Novel daidzein analogs enhance osteogenic activity of bone marrow-derived mesenchymal stem cells and adipose-derived stromal/stem cells through estrogen receptor dependent and independent mechanisms

Stem Cell Research and Therapy

Volumn 5, Issue 4, 2014, Pages

  Strong, Amy L ^a   Ohlstein, Jason F ^a   Jiang, Quan ^b   Zhang, Qiang ^b   Zheng, Shilong ^b   Boue, Stephen M ^c   Elliott, Steven ^a   Gimble, Jeffrey M ^a   Burow, Matthew E ^a   Wang, Guangdi ^b   Bunnell, Bruce A ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b XAVIER UNIVERSITY OF LOUISIANA   (United States)

^c SOUTHERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALIZARIN RED S; ALKALINE PHOSPHATASE; CALCIUM; COL1A1 PROTEIN; DAIDZEIN; DENTIN MATRIX PROTEIN 1; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; GENISTEIN; OSTEONECTIN; OSTEOPONTIN; PHOSPHATE; PHYTOESTROGEN; PROTEIN; PROTEIN C FOS; SCLEROSTIN; SILVER NITRATE; SOMATOMEDIN; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; BONE DENSITY CONSERVATION AGENT; DAIDZIN; ISOFLAVONE DERIVATIVE;

ADIPOSE DERIVED STEM CELL; ARTICLE; BONE DENSITY; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CAUCASIAN; CELL DIFFERENTIATION; COL1A1 GENE; CONTROLLED STUDY; DLX5 GENE; DMP1 GENE; DRUG EFFICACY; ENZYME ACTIVITY; FEMALE; GENE; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; IGF1 GENE; ONCOGENE C FOS; OSTEOPOROSIS; RUNX2 GENE; SOST GENE; SPARC GENE; SPP1 GENE; ADULT STEM CELL; ANALOGS AND DERIVATIVES; BONE DEVELOPMENT; BONE MARROW CELL; CELL CULTURE; DRUG EFFECTS; IC50; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; PRECLINICAL STUDY;

ADULT STEM CELLS; ALKALINE PHOSPHATASE; BONE DENSITY CONSERVATION AGENTS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; ESTRADIOL; FEMALE; HUMANS; INHIBITORY CONCENTRATION 50; ISOFLAVONES; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; OSTEOPOROSIS; PHYTOESTROGENS; RECEPTORS, ESTROGEN;

EID: 84907914899     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt493     Document Type: Article

References (58)

1. Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. Bliuc D, Nguyen ND, Milch VE, Nguyen TV, Eisman JA, Center JR, JAMA 2009 301 513 521 10.1001/jama.2009.50 19190316
2. Mortality after osteoporotic fractures. Johnell O, Kanis JA, Oden A, Sernbo I, Redlund-Johnell I, Petterson C, De Laet C, Jonsson B, Osteoporis Int 2004 15 38 42 10.1007/s00198-003-1490-4
3. Mortality after all major types of osteoporotic fracture in men and women: an observational study. Center JR, Nguyen TV, Schneider D, Sambrook PN, Eisman JA, Lancet 1999 353 878 882 10.1016/S0140-6736(98)09075-8 10093980
4. Population ageing in the United States of America: implications for public programmes. Weiner JM, Tilly J, Int J Epidemiol 2002 31 776 781 10.1093/ije/31.4.776 12177018
5. Incidence and economic burden of osteoporosis-releated fractures in the United States, 2005-2025. Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A, J Bone Miner Res 2007 22 465 475 10.1359/jbmr.061113 17144789
6. Osteoporosis and physical activity. Smith EL, Raab DM, Acta Med Scand 2009 220 149 156 10.1111/j.0954-6820.1986.tb08944.x
7. Bisphosphonate therapy for osteoporosis: combining optimal fracture risk reduction with patient preference. Beard MK, Curr Med Res Opin 2012 28 141 147 10.1185/03007995.2011.643296 22103779
8. Anabolic therapies for osteoporosis. Uihlein AV, Leder BZ, Endocrinol Metab Clin North Am 2012 41 507 525 10.1016/j.ecl.2012.05.002 22877427
9. Anabolic effect of estrogen replacement on bone in postmenopausal women with osteoporosis: histomorphometric evidence in a longitudinal study. Khastgir G, Studd J, Holland N, Alaghband-Zadeh J, Fox S, Chow J, J Clin Endocrinol Metab 2001 86 289 295 11232014
10. Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) alpha or beta. Okazaki R, Inoue D, Shibata M, Saika M, Kido S, Ooka H, Tomiyama H, Sakamoto Y, Matsumoto T, Endocrinology 2002 143 2349 2356 12021200
11. Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Collaborative Group on Hormonal Factors in Breast Cancer. Collaborative Group on Hormonal Factors in Breast Cancer, Lancet 1997 350 1047 1059 10213546
12. Menopausal estrogen and estrogen-progestin replacement therapy and breast cancer risk. Schairer C, Lubin J, Troisi R, Sturgeon S, Brinton L, Hoover R, JAMA 2000 283 485 491 10.1001/jama.283.4.485 10659874
13. The Use of estrogens and progestins and the risk of breast cancer in postmenopausal women. Colditz GA, Hankinson SE, Hunter DJ, Willett WC, Manson JE, Stampfer MJ, Hennekens C, Rosner B, Speizer FE, N Engl J Med 1995 332 1589 1593 10.1056/NEJM199506153322401 7753136
14. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. Ettinger B, Black DM, Mitlak BH, Knickerbocker RK, Nickelsen T, Genant HK, Christiansen C, Delmas PD, Zanchetta JR, Stakkestad J, Gluer CC, Krueger K, Cohen FJ, Eckert S, Ensrud KE, Avioli LV, Lips P, Cummings SR, JAMA 1999 282 637 645 10.1001/jama.282.7.637 10517716
15. Effect of raloxifene on stroke and venous thromboembolism according to subgroups in postmenopausal women at increased risk of coronary heart disease. Mosca L, Grady D, Barrett-Connor E, Collins P, Wenger N, Abramson BL, Paganini-Hill A, Geiger MJ, Dowsett SA, Amewou-Atisso M, Kornitzer M, Stroke 2009 40 147 155 10.1161/STROKEAHA.108.518621 18948611
16. Effects of soy isoflavone supplements on bone turnover markers in menopausal women: systematic review and meta-analysis of randomized controlled trials. Tuku K, Melby MK, Kurzer MS, Mizuno S, Watanabe S, Ishimi Y, Bone 2010 47 413 423 10.1016/j.bone.2010.05.001 20452475
17. The Soy Isoflavones for Reducing Bone Loss (SIRBL) Study: a 3-y randomized controlled trial in postmenopausal women. Alekel DL, Van Loan MD, Koehler KJ, Hanson LN, Stewart JW, Hanson KB, Kurzer MS, Peterson CT, Am J Clin Nutr 2010 91 218 230 10.3945/ajcn.2009.28306 19906801
18. Methoxylated isoflavones, cajanin and isoformononetin, have non-estrogenic bone forming effect via differential mitogen activated protein kinase (MAPK) signaling. Bhargavan B, Gautam AK, Singh D, Kumar A, Chaurasia S, Tyagi AM, Yadav DK, Mishra JS, Singh AB, Sanyal S, Goel A, Maurya R, Chattopadhyay N, J Cell Biochem 2009 108 388 399 10.1002/jcb.22264 19598169
19. A low dose of daidzein acts as an ERβ-selective agonist in trabecular osteoblasts of young female piglets. de Wilde A, Lieberherr M, Colin C, Pointillart A, J Cell Physiol 2004 200 253 262 10.1002/jcp.20008 15174095
20. Isoflavones: estrogenic activity, biological effect and bioavailability. Vitale DC, Piazza C, Melilli B, Drago F, Salomone S, Eur J Drug Metab Pharmacokinet 2013 38 15 25 10.1007/s13318-012-0112-y 23161396
21. Effects of 7-O substitutions on estrogenic and anti-estrogenic activities of daidzein analogues in MCF-7 breast cancer cells. Jiang Q, Payton-Stewart F, Elliott S, Driver J, Rhodes LV, Zhang Q, Zheng S, Bhatnagar D, Boue SM, Collins-Burow BM, Sridhar J, Stevens C, McLachlan JA, Wiese TE, Burow ME, Wang G, J Med Chem 2010 53 6153 6163 10.1021/jm100610w 20669983
22. Design, synthesis, and osteogenic activity of daidzein analogs on human mesenchymal stem cells. Strong AL, Jiang Q, Zhang Q, Zheng S, Bou SM, Elliott S, Burow ME, Bunnell BA, Wang G, ACS Med Chem Lett 2013 5 143 148 24900787
23. Bone tissue engineering in osteoporosis. Jakob F, Ebert R, Ignatius A, Matsushita T, Watanabe Y, Groll J, Walles H, Maturitas 2013 75 118 124 10.1016/j.maturitas.2013.03.004 23562167
24. Adipose-derived stem cells for regenerative medicine. Gimble JM, Katz AJ, Bunnell BA, Circ Res 2007 100 1249 1260 10.1161/01.RES.0000265074.83288.09 17495232
25. The diversity of sex steroid action: regulation of metabolism by estrogen signaling. Faulds MH, Zhao C, Dahlman-Wright K, Gustafsson J-A, J Endocrinol 2012 212 3 12 10.1530/JOE-11-0044 21511884
26. Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Filardo EJ, Thomas P, J Endocrinol 2012 153 2953 2962 10.1210/en.2012-1061
27. Estrogen biology: new insights into GPER function and clinical opportunities. Prossnitz ER, Barton M, Mol Cell Endocrinol 2014 389 71 83 10.1016/j.mce.2014.02.002 24530924
28. The molecular mechanisms underlying the pharmacological actions of ER modulators: implications for new drug discovery in breast cancer. McDonnell DP, Wardell SE, Curr Opin Pharmacol 2010 10 620 628 10.1016/j.coph.2010.09.007 20926342
29. Non-classical regulation of estrogen receptor-alpha by ICI182,780. Wang MW, Traystman RJ, Hurn PD, Liu T, J Steroid Biochem Mol Biol 2004 92 51 62 10.1016/j.jsbmb.2004.06.002 15544930
30. Research Resource: transcriptional profiling in a cellular model of breast cancer reveals functional and mechanistic differences between clinically relevant SERM and between SERM/Estrogen complexes. Wardell SE, Kazmin D, McDonnell DP, Mol Endocrinol 2012 26 1235 1248 10.1210/me.2012-1031 22570330
31. Effects of genistein aglycone in osteoporotic, ovariectomized rats: a comparison with alendronate, raloxifene and oestradiol. Bitto A, Burnett BP, Polito F, Marini H, Levy RM, Armbruster MA, Minutoli L, Stefano VD, Irrera N, Antoci S, Granese R, Squadrito F, Altavilla D, Br J Pharmacol 2008 155 896 905 10.1038/bjp.2008.305 18695641
32. Genistein aglycone: a dual mode of action anti-osteoporotic soy isoflavone rebalancing bone turnover towards bone formation. Bitto A, Polito F, Squadrito F, Marini H, D'Anna R, Irrera N, Minutoli L, Granese R, Altavilla D, Curr Med Chem 2010 17 3007 3018 10.2174/092986710791959738 20629630
33. Daidzein is more efficient than genistein in preventing ovariectomy-induced bone loss in rats. Picherit C, Coxam V, Bennetau-Pelissero C, Kati-Coulibaly S, Davicco M-J, Lebecque P, Barlet J-P, J Nutr 2000 130 1675 1681 10867035
34. Effect of daidzein on bone formation. Wong RWK, Rabie ABM, Front Biosci 2009 14 3673 3679
35. Down-regulation of osteoclast differentiation by daidzein via caspase 3. Rassi CM, Lieberherr M, Chaumaz G, Pointillart A, Cournot G, J Bone Miner Res 2002 17 630 638 10.1359/jbmr.2002.17.4.630 11918220
36. Daidzein together with high calcium preserve bone mass and biomechanical strength at multiple sites in ovariectomized mice. Fonseca D, Ward WE, Bone 2004 35 489 497 10.1016/j.bone.2004.03.031 15268901
37. Genistein derivatives as selective estrogen receptor modulators: sonochemical synthesis and in vivo anti-osteoporotic action. Wang SF, Jiang Q, Ye YH, Li Y, Tan RX, Bioorg Med Chem Lett 2005 13 4880 4890 10.1016/j.bmc.2005.04.082
38. One step synthesis of 2-hydroxymethylisoflavone and their osteogenic activity. Kumar M, Rawat P, Kureel J, Singh AK, Singh D, Maurya R, Bioorg Med Chem Lett 2011 21 1706 1709 10.1016/j.bmcl.2011.01.095 21320782
39. Synthetic analogs of daidzein, having more potent osteoblast stimulating effect. Yadav DK, Gautam AK, Kureel J, Srivastava K, Sahai M, Singh D, Chattopadhyay N, Maurya R, Bioorg Med Chem Lett 2011 21 677 681 10.1016/j.bmcl.2010.12.008 21194940
40. Runx2: a master organizer of gene transcription in developing and maturing osteoblasts. Schroeder TM, Jensen ED, Westendorf JJ, Birth Defects Res C Embryo Today 2005 75 213 225 10.1002/bdrc.20043 16187316
41. The regulation of differentiation in mesenchymal stem cells. Augello A, De Bari C, Hum Gene Ther 2010 21 1226 1238 10.1089/hum.2010.173 20804388
42. Osteopenia and decreased bone formation in osteonectin-deficient mice. Delany AM, Amling M, Priemel M, Howe C, Baron R, Canalis E, J Clin Invest 2000 105 915 923 10.1172/JCI7039 10749571
43. Expression profile of osteoblast lineage at defined stages of differentiation. Kalajzic I, Staal A, Yang W-P, Wu Y, Johnson SE, Feyen JHM, Krueger W, Maye P, Yu F, Zhao Y, Kuo L, Gupta RR, Achenie LE, Wang HW, Shin DG, Rowe DW, J Biol Chem 2005 280 24618 24626 10.1074/jbc.M413834200 15834136
44. Genistein and daidzein repress adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells via Wnt/β-catenin signalling or lipolysis. Kim MH, Park JS, Seo MS, Jung JW, Lee YS, Kang KS, Cell Prolif 2010 43 594 605 10.1111/j.1365-2184.2010.00709.x 21039998
45. Reduction of body weight, liver steatosis and expression of stearoyl-CoA desaturase 1 by the isoflavone daidzein in diet-induced obesity. Crespillo A, Alonso M, Vida M, Pavón F, Serrano A, Rivera P, Romero-Zerbo Y, Fernández-Llebrez P, Martínez A, Pérez-Valero V, Bermúdez-Silva FJ, Suárez J, de Fonseca FR, Br J Pharmacol 2011 164 1899 1915 10.1111/j.1476-5381.2011.01477.x 21557739
46. The inhibitory effects of soy daidzein on obesity in C57Bl/6J mice fed high fat A1099. Kim MH, Park H, Kim WG, Lee YS, FASEB J 2007 21 851 858 10.1096/fj.06-7330com 17244817
47. Antiobesity action of a daidzein derivative on male obese mice induced by a high-fat diet. Guo Y, Wu G, Yang H, Zhang J, Nutr Res 2009 29 656 663 10.1016/j.nutres.2009.09.005 19854381
48. Transcriptomics comparison between porcine adipose and bone marrow mesenchymal stem cells during in vitro osteogenic and adipogenic differentiation. Monaco E, Bionaz M, Rodriguez-Zas S, Hurley WL, Wheeler MB, PLoS One 2012 7 1 19
49. Stromal stem cells from adipose tissue and bone marrow of age-matched female donors display distinct immunophenotypic profiles. Pachon-Pena G, Yu G, Tucker HA, Wu X, Vendrell J, Bunnell BA, Gimble JM, J Cell Physiol 2011 226 843 851 10.1002/jcp.22408 20857424
50. Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Strioga M, Viswanathan S, Darinskas A, Slaby O, Michalek J, Stem Cells Dev 2012 21 2724 2752 10.1089/scd.2011.0722 22468918
51. Adipose tissue-derived stem cells and their application in bone and cartilage tissue engineering. Rada T, Reis RL, Gomes ME, Tissue Eng Part B Rev 2009 15 113 125 10.1089/ten.teb.2008.0423 19196117
52. Engineering of large osteogenic grafts with rapid engraftment capacity using mesenchymal and endothelial progenitors from human adipose tissue. Guven S, Mehrkens A, Saxer F, Schaefer DJ, Martinetti R, Martin I, Scherberich A, Biomaterials 2011 32 5801 5809 10.1016/j.biomaterials.2011.04.064 21605897
53. Inhibitory effect of genistein and daidzein on ovarian cancer cell growth. Gercel-Taylor C, Feitelson AK, Taylor DD, Anticancer Res 2004 24 795 800 15161029
54. Daidzein induces MCF-7 breast cancer cell apoptosis via the mitochondrial pathway. Jin S, Zhang QY, Kang XM, Wang JX, Zhao WH, Ann Oncol 2010 21 263 268 10.1093/annonc/mdp499 19889614
55. Effects of dietary daidzein and its metabolite, equol, at physiological concentrations on the growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in ovariectomized athymic mice. Ju YH, Fultz J, Allred KF, Doerge DR, Helferich WG, Carcinogenesis 2006 27 856 863 16399773
56. Daidzein: bioavailability, potential for reproductive toxicity, and breast cancer chemoprevention in female rats. Lamartiniere CA, Wang J, Smith-Johnson M, Eltoum I-E, Toxicol Sci 2002 65 228 238 10.1093/toxsci/65.2.228 11812927
57. Anti-breast cancer potential of daidzein in rodents. Liu X, Suzuki N, Laxmi YRS, Okamoto Y, Shibutani S, Life Sci 2012 91 415 419 10.1016/j.lfs.2012.08.022 23227466
58. Vitamin D interactions with soy isoflavones on bone after menopause: a review. Park CY, Weaver CM, Nutrients 2012 4 1610 1621 10.3390/nu4111610 23201836