering the roles of androgens and estrogens in periosteal expansion J Clin Endocrinol Metab 91 378 382 10.1210/jc.2005-1766 1:CAS:528:DC%2BD28XhsFKnt7o%3D 16303833 (Pubitemid 43236896)
63. N Shah WS Evans CY Bowers JD Veldhuis 2000 Oral estradiol administration modulates continuous intravenous growth hormone (GH)-releasing peptide-2-driven GH secretion in postmenopausal women J Clin Endocrinol Metab 85 2649 2659 10.1210/jc.85.8.2649 1:CAS:528:DC%2BD3cXnslaiurc%3D 10946861 (Pubitemid 32269131)
64. C Ohlsson JO Jansson O Isaksson 2000 Effects of growth hormone and insulin like growth factor-I on body growth and adult bone metabolism Curr Opin Rheumatol 12 346 348 10.1097/00002281-200007000-00019 1:CAS:528: DC%2BD3cXlsVGisrs%3D 10910189 (Pubitemid 30439691)
65. K Venken F Schuit L Van Lommel K Tsukamoto JJ Kopchick K Coschigano C Ohlsson S Moverare S Boonen R Bouillon D Vanderschueren 2005 Growth without growth hormone receptor: estradiol is a major growth hormone-independent regulator of hepatic IGF-I synthesis J Bone Miner Res 20 2138 2149 10.1359/JBMR.050811 1:CAS:528:DC%2BD2MXhtlWntrbI 16294267 (Pubitemid 41698777)