Serum calcium-decreasing factor, caldecrin, inhibits receptor activator of NF-κB ligand (RANKL)-mediated Ca2+signaling and actin ring formation in mature osteoclasts via suppression of Src signaling pathway

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 17963-17974

  Tomomura, Mineko ^a   Hasegawa, Hiroya ^a   Suda, Naoto ^a   Sakagami, Hiroshi ^a   Tomomura, Akito ^a  

^a MEIKAI UNIVERSITY SCHOOL OF DENTISTRY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RING FORMATION; BONE RESORPTION; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CYTOSKELETAL ORGANIZATION; KINASE ACTIVITY; NEGATIVE REGULATORS; OSTEOCLAST DIFFERENTIATION; OSTEOCLASTOGENESIS; PHOSPHOLIPASE C; PROTEASE ACTIVITIES; RECEPTOR ACTIVATOR; SERINE PROTEASE; SIGNALING PATHWAYS; TRANSIENT RECEPTOR POTENTIAL VANILLOID;

AMINO ACIDS; BODY FLUIDS; BONE; CHEMICAL ACTIVATION; LIGANDS; PHOSPHORYLATION; PROTEINS; SIGNAL TRANSDUCTION;

CALCIUM;

ACTIN; CALCIUM ION; CALDECRIN; CELL PROTEIN; FOCAL ADHESION KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCLAST DIFFERENTIATION FACTOR; PHOSPHOLIPASE C GAMMA1; PHOSPHOLIPASE C GAMMA2; PROTEIN KINASE B; PROTEIN KINASE SYK; PROTEIN SLP 76; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 4;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL FUNCTION; CELL MATURATION; CELL STIMULATION; CYTOSKELETON; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; INHIBITION KINETICS; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; BONE RESORPTION; CALCIUM SIGNALING; CELL LINE; HUMANS; MICE; OSTEOCLASTS; RANK LIGAND; SERINE ENDOPEPTIDASES; SRC-FAMILY KINASES;

EID: 84861562947     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.358796     Document Type: Article

References (49)

1. Suda, T., Takahashi, N., Udagawa, N., Jimi, E., Gillespie, M. T., and Martin, T. J. (1999) Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr. Rev. 20, 345-357 (Pubitemid 30649812)
2. Teitelbaum, S. L. (2000) Bone resorption by osteoclasts. Science 289, 1504-1508
3. Boyle, W. J., Simonet, W. S., and Lacey, D. L. (2003) Osteoclast differentiation and activation. Nature 423, 337-342 (Pubitemid 40852708)
4. Asagiri, M., and Takayanagi, H. (2007) The molecular understanding of osteoclast differentiation. Bone 40, 251-264 (Pubitemid 46054562)
5. Takayanagi, H., Kim, S., Koga, T., Nishina, H., Isshiki, M., Yoshida, H., Saiura, A., Isobe, M., Yokochi, T., Inoue, J., Wagner, E. F., Mak, T. W., Kodama, T., and Taniguchi, T. (2002) Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 3, 889-901 (Pubitemid 35460788)
6. Koga, T., Inui, M., Inoue, K., Kim, S., Suematsu, A., Kobayashi, E., Iwata, T., Ohnishi, H., Matozaki, T., Kodama, T., Taniguchi, T., Takayanagi, H., and Takai, T. (2004) Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428, 758-763 (Pubitemid 38508286)
7. Mócsai, A., Humphrey, M. B., Van Ziffle, J. A., Hu, Y., Burghardt, A., Spusta, S. C., Majumdar, S., Lanier, L. L., Lowell, C. A., and Nakamura, M. C. (2004) The immunomodulatory adapter proteins DAP12 and Fc receptor γ-chain (FcRγ) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc. Natl. Acad. Sci. U.S.A. 101, 6158-6163 (Pubitemid 38520544)
8. Jimi, E., Akiyama, S., Tsurukai, T., Okahashi, N., Kobayashi, K., Udagawa, N., Nishihara, T., Takahashi, N., and Suda, T. (1999) Osteoclast differentiation factor acts as a multifunctional regulator in murine osteoclast differentiation and function. J. Immunol. 163, 434-442 (Pubitemid 29295871)
9. Teti, A., Marchisio, P. C., and Zallone, A. Z. (1991) Clear zone in osteoclast function. Role of podosomes in regulation of bone-resorbing activity. Am. J. Physiol. 261, C1-C7
10. Zou, W., and Teitelbaum, S. L. (2010) Integrins, growth factors, and the osteoclast cytoskeleton. Ann. N.Y. Acad. Sci. 1192, 27-31
11. McHugh, K. P., Hodivala-Dilke, K., Zheng, M. H., Namba, N., Lam, J., Novack, D., Feng, X., Ross, F. P., Hynes, R. O., and Teitelbaum, S. L. (2000) Mice lacking β3 integrins are osteosclerotic because of dysfunctional osteoclasts. J. Clin. Invest. 105, 433-440 (Pubitemid 30127243)
12. Soriano, P., Montgomery, C., Geske, R., and Bradley, A. (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693-702 (Pubitemid 121001157)
13. Gil-Henn, H., Destaing, O., Sims, N. A., Aoki, K., Alles, N., Neff, L., Sanjay, A., Bruzzaniti, A., De Camilli, P., Baron, R., and Schlessinger, J. (2007) Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2-/- mice. J. Cell Biol. 178, 1053-1064 (Pubitemid 47443326)
14. 3 integrin, and phosphorylated by Src kinase. J. Clin. Invest. 102, 881-892
15. Zou, W., Kitaura, H., Reeve, J., Long, F., Tybulewicz, V. L., Shattil, S. J., Ginsberg, M. H., Ross, F. P., and Teitelbaum, S. L. (2007) Syk, c-Src, the αvβ3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J. Cell Biol. 176, 877-888 (Pubitemid 46425547)
16. Kajiya, H., Okamoto, F., Nemoto, T., Kimachi, K., Toh-Goto, K., Nakayana, S., and Okabe, K. (2010) RANKL-induced TRPV2 expression regulates osteoclastogenesis via calcium oscillations. Cell Calcium 48, 260-269
17. Masuyama, R., Vriens, J., Voets, T., Karashima, Y., Owsianik, G., Vennekens, R., Lieben, L., Torrekens, S., Moermans, K., Vanden Bosch A., Bouillon, R., Nilius, B., and Carmeliet, G. (2008) TRPV4-mediated calcium influx regulates terminal differentiation of osteoclasts. Cell Metab. 8, 257-265
18. 2+ in human osteoclasts and down-regulates bone resorption. J. Biol. Chem. 285, 25354-25362
19. Watanabe, H., Davis, J. B., Smart, D., Jerman, J. C., Smith, G. D., Hayes, P., Vriens, J., Cairns, W., Wissenbach, U., Prenen, J., Flockerzi, V., Droogmans, G., Benham, C. D., and Nilius, B. (2002) Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J. Biol. Chem. 277, 13569-13577 (Pubitemid 34967954)
20. Nilius, B., Vriens, J., Prenen, J., Droogmans, G., and Voets, T. (2004) TRPV4 calcium entry channel. A paradigm for gating diversity. Am. J. Physiol. Cell Physiol. 286, C195-C205 (Pubitemid 38146342)
21. Tomomura, A., Fukushige, T., Noda, T., Noikura, T., and Saheki, T. (1992) Serum calcium-decreasing factor (caldecrin) from porcine pancreas has proteolytic activity which has no clear connection with the calcium decrease. FEBS Lett. 301, 277-281
22. Tomomura, A., Fukushige, T., Tomomura, M., Noikura, T., Nishii, Y., and Saheki, T. (1993) Caldecrin proform requires trypsin activation for the acquisition of serum calcium-decreasing activity. FEBS Lett. 335, 213-216 (Pubitemid 23350409)
23. Tomomura, A., Tomomura, M., Fukushige, T., Akiyama, M., Kubota, N., Kumaki, K., Nishii, Y., Noikura, T., and Saheki, T. (1995) Molecular cloning and expression of serum calcium-decreasing factor (caldecrin). J. Biol. Chem. 270, 30315-30321 (Pubitemid 26006311)
24. Tomomura, A., Akiyama, M., Itoh, H., Yoshino, I., Tomomura, M., Nishii, Y., Noikura, T., and Saheki, T. (1996) Molecular cloning and expression of human caldecrin. FEBS Lett. 386, 26-28 (Pubitemid 26144946)
25. Hasegawa, H., Kido, S., Tomomura, M., Fujimoto, K., Ohi, M., Kiyomura, M., Kanegae, H., Inaba, A., Sakagami, H., and Tomomura, A. (2010) Serum calcium-decreasing factor, caldecrin, inhibits osteoclast differentiation by suppression of NFATc1 activity. J. Biol. Chem. 285, 25448-25457
26. Tomomura, A., Yamada, H., Fujimoto, K., Inaba, A., and Katoh, S. (2001) Determination of amino acid sequence responsible for suppression of bone resorption by serum calcium-decreasing factor (caldecrin). FEBS Lett. 508, 454-458 (Pubitemid 33135490)
27. Tomomura, M., Fujii, T., Sakagami, H., and Tomomura, A. (2011) Serum calcium- decreasing factor, caldecrin, ameliorates muscular dystrophy in dy/dy mice. In vivo 25, 157-163
28. Ishii, K. A., Fumoto, T., Iwai, K., Takeshita, S., Ito, M., Shimohata, N., Aburatani, H., Taketani, S., Lelliott, C. J., Vidal-Puig, A., and Ikeda, K. (2009) Coordination of PGC-1β and iron uptake in mitochondrial biogenesis and osteoclast activation. Nat. Med. 15, 259-266
29. Saltel, F., Destaing, O., Bard, F., Eichert, D., and Jurdic P. (2004) Apatite-mediated actin dynamics in resorbing osteoclasts. Mol. Biol. Cell 15, 5231-5241 (Pubitemid 39564720)
30. Boyce, B. F., Yoneda, T., Lowe, C., Soriano, P., and Mundy, G. R. (1992) Requirement of pp60c-src expression for osteoclasts to form ruffled borders and resorb bone in mice. J. Clin. Invest. 90, 1622-1627
31. Teitelbaum, S. L., and Ross, F. P. (2003) Genetic regulation of osteoclast development and function. Nat. Rev. Genet. 4, 638-649 (Pubitemid 36917505)
32. 2+-dependent potentiation of the nonselective cation channel TRPV4 is mediated by a C-terminal calmodulin binding site. J. Biol. Chem. 278, 26541-26549
33. Hunter, T. (1987) A tail of two src's. Mutatis mutandis. Cell 49, 1-4
34. Mao, D., Epple, H., Uthgenannt, B., Novack, D. V., and Faccio, R. (2006) PLCγ2 regulates osteoclastogenesis via its interaction with ITAM proteins and GAB2. J. Clin. Invest. 116, 2869-2879 (Pubitemid 44684472)
35. Wu, J. N., and Koretzky, G. A. (2004) The SLP-76 family of adapter proteins. Semin. Immunol. 16, 379-393 (Pubitemid 39488019)
36. Reeve, J. L., Zou, W., Liu, Y., Maltzman, J. S., Ross, F. P., and Teitelbaum, S. L. (2009) SLP-76 couples Syk to the osteoclast cytoskeleton. J. Immunol. 183, 1804-1812
37. 3 integrin-mediated signaling, cell adhesion, and osteoclast motility. J. Cell Biol. 152, 181-195
38. Epple, H., Cremasco, V., Zhang, K., Mao, D., Longmore, G. D., and Faccio, R. (2008) Phospholipase Cγ2 modulates integrin signaling in the osteoclast by affecting the localization and activation of Src kinase. Mol. Cell Biol. 28, 3610-3622 (Pubitemid 351732899)
39. Arias-Salgado, E. G., Lizano, S., Sarkar, S., Brugge, J. S., Ginsberg, M. H., and Shattil, S. J. (2003) Src kinase activation by direct interaction with the integrin β cytoplasmic domain. Proc. Natl. Acad. Sci. U.S.A. 100, 13298-13302 (Pubitemid 37444736)
40. Miyazaki, T., Sanjay, A., Neff, L., Tanaka, S., Horne, W. C., and Baron, R. (2004) Src kinase activity is essential for osteoclast function. J. Biol. Chem. 279, 17660-17666 (Pubitemid 38560531)
41. Faccio, R., Novack, D. V., Zallone, A., Ross, F. P., and Teitelbaum, S. L. (2003) Dynamic changes in the osteoclast cytoskeleton in response to growth factors and cell attachment are controlled by β3 integrin. J. Cell Biol. 162, 499-509 (Pubitemid 36988558)
42. Armstrong, A. P., Tometsko, M. E., Glaccum, M., Sutherland, C. L., Cosman, D., and Dougall, W. C. (2002) RANK/TRAF6-dependent signal transduction pathway is essential for osteoclast cytoskeletal organization and resorptive function. J. Biol. Chem. 277, 44347-44356 (Pubitemid 36157870)
43. Lomaga, M. A., Yeh, W. C., Sarosi, I., Duncan, G. S., Furlonger, C., Ho, A., Morony, S., Capparelli, C., Van, G., Kaufman, S., van der Heiden, A., Itie, A., Wakeham, A., Khoo, W., Sasaki, T., Cao, Z., Penninger, J. M., Paige, C. J., Lacey, D. L., Dunstan, C. R., Boyle, W. J., Goeddel, D. V., and Mak, T. W. (1999) TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13, 1015-1024 (Pubitemid 29200984)
44. Wang, K. Z., Wara-Aswapati, N., Boch, J. A., Yoshida, Y., Hu, C. D., Galson, D. L., and Auron, P. E. (2006) TRAF6 activation of PI 3-kinase-dependent cytoskeletal changes is cooperative with Ras and is mediated by an interaction with cytoplasmic Src. J. Cell Sci. 119, 1579-1591 (Pubitemid 43732984)
45. Matsubara, T., Ikeda, F., Hata, K., Nakanishi, M., Okada, M., Yasuda, H., Nishimura, R., and Yoneda, T. (2010) Cbp recruitment of Csk into lipid rafts is critical to c-Src kinase activity and bone resorption in osteoclasts. J. Bone Miner. Res. 25, 1068-1076
46. Ha, H., Kwak, H. B., Lee, S. K., Na, D. S., Rudd, C. E., Lee, Z. H., and Kim, H. H. (2003) Membrane rafts play a crucial role in receptor activator of nuclear factor κB signaling and osteoclast function. J. Biol. Chem. 278, 18573-18580 (Pubitemid 36799484)
47. Irby, R. B., and Yeatman, T. J. (2000) Role of Src expression and activation in human cancer. Oncogene 19, 5636-5642
48. Myoui, A., Nishimura, R., Williams, P. J., Hiraga, T., Tamura, D., Michigami, T., Mundy, G. R., and Yoneda, T. (2003) c-Src tyrosine kinase activity is associated with tumor colonization in bone and lung in an animal model of human breast cancer metastasis. Cancer Res. 63, 5028-5033 (Pubitemid 37022641)
49. Park, S. I., Zhang, J., Phillips, K. A., Araujo, J. C., Najjar, A. M., Volgin, A. Y., Gelovani, J. G., Kim, S. J., Wang, Z., and Gallick G. E. (2008) Targeting Src family kinases inhibits growth and lymph node metastases of prostate cancer in an orthotopic nude mouse model. Cancer Res. 68, 3323-3333