Mechanical induction of PGE2 in osteocytes blocks glucocorticoid-induced apoptosis through both the β-catenin and PKA pathways

Journal of Bone and Mineral Research

Volumn 25, Issue 12, 2010, Pages 2657-2668

  Kitase, Yukiko ^a,b   Barragan, Leonardo ^a   Qing, Hai ^a   Kondoh, Shino ^a,c   Jiang, Jean X ^d   Johnson, Mark L ^a   Bonewald, Lynda F ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF TOKYO   (Japan)

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

Author keywords

Apoptosis; MLO Y4 Cells; Osteocytes; WNT Signaling

Indexed keywords

BETA CATENIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOCORTICOID; INDOMETACIN; LITHIUM CHLORIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E2; SMALL INTERFERING RNA; WNT PROTEIN; DEXAMETHASONE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E RECEPTOR 4; PROTECTIVE AGENT; PROTEIN KINASE B;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL NUCLEUS TRANSPLANTATION; ENZYME ACTIVATION; FLUID FLOW; GLYCOGEN SYNTHESIS; LOADING TEST; MOUSE; NONHUMAN; OSTEOCYTE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SHEAR STRESS; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CELL NUCLEUS; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; FLOW KINETICS; MECHANICAL STRESS; METABOLISM; PROTEIN STABILITY; PROTEIN TRANSPORT;

ANIMALS; APOPTOSIS; BETA CATENIN; CELL LINE; CELL NUCLEUS; CULTURE MEDIA, CONDITIONED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DEXAMETHASONE; DINOPROSTONE; GLUCOCORTICOIDS; GLYCOGEN SYNTHASE KINASE 3; INDOMETHACIN; LITHIUM CHLORIDE; MICE; MODELS, BIOLOGICAL; OSTEOCYTES; PHOSPHATIDYLINOSITOL 3-KINASE; PROTECTIVE AGENTS; PROTEIN STABILITY; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, PROSTAGLANDIN E, EP2 SUBTYPE; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; RHEOLOGY; SIGNAL TRANSDUCTION; STRESS, MECHANICAL;

EID: 78649542978     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1002/jbmr.168     Document Type: Article

References (60)

1. Osteoporosis prevention, diagnosis, and therapy. NIH Consensus Statement. 2000; 17: 1-45.
2. Dovio A, Perazzolo L, Osella G, et al. Immediate fall of bone formation and transient increase of bone resorption in the course of high-dose, short-term glucocorticoid therapy in young patients with multiple sclerosis. J Clin Endocrinol Metab. 2004; 89: 4923-4928.
3. Dalle Carbonare L, Arlot ME, Chavassieux PM, Roux JP, Portero NR, Meunier PJ., Comparison of trabecular bone microarchitecture and remodeling in glucocorticoid-induced and postmenopausal osteoporosis. J Bone Miner Res. 2001; 16: 97-103.
4. Dempster DW., Bone histomorphometry in glucocorticoid-induced osteoporosis. J Bone Miner Res. 1989; 4: 137-141.
5. Manolagas SC, Weinstein RS., New developments in the pathogenesis and treatment of steroid-induced osteoporosis. J Bone Miner Res. 1999; 14: 1061-1066.
6. Lane NE, Yao W, Balooch M, 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.
7. Bonewald LF., Osteocytes as dynamic, multifunctional cells. Ann N Y Acad Sci. 2007; 1116: 281-290.
8. Taylor D, Hazenberg J, Lee TC., The cellular transducer in bone: What is it ? Technol Health Care. 2006; 14: 367-377.
9. Vezeridis PS, Semeins CM, Chen Q, Klein-Nulend J., Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation. Biochem Biophys Res Commun. 2006; 348: 1082-1088.
10. Kogianni G, Mann V, Noble BS., Apoptotic bodies convey activity capable of initiating osteoclastogenesis and localized bone destruction. J Bone Miner Res. 2008; 23: 915-927.
11. Verborgt O, Gibson GJ, Schaffler MB., Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res. 2000; 15: 60-67.
12. Tatsumi S, Ishii K, Amizuka N, et al. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab. 2007; 5: 464-475.
13. Dunstan CR, Evans RA, Hills E, Wong SY, Higgs RJ., Bone death in hip fracture in the elderly. Calcif Tissue Int. 1990; 47: 270-275.
14. Weinstein RS, Nicholas RW, Manolagas SC., Apoptosis of osteocytes in glucocorticoid-induced osteonecrosis of the hip. J Clin Endocrinol Metab. 2000; 85: 2907-2912.
15. Manolagas SC., Corticosteroids and fractures: a close encounter of the third cell kind. J Bone Miner Res. 2000; 15: 1001-1005.
16. Aguirre JI, Plotkin LI, Stewart SA, et al. Osteocyte apoptosis is induced by weightlessness in mice and precedes osteoclast recruitment and bone loss. J Bone Miner Res. 2006; 21: 605-615.
17. Noble BS, Peet N, Stevens HY, et al. Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol. 2003; 284: C934-C943.
18. Plotkin LI, Mathov I, Aguirre JI, Parfitt AM, Manolagas SC, Bellido T., Mechanical stimulation prevents osteocyte apoptosis: requirement of integrins, Src kinases, and ERKs. Am J Physiol Cell Physiol. 2005; 289: C633-C643.
19. Weinbaum S, Cowin SC, Zeng Y., A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. 1994; 27: 339-360.
20. Hillsley MV, Frangos JA., Bone tissue engineering: the role of interstitial fluid flow. Biotechnol Bioeng. 1994; 43: 573-581.
21. Knothe Tate ML., " Whither flows the fluid in bone?" An osteocyte's perspective. J Biomech. 2003; 36: 1409-1424.
22. Klein-Nulend J, van der Plas A, Semeins CM, et al. Sensitivity of osteocytes to biomechanical stress in vitro. Faseb J. 1995; 9: 441-445.
23. Johnson ML, Kamel MA, Kim-Weroha NA, Holladay B, Kotha SP., Greater sensitivity of osteocytes to shear stress as compared to osteoblasts: PGE2 production and Wnt/b-catenin signaling. J Bone Miner Res. 2007; 22 (Suppl 1): S375.
24. Kamel MA, Kitase Y, Kim-Weroha NA, et al. Fluid flow shear stress and prostaglandin E2 activates b-catenin signaling in MLO-Y4 osteocytic and 2T3 osteoblastic cells. J Bone Miner Res. 2007; 22 (Suppl 1): S375.
25. Xia X, Batra N, Shi Q, Bonewald LF, Sprague E, Jiang JX., Prostaglandin promotion of osteocyte gap junction function through transcriptional regulation of connexin 43 by glycogen synthase kinase 3/b-catenin signaling. Mole Cell Biol. 2010; 30: 206-219.
26. Lin CL, Wang JY, Ko JY, et al. Superoxide destabilization of beta-catenin augments apoptosis of high-glucose-stressed mesangial cells. Endocrinology. 2008; 149: 2934-2942.
27. Lin CL, Wang JY, Huang YT, Kuo YH, Surendran K, Wang FS., Wnt/beta-catenin signaling modulates survival of high glucose-stressed mesangial cells. J Am Soc Nephrol. 2006; 17: 2812-2820.
28. Xie H, Huang Z, Sadim MS, Sun Z., Stabilized beta-catenin extends thymocyte survival by up-regulating Bcl-xL. J Immunol. 2005; 175: 7981-7988.
29. Kato Y, Windle JJ, Koop BA, Mundy GR, Bonewald LF., Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res. 1997; 12: 2014-2023.
30. Plotkin LI, Weinstein RS, Parfitt AM, Roberson PK, Manolagas SC, Bellido T., Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J Clin Invest. 1999; 104: 1363-1374.
31. Ajubi NE, Klein-Nulend J, Nijweide PJ, Vrijheid-Lammers T, Alblas MJ, Burger EH., Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes-a cytoskeleton-dependent process. Biochem Biophys Res Commun. 1996; 225: 62-68.
32. Cherian PP, Siller-Jackson AJ, Gu S, et al. Mechanical strain opens connexin 43 hemichannels in osteocytes: a novel mechanism for the release of prostaglandin. Mol Biol Cell. 2005; 16: 3100-3106.
33. Sugimoto Y, Narumiya S., Prostaglandin E receptors. J Biol Chem. 2007; 282: 11613-11617.
34. Fujino H, West KA, Regan JW., Phosphorylation of glycogen synthase kinase-3 and stimulation of T-cell factor signaling following activation of EP2 and EP4 prostanoid receptors by prostaglandin E2. J Biol Chem. 2002; 277: 2614-2619.
35. Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS., Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science. 2005; 310: 1504-1510.
36. Shao J, Jung C, Liu C, Sheng H., Prostaglandin E2 Stimulates the beta-catenin/T cell factor-dependent transcription in colon cancer. J Biol Chem. 2005; 280: 26565-26572.
37. Jensen J, Brennesvik EO, Lai YC, Shepherd PR., GSK-3beta regulation in skeletal muscles by adrenaline and insulin: evidence that PKA and PKB regulate different pools of GSK-3. Cell Signal. 2007; 19: 204-210.
38. Li M, Wang X, Meintzer MK, Laessig T, Birnbaum MJ, Heidenreich KA., Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3beta. Mol Cell Biol. 2000; 20: 9356-9363.
39. Cherian PP, Cheng B, Gu S, Sprague E, Bonewald LF, Jiang JX., Effects of mechanical strain on the function of Gap junctions in osteocytes are mediated through the prostaglandin EP2 receptor. J Biol Chem. 2003; 278: 43146-43156.
40. Delfino DV, Agostini M, Spinicelli S, Vito P, Riccardi C., Decrease of Bcl-xL and augmentation of thymocyte apoptosis in GILZ overexpressing transgenic mice. Blood. 2004; 104: 4134-4141.
41. Leclerc N, Luppen CA, Ho VV, et al. Gene expression profiling of glucocorticoid-inhibited osteoblasts. J Mol Endocrinol. 2004; 33: 175-193.
42. Dodd JS, Raleigh JA, Gross TS., Osteocyte hypoxia: a novel mechanotransduction pathway. Am J Physiol. 1999; 277 (3 Pt 1): C598-602.
43. Gross TS, Akeno N, Clemens TL, et al. Selected contribution: Osteocytes upregulate HIF-1alpha in response to acute disuse and oxygen deprivation. J Appl Physiol. 2001; 90: 2514-2519.
44. Wang L, Wang Y, Han Y, et al. In situ measurement of solute transport in the bone lacunar-canalicular system. Proc Natl Acad Sci U S A. 2005; 102: 11911-11916.
45. Burger EH, Klein-Nulend J, van der Plas A, Nijweide PJ., Function of osteocytes in bone-their role in mechanotransduction. J Nutr. 1995; 125 (7 Suppl): 2020S-2023S.
46. Bakker A, Klein-Nulend J, Burger E., Shear stress inhibits while disuse promotes osteocyte apoptosis. Biochem Biophys Res Commun. 2004; 320: 1163-1168.
47. Aoudjit L, Potapov A, Takano T., Prostaglandin E2 promotes cell survival of glomerular epithelial cells via the EP4 receptor. Am J Physiol Renal Physiol. 2006; 290: F1534-F1542.
48. Vassiliou E, Sharma V, Jing H, Sheibanie F, Ganea D., Prostaglandin E2 promotes the survival of bone marrow-derived dendritic cells. J Immunol. 2004; 173: 6955-6964. (Pubitemid 39541084)
49. Weinreb M, Shamir D, Machwate M, Rodan GA, Harada S, Keila S., Prostaglandin E2 (PGE2) increases the number of rat bone marrow osteogenic stromal cells (BMSC) via binding the EP4 receptor, activating sphingosine kinase and inhibiting caspase activity. Prostaglandins Leukot Essent Fatty Acids. 2006; 75: 81-90.
50. Machwate M, Harada S, Leu CT, et al. Prostaglandin receptor EP(4) mediates the bone anabolic effects of PGE(2). Mol Pharmacol. 2001; 60: 36-41.
51. Miwa M, Saura R, Hirata S, Hayashi Y, Mizuno K, Itoh H., Induction of apoptosis in bovine articular chondrocyte by prostaglandin E(2) through cAMP-dependent pathway. Osteoarthritis Cartilage. 2000; 8: 17-24.
52. Hull MA, Ko SC, Hawcroft G., Prostaglandin EP receptors: targets for treatment and prevention of colorectal cancer ? Mol Cancer Ther. 2004; 3: 1031-1039. (Pubitemid 39199598)
53. Regan JW., EP2 and EP4 prostanoid receptor signaling. Life Sci. 2003; 74: 143-153.
54. Wang D, Buchanan FG, Wang H, Dey SK, DuBois RN., Prostaglandin E2 enhances intestinal adenoma growth via activation of the Ras-mitogen-activated protein kinase cascade. Cancer Res. 2005; 65: 1822-1829.
55. Wang D, Wang H, Shi Q, et al. Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta. Cancer Cell. 2004; 6: 285-295.
56. Zhang J, Rivest S., Anti-inflammatory effects of prostaglandin E2 in the central nervous system in response to brain injury and circulating lipopolysaccharide. J Neurochem. 2001; 76: 855-864.
57. Lee EO, Shin YJ, Chong YH., Mechanisms involved in prostaglandin E2-mediated neuroprotection against TNF-alpha: possible involvement of multiple signal transduction and beta-catenin/T-cell factor. J Neuroimmunol. 2004; 155: 21-31.
58. Babij P, Zhao W, Small C, et al. High bone mass in mice expressing a mutant LRP5 gene. J Bone Miner Res. 2003; 18: 960-974.
59. Sawakami K, Robling AG, Ai M, et al. The Wnt co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J Biol Chem. 2006; 281: 23698-23711.
60. Bonewald LF, Johnson ML., Osteocytes, mechanosensing and Wnt signaling. Bone. 2008; 42: 606-615.