The effect of estrogen on bone requires ERα in nonhematopoietic cells but is enhanced by ERα in hematopoietic cells

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 7, 2014, Pages E589-E595

  Henning, Petra ^a   Ohlsson, Claes ^a   Engdahl, Cecilia ^a   Farman, Helen ^a   Windahl, Sara H ^a   Carlsten, Hans ^a,b   Lagerquist, Marie K ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Bone marrow transplantation; Cortical bone; Estrogen; Estrogen receptor ; Trabecular bone

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE DENSITY; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; BONE MASS; BONE METABOLISM; CONTROLLED STUDY; CORTICAL BONE; ESTROGEN THERAPY; FAT MASS; FEMALE; HEMATOPOIETIC CELL; LYMPHOPOIESIS; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; OSTEOCLAST; OVARIECTOMY; PROTEIN EXPRESSION; TRABECULAR BONE; ANIMAL; BONE; CHIMERA; DRUG EFFECTS; KNOCKOUT MOUSE; OSTEOBLAST; PHYSIOLOGY;

ANIMALS; BONE AND BONES; BONE DENSITY; BONE MARROW TRANSPLANTATION; CHIMERA; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; MICE; MICE, KNOCKOUT; OSTEOBLASTS; OSTEOCLASTS; OVARIECTOMY;

EID: 84907795438     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00255.2014     Document Type: Article

References (32)

1. Almeida M, IyERα S, Martin-Millan M, Bartell SM, Han L, Ambrogini E, Onal M, Xiong J, Weinstein RS, Jilka RL, O’Brien CA, Manolagas SC. Estrogen receptor-alpha signaling in osteoblast progenitors stimulates cortical bone accrual. J Clin Invest 123: 394-404, 2013.
2. Börjesson AE, Windahl SH, Lagerquist MK, Engdahl C, Frenkel B, Movérare-Skrtic S, Sjögren K, Kindblom JM, Stubelius A, IslandERα U, Antal MC, Krust A, Chambon P, Ohlsson C. Roles of transactivating functions 1 and 2 of estrogen receptor-alpha in bone. Proc Natl Acad Sci USA 108: 6288-6293, 2011.
3. DempstERα DW, Compston JE, DreznERα MK, Glorieux FH, Kanis, JA, Malluche H, MeuniERα PJ, Ott SM, ReckERα RR, Parfitt AM. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone MinERα Res 28: 2-17, 2013.
4. Dupont S, Krust A, GansmullERα A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127: 4277-4291, 2000.
5. Eriksen E, Axelrod D, Melsen F. Bone Histomorphometry. New York: Raven, 1994
6. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS. Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc Natl Acad Sci USA 97: 12729-12734, 2000.
7. Horn Y, Price DC. The effect of androgens on erythroid and granulocytic marrow recovery in the irradiated rat. Acta Haematol 48: 300-306, 1972.
8. Ikeda K, Tsukui T, Horie-Inoue K, Inoue S. Conditional expression of constitutively active estrogen receptor alpha in osteoblasts increases bone mineral density in mice. FEBS Lett 585: 1303-1309, 2011.
9. Key TJ, Pike MC. The dose-effect relationship between ‘unopposed’ oestrogens and endometrial mitotic rate: its central role in explaining and predicting endometrial cancERα risk. Br J CancERα 57: 205-212, 1988.
10. Khosla S, Melton LJ III, Atkinson EJ, O’Fallon WM. Relationship of serum sex steroid levels to longitudinal changes in bone density in young versus elderly men. J Clin Endocrinol Metab 86: 3555-3561, 2001.
11. Khosla S, Melton LJ III, Riggs BL. The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone MinERα Res 26: 441-451, 2011.
12. Khosla S, OurslERα MJ, Monroe DG. Estrogen and the skeleton. Trends Endocrinol Metab 23: 576-581, 2012.
13. 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 27: 535-545, 2008.
14. Lindberg MK, Alatalo SL, Halleen JM, Mohan S, Gustafsson JA, Ohlsson C. Estrogen receptor specificity in the regulation of the skeleton in female mice. J Endocrinol 171: 229-236, 2001.
15. Lubahn DB, MoyERα JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development aftERα insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90: 11162-11166, 1993.
16. Maatta JA, Buki KG, Gu G, Alanne MH, Vaaraniemi J, Liljenback H, Poutanen M, Harkonen P, Vaananen K. Inactivation of estrogen receptor alpha in bone-forming cells induces bone loss in female mice. FASEB J 27: 478-488, 2013.
17. Martin-Millan M, Almeida M, Ambrogini E, Han L, Zhao H, Weinstein RS, Jilka RL, O’Brien CA, Manolagas SC. The estrogen receptoralpha in osteoclasts mediates the protective effects of estrogens on cancellous but not cortical bone. Mol Endocrinol 24: 323-334, 2010.
18. Masuzawa T, Miyaura C, Onoe Y, Kusano K, Ohta H, Nozawa S, Suda T. Estrogen deficiency stimulates B lymphopoiesis in mouse bone marrow. J Clin Invest 94: 1090-1097, 1994.
19. Mellström D, Vandenput L, Mallmin H, Holmberg AH, Lorentzon M, Odén A, Johansson H, Orwoll ES, Labrie F, Karlsson MK, Ljunggren O, Ohlsson C. OldERα men with low serum estradiol and high serum SHBG have an increased risk of fractures. J Bone MinERα Res 23: 1552-1560, 2008.
20. Melville KM, Kelly NH, Khan SA, Schimenti JC, Ross FP, Main RP, van dERα Meulen MC. Female mice lacking estrogen receptor-alpha in osteoblasts have compromised bone mass and strength. J Bone MinERα Res 29: 370-379, 2014.
21. 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, MetzgERα 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 130: 811-823, 2007.
22. Ohlsson C, Hellberg N, Parini P, Vidal O, Bohlooly YM, Rudling M, Lindberg MK, WarnERα M, Angelin B, Gustafsson JA. Obesity and disturbed lipoprotein profile in estrogen receptor-alpha-deficient male mice. Biochem Biophys Res Commun 278: 640-645, 2000.
23. Ribas V, Drew BG, Le JA, Soleymani T, Daraei P, Sitz D, Mohammad L, Henstridge DC, Febbraio MA, Hewitt SC, Korach KS, BensingERα SJ, HevenERα AL. Myeloid-specific estrogen receptor alpha deficiency impairs metabolic homeostasis and accelerates atherosclerotic lesion development. Proc Natl Acad Sci USA 108: 16457-16462, 2011.
24. Seitz S, KellERα J, Schilling AF, Jeschke A, Marshall RP, Stride BD, Wintermantel T, Beil FT, Amling M, Schutz G, Tuckermann J, Schinke T. Pharmacological estrogen administration causes a FSH-independent osteo-anabolic effect requiring ERα alpha in osteoblasts. PLoS One 7: e50301, 2012.
25. Sims NA, Clement-Lacroix P, Minet D, Fraslon-Vanhulle C, Gaillard-Kelly M, Resche-Rigon M, Baron R. A functional androgen receptor is not sufficient to allow estradiol to protect bone aftERα gonadectomy in estradiol receptor-deficient mice. J Clin Invest 111: 1319-1327, 2003.
26. Thompson JS, Simmons EL, Crawford MK, Severson CD. Studies on the mechanisms of estradiol-induced radioprotection. Radiat Res 40: 70-84, 1969.
27. Thurmond TS, Murante FG, Staples JE, Silverstone AE, Korach KS, Gasiewicz TA. Role of estrogen receptor alpha in hematopoietic stem cell development and B lymphocyte maturation in the male mouse. Endocrinology 141: 2309-2318, 2000.
28. Vandenput L, Ohlsson C. Estrogens as regulators of bone health in men. Nat Rev Endocrinol 5: 437-443, 2009.
29. Vanderschueren D, Vandenput L, Boonen S, Lindberg MK, Bouillon R, Ohlsson C. Androgens and bone. Endocr Rev 25: 389-425, 2004.
30. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
31. Windahl SH, Börjesson AE, Farman HH, Engdahl C, Movérare-Skrtic S, Sjögren K, Lagerquist MK, Kindblom JM, Koskela A, Tuukkanen J, Divieti Pajevic P, Feng JQ, Dahlman-Wright K, Antonson P, Gustafsson JÅ, Ohlsson C. Estrogen receptorin osteocytes is important for trabecular bone formation in male mice. Proc Natl Acad Sci USA 110: 2294-2299, 2013.
32. Xu Y, Nedungadi TP, Zhu L, Sobhani N, Irani BG, Davis KE, Zhang X, Zou F, Gent LM, HahnERα LD, Khan SA, Elias CF, Elmquist JK, Clegg DJ. Distinct hypothalamic neurons mediate estrogenic effects on energy homeostasis and reproduction. Cell Metab 14: 453-465, 2011.