Knockdown of Ron kinase inhibits mutant phosphatidylinositol 3-kinase and reduces metastasis in human colon carcinoma

Journal of Biological Chemistry

Volumn 284, Issue 16, 2009, Pages 10912-10922

  Jing, Wang ^a,b   Rajput, Ashwani ^a,b   Kan, Julie L C ^c   Rose, Rebecca ^c   Xiao Qiong, Liu ^a   Kuropatwinski, Karen ^c   Hauser, Jennie ^c   Beko, Alexander ^c   Dominiquez, Ivan ^c   Sharatt, Elizabeth A ^c   Brattain, Lisa ^a   LeVea, Charles ^d   Sun, Feng Lei ^c   Keane, David M ^c   Gibson, Neil W ^c   Brattain, Michael G ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d OSI PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKT PHOSPHORYLATION; CASPASE-3 ACTIVATION; CELL MOTILITY; COLON CANCER; COLON CANCER CELLS; CONTROL-CELL; DNA FRAGMENTATION; GAIN-OF-FUNCTION MUTANTS; GROWTH FACTOR; HUMAN CANCER; HUMAN COLON; IN-VIVO; LUNG METASTASIS; ORTHOTOPIC; PHOSPHATIDYLINOSITOL 3-KINASE; RECEPTOR TYROSINE KINASE; RNA INTERFERENCE; SIGNALING PROTEINS; STRESS-INDUCED; WOUND HEALING;

AMINO ACIDS; CELL CULTURE; CELL DEATH; NUCLEIC ACIDS; PATHOLOGY; RNA;

CELL MEMBRANES;

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; RON KINASE; UNCLASSIFIED DRUG; RON PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; COLON CARCINOMA; CONTROLLED STUDY; ENZYME INHIBITION; GENETIC GAIN; HETEROZYGOTE; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG METASTASIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; WOUND HEALING; ANIMAL; BAGG ALBINO MOUSE; CANCER INVASION; CANCER TRANSPLANTATION; COLON TUMOR; DRUG ANTAGONISM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; METASTASIS; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; RECEPTOR PROTEIN-TYROSINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 67449098154     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M809551200     Document Type: Article

References (65)

1. Rubin, J. S., Bottaro, D. P., and Aaronson, S. A. (1993) Biochim. Biophys. Acta 1155, 357-371
2. Ronsin, C., Muscatelli, F., Mattei, M. G., and Breathnach, R. (1993) Oncogene 8, 1195-1202
3. Wang, M. H., Ronsin, C., Gesnel, M. C., Coupey, L., Skeel, A., Leonard, E. J., and Breathnach, R. (1994) Science 266, 117-119
4. Gaudino, G., Follenzi, A., Naldini, L., Collesi, C., Santoro, M., Gallo, K. A., Godowski, P. J., and Comoglio, P. M. (1994) EMBO J. 13, 3524-3532
5. Santoro, M. M., Penengo, L., Orecchia, S., Cilli, M., and Gaudino, G. (2000) Oncogene 19, 5208-5211
6. Li, B. Q., Wang, M. H., Kung, H. F., Ronsin, C., Breathnach, R., Leonard, E. J., and Kamata, T. (1995) Biochem. Biophys. Res. Commun. 216, 110-118
7. Zhou, Y. Q., Chen, Y. Q., Fisher, J. H., and Wang, M. H. (2002) J. Biol. Chem. 277, 38104-38110
8. Liu, Q. P., Fruit, K., Ward, J., and Correll, P. H. (1999) J. Immunol. 163, 6606-6613
9. Santoro, M. M., Gaudino, G., and Marchisio, P. C. (2003) Dev. Cell 5, 257-271
10. Chen, Y. Q., Zhou, Y. Q., Angeloni, D., Kurtz, A. L., Qiang, X. Z., and Wang, M. H. (2000) Exp. Cell Res. 261, 229-238
11. Wang, M. H., Montero-Julian, F. A., Dauny, I., and Leonard, E. J. (1996) Oncogene 13, 2167-2175
12. Xiao, Z. Q., Chen, Y. Q., and Wang, M. H. (2000) Biochem. Biophys. Res. Commun. 267, 669-675
13. Danilkovitch-Miagkova, A., and Leonard, E. J. (2001) Histol. Histopathol. 16, 623-631
14. Follenzi, A., Bakovic, S., Gual, P., Stella, M. C., Longati, P., and Comoglio, P. M. (2000) Oncogene 19, 3041-3049
15. Waltz, S. E., McDowell, S. A., Muraoka, R. S., Air, E. L., Flick, L. M., Chen, Y. Q., Wang, M. H., and Degen, S. J. (1997) J. Biol. Chem. 272, 30526-30537
16. Wang, M. H., Dlugosz, A. A., Sun, Y., Suda, T., Skeel, A., and Leonard, E. J. (1996) Exp. Cell Res. 226, 39-46
17. Maggiora, P., Marchio, S., Stella, M. C., Giai, M., Belfiore, A., De Bortoli, M., Di Renzo, M. F., Costantino, A., Sismondi, P., and Comoglio, P. M. (1998) Oncogene 16, 2927-2933
18. Zhou, Y. Q., He, C., Chen, Y. Q., Wang, D., and Wang, M. H. (2003) Oncogene 22, 186-197
19. Lin, H. S., Berry, G. J., Fee, W. E., Jr., Terris, D. J., and Sun, Z. (2004) Arch. Otolaryngol. Head Neck Surg. 130, 311-316
20. Samuels, Y., Wang, Z., Bardelli, A., Silliman, N., Ptak, J., Szabo, S., Yan, H., Gazdar, A., Powell, S. M., Riggins, G. J., Willson, J. K., Markowitz, S., Kinzler, K. W., Vogelstein, B., and Velculescu, V. E. (2004) Science 304, 554
21. Campbell, I. G., Russell, S. E., Choong, D. Y., Montgomery, K. G., Ciavarella, M. L., Hooi, C. S., Cristiano, B. E., Pearson, R. B., and Phillips, W. A. (2004) Cancer Res. 64, 7678-7681
22. Lee, J. W., Soung, Y. H., Kim, S. Y., Lee, H. W., Park, W. S., Nam, S. W., Kim, S. H., Lee, J. Y., Yoo, N. J., and Lee, S. H. (2005) Oncogene 24, 1477-1480
23. Bachman, K. E., Argani, P., Samuels, Y., Silliman, N., Ptak, J., Szabo, S., Konishi, H., Karakas, B., Blair, B. G., Lin, C., Peters, B. A., Velculescu, V. E., and Park, B. H. (2004) Cancer Biol. Ther. 3, 772-775
24. Wang, J., Kuropatwinski, K., Hauser, J., Rossi, M. R., Zhou, Y., Conway, A., Kan, J. L., Gibson, N. W., Willson, J. K., Cowell, J. K., and Brattain, M. G. (2007) Mol. Cancer Ther. 6, 1143-1150
25. Guo, X. N., Rajput, A., Rose, R., Hauser, J., Beko, A., Kuropatwinski, K., Levea, C., Hoffman, R. M., Brattain, M. G., and Wang, J. (2007) Cancer Res. 67, 5851-5858
26. Hanahan, D., and Weinberg, R. A. (2000) Cell 100, 57-70
27. Cunningham, D., Humblet, Y., Siena, S., Khayat, D., Bleiberg, H., Santoro, A., Bets, D., Mueser, M., Harstrick, A., Verslype, C., Chau, I., and Van Cutsem, E. (2004) N. Engl. J. Med. 351, 337-345
28. Perez-Soler, R., Chachoua, A., Hammond, L. A., Rowinsky, E. K., Huberman, M., Karp, D., Rigas, J., Clark, G. M., Santabarbara, P., and Bonomi, P. (2004) J. Clin. Oncol. 22, 3238-3247
29. Saltz, L. B., Meropol, N. J., Loehrer, P. J., Sr., Needle, M. N., Kopit, J., and Mayer, R. J. (2004) J. Clin. Oncol. 22, 1201-1208
30. Portera, C. A., Jr., Berman, R. S., and Ellis, L. M. (1998) Surg. Oncol. 7, 183-195
31. Yokota, J. (2000) Carcinogenesis 21, 497-503
32. Jemal, A., Siegel, R., Ward, E., Murray, T., Xu, J., and Thun, M. J. (2007) CA-Cancer J. Clin. 57, 43-66
33. Wang, D., Shen, Q., Chen, Y. Q., and Wang, M. H. (2004) Oncogene 23, 1668-1680
34. Zinser, G. M., Leonis, M. A., Toney, K., Pathrose, P., Thobe, M., Kader, S. A., Peace, B. E., Beauman, S. R., Collins, M. H., and Waltz, S. E. (2006) Cancer Res. 66, 11967-11974
35. Peace, B. E., Toney-Earley, K., Collins, M. H., and Waltz, S. E. (2005) Cancer Res. 65, 1285-1293
36. Chambers, A. F., Naumov, G. N., Vantyghem, S. A., and Tuck, A. B. (2000) Breast Cancer Res. 2, 400-407
37. Chambers, A. F., Naumov, G. N., Varghese, H. J., Nadkarni, K. V., Mac-Donald, I. C., and Groom, A. C. (2001) Surg. Oncol. Clin. N. Am. 10, 243-255, vii
38. Chambers, A. F., Groom, A. C., and MacDonald, I. C. (2002) Nat. Rev. Cancer 2, 563-572
39. Xu, X. M., Wang, D., Shen, Q., Chen, Y. Q., and Wang, M. H. (2004) Oncogene 23, 8464-8474
40. Brattain, M. G., Levine, A. E., Chakrabarty, S., Yeoman, L. C., Willson, J. K., and Long, B. (1984) Cancer Metastasis Rev. 3, 177-191
41. Boyd, D. D., Levine, A. E., Brattain, D. E., McKnight, M. K., and Brattain, M. G. (1988) Cancer Res. 48, 2469-2474
42. Wang, J., Sun, L., Myeroff, L., Wang, X., Gentry, L. E., Yang, J., Liang, J., Zborowska, E., Markowitz, S., Willson, J. K., and Brattain, M. G. (1995) J. Biol. Chem. 270, 22044-22049
43. Wang, J., Han, W., Zborowska, E., Liang, J., Wang, X., Willson, J. K., Sun, L., and Brattain, M. G. (1996) J. Biol. Chem. 271, 17366-17371
44. Jackson, J. G., St. Clair, P., Sliwkowski, M. X., and Brattain, M. G. (2004) Cancer Res. 64, 2601-2609
45. Nakane, P. K. (1975) Ann. N. Y. Acad. Sci. 254, 203-211
46. Cereijido, M., Shoshani, L., and Contreras, R. G. (2000) Am. J. Physiol. 279, G477-G482
47. Martin, T. A., and Jiang, W. G. (2001) Histol. Histopathol. 16, 1183-1195
48. Goldie, J. H., and Coldman, A. J. (1979) Cancer Treat. Rep. 63, 1727-1733
49. Hajra, K. M., and Liu, J. R. (2004) Apoptosis 9, 691-704
50. Kato, S., Iida, S., Higuchi, T., Ishikawa, T., Takagi, Y., Yasuno, M., Enomoto, M., Uetake, H., and Sugihara, K. (2007) Int. J. Cancer 121, 1771-1778
51. Zheng, Y., Bagrodia, S., and Cerione, R. A. (1994) J. Biol. Chem. 269, 18727-18730
52. Nakamura, T., Teramoto, H., and Ichihara, A. (1986) Proc. Natl. Acad. Sci. U. S. A. 83, 6489-6493
53. Stoker, M., Gherardi, E., Perryman, M., and Gray, J. (1987) Nature 327, 239-242
54. Gherardi, E., Gray, J., Stoker, M., Perryman, M., and Furlong, R. (1989) Proc. Natl. Acad. Sci. U. S. A. 86, 5844-5848
55. Zarnegar, R., and Michalopoulos, G. (1989) Cancer Res. 49, 3314-3320
56. Medico, E., Mongiovi, A. M., Huff, J., Jelinek, M. A., Follenzi, A., Gaudino, G., Parsons, J. T., and Comoglio, P. M. (1996) Mol. Biol. Cell 7, 495-504
57. Trusolino, L., and Comoglio, P. M. (2002) Nat. Rev. Cancer 2, 289-300
58. Morrow, C. J., Gray, A., and Dive, C. (2005) FEBS Lett. 579, 5123-5128
59. Huang, C. H., Mandelker, D., Schmidt-Kittler, O., Samuels, Y., Velculescu, V. E., Kinzler, K. W., Vogelstein, B., Gabelli, S. B., and Amzel, L. M. (2007) Science 318, 1744-1748
60. Del Bufalo, D., Biroccio, A., Leonetti, C., and Zupi, G. (1997) FASEB J. 11, 947-953
61. Glinsky, G. V., Glinsky, V. V., Ivanova, A. B., and Hueser, C. J. (1997) Cancer Lett. 115, 185-193
62. Inbal, B., Cohen, O., Polak-Charcon, S., Kopolovic, J., Vadai, E., Eisenbach, L., and Kimchi, A. (1997) Nature 390, 180-184
63. Lowney, J. K., Frisella, M. M., Lairmore, T. C., and Doherty, G. M. (1998) Surgery 124, 1043-1048
64. Wolmark, N., Cruz, I., Redmond, C. K., Fisher, B., and Fisher, E. R. (1983) Cancer 51, 1315-1322
65. Greene, F. L., Page, D. L., Fleming, I. D., Fritz, A. G., Charles, B. M., Haller, D. G., and Morrow, M. (2002) Colon and Rectum in AJCC Cancer Staging Handbook, 6th Ed. pp. 127-138, Springer-Verlag New York LLC, New York