Glucocorticoid dose determines osteocyte cell fate

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3366-3376

  Jia, Junjing ^a   Yao, Wei ^a   Guan, Min ^a   Dai, Weiwei ^a   Shahnazari, Mohammad ^a   Kar, Rekha ^b   Bonewald, Lynda ^c   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)

^c UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Antioxidant; Apoptosis; Autophagy; LC3; MLO Y4 cell; Osteoporosis

Indexed keywords

ANTIOXIDANT; CATHEPSIN K; DEXAMETHASONE; HYDROCORTISONE; OSTEOCALCIN; PLACEBO; PREDNISOLONE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL FATE; CELL LINE; CONTROLLED STUDY; CORTICAL BONE; DOSE RESPONSE; DRUG PELLET; FEMUR; GENE ACTIVATION; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OSTEOCYTE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRABECULAR BONE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CATHEPSIN K; CELL LINE; DELAYED-ACTION PREPARATIONS; DEXAMETHASONE; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCOCORTICOIDS; MALE; MICE; OSTEOCYTES; PREDNISOLONE;

MUS;

EID: 80053931553     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-182519     Document Type: Article

References (79)

1. Saag, K. G. (2002) Glucocorticoid use in rheumatoid arthritis. Curr. Rheumatol. Rep. 4, 218-225
2. Saag, K. G., Shane, E., Boonen, S., Marin, F., Donley, D. W., Taylor, K. A., Dalsky, G. P., and Marcus, R. (2007) Teriparatide or alendronate in glucocorticoid-induced osteoporosis. N. Engl. J. Med. 357, 2028-2039 (Pubitemid 350106710)
3. Lane, N. E., Sanchez, S., Modin, G. W., Genant, H. K., Pierini, E., and Arnaud, C. D. (1998) Parathyroid hormone treatment can reverse corticosteroid-induced osteoporosis. Results of a randomized controlled clinical trial. J. Clin. Invest. 102, 1627-1633 (Pubitemid 28492231)
4. Lane, N. E., Sanchez, S., Modin, G. W., Genant, H. K., Pierini, E., and Arnaud, C. D. (2000) Bone mass continues to increase at the hip after parathyroid hormone treatment is discontinued in glucocorticoid-induced osteoporosis: results of a randomized controlled clinical trial. J. Bone Miner. Res. 15, 944-951 (Pubitemid 30233419)
5. Dalle Carbonare, L., Arlot, M. E., Chavassieux, P. M., Roux, J. P., Portero, N. R., and Meunier, P. J. (2001) Comparison of trabecular bone microarchitecture and remodeling in glucocorticoid- induced and postmenopausal osteoporosis. J. Bone. Miner. Res. 16, 97-103 (Pubitemid 32046193)
6. Van Staa, T. P., Laan, R. F., Barton, I. P., Cohen, S., Reid, D. M., and Cooper, C. (2003) Bone density threshold and other predictors of vertebral fracture in patients receiving oral glucocorticoid therapy. Arthritis Rheum. 48, 3224-3229 (Pubitemid 37409336)
7. Chiodini, I., Carnevale, V., Torlontano, M., Fusilli, S., Guglielmi, G., Pileri, M., Modoni, S., Di Giorgio, A., Liuzzi, A., Minisola, S., Cammisa, M., Trischitta, V., and Scillitani, A. (1998) Alterations of bone turnover and bone mass at different skeletal sites due to pure glucocorticoid excess: study in eumenorrheic patients with Cushing's syndrome. J. Clin. Endocrinol. Metab. 83, 1863-1867 (Pubitemid 28496307)
8. Bonewald, L. (2006) Osteocytes as multifunctional cells. J. Musculoskelet. Neuronal Interact. 6, 331-333
9. Boass, A., Ramp, W. K., and Toverud, S. U. (1981) Hypocalcemic, hypophosphatemic rickets in rat pups suckling vitamin D-deprived mothers. Endocrinology 109, 505-512 (Pubitemid 11040205)
10. Qing, H., and Bonewald, L. F. (2009) Osteocyte remodeling of the perilacunar and pericanalicular matrix. Int. J. Oral. Sci. 1, 59-65
11. Lester, D. R., Jr., and Seifert, M. F. (1996) Maternal high calcium diet fails to reverse rickets in the osteosclerotic mouse. Clin. Orthop. Relat. Res. 330, 271-280
12. Rasmussen, P. (1977) Calcium deficiency, pregnancy, and lactation in rats. Microscopic and microradiographic observations on bones. Calcif. Tissue Res. 23, 95-102
13. Teti, A., and Zallone, A. (2009) Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44, 11-16
14. Belanger, L. F. (1969) Osteocytic osteolysis. Calcif. Tissue Res. 4, 1-12
15. Bonewald, L. F. (2007) Osteocytes as dynamic multifunctional cells. Ann. N. Y. Acad. Sci. 1116, 281-290
16. Feng, J. Q., Ye, L., and Schiavi, S. (2009) Do osteocytes contribute to phosphate homeostasis? Curr. Opin. Nephrol. Hypertens. 18, 285-291
17. Fukumoto, S. (2009) The role of bone in phosphate metabolism. Mol. Cell. Endocrinol. 310, 63-70
18. Fukumoto, S., and Martin, T. J. (2009) Bone as an endocrine organ. Trends Endocrinol. Metab. 20, 230-236
19. Xia, X., Kar, R., Gluhak-Heinrich, J., Yao, W., Lane, N. E., Bonewald, L. F., Biswas, S. K., Lo, W. K., and Jiang, J. X. (2010) Glucocorticoid induced autophagy in osteocytes. J. Bone Miner. Res. 25, 2479-2488
20. Harman, D. (1992) Role of free radicals in aging and disease. Ann. N. Y. Acad. Sci. 673, 126-141
21. Harman, D. (1988) Free radicals in aging. Mol. Cell. Biochem. 84, 155-161
22. Hotchkiss, R. S., Strasser, A., McDunn, J. E., and Swanson, P. E. (2009) Cell death. N. Engl. J. Med. 361, 1570-1583
23. He, C., and Klionsky, D. J. (2009) Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93
24. Chen, J. L., Lin, H. H., Kim, K. J., Lin, A., Ou, J. H., and Ann, D. K. (2009) PKCδ signaling: a dual role in regulating hypoxic stress-induced autophagy and apoptosis. Autophagy 5, 244-246
25. Martinet, W., Agostinis, P., Vanhoecke, B., Dewaele, M., and De Meyer, G. R. (2009) Autophagy in disease: a double-edged sword with therapeutic potential. Clin. Sci. (Lond.) 116, 697-712
26. Todde, V., Veenhuis, M., and van der Klei, I. J. (2009) Autophagy: principles and significance in health and disease. Biochim. Biophys. Acta 1792, 3-13
27. Mizushima, N., Levine, B., Cuervo, A. M., and Klionsky, D. J. (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (Pubitemid 351317450)
28. Tsujimoto, Y., and Shimizu, S. (2005) Another way to die: autophagic programmed cell death. Cell Death Differ. 12(Suppl. 2), 1528-1534 (Pubitemid 41553989)
29. Maiuri, M. C., Zalckvar, E., Kimchi, A., and Kroemer, G. (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 8, 741-752 (Pubitemid 47312826)
30. Shibata, M., Lu, T., Furuya, T., Degterev, A., Mizushima, N., Yoshimori, T., MacDonald, M., Yankner, B., and Yuan, J. (2006) Regulation of intracellular accumulation of mutant Huntingtin by Beclin 1. J. Biol. Chem. 281, 14474-14485 (Pubitemid 43848378)
31. Walther, F. J., Jobe, A. H., and Ikegami, M. (1998) Repetitive prenatal glucocorticoid therapy reduces oxidative stress in the lungs of preterm lambs. J. Appl. Physiol. 85, 273-278 (Pubitemid 28334936)
32. Ferioli, M. E., Pinotti, O., and Pirona, L. (1999) Polyamine oxidase activity in lymphoid tissues of glucocorticoid-treated rats. Biochem. Pharmacol. 58, 1907-1914
33. Ogasawara, M., Nomura, K., Shibata, N., Ujihara, M., Kobayashi, M., and Demura, H. (1999) Surgical stress increases renal glutathione content via increased glucocorticoid, and resistance to subsequent oxidative injury in the rat: significant link between endocrine response and cell defense system under the stress. Endocr. J. 46, 99-106 (Pubitemid 29197753)
34. Adcock, I. M., and Ito, K. (2005) Glucocorticoid pathways in chronic obstructive pulmonary disease therapy. Proc. Am. Thorac. Soc. 2, 313-319; discussion 340-341
35. Lee, C. W., Chuang, J. H., Wang, P. W., Chang, N. K., Wang, H. C., Huang, C. C., Tiao, M. M., and Lo, S. K. (2006) Effect of glucocorticoid pretreatment on oxidative liver injury and survival in jaundiced rats with endotoxin cholangitis. World J. Surg. 30, 2217-2226 (Pubitemid 44888809)
36. Ong, S. L., Zhang, Y., and Whitworth, J. A. (2008) Reactive oxygen species and glucocorticoid-induced hypertension. Clin. Exp. Pharmacol. Physiol. 35, 477-482 (Pubitemid 351326783)
37. Laane, E., Tamm, K. P., Buentke, E., Ito, K., Khahariza, P., Oscarsson, J., Corcoran, M., Bjorklund, A. C., Hultenby, K., Lundin, J., Heyman, M., Soderhall, S., Mazur, J., Porwit, A., Pandolfi, P. P., Zhivotovsky, B., Panaretakis, T., and Grander, D. (2009) Cell death induced by dexamethasone in lymphoid leukemia is mediated through initiation of autophagy. Cell Death Differ. 16, 1018-1029
38. O'Brien, C. A., Jia, D., Plotkin, L. I., Bellido, T., Powers, C. C., Stewart, S. A., Manolagas, S. C., and Weinstein, R. S. (2004) Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 145, 1835-1841 (Pubitemid 38402392)
39. Weinstein, R. S. (2001) Glucocorticoid-induced osteoporosis. Rev. Endocr. Metab. Disord. 2, 65-73
40. Weinstein, R. S. (2007) Is long-term glucocorticoid therapy associated with a high prevalence of asymptomatic vertebral fractures? Nat. Clin. Pract. 3, 86-87
41. Weinstein, R. S., Chen, J. R., Powers, C. C., Stewart, S. A., Landes, R. D., Bellido, T., Jilka, R. L., Parfitt, A. M., and Manolagas, S. C. (2002) Promotion of osteoclast survival and antagonism of bisphosphonate-induced osteoclast apoptosis by glucocorticoids. J. Clin. Invest. 109, 1041-1048 (Pubitemid 34408579)
42. Weinstein, R. S., Jilka, R. L., Parfitt, A. M., and Manolagas, S. C. (1998) Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J. Clin. Invest. 102, 274-282 (Pubitemid 28335186)
43. Lane, N. E., Yao, W., Balooch, M., Nalla, R. K., Balooch, G., Habelitz, S., Kinney, J. H., and Bonewald, L. F. (2006) 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. 21, 466-476
44. Lane, N. E., Yao, W., Nakamura, M. C., Humphrey, M. B., Kimmel, D., Huang, X., Sheppard, D., Ross, F. P., and Teitelbaum, S. L. (2005) Mice lacking the integrin β5 subunit have accelerated osteoclast maturation and increased activity in the estrogen-deficient state. J. Bone Miner. Res. 20, 58-66 (Pubitemid 41716219)
45. Yao, W., Cheng, Z., Shahnazari, M., Dai, W., Johnson, M. L., and Lane, N. (2010) Overexpression of secreted frizzled-related protein 1 inhibits bone formation and attenuates PTH bone anabolic effects. J. Bone Miner. Res. 25, 190-199
46. Yao, W., Cheng, Z., Busse, C., Pham, A., Nakamura, M. C., and Lane, N. E. (2008) 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. 58, 1674-1686 (Pubitemid 351847520)
47. Yao, W., Cheng, Z., Koester, K. J., Ager, J. W., Balooch, M., Pham, A., Chefo, S., Busse, C., Ritchie, R. O., and Lane, N. E. (2007) The degree of bone mineralization is maintained with single intravenous bisphosphonates in aged estrogen-deficient rats and is a strong predictor of bone strength. Bone 41, 804-812 (Pubitemid 47576830)
48. Yao, W., Cheng, Z., Pham, A., Busse, C., Zimmermann, E. A., Ritchie, R. O., and Lane, N. E. (2008) Glucocorticoid-induced bone loss in mice can be reversed by the actions of parathyroid hormone and risedronate on different pathways for bone formation and mineralization. Arthritis Rheum. 58, 3485-3497
49. Kalajzic, I., Braut, A., Guo, D., Jiang, X., Kronenberg, M. S., Mina, M., Harris, M. A., Harris, S. E., and Rowe, D. W. (2004) Dentin matrix protein 1 expression during osteoblastic differentiation, generation of an osteocyte GFP-transgene. Bone 35, 74-82 (Pubitemid 38789150)
50. Rowe, P. S., Matsumoto, N., Jo, O. D., Shih, R. N., Oconnor, J., Roudier, M. P., Bain, S., Liu, S., Harrison, J., and Yanagawa, N. (2006) Correction of the mineralization defect in hyp mice treated with protease inhibitors CA074 and pepstatin. Bone 39, 773-786 (Pubitemid 44335882)
51. Kato, Y., Windle, J. J., Koop, B. A., Mundy, G. R., and Bonewald, L. F. (1997) Establishment of an osteocyte-like cell line, MLOY4. J. Bone Miner. Res. 12, 2014-2023 (Pubitemid 27524478)
52. Edinger, A. L. (2009) Starvation in the midst of plenty: making sense of ceramide-induced autophagy by analysing nutrient transporter expression. Biochem. Soc. Trans. 37, 253-258
53. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., and Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111 (Pubitemid 38316219)
54. Plotkin, L. I., Weinstein, R. S., Parfitt, A. M., Roberson, P. K., Manolagas, S. C., and Bellido, T. (1999) Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J. Clin. Invest. 104, 1363-1374
55. Eisenberg-Lerner, A., Bialik, S., Simon, H. U., and Kimchi, A. (2009) Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ. 16, 966-975
56. Tanida, I., Ueno, T., and Kominami, E. (2004) LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36, 2503-2518 (Pubitemid 39119762)
57. Almeida, M., Han, L., Martin-Millan, M., Plotkin, L. I., Stewart, S. A., Roberson, P. K., Kousteni, S., O'Brien, C. A., Bellido, T., Parfitt, A. M., Weinstein, R. S., Jilka, R. L., and Manolagas, S. C. (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J. Biol. Chem. 282, 27285-27297 (Pubitemid 47501960)
58. Muthusami, S., Ramachandran, I., Muthusamy, B., Vasudevan, G., Prabhu, V., Subramaniam, V., Jagadeesan, A., and Narasimhan, S. (2005) Ovariectomy induces oxidative stress and impairs bone antioxidant system in adult rats. Clin. Chim. Acta 360, 81-86 (Pubitemid 41225396)
59. Jilka, R. L., Almeida, M., Ambrogini, E., Han, L., Roberson, P. K., Weinstein, R. S., and Manolagas, S. C. (2010) Decreased oxidative stress and greater bone anabolism in the aged, when compared to the young, murine skeleton with parathyroid hormone administration. Aging Cell 9, 851-867
60. Almeida, M., Han, L., Ambrogini, E., Bartell, S. M., and Manolagas, S. C. (2010) Oxidative stress stimulates apoptosis and activates NF-κB in osteoblastic cells via a PKCβ/p66shc signaling cascade: counter regulation by estrogens or androgens. Mol. Endocrinol. 24, 2030-2037
61. Manolagas, S. C. (2010) From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr. Rev. 31, 266-300
62. Almeida, M., Martin-Millan, M., Ambrogini, E., Bradsher, R., 3rd, Han, L., Chen, X. D., Roberson, P. K., Weinstein, R. S., O'Brien, C. A., Jilka, R. L., and Manolagas, S. C. (2010) Estrogens attenuate oxidative stress and the differentiation and apoptosis of osteoblasts by DNA-binding-independent actions of the ERα. J. Bone. Miner. Res. 25, 769-781
63. Orzechowski, A., Ostaszewski, P., Wilczak, J., Jank, M., Balasinska, B., Wareski, P., and Fuller, J., Jr. (2002) 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. 49, 256-263 (Pubitemid 135748530)
64. Jilka, R. L., Weinstein, R. S., Parfitt, A. M., and Manolagas, S. C. (2007) Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. J. Bone Miner. Res. 22, 1492-1501 (Pubitemid 351229319)
65. Komatsu, F., Kudoh, H., and Kagawa, Y. (2007) 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. 62, 459-464 (Pubitemid 47065716)
66. Planey, S. L., Abrams, M. T., Robertson, N. M., and Litwack, G. (2003) Role of apical caspases and glucocorticoid-regulated genes in glucocorticoid-induced apoptosis of pre-B leukemic cells. Cancer Res. 63, 172-178 (Pubitemid 36070437)
67. Bonapace, L., Bornhauser, B. C., Schmitz, M., Cario, G., Ziegler, U., Niggli, F. K., Schafer, B. W., Schrappe, M., Stanulla, M., and Bourquin, J. P. (2010) Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J. Clin. Invest. 120, 1310-1323
68. Ke, H. Z., Jee, W. S., Ito, H., Setterberg, R. B., Li, M., Lin, B. Y., Liang, X. G., and Ma, Y. F. (1993) Greater bone formation induction occurred in aged than young cancellous bone sites. Bone 14, 481-485 (Pubitemid 23175771)
69. Jee, W. S., Li, X. J., and Schaffler, M. B. (1991) Adaptation of diaphyseal structure with aging and increased mechanical usage in the adult rat: a histomorphometrical and biomechanical study. Anat. Rec. 230, 332-338
70. Jee, W. S., and Li, X. J. (1990) Adaptation of cancellous bone to overloading in the adult rat: a single photon absorptiometry and histomorphometry study. Anat. Rec. 227, 418-426 (Pubitemid 20222174)
71. Yao, W., Jee, W. S., Chen, J., Liu, H., Tam, C. S., Cui, L., Zhou, H., Setterberg, R. B., and Frost, H. M. (2000) Making rats rise to erect bipedal stance for feeding partially prevented orchidectomy- induced bone loss and added bone to intact rats. J. Bone Miner. Res. 15, 1158-1168 (Pubitemid 30350079)
72. Yao, W., Jee, W. S., Chen, J., Tam, C. S., Setterberg, R. B., and Frost, H. M. (2000) Erect bipedal stance exercise partially prevents orchidectomy-induced bone loss in the lumbar vertebrae of rats. Bone 27, 667-675
73. Bonewald, L. F. (2011) The amazing osteocyte. J. Bone Miner. Res. 26, 229-238
74. Srinivas, V., Bohensky, J., Zahm, A. M., and Shapiro, I. M. (2009) Autophagy in mineralizing tissues: microenvironmental perspectives. Cell Cycle 8, 391-393
75. Tsuchihara, K., Fujii, S., and Esumi, H. (2009) Autophagy and cancer: dynamism of the metabolism of tumor cells and tissues. Cancer Lett. 278, 130-138
76. Kroemer, G., and Jaattela, M. (2005) Lysosomes and autophagy in cell death control. Nat. Rev. Cancer 5, 886-897 (Pubitemid 41746033)
77. Gonzalez-Polo, R. A., Boya, P., Pauleau, A. L., Jalil, A., Larochette, N., Souquere, S., Eskelinen, E. L., Pierron, G., Saftig, P., and Kroemer, G. (2005) The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J. Cell Sci. 118, 3091-3102 (Pubitemid 41149913)
78. Bardeguez, A. D., Skurnick, J. H., Perez, G., Colon, J. M., Kloser, P., and Denny, T. N. (1997) Lymphocyte shedding from genital tract of human immunodeficiency virus-infected women: immunophenotypic and clinical correlates. Am. J. Obstet. Gynecol. 176, 158-165 (Pubitemid 127780765)
79. Evans, B. J., McDowall, A., Taylor, P. C., Hogg, N., Haskard, D. O., and Landis, R. C. (2006) Shedding of lymphocyte function-associated antigen-1 (LFA-1) in a human inflammatory response. Blood 107, 3593-3599