Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation

Journal of Cell Biology

Volumn 166, Issue 5, 2004, Pages 697-708

  Mouneimne, Ghassan ^a   Soon, Lilian ^a   DesMarais, Vera ^a   Sidani, Mazen ^a   Song, Xiaoyan ^a   Yip, Shu Chin ^a   Ghosh, Mousumi ^a   Eddy, Robert ^a   Backer, Jonathan M ^a   Condeelis, John ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Actin; Chemotaxis; Motility; PI3 kinase; PLC

Indexed keywords

ANTIBODY; COFILIN; EPIDERMAL GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; SMALL INTERFERING RNA;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CARCINOMA CELL; CELL MOTION; CELL STIMULATION; CHEMOTAXIS; CONTROLLED STUDY; ENZYME INHIBITION; GENE SILENCING; LAMELLIPODIUM; NONHUMAN; PRIORITY JOURNAL; RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; ANTIBODIES; CARCINOMA; CELL LINE, TUMOR; CHEMOTAXIS; ENZYME INHIBITORS; EPIDERMAL GROWTH FACTOR; MICROFILAMENT PROTEINS; MICROFILAMENTS; NEOPLASM METASTASIS; PHOSPHOLIPASE C; PSEUDOPODIA; RATS; RNA INTERFERENCE;

ANIMALIA;

EID: 4444296491     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200405156     Document Type: Article

References (58)

1. Abercrombie, M., J.E. Heaysman, and S.M. Pegrum. 1972. Locomotion of fibroblasts in culture. V. Surface marking with concanavalin A. Exp. Cell Res. 73:536-539.
2. Allen, P.G. 2003. Actin filament uncapping localizes to ruffling lamellae and rocketing vesicles. Nat. Cell Biol. 5:972-979.
3. Arber, S., F.A. Barbayannis, H. Hanser, C. Schneider, C.A. Stanyon, O. Bernard, and P. Caroni. 1998. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature. 393:805-809.
4. Bailly, M., and J. Condeelis. 2002. Cell motility: insights from the backstage. Nat. Cell Biol. 4:E292-E294.
5. Bailly, M., I. Ichetovkin, W. Grant, N. Zebda, L.M. Machesky, J.E. Segall, and J. Condeelis. 2001. The F-actin side binding activity of the Arp2/3 complex is essential for actin nucleation and lamellipod extension. Curr. Biol. 11:620-625.
6. Bleasdale, J.E., G.L. Bundy, S. Bunting, F.A. Fitzpatrick, R.M. Huff, F.F. Sun, and J.E. Pike. 1989. Inhibition of phospholipase C dependent processes by U-73, 122. Adv. Prostaglandin Thromboxane Leukot. Res. 19:590-593.
7. Chan, A.Y., S. Raft, M. Bailly, J.B. Wyckoff, J.E. Segall, and J.S. Condeelis. 1998. EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells. J. Cell Sci. 111:199-211.
8. Chan, A. Y., M. Bailly, N. Zebda, J.E. Segall, and J.S. Condeelis. 2000. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J. Cell Biol. 148:531-542.
9. Chen, L., C. Janetopoulos, Y.E. Huang, M. Iijima, J. Borleis, and P.N. Devreotes. 2003. Two phases of actin polymerization display different dependencies on PI(3,4,5)P3 accumulation and have unique roles during chemotaxis. Mol Biol Cell. 14:5028-5037.
10. Chen, P., K. Gupta, and A. Wells. 1994. Cell movement elicited by epidermal growth factor receptor requites kinase and autophosphorylation but is separable from mitogenesis. J. Cell Biol. 124:547-555.
11. Chou, J., N.A. Burke, A. Iwabu, S.C. Watkins, and A. Wells. 2003. Directional motility induced by epidermal growth factor requires Cdc42. Exp. Cell Res. 287:47-56.
12. Comer, F.I., and C.A. Parent. 2002. PI 3-kinases and PTEN: how opposites chemoattract. Cell. 109:541-544.
13. Cooper, J.A., and D.A. Schafer. 2000. Control of actin assembly and disassembly at filament ends. Curr. Opin. Cell Biol. 12:97-103.
14. Cox, D., J. Condeelis, D. Wessels, D. Soll, H. Kern, and D.A. Knecht. 1992. Targeted disruption of the ABP-120 gene leads to cells with altered motility. J. Cell Biol. 116:943-955.
15. den Hartigh, J.C., P.M. van Bergen en Henegouwen, A.J. Verkleij, and J. Boonstra. 1992. The EGF receptor is an actin-binding protein. J Cell Biol. 119:349-355.
16. DesMarais, V., F. Macaluso, J. Condeelis, and M. Bailly. 2004. Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J. Cell Sci. 117:3499-3510.
17. Devreotes, P., and C. Janetopoulos. 2003. Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J. Biol. Chem. 278:20445-20448.
18. dos Remedios, C.G., D. Chhabra, M. Kekic, I.V. Dedova, M. Tsubakihata, D.A. Berry, and N.J. Nosworthy. 2003. Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83:433-473.
19. Eddy, R.J., J. Han, R.A. Sauterer, and J.S. Condeelis. 1996. A major agonist-regulated capping activity in Dictyostelium is due to the capping protein, cap32/ 34. Biochim. Biophys. Acta. 1314:247-259.
20. Eddy, R.J., J. Han, and J.S. Condeelis. 1997. Capping protein terminates but does not initiate chemoattractant-induced actin assembly in Dictyostelium. J. Cell Biol. 139:1243-1253.
21. Falasca, M., S.K. Logan, V.P. Lehto, G. Baccante, M.A. Lemmon, and J. Schlessinger. 1998. Activation of phospholipase C γ by PI 3-kinase-induced PH domain-mediated membrane Targeting. EMBO J. 17:414-422.
22. Funamoto, S., R. Meili, S. Lee, L. Parry, and R.A. Firtel. 2002. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell. 109:611-623.
23. Ghosh, M., X. Song, G. Mouneimne, M. Sidani, D.S. Lawrence, and J.S. Condeelis. 2004. Cofilin promotes actin polymerization and defines the direction of cell motility. Science. 304:743-746.
24. Goldschmidt-Clermont, P.J., J.W. Kim, L.M. Machesky, S.G. Rhee, and T.D. Pollard. 1991. Regulation of phospholipase C-γ 1 by profilin and tyrosine phosphorylation. Science. 251:1231-1233.
25. Hall, A.L., V. Warren, S. Dharmawardhane, and J. Condeelis. 1989. Identification of actin nucleation activity and polymerization inhibitor in ameboid cells: their regulation by chemotactic stimulation. J. Cell Biol. 109:2207-2213.
26. Higgs, H.N., and T.D. Pollard. 2001. Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70:649-676.
27. Hill, K., S. Welti, J. Yu, J.T. Murray, S.C. Yip, J.S. Condeelis, J.E. Segall, and J.M. Backer. 2000. Specific requirement for the p85-p110α phosphatidylinositol 3-kinase during epidermal growth factor-stimulated actin nucleation in breast cancer cells. J. Biol. Chem. 275:3741-3744.
28. Ichetovkin, I., J. Han, K.M. Pang, D.A. Knecht, and J.S. Condeelis. 2000. Actin filaments are severed by both native and recombinant dictyostelium cofilin but to different extents. Cell. Motil. Cytoskeleton. 45:293-306.
29. Ichetovkin, I., W. Grant, and J. Condeelis. 2002. Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr. Biol. 12:79-84.
30. Iijima, M., and P. Devreotes. 2002. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell. 109:599-610.
31. Kanamori, T., T. Hayakawa, M. Suzuki, and K. Titani. 1995. Identification of two 17-kDa rat parotid gland phosphoproteins, subjects for dephosphorylation upon β-adrenergic stimulation, as destrin- and cofilin-like proteins. J. Biol. Chem. 270:8061-8067.
32. Kassis, J., J. Moellinger, H. Lo, N.M. Greenberg, H.G. Kim, and A. Wells. 1999. A role for phospholipase C-γ-mediated signaling in tumor cell invasion. Clin. Cancer Res. 5:2251-2260.
33. Kassis, J., R. Radinsky, and A. Wells. 2002. Motility is rate-limiting for invasion of bladder carcinoma cell lines. Int. J. Biochem. Cell Biol. 34:762-775.
34. Lauffenburger, D.A., and A.F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359-369.
35. Lorenz, M., V. DesMarais, F. Macaluso, R.H. Singer, and J. Condeelis. 2004a. Measurement of barbed ends, actin polymerization, and motility in live carcinoma cells after growth factor stimulation. Cell Motil. Cytoskeleton. 57:207-217.
36. Lorenz, M., H. Yamaguchi, Y. Wang, R.H. Singer, and J. Condeelis. 2004b. Imaging sites of N-wasp activity in lamellipodia and invadopodia of carcinoma cells. Curr. Biol. 14:697-703.
37. Moriyama, K., K. Iida, and I. Yahara. 1996. Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells. 1:73-86.
38. Nishita, M., Y. Wang, C. Tomizawa, A. Suzuki, R. Niwa, T. Uemura, and K. Mizuno. 2003. Phosphoinositide 3-kinase-mediated activation of cofilin phosphatase Slingshot and its role for insulin-induced membrane protrusion. J Biol Chem. 279:7193-7198.
39. Okada, K., H. Takano-Ohmuro, T. Obinata, and H. Abe. 1996. Dephosphorylation of cofilin in polymorphonuclear leukocytes derived from peripheral blood. Exp. Cell Res. 227:116-122.
40. Payrastre, B., P.M. van Bergen en Henegouwen, M. Breton, J.C. den Hartigh, M. Plantavid, A.J. Verkleij, and J. Boonstra. 1991. Phosphoinositide kinase, diacylglycerol kinase, and phospholipase C activities associated to the Cytoskeleton: effect of epidermal growth factor. J Cell Biol. 115:121-128.
41. Piccolo, E., P.F. Innominato, M.A. Mariggio, T. Maffucci, S. Iacobelli, and M. Falasca. 2002. The mechanism involved in the regulation of phospholipase Cγ1 activity in cell migration. Oncogene. 21:6520-6529.
42. Raftopoulou, M., S. Etienne-Manneville, A. Self, S. Nicholls, and A. Hall. 2004. Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science. 303:1179-1181.
43. Rebecchi, M.J., and S.N. Pentyala. 2000. Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol. Rev. 80:1291-1335.
44. Rozelle, A.L., L.M. Machesky, M. Yamamoto, M.H. Driessens, R.H. Insall, M.G. Roth, K. Luby-Phelps, G. Marriott, A. Hall, and H.L. Yin. 2000. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10:311-320.
45. Sakisaka, T., T. Itoh, K. Miuta, and T. Takenawa. 1997. Phosphatidylinositol 4,5-bisphosphate phosphatase regulates the rearrangement of actin filaments. Mol. Cell. Biol. 17:3841-3849.
46. Servant, G., O.D. Weiner, P. Herzmark, T. Balla, J.W. Sedat, and H.R. Bourne. 2000. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science. 287:1037-1040.
47. Shibasaki, Y., H. Ishihara, N. Kizuki, T. Asano, Y. Oka, and Y. Yazaki. 1997. Massive actin polymerization induced by phosphatidylinositol-4-phosphate 5-kinase in vivo. J. Biol. Chem. 272:7578-7581.
48. Sukumvanich, P., V. DesMarais, C.V. Sermiento, Y. Wang, I. Ichetovkin, C. Mouneimne, S. Almo, and J. Condeelis. 2004. Cellular localization of activated N-WASP using a conformationally sensitive antibody. Cell Motil. Cytoskeleton. In press.
49. Sun, H.Q., M. Yamamoto, M. Mejillano, and H.L. Yin. 1999. Gelsolin, a multi-functional actin regulatory protein. J. Biol. Chem. 274:33179-33182.
50. Takenawa, T., and H. Miki. 2001. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114:1801-1809.
51. Wu, H., V. Goel, and F.G. Haluska. 2003. PTEN signaling pathways in melanoma. Oncogene. 22:3113-3122.
52. Wyckoff, J.B., J.G. Jones, J.S. Condeelis, and J.E. Segall. 2000a. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 60:2504-2511.
53. Wyckoff, J.B., J.E. Segall, and J.S. Condeelis. 2000b. The collection of the motile population of cells from a living tumor. Cancer Res. 60:5401-5404.
54. 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.
55. Yonezawa, N., E. Nishida, K. Iida, I. Yahara, and H. Sakai. 1990. Inhibition of the interactions of cofilin, destrin, and deoxyribonuclease I with actin by phosphoinositides. J. Biol. Chem. 265:8382-8386.
56. Yonezawa, N., Y. Homma, I. Yahara, H. Sakai, and E. Nishida. 1991. A short sequence responsible for both phosphoinositide binding and actin binding activities of cofilin. J. Biol. Chem. 266:17218-17221.
57. Zebda, N., O. Bernard, M. Bailly, S. Welti, D.S. Lawrence, and J.S. Condeelis. 2000. Phosphorylation of ADF/cofilin abolishes EGF-induced actin nucleation at the leading edge and subsequent lamellipod extension. J. Cell Biol. 151:1119-1128.
58. Zhan, Q., J.R. Bamburg, and J.A. Badwey. 2003. Products of phosphoinositide specific phospholipase C can trigger dephosphorylation of cofilin in chemoattractant stimulated neutrophils. Cell Motil. Cytoskeleton. 54:1-15.