Dynamin reduces Pyk2 Y402 phosphorylation and Src binding in osteoclasts

Molecular and Cellular Biology

Volumn 29, Issue 13, 2009, Pages 3644-3656

  Bruzzaniti, Angela ^a,b   Neff, Lynn ^b,c   Sandoval, Amanda ^b   Du, Liping ^a   Horne, William C ^b,c   Baron, Roland ^b,c,d  

^a INDIANA UNIVERSITY SCHOOL OF DENTISTRY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CBL PROTEIN; COLONY STIMULATING FACTOR 1; DYNAMIN; FOCAL ADHESION KINASE 2; GROWTH FACTOR RECEPTOR; GUANOSINE TRIPHOSPHATASE; INTEGRIN; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL ORGANELLE; CONTROLLED STUDY; DENDRITIC CELL; DISSOCIATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PODOSOME; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; DYNAMINS; FOCAL ADHESION KINASE 2; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MICE; OSTEOCLASTS; PHOSPHORYLATION; PROTEIN BINDING; RATS; RECOMBINANT FUSION PROTEINS; SRC-FAMILY KINASES; TYROSINE;

EID: 67650065066     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00851-08     Document Type: Article

References (67)

1. Ahn, S., J. Kim, C. L. Lucaveche, M. C. Reedy, L. M. Luttrell, R. J. Lefkowitz, and Y. Daaka. 2002. Src-dependent tyrosine phosphorylation regulates dynamin self-assembly and ligand-induced endocytosis of the epidermal growth factor receptor. J. Biol. Chem. 277:26642-26651.
2. Ahn, S., S. Maudsley, L. M. Luttrell, R. J. Lefkowitz, and Y. Daaka. 1999. Src-mediated tyrosine phosphorylation of dynamin is required for β2-adrenergic receptor internalization and mitogen-activated protein kinase signaling. J. Biol. Chem. 274:1185-1188.
3. Altschuler, Y., S. M. Barbas, L. J. Terlecky, K. Tang, S. Hardy, K. E. Mostov, and S. L. Schmid. 1998. Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J. Cell Biol. 143:1871-1881.
4. Avraham, H., S.-Y. Park, K. Schinkmann, and S. Avraham. 2000. RAFTK/ Pyk2-mediated cellular signalling. Cell Signal. 12:123-133.
5. Bain, J., H. McLauchlan, M. Elliott, and P. Cohen. 2003. The specificities of protein kinase inhibitors: an update. Biochem. J. 371:199-204.
6. Bashkirov, P. V., S. A. Akimov, A. I. Evseev, S. L. Schmid, J. Zimmerberg, and V. A. Frolov. 2008. GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135:1276-1286.
7. Bishop, A. L., and A. Hall. 2000. Rho GTPases and their effector proteins. Biochem. J. 348:241-255.
8. Bruzzaniti, A., L. Neff, A. Sanjay, W. C. Horne, P. De Camilli, and R. Baron. 2005. Dynamin forms a Src kinase-sensitive complex with Cbl and regulates podosomes and osteoclast activity. Mol. Biol. Cell 16:3301-3313.
9. Butler, B., C. Gao, A. T. Mersich, and S. D. Blystone. 2006. Purified integrin adhesion complexes exhibit actin-polymerization activity. Curr. Biol. 16:242-251.
10. Cao, H., F. Garcia, and M. A. McNiven. 1998. Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell 9:2595-2609.
11. Chen, W.-T. 1989. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J. Exp. Zool. 251:167-185.
12. Damke, H., T. Baba, D. E. Warnock, and S. L. Schmid. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:915-934.
13. Damke, H., D. D. Binns, H. Ueda, S. L. Schmid, and T. Baba. 2001. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12:2578-2589.
14. Destaing, O., F. Saltel, J.-C. Geminard, P. Jurdic, and F. Bard. 2003. Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 14:407-416.
15. Destaing, O., A. Sanjay, C. Itzstein, W. C. Horne, D. Toomre, P. De Camilli, and R. Baron. 2008. The tyrosine kinase activity of c-Src regulates actin dynamics and organization of podosomes in osteoclasts. Mol. Biol. Cell 19:394-404.
16. Dikic, I., G. Tokiwa, S. Lev, S. A. Courtneidge, and J. Schlessinger. 1996. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383:547-550.
17. 3 integrin, and phosphorylated by Src kinase. J. Clin. Investig. 102:881-892.
18. Duong, L. T., I. Nakamura, P. T. Lakkakorpi, L. Lipfert, A. J. Bett, and G. A. Rodan. 2001. Inhibition of osteoclast function by adenovirus expressing antisense protein-tyrosine kinase 2. J. Biol. Chem. 276:7484-7492.
19. 3 integrin in osteoclasts. Int. J. Biochem. Cell Biol. 38:1518-1529.
20. 3 integrin. J. Cell Biol. 162:499-509.
21. 3 integrin collaborate during osteoclast differentiation. J. Clin. Investig. 111:749-758.
22. Felsch, J. S., T. G. Cachero, and E. G. Peralta. 1998. Activation of protein tyrosine kinase PYK2 by the m1 muscarinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA 95:5051-5056.
23. Feshchenko, E. A., W. Y. Langdon, and A. Y. Tsygankov. 1998. Fyn, Yes, and Syk phosphorylation sites in c-Cbl map to the same tyrosine residues that become phosphorylated in activated T cells. J. Biol. Chem. 273:8323-8331.
24. src substrate. Mol. Cell. Biol. 13:7892-7900.
25. Foster-Barber, A., and J. M. Bishop. 1998. Src interacts with dynamin and synapsin in neuronal cells. Proc. Natl. Acad. Sci. USA 95:4673-4677.
26. -/- mice. J. Cell Biol. 178:1053-1064.
27. Herskovits, J. S., H. S. Shpetner, C. C. Burgess, and R. B. Vallee. 1993. Microtubules and Src homology 3 domains stimulate the dynamin GTPase via its C-terminal domain. Proc. Natl. Acad. Sci. USA 90:11468-11472.
28. Huang, F., A. Khvorova, W. Marshall, and A. Sorkin. 2004. Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J. Biol. Chem. 279:16657-16661.
29. Jurdic, P., F. Saltel, A. Chabadel, and O. Destaing. 2006. Podosome and sealing zone: specificity of the osteoclast model. Eur. J. Cell Biol. 85:195-202.
30. src direct stable association with tyrosine phosphorylated proteins p130 and p110. EMBO J. 10:1689-1698.
31. Lakkakorpi, P. T., A. J. Bett, L. Lipfert, G. A. Rodan, and L. T. Duong. 2003. PYK2 autophosphorylation, but not kinase activity, is necessary for adhesion-induced association with c-Src, osteoclast spreading, and bone resorption. J. Biol. Chem. 278:11502-11512.
32. 3 integrins and associated proteins in Src-deficient or tyrphostin A9-treated osteoclasts. J. Cell Sci. 114:149-160.
33. 2+-induced regulation of ion channel and MAP kinase functions. Nature 376:737-745.
34. Linder, S., and M. Aepfelbacher. 2003. Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 13:376-385.
35. Luxenburg, C., J. T. Parsons, L. Addadi, and B. Geiger. 2006. Involvement of the Src-cortactin pathway in podosome formation and turnover during polarization of cultured osteoclasts. J. Cell Sci. 119:4878-4888.
36. Lyons, P. D., J. M. Dunty, E. M. Schaefer, and M. D. Schaller. 2001. Inhibition of the catalytic activity of cell adhesion kinase β by protein-tyrosine phosphatase-PEST-mediated dephosphorylation. J. Biol. Chem. 276:24422-24431.
37. Marchisio, P. C., D. Cirillo, A. Teti, A. Zambonin-Zallone, and G. Tarone. 1987. Rous sarcoma virus-transformed fibroblasts and cells of monocytic origin display a peculiar dot-like organization of cytoskeletal proteins involved in microfilament-membrane interactions. Exp. Cell Res. 169:202-214.
38. McNiven, M. A., M. Baldassarre, and R. Buccione. 2004. The role of dynamin in the assembly and function of podosomes and invadopodia. Front. Biosci. 9:1944-1953.
39. Miller, W. E., S. Maudsley, S. Ahn, K. D. Khan, L. M. Luttrell, and R. J. Lefkowitz. 2000. β-arrestin1 interacts with the catalytic domain of the tyrosine kinase c-SRC: role of β-arrestin1-dependent targeting of c-SRC in receptor endocytosis. J. Biol. Chem. 275:11312-11319.
40. Miyazaki, T., A. Sanjay, L. Neff, S. Tanaka, W. C. Horne, and R. Baron. 2004. Src kinase activity is essential for osteoclast function. J. Biol. Chem. 279:17660-17666.
41. Miyazaki, T., H. Takayanagi, M. Isshiki, T. Takahashi, M. Okada, Y. Fukui, H. Oda, K. Nakamura, H. Hirai, T. Kurokawa, and S. Tanaka. 2000. In vitro and in vivo suppression of osteoclast function by adenovirus vector-induced csk gene. J. Bone Miner Res. 15:41-51.
42. Cas is involved in actin organization in osteoclasts. J. Biol. Chem. 273:11144-11149.
43. Ochoa, G.-C., V. I. Slepnev, L. Neff, N. Ringstad, K. Takei, L. Daniell, W. Kim, H. Cao, M. McNiven, R. Baron, and P. De Camilli. 2000. A functional link between dynamin and the actin cytoskeleton at podosomes. J. Cell Biol. 150:377-389.
44. Okamura, H., and M. D. Resh. 1995. p80/85 cortactin associates with the Src SH2 domain and colocalizes with v-Src in transformed cells. J. Biol. Chem. 270:26613-26618.
45. Orth, J. D., and M. A. McNiven. 2003. Dynamin at the actin-membrane interface. Curr. Opin. Cell Biol. 15:31-39.
46. Park, S.-Y., H. K. Avraham, and S. Avraham. 2004. RAFTK/Pyk2 activation is mediated by trans-acting autophosphorylation in a Src-independent manner. J. Biol. Chem. 279:33315-33322.
47. 3. J. Cell Sci. 114:2775-2786.
48. Ray, B. J., and A. H. Boughton. 2008. Investigations into the role of focal adhesion kinase (FAK) in bone marrow-derived osteoclasts. J. Bone Miner. Res. 23(Suppl. 1):S269.
49. Sakai, R., A. Iwamatsu, N. Hirano, S. Ogawa, T. Tanaka, H. Mano, Y. Yazaki, and H. Hirai. 1994. A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner. EMBO J. 13:3748-3756.
50. 3 integrin-mediated signaling, cell adhesion, and osteoclast motility. J. Cell Biol. 152:181-195.
51. Sanjay, A., T. Miyazaki, C. Itzstein, E. Purev, W. C. Horne, and R. Baron. 2006. Identification and functional characterization of an Src homology domain 3 domain-binding site on Cbl. FEBS J. 273:5442-5456.
52. Schlaepfer, D. D., C. R. Hauck, and D. J. Sieg. 1999. Signaling through focal adhesion kinase. Prog. Biophys. Mol. Biol. 71:435-478.
53. Schmid, S. L., M. A. McNiven, and P. De Camilli. 1998. Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10:504-512.
54. -/- mutant mice. Genes Dev. 11: 2835-2844.
55. Sever, S., H. Damke, and S. L. Schmid. 2000. Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1:385-392.
56. Shajahan, A. N., B. K. Timblin, R. Sandoval, C. Tiruppathi, A. B. Malik, and R. D. Minshall. 2004. Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells. J. Biol. Chem. 279:20392-20400.
57. - cell migration. EMBO J. 17:5933-5947.
58. Slepnev, V. I., and P. De Camilli. 2000. Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat. Rev. Neurosci. 1:161-172.
59. Soriano, P., C. Montgomery, R. Geske, and A. Bradley. 1991. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702.
60. Stickel, S. K., and Y. Wang. 1987. Alpha-actinin-containing aggregates in transformed cells are highly dynamic structures. J. Cell Biol. 104:1521-1526.
61. Takayanagi, H., S. Kim, and T. Taniguchi. 2002. Signaling crosstalk between RANKL and interferons in osteoclast differentiation. Arthritis Res. 4(Suppl. 3):S227-S232.
62. Tanaka, S., M. Amling, L. Neff, A. Peyman, E. Uhlmann, J. B. Levy, and R. Baron. 1996. c-Cbl is downstream of c-Src in a signalling pathway necessary for bone resorption. Nature 383:528-531.
63. Tanaka, S., T. Takahashi, H. Takayanagi, T. Miyazaki, H. Oda, K. Nakamura, H. Hirai, and T. Kurokawa. 1998. Modulation of osteoclast function by adenovirus vector-induced epidermal growth factor receptor. J. Bone Miner Res. 13:1714-1720.
64. Thien, C. B. F., and W. Y. Langdon. 2005. c-Cbl and Cbl-b ubiquitin ligases: substrate diversity and the negative regulation of signalling responses. Biochem. J. 391:153-166.
65. Wang, Q., Y. Xie, Q.-S. Du, X.-J. Wu, X. Feng, L. Mei, J. M. McDonald, and W.-C. Xiong. 2003. Regulation of the formation of osteoclastic actin rings by proline-rich tyrosine kinase 2 interacting with gelsolin. J. Cell Biol. 160:565-575.
66. Zhang, Z., L. Neff, A. L. M. Bothwell, R. Baron, and W. C. Horne. 2002. Calcitonin induces dephosphorylation of Pyk2 and phosphorylation of focal adhesion kinase in osteoclasts. Bone 31:359-365.
67. Zrihan-Licht, S., S. Avraham, S. Jiang, Y. Fu, and H. K. Avraham. 2004. Coupling of RAFTK/Pyk2 kinase with c-Abl and their role in the migration of breast cancer cells. Int. J. Oncol. 24:153-159.