A new regulator of osteoclastogenesis: Estrogen response element-binding protein in bone

Journal of Bone and Mineral Research

Volumn 26, Issue 10, 2011, Pages 2537-2547

  Chen, Hong ^a   Gilbert, Linda C ^a   Lu, X ^a   Liu, Zhaofan ^a   You, Shaojin ^a   Weitzmann, M Neale ^a   Nanes, Mark S ^a   Adams, John ^b,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOINT REPLACEMENT INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

bone; estrogen; hnRNP; osteoclast; osteoclastogenesis; RANKL

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; BINDING PROTEIN; CALCITONIN RECEPTOR; CALCITRIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RESPONSIVE ELEMENT BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE TISSUE; CALCIUM ABSORPTION; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; ESTROGEN RESPONSIVE ELEMENT; GENE EXPRESSION; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; LENTIVIRINAE; MONOCYTE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; SPLEEN; STROMA CELL; UPREGULATION;

ANIMALS; BASE SEQUENCE; BONE AND BONES; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; DNA PRIMERS; ESTROGENS; MICE; MICE, INBRED C57BL; OSTEOCLASTS; PROMOTER REGIONS, GENETIC; RANK LIGAND; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 80053210083     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.456     Document Type: Article

References (52)

1. Wronski TJ, Lowry PL, Walsh CC, Ignaszewski LA,. Skeletal alterations in ovariectomized rats. Calcif Tissue Int. 1985; 37 (3): 324-8. (Pubitemid 15034552)
2. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O,. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA. 1993; 90 (23): 11162-6. (Pubitemid 23354389)
3. Bilezikian JP, Morishima A, Bell J, Grumbach MM,. Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med. 1998; 339 (9): 599-603. (Pubitemid 28385657)
4. Couse JF, Korach KS,. Estrogen receptor null mice: what have we learned and where will they lead us ? Endocr Rev. 1999; 20 (3): 358-417. (Pubitemid 30654784)
5. Oursler MJ,. Direct and indirect effects of estrogen on osteoclasts. J Musculoskelet Neuronal Interact. 2003; 3 (4): 363-6; discussion 381. (Pubitemid 38111631)
6. Rosen CJ,. Clinical practice. Postmenopausal osteoporosis. N Engl J Med. 2005; 353 (6): 595-603.
7. Kovacic N, Grcevic D, Katavic V, Lukic IK, Grubisic V, Mihovilovic K, Cvija H, Croucher PI, Marusic A,. Fas receptor is required for estrogen deficiency-induced bone loss in mice. Lab Invest. 2010; 90 (3): 402-13.
8. Martin-Millan M, Almeida M, Ambrogini E, Han L, Zhao H, Weinstein RS, Jilka RL, O'Brien CA, Manolagas SC,. The estrogen receptor-α in osteoclasts mediates the protective effects of estrogens on cancellous but not cortical bone. Mol Endocrinol. 2010; 24 (2): 323-34.
9. Robinson LJ, Yaroslavskiy BB, Griswold RD, Zadorozny EV, Guo L, Tourkova IL, Blair HC,. Estrogen inhibits RANKL-stimulated osteoclastic differentiation of human monocytes through estrogen and RANKL-regulated interaction of estrogen receptor-α with BCAR1 and Traf6. Exp Cell Res. 2009; 315 (7): 1287-301.
10. Krum SA, Miranda-Carboni GA, Hauschka PV, Carroll JS, Lane TF, Freedman LP, Brown M,. Estrogen protects bone by inducing Fas ligand in osteoblasts to regulate osteoclast survival. EMBO J. 2008; 27 (3): 535-45. (Pubitemid 351225684)
11. Nakamura T, Imai Y, Matsumoto T, Sato S, Takeuchi K, Igarashi K, Harada Y, Azuma Y, Krust A, Yamamoto Y, Nishina H, Takeda S, Takayanagi H, Metzger D, Kanno J, Takaoka K, Martin TJ, Chambon P, Kato S,. Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell. 2007; 130 (5): 811-23. (Pubitemid 47332572)
12. Faloni AP, Sasso-Cerri E, Katchburian E, Cerri PS,. Decrease in the number and apoptosis of alveolar bone osteoclasts in estrogen-treated rats. J Periodontal Res. 2007; 42 (3): 193-201.
13. Saintier D, Khanine V, Uzan B, Ea HK, de Vernejoul MC, Cohen-Solal ME,. Estradiol inhibits adhesion and promotes apoptosis in murine osteoclasts in vitro. J Steroid Biochem Mol Biol. 2006; 99 (4-5): 165-73.
14. Kameda T, Mano H, Yuasa T, Mori Y, Miyazawa K, Shiokawa M, Nakamaru Y, Hiroi E, Hiura K, Kameda A, Yang NN, Hakeda Y, Kumegawa M,. Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts. J Exp Med. 1997; 186 (4): 489-95. (Pubitemid 27360793)
15. Kousteni S, Chen JR, Bellido T, Han L, Ali AA, O'Brien CA, Plotkin L, Fu Q, Mancino AT, Wen Y, Vertino AM, Powers CC, Stewart SA, Ebert R, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC,. Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science. 2002; 298 (5594): 843-6. (Pubitemid 35231540)
16. Khosla S, Atkinson EJ, Dunstan CR, O'Fallon WM,. Effect of estrogen versus testosterone on circulating osteoprotegerin and other cytokine levels in normal elderly men. J Clin Endocrinol Metab. 2002; 87 (4): 1550-4. (Pubitemid 34615237)
17. Asagiri M, Takayanagi H,. The molecular understanding of osteoclast differentiation. Bone. 2007; 40 (2): 251-64. (Pubitemid 46054562)
18. Feng X,. RANKing intracellular signaling in osteoclasts. IUBMB Life. 2005; 57 (6): 389-95. (Pubitemid 41073120)
19. Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, Capparelli C, Scully S, Tan HL, Xu W, Lacey DL, Boyle WJ, Simonet WS,. osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 1998; 12 (9): 1260-8. (Pubitemid 28213402)
20. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ,. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998; 93 (2): 165-76. (Pubitemid 28180851)
21. Lee SK, Lorenzo JA,. Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology. 1999; 140 (8): 3552-61. (Pubitemid 30645409)
22. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan HL, Trail G, Sullivan J, Davy E, Bucay N, Renshaw-Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Lee R, Boyle WJ,. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997; 89 (2): 309-19. (Pubitemid 27199902)
23. Vandenput L, Ohlsson C,. Sex steroid metabolism in the regulation of bone health in men. J Steroid Biochem Mol Biol. 2010.
24. Chen H, Arbelle JE, Gacad MA, Allegretto EA, Adams JS,. Vitamin D and gonadal steroid-resistant New World primate cells express an intracellular protein which competes with the estrogen receptor for binding to the estrogen response element. J Clin Invest. 1997; 99 (4): 669-75. (Pubitemid 27097668)
25. Chen H, Hu B, Gacad MA, Adams JS,. Cloning and expression of a novel dominant-negative-acting estrogen response element-binding protein in the heterogeneous nuclear ribonucleoprotein family. J Biol Chem. 1998; 273 (47): 31352-7. (Pubitemid 28533152)
26. Chen H, Hewison M, Hu B, Adams JS,. Heterogeneous nuclear ribonucleoprotein (hnRNP) binding to hormone response elements: a cause of vitamin D resistance. Proc Natl Acad Sci USA. 2003; 100 (10): 6109-14. (Pubitemid 36576939)
27. Chen H, Hu B, Allegretto EA, Adams JS,. The vitamin D response element-binding protein. A novel dominant-negative regulator of vitamin D-directed transactivation. J Biol Chem. 2000; 275 (45): 35557-64.
28. Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG,. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 1993; 62: 289-321. (Pubitemid 23237873)
29. Lynch M, Chen L, Ravitz MJ, Mehtani S, Korenblat K, Pazin MJ, Schmidt EV,. hnRNP K binds a core polypyrimidine element in the eukaryotic translation initiation factor 4E (eIF4E) promoter, and its regulation of eIF4E contributes to neoplastic transformation. Mol Cell Biol. 2005; 25 (15): 6436-53. (Pubitemid 41023220)
30. Okunola HL, Krainer AR,. Cooperative-binding and splicing-repressive properties of hnRNP A1. Mol Cell Biol. 2009; 29 (20): 5620-31.
31. Heiner M, Hui J, Schreiner S, Hung LH, Bindereif A,. HnRNP L-mediated regulation of mammalian alternative splicing by interference with splice site recognition. RNA Biol. 2010; 7 (1).
32. Chen H, Stuart W, Hu B, Nguyen L, Huang G, Clemens TL, Adams JS,. Creation of estrogen resistance in vivo by transgenic overexpression of the heterogeneous nuclear ribonucleoprotein-related estrogen response element binding protein. Endocrinology. 2005; 146 (10): 4266-73. (Pubitemid 41324022)
33. Chen H, Clemens TL, Hewison M, Adams JS,. Estradiol and tamoxifen mediate rescue of the dominant-negative effects of estrogen response element-binding protein in vivo and in vitro. Endocrinology. 2009; 150 (5): 2429-35.
34. Chen H, Hewison M, Adams JS,. Control of estradiol-directed gene transactivation by an intracellular estrogen-binding protein and an estrogen response element-binding protein. Mol Endocrinol. 2008; 22 (3): 559-69. (Pubitemid 351397785)
35. O'Brien CA, Kern B, Gubrij I, Karsenty G, Manolagas SC,. Cbfa1 does not regulate RANKL gene activity in stromal/osteoblastic cells. Bone. 2002; 30 (3): 453-62. (Pubitemid 34204119)
36. Feng X,. Regulatory roles and molecular signaling of TNF family members in osteoclasts. Gene. 2005; 350 (1): 1-13.
37. Park H, Jung YK, Park OJ, Lee YJ, Choi JY, Choi Y,. Interaction of Fas ligand and Fas expressed on osteoclast precursors increases osteoclastogenesis. J Immunol. 2005; 175 (11): 7193-201. (Pubitemid 41713413)
38. Roux S, Lambert-Comeau P, Saint-Pierre C, Lepine M, Sawan B, Parent JL,. Death receptors, Fas and TRAIL receptors, are involved in human osteoclast apoptosis. Biochem Biophys Res Commun. 2005; 333 (1): 42-50. (Pubitemid 40813444)
39. Wu X, Pan G, McKenna MA, Zayzafoon M, Xiong WC, McDonald JM,. RANKL regulates Fas expression and Fas-mediated apoptosis in osteoclasts. J Bone Miner Res. 2005; 20 (1): 107-16. (Pubitemid 41716225)
40. Chen JR, Plotkin LI, Aguirre JI, Han L, Jilka RL, Kousteni S, Bellido T, Manolagas SC,. Transient versus sustained phosphorylation and nuclear accumulation of ERKs underlie anti-versus pro-apoptotic effects of estrogens. J Biol Chem. 2005; 280 (6): 4632-8. (Pubitemid 40288632)
41. Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC,. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell. 2001; 104 (5): 719-30. (Pubitemid 32241022)
42. Rubio MF, Werbajh S, Cafferata EG, Quaglino A, Colo GP, Nojek IM, Kordon EC, Nahmod VE, Costas MA,. TNF-α enhances estrogen-induced cell proliferation of estrogen-dependent breast tumor cells through a complex containing nuclear factor-κB. Oncogene. 2006; 25 (9): 1367-77. (Pubitemid 43336465)
43. Ikeda F, Matsubara T, Tsurukai T, Hata K, Nishimura R, Yoneda T,. JNK/c-Jun signaling mediates an anti-apoptotic effect of RANKL in osteoclasts. J Bone Miner Res. 2008; 23 (6): 907-14. (Pubitemid 351768809)
44. Rimondi E, Zweyer M, Ricci E, Fadda R, Secchiero P,. Receptor activator of nuclear factor kappa B ligand (RANKL) modulates the expression of genes involved in apoptosis and cell cycle in human osteoclasts. Anat Rec (Hoboken). 2007; 290 (7): 838-45.
45. Liu W, Wang S, Wei S, Sun L, Feng X,. Receptor activator of NF-κB (RANK) cytoplasmic motif, 369PFQEP373, plays a predominant role in osteoclast survival in part by activating Akt/PKB and its downstream effector AFX/FOXO4. J Biol Chem. 2005; 280 (52): 43064-72. (Pubitemid 43049272)
46. Glantschnig H, Fisher JE, Wesolowski G, Rodan GA, Reszka AA,. M-CSF, TNFα and RANK ligand promote osteoclast survival by signaling through mTOR/S6 kinase. Cell Death Differ. 2003; 10 (10): 1165-77. (Pubitemid 37258582)
47. Chamoux E, Houde N, L'Eriger K, Roux S,. Osteoprotegerin decreases human osteoclast apoptosis by inhibiting the TRAIL pathway. J Cell Physiol. 2008; 216 (2): 536-42. (Pubitemid 351898482)
48. Vitovski S, Phillips JS, Sayers J, Croucher PI,. Investigating the interaction between osteoprotegerin and receptor activator of NF-κB or tumor necrosis factor-related apoptosis-inducing ligand: evidence for a pivotal role for osteoprotegerin in regulating two distinct pathways. J Biol Chem. 2007; 282 (43): 31601-9. (Pubitemid 350044899)
49. Clowes JA, Eghbali-Fatourechi GZ, McCready L, Oursler MJ, Khosla S, Riggs BL,. Estrogen action on bone marrow osteoclast lineage cells of postmenopausal women in vivo. Osteoporos Int. 2009; 20 (5): 761-9.
50. Syed F, Khosla S,. Mechanisms of sex steroid effects on bone. Biochem Biophys Res Commun. 2005; 328 (3): 688-96. (Pubitemid 40214350)
51. Cauley JA, Ewing SK, Taylor BC, Fink HA, Ensrud KE, Bauer DC, Barrett-Connor E, Marshall L, Orwoll ES,. Sex steroid hormones in older men: longitudinal associations with 4.5-year change in hip bone mineral density: the Osteoporotic Fractures In Men Study. J Clin Endocrinol Metab. 2010; 95 (9): 4314-23.
52. Manavathi B, Kumar R,. Steering estrogen signals from the plasma membrane to the nucleus: two sides of the coin. J Cell Physiol. 2006; 207 (3): 594-604. (Pubitemid 43670418)