Silencing of the type 1 insulin-like growth factor receptor increases the sensitivity to apoptosis and inhibits invasion in human lung adenocarcinoma A549 cells

• Autorzy: Ma Z , Dong A. , Kong M. , Qian J.
• Języki publikacji: EN

Abstrakty

EN

The type 1 insulin-like growth factor receptor (IGF-1R), which is over-expressed or activated in many human cancers, including lung cancer, mediates cancer cell proliferation and metastasis. Several studies indicate that blocking IGF-1R expression can inhibit tumor cell proliferation and metastasis. In this study, inhibition of the endogenous IGF-1R by recombinant adenoviruses encoding short hairpin RNAs against IGF-1R was found to significantly suppress IGF-1R expression, arrest the cell cycle, enhance the apoptotic response, and inhibit proliferation, adhesion, invasion and migration in A549 cells. Moreover, silencing IGF-1R decreases the expression of invasive-related genes including matrix metalloproteinase-2 (MMP-2), MMP-9, and urokinase-plasminogen activator (u-PA), and the phosphorylation of Akt and ERK1/2. These results suggest that the silencing of IGF-1R has the potential to be an effective cancer gene therapy strategy for human lung cancer.

Słowa kluczowe

EN

insulin-like growth factor 1; sensitivity; apoptosis; invasion; human lung; lung; adenocarcinoma; lung cancer; metastasis

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2007
• Tom: 12
• Numer: 4
• Opis fizyczny: p.556-572,fig.,ref.

Twórcy

autor

Ma Z

• Zhejiang University, Hangzhou, 310009, China

autor

Dong A.

autor

Kong M.

autor

Qian J.

Bibliografia

• 1. Mezzetti, M., Panigalli T., Giuliani, L., Raveglia, F., Giudice, F.L. and Meda, S. Personal experience in lung cancer sleeve lobectomy and sleeve pneumonectomy. Ann. Thorac. Surg. 73 (2002) 1736-1739.
• 2. Greenlee, R.T., Murray, T., Bolden, S. and Wingo, P. A. Cancer statistics, 2000: CA Cancer J. Clin. 50 (2000) 7-33.
• 3. Jiang, Y., Rom, W.N., Yie, T.A., Chi, C.X. and Tchou-Wong, K.M. Induction of tumor suppression and glandular differentiation of A549 lung carcinoma cells by dominant-negative IGF-I receptor. Oncogene 18 (1999) 6071-6077.
• 4. Min, Y., Adachi, Y., Yamamotom H., Ito, H., Itoh, F., Lee, C.T., Nadaf, S., Carbone, D.P. and Imai, K. Genetic blockade of the insulin-like growth factor-I receptor: a promising strategy for human pancreatic cancer. Cancer Res. 64 (2003) 32-41.
• 5. Zhang, D., Bar-Eli, M., Meloche, S. and Brodt, P. Dual regulation of MMP2 expression by the type 1 insulin-like growth factor receptor: the phosphatidylinositol 3-kinase/Akt and Raf/ERK pathways transmit opposing signals. J. Biol. Chem. 279 (2004) 19683-19690.
• 6. LeRoith, D., Werner, H., Beitner-Johnson, D. and Roberts, C.T. Jr. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr. Rev. 16 (1995) 143-163.
• 7. Nakanishi, Y., Mulshine, J.L., Kasprzyk, P.G., Natale, R.B., Maneckjee, R., Avis, I., Treston, A.M., Gazdar, A.F., Minna, J.D. and Cuttitta, F. Insulinlike growth factor-I can mediate autocrine proliferation of human small cell lung cancer cell lines in vitro. J. Clin. Invest. 82 (1988) 354-359.
• 8. Kaleko, M., Rutter, W.J. and Miller, A.D. Overexpression of the human insulin-like growth factor I receptor promotes ligand-dependent neoplastic transformation. Mol. Cell. Biol. 10 (1990) 464-473.
• 9. Remacle-Bonnet, M.M., Garrouste, F.L., Heller, S., Andre, F., Marvaldi, J.L. and Pommier, G.J. Insulin-like growth factor-I protects colon cancer cells from death factor-induced apoptosis by potentiating tumor necrosis factor alpha-induced mitogen-activated protein kinase and nuclear factor kappaB signaling pathways. Cancer Res. 60 (2000) 2007-2017.
• 10. Singh, P. Insulin-like growth factor system in growth, development and carcinogenesis. J. Clin. Lig. Assay 23 (2000) 214-232.
• 11. Scotlandi, K., Maini, C., Manara, M.C., Benini, S., Serra, M., Cerisano, V., Strammiello, R., Baldini, N., Lollini, P.L., Nanni, P., Nicoletti, G. and Picci, P. Effectiveness of insulin-like growth factor I receptor antisense strategy against Ewing's sarcoma cells. Cancer Gene Ther. 9 (2002) 296-307.
• 12. Turner, B.C., Haffty, B.G., Narayanan, L., Yuan, J., Havre, P.A., Gumbs, A.A., Kaplan, L., Burgaud, J.L., Carter, D., Baserga, R. and Glazer, P.M. Insulin-like growth factor-I receptor overexpression mediates cellular radioresistance and local breast cancer recurrence after lumpectomy and radiation. Cancer Res. 57 (1997) 3079-3083.
• 13. Wu, Y., Tewari, M., Cui, S. and Rubin, R. Activation of the insulin-like growth factor-I receptor inhibits tumor necrosis factor-induced cell death. J. Cell Physiol. 168 (1996) 499-509.
• 14. Grimberg, A. and Cohen, P. Growth hormone and prostate cancer: guilty by association? J. Endocrinol. Invest. 22 (1999) 64-73.
• 15. Ma, J., Pollak, M., Giovannucci, E., Chan, J.M., Tao, Y., Hennekens, C. and Stampfer, M.J. A prospective study of plasma levels of insulin-like growth factor I (IGF-I) and IGF-binding protein-3, and colorectal cancer risk among men. Growth Horm. IGF Res. 10 (2000) S28-29.
• 16. Yu, H., Spitz, M.R., Mistry, J., Gu, J., Hong, W.K. and Wu, X. Plasma levels of insulin-like growth factor-I and lung cancer risk: a case-control analysis. J. Natl. Cancer Inst. 91 (1999) 151-1516.
• 17. Maile, L.A., Imai, Y., Clarke, J.B. and Clemmons, D.R. Insulin-like growth factor I increases alpha Vbeta 3 affinity by increasing the amount of integrin-associated protein that is associated with non-raft domains of the cellular membrane. J. Biol. Chem. 277 (2002) 1800-1805.
• 18. Playford, M.P., Bicknell, D., Bodmer, W.F. and Macaulay, V.M. Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of beta-catenin. Proc. Natl. Acad. Sci. USA. 97 (2000) 12103-12108.
• 19. Sachdev, D., Hartell, J.S., Lee, A.V., Zhang, X. and Yee, D. A dominant negative type I insulin-like growth factor receptor inhibits metastasis of human cancer cells. J. Biol. Chem. 279 (2004) 5017-5024.
• 20. Cockett, M.I., Murphy, G., Birch, M.L., O’Connell, J.P., Crabbe, T., Millican, A.T., Hart, I.R. and Docherty, A.J. Matrix metalloproteinases and metastatic cancer. Biochem. Soc. Symp. 63 (1998) 295-313.
• 21. Kleiner, D.E. and Stetler-Stevenson, W.G. Matrix metalloproteinases and metastasis. Cancer Chemother. Pharmacol. 43 (1999) S42-51.
• 22. Ohbayashi, H. Matrix metalloproteinases in lung diseases. Curr. Protein Pept. Sci. 3 (2002) 409-421.
• 23. Maloney, E.K., McLaughlin, J.L., Dagdigian, N.E., Garrett, L.M., Connors, K.M., Zhou, X.M., Blattler, W.A., Chittenden, T. and Singh, R. An antiinsulin-like growth factor I receptor antibody that is a potent inhibitor of cancer cell proliferation. Cancer Res. 63 (2003) 5073-5083.
• 24. Chernicky, C.L., Yi, L., Tan, H., Gan, S.U. and Ilan, J. Treatment of human breast cancer cells with antisense RNA to the type I insulin-like growth factor receptor inhibits cell growth, suppresses tumorigenesis, alters the metastatic potential, and prolongs survival in vivo. Cancer Gene Ther. 7 (2000) 384-395.
• 25. Dykxhoorn, D.M., Novina, C.D. and Sharp, P.A. Killing the messenger: short RNAs that silence gene expression. Nat. Rev. Mol. Cell Biol. 4 (2003) 457-467.
• 26. Bohula, E.A., Salisbury, A.J., Sohail, M., Playford, M.P., Riedemann, J., Southern, E.M. and Macaulay, V.M. The efficacy of small interfering RNAs targeted to the type 1 insulin-like growth factor receptor (IGF1R) is influenced by secondary structure in the IGF1R transcript. J. Biol. Chem. 278 (2003) 15991-15997.
• 27. Lee, C.T., Park, K.H., Adachi, Y., Seol, J.Y., Yoo, C.G., Kim, Y.W., Han, S.K., Shim, Y.S., Coffee, K., Dikov, M.M. and Carbone, D.P. Recombinant adenoviruses expressing dominant negative insulin-like growth factor-I receptor demonstrate anti-tumor effects on lung cancer. Cancer Gene Ther. 10 (2003) 57-63.
• 28. Zhang, H., Ma, G., Dong, M., Zhao, M., Shen, X., Ma, Z. and Guo, K. Epidermal growth factor promotes invasiveness of pancreatic cancer cells through NF-kappaB-mediated proteinase productions. Pancreas 32 (2006) 101-109.
• 29. Scotlandi, K., Benini, S., Nanni, P., Lollini, P.L., Nicoletti, G., Landuzzi, L., Serra, M., Manara, M.C., Picci, P. and Baldini, N. Blockage of insulin-like growth factor-I receptor inhibits the growth of Ewing’s sarcoma in athymic mice. Cancer Res. 58 (1998) 4127-4131.
• 30. Lee, C.T., Wu, S., Gabrilovich, D., Chen, H., Nadaf-Rahrov, S., Ciernik, I.F. and Carbone, D.P. Anti-tumor effects of an adenovirus expressing antisense insulin-like growth factor I receptor on human lung cancer cell lines. Cancer Res. 56 (1996) 3038-3041.
• 31. Dunn, S.E., Ehrlich, M., Sharp, N.J., Reiss, K., Solomon, G., Hawkins, R., Baserga, R. and Barrett, J.C. A dominant negative mutant of the insulin-like growth factor-I receptor inhibits the adhesion, invasion, and metastasis of breast cancer. Cancer Res. 58 (1998) 3353-3361.
• 32. Zamore, P.D. RNA interference: listening to the sound of silence. Nature Structural Biology. 8 (2001) 746-750.
• 33. Miyagishi, M. and Taira, K. U6 promoter-driven siRNAs with four uridine 3’ overhangs efficiently suppress targeted gene expression in mammalian cells. Nature Biotechnology 20 (2002) 497-500.
• 34. Dong, A.Q., Kong, M.J., Ma, Z.Y., Qian, J.F. and Xu, X.H. Downregulation of IGF-IR using small, interfering, hairpin RNA (siRNA) inhibits growth of human lung cancer cell line A549 in vitro and in nude mice. Cell Biol. Int. 31 (2007) 500-507.
• 35. Dunn, S.E., Torres, J.V., Oh, J.S., Cykert, D.M. and Barrett, J.C. Upregulation of urokinase-type plasminogen activator by insulin-like growth factor-I depends upon phosphatidylinositol-3 kinase and mitogen-activated protein kinase kinase. Cancer Res. 61 (2001) 1367-1374.
• 36. Salatino, M., Schillaci, R., Proietti, C.J., Carnevale, R., Frahm, I., Molinolo, A.A., Iribarren, A., Charreau, E.H. and Elizalde, P.V. Inhibition of in vivo breast cancer growth by antisense oligodeoxynucleotides to type I insulinlike growth factor receptor mRNA involves inactivation of ErbBs, PI- 3K/Akt and p42/p44 MAPK signaling pathways but not modulation of progesterone receptor activity. Oncogene. 23 (2004) 5161-5174.
• 37. Tai, Y.T., Podar, K., Catley, L., Tseng, Y.H., Akiyama, M., Shringarpure, R., Burger, R., Hideshima, T., Chauhan, D., Mitsiades, N., Richardson, P., Munshi, N.C., Kahn, C.R., Mitsiades, C. and Anderson, K.C. Insulin-like growth factor-1 induces adhesion and migration in human multiple myeloma cells via activation of beta1-integrin and phosphatidylinositol 3’- kinase/AKT signaling. Cancer Res. 63 (2003) 5850-5858.
• 38. Muller, D., Breathnach, R., Engelmann, A., Millon, R., Bronner, G., Flesch, H., Dumont, P., Eber, M. and Abecassis, J. Expression of collagenaserelated metalloproteinase genes in human lung or head and neck tumours. Int. J. Cancer. 48 (1991) 550-556.
• 39. Kanayama, H., Yokota, K., Kurokawa, Y., Murakami, Y., Nishitani, M. and Kagawa, S. Prognostic values of matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-2 expression in bladder cancer. Cancer 82 (1998) 1359-1366.
• 40. Schmitt, M., Harbeck, N., Thomssen, C., Wilhelm, O., Magdolen, V., Reuning, U., Ulm, K., Hofler, H., Janicke, F. and Graeff, H. Clinical impact of the plasminogen activation system in tumor invasion and metastasis: prognostic relevance and target for therapy. Thromb. Haemost. 78 (1997) 285-296.
• 41. Pulukuri, S.M., Gondi, C.S., Lakka, S.S., Jutla, A., Estes, N., Gujrati, M. and Rao, J.S. RNA interference-directed knockdown of urokinase plasminogen activator and urokinase plasminogen activator receptor inhibits prostate cancer cell invasion, survival, and tumorigenicity in vivo. J. Biol. Chem. 280 (2005) 36529-36540.
• 42. Kondraganti, S., Mohanam. S., Chintala, S.K., Kin, Y., Jasti, S.L., Nirmala, C., Lakka, S.S., Adachi, Y., Kyritsis, A.P., Ali-Osman, F., Sawaya, R., Fuller, G.N. and Rao, J.S. Selective suppression of matrix metalloproteinase-9 in human glioblastoma cells by antisense gene transfer impairs glioblastoma cell invasion. Cancer Res. 60 (2000) 6851-6855.
• 43. Grzmil, M., Hemmerlein, B., Thelen, P., Schweyer, S. and Burfeind, P. Blockade of the type I IGF receptor expression in human prostate cancer cells inhibits proliferation and invasion, up-regulates IGF binding protein-3, and suppresses MMP-2 expression. J. Pathol. 202 (2004) 50-59.