Estrogen receptor α36 mediates a bone-sparing effect of 17β-estrodiol in postmenopausal women

Journal of Bone and Mineral Research

Volumn 26, Issue 1, 2011, Pages 156-168

  Xie, Hui ^a   Sun, Mei ^b   Liao, Xiao Bo ^a   Yuan, Ling Qing ^a   Sheng, Zhi Feng ^a   Meng, Ji Cai ^a   Wang, Dan ^a   Yu, Zhi Yong ^a   Zhang, Lei Yi ^a   Zhou, Hou De ^a   Luo, Xiang Hang ^a   Li, Hui ^a   Wu, Xian Ping ^a   Wei, Qi You ^a   Tang, Si Yuan ^b   Wang, Zhao Yi ^c   Liao, Er Yuan ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

APOPTOSIS; BONE MINERAL DENSITY; ESTROGEN RECEPTOR 36; OSTEOBLAST; OSTEOCLAST

Indexed keywords

BIOCHEMICAL MARKER; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA 36; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ADULT; APOPTOSIS; ARTICLE; BONE DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HORMONE BLOOD LEVEL; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOGENESIS; OSTEOBLAST; OSTEOCLAST; POSTMENOPAUSE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADULT; APOPTOSIS; BIOLOGICAL MARKERS; BONE AND BONES; BONE DENSITY; BONE REMODELING; ENZYME ACTIVATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FLAVONOIDS; HUMANS; MIDDLE AGED; MITOGENS; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; POSTMENOPAUSE; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; TISSUE CULTURE TECHNIQUES;

EID: 78650925495     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1002/jbmr.169     Document Type: Article

References (47)

1. Deroo BJ, Korach KS., Estrogen receptors and human disease. J Clin Invest. 2006; 116: 561-570.
2. Almeida M, Han L, O'Brien CA, Kousteni S, Manolagas SC., Classical genotropic versus kinase-initiated regulation of gene transcription by the estrogen receptor α. Endocrinology. 2006; 147: 1986-1996.
3. Kousteni S, Chen JR, Bellido T, et al. Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science. 2002; 298: 843-846.
4. Kousteni S, Bellido T, Plotkin LI, et al. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell. 2001; 104: 719-730.
5. Kousteni S, Han L, Chen JR, et al. Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids. J Clin Invest. 2003; 111: 1651-1664.
6. Manolagas SC., Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000; 21: 115-137.
7. Manolagas SC, Kousteni S, Jilka RL., Sex steroids and bone. Recent Prog Horm Res. 2002; 57: 385-409.
8. Manolagas SC, Kousteni S, Chen JR, Schuller M, Plotkin L, Bellido T., Kinase-mediated transcription, activators of nongenotropic estrogen-like signaling (ANGELS), and osteoporosis: a different perspective on the HRT dilemma. Kidney Int Suppl. 2004; S41-S49.
9. Chen JR, Plotkin LI, Aguirre JI, et al. Transient versus sustained phosphorylation and nuclear accumulation of ERKs underlie anti-versus pro-apoptotic effects of estrogens. J Biol Chem. 2005; 280: 4632-4638.
10. Weihua Z, Andersson S, Cheng G, Simpson ER, Warner M, Gustafsson JA., Update on estrogen signaling. FEBS Lett. 2003; 546: 17-24.
11. Nilsson S, Mäkelä S, Treuter E, et al. Mechanisms of estrogen action. Physiol Rev. 2001; 81: 1535-1565.
12. Wang Z, Zhang X, Shen P, Loggie BW, Chang Y, Deuel TF., Identification, cloning, and expression of human estrogen receptor-alpha36, a novel variant of human estrogen receptor-alpha66. Biochem Biophys Res Commun. 2005; 336: 1023-1027.
13. Wang Z, Zhang X, Shen P, Loggie BW, Chang Y, Deuel TF., A variant of estrogen receptor-{alpha}, hER-{alpha}36: transduction of estrogen- and antiestrogen-dependent membrane-initiated mitogenic signaling. Proc Natl Acad Sci U S A. 2006; 103: 9063-9068.
14. Lee LM, Cao J, Deng H, Chen P, Gatalica Z, Wang ZY., ER-alpha36, a novel variant of ER-alpha, is expressed in ER-positive and -negative human breast carcinomas. Anticancer Res. 2008; 28: 479-483.
15. Lin SL, Yan LY, Liang XW, et al. A novel variant of ER-alpha, ER-alpha36 mediates testosterone-stimulated ERK and Akt activation in endometrial cancer Hec1A cells. Reprod Biol Endocrinol. 2009; 7: 102.
16. Jiang H, Teng R, Wang Q, et al. Transcriptional analysis of estrogen receptor alpha variant mRNAs in colorectal cancers and their matched normal colorectal tissues. J Steroid Biochem Mol Biol. 2008; 112: 20-224.
17. Xu BZ, Lin SL, Li M, et al. Changes in estrogen receptor-alpha variant (ER-alpha36) expression during mouse ovary development and oocyte meiotic maturation. Histochem Cell Biol. 2009; 131: 347-354.
18. Kang L, Zhang X, Xie Y, et al. Involvement of estrogen receptor variant ER-alpha36, not GPR30, in nongenomic estrogen signaling. Mol Endocrinol. 2010; 24: 709-721.
19. Liao EY, Wu XP, Luo XH, et al. Establishment and evaluation of bone mineral density reference databases appropriate for diagnosis and evaluation of osteoporosis in Chinese women. J Bone Miner Metab. 2003; 21: 184-192.
20. Liao EY, Wu XP, Luo XH, et al. Establishment of BMD reference plots and determination of peak BMD at multiple skeletal regions in mainland Chinese women and the diagnosis of osteoporosis. Osteoporos Int. 2004; 15: 71-79.
21. Li H, Xie H, Liu W, et al. A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest. 2009; 119: 3666-3677.
22. Kanis JA, Melton LJ 3rd, Christiansen C, Johnston CC, Khaltaev N., The diagnosis of osteoporosis. J Bone Miner Res. 1994; 9: 1137-1141.
23. Shi L, Dong B, Li Z, et al. Expression of ER-{alpha}36, a novel variant of estrogen receptor {alpha}, and resistance to tamoxifen treatment in breast cancer. J Clin Oncol. 2009; 27: 3423-3429.
24. Owen TA, Aronow M, Shalhoub V, et al. Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol. 1990; 143: 420-430.
25. Chikazu D, Hakeda Y, Ogata N, et al. Fibroblast growth factor (FGF)-2 directly stimulates mature osteoclast function through activation of FGF receptor 1 and p42/p44 MAP kinase. J Biol Chem. 2000; 275: 31444-31450.
26. Luo XH, Guo LJ, Xie H, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res. 2006; 21: 1648-1656.
27. Xie H, Tang SY, Cui RR, et al. Apelin and its receptor are expressed in human osteoblasts. Regul Pept. 2006; 134: 118-125.
28. Weitzmann MN, Pacifici R., Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest. 2006; 116: 1186-1194.
29. Raisz LG., Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J Clin Invest. 2005; 115: 3318-3325.
30. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B., Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc Natl Acad Sci U S A. 2000; 97: 11603-11608.
31. Watson CS, Bulayeva NN, Wozniak AL, Alyea RA., Xenoestrogens are potent activators of nongenomic estrogenic responses. Steroids. 2007; 72: 124-134.
32. Wozniak AL, Bulayeva NN, Watson CS., Xenoestrogens at picomolar to nanomolar concentrations trigger membrane estrogen receptor-α-mediated Ca2+ fluxes and prolactin release in GH3/B6 pituitary tumor cells. Env Health Perspect. 2005; 113: 431-439.
33. Ramos JW., The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells. Int. J. Biochem. Cell Biol. 2008; 40: 2707-2719.
34. Cagnol S, Chambard JC., ERK and cell death: Mechanisms of ERK-induced cell death-apoptosis, autophagy and senescence. FEBS J. 2010; 277: 2-21.
35. Halleen JM, Räisänen SR, Alatalo SL, Väänänen HK., Potential function for the ROS-generating activity of TRACP. J Bone Miner Res. 2003; 18: 1908-1911.
36. Almeida M, Martin-Millan M, Ambrogini E, et al. Estrogens attenuate oxidative stress and the differentiation and apoptosis of osteoblasts by DNA-binding-independent actions of the ERα. J Bone Miner Res. 2010; 25: 769-781.
37. Beck MM, Hansen KK., Role of estrogen in avian osteoporosis. Poult Sci. 2004; 83: 200-206.
38. Zou Y, Ding L, Coleman M, Wang Z., Estrogen receptor-alpha (ER-alpha) suppresses expression of its variant ER-alpha 36. FEBS Lett. 2009; 583: 1368-1374.
39. Hattner R, Epker BN, Frost HM., Suggested sequential mode of control of changes in cell behaviour in adult bone remodelling. Nature. 1965; 206: 489-490.
40. Rapuri PB, Gallagher JC, Haynatzki G., Endogenous levels of serum estradiol and sex hormone binding globulin determine bone mineral density, bone remodeling, the rate of bone loss, and response to treatment with estrogen in elderly women. J Clin Endocrinol Metab. 2004; 89: 4954-4962.
41. Cummings SR, Browner WS, Bauer D, et al. Endogenous hormones and the risk of hip and vertebral fractures among older women. Study of Osteoporotic Fractures Research Group. N Engl J Med. 1998; 339: 733-738.
42. Garnero P, Sornay-Rendu E, Claustrat B, Delmas PD., Biochemical markers of bone turnover, endogenous hormones and the risk of fractures in postmenopausal women: the OFELY study. J Bone Miner Res. 2000; 15: 1526-1536.
43. Slemenda C, Longcope C, Peacock M, Hui S, Johnston CC., Sex steroids, bone mass, and bone loss. A prospective study of pre-, peri-, and postmenopausal women. J Clin Invest. 1996; 97: 14-21.
44. Barrett-Connor E, Mueller JE, von Mühlen DG, Laughlin GA, Schneider DL, Sartoris DJ., Low levels of estradiol are associated with vertebral fractures in older men, but not women: the Rancho Bernardo Study. J Clin Endocrinol Metab. 2000; 85: 219-223.
45. Chapurlat RD, Garnero P, Bréart G, Meunier PJ, Delmas PD., Serum estradiol and sex hormone-binding globulin and the risk of hip fracture in elderly women: the EPIDOS study. J Bone Miner Res. 2000; 15: 1835-1841. (Pubitemid 30666237)
46. Riggs BL, Khosla S, Atkinson EJ, Dunstan CR, Melton LJ 3rd., Evidence that type I osteoporosis results from enhanced responsiveness of bone to estrogen deficiency. Osteoporos Int. 2003; 14: 728-733.
47. Chapurlat RD, Bauer DC, Cummings SR., Association between endogenous hormones and sex hormone-binding globulin and bone turnover in older women: study of osteoporotic fractures. Bone. 2001; 29: 381-387.