Quercetin, a flavonoid, inhibits proliferation and increases osteogenic differentiation in human adipose stromal cells

Biochemical Pharmacology

Volumn 72, Issue 10, 2006, Pages 1268-1278

  Kim, Yeon Jeong ^a,b   Bae, Yong Chan ^a   Suh, Kuen Taek ^a   Jung, Jin Sup ^a,b  

^a Pusan National University School of Medicine   (South Korea)

^b Pusan National University   (South Korea)

Author keywords

Bone regeneration; ERK; Human adipose stromal cells; Osteogenic differentiation; Proliferation; Quercetin

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; CHRYSIN; ESTROGEN RECEPTOR; FLAVONOID; FULVESTRANT; KAEMPFEROL; OSTEOPONTIN; QUERCETIN; TRANSCRIPTION FACTOR RUNX2;

ADIPOSE TISSUE CELL; ARTICLE; BONE REGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKULL DEFECT; STROMA CELL; TISSUE ENGINEERING;

ADIPOCYTES; ANIMALS; BONE REGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION; HUMANS; MICE; MICE, NUDE; OSTEOGENESIS; OSTEOPONTIN; QUERCETIN; SKULL; STROMAL CELLS;

EID: 33750028804     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2006.08.021     Document Type: Article

References (56)

1. Beresford J.N., Bennett J.H., Devlin C., Leboy P.S., and Owen M.E. Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102 (1992) 341-351
2. Caplan A.I. Mesenchymal stem cells. J Orthop Res 9 (1991) 641-650
3. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999) 143-147
4. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7 (2001) 211-227
5. Banfi A., Muraglia A., Dozin B., Mastrogiacomo M., Cancedda R., and Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp Hematol 28 (2000) 707-715
6. Lieberman J.R., Ghivizzani S.C., and Evans C.H. Gene transfer approaches to the healing of bone and cartilage. Mol Ther 6 (2002) 141-147
7. Arjmandi B.H., Alekel L., Hollis B.W., Amin D., Stacewicz-Sapuntzakis M., Guo P., et al. Dietary soybean protein prevents bone loss in an ovariectomized rat model of osteoporosis. J Nutr 126 (1996) 161-167
8. Arjmandi B.H., Birnbaum R., Goyal N.V., Getlinger M.J., Juma S., Alekel L., et al. Bone-sparing effect of soy protein in ovarian-hormone-deficient rats is related to its isoflavone content. Am J Clin Nutr 68 Suppl. (1998) 1364S-1368S
9. Morabito N., Crisafulli A., Vergara C., Gaudio A., Lasco A., Frisina N., et al. Effects of genistein and hormone-replacement therapy on bone loss in early postmenopausal women: a randomized double-blind placebo-controlled study. J Bone Miner Res 10 (2002) 1904-1912
10. Ross P.D., Norimatsu H., Davis J.W., Yano K., Wasnich R.D., Fujiwara S., et al. A comparison of hip fracture incidence among native Japanese, Japanese Americans, and American Caucasians. Am J Epidemiol 133 (1991) 801-809
11. Fujita T., and Fukase M. Comparison of osteoporosis and calcium intake between Japan and the United States. Proc Soc Exp Biol Med 200 (1992) 149-152
12. Horcajada-Molteni M.N., Crespy V., Coxam V., Davicco M.J., Remesy C., and Barlet J.P. Rutin inhibits ovariectomy-induced osteopenia in rats. J Bone Miner Res 15 (2000) 2251-2258
13. Price K.R., and Rhodes M.J.C. Analysis of the major flavonol glycosides present in four varieties of onion (Allium cepa) and changes in composition resulting from autolysis. J Sci Food Agric 74 (1997) 331-339
14. Tamura G., Gold C., Fezz-Luzi A., and Ames B.N. Fecalase: a model for activation of dietary glycosides to mutagens by intestinal flora. Proc Natl Acad Sci USA 77 (1999) 4961-4965
15. Wattel A., Kamel S., Mentaverri R., Lorget F., Prouillet C., Petit J.P., et al. Potent inhibitory effect of naturally occurring flavonoids quercetin and kaempferol on in vitro osteoclastic bone resorption. Biochem Pharmacol 65 (2003) 34-42
16. Notoya M., Tsukamoto Y., Nishimura H., Woo J.T., Nagai K., Lee I.S., et al. Quercetin a flavonoid, inhibits the proliferation, differentiation, and mineralization of osteoblasts in vitro. Eur J Pharmacol 485 1-3 (2004) 89-96
17. Woo J.T., Nakagawa H., Notoya M., Yonezawa T., Udagawa N., Lee I.S., et al. Quercetin suppresses bone resorption by inhibiting the differentiation and activation of osteoclasts. Biol Pharm Bull 27 4 (2004) 504-509
18. Prouillet C., Maziere J.C., Maziere C., Wattel A., Brazier M., and Kamel S. Stimulatory effect of naturally occurring flavonols quercetin and kaempferol on alkaline phosphatase activity in MG-63 human osteoblasts through ERK and estrogen receptor pathway. Biochem Pharmacol 67 7 (2004) 1307-1313 PMID
19. Miyake M., Arai N., Ushio S., Iwaki K., Ikeda M., and Kurimoto M. Promoting effect of kaempferol on the differentiation and mineralization of murine pre-osteoblastic cell line MC3T3-E1. Biosci Biotechnol Biochem 67 (2003) 1199-1205
20. Gimble J.M., and Guilak F. Differentiation potential of adipose derived adult stem (ADAS) cells. Curr Top Dev Biol 58 (2003) 137-160
21. Cho H.H., Park H.T., Kim Y.J., Bae Y.C., Suh K.T., and Jung J.S. Induction of osteogenic differentiation of human mesenchymal stem cells by histone deacetylase inhibitors. J Cell Biochem 96 3 (2005) 533-542
22. Lee R.H., Kim B., Choi I., Kim H., Choi H.S., Suh K., et al. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 14 4-6 (2004) 311-324
23. Lai C.F., Chaudhary L., Fausto A., Halstead L.R., Ory D.S., Avioli L.V., et al. Erk is essential for growth, differentiation, integrin expression, and cell function in human osteoblastic cells. J Biol Chem 276 (2001) 14443-14450
24. Duncia J.V., Santella III J.B., Higley C.A., Pitts W.J., Wityak J., Frietze W.E., et al. MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg Med Chem Lett 8 (1998) 2839-2844
25. Favata M.F., Horiuchi K.Y., Manos E.J., Daulerio A.J., Stradley D.A., Feeser W.S., et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273 29 (1998) 18623-18632
26. DeSilva D.R., Jones E.A., Favata M.F., Jaffee B.D., Magolda R.L., Trzaskos J.M., et al. Inhibition of mitogen-activated protein kinase kinase blocks T cell proliferation but does not induce or prevent anergy. J Immunol 160 9 (1998) 4175-4181
27. Tolwinski N.S., Shapiro P.S., Goueli S., and Ahn N.G. Nuclear localization of mitogen-activated protein kinase kinase 1 (MKK1) is promoted by serum stimulation and G2-M progression. Requirement for phosphorylation at the activation lip and signaling downstream of MKK. J Biol Chem 274 10 (1999) 6168-6174
28. Li C., Kraemer F.B., Ahlborn T.E., and Liu J. Induction of low density lipoprotein receptor (LDLR) transcription by oncostatin M is mediated by the extracellular signal-regulated kinase signaling pathway and the repeat 3 element of the LDLR promoter. J Biol Chem 274 10 (1999) 6747-6753
29. Virgili F., Acconcia F., Ambra R., Rinna A., Totta P., and Marino M. Nutritional flavonoids modulate estrogen receptor alpha signaling. IUBMB Life 56 3 (2004) 145-151
30. Wakeling A.E., Dukes M., and Bowler J. A potent specific pure antiestrogen with clinical potential. Cancer Res 51 (1991) 3867-3873
31. Jordan V.C. Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 2. Clinical considerations and new agents. J Med Chem 46 7 (2003) 1081-1111
32. Xiao Y., Qian H., Young W.G., and Bartold P.M. Tissue engineering for bone regeneration using differentiated alveolar bone cells in collagen scaffolds. Tissue Eng 9 6 (2003) 1167-1177
33. Karsenty G. Transcriptional control of osteoblast differentiation. Endocrinology 142 (2001) 2731-2733
34. Diefenderfer D.L., Osyczka A.M., Garino J.P., and Leboy P.S. Regulation of BMP-induced transcription in cultured human bone marrow stromal cells. J Bone Joint Surg Am 85-A Suppl. 3 (2003) 19-28
35. Dragoo J.L., Choi J.Y., Lieberman J.R., Huang J., Zuk P.A., Zhang J., et al. Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res 21 (2003) 622-629
36. Olmsted E.A., Blum J.S., Rill D., Yotnda P., Gugala Z., Lindsey R.W., et al. Adenovirus-mediated BMP2 expression in human bone marrow stromal cells. J Cell Biochem 82 (2001) 11-21
37. Shui C., Spelsberg T.C., Riggs B.L., and Khosla S. Changes in Runx2/Cbfa1 expression and activity during osteoblastic differentiation of human bone marrow stromal cells. J Bone Miner Res 18 (2003) 213-221
38. Huang S.L., Hsu C.L., and Yen G.C. Growth inhibitory effect of quercetin on SW 872 human liposarcoma cells. Life Sci 79 2 (2006) 203-209
39. Ma L., Feugang J.M., Konarski P., Wang J., Lu J., Fu S., et al. Growth inhibitory effects of quercetin on bladder cancer cell. Front Biosci 11 (2006) 2275-2285
40. Gulati N., Laudet B., Zohrabian V.M., Murali R., and Jhanwar-Uniyal M. The antiproliferative effect of Quercetin in cancer cells is mediated via inhibition of the PI3K-Akt/PKB pathway. Anticancer Res 26 2A (2006) 1177-1181
41. Mayr G.W., Windhorst S., and Hillemeier K. Antiproliferative plant and synthetic polyphenolics are specific inhibitors of vertebrate inositol-1,4,5-trisphosphate 3-kinases and inositol polyphosphate multikinase. J Biol Chem 280 14 (2005) 13229-13240
42. Qi H., Aguiar D.J., Williams S.M., La Pean A., Pan W., and Verfaillie C.M. Identification of genes responsible for osteoblast differentiation from human mesodermal progenitor cells. Proc Natl Acad Sci USA 100 (2003) 3305-3310
43. Bianco P., Riminucci M., Bonucci E., Termine J.D., and Robey P.G. Bone sialoprotein (BSP) secretion and osteoblast differentiation: relationship to bromodeoxyuridine incorporation, alkaline phosphatase, and matrix deposition. J Histochem Cytochem 41 (1993) 183-191
44. Tu Q., Valverde P., and Chen J. Osterix enhances proliferation and osteogenic potential of bone marrow stromal cells. Biochem Biophys Res Commun 341 4 (2006) 1257-1265
45. von Knoch F., Jaquiery C., Kowalsky M., Schaeren S., Alabre C., Martin I., et al. Effects of bisphosphonates on proliferation and osteoblast differentiation of human bone marrow stromal cells. Biomaterials 26 34 (2005) 6941-6949
46. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with receptor beta. Endocrinology (1998) 4252-4263
47. Harris H.A., Bapat A.R., Gonder D.S., and Frail D.E. The ligand binding profiles of estrogen receptors alpha and beta are species dependent. Steroids 67 (2002) 379-384
48. Rodriguez J.P., Rios S., Fernandez M., and Santibanez J.F. Differential activation of ERK1,2 MAP kinase signaling pathway in mesenchymal stem cell from control and osteoporotic postmenopausal women. J Cell Biochem 92 4 (2004) 745-754
49. Jaiswal R.K., Jaiswal N., Bruder S.P., Mbalaviele G., Marshak D.R., and Pittenger M.F. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275 13 (2000) 9645-9652
50. Coleman K.M., and Smith C. Intracellular signaling pathways: nongenomic actions of estrogens and ligand-independent activation of estrogen receptors. Front Biosci 6 (2001) D1379-D1391 Review
51. Benayahu D., Kletter Y., Zipori D., and Wientroub S. Bone marrow-derived stromal cell line expressing osteoblastic phenotype in vitro and osteogenic capacity in vivo. J Cell Physiol 140 (1989) 1-7
52. Cowan C.M., Shi Y.Y., Aalami O.O., Chou Y.F., Mari C., Thomas R., et al. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22 5 (2004) 560-567
53. Krebsbach P.H., Kuznetsov S.A., Satomura K., Emmons R.V., Rowe D.W., and Robey P.G. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63 (1997) 1059-1069
54. Bruder S.P., Kurth A.A., Shea M., Hayes W.C., Jaiswal N., and Kadiyala S. Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells. J Orthop Res 16 (1998) 155-162
55. Johnstone B., and Yoo J.U. Autologous mesenchymal progenitor cells in articular cartilage repair. Clin Orthop 367 (1999) S156-S162
56. Paganga G., and Rice-Evans C.A. The identification of flavonoids as glycosides in human plasma. FEBS Lett 401 (1997) 78-82