Adenovirus vector-mediated Gli1 siRNA induces growth inhibition and apoptosis in human pancreatic cancer with Smo-dependent or Smo-independent Hh pathway activation in vitro and in vivo

Cancer Letters

Volumn 339, Issue 2, 2013, Pages 185-194

  Guo, Jiefang ^a   Gao, Jun ^a   Li, Zhaoshen ^a   Gong, Yanfang ^a   Man, Xiaohua ^a   Jin, Jing ^a   Wu, Hongyu ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Adenovirus vector; Gli1; Hedgehog signaling; Pancreatic cancer; SiRNA

Indexed keywords

ADENOVIRUS VECTOR; CYCLIN D2; PROTEIN BCL 2; PROTEIN PATCHED 1; SMALL INTERFERING RNA; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BCL 2 GENE; CANCER INHIBITION; CELL CYCLE G0 PHASE; CLINICAL ARTICLE; CONTROLLED STUDY; CYCLIN D2 GENE; EPITHELIUM; G1 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; GLI1 GENE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PANCREAS CANCER; PANCREAS DUCT; PANCREATIC DUCTAL EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PTCH1 GENE; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ADENOVIRUS VECTOR; GLI1; HEDGEHOG SIGNALING; PANCREATIC CANCER; SIRNA;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN D2; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENETIC VECTORS; HEDGEHOG PROTEINS; HUMANS; MICE; ONCOGENE PROTEINS; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

ADENOVIRIDAE; ERINACEIDAE; MUS MUSCULUS;

EID: 84883824170     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.06.010     Document Type: Article

References (35)

1. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J. Clin. 2011, 61:69-90.
2. Jones S., Zhang X., Parsons D.W., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Kamiyama H., Jimeno A., Hong S.M., Fu B., Lin M.T., Calhoun E.S., Kamiyama M., Walter K., Nikolskaya T., Nikolsky Y., Hartigan J., Smith D.R., Hidalgo M., Leach S.D., Klein A.P., Jaffee E.M., Goggins M., Maitra A., Iacobuizo-Donahue C., Eshelman J.R., Kern S.E., Hruban R.H., Karchin R., Papadopoulos N., Parmigiani G., Bogelstein B., Velculescu V.E., Kinzler K.W. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806.
3. Hidalgo M., Maitra A. The hedgehog pathway and pancreatic cancer. New Engl. J. Med. 2009, 361:2094-2096.
4. Kelleher F.C. Hedgehog signaling and therapeutics in pancreatic cancer. Carcinogenesis 2011, 32:445-451.
5. Ng J.M., Curran T. The Hedgehog's tale: developing strategies for targeting cancer. Nat. Rev. Cancer 2011, 11:493-501.
6. Kar S., Deb M., Sengupta D., Shilpi A., Bhutia S.K., Patra S.K. Intricacies of hedgehog signaling pathways: a perspective in tumorigenesis. Exp. Cell Res. 2012, 318:1959-1972.
7. Di Marco M., Macchini M., Vecchiarelli S., Sina S., Biasco G. Hedgehog signaling: from the cuirass to the heart of pancreatic cancer. Pancreatology 2012, 12:388-393.
8. Rosow D.E., Liss A.S., Strobel O., Fritz S., Bausch D., Valsangkar N.P., Alsina J., Kulemann B., Park J.K., Yamaguchi J., LaFemina J., Thayer S.P. Sonic Hedgehog in pancreatic cancer: from bench to bedside, then back to the bench. Surgery 2012, 152:S19-S32.
9. Thayer S.P., di Magliano M.P., Heiser P.W., Nielsen C.M., Roberts D.J., Lauwers G.Y., Qi Y.P., Gysin S., Fernandez-del Castillo C., Yajnik V., Antoniu B., McMahon M., Warshaw A.L., Hebrok M. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 2003, 425:851-856.
10. Feldmann G., Fendrich V., McGovern K., Bedja D., Bisht S., Alvarez H., Koorstra J.B., Habbe N., Karikari C., Mullendore M., Gabrielson K.L., Sharma R., Matsui W., Maitra A. An orally bioavailable small-molecule inhibitor of Hedgehog signaling inhibits tumor initiation and metastasis in pancreatic cancer. Mol. Cancer Ther. 2008, 7:2725-2735.
11. Lauth M., Toftgård R. Non-canonical activation of GLI transcription factors: implications for targeted anti-cancer therapy. Cell Cycle 2007, 6:2458-2463.
12. Stecca B., Ruiz I Altaba A. Context-dependent regulation of the GLI code in cancer by HEDGEHOG and non-HEDGEHOG signals. J. Mol. Cell Biol. 2010, 2:84-95.
13. Gao J., Li Z., Chen Z., Shao J., Zhang L., Xu G., Tu Z., Gong Y. Antisense SMO under the control of the PTCH1 promoter delivered by an adenoviral vector inhibits the growth of human pancreatic cancer. Gene Ther. 2006, 13:1587-1594.
14. Morris J.P., Wang W.S., Hebrok M. KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma. Nat. Rev. Cancer 2010, 10:683-695.
15. Wang Y., Ding Q., Yen C.J., Xia W., Izzo J.G., Lang J.Y., Li C.W., Hsu J.L., Miller S.A., Wang X., Lee D.F., Hsu J.M., Huo L., Labaff A.M., Liu D., Huang T.H., Lai C.C., Tsai F.J., Chang W.C., Chen C.H., Wu T.T., Buttar N.S., Wang K.K., Wu Y., Wang H., Ajani J., Hung M.C. The crosstalk of mTOR/S6K1 and Hedgehog pathways. Cancer Cell 2012, 21:374-387.
16. Aberger F., Kern D., Greil R., Hartmann T.N. Canonical and noncanonical Hedgehog/GLI signaling in hematological malignancies. Vitam. Horm. 2012, 88:25-54.
17. Blotta S., Jakubikova J., Calimeri T., Roccaro A.M., Amodio N., Azab A.K., Foresta U., Mitsiades C.S., Rossi M., Todoerti K., Molica S., Morabito F., Neri A., Tagliaferri P., Tassone P., Anderson K.C., Munshi N.C. Canonical and noncanonical Hedgehog pathway in the pathogenesis of multiple myeloma. Blood 2012, 120:5002-5013.
18. Gao J., Khan A.A., Shimokawa T., Zhan J., Strömblad S., Fang W., Zhang H. A feedback regulation between Kindlin-2 and GLI1 in prostate cancer cells. FEBS Lett. 2013, 587:631-638.
19. Nolan-Stevaux O., Lau J., Truitt M.L., Chu G.C., Hebrok M., Fernandez-Zapico M.E., Hanahan D. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev. 2009, 23:24-36.
20. Kasper M., Regl G., Frischauf A.M., Aberger F. GLI transcription factors: mediators of oncogenic Hedgehog signaling. Eur. J. Cancer 2006, 42:437-445.
21. Luo J., Deng Z.L., Luo X., Tang N., Song W.X., Chen J., Sharff K.A., Luu H.H., Haydon R.C., Kinzler K.W., Vogelstein B., He T.C. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat. Protoc. 2007, 2:1236-1247.
22. He X.P., Su C.Q., Wang X.H., Pan X., Tu Z.X., Gong Y.F., Gao J., Liao Z., Jin J., Wu H.Y., Man X.H., Li Z.S. E1B-55kD-deleted oncolytic adenovirus armed with canstatin gene yields an enhanced anti-tumor efficacy on pancreatic cancer. Cancer Lett. 2009, 285:89-98.
23. Raj L., Ide T., Gurkar A.U., Foley M., Schenone M., Li X., Tolliday N.J., Golub T.R., Carr S.A., Shamji A.F., Stern A.M., Mandinova A., Schreiber S.L., Lee S.W. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 2011, 475:231-234.
24. Talley L., Chhieng D.C., Bell W.C., Grizzle W.E., Frost A.R. Immunohistochemical detection of EGFR, p185(erbB-2), Bcl-2 and p53 in breast carcinomas in pre-menopausal and post-menopausal women. Biotech. Histochem. 2008, 83:5-14.
25. Xu L., Kwon Y.J., Frolova N., Steg A.D., Yuan K., Johnson M.R., Grizzle W.E., Desmond R.A., Frost A.R. GLI1 promotes cell survival and is predictive of a poor outcome in ERalpha-negative breast cancer. Breast Cancer Res. Treat. 2010, 123:59-71.
26. Li J., Ramani K., Sun Z., Zee C., Grant E.G., Yang H., Xia M., Oh P., Ko K., Mato J.M., Lu S.C. Forced expression of methionine adenosyltransferase 1A in human hepatoma cells suppresses in vivo tumorigenicity in mice. Am. J. Pathol. 2010, 176:2456-2466.
27. Shao J., Zhang L., Gao J., Li Z., Chen Z. Aberrant expression of PTCH (patched gene) and Smo (smoothened gene) in human pancreatic cancerous tissues and its association with hyperglycemia. Pancreas 2006, 33:38-44.
28. Desch P., Asslaber D., Kern D., Schnidar H., Mangelberger D., Alinger B., Stoecher M., Hofbauer S.W., Neureiter D., Tinhofer I., Aberger F., Hartmann T.N., Greil R. Inhibition of GLI, but not Smoothened, induces apoptosis in chronic lymphocytic leukemia cells. Oncogene 2010, 29:4885-4895.
29. Mazumdar T., DeVecchio J., Agyeman A., Shi T., Houghton J.A. The GLI genes as the molecular switch in disrupting Hedgehog signaling in colon cancer. Oncotarget 2011, 2:638-645.
30. Siomi H., Siomi M.C. On the road to reading the RNA-interference code. Nature 2009, 457:396-404.
31. Hu P.F., Chen H., Zhong W., Lin Y., Zhang X., Chen Y.X., Xie W.F. Adenovirus-mediated transfer of siRNA against PAI-1 mRNA ameliorates hepatic fibrosis in rats. J. Hepatol. 2009, 51:102-113.
32. Wang Y., Wu N.N., Mu Y.Q., Zhang R.X., Hu M., Li R.D., Chen L., He B.C., Deng Z.L. The effect of adenovirus-mediated siRNA targeting BMPR-II on UHMWPE-induced osteoclast formation. Biomaterials 2013, 34:150-159.
33. Korrapati A.B., Swaminathan G., Singh A., Khanna N., Swaminathan S. Adenovirus delivered short hairpin RNA targeting a conserved site in the 5' non-translated region inhibits all four serotypes of dengue viruses. PLoS Negl. Trop. Dis. 2012, 6:e1735.
34. Bigelow R.L., Chari N.S., Unden A.B., Spurgers K.B., Lee S., Roop D.R., Toftgard R., McDonnell T.J. Transcriptional regulation of bcl-2 mediated by the sonic hedgehog signaling pathway through gli-1. J. Biol. Chem. 2004, 279:1197-1205.
35. Shahi M.H., Afza M., Sinha S., Eberhart C.G., Rey J.A., Fan X., Castresana J.S. Regulation of sonic hedgehog-GLI1 downstream target genes PTCH1, Cyclin D2, Plakoglobin, PAX6 and NKX2.2 and their epigenetic status in medulloblastoma and astrocytoma. BMC Cancer 2010, 10:614-633.