Osteocalcin immunolabeling during the alveolar healing process in ovariectomized rats treated with estrogen or raloxifene

Bone

Volumn 46, Issue 4, 2010, Pages 1021-1029

  Luvizuto, Eloá Rodrigues ^a   Dias, Sheila Mônica Damásio ^a   Queiroz, Thallita Pereira ^a   Okamoto, Tetuo ^a   Garcia, Idelmo Rangel ^a   Okamoto, Roberta ^a   Dornelles, Rita Cássia Menegati ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Alveolar process; Estradiol; Osteocalcin; Ovariectomy; Raloxifene

Indexed keywords

ESTRADIOL; OSTEOCALCIN; RALOXIFENE;

ALVEOLAR BONE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BONE MINERALIZATION; CELL LINEAGE; CONTROLLED STUDY; ESTROGEN DEFICIENCY; ESTROGEN THERAPY; ESTRUS CYCLE; FEMALE; FRACTURE HEALING; IMMUNOHISTOCHEMISTRY; MORPHOMETRICS; NONHUMAN; OSSIFICATION; OSTEOBLAST; OVARIECTOMY; PROTEIN EXPRESSION; RAT; TOOTH EXTRACTION;

ANIMALS; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGENS; FEMALE; IMMUNOHISTOCHEMISTRY; MAXILLA; OSTEOCALCIN; OSTEOGENESIS; OVARIECTOMY; RALOXIFENE; RANDOM ALLOCATION; RATS; RATS, WISTAR; TIME FACTORS; TOOTH EXTRACTION;

EID: 77950529655     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2009.12.016     Document Type: Article

References (66)

1. Eriksen E.F., Colvard D.S., Berg N.J., Graham M.L., Mann K.G., Spelsberg T.C., et al. Evidence of estrogen receptors in normal human osteoblast-like cells. Science 1988, 241:84-86.
2. Pacifici R. Is there a causal role for IL-1 in postmenopausal bone loss?. Calcif. Tissue Int. 1992, 50:295-299.
3. Girasole G., Passeri G., Pedrazzoni M., Giuliani N., Passeri M. Interleukin-6: a pathogenetic role in the post menopausal osteoporosis?. Acta. Biomed. Ateneo Parmense. 1995, 66:125-138.
4. Lindberg M.K., Erlandsson M., Alatalo S.L., Windahl S., Andersson G., Halleen J.M., et al. Estrogen receptor alpha, but not estrogen receptor beta, is involved in the regulation of the OPG/RANKL (osteoprotegerin/receptor activator of NF-kappa B ligand) ratio and serum interleukin-6 in male mice. J. Endocrinol. 2001, 171:425-433.
5. Riggs B.L., Khosla S., Melton L.J. Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 2002, 23:279-302.
6. Payne J.B., Reinhardt R.A., Nummikoski P.V., Patil K.D. Longitudinal alveolar bone loss in post menopausal osteoporotic/osteopenic women. Osteoporosis. Int. 1999, 10:34-40.
7. Grodstein F., Colditz G.A., Stampfer M.J. Post-menopausal hormone use and tooth loss: a prospective study. J. Am. Dent. Assoc. 1996, 127:370-377.
8. Burg M.A., Fraser K., Gui S., Grant K., Kosch S.G., Nierenberg B., et al. Treatment of menopausal symptoms in family medicine settings following the Women's Health Initiative Findings. J. Am. Board. Fam. Med. 2006, 19:122-131.
9. Rodan G.A., Martin T.J. Therapeutic approaches to bone diseases. Science 2000, 289:1508-1514.
10. Regan M.M., Emond S.K., Attardo M.J., Parker R.A., Greenspan S.L. Why do older women discontinue hormone replacement therapy?. J. Womens Health Gend. Based. Med. 2001, 10:343-350.
11. Wronski T.J., Yen C.F., Burton K.W., Mehta R.C., Newman P.S., Soltis E.E., et al. Skeletal effects of calcitonin in ovariectomized rats. Endocrinology 1991, 129:2246-2250.
12. Buffo L., Rossini M., Buoncristiano A., Girardello S., Zamberlan N., Diani F., et al. Diphosphonates: an alternative to estrogen therapy in postmenopausal osteoporosis. Experience with alendronate. Minerva Ginecol. 1996, 48:263-272.
13. Cummings S.R., Eckert S., Krueger K.A., Grady D., Powles T.J., Cauley J.A., et al. The effect of raloxifene on risk of breast cancer in postmenopausal women: results from the MORE randomized trial. Multiple Outcomes of Raloxifene Evaluation. JAMA 1999, 281:2189-2197.
14. Ettinger B., Black D.M., Mitlak B.H., Knickerbocker R.K., Nickelsen T., Genant H.K., et al. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators. JAMA 1999, 282:637-645.
15. Barrett-Connor E., Grady D., Sashegyi A., Anderson P.W., Cox D.A., Hoszowshi K., et al. Raloxifene and cardiovascular events in osteoporotic postmenopausal women: Four-year results from the MORE (Multiple Outcomes of Raloxifene Evaluation) randomized trial. JAMA 2002, 287:847-857.
16. Hejdova M., Palicka V., Kucera Z., Vlcek J. Effects of alendronate and calcitonin on bone mineral density in postmenopausal osteoporotic women. An observational study. Pharm. World Sci. 2005, 27:149-153.
17. Carvalho A.C.P., Okamoto T. Cirurgia bucal: fundamentos experimentais aplicados a clínica 1987, São Paulo, Panamericana.
18. Hsieh Y.D., Devlin H., Roberts C. Early alveolar ridge osteogenesis following tooth extraction in the rat. Arch. Oral. Biol. 1994, 39:425-428.
19. Devlin H., Garland H., Sloan P. Healing of tooth extraction sockets in experimental diabetes mellitus. J. Oral. Maxillofac. Surg. 1996, 54:1087-1091.
20. Carvalho T.L., Bombonato K.F., Brentegani L.G. Histometric analysis of rat alveolar wound healing. Braz. Dent. J. 1997, 8:9-12.
21. Devlin H. Early bone healing events following rat molar tooth extraction. Cells. Tissues Organs 2000, 167:33-37.
22. Amler M.H. The time sequence of tissue regeneration in human extraction wounds. Oral. Surg. Oral. Med. Oral. Pathol. 1969, 27:309-318.
23. Shyng Y.C., Devlin H., Riccardi D., Sloan P. Expression of cartilage-derived retinoic acid-sensitive protein during healing of the rat tooth-extraction socket. Arch. Oral. Biol. 1999, 44:751-757.
24. De Oliveira P.T., Zalzal S.F., Irie K., Nanci A. Early expression of bone matrix proteins in osteogenic cell cultures. J. Histochem. Cytochem. 2003, 51:633-641.
25. Kassem M., Abdallah B.M., Saeed H. Osteoblastic cell: differentiation and trans-differentiation. Arch. Biochem. Biophys. 2008, 473:183-187.
26. National research council, guide for the care and use of laboratory animals. Department of health and human services, committee on care and use of laboratory animals of the institute of laboratory animal resources, 1985.
27. Waynforth H.B. Experimental and surgical techniques in the rat 1980, 161-163. Academic Press, New York.
28. Okamoto T., Russo M.C. Wound healing following tooth extraction: histochemical study in rats. Rev. Fac. Odontol. Araçatuba 1973, 2:153-169.
29. Harms P.G., Ojeda S.R. A rapid and simple procedure for chronic cannulation of the rat jugular vein. J. Appl. Physiol. 1974, 36:391-392.
30. Okamoto T., Fialho A.C.V. Estudo histológico comparativo entre dois métodos de obtenção de cortes de alvéolos de ratos. Rev. Odont. UNESP 1990, 19:63-74.
31. Bauss F., Wagner M., Hothorn L.H. Total administered dose of ibandronate determines its effects on bone mass and architecture in ovariectomized aged rats. J. Rheumatol. 2002, 29:990-998.
32. Wronski T.J., Cintron M., Doherty A.L., Dann L.M. Estrogen treatment prevents osteopenia and depresses bone turnover in ovariectomized rats. Endocrinology 1988, 123:681-686.
33. Sato M., Kim J., Short L.L., Slemenda C.W., Bryant H.U. Longitudinal and cross-sectional analysis of raloxifene effects on tibiae from ovariectomized aged rats. J. Pharmacol. Exp. Ther. 1995, 272:1252-1259.
34. Sato M., Rippy M.K., Bryant H.U. Raloxifene, tamoxifen, nafoxidine, or estrogen effects on reproductive and nonreproductive tissues in ovariectomized rats. FASEB J. 1996, 10:905-912.
35. Schenk R., Eggli P., Fleisch H., Rosini S. Quantitative morphometric evaluation of the inhibitory activity of new aminobisphosphonates on bone resorption in the rat. Calcif. Tissue Int. 1986, 38:342-349.
36. Suva L.J., Harm S.C., Gardner R.M., Thiede M.A. In vivo regulation of Zif268 messenger RNA expression by 17 beta-estradiol in the rat uterus. Mol. Endocrinol. 1991, 5:829-835.
37. Helvering L.M., Liu R., Kulkarni N.H., Wei T., Chen P., Huang S., et al. Expression profiling of rat femur revealed suppression of bone formation genes by treatment with alendronate and estrogen but not raloxifene. Mol. Pharmacol. 2005, 68:1225-1238.
38. Cohen F.J., Watts S., Shah A., Akers R., Plouffe L. Uterine effects of 3-year raloxifene therapy in postmenopausal women younger than age 60. Obstet. Gynecol. 2000, 95:104-110.
39. Delmas P.D., Bjarnason N.H., Mitlak B.H., Ravoux A.C., Shah A.S., Huster W.J., et al. Effects of raloxifene on bone mineral density, serum cholesterol concentrations and uterine endometrium in posmenopausal women. N. Engl. J. Med. 1997, 337:1641-1647.
40. Jolly E.E., Bjarnason N.H., Neven P., Plouffe L., Johnston C.C., Watts S.D., et al. Prevention of osteoporosis and uterine effects in postmenopausal women taking raloxifene for 5 years. Menopause 2003, 10:337-344.
41. Elovic R.P., Hipp J.A., Hayes W.C. Maxillary molar extraction causes increased bone loss in the mandible of ovariectomized rats. J. Bone Miner. Res. 1995, 10:1087-1093.
42. Hsieh Y.D., Devlin H., Mccord F. The effect of ovariectomy on the healing tooth socket of the rat. Arch. Oral. Biol. 1995, 40:529-531.
43. Jahangiri L., Kim A., Nishimura I. Effect of ovariectomy on the local residual ridge remodeling. J. Prosthet. Dent. 1997, 77:435-443.
44. Shimizu M., Sasaki T., Ishihara A., Furuya R., Kawawa T. Bone wound healing after maxillary molar extraction in ovariectomized aged rats. J. Electron. Microsc. 1995, 47:517-526.
45. Shimizu M., Furuya R., Kawawa T., Sasaki T. Bone wound healing after maxillary molar extraction in ovariectomized aged rats: quantitative backscattered electron image analysis. Anat. Rec. 2000, 259:76-85.
46. Teófilo J.M., Brentegani L.G., Lamano-Carvalho T.L. Bone healing in osteoporotic female rats following intra-alveolar grafting of bioactive glass. Arch. Oral. Biol. 2004, 49:755-762.
47. Duarte M.P., de Assis D.R., Casati M.Z., Sallum A.W., Sallum E.A., Nociti F.H. Alendronate may protect against increased periodontitis-related bone loss in estrogen-deficient rats. J. Periodontol. 2004, 75:1196-1202.
48. Duarte P.M., Gonçalves P.F., Sallum A.W., Sallum E.A., Casati M.Z., Humberto Nociti F. Effect of an estrogen-deficient state and its therapy on bone loss resulting from an experimental periodontitis in rats. J. Periodont. Res. 2004, 39:107-110.
49. Nociti F.H., Sallum A.W., Sallum E.A., Duarte P.M. Effect of estrogen replacement and calcitonin therapies on bone around titanium implants placed in ovariectomized rats: a histometric study. Int. J. Oral. Maxillofac. Implants 2002, 17:786-792.
50. Duarte P.M., Gonçalves P.F., Casati M.Z., de Toledo S., Sallum E.A., Nociti F.H. Estrogen and alendronate therapies may prevent the influence of estrogen deficiency on the tooth-supporting alveolar bone: a histometric study in rats. J. Periodont. Res. 2006, 41:541-546.
51. Zecchin K.G., Pereira M.C., Coletta R.D., Graner E., Jorge J. Ovariectomy reduces the gelatinolytic activity and expression of matrix metalloproteinases and collagen in rat molar extraction wounds. Calcif. Tissue Int. 2005, 76:136-145.
52. Ivaska K.K., Hentunen T.A., Vääräniemi J., Ylipahkala H., Pettersson K., Väänänen H.K. Release of intact and fragmented osteocalcin molecules from bone matrix during bone resorption in vitro. J. Biol. Chem. 2004, 279:18361-18369.
53. Kim D.J., Park B.L., Koh J.M., Kim G.S., Kim L.H., Cheong H.S., et al. Methionine synthase reductase polymorphisms are associated with serum osteocalcin levels in postmenopausal women. Exp. Mol. Med. 2006, 38:519-524.
54. Di Carlo C., Tommaselli G.A., Gargano V., Sammartino A., Bifulco G., Tauchmanova L., et al. Effects of estrogen-progestin therapy on serum levels of RANKL, osteoprotegerin, osteocalcin, leptin, and ghrelin in postmenopausal women. Menopause 2007, 14:38-44.
55. Dickson I.R. Bone. Connective tissue and its heritable disorders 1993, 249-285. Wiley-Liss, New York. P. Royce, B. Steinmann (Eds.).
56. Price P.A., Parthemore J.G., Deftos L.J. New biochemical marker for bone metabolism. J. Clin. Invest. 1980, 66:878-883.
57. Helvering L.M., Riting Liu R., Kulkarni N.H., Wei T., Chen P., Huang S., et al. Expression profiling of rat femur revealed suppression of bone formation genes by treatment with alendronate and estrogen but not raloxifene. Mol. Pharmacol. 2005, 68:1225-1238.
58. Cao Y., Mori S., Mashiba T., Westmore M.S., Ma L., Sato M., et al. Raloxifene, estrogen and alendronate affect the processes of fracture repair differently in ovariectomized rats. J. Bone Miner. Res. 2002, 17:2237-2246.
59. Stepan J.J., Alenfeld F., Boivin G., Feyen J.H., Lakatos P. Mechanisms of action of antiresorptive therapies of postmenopausal osteoporosis. Endocr. Regul. 2003, 37:227-240.
60. Mann V., Huber C., Kogianni G., Collins F., Noble B. The antioxidant effect of estrogen and selective estrogen receptor modulators in the inhibition of osteocyte apoptosis in vitro. Bone 2007, 40:674-684.
61. Iwamoto J., Yeh J.K., Schmidt A., Rowley E., Stanfield L., Takeda T., et al. Raloxifene and vitamin K2 combine to improve the femoral neck strength of ovariectomized rats. Calcif. Tissue Int. 2005, 77:119-126.
62. Takano-Yamamoto T., Rodan G.A. Direct effects of 17-estradiol on trabecular bone in ovariectomized rats. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:2172-2176.
63. van den Wijngaard A., Mulder W.R., Dijkema R., Boersma C.J., Mosselman S., van Zoelen E.J., et al. Antiestrogens specifically up-regulate bone morphogenetic protein-4 promoter activity in human osteoblastic cells. Mol. Endocrinol. 2000, 14:623-633.
64. Tou L., Quibria N., Alexander J.M. Regulation of human cbfa1 gene transcription in osteoblasts by selective estrogen receptor modulators (SERMs). Mol. Cell. Endocrinol. 2001, 183:71-79.
65. Messalli E.M., Mainini G., Scaffa C., Cafiero A., Salzillo P.L., Ragucci A., et al. Raloxifene therapy interacts with serum osteoprotegerin in postmenopausal women. Maturitas 2007, 56:38-44.
66. August M., Chung K., Chang Y., Glowacki J. Influence of estrogen status on endosseous implant osseointegration. J. Oral. Maxillofac. Surg. 2001, 59:1285-1289.