Glucocorticoids and osteocyte autophagy

Bone

Volumn 54, Issue 2, 2013, Pages 279-284

  Yao, Wei ^a   Dai, Weiwei ^a   Jiang, Jean X ^b   Lane, Nancy E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Autophagy; Bone fragility; Glucocorticoids

Indexed keywords

DEXAMETHASONE; FIBROBLAST GROWTH FACTOR 23; GLUCOCORTICOID; PREDNISOLONE;

APOPTOSIS; AUTOPHAGY; BONE FRAGILITY; BONE MINERALIZATION; BONE REMODELING; CALCIUM METABOLISM; CELL FUNCTION; CELL VIABILITY; CORTICAL BONE; CORTICOSTEROID INDUCED OSTEOPOROSIS; CYTOKINE PRODUCTION; DOSE RESPONSE; DRUG EFFECT; DRUG EXPOSURE; DRUG MECHANISM; DRUG MEGADOSE; GENE EXPRESSION; HUMAN; LONG TERM EXPOSURE; LOW DRUG DOSE; MINERAL METABOLISM; MOLECULAR DYNAMICS; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCYTE; OSTEOLYSIS; REVIEW;

ANIMALS; AUTOPHAGY; BONE RESORPTION; GLUCOCORTICOIDS; HUMANS; MINERALS; OSTEOCYTES;

EID: 84875833728     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.01.034     Document Type: Review

References (83)

1. Sebaldt R.J., Ioannidis G., Adachi J.D., Bensen W.G., Bianchi F., Cividino A., et al. 36month intermittent cyclical etidronate treatment in patients with established corticosteroid induced osteoporosis. J Rheumatol 1999, 26:1545-1549.
2. Adachi J.D., Bensen W.G., Brown J., Hanley D., Hodsman A., Josse R., et al. Intermittent etidronate therapy to prevent corticosteroid-induced osteoporosis. N Engl J Med 1997, 337:382-387.
3. Bolland M.J., Grey A.B., Horne A.M., Briggs S.E., Thomas M.G., Ellis-Pegler R.B., et al. Annual zoledronate increases bone density in highly active antiretroviral therapy-treated human immunodeficiency virus-infected men: a randomized controlled trial. J Clin Endocrinol Metab 2007, 92:1283-1288.
4. Saag K.G., Shane E., Boonen S., Marin F., Donley D.W., Taylor K.A., et al. Teriparatide or alendronate in glucocorticoid-induced osteoporosis. N Engl J Med 2007, 357:2028-2039.
5. Saag K.G., Emkey R., Schnitzer T.J., Brown J.P., Hawkins F., Goemaere S., et al. Alendronate for the prevention and treatment of glucocorticoid-induced osteoporosis. Glucocorticoid-induced osteoporosis intervention study group. N Engl J Med 1998, 339:292-299.
6. Reid D.M., Devogelaer J.P., Saag K., Roux C., Lau C.S., Reginster J.Y., et al. Zoledronic acid and risedronate in the prevention and treatment of glucocorticoid-induced osteoporosis (HORIZON): a multicentre, double-blind, double-dummy, randomised controlled trial. Lancet 2009, 373:1253-1263.
7. Caplan L., Saag K.G. Glucocorticoids and the risk of osteoporosis. Expert Opin Drug Saf 2009, 8:33-47.
8. Van Staa T.P., Laan R.F., Barton I.P., Cohen S., Reid D.M., Cooper C. Bone density threshold and other predictors of vertebral fracture in patients receiving oral glucocorticoid therapy. Arthritis Rheum 2003, 48:3224-3229.
9. Mart G., Gomez R., Jodar E., Loinaz C., Moreno E., Hawkins E. Long-term follow-up of bone mass after orthotopic liver transplantation: effect of steroid withdrawal from the immunosuppressive regimen. Osteoporos Int 2002, 13:147-150.
10. Lane N.E., Mroczkowski P.J., Hochberg M.C. Prevention and management of glucocorticoid-induced osteoporosis. Bull Rheum Dis 1995, 44:1-4.
11. Black D.M., Kelly M.P., Genant H.K., Palermo L., Eastell R., Bucci-Rechtweg C., et al. Bisphosphonates and fractures of the subtrochanteric or diaphyseal femur. N Engl J Med 2010, 362:1761-1771.
12. Dalle Carbonare L., Arlot M.E., Chavassieux P.M., Roux J.P., Portero N.R., Meunier P.J. Comparison of trabecular bone microarchitecture and remodeling in glucocorticoid-induced and postmenopausal osteoporosis. J Bone Miner Res 2001, 16:97-103.
13. Weinstein R.S. Glucocorticoid-induced osteoporosis. Rev Endocr Metab Disord 2001, 2:65-73.
14. Dempster D.W. Bone histomorphometry in glucocorticoid-induced osteoporosis. J Bone Miner Res 1989, 4:137-141.
15. Dalle Carbonare L., Chavassieux P.M., Arlot M.E., Meunier P.J. Bone histomorphometry in untreated and treated glucocorticoid-induced osteoporosis. Front Horm Res 2002, 30:37-48.
16. Saag K.G. Glucocorticoid use in rheumatoid arthritis. Curr Rheumatol Rep 2002, 4:218-225.
17. Mazziotti G., Angeli A., Bilezikian J.P., Canalis E., Giustina A. Glucocorticoid-induced osteoporosis: an update. Trends Endocrinol Metab 2006, 17:144-149.
18. Jia D., O'Brien C.A., Stewart S.A., Manolagas S.C., Weinstein R.S. Glucocorticoids act directly on osteoclasts to increase their life span and reduce bone density. Endocrinology 2006, 147:5592-5599.
19. Kim H.J., Zhao H., Kitaura H., Bhattacharyya S., Brewer J.A., Muglia L.J., et al. Glucocorticoids suppress bone formation via the osteoclast. J Clin Invest 2006, 116:2152-2160.
20. Canalis E., Bilezikian J.P., Angeli A., Giustina A. Perspectives on glucocorticoid-induced osteoporosis. Bone 2004, 34:593-598.
21. Weinstein R.S., Jilka R.L., Parfitt A.M., Manolagas S.C. Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J Clin Invest 1998, 102:274-282.
22. Ohnaka K., Tanabe M., Kawate H., Nawata H., Takayanagi R. Glucocorticoid suppresses the canonical Wnt signal in cultured human osteoblasts. Biochem Biophys Res Commun 2005, 329:177-181.
23. Krishnan V., Bryant H.U., Macdougald O.A. Regulation of bone mass by Wnt signaling. J Clin Invest 2006, 116:1202-1209.
24. Yao W., Cheng Z., Busse C., Pham A., Nakamura M.C., Lane N.E. Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. Arthritis Rheum 2008, 58:1674-1686.
25. Ohnaka K., Taniguchi H., Kawate H., Nawata H., Takayanagi R. Glucocorticoid enhances the expression of dickkopf-1 in human osteoblasts: novel mechanism of glucocorticoid-induced osteoporosis. Biochem Biophys Res Commun 2004, 318:259-264.
26. Li J., Sarosi I., Cattley R.C., Pretorius J., Asuncion F., Grisanti M., et al. Dkk1-mediated inhibition of Wnt signaling in bone results in osteopenia. Bone 2006, 39:754-766.
27. Smith E., Frenkel B. Glucocorticoids inhibit the transcriptional activity of LEF/TCF in differentiating osteoblasts in a glycogen synthase kinase-3beta-dependent and -independent manner. J Biol Chem 2005, 280:2388-2394.
28. Ito S., Suzuki N., Kato S., Takahashi T., Takagi M. Glucocorticoids induce the differentiation of a mesenchymal progenitor cell line, ROB-C26 into adipocytes and osteoblasts, but fail to induce terminal osteoblast differentiation. Bone 2007, 40:84-92.
29. O'Brien C.A., Jia D., Plotkin L.I., Bellido T., Powers C.C., Stewart S.A., et al. Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 2004, 145:1835-1841.
30. Lane N.E., Yao W., Balooch M., Nalla R.K., Balooch G., Habelitz S., et al. Glucocorticoid-treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo-treated or estrogen-deficient mice. J Bone Miner Res 2006, 21:466-476.
31. Boulos P., Ioannidis G., Adachi J.D. Glucocorticoid-induced osteoporosis. Curr Rheumatol Rep 2000, 2:53-61.
32. Lukert B.P. Glucocorticoid-induced osteoporosis. South Med J 1992, 85:2S48-51.
33. Yoshiko Y., Wang H., Minamizaki T., Ijuin C., Yamamoto R., Suemune S., et al. Mineralized tissue cells are a principal source of FGF23. Bone 2007, 40:1565-1573.
34. Mirams M., Robinson B.G., Mason R.S., Nelson A.E. Bone as a source of FGF23: regulation by phosphate?. Bone 2004, 35:1192-1199.
35. Fukumoto S., Martin T.J. Bone as an endocrine organ. Trends Endocrinol Metab 2009, 20:230-236.
36. Dupond J.L., Mahammedi H., Prie D., Collin F., Gil H., Blagosklonov O., et al. Oncogenic osteomalacia: diagnostic importance of fibroblast growth factor 23 and F-18 fluorodeoxyglucose PET/CT scan for the diagnosis and follow-up in one case. Bone 2005, 36:375-378.
37. Liu S., Tang W., Zhou J., Vierthaler L., Quarles L.D. Distinct roles for intrinsic osteocyte abnormalities and systemic factors in regulation of FGF23 and bone mineralization in Hyp mice. Am J Physiol Endocrinol Metab 2007, 293:E1636-E1644.
38. Wang H., Yoshiko Y., Yamamoto R., Minamizaki T., Kozai K., Tanne K., et al. Overexpression of fibroblast growth factor 23 suppresses osteoblast differentiation and matrix mineralization in vitro. J Bone Miner Res 2008, 23:939-948.
39. Ubaidus S., Li M., Sultana S., de Freitas P.H., Oda K., Maeda T., et al. FGF23 is mainly synthesized by osteocytes in the regularly distributed osteocytic lacunar canalicular system established after physiological bone remodeling. J Electron Microsc (Tokyo) 2009, 58(6):381-392.
40. Weber T.J., Liu S., Indridason O.S., Quarles L.D. Serum FGF23 levels in normal and disordered phosphorus homeostasis. J Bone Miner Res 2003, 18:1227-1234.
41. Liu S., Zhou J., Tang W., Menard R., Feng J.Q., Quarles L.D. Pathogenic role of Fgf23 in Dmp1-null mice. Am J Physiol Endocrinol Metab 2008, 295:E254-E261.
42. Juppner H., Wolf M., Salusky I.B. FGF-23: more than a regulator of renal phosphate handling?. J Bone Miner Res 2010, 25:2091-2097.
43. Kurosu H., Ogawa Y., Miyoshi M., Yamamoto M., Nandi A., Rosenblatt K.P., et al. Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem 2006, 281:6120-6123.
44. Goebel S., Lienau J., Rammoser U., Seefried L., Wintgens K.F., Seufert J., et al. FGF23 is a putative marker for bone healing and regeneration. J Orthop Res 2009, 27:1141-1146.
45. Bonewald L. Osteocytes as multifunctional cells. J Musculoskelet Neuronal Interact 2006, 6:331-333.
46. Bonewald L.F. Osteocytes as dynamic multifunctional cells. Ann N Y Acad Sci 2007, 1116:281-290.
47. Sitara D., Kim S., Razzaque M.S., Bergwitz C., Taguchi T., Schuler C., et al. Genetic evidence of serum phosphate-independent functions of FGF-23 on bone. PLoS Genet 2008, 4:e1000154.
48. Martin A., Liu S., David V., Li H., Karydis A., Feng J.Q., et al. Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. FASEB J 2011, 25:2551-2562.
49. Bonewald L.F. Mechanosensation and transduction in osteocytes. Bonekey Osteovision 2006, 3:7-15.
50. Feng J.Q., Ward L.M., Liu S., Lu Y., Xie Y., Yuan B., et al. Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet 2006, 38:1310-1315.
51. Harris S.E., Gluhak-Heinrich J., Harris M.A., Yang W., Bonewald L.F., Riha D., et al. DMP1 and MEPE expression are elevated in osteocytes after mechanical loading in vivo: theoretical role in controlling mineral quality in the perilacunar matrix. J Musculoskelet Neuronal Interact 2007, 7:313-315.
52. Irie K., Ejiri S., Sakakura Y., Shibui T., Yajima T. Matrix mineralization as a trigger for osteocyte maturation. J Histochem Cytochem 2008, 56:561-567.
53. Noble B.S. The osteocyte lineage. Arch Biochem Biophys 2008, 473:106-111.
54. Belanger L.F. Osteocytic osteolysis. Calcif Tissue Res 1969, 4:1-12.
55. Krempien B., Manegold C., Ritz E., Bommer J. The influence of immobilization on osteocyte morphology: osteocyte differential count and electron microscopical studies. Virchows Arch A Pathol Anat Histol 1976, 370:55-68.
56. Mercer R.R., Crenshaw M.A. The role of osteocytes in bone resorption during lactation: morphometric observations. Bone 1985, 6:269-274.
57. Qing La H., Dusevich V., Dallas M., Wysolmerski J.J., Bonewald L.F. Osteocytic perilacunar remodeling as a significant source of calcium during lactation. J Bone Miner Res 2008, 23:S410.
58. Heuck F. Investigations of the mineral content of the osteocyte halos. Calcif Tissue Res 1968, 81-81a. [Suppl.].
59. Eisenberg-Lerner A., Bialik S., Simon H.U., Kimchi A. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 2009, 16:966-975.
60. Hotchkiss R.S., Strasser A., McDunn J.E., Swanson P.E. Cell death. N Engl J Med 2009, 361:1570-1583.
61. Martinet W., Agostinis P., Vanhoecke B., Dewaele M., De Meyer G.R. Autophagy in disease: a double-edged sword with therapeutic potential. Clin Sci (Lond) 2009, 116:697-712.
62. Tsujimoto Y., Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ 2005, 12(Suppl. 2):1528-1534.
63. Tanida I., Ueno T., Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 2004, 36:2503-2518.
64. Cross C.E., Halliwell B., Borish E.T., Pryor W.A., Ames B.N., Saul R.L., et al. Oxygen radicals and human disease. Ann Intern Med 1987, 107:526-545.
65. Monastyrska I., Rieter E., Klionsky D.J., Reggiori F. Multiple roles of the cytoskeleton in autophagy. Biol Rev Camb Philos Soc 2009, 84:431-448.
66. van Lierop A.H., Witteveen J.E., Hamdy N.A., Papapoulos S.E. Patients with primary hyperparathyroidism have lower circulating sclerostin levels than euparathyroid controls. Eur J Endocrinol 2010, 163:833-837.
67. Fernandez L.A., Macsween J.M. The spontaneous shedding of the lymphocyte receptor for sheep red blood cells. Dev Comp Immunol 1977, 1:385-394.
68. Gooi J.H., Pompolo S., Karsdal M.A., Kulkarni N.H., Kalajzic I., McAhren S.H., et al. Calcitonin impairs the anabolic effect of PTH in young rats and stimulates expression of sclerostin by osteocytes. Bone 2010, 46:1486-1497.
69. Rondanelli E.G., Magliulo E., Carosi G., Dionisi D. Cytoplasmic shedding as a mode of formation of lymphocyte- like blast cells by newt histiocytes. Acta Haematol 1968, 40:67-74.
70. Xia X., Kar R., Gluhak-Heinrich J., Yao W., Lane N.E., Bonewald L.F., et al. Glucocorticoid induced autophagy in osteocytes. J Bone Miner Res 2010, 25(11):2479-2488.
71. Gurusamy N., Das D.K. Is autophagy a double-edged sword for the heart?. Acta Physiol Hung 2009, 96:267-276.
72. Plotkin L.I., Weinstein R.S., Parfitt A.M., Roberson P.K., Manolagas S.C., Bellido T. Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J Clin Invest 1999, 104:1363-1374.
73. Orzechowski A., Ostaszewski P., Wilczak J., Jank M., Balasinska B., Wareski P., et al. Rats with a glucocorticoid-induced catabolic state show symptoms of oxidative stress and spleen atrophy: the effects of age and recovery. J Vet Med A Physiol Pathol Clin Med 2002, 49:256-263.
74. Adcock I.M., Ito K. Glucocorticoid pathways in chronic obstructive pulmonary disease therapy. Proc Am Thorac Soc 2005, 2:313-319. [discussion 340-1].
75. Jilka R.L., Weinstein R.S., Parfitt A.M., Manolagas S.C. Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. J Bone Miner Res 2007, 22:1492-1501.
76. Komatsu F., Kudoh H., Kagawa Y. Evaluation of oxidative stress and effectiveness of low-dose glucocorticoid therapy on exacerbation of chronic obstructive pulmonary disease. J Gerontol A Biol Sci Med Sci 2007, 62:459-464.
77. Ong S.L., Zhang Y., Whitworth J.A. Reactive oxygen species and glucocorticoid-induced hypertension. Clin Exp Pharmacol Physiol 2008, 35:477-482.
78. Planey S.L., Abrams M.T., Robertson N.M., Litwack G. Role of apical caspases and glucocorticoid-regulated genes in glucocorticoid-induced apoptosis of pre-B leukemic cells. Cancer Res 2003, 63:172-178.
79. Bonapace L., Bornhauser B.C., Schmitz M., Cario G., Ziegler U., Niggli F.K., et al. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J Clin Invest 2010, 120:1310-1323.
80. Jia J., Yao W., Guan M., Dai W., Shahnazari M., Kar R., et al. Glucocorticoid dose determines osteocyte cell fate. FASEB J 2011, 25:3366-3376.
81. Maiuri M.C., Tasdemir E., Criollo A., Morselli E., Vicencio J.M., Carnuccio R., et al. Control of autophagy by oncogenes and tumor suppressor genes. Cell Death Differ 2009, 16:87-93.
82. Tasdemir E., Maiuri M.C., Orhon I., Kepp O., Morselli E., Criollo A., et al. p53 represses autophagy in a cell cycle-dependent fashion. Cell Cycle 2008, 7:3006-3011.
83. Weinstein R.S., Jia D., Powers C.C., Stewart S.A., Jilka R.L., Parfitt A.M., et al. The skeletal effects of glucocorticoid excess override those of orchidectomy in mice. Endocrinology 2004, 145:1980-1987.