Type I phosphatidylinositol phosphate kinase beta regulates focal adhesion disassembly by promoting β1 integrin endocytosis

Molecular and Cellular Biology

Volumn 30, Issue 18, 2010, Pages 4463-4479

  Chao, Wei Ting ^a   Ashcroft, Felicity ^a   Daquinag, Alexes C ^a,b   Vadakkan, Tegy ^a   Wei, Zhubo ^a   Zhang, Pumin ^a   Dickinson, Mary E ^a   Kunz, Jeannette ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CLATHRIN; DYNAMIN II; FOCAL ADHESION KINASE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL PHOSPHATE KINASE BETA TYPE I; UNCLASSIFIED DRUG; 1-PHOSPHATIDYLINOSITOL-4-PHOSPHATE 5-KINASE; CYTOSKELETON PROTEIN; DAB2 PROTEIN, HUMAN; GLYCOPROTEIN; HYBRID PROTEIN; ISOENZYME; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOTRANSFERASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; ZYX PROTEIN, HUMAN; ZYXIN;

ARTICLE; CELL MIGRATION; CELL SPREADING; COMPLEX FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; FOCAL ADHESION; GENE DELETION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; RNA INTERFERENCE; ANIMAL; CELL ADHESION; CELL LINE; CELL MOTION; GENETICS; METABOLISM; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELL LINE; CELL MOVEMENT; CLATHRIN; CYTOSKELETAL PROTEINS; DYNAMIN II; ENDOCYTOSIS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GLYCOPROTEINS; HUMANS; ISOENZYMES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TUMOR SUPPRESSOR PROTEINS; ZYXIN;

EID: 77956661153     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01207-09     Document Type: Article

References (58)

1. Achiriloaie, M., B. Barylko, and J. P. Albanesi. 1999. Essential role of the dynamin pleckstrin homology domain in receptor-mediated endocytosis. Mol. Cell. Biol. 19:1410-1415.
2. Barylko, B., D. Binns, K. M. Lin, M. A. Atkinson, D. M. Jameson, H. L. Yin, and J. P. Albanesi. 1998. Synergistic activation of dynamin GTPase by Grb2 and phosphoinositides. J. Biol. Chem. 273:3791-3797.
3. Bethoney, K. A., M. C. King, J. E. Hinshaw, E. M. Ostap, and M. A. Lemmon. 2009. A possible effector role for the pleckstrin homology (PH) domain of dynamin. Proc. Natl. Acad. Sci. U. S. A. 106:13359-13364.
4. Bhatt, A., I. Kaverina, C. Otey, and A. Huttenlocher. 2002. Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J. Cell Sci. 115:3415-3425. (Pubitemid 34994031)
5. Bretscher, M. S. 1989. Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J. 8:1341-1348. (Pubitemid 19274358)
6. Bretscher, M. S. 1996. Getting membrane flow and the cytoskeleton to cooperate in moving cells. Cell 87:601-606.
7. Bretscher, M. S. 1996. Moving membrane up to the front of migrating cells. Cell 85:465-467.
8. Bretscher, M. S., and C. Aguado-Velasco. 1998. Membrane traffic during cell locomotion. Curr. Opin. Cell Biol. 10:537-541.
9. Broussard, J. A., D. J. Webb, and I. Kaverina. 2008. Asymmetric focal adhesion disassembly in motile cells. Curr. Opin. Cell Biol. 20:85-90.
10. Burridge, K., S. K. Sastry, and J. L. Sallee. 2006. Regulation of cell adhesion by protein-tyrosine phosphatases. I. Cell-matrix adhesion. J. Biol. Chem. 281:15593-15596.
11. Caswell, P. T., M. Chan, A. J. Lindsay, M. W. McCaffrey, D. Boettiger, and J. C. Norman. 2008. Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J. Cell Biol. 183:143-155.
12. Caswell, P. T., H. J. Spence, M. Parsons, D. P. White, K. Clark, K. W. Cheng, G. B. Mills, M. J. Humphries, A. J. Messent, K. I. Anderson, M. W. McCaffrey, B. W. Ozanne, and J. C. Norman. 2007. Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell 13:496-510.
13. Chandrasekar, I., T. E. Stradal, M. R. Holt, F. Entschladen, B. M. Jockusch, and W. H. Ziegler. 2005. Vinculin acts as a sensor in lipid regulation of adhesion-site turnover. J. Cell Sci. 118:1461-1472.
14. Chao, W. T., and J. Kunz. 2009. Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett. 583:1337-1343.
15. Chavrier, P., R. G. Parton, H. P. Hauri, K. Simons, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317-329. (Pubitemid 20233538)
16. Coppolino, M. G., R. Dierckman, J. Loijens, R. F. Collins, M. Pouladi, J. Jongstra-Bilen, A. D. Schreiber, W. S. Trimble, R. Anderson, and S. Grinstein. 2002. Inhibition of phosphatidylinositol-4-phosphate 5-kinase Ialpha impairs localized actin remodeling and suppresses phagocytosis. J. Biol. Chem. 277:43849-43857.
17. Di Paolo, G., and P. De Camilli. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651-657. (Pubitemid 44564702)
18. Di Paolo, G., L. Pellegrini, K. Letinic, G. Cestra, R. Zoncu, S. Voronov, S. Chang, J. Guo, M. R. Wenk, and P. De Camilli. 2002. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature 420:85-89.
19. Doughman, R. L., A. D. Firestone, M. W. Wojtasiak, and R. A. Anderson. 2003. Membrane ruffling requires coordination between type Iα phosphatidylinositol phosphate kinase and Rac signaling. J. Biol. Chem. 278:23036-23045.
20. Ezratty, E. J., C. Bertaux, E. E. Marcantonio, and G. G. Gundersen. 2009. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J. Cell Biol. 187:733-747.
21. Ezratty, E. J., M. A. Partridge, and G. G. Gundersen. 2005. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7:581-590.
22. Franco, S. J., M. A. Rodgers, B. J. Perrin, J. Han, D. A. Bennin, D. R. Critchley, and A. Huttenlocher. 2004. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell Biol. 6:977-983.
23. Gilmore, A. P., and K. Burridge. 1996. Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature 381:531-535.
24. Hauck, C. R., D. A. Hsia, and D. D. Schlaepfer. 2002. The focal adhesion kinase - a regulator of cell migration and invasion. IUBMB Life 53:115-119.
25. Haucke, V. 2005. Phosphoinositide regulation of clathrin-mediated endocytosis. Biochem. Soc. Trans. 33:1285-1289.
26. Ilić, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, and T. Yamamoto. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
27. Ishihara, H., Y. Shibasaki, N. Kizuki, H. Katagiri, Y. Yazaki, T. Asano, and Y. Oka. 1996. Cloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase. J. Biol. Chem. 271:23611-23614.
28. Ishihara, H., Y. Shibasaki, N. Kizuki, T. Wada, Y. Yazaki, T. Asano, and Y. Oka. 1998. Type I phosphatidylinositol-4-phosphate 5-kinases. Cloning of the third isoform and deletion/substitution analysis of members of this novel lipid kinase family. J. Biol. Chem. 273:8741-8748.
29. Jović, M., N. Naslavsky, D. Rapaport, M. Horowitz, and S. Caplan. 2007. EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J. Cell Sci. 120:802-814. (Pubitemid 46523482)
30. Kaverina, I., O. Krylyshkina, and J. V. Small. 2002. Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34:746-761.
31. Klein, D. E., A. Lee, D. W. Frank, M. S. Marks, and M. A. Lemmon. 1998. The pleckstrin homology domains of dynamin isoforms require oligomerization for high affinity phosphoinositide binding. J. Biol. Chem. 273:27725-27733.
32. Kunz, J., M. P. Wilson, M. Kisseleva, J. H. Hurley, P. W. Majerus, and R. A. Anderson. 2000. The activation loop of phosphatidylinositol phosphate kinases determines signaling specificity. Mol. Cell 5:1-11.
33. Lacalle, R. A., R. M. Peregil, J. P. Albar, E. Merino, A. C. Martinez, I. Merida, and S. Manes. 2007. Type I phosphatidylinositol 4-phosphate 5-kinase controls neutrophil polarity and directional movement. J. Cell Biol. 179:1539-1553.
34. Laukaitis, C. M., D. J. Webb, K. Donais, and A. F. Horwitz. 2001. Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153:1427-1440.
35. Lee, S. Y., S. Voronov, K. Letinic, A. C. Nairn, G. Di Paolo, and P. De Camilli. 2005. Regulation of the interaction between PIPKI gamma and talin by proline-directed protein kinases. J. Cell Biol. 168:789-799.
36. Lin, H. C., B. Barylko, M. Achiriloaie, and J. P. Albanesi. 1997. Phosphatidylinositol (4,5)-bisphosphate-dependent activation of dynamins I and II lacking the proline/arginine-rich domains. J. Biol. Chem. 272:25999-26004.
37. Ling, K., R. L. Doughman, A. J. Firestone, M. W. Bunce, and R. A. Anderson. 2002. Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420:89-93.
38. Ling, K., N. J. Schill, M. P. Wagoner, Y. Sun, and R. A. Anderson. 2006. Movin' on up: the role of PtdIns(4,5)P(2) in cell migration. Trends Cell Biol. 16:276-284.
39. Loijens, J. C., and R. A. Anderson. 1996. Type I phosphatidylinositol-4- phosphate 5-kinases are distinct members of this novel lipid kinase family. J. Biol. Chem. 271:32937-32943.
40. McNamee, H. P., H. G. Liley, and D. E. Ingber. 1996. Integrin-dependent control of inositol lipid synthesis in vascular endothelial cells and smooth muscle cells. Exp. Cell Res. 224:116-122.
41. Nishimura, T., and K. Kaibuchi. 2007. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13:15-28. (Pubitemid 46972036)
42. Prigozhina, N. L., and C. M. Waterman-Storer. 2006. Decreased polarity and increased random motility in PtK1 epithelial cells correlate with inhibition of endosomal recycling. J. Cell Sci. 119:3571-3582.
43. Ramachandran, R., and S. L. Schmid. 2008. Real-time detection reveals that effectors couple dynamin's GTP-dependent conformational changes to the membrane. EMBO J. 27:27-37.
44. Ren, X. D., and M. A. Schwartz. 2000. Determination of GTP loading on Rho. Methods Enzymol. 325:264-272.
45. Roberts, M., S. Barry, A. Woods, P. van der Sluijs, and J. Norman. 2001. PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11:1392-1402.
46. Saunders, R. M., M. R. Holt, L. Jennings, D. H. Sutton, I. L. Barsukov, A. Bobkov, R. C. Liddington, E. A. Adamson, G. A. Dunn, and D. R. Critchley. 2006. Role of vinculin in regulating focal adhesion turnover. Eur. J. Cell Biol. 85:487-500.
47. Sechi, A. S., and J. Wehland. 2000. The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci. 113:3685-3695.
48. Sever, S., H. Damke, and S. L. Schmid. 2000. Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J. Cell Biol. 150:1137-1148.
49. 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.
50. Sottile, J., D. C. Hocking, and P. J. Swiatek. 1998. Fibronectin matrix assembly enhances adhesion-dependent cell growth. J. Cell Sci. 111:2933-2943.
51. Takenawa, T., and T. Itoh. 2001. Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim. Biophys. Acta 1533:190-206.
52. Valdembri, D., P. T. Caswell, K. I. Anderson, J. P. Schwarz, I. Konig, E. Astanina, F. Caccavari, J. C. Norman, M. J. Humphries, F. Bussolino, and G. Serini. 2009. Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol. 7:e25.
53. Vallis, Y., P. Wigge, B. Marks, P. R. Evans, and H. T. McMahon. 1999. Importance of the pleckstrin homology domain of dynamin in clathrinmediated endocytosis. Curr. Biol. 9:257-260.
54. Volberg, T., B. Geiger, Z. Kam, R. Pankov, I. Simcha, H. Sabanay, J. L. Coll, E. Adamson, and A. Ben-Ze'ev. 1995. Focal adhesion formation by F9 embryonal carcinoma cells after vinculin gene disruption. J. Cell Sci. 108:2253-2260.
55. Webb, D. J., K. Donais, L. A. Whitmore, S. M. Thomas, C. E. Turner, J. T. Parsons, and A. F. Horwitz. 2004. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6:154-161.
56. Webb, D. J., J. T. Parsons, and A. F. Horwitz. 2002. Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell Biol. 4:E97-E100.
57. Yin, H. L., and P. A. Janmey. 2003. Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65:761-789.
58. Zoncu, R., R. M. Perera, R. Sebastian, F. Nakatsu, H. Chen, T. Balla, G. Ayala, D. Toomre, and P. V. De Camilli. 2007. Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc. Natl. Acad. Sci. U. S. A. 104:3793-3798.