Regulation by heat shock protein 27 of osteocalcin synthesis in osteoblasts

Endocrinology

Volumn 152, Issue 5, 2011, Pages 1872-1882

  Kato, Kenji ^a,b   Adachi, Seiji ^b   Matsushima Nishiwaki, Rie ^b   Minamitani, Chiho ^a   Natsume, Hideo ^a,b   Katagiri, Yasuo ^b   Hirose, Yoshinobu ^b   Mizutani, Jun ^a   Tokuda, Haruhiko ^b,c   Kozawa, Osamu ^b,d   Otsuka, Takanobu ^a  

^a NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^b GIFU UNIVERSITY HOSPITAL   (Japan)

^c NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^d GIFU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOMYCIN; ARSENITE SODIUM; BONE MORPHOGENETIC PROTEIN 4; HEAT SHOCK PROTEIN 27; OSTEOCALCIN; SPHINGOSINE 1 PHOSPHATE;

ANIMAL CELL; ARTICLE; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETIC TRANSFECTION; HEAT STRESS; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS;

3T3 CELLS; ANIMALS; ANISOMYCIN; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 4; CALCIFICATION, PHYSIOLOGIC; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM; EXTRACELLULAR MATRIX; HOT TEMPERATURE; HSP27 HEAT-SHOCK PROTEINS; HUMANS; LYSOPHOSPHOLIPIDS; MICE; MICROSCOPY, FLUORESCENCE; MUTATION; NUCLEIC ACID SYNTHESIS INHIBITORS; OSTEOBLASTS; OSTEOCALCIN; PHOSPHORYLATION; SPHINGOSINE; TIME FACTORS; TRANSFECTION; TRIIODOTHYRONINE;

EID: 79955379858     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-1062     Document Type: Article

References (67)

1. Hendrick JP, Hartl FU 1993 Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62:349-384 (Pubitemid 23237875)
2. Liu AY, Lin Z, Choi HS, Sorhage F, Li B 1989 Attenuated induction of heat shock gene expression in aging diploid fibroblasts. J Biol Chem 264:12037-12045 (Pubitemid 19185380)
3. Taylor RP, Benjamin IJ 2005 Small heat shock proteins: a new classification scheme in mammals. J Mol Cell Cardiol 38:433-444 (Pubitemid 40331934)
4. Benjamin IJ, McMillan DR 1998 Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 83:117-132 (Pubitemid 28354456)
5. Mackay DS, Andley UP, Shiels A 2003 Cell death triggered by a novel mutation in the αA-crystallin gene underlies autosomal dominant cataract linked to chromosome 21q. Eur J Hum Genet 11:784-793 (Pubitemid 37337062)
6. Meehan S, Berry Y, Luisi B, Dobson CM, Carver JA, MacPhee CE 2004 Amyloid fibril formation by lens crystallin proteins and its implications for cataract formation. J Biol Chem 279:3413-3419 (Pubitemid 38140578)
7. Martin JL, Mestril R, Hilal-Dandan R, Brunton LL, Dillmann WH 1997 Small heat shock proteins and protection against ischemic injury in cardiac myocytes. Circulation 96:4343-4348 (Pubitemid 28007464)
8. van Noort JM, van Sechel AC, Bajramovic JJ, El Ouagmiri M, Polman CH, Lassmann H, Ravid R 1995 The small heat-shock protein αB-crystallin as candidate autoantigen in multiple sclerosis. Nature 375:798-801
9. Chelouche-Lev D, Kluger HM, Berger AJ, Rimm DL, Price JE 2004 αB-crystallin as a marker of lymph node involvement in breast carcinoma. Cancer 100:2543-2548 (Pubitemid 38715757)
10. Kostenko S, Moens U 2009 Heat shock protein 27 phosphorylation: kinases, phosphatases, functions and pathology. Cell Mol Life Sci 66:3289-3307
11. Kostenko S, Johannessen M, Moens U 2009 PKA-induced F-actin rearrangement requires phosphorylation of Hsp27 by the MAPKAP kinase MK5. Cell Signal 21:712-718
12. Barutta F, Pinach S, Giunti S, Vittone F, Forbes JM, Chiarle R, Arnstein M, Perin PC, Camussi G, Cooper ME, Gruden G 2008 Heat shock protein expression in diabetic nephropathy. Am J Physiol Renal Physiol 295:F1817-F1824
13. Singh D, McCann KL, Imani F 2007 MAPK and heat shock protein 27 activation are associated with respiratory syncytial virus induction of human bronchial epithelial monolayer disruption. Am J Physiol Lung Cell Mol Physiol 293:L436-L445 (Pubitemid 47205024)
14. Yasuda E, Kumada T, Takai S, Ishisaki A, Noda T, Matsushima-Nishiwaki R, Yoshimi N, Kato K, Toyoda H, Kaneoka Y, Yamaguchi A, Kozawa O 2005 Attenuated phosphorylation of heat shock protein 27 correlates with tumor progression in patients with hepatocellular carcinoma. Biochem Biophys Res Commun 337:337-342 (Pubitemid 41393799)
15. Nijweide PJ, Burger EH, Feyen JH 1986 Cells of bone: proliferation, differentiation, and hormonal regulation. Physiol Rev 66:855-886 (Pubitemid 17181295)
16. Uozaki H, Horiuchi H, Ishida T, Iijima T, Imamura T, Machinami R 1997 Overexpression of resistance-related proteins (metallothio-neins, glutathione-S-transferase pi, heat shock protein 27, and lung resistance-related protein) in osteosarcoma. Relationship with poor prognosis. Cancer 79:2336-2344 (Pubitemid 27251016)
17. Tiffee JC, Griffin JP, Cooper LF 2000 Immunolocalization of stress proteins and extracellular matrix proteins in the rat tibia. Tissue Cell 32:141-147 (Pubitemid 30251276)
18. Leonardi R, Barbato E, Paganelli C, Lo Muzio L 2004 Immunolocalization of heat shock protein 27 in developing jaw bones and tooth germs of human fetuses. Calcif Tissue Int 75:509-516 (Pubitemid 40174510)
19. Lavoie JN, Gingras-Breton G, Tanguay RM, Landry J 1993 Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization. J Biol Chem 268:3420-3429 (Pubitemid 23070978)
20. Blackburn RV, Galoforo SS, Berns CM, Armour EP, McEachern D, Corry PM, Lee YJ 1997 Comparison of tumor growth between hsp25-and hsp27-transfected murine L929 cells in nude mice. Int J Cancer 72:871-877 (Pubitemid 27431533)
21. Hedges JC, Dechert MA, Yamboliev IA, Martin JL, Hickey E, Weber LA, Gerthoffer WT 1999 A role for p38 (MAPK)/HSP27 pathway in smooth muscle cell migration. J Biol Chem 274:24211-24219
22. Shakoori AR, Oberdorf AM, Owen TA, Weber LA, Hickey E, Stein JL, Lian JB, Stein GS 1992 Expression of heat shock genes during differentiation of mammalian osteoblasts and promyelocytic leukemia cells. J Cell Biochem 48:277-287
23. Kozawa O, Otsuka T, Hatakeyama D, Niwa M, Matsuno H, Ito H, Kato K, Matsui N, Uematsu T 2001 Mechanism of prostaglandin D2-stimulated heat shock protein 27 induction in osteoblasts. Cell Signal 13:p535-541 (Pubitemid 32722112)
24. Hatakeyama D, Kozawa O, Niwa M, Matsuno H, Kato K, Tatematsu N, Shibata T, Uematsu T 2001 Inhibition by adenylyl cyclase-cAMP system of ET-1-induced HSP27 in osteoblasts. AmJ Physiol Endocrinol Metab 281:E1260-E1266 (Pubitemid 34001202)
25. Tokuda H, Kozawa O, Niwa M, Matsuno H, Kato K, Uematsu T 2002 Mechanismof prostaglandin E2-stimulated heat shock protein 27 induction in osteoblast-like MC3T3-E1 cells. J Endocrinol 172:271-281 (Pubitemid 34183076)
26. Tokuda H, Niwa M, Ishisaki A, Nakajima K, Ito H, Kato K, Kozawa O 2004 Involvement of stress-activated protein kinase (SAPK)/c-Jun. N-terminal kinase (JNK) in prostaglandin F2α-induced heat shock protein 27 in osteoblasts. Prostaglandins Leukot Essent Fatty Acids 70:441-447 (Pubitemid 38482605)
27. Hayashi K, Takai S, Matsushima-Nishiwaki R, Hanai Y, Kato K, Tokuda H, Kozawa O 2008 (-)-Epigallocatechin gallate reduces transforming growth factor β-stimulated HSP27 induction through the suppression of stress-activated protein kinase/c-Jun. N-terminal kinase in osteoblasts. Life Sci 82:1012-1017
28. Takai S, Tokuda H, Yoshida M, Yasuda E, Matsushima-Nishiwaki R, Harada A, Kato K, Kozawa O 2006 Prostaglandin D2 induces the phosphorylation of HSP27 in osteoblasts: function of the MAP kinase superfamily. Prostaglandins Leukot Essent Fatty Acids 75:61-67 (Pubitemid 44287470)
29. Hauschka PV, Lian JB, Cole DE, Gundberg CM 1989 Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiol Rev 69:990-1047 (Pubitemid 19184853)
30. Lee NK, Karsenty G 2008 Reciprocal regulation of bone and energy metabolism. Trends Endocrinol Metab 19:161-166 (Pubitemid 351847838)
31. Reddi AH 1994 Bone and cartilage differentiation. Curr Opin Genet Dev 4:737-744 (Pubitemid 24322911)
32. Kawabata M, Imamura T, Miyazono K 1998 Signal transduction by bone morphogenetic proteins. Cytokine Growth Factor Rev 9:49-61 (Pubitemid 28280536)
33. Heldin CH, Miyazono K, ten Dijke P 1997 TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465-471 (Pubitemid 28013118)
34. Yamaguchi K, Nagai S, Ninomiya-Tsuji J, Nishita M, Tamai K, Irie K, Ueno N, Nishida E, Shibuya H, Matsumoto K 1999 XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. EMBO J 18:179-187 (Pubitemid 29005034)
35. Kozawa O, Hatakeyama D, Uematsu T 2002 Divergent regulation by p44/p42 MAP kinase and p38 MAP kinase of bone morphoge-neticprotein-4-stimulated osteocalcin synthesis in osteoblasts. J Cell Biochem 84:583-589 (Pubitemid 34111192)
36. Kanno Y, Ishisaki A, Yoshida M, Nakajima K, Tokuda H, Numata O, Kozawa O 2005 Adenylyl cyclase-cAMP system inhibits thyroid hormone-stimulated osteocalcin synthesis in osteoblasts. Mol Cell Endocrinol 229:75-82 (Pubitemid 40018085)
37. Kozawa O, Suzuki A, Kaida T, Tokuda H, Uematsu T1997 Tumor necrosis factor-α autoregulates interleukin-6 synthesis via activation of protein kinase C. Function of sphingosine 1-phosphate and phosphatidylcholine-specific phospholipase C. J Biol Chem 272:25099-25104 (Pubitemid 27415692)
38. Kozawa O, Niwa M, Matsuno H, Tokuda H, Miwa M, Ito H, Kato K, Uematsu T 1999 Sphingosine 1-phosphate induces heat shock protein 27 via p38 mitogen-activated protein kinase activation in osteoblasts. J Bone Miner Res 14:1761-1767 (Pubitemid 29455825)
39. Sudo H, Kodama HA, Amagai Y, Yamamoto S, Kasai S 1983 In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria. J Cell Biol 96:191-198 (Pubitemid 13155577)
40. Kozawa O, Suzuki A, Tokuda H, Uematsu T 1997 Prostaglandin F2α stimulates interleukin-6 synthesis via activation of PKC in osteoblast-like cells. AmJ Physiol 272:E208-E211
41. Natsume H, Tokuda H, Adachi S, Takai S, Matsushima-Nishiwaki R, Kato K, Minamitani C, Niida S, Mizutani J, Kozawa O, Otsuka T 2010 Rho-kinase limits FGF-2-stimulated VEGF release in osteoblasts. Bone46:1068-1074
42. Watanabe A, Maruo S, Ito T, Ito M, Katsumura KR, Takada K 2010 Epstein-Barr virus-encoded Bcl-2 homologue functions as a survival factor in Wp-restricted Burkitt lymphoma cell line P3HR-1. J Virol 84:2893-2901
43. 4. Nature 227:680-685
44. Kato K, Ito H, Hasegawa K, Inaguma Y, Kozawa O, Asano T 1996 Modulation of the stress-induced synthesis of hsp27 and αB-crys-tallin by cyclic AMP in C6 rat glioma cells. J Neurochem 66:946-950 (Pubitemid 26065890)
45. Suzuki A, Kozawa O, Oiso Y, Kato K 1996 Protein kinase C activation inhibits stress-induced synthesis of heat shock protein 27 in osteoblast-like cells: function of arachidonic acid. J Cell Biochem 62:69-75 (Pubitemid 26286283)
46. Miwa M, Kozawa O, Tokuda H, Uematsu T 2000 Involvement of arachidonic acid in chemical stress-induced interleukin-6 synthesis in osteoblast-like cells: comparison with heat shock protein 27 induction. Prostaglandins Leukot Essent Fatty Acids 62:189-193 (Pubitemid 30333208)
47. Kozawa O, Niwa M, Matsuno H, Ishisaki A, Kato K, Uematsu T 2001 Stimulatory effect of basic fibroblast growth factor on induction of heat shock protein 27 in osteoblasts: role of protein kinase C. Arch Biochem Biophys 388:237-242 (Pubitemid 32911615)
48. Hazzalin CA, Le Panse R, Cano E, Mahadevan LC 1998 Anisomycin selectively desensitizes signalling components involved in stress kinase activation and fos and jun induction. Mol Cell Biol 18:1844-1854 (Pubitemid 28152633)
49. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC 1995 SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and in-terleukin-1. FEBS Lett 364:229-233
50. Seamon K, Daly JW 1981 Activation of adenylate cyclase by the diterpene forskolin does not require the guanine nucleotide regulatory protein. J Biol Chem 256:9799-9801 (Pubitemid 12176176)
51. Nishizuka y 1992 Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258:607-614
52. Michalak M, Milner RE, Burns K, Opas M 1992 Calreticulin. Biochem J 285 (Pt 3):681-692
53. Trott D, McManus CA, Martin JL, Brennan B, Dunn MJ, Rose ML 2009 Effect of phosphorylated hsp27 on proliferation of human endothelial and smooth muscle cells. Proteomics 9:3383-3394
54. Chaudhuri S, Smith PG 2008 Cyclic strain-induced HSP27 phosphorylation modulates actin filaments in airway smooth muscle cells. Am J Respir Cell Mol Biol 39:270-278
55. Kubisch C, Dimagno MJ, Tietz AB, Welsh MJ, Ernst SA, Brandt-Nedelev B, Diebold J, Wagner AC, Goke B, Williams JA, Schafer C 2004 Overexpression of heat shock protein Hsp27 protects against cerulein-induced pancreatitis. Gastroenterology 127:275-286 (Pubitemid 38962294)
56. Corsi AK, Schekman R 1996 Mechanism of polypeptide translocation into the endoplasmic reticulum. J Biol Chem 271:30299-30302 (Pubitemid 26404024)
57. Kappe G, Franck E, Verschuure P, Boelens WC, Leunissen JA, de Jong WW 2003 The human genome encodes 10 α-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones 8:53-61 (Pubitemid 36444090)
58. Lambert H, Charette SJ, Bernier AF, Guimond A, Landry J 1999 HSP27 multimerization mediated by phosphorylation-sensitive in-termolecular interactions at the amino terminus. J Biol Chem 274:9378-9385
59. Sun X, Welsh MJ, Benndorf R 2006 Conformational changes resulting from pseudophosphorylation of mammalian small heat shock proteins - a two-hybrid study. Cell Stress Chaperones 11:61-70 (Pubitemid 43363826)
60. Lian JB, Stein GS 1995 Development of the osteoblast phenotype: molecular mechanisms mediating osteoblast growth and differentiation. Iowa Orthop J 15:118-140
61. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, Smith E, Bonadio J, Goldstein S, Gundberg C, Bradley A, Karsenty G 1996 Increased bone formation in osteocalcin-deficient mice. Nature 382:448-452 (Pubitemid 26264860)
62. Kavukcuoglu NB, Patterson-Buckendahl P, Mann AB 2009 Effect of osteocalcin deficiency on the nanomechanics and chemistry of mouse bones. J Mech Behav Biomed Mater 2:348-354
63. Fukumoto S, Martin TJ 2009 Bone as an endocrine organ. Trends Endocrinol Metab 20:230-236
64. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G 2007 Endocrine regulation of energy metabolism by the skeleton. Cell 130:456-469 (Pubitemid 47208519)
65. Ferron M, Hinoi E, Karsenty G, Ducy P 2008 Osteocalcin differentially regulates β cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA 105:5266-5270 (Pubitemid 351738545)
66. Kindblom JM, Ohlsson C, Ljunggren O, Karlsson MK, Tivesten A, Smith U, Mellstrom D 2009 Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 24:785-791
67. Brussee V, Guo G, Dong Y, Cheng C, Martinez JA, Smith D, Glazner GW, Fernyhough P, Zochodne DW 2008 Distal degenerative sensory neuropathy in a long-term type 2 diabetes rat model. Diabetes 57:1664-1673