Vascular smooth muscle cell motility is mediated by a physical and functional interaction of Ca2+/calmodulin-dependent protein kinase IIδ2 and fyn

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29703-29712

  Ginnan, Roman ^a   Zou, Xiaojing ^a,b   Pfleiderer, Paul J ^c   Mercure, Melissa Z ^d   Barroso, Margarida ^a   Singer, Harold A ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c CAHG   (United States)

^d VIRGINIA TECH CARILION SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFOCAL IMMUNOFLUORESCENCE; CONSTITUTIVELY ACTIVES; FUNCTIONAL INTERACTION; PERIPHERAL MEMBRANES; PHARMACOLOGICAL INHIBITORS; PHYSICAL INTERACTIONS; VASCULAR SMOOTH MUSCLE CELLS; VASCULAR SMOOTH MUSCLES;

AMINO ACIDS; CALCIUM; CALMODULIN; CELLS; CYTOLOGY;

ENZYMES;

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II DELTA2; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE FYN; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; GOLGI COMPLEX; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; THORACIC AORTA; VASCULAR SMOOTH MUSCLE;

CALCIUM SIGNALING; CALCIUM/CALMODULIN-DEPENDENT PROTEIN KINASE (CAMK); CELL MIGRATION; PROTEIN COMPLEXES; PROTEIN KINASES; VASCULAR SMOOTH MUSCLE CELLS;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL MOVEMENT; CELLS, CULTURED; IMMUNOBLOTTING; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-FYN; PYRIMIDINES; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SRC-FAMILY KINASES;

EID: 84885665881     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.477257     Document Type: Article

References (48)

1. House, S. J., and Singer, H. A. (2008) CaMKII-δ isoform regulation of neointima formation after vascular injury. Arterioscler. Thromb. Vasc. Biol. 28, 441-447
2. Traver, D., and Zon, L. I. (2002) Walking the walk: migration and other common themes in blood and vascular development. Cell 108, 731-734
3. Rosenfeldt, H. M., Hobson, J. P., Milstien, S., and Spiegel, S. (2001) The sphingosine-1-phosphate receptor EDG-1 is essential for platelet-derived growth factor-induced cell motility. Biochem. Soc. Trans. 29, 836-839
4. Mercure, M. Z., Ginnan, R., and Singer, H. A. (2008) CaM kinase II δ2-dependent regulation of vascular smooth muscle cell polarization and migration. Am. J. Physiol. Cell Physiol. 294, C1465-C1475
5. Gerthoffer, W. T. (2007) Mechanisms of vascular smooth muscle cell migration. Circ. Res. 100, 607-621
6. Taniyama, Y., Weber, D. S., Rocic, P., Hilenski, L., Akers, M. L., Park, J., Hemmings, B. A., Alexander, R. W., and Griendling, K. K. (2003) Pyk2- and Src-dependent tyrosine phosphorylation of PDK1 regulates focal adhesions. Mol. Cell. Biol. 23, 8019-8029
7. Li, W., Li, H., Sanders, P. N., Mohler, P. J., Backs, J., Olson, E. N., Anderson, M. E., and Grumbach, I. M. (2011) The multifunctional Ca2+/calmodulindependent kinase IIδ (CaMKIIδ) controls neointima formation after carotid ligation and vascular smooth muscle cell proliferation through cell cycle regulation by p21. J. Biol. Chem. 286, 7990-7999
8. Bilato, C., Pauly, R. R., Melillo, G., Monticone, R., Gorelick-Feldman, D., Gluzband, Y. A., Sollott, S. J., Ziman, B., Lakatta, E. G., and Crow, M. T. (1995) Intracellular signaling pathways required for rat vascular smooth muscle cell migration. Interactions between basic fibroblast growth factor and platelet-derived growth factor. J. Clin. Invest. 96, 1905-1915
9. Lu, K. K., Armstrong, S. E., Ginnan, R., and Singer, H. A. (2005) Adhesiondependent activation of CaMKII and regulation of ERK activation in vascular smooth muscle. Am. J. Physiol. Cell Physiol. 289, C1343-C1350
10. Scott, J. A., Xie, L., Li, H., Li, W., He, J. B., Sanders, P. N., Carter, A. B., Backs, J., Anderson, M. E., and Grumbach, I. M. (2012) The multifunctional Ca2+/calmodulin-dependent kinase II regulates vascular smooth muscle migration through matrix metalloproteinase 9. Am. J. Physiol. Heart Circ. Physiol. 302, H1953-H1964
11. Easley, C. A., 4th, Brown, C. M., Horwitz, A. F., and Tombes, R. M. (2008) CaMK-II promotes focal adhesion turnover and cell motility by inducing tyrosine dephosphorylation of FAK and paxillin. Cell Motil. Cytoskeleton 65, 662-674
12. Blystone, S. D., Slater, S. E., Williams, M. P., Crow, M. T., and Brown, E. J. (1999) A molecular mechanism of integrin crosstalk: αvβ3 suppression of calcium/calmodulin-dependent protein kinase II regulates α5β1 function. J. Cell Biol. 145, 889-897
13. Bilato, C., Curto, K. A., Monticone, R. E., Pauly, R. R., White, A. J., and Crow, M. T. (1997) The inhibition of vascular smooth muscle cell migration by peptide and antibody antagonists of the αvβ3 integrin complex is reversed by activated calcium/calmodulin-dependent protein kinase II. J. Clin. Invest. 100, 693-704
14. 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
15. Govindarajan, G., Eble, D. M., Lucchesi, P. A., and Samarel, A. M. (2000) Focal adhesion kinase is involved in angiotensin II-mediated protein synthesis in cultured vascular smooth muscle cells. Circ. Res. 87, 710-716
16. Yeo, M. G., Oh, H. J., Cho, H. S., Chun, J. S., Marcantonio, E. E., and Song, W. K. (2011) Phosphorylation of Ser 21 in Fyn regulates its kinase activity, focal adhesion targeting, and is required for cell migration. J. Cell. Physiol. 226, 236-247
17. McMullen, M., Keller, R., Sussman, M., and Pumiglia, K. (2004) Vascular endothelial growth factor-mediated activation of p38 is dependent upon Src and RAFTK/Pyk2. Oncogene 23, 1275-1282
18. Sieg, D. J., Hauck, C. R., Ilic, D., Klingbeil, C. K., Schaefer, E., Damsky, C. H., and Schlaepfer, D. D. (2000) FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2, 249-256
19. Saito, Y., Haendeler, J., Hojo, Y., Yamamoto, K., and Berk, B. C. (2001) Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol. Cell. Biol. 21, 6387-6394
20. Eguchi, S., Iwasaki, H., Inagami, T., Numaguchi, K., Yamakawa, T., Motley, E. D., Owada, K. M., Marumo, F., and Hirata, Y. (1999) Involvement of PYK2 in angiotensin II signaling of vascular smooth muscle cells. Hypertension 33, 201-206
21. Ginnan, R., and Singer, H. A. (2002) CaM kinase II-dependent activation of tyrosine kinases and ERK1/2 in vascular smooth muscle. Am. J. Physiol. Cell Physiol. 282, C754-C761
22. Ginnan, R., Pfleiderer, P. J., Pumiglia, K., and Singer, H. A. (2004) PKC-delta and CaMKII-delta 2 mediate ATP-dependent activation of ERK1/2 in vascular smooth muscle. Am. J. Physiol. Cell Physiol. 286, C1281-C1289
23. Schworer, C. M., Rothblum, L. I., Thekkumkara, T. J., and Singer, H. A. (1993) Identification of novel isoforms of the δ subunit of Ca2+/calmodulin- dependent protein kinase II. Differential expression in rat brain and aorta. J. Biol. Chem. 268, 14443-14449
24. Geisterfer, A. A., Peach, M. J., and Owens, G. K. (1988) Angiotensin II induces hypertrophy, not hyperplasia, of cultured rat aortic smooth muscle cells. Circ. Res. 62, 749-756
25. Abraham, S. T., Benscoter, H., Schworer, C. M., and Singer, H. A. (1996) In situ Ca2+ dependence for activation of Ca2+/calmodulin-dependent protein kinase II in vascular smooth muscle cells. J. Biol. Chem. 271, 2506-2513
26. Hanke, J. H., Gardner, J. P., Dow, R. L., Changelian, P. S., Brissette, W. H., Weringer, E. J., Pollok, B. A., and Connelly, P. A. (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701
27. Blake, R. A., Broome, M. A., Liu, X., Wu, J., Gishizky, M., Sun, L., and Courtneidge, S. A. (2000) SU6656, a selective Src family kinase inhibitor, used to probe growth factor signaling. Mol. Cell. Biol. 20, 9018-9027
28. Lavoie, J. N., Landry, M. C., Faure, R. L., and Champagne, C. (2010) Srcfamily kinase signaling, actin-mediated membrane trafficking and organellar dynamics in the control of cell fate: lessons to be learned from the adenovirus E4orf4 death factor. Cell. Signal. 22, 1604-1614
29. Bodrikov, V., Sytnyk, V., Leshchyns'ka, I., den Hertog, J., and Schachner, M. (2008) NCAM induces CaMKIIα-mediated RPTPα phosphorylation to enhance its catalytic activity and neurite outgrowth. J. Cell Biol. 182, 1185-1200
30. Mariotti, A., Kedeshian, P. A., Dans, M., Curatola, A. M., Gagnoux-Palacios, L., and Giancotti, F. G. (2001) EGF-R signaling through Fyn kinase disrupts the function of integrin α6β4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J. Cell Biol. 155, 447-458
31. Hudmon, A., and Schulman, H. (2002) Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem. J. 364, 593-611
32. Mayer, B. J. (2001) SH3 domains: complexity in moderation. J. Cell Sci. 114, 1253-1263
33. Musacchio, A. (2002) How SH3 domains recognize proline. Adv. Protein Chem. 61, 211-268
34. Wang, Z., Ginnan, R., Abdullaev, I. F., Trebak, M., Vincent, P. A., and Singer, H. A. (2010) Calcium/calmodulin-dependent protein kinase II delta 6 (CaMKIIδ6) and RhoA involvement in thrombin-induced endothelial barrier dysfunction. J. Biol. Chem. 285, 21303-21312
35. Bhandari, V., Lim, K. L., and Pallen, C. J. (1998) Physical and functional interactions between receptor-like protein-tyrosine phosphatase α and p59fyn. J. Biol. Chem. 273, 8691-8698
36. Vacaresse, N., Møller, B., Danielsen, E. M., Okada, M., and Sap, J. (2008) Activation of c-Src and Fyn kinases by protein-tyrosine phosphatase RPTPα is substrate-specific and compatible with lipid raft localization. J. Biol. Chem. 283, 35815-35824
37. Andoniou, C. E., Lill, N. L., Thien, C. B., Lupher, M. L., Jr., Ota, S., Bowtell, D. D., Scaife, R. M., Langdon, W. Y., and Band, H. (2000) The Cbl protooncogene product negatively regulates the Src-family tyrosine kinase Fyn by enhancing its degradation. Mol. Cell. Biol. 20, 851-867
38. Kaabeche, K., Lemonnier, J., Le Mée, S., Caverzasio, J., and Marie, P. J. (2004) Cbl-mediated degradation of Lyn and Fyn induced by constitutive fibroblast growth factor receptor-2 activation supports osteoblast differentiation. J. Biol. Chem. 279, 36259-36267
39. Baillat, G., Siret, C., Delamarre, E., and Luis, J. (2008) Early adhesion induces interaction of FAK and Fyn in lipid domains and activates raft-dependent Akt signaling in SW480 colon cancer cells. Biochim. Biophys. Acta 1783, 2323-2331
40. Lauffenburger, D. A., and Horwitz, A. F. (1996) Cell migration: a physically integrated molecular process. Cell 84, 359-369
41. Bard, F., Mazelin, L., Péchoux-Longin, C., Malhotra, V., and Jurdic, P. (2003) Src regulates Golgi structure and KDEL receptor-dependent retrograde transport to the endoplasmic reticulum. J. Biol. Chem. 278, 46601-46606
42. Sato, I., Obata, Y., Kasahara, K., Nakayama, Y., Fukumoto, Y., Yamasaki, T., Yokoyama, K. K., Saito, T., and Yamaguchi, N. (2009) Differential trafficking of Src, Lyn, Yes and Fyn is specified by the state of palmitoylation in the SH4 domain. J. Cell Sci. 122, 965-975
43. Lippincott-Schwartz, J., Roberts, T. H., and Hirschberg, K. (2000) Secretory protein trafficking and organelle dynamics in living cells. Annu. Rev. Cell Dev. Biol. 16, 557-589
44. Bodrikov, V., Leshchyns'ka, I., Sytnyk, V., Overvoorde, J., den Hertog, J., and Schachner, M. (2005) RPTPα is essential for NCAM-mediated p59fyn activation and neurite elongation. J. Cell Biol. 168, 127-139
45. Gosens, R., Stelmack, G. L., Dueck, G., McNeill, K. D., Yamasaki, A., Gerthoffer, W. T., Unruh, H., Gounni, A. S., Zaagsma, J., and Halayko, A. J. (2006) Role of caveolin-1 in p42/p44 MAP kinase activation and proliferation of human airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L523-L534
46. McGinnis, L. K., Carroll, D. J., and Kinsey, W. H. (2011) Protein tyrosine kinase signaling during oocyte maturation and fertilization. Mol. Reprod. Dev. 78, 831-845
47. Yoo, S. K., Freisinger, C. M., LeBert, D. C., and Huttenlocher, A. (2012) Early redox, Src family kinase, and calcium signaling integrate wound responses and tissue regeneration in zebrafish. J. Cell Biol. 199, 225-234
48. Hoefen, R. J., and Berk, B. C. (2006) The multifunctional GIT family of proteins. J. Cell Sci. 119, 1469-1475