CaMK-II promotes focal adhesion turnover and cell motility by inducing tyrosine dephosphorylation of FAK and paxillin

Cell Motility and the Cytoskeleton

Volumn 65, Issue 8, 2008, Pages 662-674

  Easley IV, Charles A ^a   Brown, Claire M ^b,c   Horwitz, Alan F ^b   Tombes, Robert M ^a,d  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d NONE   (United States)

Author keywords

Calmodulin; CaM kinase II; Fibroblast; Fibronectin; TIRF

Indexed keywords

CALCIUM ION; FIBRONECTIN; FOCAL ADHESION KINASE; MYRISTOLYATED AUTOCAMTIDE 2 INHIBITORY PEPTIDE; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; PAXILLIN; PROTEIN INHIBITOR; PROTEIN KINASE (CALCIUM,CALMODULIN) II; TYROSINE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL METABOLISM; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; FIBROBLAST; FOCAL ADHESION; LAMELLIPODIUM; MICROSCOPY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION;

ANIMALS; BENZYLAMINES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CELL MOVEMENT; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; IMMUNOBLOTTING; MICE; MICROSCOPY, FLUORESCENCE; NIH 3T3 CELLS; PAXILLIN; PHOSPHOPROTEINS; PROTEIN KINASE INHIBITORS; SULFONAMIDES; TYROSINE;

EID: 46749113528     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20294     Document Type: Article

References (69)

1. Bellis SL, Miller JT, Turner CE. 1995. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J Biol Chem 270(29):17437-17441.
2. Bilato C, Curto KA, Monticone RE, Pauly RR, White AJ, Crow MT. 1997. The inhibition of vascular smooth muscle cell migration by peptide and antibody antagonists of the alphavbeta3 integrin complex is reversed by activated calcium/calmodulin- dependent protein kinase II. J Clin Invest 100(3):693-704.
3. Blystone SD, Slater SE, Williams MP, Crow MT, Brown EJ. 1999. A molecular mechanism of integrin crosstalk: Alphavbeta3 suppression of calcium/calmodulin-dependent protein kinase II regulates alpha5beta1 function. J Cell Biol 145(4):889-897.
4. Bouvard D, Block MR. 1998. Calcium/calmodulin-dependent protein kinase II controls integrin alpha5beta1-mediated cell adhesion through the integrin cytoplasmic domain associated protein-1alpha. Biochem Biophys Res Commun 252(1)46-50.
5. Bouvard D, Molla A, Block MR. 1998. Calcium/calmodulin-dependent protein kinase II controls alpha5beta1 integrin-mediated inside-out signaling. J Cell Sci 111 (Partt 5):657-665.
6. Bouvard D, Vignoud L, Dupe-Manet S, Abed N, Fournier HN, Vincent-Monegat C, Retta SF, Fassler R, Block MR. 2003. Disruption of focal adhesions by integrin cytoplasmic domain-associated protein-1 alpha. J Biol Chem 278(8):6567-6574.
7. Brown CM, Hebert B, Kolin DL, Zareno J, Whitmore L, Horwitz AR, Wiseman PW. 2006. Probing the integrin-actin linkage using high-resolution protein velocity mapping. J Cell Sci 119(Part 24):5204-5214.
8. Caran N, Johnson LD, Jenkins KJ, Tombes RM. 2001. Cytosolic targeting domains of gamma and delta calmodulin-dependent protein kinase II. J Biol Chem 276(45)42514-42519.
9. Cary LA, Han DC, Polte TR, Hanks SK, Guan JL. 1998. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol 140(1):211-221.
10. Conklin MW, Lin MS, Spitzer NC. 2005. Local calcium transients contribute to disappearance of pFAK, focal complex removal and deadhesion of neuronal growth cones and fibroblasts. Dev Biol 287(1):201-212.
11. Crawford BD, Henry CA, Clason TA, Becker AL, Hille MB. 2003. Activity and distribution of paxillin, focal adhesion kinase, and Cadherin indicate cooperative roles during zebrafish morphogenesis. Mol Biol Cell 14(8):3065-3081.
12. Easley CA, Faison MO, Kirsch TL, Lee JA, Seward ME, Tombes RM. 2006. Laminin activates CaMK-II to stabilize nascent embryonic axons. Brain Res 1092(1):59-68.
13. 2+/calmodulin-dependent protein kinase II in developing P19 neurons. Int J Dev Neurosci 20(8):585-592.
14. 2+/calmodulin-dependent kinase II. J Biol Chem 280(25):24212-24220.
15. Fink CC, Bayer KU, Myers JW, Ferrell JE Jr., Schulman H, Meyer T. 2003. Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron 39(2):283-297.
16. 2+/calmodulin-dependent protein kinase II regulates Tiam1 by reversible protein phosphorylation. J Biol Chem 274(18):12753-12758.
17. Franco SJ, Rodgers MA, Perrin BJ, Han J, Bennin DA, Critchley DR, Huttenlocher A. 2004. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat Cell Biol 6(10):977-983.
18. Giannone G, Ronde P, Gaire M, Haiech J, Takeda K. 2002. Calcium oscillations trigger focal adhesion disassembly in human U87 astrocytoma cells. J Biol Chem 277(29):26364-26371.
19. Giannone G, Ronde P, Gaire M, Beaudouin J, Haiech J, Ellenberg J, Takeda K. 2004. Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J Biol Chem 279(27):28715-28723.
20. Hagel M, George EL, Kim A, Tamimi R, Opitz SL, Turner CE, Imamoto A, Thomas SM. 2002. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol Cell Biol 22(3):901-915.
21. Hamelers IH, Olivo C, Mertens AE, Pegtel DM, van der Kammen RA, Sonnenberg A, Collard JG. 2005. The Rac activator Tiam1 is required for (alpha)3(beta)1-mediated laminin-5 deposition, cell spreading, and cell migration. J Cell Biol 171(5):871-881.
22. Henry CA, Crawford BD, Yan YL, Postlethwait J, Cooper MS, Hille MB. 2001. Roles for zebrafish focal adhesion kinase in notochord and somite morphogenesis. Dev Biol 240(2)474-487.
23. Hidaka H, Ishikawa T. 1992. Molecular pharmacology of calmodulin pathways in the cell functions. Cell Calcium 13(6-7)465-472.
24. Huttenlocher A, Sandborg RR, Horwitz AF. 1995. Adhesion in cell migration. Curr Opin Cell Biol 7(5):697-706.
25. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377(6549):539-544.
26. Illario M, Cavallo AL, Monaco S, Di Vito E, Mueller F, Marzano LA, Troncone G, Fenzi G, Rossi G, Vitale M. 2005. Fibronectin-induced proliferation in thyroid cells is mediated by alphavbeta3 integrin through Ras/Raf-1/MEK/ERK and calcium/CaMKII signals. J Clin Endocrinol Metab 90(5):2865-2873.
27. Inagaki K, Noguchi T, Matozaki T, Horikawa T, Fukunaga K, Tsuda M, Ichihashi M, Kasuga M. 2000. Roles for the protein tyrosine phosphatase SHP-2 in cytoskeletal organization, cell adhesion and cell migration revealed by overexpression of a dominant negative mutant. Oncogene 19(1):75-84.
28. Johnson LD, Willoughby CA, Burke SH, Paik DS, Jenkins KJ, Tombes RM. 2000. Delta Ca(2+)/calmodulin-dependent protein kinase II isozyme-specific induction of neunte outgrowth in P19 embryonal carcinoma cells. J Neurochem 75(6):2380-2391.
29. Kerr BA, Otani T, Koyama E, Freeman TA, Enomoto-Iwamoto M. 2008. Small GTPase protein Rac-1 is activated with maturation and regulates cell morphology and function in chondrocytes. Exp Cell Res 314(6):1301-1312.
30. Kohn AD, Moon RT. 2005. Wnt and calcium signaling: Beta-catenin- independent pathways. Cell Calcium 38(3-4):439-446.
31. 2+ pathway: A new vertebrate Wnt signaling pathway takes shape. Trends Genet 16(7):279-283.
32. Laabich A, Cooper NG. 2000. Neuroprotective effect of AIP on N-methyl-D-aspartate-induced cell death in retinal neurons. Brain Res Mol Brain Res 85(1-2):32-40.
33. Lantsman K, Tombes RM. 2005. CaMK-II oligomerization potential determined using CFP/YFP FRET. Biochim Biophys Acta 1746(1)45-54.
34. Lauffenburger DA, Horwitz AF. 1996. Cell migration: A physically integrated molecular process. Cell 84(3):359-369.
35. Lee SY, Voronov S, Letinic K, Nairn AC, Di Paolo G, De Camilli P. 2005. Regulation of the interaction between PIPKI gamma and talin by proline-directed protein kinases. J Cell Biol 168(5):789-799.
36. Lin YH, Park ZY, Lin D, Brahmbhatt AA, Rio MC, Yates JR III, Klemke RL. 2004. Regulation of cell migration and survival by focal adhesion targeting of Lasp-1. J Cell Biol 165(3)421-432.
37. Lundberg MS, Curto KA, Bilato C, Monticone RE, Crow MT. 1998. Regulation of vascular smooth muscle migration by mitogen-activated protein kinase and calcium/calmodulin-dependent protein kinase II signaling pathways. J Mol Cell Cardiol 30(11):2377-23789.
38. MacGillivray M, Herrera-Abreu MT, Chow CW, Shek C, Wang Q, Vachon E, Feng GS, Siminovitch KA, McCulloch CA, Downey GP. 2003. The protein tyrosine phosphatase SHP-2 regulates interleukin-1-induced ERK activation in fibroblasts. J Biol Chem 278(29):27190-27198.
39. Manes S, Mira E, Gomez-Mouton C, Zhao ZJ, Lacalle RA, Martinez AC. 1999. Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol Cell Biol 19(4):3125-3135.
40. Marks PW, Maxfield FR. 1990. Transient increases in cytosolic free calcium appear to be required for the migration of adherent human neutrophils. J Cell Biol 110(1)43-52.
41. 2+/calmodulin-dependent protein kinase II gamma B impairs positive selection of T cells by modulating TCR signaling. J Immunol 175(2):656-664.
42. Mitra SK, Hanson DA, Schlaepfer DD. 2005. Focal adhesion kinase: In command and control of cell motility. Nat Rev Mol Cell Biol 6(1):56-68.
43. Pauly RR, Bilato C, Sollott SJ, Monticone R, Kelly PT, Lakatta EG, Crow MT. 1995. Role of calcium/calmodulin-dependent protein kinase II in the regulation of vascular smooth muscle cell migration. Circulation 91(4):1107-1115.
44. Pfleiderer PJ, Lu KK, Crow MT, Keller RS, Singer HA. 2004. Modulation of vascular smooth muscle cell migration by calcium/calmodulin-dependent protein kinase II-delta 2. Am J Physiol Cell Physiol 286(6):C1238-C1245.
45. Poole AW, Jones ML. 2005. A SHPing tale: Perspectives on the regulation of SHP-1 and SHP-2 tyrosine phosphatases by the C-terminal tail. Cell Signal 17(11):1323-1332.
46. 2+ signaling. Am J Physiol Renal Physiol 287(5):F969-F78.
47. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. 2003. Cell migration: Integrating signals from front to back. Science 302(5651):1704-1709.
48. Saxton TM, Ciruna BG, Holmyard D, Kulkarni S, Harpal K, Rossant J, Pawson T. 2000. The SH2 tyrosine phosphatase shp2 is required for mammalian limb development. Nat Genet 24(4): 420-423.
49. Schaller MD, Parsons JT. 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol Cell Biol 15(5):2635-2645.
50. Schlaepfer DD, Mitra SK, Ilic D. 2004. Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta 1692(2-3):77-102.
51. Shao H, Chou J, Baty CJ, Burke NA, Watkins SC, Stolz DB, Wells A. 2006. Spatial localization of m-calpain to the plasma membrane by phosphoinositide biphosphate binding during epidermal growth factor receptor-mediated activation. Mol Cell Biol 26(14):5481-5496.
52. 2+ flux. PKC, and CaMKII in vertebrate embryos. J Cell Biol 161:769-777.
53. Shen K, Teruel MN, Subramanian K, Meyer T. 1998. CaMKIIbeta functions as an F-actin targeting module that localizes CaM-KIIalpha/beta heterooligomers to dendritic spines. Neuron 21(3):593-606.
54. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, Schlaepfer DD. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2(5):249-256.
55. 2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem Biophys Res Commun 181(3):968-975.
56. Suzuki K, Takahashi K. 2003. Reduced cell adhesion during mitosis by threonine phosphorylation of beta1 integrin. J Cell Physiol 197(2):297-305.
57. Tahinci E, Symes K. 2003. Distinct functions of Rho and Rac are required for convergent extension during Xenopus gastrulation. Dev Biol 259(2):318-335.
58. Takahashi K. 2001. The linkage between beta1 integrin and the actin cytoskeleton is differentially regulated by tyrosine and serine/threonine phosphorylation of beta1 integrin in normal and cancerous human breast cells. BMC Cell Biol 2:23.
59. 2+/CaM kinase). Cell Growth Differ 6(9):1063-1070.
60. Tombes RM, Mikkelsen RB, Jarvis WD, Grant S. 1999. Downregulation of delta CaM kinase II in human tumor cells. Biochim Biophys Acta 1452(1):1-11.
61. Tombes RM, Faison MO, Turbeville JM. 2003. Organization and evolution of multifunctional Ca(2+)/CaM-dependent protein kinase genes. Gene 322:17-31.
62. Tran PO, Hinman LE, Unger GM, Sammak PJ. 1999. A wound-induced [Ca2+]i increase and its transcriptional activation of immediate early genes is important in the regulation of motility. Exp Cell Res 246(2):319-326.
63. Vadlamudi RK, Adam L, Nguyen D, Santos M, Kumar R. 2002. Differential regulation of components of the focal adhesion complex by heregulin: Role of phosphatase SHP-2. J Cell Physiol 190(2):189-199.
64. von Wiehert G, Haimovich B, Feng GS, Sheetz MP. 2003. Force-dependent integrin-cytoskeleton linkage formation requires downregulation of focal complex dynamics by Shp2. EMBO J 22(19):5023-5035.
65. Wang FM, Liu HQ, Liu SR, Tang SP, Yang L, Feng GS. 2005. SHP-2 promoting migration and metastasis of MCF-7 with loss of E-cadherin, dephosphorylation of FAK and secretion of MMP-9 induced by IL-1beta in vivo and in vitro. Breast Cancer Res Treat 89(1):5-14.
66. 2+ signaling. J Biol Chem 281(41):31093-31105.
67. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF. 2004. FAK-Src signalling through paxillin. ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 6(2):154-161.
68. Wennerberg K, Fassler R, Warmegard B, Johansson S. 1998. Mutational analysis of the potential phosphorylation sites in the cytoplasmic domain of integrin beta1A. Requirement for threonines 788-789 in receptor activation. J Cell Sci 111(8):1117-1126.
69. Yu DH, Qu CK, Henegariu O, Lu X, Feng GS. 1998. Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J Biol Chem 273(33):21125-21131.