Therapeutic potential of human mesenchymal stem cells producing IL-12 in a mouse xenograft model of renal cell carcinoma

Cancer Letters

Volumn 290, Issue 2, 2010, Pages 157-166

  Gao, Peng ^a   Ding, Qiang ^a   Wu, Zhong ^a   Jiang, Haowen ^a   Fang, Zujun ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Gene therapy; Interleukin 12; Mesenchymal stem cells; Renal cell carcinoma

Indexed keywords

ADENOVIRUS VECTOR; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; KIDNEY CARCINOMA; MALE; MESENCHYMAL STEM CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; NUDE MOUSE; PHENOTYPE; PRIORITY JOURNAL; SINGLE DRUG DOSE; TUMOR XENOGRAFT; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; CARCINOMA, RENAL CELL; CHEMOKINE CXCL10; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE THERAPY; GENETIC VECTORS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-2; KIDNEY NEOPLASMS; KILLER CELLS, NATURAL; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MICE, NUDE; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MURINAE; MUS MUSCULUS;

EID: 77649185403     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.08.031     Document Type: Article

References (43)

1. Fernandez N.C., Levraud J.P., Haddada H., Perricaudet M., and Kourilsky P. High frequency of specific CD8+ T cells in the tumor and blood is associated with efficient local IL-12 gene therapy of cancer. J. Immunol. 162 (1999) 609-617
2. Lode H.N., Dreier T., Xiang R., Varki N.M., Kang A.S., and Reisfeld R.A. Gene therapy with a single chain interleukin 12 fusion protein induces T cell-dependent protective immunity in a syngeneic model of murine neuroblastoma. Proc. Natl. Acad. Sci. USA. 95 (1998) 2475-2480
3. Yao L., Sgadari C., Furuke K., Bloom E.T., Teruya-Feldstein J., and Tosato G. Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood 93 (1999) 1612-1621
4. Watanabe M., Fenton R.G., Wigginton J.M., McCormick K.L., Volker K.M., Fogler W.E., Roessler P.G., and Wiltrout R.H. Intradermal delivery of IL-12 naked DNA induces systemic NK cell activation and Th1 response in vivo that is independent of endogenous IL-12 production. J. Immunol. 163 (1999) 1943-1950
5. Rakhmilevich A.L., Janssen K., Hao Z., Sondel P.M., and Yang N.S. Interleukin 12 gene therapy of a weakly immunogenic mouse mammary carcinoma results in reduction of spontaneous lung metastases via a T cell-independent mechanism. Cancer Gene Ther. 7 (2000) 826-838
6. Cui J., Shin T., Kawano T., Sato H., Kondo E., Toura I., Kaneko Y., Koseki H., Kanno M., and Taniguchi M. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 278 (1997) 1623-1626
7. Tannenbaum C.S., Wicker N., Armstrong D., Tubbs R., Finke J., Bukowski R.M., and Hamilton T.A. Cytokine and chemokine expression in tumors of mice receiving systemic therapy with IL-12. J. Immunol. 156 (1996) 693-699
8. Tannenbaum C.S., Tubbs R., Armstrong D., Finke J.H., Bukowski R.M., and Hamilton T.A. The CXC chemokines IP-10 and Mig are necessary for IL-12-mediated regression of the mouse RENCA tumor. J. Immunol. 161 (1998) 927-932
9. Kobayashi M., Fitz L., Ryan M., Hewick R.M., Clark S.C., Chan S., Loudon R., Sherman F., Perussia B., and Trinchieri G. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med. 170 (1989) 827-845
10. Wolf S.F., Temple P.A., Kobayashi M., Young D., Dicig M., Lowe L., Dzialo R., Fitz L., Ferenz C., Hewick R.M., Kelleher K., Herrmann S.H., Clark S.C., Azzoni L., Chan S.H., Trinchieri G., and Perussia B. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J. Immunol. 146 (1991) 3074-3081
11. Nastala C.L., Edington H.D., McKinney T.G., Tahara H., Nalesnik M.A., Brunda M.J., Gately M.K., Wolf S.F., Schreiber R.D., Storkus W.J., and Lotze M.T. Recombinant IL-12 administration induces tumor regression in associated with IFN-γ production. J. Immunol. 153 (1994) 1697-1706
12. Rakhmilevich A.L., Turner J., Ford M.J., McCabe D., Sun W.H., Sondel P.M., Grota K., and Yang N.S. Gene gun-mediated skin transfection with interleukin 12 gene results in regression of established primary and metastatic murine tumors. Proc. Natl. Acad. Sci. USA. 93 (1996) 6291-6296
13. Watanabe M., Fenton R.G., Wigginton J.M., McCormick K.L., Volker K.M., Fogler W.E., Roessler P.G., and Wiltrout R.H. Intradermal delivery of IL-12 naked DNA induces systemic NK cell activation and Th1 response in vivo that is independent of endogenous IL-12 production. J. Immunol. 163 (1999) 1943-1950
14. Tahara H., Zitvogel L., Storkus W.J., Robbins P.D., and Lotze M.T. Murine models of cancer cytokine gene therapy using interleukin-12. Ann. NY Acad. Sci. 795 (1996) 275-283
15. Golab J., and Zagozdzon R. Antitumor effects of interleukin-12 in pre-clinical and early clinical studies. Int. J. Mol. Med. 3 (1999) 537-544
16. Rook A.H., Wood G.S., Yoo E.K., Elenitsas R., Kao D.M., Sherman M.L., Witmer W.K., Rockwell K.A., Shane R.B., Lessin S.R., and Vonderheid E.C. Interleukin-12 therapy of cutaneous T-cell lymphoma induces lesion regression and cytotoxic T-cell responses. Blood 94 (1999) 902-908
17. Marshall E. Cancer trial of interleukin-12 halted. Science 268 1995 (1555)
18. Car B.D., Eng V.M., Lipman J.M., and Anderson T.D. The toxicology of interleukin-12: a review. Toxicol. Pathol. 27 (1999) 58-63
19. Saffran D.C., Horton H.M., Yankauckas M.A., Anderson D., Barnhart K.M., Abai A.M., Hobart P., Manthorpe M., Norman J.A., and Parker S.E. Immunotherapy of established tumors in mice by intratumoral injection of interleukin-2 plasmid DNA: induction of CD8+ T-cell immunity. Cancer. Gene Ther. 5 (1998) 321-330
20. Colombo M.P., Vagliani M., Spreafico F., Parenza M., Chiodoni C., Melani C., and Stoppacciaro A. Amount of interleukin 12 available at the tumor site is critical for tumor regression. Cancer Res. 56 (1996) 2531-2534
21. Rakhmilevich A.L., Timmins J.G., Janssen K., Pohlmann E.L., Sheehy M.J., and Yang N.S. Gene gun-mediated IL-12 gene therapy induces antitumor effects in the absence of toxicity: a direct comparison with systemic IL-12 protein therapy. J. Immunother. 22 (1999) 135-144
22. Schultz J., Heinzerling L., Pavlovic J., and Moelling K. Induction of long-lasting cytokine effect by injection of IL-12 encoding plasmid DNA. Cancer Gene Ther. 7 (2000) 1557-1565
23. Tahara H., Zeh H.J., Storkus W.J., Pappo I., Watkins S.C., Gubler U., Wolf S.F., Robbins P.D., and Lotze M.T. Fibroblasts genetically engineered to secrete interleukin 12 can suppress tumor growth and induce antitumor immunity to a murine melanoma in vivo. Cancer Res. 54 (1994) 182-189
24. Chen L., Chen D., Block E., O'Donnell M., Kufe D.W., and Clinton S.K. Eradication of murine bladder carcinoma by intratumoral injection of a bicistronic adenoviral vector carrying cDNAs for the IL-12 heterodimer and its inhibition by the IL-12 p40 subunit homodimer. J. Immunol. 159 (1997) 351-359
25. Meko J.B., Yim J.H., Tsung K., and Norton J.A. High cytokine production and effective antitumor activity of a recombinant vaccinia virus encoding murine interleukin 12. Cancer Res. 55 (1995) 4765-4770
26. Nauta A.J., Kruisselbrink A.B., Lurvink E., Willemze R., and Fibbe W.E. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J. Immunol. 177 (2006) 2080-2087
27. Ryan J.M., Barry F.P., Murphy J.M., and Mahon B.P. Mesenchymal stem cells avoid allogeneic rejection. J. Inflamm. 2 (2005) 8-19
28. Stoff-Khalili M.A., Rivera A.A., Mathis J.M., Banerjee N.S., Moon A.S., Hess A., Rocconi R.P., Numnum T.M., Everts M., Chow L.T., Douglas J.T., Siegal G.P., Zhu Z.B., Bender H.G., Dall P., Stoff A., Pereboeva L., and Curiel D.T. Mesenchymal stem cells as a vehicle for targeted delivery of CRAds to lung metastases of breast carcinoma. Breast Cancer Res. Treat. 105 (2007) 157-167
29. Nakamura K., Ito Y., Kawano Y., Kurozumi K., Kobune M., Tsuda H., Bizen A., Honmou O., Niitsu Y., and Hamada H. Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther. 11 (2004) 1155-1164
30. Hung S.C., Deng W.P., Yang W.K., Liu R.S., Lee C.C., Su T.C., Lin R.J., Yang D.M., Chang C.W., Chen W.H., Wei H.J., and Gelovani J.G. Mesenchymal stem cell targeting of microscopic tumors and tumor stroma development monitored by noninvasive in vivo positron emission tomography imaging. Clin. Cancer Res. 11 (2005) 7749-7756
31. Komarova S., Kawakami Y., Stoff-Khalili M.A., Curiel D.T., and Pereboeva L. Mesenchymal progenitor cells as cellular vehicles for delivery of oncolytic adenoviruses. Mol. Cancer Ther. 5 (2006) 755-766
32. Igarashi M., Yogiashi Y., Mihara M., Takada I., Kitagawa H., and Kato S. Vitamin K induces osteoblast differentiation through pregnane X receptor-mediated transcriptional control of the Msx2 gene. Mol. Cell Biol. 27 (2007) 7947-7954
33. Meirelles L.D., and Nardi N.B. Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Br. J. Haematol. 123 (2003) 702-711
34. Phinney D.G., Kopen G., Isaacson R.L., and Prockop D.J. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J. Cell. Biochem. 72 (1999) 570-585
35. Sotiropoulou P.A., Perez S.A., Salagianni M., Baxevanis C.N., and Papamichail M. Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells. Stem Cells 24 (2006) 462-471
36. Elzaouk L., Moelling K., and Pavlovic J. Anti-tumor activity of mesenchymal stem cells producing IL-12 in a mouse melanoma model. Exp. Dermatol. 15 (2006) 865-874
37. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
38. Studeny M., Marini F.C., Champlin R.E., Zompetta C., Fidler I.J., and Andreeff M. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res. 62 (2002) 3603-3608
39. Ogawa M., Yu W.G., Umehara K., Iwasaki M., Wijesuriya R., Tsujimura T., Kubo T., Fujiwara H., and Hamaoka T. Multiple roles of interferon-gamma in the mediation of interleukin 12-induced tumor regression. Cancer Res. 58 (1998) 2426-2432
40. Kondadasula S.V., Roda J.M., Parihar R., Yu J., Lehman A., Caligiuri M.A., Tridandapani S., Burry R.W., and Carson W.E. Colocalization of the IL-12 receptor and FcgammaRIIIa to natural killer cell lipid rafts leads to activation of ERK and enhanced production of interferon-gamma. Blood 111 (2008) 4173-4183
41. Strieter R.M., Kunkel S.L., Arenberg D.A., Burdick M.D., and Polverini P.J. Interferon γ-inducible protein 10 (IP-10), a member of the C-X-C chemokine family, is an inhibitor of angiogenesis. Biochem. Biophys. Res. Commun. 210 (1995) 51-57
42. Gao J., Dennis J.E., Muzic R.F., Lundberg M., and Caplan A.I. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues, Organs 169 (2001) 12-20
43. Ren C., Kumar S., Chanda D., Kallman L., Chen J., Mountz J.D., and Ponnazhagan S. Cancer gene therapy using mesenchymal stem cells expressing interferon-beta in a mouse prostate cancer lung metastasis model. Gene Ther. 15 (2008) 1446-1453