Zoledronate, ibandronate and clodronate enhance osteoblast differentiation in a dose dependent manner - A quantitative in vitro gene expression analysis of Dlx5, Runx2, OCN, MSX1 and MSX2

Journal of Cranio-Maxillofacial Surgery

Volumn 39, Issue 8, 2011, Pages 562-569

  Koch, Felix Peter ^a   Merkel, Christina ^a   Al Nawas, Bilal ^a   Smeets, Ralf ^b   Ziebart, Thomas ^a   Walter, Christian ^a   Wagner, Wilfried ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Bisphosphonate; Differentiation; Gene expression; In vitro; Osteoblasts

Indexed keywords

CLODRONIC ACID; IBANDRONIC ACID; MESSENGER RNA; OSTEOCALCIN; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR RUNX2; ZOLEDRONIC ACID;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFECT; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; OSTEOBLAST; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION;

BIOLOGICAL MARKERS; BONE DENSITY CONSERVATION AGENTS; BONE REMODELING; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CLODRONIC ACID; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DIPHOSPHONATES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; IMIDAZOLES; MSX1 TRANSCRIPTION FACTOR; OSTEOBLASTS; OSTEOCALCIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 80055049165     PISSN: 10105182     EISSN: 18784119     Source Type: Journal    
DOI: 10.1016/j.jcms.2010.10.007     Document Type: Article

References (50)

1. M.H. Abu-Id, Y. Acil, J. Gottschalk, and T. Kreusch Bisphosphonate- associated osteonecrosis of the jaw Mund Kiefer Gesichtschir 10 2006 73 81 (Pubitemid 43399262)
2. J.E. Aubin, and J.T. Triffitt Mesenchymal stem cell and osteoblast differentiation J.P. Bilezikian, L.G. Raisz, G.A. Rodan, Principles of bone biology 2nd ed. 2002 Academic Press San Diego, San Francisco, New York, Boston, London, Sydney, Tokyo 59 81
3. R. Balena, B.C. Toolan, M. Shea, A. Markatos, E.R. Myers, and S.C. Lee The effects of 2-year treatment with the aminobisphosphonate alendronate on bone metabolism, bone histomorphometry, and bone strength in ovariectomized nonhuman primates J Clin Invest 92 1993 2577 2586 (Pubitemid 24006520)
4. A. Bamias, E. Kastritis, C. Bamia, L.A. Moulopoulos, I. Melakopoulos, and G. Bozas Osteonecrosis of the jaw in cancer after treatment with bisphosphonates: incidence and risk factors J Clin Oncol 23 2005 8580 8587 (Pubitemid 46211499)
5. A. Bedogni, G. Saia, L. Chiarini, and P.F. Nocini Bisphosphonate- associated jawbone osteomyelitis: clinical, radiological and histological features J Craniomaxillofac Surg 34 2006 35
6. D.M. Black, S.R. Cummings, D.B. Karpf, J.A. Cauley, D.E. Thompson, and M.C. Nevitt Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Fracture Intervention Trial Research Group Lancet 348 1996 1535 1541 (Pubitemid 26411651)
7. H.G. Bone, D. Hosking, J.P. Devogelaer, J.R. Tucci, R.D. Emkey, and R.P. Tonino Ten years' experience with alendronate for osteoporosis in postmenopausal women N Engl J Med 350 2004 1189 1199 (Pubitemid 38339363)
8. P.M. Chavassieux, M.E. Arlot, C. Reda, L. Wei, A.J. Yates, and P.J. Meunier Histomorphometric assessment of the long-term effects of alendronate on bone quality and remodeling in patients with osteoporosis J Clin Invest 100 1997 1475 1480 (Pubitemid 27425772)
9. M.M. Cohen Jr. The new bone biology: pathologic, molecular, and clinical correlates Am J Med Genet A 140 2006 2646 2706 (Pubitemid 44865095)
10. F.P. Coxon, K. Thompson, and M.J. Rogers Recent advances in understanding the mechanism of action of bisphosphonates Curr Opin Pharmacol 6 2006 307 312 (Pubitemid 43670914)
11. J.P. Devogelaer, H. Broll, R. Correa-Rotter, D.C. Cumming, C.N. De Deuxchaisnes, and P. Geusens Oral alendronate induces progressive increases in bone mass of the spine, hip, and total body over 3 years in postmenopausal women with osteoporosis Bone 18 1996 141 150 (Pubitemid 26092594)
12. J.E. Dunford, M.J. Rogers, F.H. Ebetino, R.J. Phipps, and F.P. Coxon Inhibition of protein prenylation by bisphosphonates causes sustained activation of Rac, Cdc42, and Rho GTPases J Bone Miner Res 21 2006 684 694
13. J.E. Dunford, K. Thompson, F.P. Coxon, S.P. Luckman, F.M. Hahn, and C.D. Poulter Structure-activity relationships for inhibition of farnesyl diphosphate synthase in vitro and inhibition of bone resorption in vivo by nitrogen-containing bisphosphonates J Pharmacol Exp Ther 296 2001 235 242 (Pubitemid 32112446)
14. J.E. Fisher, G.A. Rodan, and A.A. Reszka In vivo effects of bisphosphonates on the osteoclast mevalonate pathway Endocrinology 141 2000 4793 4796 (Pubitemid 32055161)
15. J.E. Fisher, M.J. Rogers, J.M. Halasy, S.P. Luckman, D.E. Hughes, and P.J. Masarachia Alendronate mechanism of action: geranylgeraniol, an intermediate in the mevalonate pathway, prevents inhibition of osteoclast formation, bone resorption, and kinase activation in vitro Proc Natl Acad Sci U S A 96 1999 133 138 (Pubitemid 29036065)
16. O. Fromigue, and J.J. Body Bisphosphonates influence the proliferation and the maturation of normal human osteoblasts J Endocrinol Invest 25 2002 539 546 (Pubitemid 34661843)
17. N. Giuliani, M. Pedrazzoni, G. Negri, G. Passeri, M. Impicciatore, and G. Girasole Bisphosphonates stimulate formation of osteoblast precursors and mineralized nodules in murine and human bone marrow cultures in vitro and promote early osteoblastogenesis in young and aged mice in vivo Bone 22 1998 455 461
18. N. Giuliani, M. Pedrazzoni, G. Passeri, G. Negri, M. Impicciatore, and G. Girasole Bisphosphonates stimulate the production of basic fibroblast growth factor and the formation of bone marrow precursors of osteoblasts. New findings about their mechanism of action Minerva Med 89 1998 249 258 (Pubitemid 28535329)
19. M. Glatt, A. Pataki, G.P. Evans, S.B. Hornby, and J.R. Green Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid Osteoporos Int 15 2004 707 715 (Pubitemid 39222653)
20. 2-terminal kinase by BMP-2 and their implication in the stimulation of osteoblastic cell differentiation J Bone Miner Res 18 2003 2060 2068 (Pubitemid 37377457)
21. S.B. Hornby, G.P. Evans, S.L. Hornby, A. Pataki, M. Glatt, and J.R. Green Long-term zoledronic acid treatment increases bone structure and mechanical strength of long bones of ovariectomized adult rats Calcif Tissue Int 72 2003 519 527 (Pubitemid 36919519)
22. G.I. Im, S.A. Qureshi, J. Kenney, H.E. Rubash, and A.S. Shanbhag Osteoblast proliferation and maturation by bisphosphonates Biomaterials 25 2004 4105 4115 (Pubitemid 38388576)
23. P.P. Lehenkari, M. Kellinsalmi, J.P. Napankangas, K.V. Ylitalo, J. Monkkonen, and M.J. Rogers Further insight into mechanism of action of clodronate: inhibition of mitochondrial ADP/ATP translocase by a nonhydrolyzable, adenine-containing metabolite Mol Pharmacol 61 2002 1255 1262 (Pubitemid 34441791)
24. U.A. Liberman, S.R. Weiss, J. Broll, H.W. Minne, H. Quan, and N.H. Bell Effect of oral alendronate on bone mineral density and the incidence of fractures in postmenopausal osteoporosis. The Alendronate Phase III Osteoporosis Treatment Study Group N Engl J Med 333 1995 1437 1443
25. S.P. Luckman, F.P. Coxon, F.H. Ebetino, R.G. Russell, and M.J. Rogers Heterocycle-containing bisphosphonates cause apoptosis and inhibit bone resorption by preventing protein prenylation: evidence from structure-activity relationships in J774 macrophages J Bone Miner Res 13 1998 1668 1678 (Pubitemid 28491995)
26. S.P. Luckman, D.E. Hughes, F.P. Coxon, R. Graham, G. Russell, and M.J. Rogers Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras J Bone Miner Res 13 1998 581 589 (Pubitemid 28163009)
27. S.P. Luckman, D.E. Hughes, F.P. Coxon, G.G. Russell, and M.J. Rogers JBMR anniversary classic. Nitrogen-containing biophosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras J Bone Miner Res 20 2005 1265 1274 Originally published in Volume 7, number 4, pp. 581-9 (1998)
28. R.E. Marx, Y. Sawatari, M. Fortin, and V. Broumand Bisphosphonate-induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk factors, recognition, prevention, and treatment J Oral Maxillofac Surg 63 2005 1567 1575 (Pubitemid 41525412)
29. L. Mortensen, P. Charles, P.J. Bekker, J. Digennaro, and C.C. Johnston Jr. Risedronate increases bone mass in an early postmenopausal population: two years of treatment plus one year of follow-up J Clin Endocrinol Metab 83 1998 396 402 (Pubitemid 28496512)
30. G. Mundy, R. Garrett, S. Harris, J. Chan, D. Chen, and G. Rossini Stimulation of bone formation in vitro and in rodents by statins Science 286 1999 1946 1949 (Pubitemid 129515901)
31. A. Pataki, K. Muller, J.R. Green, Y.F. Ma, Q.N. Li, and W.S. Jee Effects of short-term treatment with the bisphosphonates zoledronate and pamidronate on rat bone: a comparative histomorphometric study on the cancellous bone formed before, during, and after treatment Anat Rec 249 1997 458 468 (Pubitemid 27521594)
32. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res 29 2001 e45
33. S. Ponader, H. Brandt, E. Vairaktaris, C. von Wilmowsky, E. Nkenke, and K.A. Schlegel In vitro response of hFOB cells to pamidronate modified sodium silicate coated cellulose scaffolds Colloids Surf B Biointerfaces 64 2008 275 283
34. A.J. Roelofs, K. Thompson, S. Gordon, and M.J. Rogers Molecular mechanisms of action of bisphosphonates: current status Clin Cancer Res 12 2006 6222s 6230s (Pubitemid 44703794)
35. M.J. Rogers, S. Gordon, H.L. Benford, F.P. Coxon, S.P. Luckman, and J. Monkkonen Cellular and molecular mechanisms of action of bisphosphonates Cancer 88 2000 2961 2978 (Pubitemid 30413179)
36. S.L. Ruggiero, B. Mehrotra, T.J. Rosenberg, and S.L. Engroff Osteonecrosis of the jaws associated with the use of bisphosphonates: a review of 63 cases J Oral Maxillofac Surg 62 2004 527 534 (Pubitemid 38542516)
37. R.G. Russell, and M.J. Rogers Bisphosphonates: from the laboratory to the clinic and back again Bone 25 1999 97 106 (Pubitemid 29322070)
38. R.G. Russell, M.J. Rogers, J.C. Frith, S.P. Luckman, F.P. Coxon, and H.L. Benford The pharmacology of bisphosphonates and new insights into their mechanisms of action J Bone Miner Res 14 Suppl. 2 1999 53 65 (Pubitemid 29455800)
39. K.S. Selander, J. Monkkonen, E.K. Karhukorpi, P. Harkonen, R. Hannuniemi, and H.K. Vaananen Characteristics of clodronate-induced apoptosis in osteoclasts and macrophages Mol Pharmacol 50 1996 1127 1138 (Pubitemid 26384851)
40. T. Storm, T. Steiniche, G. Thamsborg, and F. Melsen Changes in bone histomorphometry after long-term treatment with intermittent, cyclic etidronate for postmenopausal osteoporosis J Bone Miner Res 8 1993 199 208 (Pubitemid 23060638)
41. M.B. Tereshina, A.G. Zaraisky, and V.V. Novoselov Ras-dva, a member of novel family of small GTPases, is required for the anterior ectoderm patterning in the Xenopus laevis embryo Development 133 2006 485 494 (Pubitemid 43273834)
42. R.P. Tonino, P.J. Meunier, R. Emkey, J.A. Rodriguez-Portales, C.J. Menkes, and R.D. Wasnich Skeletal benefits of alendronate: 7-year treatment of postmenopausal osteoporotic women. Phase III Osteoporosis Treatment Study Group J Clin Endocrinol Metab 85 2000 3109 3115
43. M. Tsuchimoto, Y. Azuma, O. Higuchi, I. Sugimoto, N. Hirata, and M. Kiyoki Alendronate modulates osteogenesis of human osteoblastic cells in vitro Jpn J Pharmacol 66 1994 25 33 (Pubitemid 24326178)
44. E.R. van Beek, L.H. Cohen, I.M. Leroy, F.H. Ebetino, C.W. Lowik, and S.E. Papapoulos Differentiating the mechanisms of antiresorptive action of nitrogen containing bisphosphonates Bone 33 2003 805 811 (Pubitemid 37406665)
45. J. Vandesompele, K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, and A. De Paepe Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol 3 2002 RESEARCH0034
46. F. von Knoch, C. Jaquiery, M. Kowalsky, S. Schaeren, C. Alabre, and I. Martin Effects of bisphosphonates on proliferation and osteoblast differentiation of human bone marrow stromal cells Biomaterials 26 2005 6941 6949 (Pubitemid 41095518)
47. C. Walter, B. Al-Nawas, A. du Bois, L. Buch, P. Harter, and K.A. Grotz Incidence of bisphosphonate-associated osteonecrosis of the jaws in breast cancer patients Cancer 115 2009 1631 1637
48. C. Walter, B. Al-Nawas, K.A. Grotz, C. Thomas, J.W. Thuroff, and V. Zinser Prevalence and risk factors of bisphosphonate-associated osteonecrosis of the jaw in prostate cancer patients with advanced disease treated with zoledronate Eur Urol 54 2008 1066 1072
49. C. Walter, K.A. Grotz, M. Kunkel, and B. Al-Nawas Prevalence of bisphosphonate associated osteonecrosis of the jaw within the field of osteonecrosis Support Care Cancer 15 2007 197 202 (Pubitemid 46332925)
50. F.L. Zhang, and P.J. Casey Protein prenylation: molecular mechanisms and functional consequences Annu Rev Biochem 65 1996 241 269 (Pubitemid 26250610)