Diacylglycerol kinase ζ (DGKζ) is a critical regulator of bone homeostasis via modulation of c-fos levels in osteoclasts

Journal of Bone and Mineral Research

Volumn 30, Issue 10, 2015, Pages 1852-1863

  Zamani, Ali ^a   Decker, Corinne ^a   Cremasco, Viviana ^a   Hughes, Lindsey ^a   Novack, Deborah V ^a   Faccio, Roberta ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

C FOS; DAG; DGK ; M CSF; osteoclasts

Indexed keywords

COLONY STIMULATING FACTOR 1; DIACYLGLYCEROL; DIACYLGLYCEROL KINASE; DIACYLGLYCEROL KINASE ZETA; NFATC1 PROTEIN; OSTEOCLAST DIFFERENTIATION FACTOR; PHOSPHOLIPASE C GAMMA2; PROTEIN C FOS; REGULATOR PROTEIN; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; DIACYLGLYCEROL KINASE ZETA, MOUSE; NFATC1 PROTEIN, MOUSE; PHOSPHOLIPASE C GAMMA; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TNFRSF11A PROTEIN, MOUSE; TNFSF11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE; BONE MARROW DERIVED MACROPHAGE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE SILENCING; HOMEOSTASIS; LUCIFERASE ASSAY; MALE; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; SECOND MESSENGER; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; CYTOLOGY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; DIACYLGLYCEROL KINASE; GENE EXPRESSION REGULATION; MACROPHAGE COLONY-STIMULATING FACTOR; MICE; MICE, KNOCKOUT; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; PHOSPHOLIPASE C GAMMA; PROTO-ONCOGENE PROTEINS C-FOS; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RESPONSE ELEMENTS;

EID: 84942199541     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2533     Document Type: Article

References (46)

1. Carrasco S, Merida I,. Diacylglycerol, when simplicity becomes complex. Trends Biochem Sci. 2007; 32 (1): 27-36.
2. Coleman RA, Lee DP., Enzymes of triacylglycerol synthesis and their regulation. Prog Lipid Res. 2004; 43 (2): 134-76.
3. Baldanzi G., Inhibition of diacylglycerol kinases as a physiological way to promote diacylglycerol signaling. Adv Biol Regul. 2014; 55: 39-49.
4. Wakelam MJ., Diacylglycerol-when is it an intracellular messenger? Biochim Biophys Acta. 1998; 1436 (1-2): 117-26.
5. Teitelbaum SL., Bone resorption by osteoclasts. Science. 2000; 289 (5484): 1504-8.
6. Mao D, Epple H, Uthgenannt B, Novack DV, Faccio R., PLCgamma2 regulates osteoclastogenesis via its interaction with ITAM proteins and G AB2. J Clin Invest. 2006; 116 (11): 2869-79.
7. Epple H, Cremasco V, Zhang K, Mao D, Longmore GD, Faccio R., Phospholipase Cgamma2 modulates integrin signaling in the osteoclast by affecting the localization and activation of Src kinase. Mol Cell Biol. 2008; 28 (11): 3610-22.
8. Cremasco V, Decker CE, Stumpo D, et al., 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. 2012; 27 (12): 2452-63.
9. Lee SW, Kwak HB, Chung WJ, Cheong H, Kim HH, Lee ZH., Participation of protein kinase C beta in osteoclast differentiation and function. Bone. 2003; 32 (3): 217-27.
10. Sorensen MG, Karsdal MA, Dziegiel MH, Boutin JA, Nosjean O, Henriksen K., Screening of protein kinase inhibitors identifies PKC inhibitors as inhibitors of osteoclastic acid secretion and bone resorption. BMC Musculoskelet Disord. 2010; 11: 250.
11. Drosatos-Tampakaki Z, Drosatos K, Siegelin Y, et al., Palmitic acid and DGAT1 deficiency enhance osteoclastogenesis, while oleic acid-induced triglyceride formation prevents it. J Bone Miner Res. 2014; 29 (5): 1183-95.
12. Murrills RJ, Stein LS, Horbert WR, Dempster DW., Effects of phorbol myristate acetate on rat and chick osteoclasts. J Bone Miner Res. 1992; 7 (4): 415-23.
13. Moonga BS, Stein LS, Kilb JM, Dempster DW., Effect of diacylglycerols on osteoclastic bone resorption. Calcif Tissue Int. 1996; 59 (2): 105-8.
14. Abraham DC, Wadkins CL, Conaway HH., Enhancement of fetal rat limb bone resorption by phorbol ester (PMA) and ionophore A-23187. Calcif Tissue Int. 1988; 42 (3): 191-5.
15. Shulga YV, Topham MK, Epand RM., Regulation and functions of diacylglycerol kinases. Chem Rev. 2011; 111 (10): 6186-208.
16. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R., Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010; 25 (7): 1468-86.
17. Takeshita S, Kaji K, Kudo A., Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J Bone Miner Res. 2000; 15 (8): 1477-88.
18. Bligh EG, Dyer WJ., A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959; 37 (8): 911-7.
19. Topham MK, Prescott SM., Mammalian diacylglycerol kinases, a family of lipid kinases with signaling functions. J Biol Chem. 1999; 274 (17): 11447-50.
20. Grigoriadis AE, Wang ZQ, Cecchini MG, et al., c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science. 1994; 266 (5184): 443-8.
21. Matsuo K, Owens JM, Tonko M, Elliott C, Chambers TJ, Wagner EF., Fosl1 is a transcriptional target of c-Fos during osteoclast differentiation. Nat Genet. 2000; 24 (2): 184-7.
22. Takayanagi H, Kim S, Matsuo K, et al., RANKL maintains bone homeostasis through c-Fos-dependent induction of interferon-beta. Nature. 2002; 416 (6882): 744-9.
23. Schutze S, Machleidt T, Kronke M., The role of diacylglycerol and ceramide in tumor necrosis factor and interleukin-1 signal transduction. J Leukoc Biol. 1994; 56 (5): 533-41.
24. Wagner EF, Matsuo K., Signalling in osteoclasts and the role of Fos/AP1 proteins. Ann Rheum Dis. 2003; 62Suppl 2: ii83-5.
25. Robertson LM, Kerppola TK, Vendrell M, et al., Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron. 1995; 14 (2): 241-52.
26. Wang Y, Prywes R., Activation of the c-fos enhancer by the erk MAP kinase pathway through two sequence elements: the c-fos AP-1 and p62TCF sites. Oncogene. 2000; 19 (11): 1379-85.
27. Cremasco V, Benasciutti E, Cella M, Kisseleva M, Croke M, Faccio R., Phospholipase C gamma 2 is critical for development of a murine model of inflammatory arthritis by affecting actin dynamics in dendritic cells. PloS One. 2010; 5 (1): e8909.
28. Veis N, Hamilton JA., Colony stimulating factor-1 stimulates diacylglycerol generation in murine bone marrow-derived macrophages, but not in resident peritoneal macrophages. J Cell Physiol. 1991; 147 (2): 298-305.
29. Song JG, Pfeffer LM, Foster DA., v-Src increases diacylglycerol levels via a type D phospholipase-mediated hydrolysis of phosphatidylcholine. Mol Cell Biol. 1991; 11 (10): 4903-8.
30. Oancea E, Teruel MN, Quest AF, Meyer T., Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. J Cell Biol. 1998; 140 (3): 485-98.
31. Violin JD, Zhang J, Tsien RY, Newton AC., A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. J Cell Biol. 2003; 161 (5): 899-909.
32. Fuller K, Owens JM, Jagger CJ, Wilson A, Moss R, Chambers TJ., Macrophage colony-stimulating factor stimulates survival and chemotactic behavior in isolated osteoclasts. J Exp Med. 1993; 178 (5): 1733-44.
33. Arai F, Miyamoto T, Ohneda O, et al., Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J Exp Med. 1999; 190 (12): 1741-54.
34. Simonet WS, Lacey DL, Dunstan CR, et al., Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997; 89 (2): 309-19.
35. Nakamura I, Lipfert L, Rodan GA, Le TD,. Convergence of alpha(v) beta(3) integrin- and macrophage colony stimulating factor-mediated signals on phospholipase Cgamma in prefusion osteoclasts. J Cell Biol. 2001; 152 (2): 361-73.
36. Zhong XP, Hainey EA, Olenchock BA, et al., Enhanced T cell responses due to diacylglycerol kinase zeta deficiency. Nat Immunol. 2003; 4 (9): 882-90.
37. Huang Y, Zhang H, Shao Z, et al., Suppression of endothelin-1-induced cardiac myocyte hypertrophy by PPAR agonists: role of diacylglycerol kinase zeta. Cardiovasc Res. 2011; 90 (2): 267-75.
38. Stensman H, Raghunath A, Larsson C., Autophosphorylation suppresses whereas kinase inhibition augments the translocation of protein kinase Calpha in response to diacylglycerol. J Biol Chem. 2004; 279 (39): 40576-83.
39. Madani S, Hichami A, Legrand A, Belleville J, Khan NA,. Implication of acyl chain of diacylglycerols in activation of different isoforms of protein kinase C. FASEB. J. 2001; 15 (14): 2595-601.
40. Faccio R, Takeshita S, Zallone A, Ross FP, Teitelbaum SL., c-Fms and the alphavbeta3 integrin collaborate during osteoclast differentiation. J Clin Invest. 2003; 111 (5): 749-58.
41. Faccio R, Teitelbaum SL, Fujikawa K, et al., Vav3 regulates osteoclast function and bone mass. Nat Med. 2005; 11 (3): 284-90.
42. Faccio R, Zou W, Colaianni G, Teitelbaum SL, Ross FP., High dose M-CSF partially rescues the Dap12-/- osteoclast phenotype. J Cell Biochem. 2003; 90 (5): 871-83.
43. Kitaura H, Zhou P, Kim HJ, Novack DV, Ross FP, Teitelbaum SL., M-CSF mediates TNF-induced inflammatory osteolysis. J Clin Invest. 2005; 115 (12): 3418-27.
44. Yang PT, Kasai H, Xiao WG, et al., Increased expression of macrophage colony-stimulating factor in ankylosing spondylitis and rheumatoid arthritis. Ann Rheum Dis. 2006; 65 (12): 1671-2.
45. Korkosz M, Bukowska-Strakova K, Sadis S, Grodzicki T, Siedlar M., Monoclonal antibodies against macrophage colony-stimulating factor diminish the number of circulating intermediate and nonclassical (CD14(++)CD16(+)/CD14(+)CD16(++)) monocytes in rheumatoid arthritis patient. Blood. 2012; 119 (22): 5329-30.
46. Paniagua RT, Chang A, Mariano MM, et al., c-Fms-mediated differentiation and priming of monocyte lineage cells play a central role in autoimmune arthritis. Arthritis Res Ther. 2010; 12 (1): R32.