The Phytoestrogen Genistein Enhances Osteogenesis and Represses Adipogenic Differentiation of Human Primary Bone Marrow Stromal Cells

Endocrinology

Volumn 145, Issue 2, 2004, Pages 848-859

  Heim, M ^a,b   Frank, O ^c   Kampmann, G ^a   Sochocky, N ^a   Pennimpede, T ^a   Fuchs, P ^a   Hunziker, W ^a   Weber, P ^a   Martin, I ^c   Bendik, I ^a  

^a F HOFFMANN LA ROCHE LTD   (Switzerland)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPSIN; ALKALINE PHOSPHATASE; AROMATASE; CCAAT ENHANCER BINDING PROTEIN ALPHA; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FAT DROPLET; GENISTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPROTEIN LIPASE; MESSENGER RNA; OSTEOPROTEGERIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHYTOESTROGEN; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; ARTICLE; AUTOCRINE EFFECT; BONE DEVELOPMENT; BONE MARROW CELL; CELL COUNT; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HORMONE ACTION; HUMAN; HUMAN CELL; MARKER GENE; OSTEOBLAST; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEM CELL; STROMA CELL; UPREGULATION;

ADIPOCYTES; ALKALINE PHOSPHATASE; BONE MARROW CELLS; CARRIER PROTEINS; CELL COUNT; CELL DIFFERENTIATION; COMPLEMENT FACTOR D; ESTRADIOL; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENISTEIN; GLYCOPROTEINS; HUMANS; KINETICS; LIPOPROTEIN LIPASE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; OSTEOBLASTS; OSTEOGENESIS; OSTEOPONTIN; OSTEOPROTEGERIN; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, ESTROGEN; RECEPTORS, TUMOR NECROSIS FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SIALIC ACIDS; SIALOGLYCOPROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; STROMAL CELLS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 10744224568     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2003-1014     Document Type: Article

References (56)

1. Gruber CJ, Tschugguel W, Schneeberger C, Huber JC 2002 Production and actions of estrogens. N Engl J Med 346:340-352
2. Hall JM, Couse JF, Korach KS 2001 The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 276:36869-36872
3. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA 1997 Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 138: 863-870
4. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA 1998 Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139:4252-4263
5. Compston JE 2001 Sex steroids and bone. Physiol Rev 81:419-447
6. Spelsberg TC, Subramaniam M, Riggs BL, Khosla S 1999 The actions and interactions of sex steroids and growth factors/cytokines on the skeleton. Mol Endocrinol 13:819-828
7. Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T, Kassem M 2001 Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology 2:165-171
8. Gambacciani M, Ciaponi M, Cappagli B, Piaggesi L, De Simone L, Orlandi R, Genazzani AR 1997 Body weight, body fat distribution, and hormonal replacement therapy in early postmenopausal women. J Clin Endocrinol Metab 82:414-417
9. Park SR, Oreffo RO, Triffitt JT 1999 Interconversion potential of cloned human marrow adipocytes in vitro. Bone 24:549-554
10. Nuttall ME, Patton AJ, Olivera DL, Nadeau DP, Gowen M 1998 Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: implications for osteopenic disorders. J Bone Miner Res 13:371-382
11. Jones ME, Thorburn AW, Britt KL, Hewitt KN, Wreford NG, Proietto J, Oz OK, Leury BJ, Robertson KM, Yao S, Simpson ER 2000 Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. Proc Natl Acad Sci USA 97:12735-12740
12. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS 2000 Increased adipose tissue in male and female estrogen receptor-α knockout mice. Proc Natl Acad Sci USA 97:12729-12734
13. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T 1997 Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764
14. Rosen ED, Spiegelman BM 2000 Molecular regulation of adipogenesis. Annu Rev Cell Dev Biol 16:145-171
15. Rosen ED, Hsu CH, Wang X, Sakai S, Freeman MW, Gonzalez FJ, Spiegelman BM 2002 C/EBPα induces adipogenesis through PPARá: a unified pathway. Genes Dev 16:22-26
16. Szkudelska K, Nogowski L, Szkudelski T 2000 Genistein affects lipogenesis and lipolysis in isolated rat adipocytes. J Steroid Biochem Mol Biol 75:265-271
17. Dang ZC, van Bezooijen RL, Karperien M, Papapoulos SE, Lowik CW 2002 Exposure of KS483 cells to estrogen enhances osteogenesis and inhibits adipogenesis. J Bone Miner Res 17:394-405
18. Okazaki R, Inoue D, Shibata M, Saika M, Kido S, Ooka H, Tomiyama H, Sakamoto Y, Matsumoto T 2002 Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) α or â. Endocrinology 143:2349-2356
19. Harmon AW, Patel YM, Harp JB 2002 Genistein inhibits CCAAT/enhancer- binding protein β (C/EBPβ) activity and 3T3-L1 adipogenesis by increasing C/EBP homologous protein expression. Biochem J 367:203-208
20. Bianco P, Gehron Robey P 2000 Marrow stromal stem cells. J Clin Invest 105:1663-1668
21. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR 1999 Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147
22. Frank O, Heim M, Jakob M, Barbero A, Schafer D, Bendik I, Dick W, Heberer M, Martin I 2002 Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J Cell Biochem 85:737-746
23. Heim M, Johnson J, Boess F, Bendik I, Weber P, Hunziker W, Fluhmann B 2002 Phytanic acid, a natural peroxisome proliferator-activated receptor (PPAR) agonist, regulates glucose metabolism in rat primary hepatocytes. FASEB J 16:718-720
24. Muraglia A, Cancedda R, Quarto R 2000 Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 113:1161-1166
25. Moore JT, McKee DD, Slentz-Kesler K, Moore LB, Jones SA, Horne EL, Su JL, Kliewer SA, Lehmann JM, Willson TM 1998 Cloning and characterization of human estrogen receptor beta isoforms. Biochem Biophys Res Commun 247:75-78
26. Ogawa S, Inoue S, Watanabe T, Orimo A, Hosoi T, Ouchi Y, Muramatsu M 1998 Molecular cloning and characterization of human estrogen receptor âcx: a potential inhibitor of estrogen action in human. Nucleic Acids Res 26:3505-3512
27. Arts J, Kuiper GG, Janssen JM, Gustafsson JA, Lowik CW, Pols HA, van Leeuwen JP 1997 Differential expression of estrogen receptors α and â mRNA during differentiation of human osteoblast SV-HFO cells. Endocrinology 138: 5067-5070
28. Crandall DL, Busler DE, Novak TJ, Weber RV, Kral JG 1998 Identification of estrogen receptor β RNA in human breast and abdominal subcutaneous adipose tissue. Biochem Biophys Res Commun 248:523-526
29. Mizutani T, Nishikawa Y, Adachi H, Enomoto T, Ikegami H, Kurachi H, Nomura T, Miyake A 1994 Identification of estrogen receptor in human adipose tissue and adipocytes. J Clin Endocrinol Metab 78:950-954
30. Jones ME, Thorburn AW, Britt KL, Hewitt KN, Misso ML, Wreford NG, Proietto J, Oz OK, Leury BJ, Robertson KM, Yao S, Simpson ER 2001 Aromatase-deficient (ArKO) mice accumulate excess adipose tissue. J Steroid Biochem Mol Biol 79:3-9
31. Simpson ER, Davis SR 2001 Minireview: aromatase and the regulation of estrogen biosynthesis-some new perspectives. Endocrinology 142:4589-9454
32. Simpson ER, Clyne C, Speed C, Rubin G, Bulun S 2001 Tissue-specific estrogen biosynthesis and metabolism. Ann NY Acad Sci 949:58-67
33. Mahendroo MS, Mendelson CR, Simpson ER 1993 Tissue-specific and hormonally controlled alternative promoters regulate aromatase cytochrome P450 gene expression in human adipose tissue. J Biol Chem 268:19463-19470
34. Sasano H, Uzuki M, Sawai T, Nagura H, Matsunaga G, Kashimoto O, Harada N 1997 Aromatase in human bone tissue. J Bone Miner Res 12:1416-1423
35. Shozu M, Simpson ER 1998 Aromatase expression of human osteoblast-like cells. Mol Cell Endocrinol 139:117-129
36. Price TM, O'Brien SN 1993 Determination of estrogen receptor messenger ribonucleic acid (mRNA) and cytochrome P450 aromatase mRNA levels in adipocytes and adipose stromal cells by competitive polymerase chain reaction amplification. J Clin Endocrinol Metab 77:1041-1045
37. Rubin GL, Zhao Y, Kalus AM, Simpson ER 2000 Peroxisome proliferator-activated receptor gamma ligands inhibit estrogen biosynthesis in human breast adipose tissue: possible implications for breast cancer therapy. Cancer Res 60:1604-1608
38. Lecka-Czernik B, Gubrij I, Moerman EJ, Kajkenova O, Lipschitz DA, Manolagas SC, Jilka RL 1999 Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPARγ2. J Cell Biochem 74:357-371
39. 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 1998 Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176
40. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G, Itie A, Khoo W, Wakeham A, Dunstan CR, Lacey DL, Mak TW, Boyle WJ, Penninger JM 1999 OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397:315-323
41. Gori F, Hofbauer LC, Dunstan CR, Spelsberg TC, Khosla S, Riggs BL 2000 The expression of osteoprotegerin and RANK ligand and the support of osteoclast formation by stromal-osteoblast lineage cells is developmentally regulated. Endocrinology 141:4768-4776
42. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Spelsberg TC, Riggs BL 1999 Estrogen stimulates gene expression and protein production of osteoprotegerin in human osteoblastic cells. Endocrinology 140:4367-4370
43. Viereck V, Grundker C, Blaschke S, Siggelkow H, Emons G, Hofbauer LC 2002 Phytoestrogen genistein stimulates the production of osteoprotegerin by human trabecular osteoblasts. J Cell Biochem 84:725-735
44. Dang ZC, Audinot V, Papapoulos SE, Boutin JA, Lowik CW 2003 Peroxisome proliferator-activated receptor γ (PPARγ) as a molecular target for the soy phytoestrogen genistein. J Biol Chem 278:962-967
45. Ignotz RA, Massague J 1985 Type å transforming growth factor controls the adipogenic differentiation of 3T3 fibroblasts. Proc Natl Acad Sci USA 82:8530-8534
46. Centrella M, Horowitz MC, Wozney JM, McCarthy TL 1994 Transforming growth factor-β gene family members and bone. Endocr Rev 15:27-39
47. Finkelman RD, Bell NH, Strong DD, Demers LM, Baylink DJ 1992 Ovariectomy selectively reduces the concentration of transforming growth factor â in rat bone: implications for estrogen deficiency-associated bone loss. Proc Natl Acad Sci USA 89:12190-12193
48. Hughes DE, Dai A, Tiffee JC, Li HH, Mundy GR, Boyce BF 1996 Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-β. Nat Med 2:1132-1136
49. Harmon AW, Harp JB 2001 Differential effects of flavonoids on 3T3-L1 adipogenesis and lipolysis. Am J Physiol Cell Physiol 280:C807-C813
50. Massague J 1996 TGFâ signaling: receptors, transducers, and Mad proteins. Cell 85:947-950
51. Choy L, Skillington J, Derynck R 2000 Roles of autocrine TGF-β receptor and Smad signaling in adipocyte differentiation. J Cell Biol 149:667-682
52. Massague J, Chen YG 2000 Controlling TGF-β signaling. Genes Dev 14:627-644
53. Han J, Hajjar DP, Tauras JM, Feng J, Gotto Jr AM, Nicholson AC 2000 Transforming growth factor-β1 (TGF-β1) and TGF-β2 decrease expression of CD36, the type B scavenger receptor, through mitogen-activated protein kinase phosphorylation of peroxisome proliferator-activated receptor-γ. J Biol Chem 275:1241-1246
54. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR, Pittenger MF 2000 Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275:9645-9652
55. 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 2001 Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719-770
56. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y 1987 Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262:5592-5595