Cancer Letters
Volume 290, Issue 2 , Pages 157-166 , 28 April 2010

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

Received 30 May 2009 ,Revised 1 August 2009 ,Accepted 31 August 2009.

References 

  1. Fernandez NC, Levraud JP, Haddada H, Perricaudet M, 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. 1999;162:609–617
  2. Lode HN, Dreier T, Xiang R, Varki NM, Kang AS, Reisfeld RA. 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. 1998;95:2475–2480
  3. Yao L, Sgadari C, Furuke K, Bloom ET, Teruya-Feldstein J, Tosato G. Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood. 1999;93:1612–1621
  4. Watanabe M, Fenton RG, Wigginton JM, McCormick KL, Volker KM, Fogler WE, et al. 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. 1999;163:1943–1950
  5. Rakhmilevich AL, Janssen K, Hao Z, Sondel PM, Yang NS. 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. 2000;7:826–838
  6. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, et al. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science. 1997;278:1623–1626
  7. Tannenbaum CS, Wicker N, Armstrong D, Tubbs R, Finke J, Bukowski RM, et al. Cytokine and chemokine expression in tumors of mice receiving systemic therapy with IL-12. J. Immunol. 1996;156:693–699
  8. Tannenbaum CS, Tubbs R, Armstrong D, Finke JH, Bukowski RM, Hamilton TA. The CXC chemokines IP-10 and Mig are necessary for IL-12-mediated regression of the mouse RENCA tumor. J. Immunol. 1998;161:927–932
  9. Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med. 1989;170:827–845
  10. Wolf SF, Temple PA, Kobayashi M, Young D, Dicig M, Lowe L, et al. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J. Immunol. 1991;146:3074–3081
  11. Nastala CL, Edington HD, McKinney TG, Tahara H, Nalesnik MA, Brunda MJ, et al. Recombinant IL-12 administration induces tumor regression in associated with IFN-γ production. J. Immunol. 1994;153:1697–1706
  12. Rakhmilevich AL, Turner J, Ford MJ, McCabe D, Sun WH, Sondel PM, et al. Gene gun-mediated skin transfection with interleukin 12 gene results in regression of established primary and metastatic murine tumors. Proc. Natl. Acad. Sci. USA. 1996;93:6291–6296
  13. Watanabe M, Fenton RG, Wigginton JM, McCormick KL, Volker KM, Fogler WE, et al. 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. 1999;163:1943–1950
  14. Tahara H, Zitvogel L, Storkus WJ, Robbins PD, Lotze MT. Murine models of cancer cytokine gene therapy using interleukin-12. Ann. NY Acad. Sci. 1996;795:275–283
  15. Golab J, Zagozdzon R. Antitumor effects of interleukin-12 in pre-clinical and early clinical studies. Int. J. Mol. Med. 1999;3:537–544
  16. Rook AH, Wood GS, Yoo EK, Elenitsas R, Kao DM, Sherman ML, et al. Interleukin-12 therapy of cutaneous T-cell lymphoma induces lesion regression and cytotoxic T-cell responses. Blood. 1999;94:902–908
  17. Marshall E. Cancer trial of interleukin-12 halted. Science. 1555;268(1995):
  18. Car BD, Eng VM, Lipman JM, Anderson TD. The toxicology of interleukin-12: a review. Toxicol. Pathol. 1999;27:58–63
  19. Saffran DC, Horton HM, Yankauckas MA, Anderson D, Barnhart KM, Abai AM, et al. Immunotherapy of established tumors in mice by intratumoral injection of interleukin-2 plasmid DNA: induction of CD8+ T-cell immunity. Cancer. Gene Ther. 1998;5:321–330
  20. Colombo MP, Vagliani M, Spreafico F, Parenza M, Chiodoni C, Melani C, et al. Amount of interleukin 12 available at the tumor site is critical for tumor regression. Cancer Res. 1996;56:2531–2534
  21. Rakhmilevich AL, Timmins JG, Janssen K, Pohlmann EL, Sheehy MJ, Yang NS. 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. 1999;22:135–144
  22. Schultz J, Heinzerling L, Pavlovic J, Moelling K. Induction of long-lasting cytokine effect by injection of IL-12 encoding plasmid DNA. Cancer Gene Ther. 2000;7:1557–1565
  23. Tahara H, Zeh HJ, Storkus WJ, Pappo I, Watkins SC, Gubler U, et al. Fibroblasts genetically engineered to secrete interleukin 12 can suppress tumor growth and induce antitumor immunity to a murine melanoma in vivo. Cancer Res. 1994;54:182–189
  24. Chen L, Chen D, Block E, O’Donnell M, Kufe DW, Clinton SK. 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. 1997;159:351–359
  25. Meko JB, Yim JH, Tsung K, Norton JA. High cytokine production and effective antitumor activity of a recombinant vaccinia virus encoding murine interleukin 12. Cancer Res. 1995;55:4765–4770
  26. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J. Immunol. 2006;177:2080–2087
  27. Ryan JM, Barry FP, Murphy JM, Mahon BP. Mesenchymal stem cells avoid allogeneic rejection. J. Inflamm. 2005;2:8–19
  28. Stoff-Khalili MA, Rivera AA, Mathis JM, Banerjee NS, Moon AS, Hess A, et al. Mesenchymal stem cells as a vehicle for targeted delivery of CRAds to lung metastases of breast carcinoma. Breast Cancer Res. Treat. 2007;105:157–167
  29. Nakamura K, Ito Y, Kawano Y, Kurozumi K, Kobune M, Tsuda H, et al. Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther. 2004;11:1155–1164
  30. Hung SC, Deng WP, Yang WK, Liu RS, Lee CC, Su TC, et al. Mesenchymal stem cell targeting of microscopic tumors and tumor stroma development monitored by noninvasive in vivo positron emission tomography imaging. Clin. Cancer Res. 2005;11:7749–7756
  31. Komarova S, Kawakami Y, Stoff-Khalili MA, Curiel DT, Pereboeva L. Mesenchymal progenitor cells as cellular vehicles for delivery of oncolytic adenoviruses. Mol. Cancer Ther. 2006;5:755–766
  32. Igarashi M, Yogiashi Y, Mihara M, Takada I, Kitagawa H, Kato S. Vitamin K induces osteoblast differentiation through pregnane X receptor-mediated transcriptional control of the Msx2 gene. Mol. Cell Biol. 2007;27:7947–7954
  33. Meirelles LD, Nardi NB. Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Br. J. Haematol. 2003;123:702–711
  34. Phinney DG, Kopen G, Isaacson RL, Prockop DJ. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J. Cell. Biochem. 1999;72:570–585
  35. Sotiropoulou PA, Perez SA, Salagianni M, Baxevanis CN, Papamichail M. Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells. Stem Cells. 2006;24:462–471
  36. Elzaouk L, Moelling K, Pavlovic J. Anti-tumor activity of mesenchymal stem cells producing IL-12 in a mouse melanoma model. Exp. Dermatol. 2006;15:865–874
  37. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70
  38. Studeny M, Marini FC, Champlin RE, Zompetta C, Fidler IJ, Andreeff M. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res. 2002;62:3603–3608
  39. Ogawa M, Yu WG, Umehara K, Iwasaki M, Wijesuriya R, Tsujimura T, et al. Multiple roles of interferon-gamma in the mediation of interleukin 12-induced tumor regression. Cancer Res. 1998;58:2426–2432
  40. Kondadasula SV, Roda JM, Parihar R, Yu J, Lehman A, Caligiuri MA, et al. 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. 2008;111:4173–4183
  41. Strieter RM, Kunkel SL, Arenberg DA, Burdick MD, Polverini PJ. 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. 1995;210:51–57
  42. Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues, Organs. 2001;169:12–20
  43. Ren C, Kumar S, Chanda D, Kallman L, Chen J, Mountz JD, et al. Cancer gene therapy using mesenchymal stem cells expressing interferon-beta in a mouse prostate cancer lung metastasis model. Gene Ther. 2008;15:1446–1453

PII: S0304-3835(09)00571-0

doi: 10.1016/j.canlet.2009.08.031

Cancer Letters
Volume 290, Issue 2 , Pages 157-166 , 28 April 2010