Interaction of Crk with myosin-1c participates in fibronectin-induced cell spreading

International Journal of Biological Sciences

Volumn 9, Issue 8, 2013, Pages 778-791

  Oh, Hyejin ^a   Kim, Hwan ^a   Shin, Baehyun ^a   Lee, Kun Ho ^b   Yeo, Myeong Gu ^c   Song, Woo Keun ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b Chosun University   (South Korea)

^c Nambu University   (South Korea)

Author keywords

Cell adhesion; Cell spreading; Myosin 1c; v Crk

Indexed keywords

CRK PROTEIN, MOUSE; FIBRONECTIN; MYO1C PROTEIN, MOUSE; MYOSIN I; NEUROPEPTIDE; ONCOPROTEIN; PRIMER DNA; RAC1 PROTEIN; RAC1 PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL; ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL MOTION; CELL SPREADING; FIBROBLAST; GENE SILENCING; GENETICS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; MOUSE; MYOSIN-1C; PHYSIOLOGY; STROBOSCOPY; V-CRK;

CELL ADHESION; CELL SPREADING; MYOSIN-1C; V-CRK;

ANIMALS; CELL ADHESION; CELL MEMBRANE; CELL MOVEMENT; DNA PRIMERS; FIBROBLASTS; FIBRONECTINS; GENE KNOCKDOWN TECHNIQUES; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MYOSIN TYPE I; NEUROPEPTIDES; PROTO-ONCOGENE PROTEINS C-CRK; RAC1 GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; STROBOSCOPY;

EID: 84884225997     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.6459     Document Type: Article

References (52)

1. Ryan G.L., Watanabe N., and Vavylonis D. A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells. Cytoskeleton (Hoboken). 2012; 69: 195-206.
2. Hagel M., George E.L., Kim A., Tamimi R., Opitz S.L., Turner C.E., Imamoto A., and Thomas S.M. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol Cell Biol. 2002; 22: 901-915.
3. Yamazaki D., Fujiwara T., Suetsugu S., and Takenawa T. A novel function of WAVE in lamellipodia: WAVE1 is required for stabilization of lamellipodial protrusions during cell spreading. Genes Cells. 2005; 10: 381-392.
4. Huttenlocher A. and Horwitz A.R. Integrins in cell migration. Cold Spring Harb Perspect Biol. 2011; 3: a005074.
5. Ballestrem C., Erez N., Kirchner J., Kam Z., Bershadsky A., and Geiger B. Molecular mapping of tyrosine-phosphorylated proteins in focal adhesions using fluorescence resonance energy transfer. Journal of Cell Science. 2006; 119: 866-875.
6. Vuori K. Integrin signaling: tyrosine phosphorylation events in focal adhesions. J Membr Biol. 1998; 165: 191-199.
7. Juliano R.L., Reddig P., Alahari S., Edin M., Howe A., and Aplin A. Integrin regulation of cell signalling and motility. Biochem Soc Trans. 2004; 32: 443-446.
8. Mayer B.J., Hamaguchi M., and Hanafusa H. A novel viral oncogene with structural similarity to phospholipase C. Nature. 1988; 332: 272-275.
9. Birge R.B., Fajardo J.E., Mayer B.J., and Hanafusa H. Tyrosine-phosphorylated epidermal growth factor receptor and cellular p130 provide high affinity binding substrates to analyze Crk-phosphotyrosine-dependent interactions in vitro. J Biol Chem. 1992; 267: 10588-10595.
10. Tanaka S., Morishita T., Hashimoto Y., Hattori S., Nakamura S., Shibuya M., Matuoka K., Takenawa T., Kurata T., Nagashima K., et al. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins. Proc Natl Acad Sci U S A. 1994; 91: 3443-3447.
11. Feller S.M., Knudsen B., and Hanafusa H. Cellular proteins binding to the first Src homology 3 (SH3) domain of the proto-oncogene product c-Crk indicate Crk-specific signaling pathways. Oncogene. 1995; 10: 1465-1473.
12. Hasegawa H., Kiyokawa E., Tanaka S., Nagashima K., Gotoh N., Shibuya M., Kurata T., and Matsuda M. DOCK180, a major CRK-binding protein, alters cell morphology upon translocation to the cell membrane. Mol Cell Biol. 1996; 16: 1770-1776.
13. Smit L., van der Horst G., and Borst J. Sos, Vav, and C3G participate in B cell receptor-induced signaling pathways and differentially associate with Shc-Grb2, Crk, and Crk-L adaptors. J Biol Chem. 1996; 271: 8564-8569.
14. Gotoh T., Hattori S., Nakamura S., Kitayama H., Noda M., Takai Y., Kaibuchi K., Matsui H., Hatase O., Takahashi H., et al. Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G. Mol Cell Biol. 1995; 15: 6746-6753.
15. Okino K., Nagai H., Nakayama H., Doi D., Yoneyama K., Konishi H., and Takeshita T. Inactivation of Crk SH3 domain-binding guanine nucleotide-releasing factor (C3G) in cervical squamous cell carcinoma. Int J Gynecol Cancer. 2006; 16: 763-771.
16. Chen H., Wu X., Pan Z.K., and Huang S. Integrity of SOS1/EPS8/ABI1 tri-complex determines ovarian cancer metastasis. Cancer Res. 2010; 70: 9979-9990.
17. Zheng J., Machida K., Antoku S., Ng K.Y., Claffey K.P., and Mayer B.J. Proteins that bind the Src homology 3 domain of CrkI have distinct roles in Crk transformation. Oncogene. 2010; 29: 6378-6389.
18. Kiyokawa E., Hashimoto Y., Kobayashi S., Sugimura H., Kurata T., and Matsuda M. Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 1998; 12: 3331-3336.
19. Kiyokawa E., Hashimoto Y., Kurata T., Sugimura H., and Matsuda M. Evidence that DOCK180 up-regulates signals from the CrkII-p130(Cas) complex. J Biol Chem. 1998; 273: 24479-24484.
20. Mayer B.J. and Hanafusa H. Association of the v-crk oncogene product with phosphotyrosine-containing proteins and protein kinase activity. Proc Natl Acad Sci U S A. 1990; 87: 2638-2642.
21. Dey T., Mann M.C., and Goldmann W.H. Comparing mechano-transduction in fibroblasts deficient of focal adhesion proteins. Biochem Biophys Res Commun. 2011; 413: 541-544.
22. Klemke R.L., Leng J., Molander R., Brooks P.C., Vuori K., and Cheresh D.A. CAS/Crk coupling serves as a molecular switch for induction of cell migration. J Cell Biol. 1998; 140: 961-972.
23. Meenderink L.M., Ryzhova L.M., Donato D.M., Gochberg D.F., Kaverina I., and Hanks S.K. P130Cas Src-binding and substrate domains have distinct roles in sustaining focal adhesion disassembly and promoting cell migration. PLoS One. 2010; 5: e13412.
24. Rodrigues S.P., Fathers K.E., Chan G., Zuo D., Halwani F., Meterissian S., and Park M. CrkI and CrkII function as key signaling integrators for migration and invasion of cancer cells. Mol Cancer Res. 2005; 3: 183-194.
25. Park T.J., Boyd K., and Curran T. Cardiovascular and craniofacial defects in Crk-null mice. Mol Cell Biol. 2006; 26: 6272-6282.
26. Yeo M.G., Sung B.H., Oh H.J., Park Z.Y., Marcantonio E.E., and Song W.K. Focal adhesion targeting of v-Crk is essential for FAK phosphorylation and cell migration in mouse embryo fibroblasts deficient src family kinases or p130CAS. J Cell Physiol. 2008; 214: 604-613.
27. Perry S.V. and Cotterill J. Interaction of actin and myosin. Nature. 1965; 206: 161-163.
28. Huxley H.E. Muscular contraction and cell motility. Nature. 1973; 243: 445-449.
29. Kneussel M. and Wagner W. Myosin motors at neuronal synapses: drivers of membrane transport and actin dynamics. Nat Rev Neurosci. 2013; 14: 233-247.
30. Giannone G., Dubin-Thaler B.J., Rossier O., Cai Y., Chaga O., Jiang G., Beaver W., Dobereiner H.G., Freund Y., Borisy G., and Sheetz M.P. Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell. 2007; 128: 561-575.
31. Terry S.J., Elbediwy A., Zihni C., Harris A.R., Bailly M., Charras G.T., Balda M.S., and Matter K. Stimulation of cortical myosin phosphorylation by p114RhoGEF drives cell migration and tumor cell invasion. PLoS One. 2012; 7: e50188.
32. Cheney R.E. and Mooseker M.S. Unconventional myosins. Curr Opin Cell Biol. 1992; 4: 27-35.
33. Barylko B., Jung G., and Albanesi J.P. Structure, function, and regulation of myosin 1C. Acta Biochim Pol. 2005; 52: 373-380.
34. Diefenbach T.J., Latham V.M., Yimlamai D., Liu C.A., Herman I.M., and Jay D.G. Myosin 1c and myosin IIB serve opposing roles in lamellipodial dynamics of the neuronal growth cone. J Cell Biol. 2002; 158: 1207-1217.
35. Brandstaetter H., Kendrick-Jones J., and Buss F. Myo1c regulates lipid raft recycling to control cell spreading, migration and Salmonella invasion. J Cell Sci. 2012; 125: 1991-2003.
36. Bose A., Guilherme A., Robida S.I., Nicoloro S.M., Zhou Q.L., Jiang Z.Y., Pomerleau D.P., and Czech M.P. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature. 2002; 420: 821-824.
37. Price L.S., Leng J., Schwartz M.A., and Bokoch G.M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol Biol Cell. 1998; 9: 1863-1871.
38. Wells C.M., Walmsley M., Ooi S., Tybulewicz V., and Ridley A.J. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J Cell Sci. 2004; 117: 1259-1268.
39. Sung B.H., Yeo M.G., Oh H.J., and Song W.K. v-Crk induces Rac-dependent membrane ruffling and cell migration in CAS-deficient embryonic fibroblasts. Mol Cells. 2008; 25: 131-137.
40. Wang L., Tabu K., Kimura T., Tsuda M., Linghu H., Tanino M., Kaneko S., Nishihara H., and Tanaka S. Signaling adaptor protein Crk is indispensable for malignant feature of glioblastoma cell line KMG4. Biochem Biophys Res Commun. 2007; 362: 976-981.
41. Birge R., Kalodimos C., Inagaki F., and Tanaka S. Crk and CrkL adaptor proteins: networks for physiological and pathological signaling. Cell Communication and Signaling. 2009; 7: 13.
42. Matsuda M., Mayer B.J., Fukui Y., and Hanafusa H. Binding of transforming protein, P47gag-crk, to a broad range of phosphotyrosine-containing proteins. Science. 1990; 248: 1537-1539.
43. Schaller M.D. and Schaefer E.M. Multiple stimuli induce tyrosine phosphorylation of the Crk-binding sites of paxillin. Biochem J. 2001; 360: 57-66.
44. Stam J.C., Geerts W.J., Versteeg H.H., Verkleij A.J., and van Bergen en Henegouwen P.M. The v-Crk oncogene enhances cell survival and induces activation of protein kinase B/Akt. J Biol Chem. 2001; 276: 25176-25183.
45. Birge R.B., Fajardo J.E., Reichman C., Shoelson S.E., Songyang Z., Cantley L.C., and Hanafusa H. Identification and characterization of a high-affinity interaction between v-Crk and tyrosine-phosphorylated paxillin in CT10-transformed fibroblasts. Mol Cell Biol. 1993; 13: 4648-4656.
46. Schaller M.D. and Parsons J.T. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol Cell Biol. 1995; 15: 2635-2645.
47. Iwahara T., Akagi T., Fujitsuka Y., and Hanafusa H. CrkII regulates focal adhesion kinase activation by making a complex with Crk-associated substrate, p130Cas. Proceedings of the National Academy of Sciences of the United States of America. 2004; 101: 17693-17698.
48. Wagner M.C., Barylko B., and Albanesi J.P. Tissue distribution and subcellular localization of mammalian myosin I. J Cell Biol. 1992; 119: 163-170.
49. Jay D.G. The clutch hypothesis revisited: ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone. J Neurobiol. 2000; 44: 114-125.
50. Antoku S., Saksela K., Rivera G.M., and Mayer B.J. A crucial role in cell spreading for the interaction of Abl PxxP motifs with Crk and Nck adaptors. J Cell Sci. 2008; 121: 3071-3082.
51. Saarikangas J., Hakanen J., Mattila P.K., Grumet M., Salminen M., and Lappalainen P. ABBA regulates plasma-membrane and actin dynamics to promote radial glia extension. J Cell Sci. 2008; 121: 1444-1454.
52. Zheng D., Niu S., Yu D., Zhan X.H., Zeng X., Cui B., Chen Y., Yoon J., Martin S.S., Lu X., and Zhan X. Abba promotes PDGF-mediated membrane ruffling through activation of the small GTPase Rac1. Biochem Biophys Res Commun. 2010; 401: 527-532.