Decrease in the number and apoptosis of alveolar bone osteoclasts in estrogen-treated rats

Journal of Periodontal Research

Volumn 42, Issue 3, 2007, Pages 193-201

  Faloni, A P S ^a   Sasso Cerri, E ^b   Katchburian, E ^a   Cerri, P S ^b  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Alveolar bone; Estradiol; Osteoclast; Programmed cell death

Indexed keywords

ACID PHOSPHATASE; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ESTROGEN; ISOENZYME; TARTRATE-RESISTANT ACID PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL; APOPTOSIS; ARTICLE; CYTOLOGY; DRUG EFFECT; FEMALE; JAW; NICK END LABELING; OSTEOCLAST; OSTEOLYSIS; RAT; TRANSMISSION ELECTRON MICROSCOPY;

ACID PHOSPHATASE; ALVEOLAR PROCESS; ANIMALS; APOPTOSIS; BONE RESORPTION; ESTROGENS; FEMALE; IN SITU NICK-END LABELING; ISOENZYMES; MICROSCOPY, ELECTRON, TRANSMISSION; OSTEOCLASTS; RATS;

EID: 34247501842     PISSN: 00223484     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0765.2006.00932.x     Document Type: Article

References (53)

1. Sleeve KT, Marc P, Sandrine T, Dominique H, Yannick F. IL-6, RANKL, TNF-α/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev 2004; 15:49-60.
2. Raisz LG, Rodan GA. Embryology and cellular biology of bone. In: Avioli LV, Krane SM, eds. Metabolic Bone Disease and Clinically Related Disorders. New York: Academic Press, 1998:1-22.
3. Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 2000;21:115-137.
4. Bernick S, Ershoff BH. Histochemical study of bone in estrogen-treated rats. J Dent Res 1963;42:981-989.
5. Tapp E. The effects of hormones on bone in growing rats. J Bone Joint Surg Br 1966;48:526-531.
6. Liu CC, Howard GA. Bone-cell changes in estrogen-induced bone-mass increase in mice: dissociation of osteoclasts from bone surfaces. Anat Rec 1991;229: 240-250.
7. Tanaka M, Ejiri S, Toyooka E, Kohno S, Ozawa H. Effects of ovariectomy on trabecular structures of rat alveolar bone. J Periodont Res 2002;37:161-165.
8. Duarte PM, Gonçalves PF, Sallum AW, Sallum EA, Casati MZ, Nociti Jr FH. Effect of an estrogen-deficient state and its therapy on bone loss resulting from an experimental periodontitis in rats. J Petriodont Res 2004;39:107-110.
9. Aubin JE, Bonnelye E. Osteoprotegerin and its ligand: a new paradigm for regulation of osteoclastogenesis and bone resorption. Oxteoparox Int 2000;11:905-913.
10. Hofbauer LC, Kuhne CA, Viereck V. The OPG/RANKL/RANK system in metabolic bone diseases. J Musculoskelet Neuronal Interact 2004;3:268-275.
11. Hofbauer LC, Schoppet M. Clinical implications of the osteprotegerin/RANKL/ RANK system for bone and vascular diseases. JAMA 2004;292:490-495.
12. Boyce BF, Yamashita T, Yao Z, Zhang Q, Li F, Xing L. Roles for NF-KappaB and c-fos in osteoclasts. J Bone Miner Metab 2005;23(suppl):11-15.
13. Hughes DE, Dai A, Tiffee JC, Li HH, Mundy OR, Boyce BF. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-β. Nat Med 1996;2:1132-1135.
14. Rogers A, Saleh G, Hannon RA, Green-field D, Eastell R. Circulating estradiol and osteoprotegerin as determinants of bone turnover and bone density in postmenopausal women. J Clin Endocrinol Metab 2002;87:4470- 4475.
15. Hill PA, Tumber A, Meikle MC. Multiple extracellular signals promote osteoblasts survival and apoptosis. Endocrinology 1997;138:3849- 3858.
16. Tomkinson A, Reeve J, Shaw RW, Noble BS. The death of osteocytes via apoptosis accompanies estrogen withdrawal in human bone. J Clin Endocrinol Metab 1997;82:3128-3135.
17. Tomkinson A, Gevers EF, Wit JM, Reeve J, Noble BS. The role of estrogen in control of rat osteocyte apoptosis. J Bone Miner Res 1998;13:1243-1250.
18. Xing L, Boyce BF. Regulation of apoptosis in osteoclasts and osteoblastic cells. Blochem Biophys Res Commun 2005; 328:709-720.
19. Hughes DE, Boyce BF. Apoptosis in bone physiology and disease. J Clin Pathol: Mol Pathol 1997;50:132-137.
20. Boabaid F, Cerri PS, Katchburian E. Apoptotic bone cells may be engulfed by osteoclasts during alveolar bone resorption in young rats. Tissue Cell 2001;33:318-325.
21. Cerri PS, Boabaid F, Katchburian E. Combined TUNEL and TRAP methods suggest that apoptotic bone cells are inside vacuoles of alveolar bone osteoclasts in young rats. J Periodunt Res 2003;38:223-226.
22. Cerri PS. Osteoblasts engulf apoptotic bodies during alveolar bone formation in the rat maxilla. Anat Rec A Discov Mol Cell Evol Biol 2005;286:833-840.
23. Ou G, Mulari M, Peng Z, Hentunen TA, Väänänen HK. Death of osteocytes turns off the inhibition of osteoclasts and triggers local bone resorption. Biochem Biophys Res Commun 2005;4:1095-1101.
24. Jilka RL, Weinstein RS, Belido T, Parfitt AM, Manolagas SC. Osteoblast programmed cell death (apoptosis): Modulation by growth factors and cytokines. J Bone Miner Res 1998; 13:793-802.
25. Marks SC, Schroeder HE. Tooth eruption: theories and facts. Anat Rec 1996;245:374-393.
26. Silberberg M, Silberberg R. Further investigations concerning the influence of estrogen on skeletal tissues. Am J Anat 1941;69:295- 331.
27. Chow JWM, Lean JM, Chambers TJ. 17β-Estradiol stimulates cancellous bone formation in female rats. Endocrinology 1992;130:3025-3032.
28. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
29. Cerri PS, Freymüller E, Katchburian E. Apoptosis in the early developing periodontium of rat molars. Anat Rec 2000;258:136-144.
30. Minkin C. Bone acid phosphatase: tartrate-resistant acid phosphatase as a marker of osteoclast function. Calcif Tissue Int 1982;34:285-290.
31. Kameda T, Mano H, Yuasa T et al. Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts. J Exp Med 1997;186:489-495.
32. Srivastava S, Toraldo G, Weitzmann MN, Cenci SC, Ross FP, Pacifici R. Estrogen decreases osteoclast formation by down-regulating receptor activator of NF-kB ligand (RANKL)-induced INK activation. J Biol Chem 2001:276:8836-8840.
33. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239-257.
34. Wyllie AH, Kerr JFR, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980;68:251-306.
35. Cerri PS, Katchburian E. Apoptosis in the epithelial cells of the rests of Malassez of the periodontium of rat molars. J Periodonl Res 2005;40:365-372.
36. Cohen JJ. Apoptosis: mechanisms of life and death in the immune system. J Allergy Clin Immunol 1999;103:548-554.
37. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004;116:205-219.
38. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis and autolytic cell death: a cautionary note. Hepatology 1995;21:1465-1468.
39. Torres C, Munell F, Roig M, Reventós J, Macaya A. Naturally occurring cell death during postnatal development of rat skeletal muscle. Muscle Nerve 2002;26:777-783.
40. Elmardi AS, Katchburian MV, Katchburian E. Electron microscopy of developing calvaria reveals images that suggest that osteoclasts engulf and destroy osteocytes during bone resorption. Calcif Tissue Int 1990;46:239-245.
41. Taniwaki NN, Katchburian E. Ultrastructural and lanthanum tracer examination of rapidly resorbing rat alveolar bone suggests that osteoclasts internalize dying bone cells. Cell Tissue Res 1998;293:173-176.
42. Ito M, Amizuka N, Nakajima T, Ozawa H. Ultrastructural and cytochemical studies on cell death of osteoclasts induced by bisphosphonate treatment. Bone 1999;25:447-452.
43. Ito M, Amizuka N, Nakajima T, Ozawa H. Bisphosphonate acts on osteoclasts independent of ruffled borders in osteoclerotic (oc/oc) mice. Bone 2001;28:609-616.
44. Huppertz B, Frank HG, Kaufmann P. The apoptosis cascade - morphological and immunohistochemical methods for its visualization. Anat Embryol 1999;200:1-18.
45. Clarke PGH. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 1990;181:195-213.
46. Roach HI, Clarke NMP. 'Cell paralysis' as an intermediate stage in the programmed cell death of epiphyseal chondrocytes during development. J Bonn Miner Res 1999;14:1367-1378.
47. Raff M. Cell suicide for beginners. Nature 1998;396:119- 122.
48. Kanieda T, Ishikawa H, Tsutsui T. Detection and characterization of apoptosis in osteoclasts in vitro. Biochem Biophys Res Commun 1995;207:753-760.
49. Noxon SJ, King GJ, Ou G, Huang G. Osteoclast clearance from periodontal tis sues during orthodontic tooth movement. Am J Orthod Dentofacial Orthop 2001;120:466-476.
50. Cenci S, Weitzmann MN, Roggia C et al. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-α. J Clin Invest 2000;106:1229-1237.
51. Pacifici R. Estrogen, cytokines and pathogenesis of postmenopausal osteoporosis. J Bons Miner Res 1996;11:1043-1051.
52. Hainey L, Batra G, Selby PL, Saunders P, Hoyland JA, Braidman IP. Oestrogen receptor beta in vivo in osteoclasts and other bone cells of adult men and women [abstract]. J Bone Miner Res 2000;15:1217.
53. Bonnelye E, Kung V, Laplace C, Galson DL, Aubin JE. Estrogen receptor-related receptor a impinges on the estrogen axis in bone: potential function in osteoporosis. Endocrinology 2002;143:3658-3670.