Rac1 is required for oncolytic NDV replication in human cancer cells and establishes a link between tumorigenesis and sensitivity to oncolytic virus

Oncogene

Volumn 29, Issue 15, 2010, Pages 2205-2216

  Puhlmann, J ^a,b   Puehler, F ^a   Mumberg, D ^a   Boukamp, P ^c   Beier, R ^a  

^a BAYER PHARMA AG   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Interferon; Newcastle disease virus; Oncolytic; Rac1; Ras; Transformation

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON; INTERFERON; ONCOLYTIC VIRUS; RAC1 PROTEIN; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT2 PROTEIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; NEWCASTLE DISEASE PARAMYXOVIRUS; ONCOGENE H RAS; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS REPLICATION;

CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; NEOPLASMS; NEWCASTLE DISEASE VIRUS; ONCOLYTIC VIRUSES; RAC1 GTP-BINDING PROTEIN; RAS PROTEINS; RNA, SMALL INTERFERING; VIRUS REPLICATION;

NEWCASTLE DISEASE VIRUS;

EID: 77951076912     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.507     Document Type: Article

References (42)

1. Balachandran S, Barber GN. (2004). Defective translational control facilitates vesicular stomatitis virus oncolysis. Cancer Cell 5: 51-65.
2. Bergmann M, Romirer I, Sachet M, Fleischhacker R, Garcia-Sastre A, Palese P et al. (2001). A genetically engineered influenza A virus with ras-dependent oncolytic properties. Cancer Res 61: 8188-8193.
3. Bosco EE, Mulloy JC, Zheng Y. (2009). Rac1 GTPase: a 'Rac' of all trades. Cell Mol Life Sci 66: 370-374.
4. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. (1988). Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106: 761-771.
5. Boukamp P, Stanbridge EJ, Foo DY, Cerutti PA, Fusenig NE. (1990). c-Ha-ras oncogene expression in immortalized human keratinocytes (HaCaT) alters growth potential in vivo but lacks correlation with malignancy. Cancer Res 50: 2840-2847.
6. Cassel WA, Garrett RE. (1965). Relationship between viral neurotropism and oncolysis. II. Study of influenza virus. Cancer 18: 863-868.
7. Chan AY, Coniglio SJ, Chuang YY, Michaelson D, Knaus UG, Philips MR et al. (2005). Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 24: 7821-7829.
8. Darnell Jr JE., Kerr IM, Stark GR. (1994). Role of STAT2 in the alpha interferon signaling pathway. Science 264: 1415-1421.
9. Espina C, Cespedes MV, Garcia-Cabezas MA, Gomez del Pulgar MT, Boluda A, Oroz LG et al. (2008). A critical role for Rac1 in tumor progression of human colorectal adenocarcinoma cells. Am J Pathol 172: 156-166.
10. Farassati F, Yang AD, Lee PW. (2001). Oncogenes in Ras signalling pathway dictate host-cell permissiveness to herpes simplex virus 1. Nat Cell Biol 3: 745-750.
11. Fiola C, Peeters B, Fournier P, Arnold A, Bucur M, Schirrmacher V. (2006). Tumor selective replication of Newcastle disease virus: association with defects of tumor cells in antiviral defence. Int J Cancer 119: 328-338.
12. Fusenig NE, Boukamp P. (1998). Multiple stages and genetic alterations in immortalization, malignant transformation, and tumor progression of human skin keratinocytes. Mol Carcinog 23: 144-158.
13. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. (2004). Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 101: 7618-7623.
14. Gros A, Martinez-Quintanilla J, Puig C, Guedan S, Mollevi DG, Alemany R et al. (2008). Bioselection of a gain of function mutation that enhances adenovirus 5 release and improves its antitumoral potency. Cancer Res 68: 8928-8937.
15. Hancock JF. (2003). Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 4: 373-384.
16. Hoppe S, Schelhaas M, Jaeger V, Liebig T, Petermann P, Knebel-Morsdorf D. (2006). Early herpes simplex virus type 1 infection is dependent on regulated Rac1/Cdc42 signalling in epithelial MDCKII cells. J Gen Virol 87: 3483-3494.
17. Hotte SJ, Lorence RM, Hirte HW, Polawski SR, Bamat MK, ONeil JD et al. (2007). An optimized clinical regimen for the oncolytic virus PV701. Clin Cancer Res 13: 977-985.
18. Khosravi-Far R, Solski PA, Clark GJ, Kinch MS, Der CJ. (1995). Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation. Mol Cell Biol 15: 6443-6453.
19. Kissil JL, Walmsley MJ, Hanlon L, Haigis KM, Bender Kim CF, Sweet-Cordero A et al. (2007). Requirement for Rac1 in a K-ras induced lung cancer in the mouse. Cancer Res 67: 8089-8094.
20. Krishnamurthy S, Takimoto T, Scroggs RA, Portner A. (2006). Differentially regulated interferon response determines the outcome of Newcastle disease virus infection in normal and tumor cell lines. J Virol 80: 5145-5155.
21. Kwei KA, Finch JS, Ranger-Moore J, Bowden GT. (2006). The role of Rac1 in maintaining malignant phenotype of mouse skin tumor cells. Cancer Lett 231: 326-338.
22. Lorence RM, Katubig BB, Reichard KW, Reyes HM, Phuangsab A, Sassetti MD et al. (1994). Complete regression of human fibrosarcoma xenografts after local Newcastle disease virus therapy. Cancer Res 54: 6017-6021. (Pubitemid 24378619)
23. Lu X, Wu X, Plemenitas A, Yu H, Sawai ET, Abo A et al. (1996). CDC42 and Rac1 are implicated in the activation of the Nef-associated kinase and replication of HIV-1. Curr Biol 6: 1677-1684.
24. Mueller MM, Peter W, Mappes M, Huelsen A, Steinbauer H, Boukamp P et al. (2001). Tumor progression of skin carcinoma cells in vivo promoted by clonal selection, mutagenesis, and autocrine growth regulation by granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor. Am J Pathol 159: 1567-1579.
25. Mundschau LJ, Faller DV. (1992). Oncogenic ras induces an inhibitor of double-stranded RNA-dependent eukaryotic initiation factor 2 alpha-kinase activation. J Biol Chem 267: 23092-23098.
26. Norman KL, Hirasawa K, Yang AD, Shields MA, Lee PW. (2004). Reovirus oncolysis: the Ras/RalGEF/p38 pathway dictates host cell permissiveness to reovirus infection. Proc Natl Acad Sci USA 101: 11099-11104.
27. Noser JA, Mael AA, Sakuma R, Ohmine S, Marcato P, Wk Lee P et al. (2007). The RAS/Raf1/MEK/ERK signaling pathway facilitates VSV-mediated oncolysis: implication for the defective interferon response in cancer cells. Mol Ther 15: 1531-1536.
28. Pecora AL, Rizvi N, Cohen GI, Meropol NJ, Sterman D, Marshall JL et al. (2002). Phase I trial of intravenous administration of PV701, an oncolytic virus, in patients with advanced solid cancers. J Clin Oncol 20: 2251-2266.
29. Puhler F, Willuda J, Puhlmann J, Mumberg D, Romer-Oberdorfer A, Beier R. (2008). Generation of a recombinant oncolytic Newcastle disease virus and expression of a full IgG antibody from two transgenes. Gene Ther 15: 371-383.
30. Reichard KW, Lorence RM, Cascino CJ, Peeples ME, Walter RJ, Fernando MB et al. (1992). Newcastle disease virus selectively kills human tumor cells. J Surg Res 52: 448-453.
31. Saeed MF, Kolokoltsov AA, Freiberg AN, Holbrook MR, Davey RA. (2008). Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. PLoS Pathog 4: e1000141.
32. Schirrmacher V, Fournier P. (2009). Newcastle disease virus: a promising vector for viral therapy, immune therapy, and gene therapy of cancer. Methods Mol Biol 542: 565-605.
33. Schowalter RM, Wurth MA, Aguilar HC, Lee B, Moncman CL, McCann RO et al. (2006). Rho GTPase activity modulates paramyxovirus fusion protein-mediated cell-cell fusion. Virology 350: 323-334.
34. Singh A, Karnoub AE, Palmby TR, Lengyel E, Sondek J, Der CJ. (2004). Rac1b, a tumor associated, constitutively active Rac1 splice variant, promotes cellular transformation. Oncogene 23: 9369-9380.
35. Sinkovics JG, Horvath JC. (2000). Newcastle disease virus (NDV): brief history of its oncolytic strains. J Clin Virol 16: 1-15.
36. Smith KD, Mezhir JJ, Bickenbach K, Veerapong J, Charron J, Posner MC et al. (2006). Activated MEK suppresses activation of PKR and enables efficient replication and in vivo oncolysis by Deltagamma(1)34.5 mutants of herpes simplex virus 1. J Virol 80: 1110-1120.
37. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. (1998). How cells respond to interferons. Annu Rev Biochem 67: 227-264.
38. Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N et al. (2000). Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat Med 6: 821-825.
39. Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW. (1998). The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. Embo J 17: 3351-3362.
40. Tang Y, Yu J, Field J. (1999). Signals from the Ras, Rac, and Rho GTPases converge on the Pak protein kinase in Rat-1 fibroblasts. Mol Cell Biol 19: 1881-1891.
41. Wheelock EF, Dingle JH. (1964). Observations on the repeated administration of viruses to a patient with acute leukemia. A preliminary report. N Engl J Med 271: 645-651.
42. Wilden H, Fournier P, Zawatzky R, Schirrmacher V. (2009). Expression of RIG-I, IRF3, IFN-beta and IRF7 determines resistance or susceptibility of cells to infection by Newcastle Disease Virus. Int J Oncol 34: 971-982.