Isoquercitrin and polyphosphate co-enhance mineralization of human osteoblast-like SaOS-2 cells via separate activation of two RUNX2 cofactors AFT6 and Ets1

Biochemical Pharmacology

Volumn 89, Issue 3, 2014, Pages 413-421

  Wang, Xiaohong ^a   Schröder, Heinz C ^a   Feng, Qingling ^b   Diehl Seifert, Bärbel ^c   Grebenjuk, Vladislav A ^a   Müller, Werner E G ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b TSINGHUA UNIVERSITY   (China)

^c NanotecMARIN GmbH   (Germany)

Author keywords

Alkaline phosphatase; Bone metabolism; Isoquercitrin; Osteoblasts; Osteocalcin; Quercetin

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ISOQUERCITRIN; POLYPHOSPHATE; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR RUNX2;

ARTICLE; BIOMINERALIZATION; BONE MINERALIZATION; CELL LEVEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SAOS 2 CELL LINE; SIGNAL TRANSDUCTION; STEADY STATE; UPREGULATION;

ALKALINE PHOSPHATASE; BONE METABOLISM; ISOQUERCITRIN; OSTEOBLASTS; OSTEOCALCIN; QUERCETIN;

ACTIVATING TRANSCRIPTION FACTOR 6; CALCIFICATION, PHYSIOLOGIC; CALCIUM; CELL LINE, TUMOR; DRUG SYNERGISM; GENE EXPRESSION REGULATION; HUMANS; OSTEOBLASTS; POLYPHOSPHATES; PROTO-ONCOGENE PROTEIN C-ETS-1; QUERCETIN;

EID: 84899961246     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.03.020     Document Type: Article

References (60)

1. N.E. Lane Epidemiology, etiology, and diagnosis of osteoporosis Am J Obstet Gynecol 194 Suppl 2006 S3 S11
2. F. Branca Dietary phyto-oestrogens and bone health Proc Nutr Soc 62 2003 877 887
3. A. Wattel, S. Kamel, R. Mentaverri, F. Lorget, C. Prouillet, and J.P. Petit et al. Potent inhibitory effect of naturally occurring flavonoids quercetin and kaempferol on in vitro osteoclastic bone resorption Biochem Pharmacol 65 2003 35 42
4. M. Notoya, Y. Tsukamoto, H. Nishimura, J.T. Woo, K. Nagai, and I.S. Lee et al. Quercetin, a flavonoid, inhibits the proliferation, differentiation, and mineralization of osteoblasts in vitro Eur J Pharmacol 485 2004 89 96
5. C. Prouillet, J.C. Mazière, C. Mazière, A. Wattel, M. Brazier, and S. Kamel 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 2004 1307 1313
6. Y.O. Son, S.H. Kook, K.C. Choi, Y.S. Jang, Y.M. Jeon, and J.G. Kim et al. Quercetin, a bioflavonoid, accelerates TNF-alpha-induced growth inhibition and apoptosis in MC3T3-E1 osteoblastic cells Eur J Pharmacol 529 2006 24 32
7. P. Košinová, K. Berka, M. Wykes, M. Otyepka, and P. Trouillas Positioning of antioxidant quercetin and its metabolites in lipid bilayer membranes: implication for their lipid-peroxidation inhibition J Phys Chem B 116 2012 1309 1318
8. W.J. Oh, M. Endale, S.C. Park, J.Y. Cho, and M.H. Rhee Dual roles of quercetin in platelets: phosphoinositide-3-kinase and MAP kinases inhibition, and cAMP-dependent vasodilator-stimulated phosphoprotein stimulation Evid Based Complement Alternat Med 2012 2012 485262 doi: 10.1155/2012/485262
9. L. Mezesova, M. Bartekova, V. Javorkova, J. Vlkovicova, A. Breier, and N. Vrbjar Effect of quercetin on kinetic properties of renal Na,K-ATPase in normotensive and hypertensive rats J Physiol Pharmacol 61 2010 593 598
10. E. Van der Heiden, N. Bechoux, M. Muller, Y.J. Schneider, Y. Larondelle, and G. Maghuin-Rogister Food flavonoid aryl hydrocarbon receptor-mediated agonistic/antagonistic/synergic activities in human and rat reporter gene assays Anal Chim Acta 637 2009 337 345
11. 2+ level in osteoblasts (SaOS-2 cells) in vitro Acta Biomater 7 2011 2661 2671
12. X.H. Wang, H.C. Schröder, M. Wiens, H. Ushijima, and W.E.G. Müller Bio-silica and bio-polyphosphate: applications in biomedicine (bone formation) Curr Opin Biotechnol 23 2012 570 578
13. M. Wiens, X.H. Wang, H.C. Schröder, U. Kolb, U. Schloßmacher, and H. Ushijima et al. The role of biosilica in the osteoprotegerin/RANKL ratio in human osteoblastlike cells Biomaterials 31 2010 7716 7725
14. X.H. Wang, H.C. Schröder, U. Schlossmacher, M. Neufurth, Q. Feng, and B. Diehl-Seifert et al. Modulation of the initial mineralization process of SaOS-2 cells by carbonic anhydrase activators and polyphosphate Calcif Tissue Int 94 2014 495 509
15. W.E.G. Müller, X.H. Wang, V. Grebenjuk, B. Diehl-Seifert, R. Steffen, and U. Schloßmacher et al. Silica as a morphogenetically active inorganic polymer: effect on the BMP-2-dependent and RUNX2-independent pathway in osteoblast-like SaOS-2 cells Biomater Sci 1 2013 669 678
16. G. Leyhausen, B. Lorenz, H. Zhu, W. Geurtsen, R. Bohnensack, and W.E.G. Müller et al. Inorganic polyphosphate in human osteoblast-like cells J Bone Mineral Res 13 1998 803 812
17. B. Lorenz, J. Münkner, M.P. Oliveira, A. Kuusksalu, J.M. Leitão, and W.E.G. Müller et al. Changes in metabolism of inorganic polyphosphate in rat tissues and human cells during development and apoptosis Biochim Biophys Acta 1335 1997 51 60
18. S. Omelon, J. Georgiou, Z.J. Henneman, L.M. Wise, B. Sukhu, and T. Hunt et al. Control of vertebrate skeletal mineralization by polyphosphates PLoS One 4 2009 e5634 10.1371/journal.pone.0005634
19. S.J. Omelon, and M.D. Grynpas Relationships between polyphosphate chemistry, biochemistry and apatite biomineralization Chem Rev 108 2008 4694 4715
20. K.A. Johnson, L. Hessle, S. Vaingankar, C. Wennberg, S. Mauro, and S. Narisawa et al. Osteoblast tissue-nonspecific alkaline phosphatase antagonizes and regulates PC-1 Am J Physiol Regul Integr Comp Physiol 279 2000 R1365 R1377
21. H. Fleisch, F. Straumann, R. Schenk, S. Bisaz, and M. Allgöwer Effect of condensed phosphates on calcification of chick embryo femurs in tissue culture Am J Physiol 211 1966 821 825
22. L. Hessle, K.A. Johnson, H.C. Anderson, S. Narisawa, A. Sali, and J.W. Goding et al. Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization Proc Natl Acad Sci USA 99 2002 9445 9449
23. W.E.G. Müller, H.C. Schröder, U. Schlossmacher, V.A. Grebenjuk, H. Ushijima, and X.H. Wang Induction of carbonic anhydrase in SaOS-2 cells, exposed to bicarbonate and consequences for calcium phosphate crystal formation Biomaterials 34 2013 8671 8680
24. E. Pavlov, R. Aschar-Sobbi, M. Campanella, R.J. Turner, M.R. Gómez-García, and A.Y. Abramov Inorganic polyphosphate and energy metabolism in mammalian cells J Biol Chem 285 2010 9420 9428
25. X.H. Wang, H.C. Schröder, B. Diehl-Seifert, K. Kropf, U. Schlossmacher, and M. Wiens et al. Dual effect of inorganic polymeric phosphate/polyphosphate on osteoblasts and osteoclasts in vitro J Tissue Eng Regen Med 7 2013 767 776
26. A. Paulke, G.P. Eckert, M. Schubert-Zsilavecz, and M. Wurglics Isoquercitrin provides better bioavailability than quercetin: comparison of quercetin metabolites in body tissue and brain sections after six days administration of isoquercitrin and quercetin Pharmazie 67 2012 991 996
27. E. Selenge, T. Murata, K. Kobayashi, J. Batkhuu, and F. Yoshizaki Flavone tetraglycosides and benzyl alcohol glycosides from the Mongolian medicinal plant Dracocephalum ruyschiana J Nat Prod 76 2013 186 193
28. S. Bhagwat, D.B. Haytowitz, and J.M. Holden USDA database for the flavonoid content of selected foods; release 3 2011 US Department of Agriculture Beltsville, MD
29. J. Kalinova, and N. Vrchotova Level of catechin, myricetin, quercetin and isoquercitrin in buckwheat (Fagopyrum esculentum Moench), changes of their levels during vegetation and their effect on the growth of selected weeds J Agric Food Chem 57 2009 2719 2725
30. J.K. Dunnick, and J.R. Hailey Toxicity and carcinogenicity studies of quercetin, a natural component of foods Fundam Appl Toxicol 19 1992 423 431
31. M.S. Drozen, and J.F. Foley Gras notification: alpha-glycosyl isoquercitrin 2007 http://www.fda.gov/ucm/groups/fdagov-public/@fdagov-foods- gen/documents/document/ucm269110.pdf
32. H.J. Hausser, and R.E. Brenner Phenotypic instability of SaOS-2 cells in long-term culture Biochem Biophys Res Commun 333 2005 216 222
33. J. Fogh, J.M. Fogh, and T. Orfeo One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice J Natl Cancer Inst 59 1977 221 226
34. T. Mikami, T. Koyama, T. Koyama, A. Imakiire, K. Yamamoto, and M. Furuhata et al. C-jun N-terminal kinase activation is required for apoptotic cell death induced by TNF-related apoptosis-inducing ligand plus DNA-damaging agents in sarcoma cell lines Anticancer Res 26 2006 1153 1160
35. H.C. Schröder, A. Borejko, A. Krasko, A. Reiber, H. Schwertner, and W.E.G. Müller Mineralization of SaOS-2 cells on enzymatically (silicatein) modified bioactive osteoblast-stimulating surfaces J Biomed Mater Res B Appl Biomater 75B 2005 387 392
36. W.E.G. Müller, A. Boreiko, X.H. Wang, A. Krasko, W. Geurtsen, and M.R. Custódio et al. Morphogenetic activity of silica and bio-silica on the expression of genes, controlling biomineralization using SaOS-2 cells Calcif Tissue Intern 81 2007 382 393
37. M. Wiens, X.H. Wang, U. Schloßmacher, I. Lieberwirth, G. Glasser, and H. Ushijima et al. Osteogenic potential of bio-silica on human osteoblast-like (SaOS-2) cells Calcif Tissue Intern 87 2010 513 524
38. K. Mori, M. Berreur, F. Blanchard, C. Chevalier, I. Guisle-Marsollier, and M. Masson et al. Receptor activator of nuclear factor-kappaB ligand (RANKL) directly modulates the gene expression profile of RANK-positive Saos-2 human osteosarcoma cells Oncol Rep 18 2007 1365 1371
39. C.A. Gregory, W.G. Gunn, A. Peister, and D.J. Prockop An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction Anal Biochem 329 2004 77 84
40. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res 29 2001 2002 2007
41. J.S. Johnston, A. Johnson, Y. Gan, M.G. Wientjes, and J.L.S. Au Synergy between 3-azido-3-deoxythymidine and paclitaxel in human pharynx FaDu cells Pharm Res 20 2003 957 961
42. W.G. Jang, E.J. Kim, D.K. Kim, H.M. Ryoo, K.B. Lee, and S.H. Kim et al. BMP2 protein regulates osteocalcin expression via Runx2-mediated Atf6 gene transcription J Biol Chem 287 2012 905 915
43. L. Dalle Carbonare, G. Innamorati, and M.T. Valenti Transcription factor Runx2 and its application to bone tissue engineering Stem Cell Rev 8 2012 891 897
44. T. Itoh, M. Ando, Y. Tsukamasa, and Y. Akao Expression of BMP-2 and Ets1 in BMP-2-stimulated mouse pre-osteoblast differentiation is regulated by microRNA-370 FEBS Lett 586 2012 1693 1701
45. T. Itoh, S. Takeda, and Y. Akao MicroRNA-208 modulates BMP-2-stimulated mouse preosteoblast differentiation by directly targeting V-ets erythroblastosis virus E26 oncogene homolog 1 J Biol Chem 285 2010 27745 27752
46. S. Zhang, Z. Xiao, J. Luo, N. He, J. Mahlios, and L.D. Quarles Dose-dependent effects of Runx2 on bone development J Bone Miner Res 24 2009 1889 1904
47. X.H. Wang, H.C. Schröder, V. Grebenjuk, B. Diehl-Seifert, V. Mailänder, and R. Steffen et al. The marine sponge-derived inorganic polymers, biosilica and polyphosphate, as morphogenetically active matrices/scaffolds for differentiation of human multipotent stromal cells: potential application in 3D printing and distraction osteogenesis Mar Drugs 12 2014 1131 1147
48. J.T. Woo, H. Nakagawa, M. Notoya, T. Yonezawa, N. Udagawa, and I.S. Lee et al. Quercetin suppresses bone resorption by inhibiting the differentiation and activation of osteoclasts Biol Pharm Bull 27 2004 504 509
49. T. Murakami, A. Saito, S. Hino, S. Kondo, S. Kanemoto, and K. Chihara et al. Signalling mediated by the endoplasmic reticulum stress transducer OASIS is involved in bone formation Nat Cell Biol 11 2009 1205 1211
50. Y.J. Kim, Y.C. Bae, K.T. Suh, and J.S. Jung Quercetin, a flavonoid, inhibits proliferation and increases osteogenic differentiation in human adipose stromal cells Biochem Pharmacol 72 2006 1268 1278
51. S. Barille, C. Pellat-Deceunynck, R. Bataille, and M. Amiot Ectopic secretion of osteocalcin, the major non-collagenous bone protein, by the myeloma cell line NCI-H929 J Bone Miner Res 11 1996 466 471
52. A. Patti, L. Gennari, D. Merlotti, F. Dotta, and R. Nuti Endocrine actions of osteocalcin Intern J Endocrinol 2013 2013 (ID 846480)
53. A.F. Okuducu, U. Zils, S.A. Michaelis, C. Mawrin, and A. von Deimling Increased expression of avian erythroblastosis virus E26 oncogene homolog 1 in World Health Organization grade 1 meningiomas is associated with an elevated risk of recurrence and is correlated with the expression of its target genes matrix metalloproteinase-2 and MMP-9 Cancer 107 2006 1365 1372
54. H.J. Kim, and S.H. Kim Tanshinone IIA enhances BMP-2-stimulated commitment of C2C12 cells into osteoblasts via p38 activation Amino Acids 39 2010 1217 1226
55. A. Kornberg, N.N. Rao, and D. Ault-Riche Inorganic polyphosphate: a molecule of many functions Annu Rev Biochem 68 1999 89 125
56. E. Zakharian, B. Thyagarajan, R.J. French, E. Pavlov, and T. Rohacs Inorganic polyphosphate modulates TRPM8 channels PLoS One 4 2009 e5404 doi:10.1371
57. A.Y. Abramov, C. Fraley, C.T. Diao, R. Winkfein, M.A. Colicos, and M.R. Duchen et al. Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calcium-dependent cell death Proc Natl Acad Sci USA 104 2007 18091 18096
58. 2+ channels in the plasma membranes of Escherichia coli Biophys J 69 1995 754 766
59. Z. Gu, H. Wang, L. Li, Q. Wang, and X. Yu Cell-mediated degradation of strontium-doped calcium polyphosphate scaffold for bone tissue engineering Biomed Mater 7 6 2012 065007 10.1088/1748-6041/7/6/065007
60. J.H. Morrissey, S.H. Choi, and S.A. Smith Polyphosphate: an ancient molecule that links platelets, coagulation, and inflammation Blood 119 2012 5972 5979