Increased circulating heat shock protein 60 induced by menopause, stimulates apoptosis of osteoblast-lineage cells via up-regulation of toll-like receptors

Bone

Volumn 45, Issue 1, 2009, Pages 68-76

  Kim, Yang Soon ^b   Koh, Jung Min ^a   Lee, Young Sun ^b   Kim, Beom Jun ^a   Lee, Seung Hun ^a   Lee, Ki Up ^a   Kim, Ghi Su ^a  

^a University of Ulsan College of Medicine   (South Korea)

^b Asan Institute for Life Sciences   (South Korea)

Author keywords

Apoptosis; Heat shock protein 60; Osteoblasts; Toll like receptors

Indexed keywords

CASPASE 3; CASPASE 9; CYTOCHROME C; HEAT SHOCK PROTEIN 60; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ADULT; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MENOPAUSE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOLYSIS; OVARIECTOMY; POSTMENOPAUSE; POSTMENOPAUSE OSTEOPOROSIS; PREMENOPAUSE; PROTEIN EXPRESSION; RECEPTOR UPREGULATION;

ADULT; ANIMALS; APOPTOSIS; BONE RESORPTION; CASPASES; CELL LINEAGE; CELL SURVIVAL; CHAPERONIN 60; FEMALE; HUMANS; MENOPAUSE; MICE; MICE, KNOCKOUT; MIDDLE AGED; MITOCHONDRIA; OSTEOBLASTS; OVARIECTOMY; POSTMENOPAUSE; PREMENOPAUSE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; UP-REGULATION;

EID: 67349183354     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2009.03.658     Document Type: Article

References (46)

1. Riggs B.L., Khosla S., and Melton III L.J. Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 23 (2002) 279-302
2. Heaney R.P., Recker R.R., and Saville P.D. Menopausal changes in bone remodeling. J. Lab. Clin. Med. 92 (1978) 964-970
3. Khosla S., Atkinson E.J., Melton III L.J., and Riggs B.L. Effects of age and estrogen status on serum parathyroid hormone levels and biochemical markers of bone turnover in women: a population-based study. J. Clin. Endocrinol. Metab. 82 (1997) 1522-1527
4. Ross P.D., and Knowlton W. Rapid bone loss is associated with increased levels of biochemical markers. J. Bone Miner. Res. 13 (1998) 297-302
5. Garnero P., Sornay-Rendu E., Chapuy M.C., and Delmas P.D. Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. J. Bone Miner. Res. 11 (1996) 337-349
6. Bord S., Beavan S., Ireland D., Horner A., and Compston J.E. Mechanisms by which high-dose estrogen therapy produces anabolic skeletal effects in postmenopausal women: role of locally produced growth factors. Bone 29 (2001) 216-222
7. Khastgir G., Studd J., Holland N., Alaghband-Zadeh J., Fox S., and Chow J. Anabolic effect of estrogen replacement on bone in postmenopausal women with osteoporosis: histomorphometric evidence in a longitudinal study. J. Clin. Endocrinol. Metab. 86 (2001) 289-295
8. Taxel P., Kennedy D.G., Fall P.M., Willard A.K., Clive J.M., and Raisz L.G. The effect of aromatase inhibition on sex steroids, gonadotropins, and markers of bone turnover in older men. J. Clin. Endocrinol. Metab. 86 (2001) 2869-2874
9. Okazaki R., Inoue D., Shibata M., Saika M., Kido S., Ooka H., et al. Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) alpha or beta. Endocrinology 143 (2002) 2349-2356
10. Fujita M., Urano T., Horie K., Ikeda K., Tsukui T., Fukuoka H., et al. Estrogen activates cyclin-dependent kinases 4 and 6 through induction of cyclin D in rat primary osteoblasts. Biochem. Biophys. Res. Commun. 299 (2002) 222-228
11. Kousteni S., Bellido T., Plotkin L.I., O'Brien C.A., Bodenner D.L., Han L., et al. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104 (2001) 719-730
12. Raisz L.G. Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J. Clin. Invest. 115 (2005) 3318-3325
13. Gao Y., Qian W.P., Dark K., Toraldo G., Lin A.S., Guldberg R.E., et al. Estrogen prevents bone loss through transforming growth factor beta signaling in T cells. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16618-16623
14. Hughes D.E., Dai A., Tiffee J.C., Li H.H., Mundy G.R., and Boyce B.F. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat. Med. 2 (1996) 1132-1136
15. Gullo C.A., and Teoh G. Heat shock proteins: to present or not, that is the question. Immunol. Lett. 94 (2004) 1-10
16. Lewthwaite J., Owen N., Coates A., Henderson B., and Steptoe A. Circulating human heat shock protein 60 in the plasma of British civil servants: relationship to physiological and psychosocial stress. Circulation 106 (2002) 196-201
17. Pockley A.G., Bulmer J., Hanks B.M., and Wright B.H. Identification of human heat shock protein 60 (Hsp60) and anti-Hsp60 antibodies in the peripheral circulation of normal individuals. Cell Stress Chaperones 4 (1999) 29-35
18. Meghji S., Lillicrap M., Maguire M., Tabona P., Gaston J.S., Poole S., et al. Human chaperonin 60 (Hsp60) stimulates bone resorption: structure/function relationships. Bone 33 (2003) 419-425
19. Reddi K., Meghji S., Nair S.P., Arnett T.R., Miller A.D., Preuss M., et al. The Escherichia coli chaperonin 60 (groEL) is a potent stimulator of osteoclast formation. J. Bone Miner. Res. 13 (1998) 1260-1266
20. Kim S.H., Lee S.U., Kim M.H., Kim B.T., and Min Y.K. Mitogenic estrogen metabolites alter the expression of 17beta-estradiol-regulated proteins including heat shock proteins in human MCF-7 breast cancer cells. Mol. Cells 20 (2005) 378-384
21. Voss M.R., Stallone J.N., Li M., Cornelussen R.N., Knuefermann P., and Knowlton A.A. Gender differences in the expression of heat shock proteins: the effect of estrogen. Am. J. Physiol, Heart Circ. Physiol. 285 (2003) H687-H692
22. Byun C.H., Koh J.M., Kim D.K., Park S.I., Lee K.U., and Kim G.S. Alpha-lipoic acid inhibits TNF-alpha-induced apoptosis in human bone marrow stromal cells. J. Bone Miner. Res. 20 (2005) 1125-1135
23. Kim D.J., Koh J.M., Lee O., Kim N.J., Lee Y.S., Kim Y.S., et al. Homocysteine enhances apoptosis in human bone marrow stromal cells. Bone 39 (2006) 582-590
24. Kim G.S., Hong J.S., Kim S.W., Koh J.M., An C.S., Choi J.Y., et al. Leptin induces apoptosis via ERK/cPLA2/cytochrome c pathway in human bone marrow stromal cells. J. Biol. Chem. 278 (2003) 21920-21929
25. Cheng S.L., Yang J.W., Rifas L., Zhang S.F., and Avioli L.V. Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. Endocrinology 134 (1994) 277-286
26. Kim C.H., Cheng S.L., and Kim G.S. Lack of autocrine effects of IL-6 on human bone marrow stromal osteoprogenitor cells. Endocr. Res. 23 (1997) 181-190
27. Koh J.M., Lee Y.S., Kim Y.S., Kim D.J., Kim H.H., Park J.Y., et al. Homocysteine enhances bone resorption by stimulation of osteoclast formation and activity through increased intracellular ROS generation. J. Bone Miner. Res. 21 (2006) 1003-1011
28. Liu X., Kim C.N., Yang J., Jemmerson R., and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86 (1996) 147-157
29. Kol A., Bourcier T., Lichtman A.H., and Libby P. Chlamydial and human heat shock protein 60s activate human vascular endothelium, smooth muscle cells, and macrophages. J. Clin. Invest. 103 (1999) 571-577
30. Vabulas R.M., Ahmad-Nejad P., da Costa C., Miethke T., Kirschning C.J., Hacker H., et al. Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276 (2001) 31332-31339
31. Akira S., Uematsu S., and Takeuchi O. Pathogen recognition and innate immunity. Cell 124 (2006) 783-801
32. Maruyama K., Sano G., and Matsuo K. Murine osteoblasts respond to LPS and IFN-gamma similarly to macrophages. J. Bone Miner. Metab. 24 (2006) 454-460
33. Hou L., Sasaki H., and Stashenko P. Toll-like receptor 4-deficient mice have reduced bone destruction following mixed anaerobic infection. Infect. Immun. 68 (2000) 4681-4687
34. Kousteni S., Chen J.R., Bellido T., Han L., Ali A.A., O'Brien C.A., et al. Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science 298 (2002) 843-846
35. Manolagas S.C. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev. 21 (2000) 115-137
36. Hock J.M., Krishnan V., Onyia J.E., Bidwell J.P., Milas J., and Stanislaus D. Osteoblast apoptosis and bone turnover. J. Bone Miner. Res. 16 (2001) 975-984
37. Bottero V., Rossi F., Samson M., Mari M., Hofman P., and Peyron J.F. Ikappa b-alpha, the NF-kappa B inhibitory subunit, interacts with ANT, the mitochondrial ATP/ADP translocator. J. Biol. Chem. 276 (2001) 21317-21324
38. Petronilli V., Penzo D., Scorrano L., Bernardi P., and Di Lisa F. The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J. Biol. Chem. 276 (2001) 12030-12034
39. Zamora M., Merono C., Vinas O., and Mampel T. Recruitment of NF-kappaB into mitochondria is involved in adenine nucleotide translocase 1 (ANT1)-induced apoptosis. J. Biol. Chem. 279 (2004) 38415-38423
40. Aoki M., Nata T., Morishita R., Matsushita H., Nakagami H., Yamamoto K., et al. Endothelial apoptosis induced by oxidative stress through activation of NF-kappaB: antiapoptotic effect of antioxidant agents on endothelial cells. Hypertension 38 (2001) 48-55
41. Choi W.S., Eom D.S., Han B.S., Kim W.K., Han B.H., Choi E.J., et al. Phosphorylation of p38 MAPK induced by oxidative stress is linked to activation of both caspase-8- and -9-mediated apoptotic pathways in dopaminergic neurons. J. Biol. Chem. 279 (2004) 20451-20460
42. Ghatan S., Larner S., Kinoshita Y., Hetman M., Patel L., Xia Z., et al. p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J. Cell Biol. 150 (2000) 335-347
43. Zhou F.H., Foster B.K., Zhou X.F., Cowin A.J., and Xian C.J. TNF-alpha mediates p38 MAP kinase activation and negatively regulates bone formation at the injured growth plate in rats. J. Bone Miner. Res. 21 (2006) 1075-1088
44. Ranford J.C., and Henderson B. Chaperonins in disease: mechanisms, models, and treatments. Mol. Pathol. 55 (2002) 209-213
45. Kol A., Lichtman A.H., Finberg R.W., Libby P., and Kurt-Jones E.A. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J. Immunol. 164 (2000) 13-17
46. Chen W., Wang J., An H., Zhou J., Zhang L., and Cao X. Heat shock up-regulates TLR9 expression in human B cells through activation of ERK and NF-kappaB signal pathways. Immunol. Lett. 98 (2005) 153-159