Regulation of the formation of osteoclastic actin rings by proline-rich tyrosine kinase 2 interacting with gelsolin

Journal of Cell Biology

Volumn 160, Issue 4, 2003, Pages 565-575

  Wang, Qiang ^b   Xie, Yi ^a   Du, Quan Sheng ^a,e   Wu, Xiao Jun ^a   Feng, Xu ^a   Mei, Lin ^a,b,c   McDonald, Jay M ^a,d   Xiong, Wen Cheng ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d BIRMINGHAM VA MEDICAL CENTER   (United States)

^e UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Actin cytoskeleton; FAK; Focal adhesions; Podosomes; PYK2

Indexed keywords

ACTIN; GELSOLIN; PHOSPHATIDYLINOSITOL; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; BONE DISEASE; BONE REMODELING; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CONTROLLED STUDY; CYTOSKELETON; FIBROBLAST; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION;

ACTINS; AMINO ACID MOTIFS; ANIMALS; CELL ADHESION; CELL LINE; CYTOSKELETON; FIBROBLASTS; FLUORESCENT DYES; FOCAL ADHESION KINASE 2; GELSOLIN; HUMANS; MICE; MICE, KNOCKOUT; OSTEOCLASTS; PHALLOIDINE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; RECOMBINANT FUSION PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

ANIMALIA;

EID: 0037450657     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200207036     Document Type: Article

References (46)

1. Akisaka, T., H. Yoshida, S. Inoue, and K. Shimizu. 2001. Organization of cytoskeletal F-actin, G-actin, and gelsolin in the adhesion structures in cultured osteoclast. J. Bone Miner. Res. 16:1248-1255.
2. Azuma, T., W. Witke, T.P. Stossel, J.H. Hartwig, and D.J. Kwiatkowski. 1998. Gelsolin is a downstream effector of rac for fibroblast motility. EMBO J. 17:1362-1370.
3. Boyce, B.F., T. Yoneda, C. Lowe, P. Soriano, and G.R. Mundy. 1992. Requirement of pp60src expression for osteoclasts to form ruffled borders and resorb bone in mice. J. Clin. Invest. 90:1622-1627.
4. Brinson, A.E., T. Harding, P.A. Diliberto, Y. He, X. Li, D. Hunter, B. Herman, H.S. Earp, and L.M. Graves. 1998. Regulation of a calcium-dependent tyrosine kinase in vascular smooth muscle cells by angiotensin II and platelet-derived growth factor. Dependence on calcium and the actin cytoskeleton. J Biol. Chem. 273:1711-1718.
5. Brown, M.C., J.A. Perrotta, and C.E. Turner. 1996. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol. 135:1109-1123.
6. 2+-independent pathways. J. Exp. Med. 165:97-106.
7. Chellaiah, M., and K.A. Hruska. 1996. Osteopontin stimulates gelsolin associated phosphoinositide levels and PtdIns 3-hydroxyl kinase. Mol. Biol. Cell. 7:743-753.
8. Chellaiah, M., N. Kizer, M. Silva, U. Alvarez, D. Kwiatkowski, and K.A. Hruska. 2000. Gelsolin deficiency blocks podosome assembly and produces increased bone mass and strength. J. Cell Biol. 148:665-678.
9. De Corte, V., J. Gettemans, and J. Vandekerckhove. 1997. Phosphatidylinositol 4,5-bisphosphate specifically stimulates PP60(c-src) catalyzed phosphorylation of gelsolin and related actin-binding proteins. FEBS Lett. 401:191-196.
10. De Corte, V., H. Demol, M. Goethals, J. Van Damme, J. Gettemans, and J. Vandekerckhove. 1999. Identification of Tyr438 as the major in vitro c-Src phosphorylation site in human gelsolin: a mass spectrometric approach. Protein Sci. 8:234-241.
11. Du, Q.-S., X.-R. Ren, Y. Xie, Q. Wang, L. Mei, and W.-C. Xiong. 2001. Inhibition of PYK2-induced cytoskeletal reorganization, PYK2 autophosphorylation, and focal adhesion targeting by FAK. J. Cell Sci. 114:2977-2987.
12. Duong, L.T., P.T. Lakkakorpi, I. Nakamura, M. Machware, R.M. Nagy, and G.A. Rodan. 1998. PYK2 in osteoclasts is an adhesion kinase, localized in the sealing zone, activated by ligation of αvβ3 integrin, and phosphorylated by Src kinase. J. Clin. Invest. 102:881-892.
13. 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 PYK2. J. Biol. Chem. 276:7484-7492.
14. Feng, X., D.V. Novack, R. Faccio, D.S. Ory, K. Aya, M.I. Boyer, K.P. McHugh, F.P. Ross, and S.L. Teitelbaum. 2001. A Glanzmann's mutation in beta 3 integrin specifically impairs osteoclast function. J. Clin. Invest. 107:1137-1144.
15. He, T-C., S. Zhou, L.T. Da Costa, J. Yu, K.W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA. 95:2509-2514.
16. Janmey, P.A., and T.P. Stossel. 1987. Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate. Nature. 325:362-364.
17. Janmey, P.A., C. Chaponnier, S.E. Lind, K.S. Zaner, T.P. Stossel, and H.L. Yin. 1985. Interactions of gelsolin and gelsolin-actin complexes with actin. Effects of calcium on actin nucleation, filament severing, and end blocking. Biochemistry. 24:3714-3723.
18. Kanehisa, J., T. Yamanaka, S. Doi, K. Turksen, J.N.M. Heersche, J.E. Aubin, and H. Takeuchi. 1990. A band of F-actin containing podosomes is involved in bone resorption by osteoclasts. Bone. 11:287-293.
19. 2+-insensitive functions. J. Biol. Chem. 258:10895-10903.
20. Kwiatkowski, D.J. 1999. Functions of gelsolin: motility, signaling, apoptosis, and cancer. Curr. Opin. Cell Biol. 11:103-108.
21. Kwiatkowski, D.J., P.A. Janmey, and H.L. Yin. 1989. Identification of critical functional and regulatory domains in gelsolin. J. Cell Biol. 108:1717-1726.
22. Lakkakorpi, P.T., I. Nakamura, R.M. Nagy, J.T. Parsons, G.A. Rodan, and L.T. Duong. 1999. Stable association of PYK2 and p130(Cas) in osteoclasts and their co-localization in the sealing zone. J. Biol. Chem. 27:4900-4907.
23. 2+-induced regulation of ion channel and MAP kinase functions. Nature. 376:737-745.
24. Lev, S., J. Hernandez, R. Martinez, A. Chen, G. Plowman, and J. Schlessinger. 1999. Identification of a novel family of targets of PYK2 related to Drosophila retinal degeneration B (rdgB) protein. Mol. Cell. Biol. 19:2278-2288.
25. Lind, S.E., H.L. Yin, and T.P. Stossel. 1982. Human platelets contain gelsolin. A regulator of actin filament length. J. Clin. Invest. 69:1384-1387.
26. Lind, S.E., P.A. Janmey, C. Chaponnier, T.J. Herbert, and T.P. Stossel. 1987. Reversible binding of actin to gelsolin and profilin in human platelet extracts. J. Cell Biol. 105:833-842.
27. Luo, Z.G., Q. Wang, J.Z. Zhou, J. Wang, Z. Luo, M.Y. Liu, X. He, A. Wynshaw-Boris, W.C. Xiong, B. Lu, and L. Mei. 2002. Regulation of AChR clustering by Dishevelled interacting with MuSK and PAK1. Neuron. 35:489-505.
28. Marchisio, P.C., D. Cirillo, L. Naldini, M.V. Primavera, A. Teti, and A. Zambonin-Zallone. 1984. Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures. J. Cell Biol. 99:1696-1705.
29. Matsuya, M., H. Sasaki, H. Aoto, T. Mitaka, K. Nagura, T. Ohba, M. Ishino, S. Takahashi, R. Suzuki, and T. Sasaki. 1998. Cell adhesion kinase beta forms a complex with a new member, Hic-5, of proteins localized at focal adhesions. J. Biol. Chem. 273:1003-1014.
30. Pfaff, M., and P. Jurdic. 2001. Podosomes in osteoclast-like cells: structural analysis and cooperative roles of paxillin, proline-rich tyrosine kinase 2 (PYK2) and integrin αvβ3. J. Cell Sci. 114:2775-2786.
31. Ren, X.R., Q.S. Du, Y.Z. Huang, S.Z. Ao, L. Mei, and W.C. Xiong. 2001. Regulation of CDC42 GTPase by PYK2 interacting with PSGAP, a novel PH and SH3 domain containing rhoGAP protein. J. Cell Biol. 152:971-983.
32. Robinson, R.C., M. Meijillano, V.P. Le, L.D. Burtnick, H.L. Yin, and S. Choe. 2000. Domain movement in gelsolin: a calcium-activated switch. Science. 286:1939-1942.
33. Sasaki, H., K. Nagura, M. Ishino, H. Tobioka, K. Kotani, and T. Sasaki. 1995. Cloning and characterization of cell adhesion kinase β, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J. Biol. Chem. 270:21206-21219.
34. FAK, a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA. 89:5192-5196.
35. Schwartzberg, P.L., L. Xing, O. Hoffmann, C.A. Lowell, L. Garrett, B.F. Boyce, and H.E. Varmus. 1997. Rescue of osteoclast function by transgenic expression of kinase-deficient Src in Src-/- mutant mice. Genes Dev. 11:2835-2844.
36. 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.
37. Sun, H.Q., M. Yamamoto, M. Meijillano, and H.L. Yin. 2000. Gelsolin, a multifunctional actin regulatory protein. J. Biol. Chem. 274:33179-33182.
38. FAK. J. Exp. Med. 182:1089-1100.
39. 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 signaling pathway necessary for bone resorption. Nature. 383:528-531.
40. Tarone, G., D. Cirillo, F.G. Giancotti, P.M. Comoglio, and P.C. Marchisio. 1985. Rous sarcoma virus-transformed fibroblasts adhere primarily as discrete protrusions of the ventral membrane called podosomes. Exp. Cell Res. 159:141-157.
41. Turner, C.E. 2000. Paxillin and focal adhesion signaling. Nat. Cell Biol 2:E231-E236.
42. Wang, L.L., and J. Bryan. 1981. Isolation of calcium-dependent platelet proteins that interact with actin. Cell. 25:637-649.
43. +-ATPase and bone resorption by tamoxifen and calmodulin antagonists. Effects independent of steroid receptors. J. Biol. Chem. 271:12488-12495.
44. Witke, W., A.H. Sharpe, J.H. Hartwig, T. Azuma, T.P. Stossel, and D.J. Kwiatkowski. 1995. Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin. Cell. 81:41-51.
45. Xiong, W.C., and J.T. Parsons. 1997. Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally related to focal adhesion kinase. J. Cell Biol. 139:529-539.
46. Yamamoto, M., D.H. Hilgemann, S. Feng, H. Bito, H. Ishihara, Y. Shibasaki, and H.L. Yin. 2001. Phosphatidylinositol 4,5-bisphosphate induces actin stress-fiber formation and inhibits membrane ruffling in CV1 cells. J. Cell Biol. 152:867-876.