Bisphosphonate-osteoclasts: Changes in osteoclast morphology and function induced by antiresorptive nitrogen-containing bisphosphonate treatment in osteoporosis patients

Bone

Volumn 59, Issue , 2014, Pages 37-43

  Jobke, Björn ^a   Milovanovic, Petar ^a,b   Amling, Michael ^a   Busse, Björn ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Bisphosphonate osteoclasts; Bisphosphonates; Bone histomorphometry; Osteoclasts; Osteoporosis

Indexed keywords

ALENDRONIC ACID; ALKALINE PHOSPHATASE; BISPHOSPHONIC ACID DERIVATIVE; CALCIUM; CREATININE; IBANDRONIC ACID; NITROGEN; PAMIDRONIC ACID; PHOSPHORUS; VITAMIN D;

ADULT; ALBERS SCHOENBERG DISEASE; ALKALINE PHOSPHATASE BLOOD LEVEL; APOPTOSIS; ARTICLE; BONE BIOPSY; BONE DISEASE; BONE MASS; BONE TURNOVER; CALCIUM BLOOD LEVEL; CELL FUNCTION; CELL STRUCTURE; CELL VIABILITY; CLINICAL ARTICLE; CREATININE BLOOD LEVEL; CYTOSKELETON; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMALE; HUMAN; HUMAN TISSUE; HYPERPARATHYROIDISM; IN VIVO STUDY; MALE; MORPHOMETRICS; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OSTEOPOROSIS; PAGET BONE DISEASE; PHOSPHATE BLOOD LEVEL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS;

BISPHOSPHONATE-OSTEOCLASTS; BISPHOSPHONATES; BONE HISTOMORPHOMETRY; OSTEOCLASTS; OSTEOPOROSIS;

APOPTOSIS; BONE DENSITY CONSERVATION AGENTS; BONE RESORPTION; CELL SHAPE; CELL SIZE; DIPHOSPHONATES; FEMALE; HUMANS; MALE; MIDDLE AGED; NITROGEN; OSTEOCLASTS; OSTEOPOROSIS;

EID: 84888036721     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.10.024     Document Type: Article

References (73)

1. Black D.M., Schwartz A.V., Ensrud K.E., Cauley J.A., Levis S., Quandt S.A., et al. Effects of continuing or stopping alendronate after 5years of treatment - the Fracture Intervention Trial long-term extension (FLEX): a randomized trial. JAMA 2006, 296:2927-2938.
2. Bone H.G., Hosking D., Devogelaer J., Tucci J.R., Emkey R.D., Tonino R.P., et al. Ten years' experience with alendronate for osteoporosis in postmenopausal women. N Engl J Med 2004, 350:1189-1199.
3. Boonen S., Black D.M., Colon-Emeric C.S., Eastell R., Magaziner J.S., Eriksen E.F., et al. Efficacy and safety of a once-yearly intravenous zoledronic acid 5mg for fracture prevention in elderly postmenopausal women with osteoporosis aged 75 and older. J Am Geriatr Soc 2010, 58:292-299.
4. Fleisch H., Russell R.G.G., Francis M.D. Diphosphonates inhibit hydroxyapatite dissolution in vitro and bone resorption in tissue culture and in vivo. Science 1969, 165:1262-1264.
5. Bauer D.C., Garnero P., Hochberg M.C., Santora A., Delmas P., Ewing S.K., et al. Pretreatment levels of bone turnover and the antifracture efficacy of alendronate: the fracture intervention trial. J Bone Miner Res 2006, 21:292-299.
6. Bone H.G., Downs R.W., Tucci J.R., Harris S.T., Weinstein R.S., Licata A.A., et al. Dose-response relationships for alendronate treatment in osteoporotic elderly women. J Clin Endocrinol Metabol 1997, 82:265-274.
7. Borah B., Ritman E.L., Dufresne T.E., Jorgensen S.M., Liu S., Sacha J., et al. The effect of risedronate on bone mineralization as measured by micro-computed tomography with synchrotron radiation: correlation to histomorphometric indices of turnover. Bone 2005, 37:1-9.
8. Delmas P.D., Vrijens B., Eastell R., Roux C., Pols H.A.P., Ringe J.D., et al. Effect of monitoring bone turnover markers on persistence with risedronate treatment of postmenopausal osteoporosis. J Clin Endocrinol Metabol 2007, 92:1296-1304.
9. Eriksen E.F., Melsen F., Sod E., Barton I., Chines A. Effects of long-term risedronate on bone quality and bone turnover in women with postmenopausal osteoporosis. Bone 2002, 31:620-625.
10. Garnero P., Sornay-Rendu E., Duboeuf F., Delmas P.D. Markers of bone turnover predict postmenopausal forearm bone loss over 4years: the OFELY study. J Bone Miner Res 1999, 14:1614-1621.
11. McClung M., Harris S.T., Miller P.D., Bauer D.C., Davison K.S., Dian L., et al. Bisphosphonate therapy for osteoporosis: benefits, risks, and drug holiday. Am J Med 2013, 126:13-20.
12. Watts N.B., Chines A., Olszynski W.P., McKeever C.D., McClung M.R., Zhou X., et al. Fracture risk remains reduced one year after discontinuation of risedronate. Osteoporos Int 2008, 19:365-372.
13. Schilcher J., Koeppen V., Ranstam J., Skripitz R., Michaelsson K., Aspenberg P. Atypical femoral fractures are a separate entity, characterized by highly specific radiographic features. A comparison of 59 cases and 218 controls. Bone 2013, 52:389-392.
14. Schneider J.P., Hinshaw W.B., Su C., Solow P. Atypical femur fractures: 81 individual personal histories. J Clin Endocrinol Metabol 2012, 97:4324-4328.
15. Schilcher J., Michaelsson K., Aspenberg P. Bisphosphonate use and atypical fractures of the femoral shaft. N Eng J Med 2011, 364:1728-1737.
16. Jung T.I., Hoffmann F., Glaeske G., Felsenberg D. Disease-specific risk for an osteonecrosis of the jaw under bisphosphonate therapy. J Cancer Res Clin Oncol 2010, 136:363-370.
17. Odvina C.V., Zerwekh J.E., Rao D.S., Maalouf N., Gottschalk F.A., Pak C.Y.C. Severely suppressed bone turnover: a potential complication of alendronate therapy. J Clin Endocrinol Metabol 2005, 90:1294-1301.
18. Shane E., Burr D., Abrahamsen B., Adler R.A., Brown T.D., Cheung A.M., et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res 2013, 10.1002/jbmr.1998.
19. Shane E., Burr D., Ebeling P.R., Abrahamsen B., Adler R.A., Brown T.D., et al. Atypical subtrochanteric and diaphyseal femoral fractures: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res 2010, 25:2267-2294.
20. Fleisch H. Bisphosphonates - history and experimental basis. Bone 1987, 8:S23-S28.
21. Fisher J.E., Rodan G.A., Reszka A.A. In vivo effects of bisphosphonates on the osteoclast mevalonate pathway. Endocrinology 2000, 141:4793-4796.
22. Gruber H.E., Ivey J.L., Thompson E.R., Chesnut C.H., Baylink D.J. Osteoblast and osteoclast cell number and cell-activity in postmenopausal osteoporosis. Miner Electrolyte Metab 1986, 12:246-254.
23. Weinstein R.S., Bell N.H. Diminished rates of bone-formation in normal black adults. N Eng J Med 1988, 319:1698-1701.
24. Weinstein R.S., Manolagas S.C. Apoptosis and osteoporosis. Am J Med 2000, 108:153-164.
25. Weinstein R.S., Roberson P.K., Manolagas S.C. Giant osteoclast formation and long-term oral bisphosphonate therapy reply. N Eng J Med 2009, 360:1677-1678.
26. Cheung M.S., Glorieux F.H., Rauch F. Large osteoclasts in pediatric osteogenesis imperfecta patients receiving intravenous pamidronate. J Bone Miner Res 2009, 24:669-674.
27. Dempster D.W., Zhou H., Nieves J.W., Barbuto N., Bostrom M., Cosman F., et al. Unusual osteoclast morphology in teriparatide-treated patients who have been pretreated with alendronate. J Bone Miner Res 2007, 22:S29-S.
28. Fisher J.E., Reszka A.A. Evidence that high-dose, intermittent ibandronate and zoledronate inhibit osteoclastic bone resorption through a mechanism independent of the mevalonate pathway. J Bone Miner Res 2006, 21:S414-S415.
29. Jobke B., Kulle B., Semler J., Delling G. Bisphosphonates improve bone microarchitecture in middle-aged males with osteoporosis by reducing bone turnover: a paired biopsy micro-CT analysis over 38months. J Bone Miner Res 2006, 21:S87-S.
30. Glowacki J. The deceiving appearances of osteoclasts. N Eng J Med 2009, 360:80-82.
31. Jobke B. Giant osteoclast formation and long-term oral bisphosphonate therapy. N Eng J Med 2009, 360:1676-1676.
32. Jobke B., Muche B., Burghardt A.J., Semler J., Link T.M., Majumdar S. Teriparatide in bisphosphonate-resistant osteoporosis: microarchitectural changes and clinical results after 6 and 18months. Calcif Tissue Int 2011, 89:130-139.
33. Dunstan C.R., Evans R.A. Quantitative bone histology: a new method. Pathology 1980, 12:255-264.
34. Busse B., Jobke B., Hahn M., Priemel M., Niecke M., Seitz S., et al. Effects of strontium ranelate administration on bisphosphonate-altered hydroxyapatite: matrix incorporation of strontium is accompanied by changes in mineralization and microstructure. Acta Biomater 2010, 6:4513-4521.
35. Jobke B., Burghardt A.J., Muche B., Hahn M., Semler J., Amling M., et al. Trabecular reorganization in consecutive iliac crest biopsies when switching from bisphosphonate to strontium ranelate treatment. PLoS one 2011, 6:e23638.
36. Recker R.R., Weinstein R.S., Chesnut C.H., Schimmer R.C., Mahoney P., Hughes C., et al. Histomorphometric evaluation of daily and intermittent oral ibandronate in women with postmenopausal osteoporosis: results from the BONE study. Osteoporos Int 2004, 15:231-237.
37. Dempster D.W., Compston J.E., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., et al. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2013, 28:1-16.
38. Chavassieux P.M., Arlot M.E., Reda C., Wei L., Yates A.J., Meunier P.J. Histomorphometric assessment of the long-term effects of alendronate on bone quality and remodeling in patients with osteoporosis. J Clin Investig 1997, 100:1475-1480.
39. Kaye M., Zucker S.W., Leclerc Y.G., Prichard S., Hodsman A.B.., Barré P.-E. Osteoclast enlargement in endstage renal disease. Kidney Int 1985, 27:574-581.
40. Chappard D., Rossi J.F., Bataille R., Alexandre C. Osteoclast cytomorphometry demonstrates an abnormal population in B cell malignancies but not in multiple myeloma. Calcif Tissue Int 1991, 48:13-17.
41. Walsh W.R., Walton M., Bruce W., Yu Y., Gillies R.M., Svehla M. Cell structure and biology of bone and cartilage. Handbook of histology methods for bone and cartilage 2003, 35-58. Humana Press, Totowa - New Jersey. Y.H. An, K.L. Martin (Eds.).
42. Safadi F., Barbe M., Abdelmagid S., Rico M., Aswad R., Litvin J., et al. Bone structure, development and bone biology. Bone pathology 2009, 1-51. Humana Press, Philadelphia. J. Khurana (Ed.).
43. Dion N., Petit J.L., Ste-Marie L.G. Atypical osteoclast phenotype after long-term alendronate therapy for osteoporosis: a paired bone biopsies report. J Bone Miner Res 2008, 23:S343-S.
44. Boyle W.J., Simonet W.S., Lacey D.L. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
45. Teitelbaum S.L. Bone resorption by osteoclasts. Science 2000, 289:1504-1508.
46. Katoh Y., Tsuji H., Matsui H., Maruta K., Morita Y. Effects of ethane-1-hydroxy-1, 1-diphosphonate on cell-differentiation, and proteoglycan and calcium-metabolism, in the proximal tibia of young-rats. Bone 1991, 12:59-65.
47. Miller S.C., Jee W.S.S., Kimmel D.B., Woodbury L. Ethane-1-hydroxy-1,1-diphosphonate (EHDP) effects on incorporation and accumulation of osteoclast nuclei. Calcif Tissue Res 1977, 22:243-252.
48. Plasmans C.M.T., Jap P.H.K., Kuijpers W., Slooff T.J.J.H., Wijers M. Influence of a diphosphonate on the cellular aspect of young bone tissue. Calcif Tissue Int 1980, 32:247-256.
49. Rowe D.J., Hausmann E. Alteration of osteoclast morphology by diphosphonates in bone organ-culture. Calcif Tissue Res 1976, 20:53-60.
50. Evans R.A., Howlett C.R., Dunstan C.R., Hills E. The effect of long-term low-dose diphosphonate treatment on rat bone. Clin Orthop Relat Res 1982, 290-299.
51. Thompson E.R., Baylink D.J., Wergedal J.E. Increases in number and size of osteoclasts in response to calcium or phosphorus deficiency in rat. Endocrinology 1975, 97:283-289.
52. Jones S.J., Boyde A. Histomorphometry of how ships lacunae formed invivo and invitro - depths and volumes measured by scanning electron and confocal microscopy. Bone 1993, 14:455-460.
53. Piper K., Boyde A., Jones S.J. The relationship between the number of nuclei of an osteoclast and its resorptive capability invitro. Anat Embryol 1992, 186:291-299.
54. Zheng M.H., Papadimitriou J.M., Nicholson G.C. RNA-synthesis in isolated rat osteoclasts - inhibitory effect of calcitonin. Bone 1991, 12:317-322.
55. Piper K., Boyde A., Jones S.J. Effect of 3-amino-1-hydroxypropylidene-1,1-bisphosphonate (APD) on the resorptive function of osteoclasts of known nuclear number. Calcif Tissue Int 1994, 54:56-61.
56. Hughes D.E., Mian M., Guillandcumming D.F., Russell R.G.G. The cellular mechanism of action of bisphosphonates. Drugs Exp Clin Res 1991, 17:109-114.
57. Rogers M.J., Gordon S., Benford H.L., Coxon F.P., Luckman S.P., Monkkonen J., et al. Cellular and molecular mechanisms of action of bisphosphonates. Cancer 2000, 88:2961-2978.
58. 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.
59. Allen M.R., Erickson A.M., Wang X., Burr D.B., Martin R.B., Hazelwood S.J. Morphological assessment of basic multicellular unit resorption parameters in dogs shows additional mechanisms of bisphosphonate effects on bone. Calcif Tissue Int 2010, 86:67-71.
60. Karsdal M.A., Martin T.J., Bollerslev J., Christiansen C., Henriksen K. Are nonresorbing osteoclasts sources of bone anabolic activity?. J Bone Miner Res 2007, 22:487-494.
61. Ravn P., Fledelius C., Rosenquist C., Overgaard K., Christiansen C. High bone turnover is associated with low bone mass in both pre- and postmenopausal women. Bone 1996, 19:291-298.
62. Ravn P. Bisphosphonates for prevention of postmenopausal osteoporosis. Dan Med Bull 2002, 49:1-18.
63. Ravn P., Thompson D.E., Ross P.D., Christiansen C. Biochemical markers for prediction of 4-year response in bone mass during bisphosphonate treatment for prevention of postmenopausal osteoporosis. Bone 2003, 33:150-158.
64. Brown J.P., Dempster D.W., Ding B.Y., Dent-Acosta R., San Martin J., Grauer A., et al. Bone remodeling in postmenopausal women who discontinued denosumab treatment: off-treatment biopsy study. J Bone Miner Res 2011, 26:2737-2744.
65. Papapoulos S., Chapurlat R., Libanati C., Brandi M.L., Brown J.P., Czerwinski E., et al. Five years of denosumab exposure in women with postmenopausal osteoporosis: results from the first two years of the FREEDOM extension. J Bone Miner Res 2012, 27:694-701.
66. Reid I.R., Miller P.D., Brown J.P., Kendler D.L., Fahrleitner-Pammer A., Valter I., et al. Effects of denosumab on bone histomorphometry: the FREEDOM and STAND studies. J Bone Miner Res 2010, 25:2256-2265.
67. Miller P.D., Bolognese M.A., Lewiecki E.M., McClung M.R., Ding B., Austin M., et al. Effect of denosumab on bone density and turnover in postmenopausal women with low bone mass after long-term continued, discontinued, and restarting of therapy: a randomized blinded phase 2 clinical trial. Bone 2008, 43:222-229.
68. Shyu J.F., Shih C., Tseng C.Y., Lin C.H., Sun D.T., Liu H.T., et al. Calcitonin induces podosome disassembly and detachment of osteoclasts by modulating Pyk2 and Src activities. Bone 2007, 40:1329-1342.
69. Gruber H.E., Norton H.J., Singer F.R. In vivo morphologic changes in the rat osteoclast induced by gallium nitrate: the result of toxicity or other effects?. Miner Electrolyte Metab 1999, 25:127-134.
70. Jobke B., Pfeifer M., Minne H. Teriparatide following bisphosphonates: initial and long-term effects on microarchitecture and bone remodeling at the human iliac crest. Connect Tissue Res 2009, 50:46-54.
71. Jain N., Weinstein R.S. Giant osteoclasts after long-term bisphosphonate therapy: diagnostic challenges. Nat Rev Rheumatol 2009, 5:341-346.
72. Teitelbaum S.L., Coccia P.F., Brown D.M., Kahn A.J. Malignant osteopetrosis - a disease of abnormal osteoclast proliferation. Metab Bone Dis Relat Res 1981, 3:99-105.
73. Rasmussen H., Bordier P. The physiological and cellular basis of metabolic bone disease 1974, Williams and Wilkins Co., Baltimore.