Overexpression of CRKII increases migration and invasive potential in oral squamous cell carcinoma

Cancer Letters

Volumn 303, Issue 2, 2011, Pages 84-91

  Yamada, Shin ichi ^a   Yanamoto, Souichi ^a   Kawasaki, Goro ^a   Rokutanda, Satoshi ^a   Yonezawa, Hisanobu ^a   Kawakita, Akiko ^a   Nemoto, Takayuki K ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

Author keywords

CRKII; Invasion; Metastasis; Oral squamous cell carcinoma; RNA interference

Indexed keywords

ADAPTOR PROTEIN; CORTACTIN; CRK ASSOCIATED SUBSTRATE PROTEIN; CT10 REGULATOR OF KINASE II; MEMBRANE PROTEIN; PROTEIN DOCK180; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CANCER CELL CULTURE; CANCER CLASSIFICATION; CANCER GENE THERAPY; CANCER GRADING; CANCER INVASION; CARCINOGENESIS; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MOLECULARLY TARGETED THERAPY; MOUTH CARCINOMA; MOUTH MUCOSA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SQUAMOUS CELL CARCINOMA; TUMOR BIOPSY;

CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; MODELS, BIOLOGICAL; MOUTH NEOPLASMS; NEOPLASM INVASIVENESS; PROTO-ONCOGENE PROTEINS C-CRK; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

EID: 79952043247     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.01.004     Document Type: Article

References (57)

1. Mao L., Hong W.K., Papadimitrakopoulou V.A. Focus on head and neck cancer. Cancer Cell 2004, 5:311-316.
2. Hicks W.L., North J.H., Loree T.R., Maamoun S., Mullins A., Orner J.B., et al. Surgery as a single modality therapy for squamous cell carcinoma of the oral tongue. Am. J. Otolaryngol. 1998, 19:24-28.
3. Sessions D.G., Lenox J., Spector G.J., Chao C., Chaudry O.A. Analysis of treatment results for base of tongue cancer. Laryngoscope 2003, 113:1252-1261.
4. González-García R., Naval-Gías L., Sastre-Pérez J., Rodríguez-Campo F.J., Muñoz-Guerra M.F., Usandizaga J.L., et al. Contralateral lymph neck node metastasis of squamous cell carcinoma of the oral cavity: a retrospective analytic study in 315 patients. J. Oral Maxillofac. Surg. 2008, 66:1390-1398.
5. Ziober B.L., Silverman S.S., Kramer R.H. Adhesive mechanisms regulating invasion and metastasis in oral cancer. Crit. Rev. Oral Biol. Med. 2001, 12:499-510.
6. Bánkfalvi A., Krassort M., Buchwalow I.B., Végh A., Felszeghy E., Piffkó J. Gains and losses of adhesion molecules (CD44, E-cadherin, and beta-catenin) during oral carcinogenesis and tumour progression. J. Pathol. 2002, 198:343-351.
7. Arora S., Kaur J., Sharma C., Mathur M., Bahadur S., Shukla N.K., et al. Stromelysin 3, Ets-1, and vascular endothelial growth factor expression in oral precancerous and cancerous lesions: correlation with microvessel density, progression, and prognosis. Clin. Cancer Res. 2005, 11:2272-2284.
8. Yanamoto S., Kawasaki G., Yoshitomi I., Iwamoto T., Hirata K., Mizuno A. Clinicopathologic significance of EpCAM expression in squamous cell carcinoma of the tongue and its possibility as a potential target for tongue cancer gene therapy. Oral Oncol. 2007, 43:869-877.
9. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
10. Clark E.A., Brugge J.S. Integrins and signal transduction pathways: the road taken. Science 1995, 268:233-239.
11. Birge R.B., Knudsen B.S., Besser D., Hanafusa H. SH2 and SH3-containing adaptor proteins: redundant or independent mediators of intracellular signal transduction. Genes Cells 1996, 1:595-613.
12. Mayer B.J., Hamaguchi M., Hanafusa H. A novel viral oncogene with structural similarity to phospholipase C. Nature Mar. 1988, 172:272-275.
13. Matsuda M., Tanaka S., Nagata S., Kojima A., Kurata T., Shibuya M. Two species of human CRK cDNA encode proteins with distinct biological activities. Mol. Cell Biol. 1992, 12:3482-3489.
14. Feller S.M. Crk family adaptors-signalling complex formation and biological roles. Oncogene 2001, 20:6348-6371.
15. Nishihara H., Tanaka S., Tsuda M., Oikawa S., Maeda M., Shimizu M., et al. Molecular and immunohistochemical analysis of signaling adaptor protein Crk in human cancers. Cancer Lett. 2002, 180:55-61.
16. Takino T., Nakada M., Miyamori H., Yamashita J., Yamada K.M., Sato H. CrkI adapter protein modulates cell migration and invasion in glioblastoma. Cancer Res. 2003, 63:2335-2337.
17. Miller C.T., Chen G., Gharib T.G., Wang H., Thomas D.G., Misek D.E., et al. Increased C-CRK proto-oncogene expression is associated with an aggressive phenotype in lung adenocarcinomas. Oncogene 2003, 22:7950-7957.
18. Chodniewicz D., Klemke R.L. Regulation of integrin-mediated cellular responses through assembly of a CAS/Crk scaffold. Biochim. Biophys. Acta 2004, 1692(2-3):63-76.
19. Lamorte L., Rodrigues S., Naujokas M., Park M. Crk synergizes with epidermal growth factor for epithelial invasion and morphogenesis and is required for the met morphogenic program. J. Biol. Chem. 2002, 277(40):37904-37911. Epub 2002 Jul 23.
20. Garcia-Guzman M., Dolfi F., Zeh K., Vuori K. Met-induced JNK activation is mediated by the adapter protein Crk and correlates with the Gab1 - Crk signaling complex formation. Oncogene 1999, 18(54):7775-7786.
21. Maroun C.R., Holgado-Madruga M., Royal I., Naujokas M.A., Fournier T.M., Wong A.J., Park M. The Gab1 PH domain is required for localization of Gab1 at sites of cell-cell contact and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol. Cell Biol. 1999, 19(3):1784-1799.
22. 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(12):6746-6753.
23. Nolan K.M., Barrett K., Lu Y., Hu K.Q., Vincent S., Settleman J. Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes. Genes Dev. 1998, 12(21):3337-3342.
24. Feller S.M., Knudsen B., Hanafusa H. C-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 1994, 13(10):2341-2351.
25. Liu F., Hill D.E., Chernoff J. Direct binding of the proline-rich region of protein tyrosine phosphatase 1B to the Src homology 3 domain of p130(Cas). J. Biol. Chem. 1996, 271(49):31290-31295.
26. Gelkop S., Babichev Y., Isakov N. T cell activation induces direct binding of the Crk adapter protein to the regulatory subunit of phosphatidylinositol 3-kinase (p85) via a complex mechanism involving the Cbl protein. J. Biol. Chem. 2001, 276(39):36174-36182.
27. Friedl P., Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 2003, 3(5):362-374.
28. Klemke R.L., Leng J., Molander R., Brooks P.C., Vuori K., Cheresh D.A. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 1998, 140(4):961-972.
29. Kiyokawa E., Hashimoto Y., Kurata T., Sugimura H., Matsuda M. Evidence that DOCK180 up-regulates signals from the CrkII-p130(Cas) complex. J. Biol. Chem. 1998, 273(38):24479-24484.
30. Bryne M., Boysen M., Alfsen C.G., Abeler V.M., Sudbø J., Nesland J.M., Kristensen G.B., Piffko J., Bankfalvi A. The invasive front of carcinomas. The most important area for tumour prognosis?. Anticancer Res. 1998, 18(6B):4757-4764.
31. Fu L., Qin Y.R., Xie D., Chow H.Y., Ngai S.M., Kwong D.L., Li Y., Guan X.Y. Identification of alpha-actinin 4 and 67 kDa laminin receptor as stage-specific markers in esophageal cancer via proteomic approaches. Cancer 2007, 110(12):2672-2681.
32. Yamada S., Yanamoto S., Yoshida H., Yoshitomi I., Kawasaki G., Mizuno A., Nemoto T.K. RNAi-mediated down-regulation of alpha-actinin-4 decreases invasion potential in oral squamous cell carcinoma. Int. J. Oral Maxillofac. Surg. 2010, 39(1):61-67.
33. Yamada S.I., Yanamoto S., Kawasaki G., Mizuno A., Nemoto T.K. Overexpression of Cortactin Increases Invasion Potential in Oral Squamous Cell Carcinoma. Pathol. Oncol. Res. 2010, (January 13).
34. Albert M.L., Kim J.I., Birge R.B. Alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat. Cell Biol. 2000, 2(12):899-905.
35. Wu Y.C., Horvitz HR C. Elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 1998, 392(6675):501-504.
36. Reddien P.W., Horvitz H.R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2000, 2(3):131-136.
37. Brugnera E., Haney L., Grimsley C., Lu M., Walk S.F., Tosello-Trampont A.C., Macara I.G., Madhani H., Fink G.R., Ravichandran K.S. Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat. Cell Biol. 2002, 4(8):574-582.
38. Côté J.F., Vuori K. Identification of an evolutionarily conserved superfamily of DOCK180-related proteins with guanine nucleotide exchange activity. J. Cell Sci. 2002, 115(Pt 24):4901-4913.
39. Weed S.A., Parsons J.T. Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 2001, 20(44):6418-6434.
40. Daly R.J. Cortactin signalling and dynamic actin networks. Biochem. J. 2004, 382(Pt 1):13-25.
41. Bougnères L., Girardin S.E., Weed S.A., Karginov A.V., Olivo-Marin J.C., Parsons J.T., Sansonetti P.J., Van Nhieu G.T. Cortactin and Crk cooperate to trigger actin polymerization during Shigella invasion of epithelial cells. J. Cell Biol. 2004, 166(2):225-235.
42. Hasegawa H., Kiyokawa E., Tanaka S., Nagashima K., Gotoh N., Shibuya M., Kurata T., Matsuda M. DOCK180, a major CRK-binding protein, alters cell morphology upon translocation to the cell membrane. Mol. Cell Biol. 1996, 16(4):1770-1776.
43. Cheresh D.A., Leng J., Klemke R.L. Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells. J. Cell Biol. 1999, 146(5):1107-1116.
44. Wehrle-Haller B., Imhof B.A. Actin, microtubules and focal adhesion dynamics during cell migration. Int. J. Biochem. Cell Biol. 2003, 35(1):39-50.
45. Vallés A.M., Beuvin M., Boyer B. Activation of Rac1 by paxillin-Crk-DOCK180 signaling complex is antagonized by Rap1 in migrating NBT-II cells. J. Biol. Chem. 2004, 279(43):44490-44496.
46. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420(6916):629-635.
47. Ridley A.J. Rho GTPases and cell migration. J. Cell Sci. 2001, 114(Pt 15):2713-2722.
48. Nojima Y., Morino N., Mimura T., Hamasaki K., Furuya H., Sakai R., Sato T., Tachibana K., Morimoto C., Yazaki Y., et al. Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130Cas, a Src homology 3-containing molecule having multiple Src homology 2-binding motifs. J. Biol. Chem. 1995, 270(25):15398-15402.
49. Nakamoto T., Sakai R., Honda H., Ogawa S., Ueno H., Suzuki T., Aizawa S., Yazaki Y., Hirai H. Requirements for localization of p130cas to focal adhesions. Mol. Cell Biol. 1997, 17(7):3884-3897.
50. Vuori K., Ruoslahti E. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 1995, 270(38):22259-22262.
51. Vuori K., Hirai H., Aizawa S., Ruoslahti E. Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell Biol. 1996, 16(6):2606-2613.
52. Nievers M.G., Birge R.B., Greulich H., Verkleij A.J., Hanafusa H., en Henegouwen P.M. V-Crk-induced cell transformation: changes in focal adhesion composition and signaling. J. Cell Sci. 1997, 110(Pt 3):389-399.
53. Lamorte L., Royal I., Naujokas M., Park M. Crk adapter proteins promote an epithelial-mesenchymal-like transition and are required for HGF-mediated cell spreading and breakdown of epithelial adherens junctions. Mol. Biol Cell. 2002, 13(5):1449-1461.
54. Miki H., Yamaguchi H., Suetsugu S., Takenawa T. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 2000, 408(6813):732-735.
55. Tuschl T. Expanding small RNA interference. Nat. Biotechnol. 2002, 20(5):446-448.
56. Kudo Y., Kitajima S., Ogawa I., Kitagawa M., Miyauchi M., Takata T. Small interfering RNA targeting of S phase kinase-interacting protein 2 inhibits cell growth of oral cancer cells by inhibiting p27 degradation. Mol. Cancer Ther. 2005, 4(3):471-476.
57. Yanamoto S., Iwamoto T., Kawasaki G., Yoshitomi I., Baba N., Mizuno A. Silencing of the p53R2 gene by RNA interference inhibits growth and enhances 5-fluorouracil sensitivity of oral cancer cells. Cancer Lett. 2005, 223(1):67-76. Epub 2004 Nov 25.