Loss of Protein Kinase C-δ Protects against LPS-Induced Osteolysis Owing to an Intrinsic Defect in Osteoclastic Bone Resorption

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Khor, Ee Cheng ^a   Abel, Tamara ^a   Tickner, Jennifer ^a   Chim, Shek Man ^a   Wang, Cathy ^a   Cheng, Taksum ^a   Ng, Benjamin ^a   Ng, Pei Ying ^a   Teguh, Dian Astari ^a   Kenny, Jacob ^a   Yang, Xiaohong ^b   Chen, Honghui ^b   Nakayama, Keiichi I ^c   Nakayama, Keiko ^c   Pavlos, Nathan ^a   Zheng, Ming H ^a   Xu, Jiake ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b JINAN UNIVERSITY   (China)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN K; LIPOPOLYSACCHARIDE; MARCKS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C ETA; PROTEIN KINASE C GAMMA; PROTEIN KINASE C LAMBDA; PROTEIN KINASE C THETA; PROTEIN KINASE C ZETA;

ALBERS SCHOENBERG DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DISEASE; BONE MASS; CARTILAGE MATRIX; CATHEPSIN K GENE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EX VIVO STUDY; FEMALE; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOSS; HUMAN; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOLYSIS OWING; PHENOTYPE; PROTEIN KINASE C ALPHA GENE; PROTEIN KINASE C BETA GENE; PROTEIN KINASE C DELTA GENE; PROTEIN KINASE C EPSILON GENE; PROTEIN KINASE C ETA GENE; PROTEIN KINASE C GAMMA GENE; PROTEIN KINASE C LAMBDA GENE; PROTEIN KINASE C THETA GENE; PROTEIN KINASE C ZETA GENE; PROTEIN PHOSPHORYLATION; REGULATOR GENE; SIGNAL TRANSDUCTION; SURFACE PROPERTY; TRABECULAR BONE; UPREGULATION;

ACETOPHENONES; ANIMALS; BENZOPYRANS; BONE RESORPTION; CATHEPSIN K; CELLS, CULTURED; ENZYME INHIBITORS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOCLASTS; OSTEOLYSIS; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; SIGNAL TRANSDUCTION;

EID: 84881321177     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070815     Document Type: Article

References (68)

1. Kular J, Tickner J, Chim SM, Xu J, (2012) An overview of the regulation of bone remodelling at the cellular level. Clinical Biochemistry 45: 863-873.
2. Rodan GA, Martin TJ, (2000) Therapeutic Approaches to Bone Diseases. Science 289: 1508-1514.
3. Teitelbaum SL, (2000) Bone resorption by osteoclasts. Science 289: 1504-1508.
4. Arai F, Miyamoto T, Ohneda O, Inada T, Sudo T, et al. (1999) Commitment and Differentiation of Osteoclast Precursor Cells by the Sequential Expression of c-Fms and Receptor Activator of Nuclear Factor {kappa}B (RANK) Receptors. J Exp Med 190: 1741-1754.
5. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, et al. (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. PNAS 95: 3597-3602.
6. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, et al. (1998) Osteoprotegerin Ligand Is a Cytokine that Regulates Osteoclast Differentiation and Activation. Cell 93: 165-176.
7. Burgess TL, Qian Y, Kaufman S, Ring BD, Van G, et al. (1999) The ligand for osteoprotegerin (OPGL) directly activates mature osteoclasts. J Cell Biol 145: 527-538.
8. Soriano P, Montgomery C, Geske R, Bradley A, (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64: 693-702.
9. Lee SW, Kwak HB, Chung WJ, Cheong H, Kim HH, et al. (2003) Participation of protein kinase C beta in osteoclast differentiation and function. Bone 32: 217-227.
10. Rahman A, Anwar KN, Uddin S, Xu N, Ye RD, et al. (2001) Protein Kinase C-{delta} Regulates Thrombin-Induced ICAM-1 Gene Expression in Endothelial Cells via Activation of p38 Mitogen-Activated Protein Kinase. Mol Cell Biol 21: 5554-5565.
11. Nishizuka Y, (1992) Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science. 258: 607-614.
12. Gutcher I, Webb PR, Anderson NG, (2003) The isoform-specific regulation of apoptosis by protein kinase C. Cell Mol Life Sci. 60: 1061-1070.
13. Wang C, Steer JH, Joyce DA, Yip KH, Zheng MH, et al. (2003) 12-O-tetradecanoylphorbol-13-acetate (TPA) inhibits osteoclastogenesis by suppressing RANKL-induced NF-kappaB activation. J Bone Miner Res 18: 2159-2168.
14. Su Y, Chakraborty M, Nathanson MH, Baron R, (1992) Differential effects of the 3′,5′-cyclic adenosine monophosphate and protein kinase C pathways on the response of isolated rat osteoclasts to calcitonin. Endocrinology 131: 1497-1502.
15. Moonga BS, Stein LS, Kilb JM, Dempster DW, (1996) Effect of diacylglycerols on osteoclastic bone resorption. Calcif Tissue Int 59: 105-108.
16. Moonga BS, Dempster DW, (1998) Effects of peptide fragments of protein kinase C on isolated rat osteoclasts. Exp Physiol 83: 717-725.
17. Liu J, Yang D, Minemoto Y, Leitges M, Rosner MR, et al. (2006) NF-κB Is Required for UV-Induced JNK Activation via Induction of PKĆ. Molecular Cell 21: 467-480.
18. Tracy S, van der Geer P, Hunter T, (1995) The receptor-like protein-tyrosine phosphatase, RPTP alpha, is phosphorylated by protein kinase C on two serines close to the inner face of the plasma membrane. J Biol Chem 270: 10587-10594.
19. Yoshida K, Miki Y, Kufe D, (2002) Activation of SAPK/JNK signaling by protein kinase Cdelta in response to DNA damage. J Biol Chem 277: 48372-48378.
20. Zheng X-M, Resnick RJ, Shalloway D, (2002) Mitotic Activation of Protein-tyrosine Phosphatase α and Regulation of Its Src-mediated Transforming Activity by Its Sites of Protein Kinase C Phosphorylation. J Biol Chem 277: 21922-21929.
21. Tu X, Joeng KS, Nakayama KI, Nakayama K, Rajagopal J, et al. (2007) Noncanonical Wnt Signaling through G Protein-Linked PKC [delta] Activation Promotes Bone Formation. Dev Cell 12: 113-127.
22. Miyamoto A, Nakayama K, Imaki H, Hirose S, Jiang Y, et al. (2002) Increased proliferation of B cells and auto-immunity in mice lacking protein kinase Cdelta. Nature 416: 865-869.
23. Takeshita S, Kaji K, Kudo A, (2000) Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J Bone Miner Res 15: 1477-1488.
24. Xu J, Tan JW, Huang L, Gao X-H, Laird R, et al. (2000) Cloning, Sequencing, and Functional Characterization of the Rat Homologue of Receptor Activator of NF-κB Ligand. J Bone Miner Res 15: 2178-2186.
25. Huang L, Xu J, Wood DJ, Zheng MH, (2000) Gene expression of osteoprotegerin ligand, osteoprotegerin, and receptor activator of NF-kappaB in giant cell tumor of bone: possible involvement in tumor cell-induced osteoclast-like cell formation. Am J Pathol 156: 761-767.
26. Bakker A, Klein-Nulend J, (2003) Osteoblast isolation from murine calvariae and long bones. Methods Mol Med 80: 19-28.
27. Pavlos NJ, Cheng TS, Qin A, Ng PY, Feng H-T, et al. (2011) Tctex-1, a Novel Interaction Partner of Rab3D, Is Required for Osteoclastic Bone Resorption. Mol Cell Biol 31: 1551-1564.
28. Qin A, Cheng TS, Lin Z, Cao L, Chim SM, et al. (2012) Prevention of Wear Particle-Induced Osteolysis by a Novel V-ATPase Inhibitor Saliphenylhalamide through Inhibition of Osteoclast Bone Resorption. PLoS ONE 7: e34132.
29. Helfrich MH, Aronson DC, Everts V, Mieremet RHP, Gerritsen EJA, et al. (1991) Morphologic features of bone in human osteopetrosis. Bone 12: 411-419.
30. Walker DG, (1973) Osteopetrosis cured by temporary parabiosis. Science 180: 875.
31. Wang ZZ-Q, Ovitt CC, (1992) Bone and haematopoietic defects in mice lacking c-fos. Nature 360: 741.
32. Leitges M, Mayr M, Braun U, Mayr U, Li C, et al. (2001) Exacerbated vein graft arteriosclerosis in protein kinase Cdelta-null mice. J Clin Invest 108: 1505-1512.
33. Jacquin C, Gran DE, Lee SK, Lorenzo JA, Aguila HL, (2006) Identification of Multiple Osteoclast Precursor Populations in Murine Bone Marrow. J Bone Miner Res 21: 67-77.
34. Tanaka S, Takahashi N, Udagawa N, Tamura T, Akatsu T, et al. (1993) Macrophage colony-stimulating factor is indispensable for both proliferation and differentiation of osteoclast progenitors. J Clin Invest 91: 257-263.
35. Yasuda H, Shima N, Nakagawa N, Mochizuki S-I, Yano K, et al. (1998) Identity of Osteoclastogenesis Inhibitory Factor (OCIF) and Osteoprotegerin (OPG): A Mechanism by which OPG/OCIF Inhibits Osteoclastogenesis in Vitro. Endocrinology 139: 1329-1337.
36. Sorensen M, Karsdal M, Dziegiel M, Boutin J, Nosjean O, et al. (2010) Screening of protein kinase inhibitors identifies PKC inhibitors as inhibitors of osteoclastic acid secretion and bone resorption. BMC Musculoskeletal Disorders 11: 250.
37. Cremasco V, Decker CE, Stumpo D, Blackshear PJ, Nakayama KI, et al. (2012) Protein kinase C-delta deficiency perturbs bone homeostasis by selective uncoupling of cathepsin K secretion and ruffled border formation in osteoclasts. J Bone Miner Res 27: 2452-2463.
38. Rucci N, DiGiacinto C, Orru L, Millimaggi D, Baron R, et al. (2005) A novel protein kinase C {alpha}-dependent signal to ERK1/2 activated by {alpha}V{beta}3 integrin in osteoclasts and in Chinese hamster ovary (CHO) cells. J Cell Sci 118: 3263-3275.
39. Lampasso JD, Marzec N, Margarone J, Dziak R, (2002) Role of Protein Kinase C α in Primary Human Osteoblast Proliferation. J Bone Miner Res 17: 1968-1976.
40. Lima F, Niger C, Hebert C, Stains JP, (2009) Connexin43 Potentiates Osteoblast Responsiveness to Fibroblast Growth Factor 2 via a Protein Kinase C-Delta/Runx2-dependent Mechanism. Mol Biol Cell 20: 2697-2708.
41. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, et al. (2007) Defective Microtubule-Dependent Podosome Organization in Osteoclasts Leads to Increased Bone Density in Pyk2-/- mice. J Cell Biol 178: 1053-1064.
42. Margolis D, Szivek J, Lai L-W, Lien Y-H, (2008) Phenotypic Characteristics of Bone in Carbonic Anhydrase II-Deficient Mice. Calcif Tissue Int 82: 66-76.
43. Gowen M, Lazner F, Dodds R, Kapadia R, Feild J, et al. (1999) Cathepsin K Knockout Mice Develop Osteopetrosis Due to a Deficit in Matrix Degradation but Not Demineralization. J Bone Miner Res 14: 1654-1663.
44. Humphries MJ, Limesand KH, Schneider JC, Nakayama KI, Anderson SM, et al. (2006) Suppression of Apoptosis in the Protein Kinase Cδ Null Mouse in Vivo. J Biol Chem 281: 9728-9737.
45. Miyazaki T, Katagiri H, Kanegae Y, Takayanagi H, Sawada Y, et al. (2000) Reciprocal Role of ERK and Nf-κb Pathways in Survival and Activation of Osteoclasts. J Cell Biol 148: 333-342.
46. Li Y, Toraldo G, Li A, Yang X, Zhang H, et al. (2007) B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood 109: 3839-3848.
47. Schwartzberg PL, Xing L, Hoffmann O, Lowell CA, Garrett L, et al. (1997) Rescue of osteoclast function by transgenic expression of kinase-deficient Src insrc-/- mutant mice. Genes Dev 11: 2835-2844.
48. Miyazaki T, Sanjay A, Neff L, Tanaka S, Horne WC, et al. (2004) Src Kinase Activity Is Essential for Osteoclast Function. J Biol Chem 279: 17660-17666.
49. Sanjay A, Houghton A, Neff L, DiDomenico E, Bardelay C, et al. (2001) Cbl Associates with Pyk2 and Src to Regulate Src Kinase Activity, αvβ3 Integrin-Mediated Signaling, Cell Adhesion, and Osteoclast Motility. J Cell Biol 152: 181-196.
50. Horne WC, Sanjay A, Bruzzaniti A, Baron R, (2005) The role(s) of Src kinase and Cbl proteins in the regulation of osteoclast differentiation and function. Immunol Rev 208: 106-125.
51. Brandt DT, Goerke A, Heuer M, Gimona M, Leitges M, et al. (2003) Protein kinase C delta induces Src kinase activity via activation of the protein tyrosine phosphatase PTP alpha. J Biol Chem 278: 34073-34078.
52. Buitrago C, Costabel M, Boland R, (2011) PKC and PTP [alpha] participate in Src activation by 1 [alpha],25(OH)2 vitamin D3 in C2C12 skeletal muscle cells. Mol Cell Endocrinol 339: 9.
53. Ponniah S, Wang DZ, Lim KL, Pallen CJ, (1999) Targeted disruption of the tyrosine phosphatase PTPalpha leads to constitutive downregulation of the kinases Src and Fyn. Curr Biol 9: 535-538.
54. Adapala NS, Barbe MF, Langdon WY, Nakamura MC, Tsygankov AY, et al. (2010) The loss of Cbl-phosphatidylinositol 3-kinase interaction perturbs RANKL-mediated signaling, inhibiting bone resorption and promoting osteoclast survival. J Biol Chem 285: 36745-36758.
55. Shinohara M, Nakamura M, Masuda H, Hirose J, Kadono Y, et al. (2012) Class IA phosphatidylinositol 3-kinase regulates osteoclastic bone resorption through Akt-mediated vesicle transport. J Bone Miner Res 27: 2464-2475.
56. Kikuchi T, Matsuguchi T, Tsuboi N, Mitani A, Tanaka S, et al. (2001) Gene Expression of Osteoclast Differentiation Factor Is Induced by Lipopolysaccharide in Mouse Osteoblasts Via Toll-Like Receptors. J Immunol 166: 3574-3579.
57. Zhuang L, Jung JY, Wang EW, Houlihan P, Ramos L, et al. (2007) Pseudomonas aeruginosa Lipopolysaccharide Induces Osteoclastogenesis Through a Toll-Like Receptor 4 Mediated Pathway in Vitro and in Vivo. The Laryngoscope 117: 841-847.
58. Sismey-Durrant HJ, Hopps RM, (1991) Effect of lipopolysaccharide from Porphyromonas gingivalis on prostaglandin E2 and interleukin-1-beta release from rat periosteal and human gingival fibroblasts in vitro. Oral Microbiol Immunol 6: 378-380.
59. Chiang CY, Kyritsis G, Graves DT, Amar S, (1999) Interleukin-1 and tumor necrosis factor activities partially account for calvarial bone resorption induced by local injection of lipopolysaccharide. Infect Immun 67: 4231-4236.
60. Kozuka Y, Ozaki Y, Ukai T, Kaneko T, Hara Y, (2006) B Cells Play an Important Role in Lipopolysaccharide-Induced Bone Resorption. Calcified Tissue International 78: 125-132.
61. Ozaki Y, Ukai T, Yamaguchi M, Yokoyama M, Ayón Haro ER, et al. (2009) Locally administered T cells from mice immunized with lipopolysaccharide (LPS) accelerate LPS-induced bone resorption. Bone 44: 1169-1176.
62. Ha J, Lee Y, Kim H-H, (2011) CXCL2 mediates lipopolysaccharide-induced osteoclastogenesis in RANKL-primed precursors. Cytokine 55: 48-55.
63. Zou W, Bar-Shavit Z, (2002) Dual Modulation of Osteoclast Differentiation by Lipopolysaccharide. J Bone Miner Res 17: 1211-1218.
64. Boyce BF, Yoneda T, Lowe C, Soriano P, Mundy GR, (1992) Requirement of pp60c-src expression for osteoclasts to form ruffled borders and resorb bone in mice. J Clin Invest 90: 1622-1627.
65. Weinstein RS, Roberson PK, Manolagas SC, (2009) Giant Osteoclast Formation and Long-Term Oral Bisphosphonate Therapy. NEJ Med 360: 53-62.
66. Gschwendt M, Muller HJ, Kielbassa K, Zang R, Kittstein W, et al. (1994) Rottlerin, a novel protein kinase inhibitor. Biochem Biophys Res Commun 199: 93-98.
67. Davies SP, Reddy H, Caivano M, Cohen P, (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105.
68. Soltoff SP, (2007) Rottlerin: an inappropriate and ineffective inhibitor of PKCdelta. Trends Pharmacol Sci 28: 453-458.