Zoledronic acid induces S-phase arrest via a DNA damage response in normal human oral keratinocytes

Archives of Oral Biology

Volumn 57, Issue 7, 2012, Pages 906-917

  Ohnuki, Hisashi ^a   Izumi, Kenji ^a   Terada, Michiko ^a   Saito, Taro ^a   Kato, Hiroko ^a   Suzuki, Akiko ^a   Kawano, Yoshiro ^a   Nozawa Inoue, Kayoko ^a   Takagi, Ritsuo ^a   Maeda, Takeyasu ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

BRONJ; DNA damage; Oral keratinocytes; S phase arrest; Zoledronic acid

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; BONE DENSITY CONSERVATION AGENT; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; GMNN PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; ZOLEDRONIC ACID;

ANALYSIS OF VARIANCE; ARTICLE; CELL CULTURE; CELL CYCLE S PHASE; CELL PROLIFERATION; DNA DAMAGE; DOSE RESPONSE; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HUMAN; KERATINOCYTE; METABOLISM; MOUTH MUCOSA;

ANALYSIS OF VARIANCE; BONE DENSITY CONSERVATION AGENTS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DIPHOSPHONATES; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMIDAZOLES; KERATINOCYTES; MOUTH MUCOSA; S PHASE;

EID: 84862876498     PISSN: 00039969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.archoralbio.2011.11.015     Document Type: Article

References (59)

1. N.B. Watts, and D.L. Diab Long-term use of bisphosphonates in osteoporosis J Clin Endocrinol Metab 95 4 2010 1555 1565
2. R.G. Russell, N.B. Watts, F.H. Ebetino, and M.J. Rogers Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy Osteoporos Int 19 6 2008 733 759
3. C.H. Van Poznak The use of bisphosphonates in patients with breast cancer Cancer Control 9 6 2002 480 489 (Pubitemid 35462553)
4. M.T. Drake, B.L. Clarke, and S. Khosla Bisphosphonates: mechanism of action and role in clinical practice Mayo Clin Proc 83 9 2008 1032 1045
5. A.A. Reszka, J. Halasy-Nagy, and G.A. Rodan Nitrogen-bisphosphonates block retinoblastoma phosphorylation and cell growth by inhibiting the cholesterol biosynthetic pathway in a keratinocyte model for esophageal irritation Mol Pharmacol 59 2 2001 193 202 (Pubitemid 32108550)
6. Y. Kobayashi, T. Hiraga, A. Ueda, L. Wang, M. Matsumoto-Nakano, and K. Hata Zoledronic acid delays wound healing of the tooth extraction socket, inhibits oral epithelial cell migration, and promotes proliferation and adhesion to hydroxyapatite of oral bacteria, without causing osteonecrosis of the jaw, in mice J Bone Miner Metab 28 2 2010 165 175
7. 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 5 2004 527 534 (Pubitemid 38542516)
8. O. Filleul, E. Crompot, and S. Saussez Bisphosphonate-induced osteonecrosis of the jaw: a review of 2,400 patient cases J Cancer Res Clin Oncol 136 8 2010 1117 1124
9. 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 Maxillofacial Surg 63 11 2005 1567 1575 (Pubitemid 41525412)
10. S.L. Ruggiero, T.B. Dodson, L.A. Assael, R. Landesberg, R.E. Marx, and B. Mehrotra American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaws - 2009 update J Oral Maxillofac Surg 67 Suppl. 5 2009 2 12
11. M.R. Allen, and D.B. Burr The pathogenesis of bisphosphonate-related osteonecrosis of the jaw: so many hypotheses, so few data J Oral Maxillofac Surg 67 Suppl. 5 2009 61 70
12. I.R. Orriss, M.L. Key, K.W. Colston, and T.R. Arnett Inhibition of osteoblast function in vitro by aminobisphosphonates J Cell Biochem 106 1 2009 109 118
13. J. Wood, K. Bonjean, S. Ruetz, A. Bellahcène, L. Devy, and J.M. Foidart Novel antiangiogenic effects of the bisphosphonate compound zoledronic acid J Pharmacol Exp Ther 302 3 2002 1055 1061 (Pubitemid 34920226)
14. R.E. Marx Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic J Oral Maxillofac Surg 61 9 2003 1115 1117 (Pubitemid 37064711)
15. S.L. Ruggiero Bisphosphonate-related osteonecrosis of the jaw: an overview Ann N Y Acad Sci 1218 2011 38 46
16. R. Landesberg, V. Woo, S. Cremers, M. Cozin, D. Marolt, and G. Vunjak-Novakovic Potential pathophysiological mechanisms in osteonecrosis of the jaw Ann N Y Acad Sci 1218 2011 62 79
17. G.L. Borromeo, C.E. Tsao, I.B. Darby, and P.R. Ebeling A review of the clinical implications of bisphosphonates in dentistry Aust Dent J 56 1 2011 2 9
18. R. Landesberg, M. Cozin, S. Cremers, V. Woo, S. Kousteni, and S. Sinha Inhibition of oral mucosal cell wound healing by bisphosphonates J Oral Maxillofac Surg 66 5 2008 839 847 (Pubitemid 351522817)
19. I.R. Reid, M.J. Bolland, and A.B. Grey Is bisphosphonate-associated osteonecrosis of the jaw caused by the soft tissue toxicity? Bone 41 3 2007 318 320 (Pubitemid 47199147)
20. C. Walter, A. Pabst, T. Ziebart, M. Klein, and B. Al-Nawas Bisphosphonates affect migration ability and cell viability of HUVEC, fibroblasts and osteoblasts in vitro Oral Dis 17 2 2011 194 199
21. Pabst AM, Ziebart T, Koch FP, Taylor KY, Al-Nawas B, Walter C. The influence of bisphosphonates on viability, migration, and apoptosis of human oral keratinocytes-in vitro study. Clin Oral Investig, Published online: 12 January 2011, doi:10.1007/s00784-010-0507-6, in press.
22. M.A. Scheper, A. Badros, R. Chaisuparat, K.J. Cullen, and T.F. Meiller Effect of zoledronic acid on oral fibroblasts and epithelial cells: a potential mechanism of bisphosphonate-associated osteonecrosis Br J Haematol 144 5 2009 667 676
23. H. Agis, J. Blei, G. Watzek, and R. Gruber Is zoledronate toxic to human periodontal fibroblasts? J Dent Res 89 1 2010 40 45
24. M.J. Ravosa, J. Ning, Y. Liu, and M.S. Stack Bisphosphonate effects on the behaviour of oral epithelial cells and oral fibroblasts Arch Oral Biol 56 5 2011 491 498
25. M. Cozin, B.M. Pinker, K. Solemani, J.M. Zuniga, S.C. Dadaian, and S. Cremers Novel therapy to reverse the cellular effects of bisphosphonates on primary human oral fibroblasts J Oral Maxillofac Surg 69 10 2011 2564 2578
26. S.B. Woo, J.W. Hellstein, and J.R. Kalmar Systematic review: bisphosphonates and osteonecrosis of the jaws Ann Intern Med 144 10 2006 753 761 (Pubitemid 46780635)
27. R.B. Presland, and R.J. Jurevic Making sense of the epithelial barrier: what molecular biology and genetics tell us about the functions of oral mucosal and epidermal tissues J Dent Educ 66 4 2002 564 574
28. K. Izumi, S.E. Feinberg, A. Iida, and M. Yoshizawa Intraoral grafting of an ex vivo produced oral mucosa equivalent: a preliminary report Int J Oral Maxillofac Surg 32 2 2003 188 197 (Pubitemid 36592572)
29. T. Tobita, K. Izumi, and S.E. Feinberg Development of an in vitro model for radiation-induced effects on oral keratinocytes Int J Oral Maxillofac Surg 39 4 2010 364 370
30. K. Izumi, T. Tobita, and S.E. Feinberg Isolation of human oral keratinocyte progenitor/stem cells J Dent Res 86 4 2007 341 346
31. K. Izumi, H. Terashi, C.L. Marcelo, and S.E. Feinberg Development and characterization of a tissue-engineered human oral mucosa equivalent produced in a serum-free culture system J Dent Res 79 3 2000 798 805 (Pubitemid 32489382)
32. C. Walter, M.O. Klein, A. Pabst, B. Al-Nawas, H. Duschner, and T. Ziebart Influence of bisphosphonates on endothelial cells, fibroblasts, and osteogenic cells Clin Oral Investig 14 1 2010 35 41
33. T. Ziebart, A. Pabst, M.O. Klein, P. Kämmerer, L. Gauss, and D. Brüllmann Bisphosphonates: restrictions for vasculogenesis and angiogenesis: inhibition of cell function of endothelial progenitor cells and mature endothelial cells in vitro Clin Oral Investig 15 1 2011 105 111
34. I.R. Reid Osteonecrosis of the jaw: who gets it, and why? Bone 44 1 2009 4 10
35. M. Sato, W. Grasser, N. Endo, R. Akins, H. Simmons, and D.D. Thompson Bisphosphonate action. Alendronate localization in rat bone and effects on osteoclast ultrastructure J Clin Invest 88 6 1991 2095 2105
36. A. Skerjanec, J. Berenson, C. Hsu, P. Major, W.H. Miller Jr., and C. Ravera The pharmacokinetics and pharmacodynamics of zoledronic acid in cancer patients with varying degrees of renal function J Clin Pharmacol 43 2 2003 154 162 (Pubitemid 36125942)
37. T. Chen, J. Berenson, R. Vescio, R. Swift, A. Gilchick, and S. Goodin Pharmacokinetics and pharmacodynamics of zoledronic acid in cancer patients with bone metastases J Clin Pharmacol 42 11 2002 1228 1236 (Pubitemid 35205058)
38. E.L. Scheller, C.M. Baldwin, S. Kuo, N.J. D'Silva, S.E. Feinberg, and P.H. Krebsbach Bisphosphonates inhibit expression of p63 by oral keratinocytes J Dent Res 90 7 2011 894 899
39. A. Torres-Rendon, S. Roy, G.T. Craig, and P.M. Speight Expression of Mcm2, geminin and Ki67 in normal oral mucosa, oral epithelial dysplasias and their corresponding squamous-cell carcinomas Br J Cancer 100 7 2009 1128 1134
40. B. Ory, F. Blanchard, S. Battaglia, F. Gouin, F. Rédini, and D. Heymann Zoledronic acid activates the DNA S-phase checkpoint and induces osteosarcoma cell death characterized by apoptosis-inducing factor and endonuclease-G translocation independently of p53 and retinoblastoma status Mol Pharmacol 71 1 2007 333 343 (Pubitemid 46021003)
41. T. Iguchi, Y. Miyakawa, K. Saito, C. Nakabayashi, M. Nakanishi, and H. Saya Zoledronate-induced S phase arrest and apoptosis accompanied by DNA damage and activation of the ATM/Chk1/cdc25 pathway in human osteosarcoma cells Int J Oncol 31 2 2007 285 291
42. Y.Y. Li, J.W. Chang, W.C. Chou, C.C. Liaw, H.M. Wang, and J.S. Huang Zoledronic acid is unable to induce apoptosis, but slows tumor growth and prolongs survival for non-small-cell lung cancers Lung Cancer 59 2 2008 180 191 (Pubitemid 351181343)
43. A.A. Romani, S. Desenzani, M.M. Morganti, S. La Monica, A.F. Borghetti, and P. Soliani Zoledronic acid determines S-phase arrest but fails to induce apoptosis in cholangiocarcinoma cells Biochem Pharmacol 78 2 2009 133 141
44. T. Tamura, K. Shomori, M. Nakabayashi, N. Fujii, K. Ryoke, and H. Ito Zoledronic acid, a third-generation bisphosphonate, inhibits cellular growth and induces apoptosis in oral carcinoma cell lines Oncol Rep 25 4 2011 1139 1143
45. B. Kubista, K. Trieb, F. Sevelda, C. Toma, F. Arrich, and P. Heffeter Anticancer effects of zoledronic acid against human osteosarcoma cells J Orthop Res 24 6 2006 1145 1152 (Pubitemid 43870876)
46. R.H. Kim, R.S. Lee, D. Williams, S. Bae, J. Woo, and M. Lieberman Bisphosphonates induce senescence in normal human oral keratinocytes J Dent Res 90 6 2011 810 816
47. P.H. Lee, M.C. Chang, W.H. Chang, T.M. Wang, Y.J. Wang, and L.J. Hahn Prolonged exposure to arecoline arrested human KB epithelial cell growth: regulatory mechanisms of cell cycle and apoptosis Toxicology 220 2-3 2006 81 89
48. Y. Kudo, S. Kitajima, I. Ogawa, M. Miyauchi, and T. Takata Down-regulation of Cdk inhibitor p27 in oral squamous cell carcinoma Oral Oncol 41 2 2005 105 116 (Pubitemid 40202876)
49. R.P. Perez, L.D. Lewis, A.P. Beelen, A.J. Olszanski, N. Johnston, and C.H. Rhodes Modulation of cell cycle progression in human tumors: a pharmacokinetic and tumor molecular pharmacodynamic study of cisplatin plus the Chk1 inhibitor UCN-01 (NSC 638850) Clin Cancer Res 12 23 2006 7079 7085 (Pubitemid 44974507)
50. E. Nakuci, M. Xu, M.A. Pujana, J. Valls, and W.M. Elshamy Geminin is bound to chromatin in G2/M phase to promote proper cytokinesis Int J Biochem Cell Biol 38 7 2006 1207 1220
51. L.J. Mah, A. El-Osta, and T.C. Karagiannis gamma H2AX: a sensitive molecular marker of DNA damage and repair Leukemia 24 4 2010 679 686
52. N. Okita, Y. Kudo, and S. Tanuma Checkpoint kinase 1 is cleaved in a caspase-dependent pathway during genotoxic stress-induced apoptosis Biol Pharm Bull 30 2 2007 359 362
53. Y. Kudo, T. Tsunematsu, and T. Takata Deregulation of anaphase-promoting complex/cyclosome-dependent proteolysis in cancer J Oral Biosci 52 4 2010 388 401
54. J.M. Peters The anaphase promoting complex/cyclosome: a machine designed to destroy Nat Rev Mol Cell Biol 7 9 2006 644 656
55. T. Cardozo, and M. Pagano The SCF ubiquitin ligase: insights into a molecular machine Nat Rev Mol Cell Biol 5 9 2004 739 751 (Pubitemid 39208183)
56. Y. Kudo, S. Kitajima, I. Ogawa, M. Kitagawa, M. Miyauchi, and T. Takata Small interfering RNA targeting of S phase kinase-interacting protein 2 inhibits cell growth of oral cancer cells by inhibiting p27 degradation Mol Cancer Ther 4 3 2005 471 476 (Pubitemid 40443932)
57. R. van Leuken, L. Clijsters, and R. Wolthuis To cell cycle, swing the APC/C Biochim Biophys Acta 1786 1 2008 49 59
58. D.Y. Graham What the gastroenterologist should know about the gastrointestinal safety profiles of bisphosphonates Dig Dis Sci 47 8 2002 1665 1678 (Pubitemid 34833194)
59. P. Vestergaard, K. Schwartz, E.M. Pinholt, L. Rejnmark, and L. Mosekilde Gastric and esophagus events before and during treatment of osteoporosis Calcif Tissue Int 86 2 2010 110 115