Effect of zoledronate on oral wound healing in rats

Clinical Cancer Research

Volumn 17, Issue 6, 2011, Pages 1405-1414

  Yamashita, Junro ^a   Koi, Kiyono ^a   Yang, Dong Ye ^a   McCauley, Laurie K ^b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD68 ANTIGEN; CELL PROTEIN; CHEMOKINE RECEPTOR CXCR4; COLLAGENASE 3; PROTEIN EMR1; STROMAL CELL DERIVED FACTOR 1; T CELL IMMUNE REGULATOR 1; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN C; ZOLEDRONIC ACID;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE MARROW; CD31 GENE; CELL DEATH; COLLAGENASE 3 GENE; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG MEGADOSE; FEMALE; GENE; GENE EXPRESSION; GENE REPRESSION; GINGIVA; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; JAW OSTEONECROSIS; LYMPHANGIOGENESIS; MALE; MOUTH CAVITY; MOUTH INJURY; NONHUMAN; OSTEOCLAST; OSTEOCYTE; OSTEOLYSIS; PALATE; PRIORITY JOURNAL; RAT; SOFT TISSUE DISEASE; T CELL IMMUNE REGULATOR 1 GENE; TISSUE REPAIR; TISSUE SPECIFICITY; VASCULOTROPIN A GENE; WOUND HEALING;

ANIMALS; ANTIGENS, CD31; BONE MARROW; DIPHOSPHONATES; GENE EXPRESSION REGULATION; GINGIVA; HOMEOSTASIS; IMIDAZOLES; MATRIX METALLOPROTEINASE 13; OSTEONECROSIS; RATS; RATS, SPRAGUE-DAWLEY; VACUOLAR PROTON-TRANSLOCATING ATPASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 79952731632     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-1614     Document Type: Article

References (47)

1. Black DM, Delmas PD, Eastell R, Reid IR, Boonen S, Cauley JA, et al. Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N Engl J Med 2007;356:1809-22. (Pubitemid 46698462)
2. Costa L, Major PP. Effect of bisphosphonates on pain and quality of life in patients with bone metastases. Nat Clin Pract Oncol 2009;6: 163-74.
3. Hirbe AC, Roelofs AJ, Floyd DH, Deng H, Becker SN, Lanigan LG, et al. The bisphosphonate zoledronic acid decreases tumor growth in bone in mice with defective osteoclasts. Bone 2009;44:908-16.
4. Marx RE. Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic. J Oral Maxillofac Surg 2003;61:1115-7. (Pubitemid 37064711)
5. Ruggiero SL, Mehrotra B, Rosenberg TJ, Engroff SL. Osteonecrosis of the jaws associated with the use of bisphosphonates: a review of 63 cases. J Oral Maxillofac Surg 2004;62:527-34. (Pubitemid 38542516)
6. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 2006;12: 657-64. (Pubitemid 43865234)
7. Miyamoto T, Ohneda O, Arai F, Iwamoto K, Okada S, Takagi K, et al. Bifurcation of osteoclasts and dendritic cells from common progenitors. Blood 2001;98:2544-54.
8. Pierce AM, Lindskog S. Evidence for capping of Fc gamma receptors on osteoclasts. Calcif Tissue Int 1986;39:109-16. (Pubitemid 16036850)
9. Rothe L, Collin-Osdoby P, Chen Y, Sunyer T, Chaudhary L, Tsay A, et al. Human osteoclasts and osteoclast-like cells synthesize and release high basal and inflammatory stimulated levels of the potent chemokine interleukin-8. Endocrinology 1998;139:4353-63. (Pubitemid 28513725)
10. Yao Z, Xing L, Qin C, Schwarz EM, Boyce BF. Osteoclast precursor interaction with bone matrix induces osteoclast formation directly by an interleukin-1-mediated autocrine mechanism. J Biol Chem 2008;283:9917-24.
11. Li H, Hong S, Qian J, Zheng Y, Yang J, Yi Q. Cross talk between the bone and immune systems: osteoclasts function as antigen-presenting cells and activate CD4+and CD8+T cells. Blood 2010;116;210-7.
12. Horner A, Bord S, Kelsall AW, Coleman N, Compston JE. Tie2 ligands angiopoietin-1 and angiopoietin-2 are coexpressed with vascular endothelial cell growth factor in growing human bone. Bone 2001;28: 65-71. (Pubitemid 32112063)
13. Haeusler G, Walter I, Helmreich M, Egerbacher M. Localization of matrix metalloproteinases, (MMPs) their tissue inhibitors, and vascular endothelial growth factor (VEGF) in growth plates of children and adolescents indicates a role for MMPs in human postnatal growth and skeletal maturation. Calcif Tissue Int 2005;76:326-35.
14. Coxon FP, Thompson K, Roelofs AJ, Ebetino FH, Rogers MJ. Visualizing mineral binding and uptake of bisphosphonate by osteoclasts and non-resorbing cells. Bone 2008;42:848-60.
15. Cackowski FC, Anderson JL, Patrene KD, Choksi RJ, Shapiro SD, Windle JJ, et al. Osteoclasts are important for bone angiogenesis. Blood 2010;115;140-9.
16. Croucher PI, De Hendrik R, Perry MJ, Hijzen A, Shipman CM, Lippitt J, et al. Zoledronic acid treatment of 5T2MM-bearing mice inhibits the development of myeloma bone disease: evidence for decreased osteolysis, tumor burden and angiogenesis, and increased survival. J Bone Miner Res 2003;18:482-92. (Pubitemid 36241065)
17. Yaccoby S, Pearse RN, Johnson CL, Barlogie B, Choi Y, Epstein J. Myeloma interacts with the bone marrow microenvironment to induce osteoclastogenesis and is dependent on osteoclast activity. Br J Haematol 2002;116:278-90. (Pubitemid 34156975)
18. Yamashita J, Datta NS, Chun YH, Yang DY, Carey AA, Kreider JM, et al. Role of Bcl2 in osteoclastogenesis and PTH anabolic actions in bone. J Bone Miner Res 2008;23:621-32. (Pubitemid 351575016)
19. Dobson KR, Reading L, Haberey M, Marine X, Scutt A. Centrifugal isolation of bone marrow from bone: an improved method for the recovery and quantitation of bone marrow osteoprogenitor cells from rat tibiae and femurae. Calcif Tissue Int 1999;65:411-3. (Pubitemid 29514082)
20. Enlow DH. Osteocyte necrosis in normal bone. J Dent Res 1966; 45:213.
21. Hale LV, Galvin RJ, Risteli J, Ma YL, Harvey AK, Yang X, et al. PINP: a serum biomarker of bone formation in the rat. Bone 2007;40:1103-9. (Pubitemid 46386558)
22. Oreffo RO, Mundy GR, Seyedin SM, Bonewald LF. Activation of the bone-derived latent TGF beta complex by isolated osteoclasts. Biochem Biophys Res Commun 1989;158:817-23. (Pubitemid 19075997)
23. Utku N, Heinemann T, Tullius SG, Bulwin GC, Beinke S, Blumberg RS, et al. Prevention of acute allograft rejection by antibody targeting of TIRC7, a novel T cell membrane protein. Immunity 1998;9:509-18.
24. Quarello P, Forni M, Barberis L, Defilippi C, Campagnoli MF, Silvestro L, et al. Severe malignant osteopetrosis caused by a GL gene mutation. J Bone Miner Res 2004;19:1194-9. (Pubitemid 41110573)
25. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol 2005;23:901-44. (Pubitemid 40563189)
26. Nannuru KC, Futakuchi M, Varney ML, Vincent TM, Marcusson EG, Singh RK. Matrix metalloproteinase (MMP)-13 regulates mammary tumor-induced osteolysis by activating MMP9 and transforming growth factor-beta signaling at the tumor-bone interface. Cancer Res 70:3494-504.
27. Singh S, Singh UP, Grizzle WE, Lillard JW Jr. CXCL12-CXCR4 interactions modulate prostate cancer cell migration, metalloproteinase expression and invasion. Lab Invest 2004;84:1666-76. (Pubitemid 39600573)
28. Lester KS. The unusual nature of root formation in molar teeth of the laboratory rat. J Ultrastruct Res 1969;28:481-506.
29. Pietrokovski J, Massler M. Ridge remodeling after tooth extraction in rats. J Dent Res 1967;46:222-31.
30. Rothmann C, Barshack I, Kopolovic J, Malik Z. Spectrally resolved morphometry of the nucleus in hepatocytes stained by four histological methods. Histochem J 1998;30:539-47. (Pubitemid 28423708)
31. Green JR. Chemical and biological prerequisites for novel bisphosphonate molecules: results of comparative preclinical studies. Semin Oncol 2001;28:4-10. (Pubitemid 32494619)
32. Kobayashi Y, Hiraga T, Ueda A, Wang L, Matsumoto-Nakano M, Hata K, et al. 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;165-75.
33. Peyruchaud O, Winding B, Pécheur I, Serre CM, Delmas P, Clézardin P. Early detection of bone metastases in a murine model using fluorescent human breast cancer cells: application to the use of the bisphosphonate zoledronic acid in the treatment of osteolytic lesions. J Bone Miner Res 2001;16:2027-34. (Pubitemid 32995393)
34. Fournier P, Boissier S, Filleur S, Guglielmi J, Cabon F, Colombel M, et al. Bisphosphonates inhibit angiogenesis in vitro and testosterone-stimulated vascular regrowth in the ventral prostate in castrated rats. Cancer Res 2002;62:6538-44. (Pubitemid 35364119)
35. Santini D, Vincenzi B, Dicuonzo G, Avvisati G, Massacesi C, Battistoni F, et al. Zoledronic acid induces significant and long-lasting modifications of circulating angiogenic factors in cancer patients. Clin Cancer Res 2003;9:2893-7. (Pubitemid 36993246)
36. Tas F, Duranyildiz D, Oguz H, Camlica H, Yasasever V, Topuz E. Effect of zoledronic acid on serum angiogenic factors in patients with bone metastases. Med Oncol 2008;25:346-9.
37. Maruyama K, Asai J, Ii M, Thorne T, Losordo DW, D'Amore PA. Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing. Am J Pathol 2007;170:1178-91. (Pubitemid 47339326)
38. Li D, Gromov K, Proulx ST, Xie C, Li J, Crane DP, et al. Effects of antiresorptive agents on osteomyelitis: novel insights into the pathogenesis of osteonecrosis of the jaw. Ann N Y Acad Sci 2010;1192:84-94.
39. Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med 1999;341:738-46. (Pubitemid 29407375)
40. Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. J Bone Miner Res 2009; 24:597-605.
41. Huja SS, Beck FM. Bone remodeling in maxilla, mandible, and femur of young dogs. Anat Rec (Hoboken) 2008;291:1-5.
42. Allen MR, Burr DB. Mandible matrix necrosis in beagle dogs after 3 years of daily oral bisphosphonate treatment. J Oral Maxillofac Surg 2008;66:987-94. (Pubitemid 351522818)
43. Zwolak P, Manivel JC, Jasinski P, Kirstein MN, Dudek AZ, Fisher J, et al. Cytotoxic effect of zoledronic acid-loaded bone cement on giant cell tumor, multiple myeloma, and renal cell carcinoma cell lines. J Bone Joint Surg Am 92:162-8.
44. Sminia T, Dijkstra CD. The origin of osteoclasts: an immunohisto-chemical study on macrophages and osteoclasts in embryonic rat bone. Calcif Tissue Int 1986;39:263-6. (Pubitemid 16004326)
45. Weinstein RS, Roberson PK, Manolagas SC. Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 2009;360:53-62.
46. Zhou Z, Wang J, Cao R, Morita H, Soininen R, Chan KM, et al. Impaired angiogenesis, delayed wound healing and retarded tumor growth in perlecan heparan sulfate-deficient mice. Cancer Res. 2004;64:4699-702. (Pubitemid 38924508)
47. Landesberg R, Cozin M, Cremers S, Woo V, Kousteni S, Sinha S, et al. Inhibition of oral mucosal cell wound healing by bisphosphonates. J Oral Maxillofac Surg 2008;66:839-47. (Pubitemid 351522817)