Emerging roles for Crk in human cancer

Genes and Cancer

Volumn 1, Issue 11, 2010, Pages 1132-1139

  Sriram, Ganapathy ^a   Birge, Raymond B ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Cell motility; Crk adaptor proteins; Human cancer; Malignant phenotype

Indexed keywords

ADAPTOR PROTEIN; BIOLOGICAL MARKER; CELL PROTEIN; CRK LIKE PROTEIN; CRK PROTEIN; ONCOPROTEIN; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGICAL ACTIVITY; CANCER CELL; CELL TRANSFORMATION; DRUG TARGETING; ENZYME SUBSTRATE; FIBROBLAST; HUMAN; NEOPLASM; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN VARIANT; SIGNAL TRANSDUCTION; STOICHIOMETRY; TUMOR;

EID: 79960045948     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601910397188     Document Type: Article

References (67)

1. Mayer BJ, Hamaguchi M, Hanafusa H. A novel viral oncogene with structural similarity to phospholipase C. Nature. 1988;332:272-5.
2. 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;12:3482-9.
3. Reichman CT, Mayer BJ, Keshav S, Hanafusa H. The product of the cellular crk gene consists primarily of SH2 and SH3 regions. Cell Growth Differ. 1992;3:451-60.
4. ten Hoeve J, Morris C, Heisterkamp N, Groffen J. Isolation and chromosomal localization of CRKL, a human crk-like gene. Oncogene. 1993;8:2469-74.
5. Birge RB, Kalodimos C, Inagaki F, Tanaka S. Crk and CrkL adaptor proteins: networks for physiological and pathological signaling. Cell Commun Signal. 2009;7:13.
6. Feller SM. Crk family adaptors-signalling complex formation and biological roles. Oncogene. 2001;20:6348-71.
7. Muralidharan V, Dutta K, Cho J, et al. Solution structure and folding characteristics of the Cterminal SH3 domain of c-Crk-II. Biochemistry. 2006;45:8874-84.
8. Reichman C, Singh K, Liu Y, et al. Transactivation of Abl by the Crk II adapter protein requires a PNAY sequence in the Crk C-terminal SH3 domain. Oncogene. 2005;24:8187-99.
9. Prosser S, Sorokina E, Pratt P, Sorokin A. CrkIII: a novel and biologically distinct member of the Crk family of adaptor proteins. Oncogene. 2003;22:4799-806.
10. Guris DL, Fantes J, Tara D, Druker BJ, Imamoto A. Mice lacking the homologue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syndrome. Nat Genet. 2001;27:293-8.
11. Park TJ, Boyd K, Curran T. Cardiovascular and craniofacial defects in Crk-null mice. Mol Cell Biol. 2006;26:6272-82.
12. Matsuda M, Mayer BJ, Fukui Y, Hanafusa H. Binding of transforming protein, P47gag-crk, to a broad range of phosphotyrosine-containing proteins. Science. 1990;248:1537-9.
13. Matsuda M, Mayer BJ, Hanafusa H. Identification of domains of the v-crk oncogene product sufficient for association with phosphotyrosinecontaining proteins. Mol Cell Biol. 1991;11: 1607-13.
14. Birge RB, Fajardo JE, Reichman C, et al. Identification and characterization of a highaffinity interaction between v-Crk and tyrosinephosphorylated paxillin in CT10-transformed fibroblasts. Mol Cell Biol. 1993;13:4648-56.
15. Songyang Z, Shoelson SE, Chaudhuri M, et al. SH2 domains recognize specific phosphopeptide sequences. Cell. 1993;72:767-78.
16. Liu BA, Jablonowski K, Shah EE, Engelmann BW, Jones RB, Nash PD. SH2 domains recognize contextual peptide sequence information to determine selectivity. Mol Cell Proteomics. 2010;9:2391-404.
17. Knudsen BS, Feller SM, Hanafusa H. Four proline-rich sequences of the guanine-nucleotide exchange factor C3G bind with unique specificity to the first Src homology 3 domain of Crk. J Biol Chem. 1994;269:32781-7.
18. Feng S, Kasahara C, Rickles RJ, Schreiber SL. Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc Natl Acad Sci U S A. 1995;92:12408-15.
19. Rickles RJ, Botfield MC, Zhou XM, Henry PA, Brugge JS, Zoller MJ. Phage display selection of ligand residues important for Src homology 3 domain binding specificity. Proc Natl Acad Sci U S A. 1995;92:10909-13.
20. Kobashigawa Y, Sakai M, Naito M, et al. Structural basis for the transforming activity of human cancer-related signaling adaptor protein CRK. Nat Struct Mol Biol. 2007;14:503-10.
21. Sarkar P, Reichman C, Saleh T, Birge RB, Kalodimos CG. Proline cis-trans isomerization controls autoinhibition of a signaling protein. Mol Cell. 2007;25:413-26.
22. Feller SM, Knudsen B, Hanafusa H. c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 1994;13:2341-51.
23. Ren R, Ye ZS, Baltimore D. Abl protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites. Genes Dev. 1994;8: 783-95.
24. Rosen MK, Yamazaki T, Gish GD, Kay CM, Pawson T, Kay LE. Direct demonstration of an intramolecular SH2-phosphotyrosine interaction in the Crk protein. Nature. 1995;374:477-9.
25. Cartwright CA, Eckhart W, Simon S, Kaplan PL. Cell transformation by pp60c-src mutated in the carboxy-terminal regulatory domain. Cell. 1987; 49:83-91.
26. Jove R, Hanafusa H. Cell transformation by the viral src oncogene. Annu Rev Cell Biol. 1987;3:31-56.
27. Senechal K, Halpern J, Sawyers CL. The CRKL adaptor protein transforms fibroblasts and functions in transformation by the BCR-ABL oncogene. J Biol Chem. 1996;271:23255-61.
28. Senechal K, Heaney C, Druker B, Sawyers CL. Structural requirements for function of the Crkl adapter protein in fibroblasts and hematopoietic cells. Mol Cell Biol. 1998;18:5082-90.
29. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin. 2009;59:225-49.
30. Miller CT, Chen G, Gharib TG, et al. Increased C-CRK proto-oncogene expression is associated with an aggressive phenotype in lung adenocarcinomas. Oncogene. 2003;22:7950-7.
31. Kim YH, Kwei KA, Girard L, et al. Genomic and functional analysis identifies CRKL as an oncogene amplified in lung cancer. Oncogene. 2010;29:1421-30.
32. Rodrigues SP, Fathers KE, Chan G, et al. CrkI and CrkII function as key signaling integrators for migration and invasion of cancer cells. Mol Cancer Res. 2005;3:183-94.
33. Fathers KE, Rodrigues S, Zuo D, et al. CrkII transgene induces atypical mammary gland development and tumorigenesis. Am J Pathol. 2010;176:446-60.
34. Lamorte L, Royal I, Naujokas M, Park M. Crk adapter proteins promote an epithelialmesenchymal-like transition and are required for HGF-mediated cell spreading and breakdown of epithelial adherens junctions. Mol Biol Cell. 2002;13:1449-61.
35. Kain KH, Gooch S, Klemke RL. Cytoplasmic c-Abl provides a molecular 'Rheostat' controlling carcinoma cell survival and invasion. Oncogene. 2003;22:6071-80.
36. Klemke RL, Leng J, Molander R, Brooks PC, Vuori K, Cheresh DA. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J Cell Biol. 1998;140:961-72.
37. Noren NK, Foos G, Hauser CA, Pasquale EB. The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat Cell Biol. 2006;8:815-25.
38. Wang JY. Eph tumour suppression: the dark side of Gleevec. Nat Cell Biol. 2006;8:785-6.
39. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114:97-109.
40. Takino T, Nakada M, Miyamori H, Yamashita J, Yamada KM, Sato H. CrkI adapter protein modulates cell migration and invasion in glioblastoma. Cancer Res. 2003;63:2335-7.
41. Wang L, Tabu K, Kimura T, et al. Signaling adaptor protein Crk is indispensable for malignant feature of glioblastoma cell line KMG4. Biochem Biophys Res Commun. 2007;362:976-81.
42. Birchmeier W, Behrens J, Weidner KM, Hulsken J, Birchmeier C. Epithelial differentiation and the control of metastasis in carcinomas. Curr Top Microbiol Immunol. 1996;213(Pt 2):117-35.
43. Weidner KM, Sachs M, Birchmeier W. The Met receptor tyrosine kinase transduces motility, proliferation, and morphogenic signals of scatter factor/hepatocyte growth factor in epithelial cells. J Cell Biol. 1993;121:145-54.
44. Watanabe T, Tsuda M, Makino Y, et al. Adaptor molecule Crk is required for sustained phosphorylation of Grb2-associated binder 1 and hepatocyte growth factor-induced cell motility of human synovial sarcoma cell lines. Mol Cancer Res. 2006;4:499-510.
45. Watanabe T, Tsuda M, Tanaka S, et al. Adaptor protein Crk induces Src-dependent activation of p38 MAPK in regulation of synovial sarcoma cell proliferation. Mol Cancer Res. 2009;7:1582-92.
46. Linghu H, Tsuda M, Makino Y, et al. Involvement of adaptor protein Crk in malignant feature of human ovarian cancer cell line MCAS. Oncogene. 2006;25:3547-56.
47. Wang H, Linghu H, Wang J, et al. The role of Crk/Dock180/Rac1 pathway in the malignant behavior of human ovarian cancer cell SKOV3. Tumour Biol. 2010;31:59-67.
48. Oda T, Heaney C, Hagopian JR, Okuda K, Griffin JD, Druker BJ. Crkl is the major tyrosine- phosphorylated protein in neutrophils from patients with chronic myelogenous leukemia. J Biol Chem. 1994;269:22925-8.
49. Mizutani T, Kondo T, Darmanin S, et al. A novel FRET-based biosensor for the measurement of BCR-ABL activity and its response to drugs in living cells. Clin Cancer Res. 2010;16:3964-75.
50. Tunceroglu AS, Matsuda M, Birge RB. Realtime FRET to monitor drug resistance in chronic myelogenous leukemia. Mol Cancer Ther. 2010;9:3065-73.
51. Salgia R, Uemura N, Okuda K, et al. CRKL links p210BCR/ABL with paxillin in chronic myelogenous leukemia cells. J Biol Chem. 1995; 270:29145-50.
52. Heaney C, Kolibaba K, Bhat A, et al. Direct binding of CRKL to BCR-ABL is not required for BCR-ABL transformation. Blood. 1997;89: 297-306.
53. Hemmeryckx B, Reichert A, Watanabe M, et al. BCR/ABL P190 transgenic mice develop leukemia in the absence of Crkl. Oncogene. 2002;21:3225-31.
54. Johnson KJ, Griswold IJ, O'Hare T, et al. A BCR-ABL mutant lacking direct binding sites for the GRB2, CBL and CRKL adapter proteins fails to induce leukemia in mice. PLoS One. 2009;4:e7439.
55. Shishido T, Akagi T, Chalmers A, et al. Crk family adaptor proteins trans-activate c-Abl kinase. Genes Cells. 2001;6:431-40.
56. Crawford M, Brawner E, Batte K, et al. MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochem Biophys Res Commun. 2008;373:607-12.
57. Li X, Shen Y, Ichikawa H, Antes T, Goldberg GS. Regulation of miRNA expression by Src and contact normalization: effects on nonanchored cell growth and migration. Oncogene. 2009;28: 4272-83.
58. Feng R, Chen X, Yu Y, et al. miR-126 functions as a tumour suppressor in human gastric cancer. Cancer Lett. 2010;298:50-63.
59. Nishihara H, Tanaka S, Tsuda M, et al. Molecular and immunohistochemical analysis of signaling adaptor protein Crk in human cancers. Cancer Lett. 2002;180:55-61.
60. Liu S, Sun MZ, Tang JW, Wang Z, Sun C, Greenaway FT. High-performance liquid chromatography/ nano-electrospray ionization tandem mass spectrometry, two-dimensional difference in-gel electrophoresis and gene microarray identification of lymphatic metastasis-associated biomarkers. Rapid Commun Mass Spectrom. 2008;22:3172-8.
61. Luo B, Cheung HW, Subramanian A, et al. Highly parallel identification of essential genes in cancer cells. Proc Natl Acad Sci U S A. 2008;105:20380-5.
62. Tanaka S, Morishita T, Hashimoto Y, 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;91:3443-7.
63. Zheng J, Machida K, Antoku S, Ng KY, Claffey KP, Mayer BJ. Proteins that bind the Src homology 3 domain of CrkI have distinct roles in Crk transformation. Oncogene. 2010;29:6378-89.
64. Srinivasan D, Plattner R. Activation of Abl tyrosine kinases promotes invasion of aggressive breast cancer cells. Cancer Res. 2006;66:5648-55.
65. Srinivasan D, Sims JT, Plattner R. Aggressive breast cancer cells are dependent on activated Abl kinases for proliferation, anchorage-independent growth and survival. Oncogene. 2008;27: 1095-105.
66. Hashimoto Y, Katayama H, Kiyokawa E, et al. Phosphorylation of CrkII adaptor protein at tyrosine 221 by epidermal growth factor receptor. J Biol Chem. 1998;273:17186-91.
67. Johnson FM, Gallick GE. SRC family nonreceptor tyrosine kinases as molecular targets for cancer therapy. Anticancer Agents Med Chem. 2007;7:651-9.