PLCγ1 is essential for early events in integrin signalling required for cell motility

Journal of Cell Science

Volumn 118, Issue 12, 2005, Pages 2695-2706

  Jones, Neil P ^a   Peak, Joanna ^a   Brader, Sharon ^a   Eccles, Suzanne A ^a   Katan, Matilda ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Extracellular matrix; Motility; PLC 1; Signalling

Indexed keywords

BETA1 INTEGRIN; CALCIUM; GROWTH FACTOR; INTEGRIN; PHOSPHOLIPASE C GAMMA; PHOSPHOLIPASE C GAMMA1; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CDED PROTEIN, MOUSE; INOSITOL 1,4,5 TRISPHOSPHATE; MUSCLE PROTEIN; PHOSPHOLIPASE C;

ARTICLE; BIOCHEMISTRY; CALCIUM CELL LEVEL; CANCER CELL; CELL ADHESION; CELL ELONGATION; CELL INVASION; CELL LYSATE; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MORPHOGENESIS; PHARMACOLOGICAL BLOCKING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; BASEMENT MEMBRANE; CALCIUM SIGNALING; CELL CULTURE; CELL MOTION; CELL SHAPE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; FIBROBLAST; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION; TIME;

ANIMALS; BASEMENT MEMBRANE; CALCIUM SIGNALING; CELL MOVEMENT; CELL SHAPE; ENDOTHELIAL CELLS; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; INTEGRINS; MICE; MUSCLE PROTEINS; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PHOSPHORYLATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 21644478210     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02374     Document Type: Article

References (48)

1. Cary, L. A., Klinghoffer, R. A., Sachsenmaier, C. and Cooper, J. A. (2002). SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading. Mol. Cell. Biol. 22, 2427-2440.
2. Chen, P., Xie, H., Sekar, M. C., Gupta, K. and Wells, A. (1994). Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J. Cell Biol. 127, 847-857.
3. Connolly, J., Simpson, N., Hewlett, L. and Hall, A. (2002). Rac regulates endothelial morphogenesis and capillary assembly. Mol. Biol. Cell 13, 2474-2485.
4. Davis, G. E., Bayless, K. J. and Mavila, A. (2002). Molecular basis of endothelial cell morphogenesis in three-dimensional extracellular matrices. Anat. Rec. 268, 252-275.
5. 2+ /calmodulin-dependent protein kinase II are involved in platelet-derived growth factor-induced phosphorylation of Tiam1. FEBS Lett. 249, 229-233.
6. Friedl, P. and Brocker, E. B. (2000). The biology of cell locomotion within three-dimensional extracellular matrix. Cell. Mol. Life Sci. 57, 41-64.
7. Friedl, P. and Wolf, K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
8. Haendeler, J., Yin, G., Hojo, Y., Saito, Y., Melaragno, M., Yan, C., Sharma, V. K., Heller, M., Aebersold, R. and Berk, B. C. (2003). GIT1 mediates Src-dependent activation of phospholipase Cγ by angiotensin II and epidermal growth factor. J. Biol. Chem. 278, 49936-49944.
9. Inoue, O., Suzuki-Inoue, K., Dean, W. L., Frampton, J. and Watson, S. P. (2003). Integrin α2β1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLCγ2. J. Cell Biol. 160, 769-780.
10. Ji, Q. S., Winnier, G. E., Niswender, K. D., Horstman, D., Wisdom, R., Magnuson, M. A. and Carpenter, G. (1997). Essential role of the tyrosine kinase substrate phospholipase C-gamma1 in mammalian growth and development. Proc. Natl. Acad. Sci. USA 94, 2999-3003.
11. Ji, Q. S., Ermini, S., Baulida, J., Sun, F. L. and Carpenter, G. (1998). Epidermal growth factor signaling and mitogenesis in Plcg1 null mouse embryonic fibroblasts. Mol. Biol. Cell 9, 749-757.
12. Kao, J. P. Y., Harootunian, A. T. and Tsien, R. Y. (1989). Photochemically generated cytosolic calcium pulses and their detection by Fluo-3. J. Biol. Chem. 264, 8179-8184.
13. Kassis, J., Moellinger, J., Lo, H., Greenberg, N. M., Kim, H. G. and Wells, A. (1999). A role for phospholipase C-gamma-mediated signaling in tumor cell invasion. Clin. Cancer Res. 5, 2251-2260.
14. Kassis, J., Lauffenburger, D. A., Turner, T. and Wells, A. (2001). Tumor invasion as dysregulated cell motility. Semin. Cancer Biol. 11, 105-117.
15. Katan, M. (1998). Families of phosphoinositide-specific phospholipase C: structure and function. Biochem. Biophys. Acta 1436, 5-17.
16. Klinghoffer, R. A., Sachsenmaier, C., Cooper, J. A. and Soriano, P. (1999). Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18, 2459-2471.
17. Kundra, V., Escobedo, J. A., Kazlauskas, A., Kim, H. K., Rhee, S. G., Williams, L. T. and Zetter, B. R. (1994). Regulation of chemotaxis by the platelet-derived growth factor receptor-beta. Nature 367, 474-476.
18. Langholz, O., Roeckel, D., Petersohn, D., Broermann, E., Eckes, B. and Krieg, T. (1997). Cell-matrix interactions induce tyrosine phosphorylation of MAP kinases ERK1 and ERK2 and PLCgamma-1 in two-dimensional and three-dimensional cultures of human fibroblasts. Exp. Cell. Res. 235, 22-27.
19. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
20. Liao, F., Shin, H. S. and Rhee, S. G. (1993). In vitro tyrosine phosphorylation of PLC-gamma 1 and PLC-gamma 2 by src-family protein tyrosine kinases. Biochem. Biophys. Res. Commun. 191, 1028-1033.
21. Liao, H. J., Kume, T., McKay, C., Xu, M. J., Ihle, J. N. and Carpenter, G. (2002). Absence of erythrogenesis and vasculogenesis in Plcg1-deficient mice. J. Biol. Chem. 277, 9335-9341.
22. Manabe, R. R., Kovalenko, M., Webb, D. J. and Horwitz, A. R. (2002). GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J. Cell Sci. 115, 1497-1510.
23. Mangin, P., Yuan, Y., Goncalves, I., Eckly, A., Freund, M., Cazenave, J. P., Gachet, C., Jackson, S. P. and Lanza, F. (2003). Signaling role for phospholipase C gamma 2 in platelet glycoprotein Ib alpha calcium flux and cytoskeletal reorganization. Involvement of a pathway distinct from FcR gamma chain and Fc gamma RIIA. J. Biol. Chem. 278, 32880-32891.
24. Miranti, C. K. and Brugge, J. S. (2002). Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell. Biol. 4, E83-E90.
25. Mullinax, T. R., Henrich, G., Kasila, P., Ahern, D. G., Wenke, E. A., Hou, C., Argentieri, D. and Bembenek, M. E. (1999). Monitoring inositol-specific phospholipase C activity using a phospholipid FlashPlate. J. Biomol. Screening 4, 151-155.
26. Nakamura, I., Lipfert, L., Rodan, G. A. and Duong, L. T. (2001). Convergence of alpha(v)beta(3) integrin- and macrophage colony stimulating factor-mediated signals on phospholipase Cgamma in prefusion osteoclasts. J. Cell Biol. 152, 361-373.
27. Nehls, V., Herrmann, R. and Huhnken, M. (1998). Guided migration as a novel mechanism of capillary network remodeling is regulated by basic fibroblast growth factor. Histochem. Cell. Biol. 109, 319-329.
28. Nogami, M., Yamazaki, M., Watanabe, H., Okabayashi, Y., Kido, Y., Kasuga, M., Sasaki, T., Maehama, T. and Kanaho, Y. (2003). Requirement of autophosphorylated tyrosine 992 of EGF receptor and its docking protein phospholipase C gamma 1 for membrane ruffle formation. FEBS Lett. 536, 71-76.
29. 2+ entry. Cell 111, 529-541.
30. Price, J. T., Tiganis, T., Agarwal, A., Djakiew, D. and Thompson, E. W. (1999). Epidermal growth factor promotes NMA-MB-231 breast cancer cell migration through a phosphatidylinositol 3′-kinase and phospholipase C-dependent mechanism. Cancer Res. 59, 5475-5478.
31. Putney, J. W. (2002). PLC-gamma: an old player has a new role. Nat. Cell. Biol. 4, E280-E281.
32. Raucher, D., Stauffer, T., Chen, W., Shen, K., Guo, S., York, J. D., Sheetz, M. P. and Meyer, T. (2000). Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228.
33. Rebecchi, M. J. and Pentyala, S. N. (2000). Structure, function, and control of phosphoinositide-specific phospholipase C. Physiolosical Reviews 80, 1291-1335.
34. Rhee, S.-G. (2001). Regulation of phophoinositide-specific phospholipase C. Annu. Rev. Biochem. 70, 281-312.
35. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
36. Rodriguez, R., Matsuda, M., Perisic, O., Bravo, J., Paul, A., Jones, N. P., Light, Y., Swann, K., Williams, R. L. and Katan, M. (2001). Tyrosine residues in phospholipase Cgamma 2 essential for the enzyme function in B-cell signaling. J. Biol. Chem. 276, 47982-47992.
37. Ronnstrand, L., Siegbahn, A., Rorsman, C., Johnell, M., Hansen, K. and Heldin, C. H. (1999). Overactivation of phospholipase C-gamma1 renders platelet-derived growth factor beta-receptor-expressing cells independent of the phosphatidylinositol 3-kinase pathway for chemotaxis. J. Biol. Chem. 274, 22089-22094.
38. Sahai, E. and Marshall, C. J. (2003). Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell. Biol. 5, 711-719.
39. Smith, M. R., Liu, Y. L., Matthews, N. T., Rhee, S. G., Sung, W. K. and Kung, H. F. (1994). Phospholipase C-gamma 1 can induce DNA synthesis by a mechanism independent of its lipase activity. Proc. Natl. Acad. Sci. USA 91, 6554-6558.
40. Thomas, S. M., Coppelli, F. M., Wells, A., Gooding, W. E., Song, J., Kassis, J., Drenning, S. D. and Grandis, J. R. (2003). Epidermal growth factor receptor-stimulated activation of phospholipase Cgamma-1 promotes invasion of head and neck squamous cell carcinoma. Cancer Res. 63, 5629-5635.
41. Turner, T., Epps-Fung, M. V., Kassis, J. and Wells, A. (1997). Molecular inhibition of phospholipase cgamma signaling abrogates DU-145 prostate tumor cell invasion. Clin. Cancer Res. 3, 2275-2282.
42. Wells, A. (2000). Tumor invasion: role of growth factor-induced cell motility. Adv. Cancer Res. 78, 31-101.
43. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Brocker, E. B. and Friedl, P. (2003). Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160, 267-277.
44. Wonerow, P., Pearce, A. C., Vaux, D. J. and Watson, S. P. (2003). A critical role for phospholipase Cγ2 in αIIbβ3-mediated platelet spreading. J. Biol. Chem. 278, 37520-37529.
45. Ye, K., Aghdasi, B., Luo, H. R., Moriarity, J. L., Wu, F. Y., Hong, J. J., Hurt, K. J. B. S., Suh, P. G. and Snyder, S. H. (2002). Phospholipase C gamma 1 is a physiological guanine nucleotide exchange factor for the nuclear GTPase PIKE. Nature 415, 541-544.
46. Zachary, I. (2003). VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem. Soc. Trans. 31, 1171-1177.
47. Zhang, X., Chattopadhyay, A., Ji, Q. S., Owen, J. D., Ruest, P. J., Carpenter, G. and Hanks, S. K. (1999). Focal adhesion kinase promotes phospholipase C-gamma1 activity. Proc. Natl. Acad Sci. USA 96, 9021-9026.
48. Zhao, Z. S., Manser, E., Loo, T. H. and Lim, L. (2000). Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol. Cell. Biol. 20, 6354-6363.