Reversal of tumor growth by gene modification of mesenchymal stem cells using spermine-pullulan/DNA nanoparticles

Journal of Biomedical Nanotechnology

Volumn 10, Issue 2, 2014, Pages 299-308

  Hu, Yu Lan ^a   Miao, Pei Hong ^b   Huang, Bing ^a   Zhang, Tian Yuan ^a   Hu, Zhong Jie ^b   Tabata, Yasuhiko ^c   Gao, Jian Qing ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b Zhejiang Provincial Corps Hospital of Chinese People's Armed Forces   (China)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

IL 12; MSCs; Non viral transfection; Tumor targeting

Indexed keywords

CELLULAR INTERNALIZATION; IL-12; INTRATUMORAL INJECTION; MESENCHYMAL STEM CELL; MSCS; NON-VIRAL TRANSFECTIONS; PHYSIOLOGIC CONDITIONS; TUMOR-TARGETING;

FLOWCHARTING; GENES; GENETIC ENGINEERING; MOLECULAR BIOLOGY; NANOPARTICLES; PATHOLOGY; PHYSIOLOGY; TUMORS;

CELL CULTURE;

DNA; INTERLEUKIN 12; NANOPARTICLE; PULLULAN; SPERMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DNA MODIFICATION; GENETIC ENGINEERING; GENETIC TRANSFECTION; IN VIVO STUDY; LUNG METASTASIS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; RAT; TUMOR GROWTH;

ANIMALS; CELL DEATH; CELL MOVEMENT; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DNA; FEMALE; GLUCANS; INJECTIONS, INTRAVENOUS; INTERLEUKIN-12; LUNG NEOPLASMS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; NANOPARTICLES; NEOPLASMS; RATS; RECOMBINATION, GENETIC; SPERMINE; SUBCUTANEOUS TISSUE; SURVIVAL ANALYSIS; TRANSFECTION;

EID: 84893204121     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2014.1712     Document Type: Article

References (47)

1. M. F. Pittenger, A. M. Mackay, S. C. Beck, R. K. Jaiswal, R. Douglas, J. D. Mosca, M. A. Moorman, D. W. Simonetti, S. Craig, and D. R. Marshak, Multilineage potential of adult human mesenchymal stem cells. Science 284, 143 (1999).
2. M. Studeny, F. C. Marini, R. E. Champlin, C. Zompetta, I. J. Fidler, and M. Andreeff, Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res. 62, 3603 (2002).
3. A. Nakamizo, F. Marini, T. Amano, A. Khan, M. Studeny, J. Gumin, J. Chen, S. Hentschel, G. Vecil, J. Dembinski, M. Andreeff, and F. F. Lang, Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res. 65, 3307 (2005).
4. K. Nakamura, Y. Ito, Y. Kawano, K. Kurozumi, M. Kobune, H. Tsuda, A. Bizen, O. Honmou, Y. Niitsu, and H. Hamada, Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther. 11, 1155 (2004).
5. J. Stagg, L. Lejeune, A. Paquin, and J. Galipeau, Marrow stromal cells for interleukin-2 delivery in cancer immunotherapy. Hum Gene Ther. 15, 597 (2004).
6. N. Eliopoulos, M. Francois, M. N. Boivin, D. Martineau, and J. Galipeau, Neo-organoid of marrow mesenchymal stromal cells secreting interleukin-12 for breast cancer therapy. Cancer Res. 68, 4810 (2008).
7. P. Gao, Q. Ding, Z. Wu, H. Jiang, and Z. Fang, Therapeutic potential of human mesenchymal stem cells producing IL-12 in a mouse xenograft model of renal cell carcinoma. Cancer Lett. 290, 157 (2009).
8. M. R. Loebinger, A. Eddaoudi, D. Davies, and S. M. Janes, Mesenchymal stem cell delivery of TRAIL can eliminate metastatic cancer. Cancer Res. 69, 4134 (2009).
9. Y. L. Hu, B. Huang, T. Y. Zhang, P. H. Miao, G. P. Tang, Y. Tabata, and J. Q. Gao, Mesenchymal stem cells as a novel carrier for targeted delivery of gene in cancer therapy based on nonviral transfection. Mol. Pharm. 9, 2698 (2012).
10. P. A. Sotiropoulou, S. A. Perez, M. Salagianni, C. N. Baxevanis, and M. Papamichail, Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells. Stem Cells 24, 462 (2006).
11. L. Li and W. B. Neaves, Normal stem cells and cancer stem cells: the niche matters. Cancer Res. 66, 4553 (2006).
12. M. S. Wicha, Cancer stem cells and metastasis: Lethal seeds. Clin. Cancer Res. 12, 5606 (2006).
13. X. Chen, X. Lin, J. Zhao, W. Shi, H. Zhang, Y. Wang, B. Kan, L. Du, B. Wang, Y. Wei, Y. Liu, and X. Zhao, A tumor-selective biotherapy with prolonged impact on established metastases based on cytokine gene-engineered MSCs. Mol Ther. 16, 749 (2008).
14. W. Zhu, W. Xu, R. Jiang, H. Qian, M. Chen, J. Hu, W. Cao, C. Han, and Y. Chen, Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp. Mol. Pathol. 80, 267 (2006).
15. A. E. Karnoub, A. B. Dash, A. P. Vo, A. Sullivan, M. W. Brooks, G. W. Bell, A. L. Richardson, K. Polyak, R. Tubo, and R. A. Weinberg, Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449, 557 (2007).
16. J. Jo, T. Ikai, A. Okazaki, M. Yamamoto, Y. Hirano, and Y. Tabata, Expression profile of plasmid DNA by spermine derivatives of pullulan with different extents of spermine introduced. J. Control. Release 118, 389 (2007).
17. C. X. He, Y. Tabata, and J. Q. Gao, Non-viral gene delivery carrier and its three-dimensional transfection system. Int. J. Pharm. (2009).
18. J. Jo, A. Okazaki, K. Nagane, M. Yamamoto, and Y. Tabata, Preparation of cationized polysaccharides as gene transfection carrier for bone marrow-derived mesenchymal stem cells. J. Biomater. Sci. Polym. Ed. 21, 185 (2010).
19. G. Trinchieri and P. Scott, Interleukin-12: Basic principles and clinical applications. Curr. Top Microbiol. Immunol. 238, 57 (1999).
20. M. S. Gee, C. J. Koch, S. M. Evans, W. T. Jenkins, C. H. Pletcher, Jr, J. S. Moore, H. K. Koblish, J. Lee, E. M. Lord, G. Trinchieri, and W. M. Lee, Hypoxia-mediated apoptosis from angiogenesis inhibition underlies tumor control by recombinant interleukin 12. Cancer Res. 59, 4882 (1999).
21. E. E. Voest, B. M. Kenyon, M. S. O'Reilly, G. Truitt, R. J. D'Amato, and J. Folkman, Inhibition of angiogenesis in vivo by interleukin 12. J. Natl. Cancer Inst. 87, 581 (1995).
22. M. Del Vecchio, E. Bajetta, S. Canova, M. T. Lotze, A. Wesa, G. Parmiani, and A. Anichini, Interleukin-12: Biological properties and clinical application. Clin. Cancer Res. 13, 4677 (2007).
23. M. P. Colombo and G. Trinchieri, Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev. 13, 155 (2002).
24. J. Cohen, IL-12 deaths: Explanation and a puzzle. Science 270, 908 (1995).
25. C. X. He, N. Li, Y. L. Hu, X. M. Zhu, H. J. Li, M. Han, P. H. Miao, Z. J. Hu, G. Wang, W. Q. Liang, Y. Tabata, and J. Q. Gao, Effective gene delivery to mesenchymal stem cells based on the reverse transfection and three-dimensional cell culture system. Pharm. Res. 28, 1577 (2011).
26. M. Feng, D. Lee, and P. Li, Intracellular uptake and release of poly(ethyleneimine)-co-poly(methyl methacrylate) nanoparticle/pDNA complexes for gene delivery. Int. J. Pharm. 311, 209 (2006).
27. R. F. Hwang, T. Moore, T. Arumugam, V. Ramachandran, K. D. Amos, A. Rivera, B. Ji, D. B. Evans, and C. D. Logsdon, Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 68, 918 (2008).
28. E. L. Spaeth, J. L. Dembinski, A. K. Sasser, K. Watson, A. Klopp, B. Hall, M. Andreeff, and F. Marini, Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLoS One 4, e4992 (2009).
29. A. Y. Khakoo, S. Pati, S. A. Anderson, W. Reid, M. F. Elshal, Rovira, II, A. T. Nguyen, D. Malide, C. A. Combs, G. Hall, J. Zhang, M. Raffeld, T. B. Rogers, W. Stetler-Stevenson, J. A. Frank, M. Reitz, and T. Finkel, Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J. Exp. Med. 203, 1235 (2006).
30. A. H. Klopp, A. Gupta, E. Spaeth, M. Andreeff, and F. Marini, 3rd, Dissecting a discrepancy in the literature: Do mesenchymal stem cells support or suppress tumor growth? Stem Cells (2011).
31. B. D. Roorda, A. ter Elst, W. A. Kamps, and E. S. de Bont, Bone marrow-derived cells and tumor growth: Contribution of bone marrow-derived cells to tumor micro-environments with special focus on mesenchymal stem cells. Crit. Rev. Oncol. Hematol. 69, 187 (2009).
32. D. Bexell, S. Gunnarsson, A. Tormin, A. Darabi, D. Gisselsson, L. Roybon, S. Scheding, and J. Bengzon, Bone marrow multipotent mesenchymal stroma cells act as pericyte-like migratory vehicles in experimental gliomas. Mol. Ther. 17, 183 (2009).
33. A. Al-Khaldi, N. Eliopoulos, D. Martineau, L. Lejeune, K. Lachapelle, and J. Galipeau, Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther. 10, 621 (2003).
34. M. Di Nicola, C. Carlo-Stella, M. Magni, M. Milanesi, P. D. Longoni, P. Matteucci, S. Grisanti, and A. M. Gianni, Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99, 3838 (2002).
35. F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, J. Sany, D. Noel, and C. Jorgensen, Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102, 3837 (2003).
36. M. J. Brunda, L. Luistro, R. R. Warrier, R. B. Wright, B. R. Hubbard, M. Murphy, S. F. Wolf, and M. K. Gately, Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J. Exp. Med. 178, 1223 (1993).
37. J. Schultz, L. Heinzerling, J. Pavlovic, and K. Moelling, Induction of long-lasting cytokine effect by injection of IL-12 encoding plasmid DNA. Cancer Gene Ther. 7, 1557 (2000).
38. B. D. Car, V. M. Eng, J. M. Lipman, and T. D. Anderson, The toxicology of interleukin-12: A review. Toxicol Pathol. 27, 58 (1999).
39. X. Duan, H. Guan, Y. Cao, and E. S. Kleinerman, Murine bone marrow-derived mesenchymal stem cells as vehicles for interleukin-12 gene delivery into Ewing sarcoma tumors. Cancer 115, 13 (2009).
40. A. Okazaki, J. Jo, and Y. Tabata, A reverse transfection technology to genetically engineer adult stem cells. Tissue Eng. 13, 245 (2007).
41. L. Elzaouk, K. Moelling, and J. Pavlovic, Anti-tumor activity of mesenchymal stem cells producing IL-12 in a mouse melanoma model. Exp. Dermatol. 15, 865 (2006).
42. Y. L. Hu, Y. H. Fu, Y. Tabata, and J. Q. Gao, Mesenchymal stem cells: A promising targeted-delivery vehicle in cancer gene therapy. J. Control. Release 147, 154 (2010).
43. C. Ren, S. Kumar, D. Chanda, L. Kallman, J. Chen, J. D. Mountz, and S. Ponnazhagan, Cancer gene therapy using mesenchymal stem cells expressing interferon-beta in a mouse prostate cancer lung metastasis model. Gene Ther. 15, 1446 (2008).
44. A. Mohr, M. Lyons, L. Deedigan, T. Harte, G. Shaw, L. Howard, F. Barry, T. O'Brien, and R. Zwacka, Mesenchymal stem cells expressing TRAIL lead to tumour growth inhibition in an experimental lung cancer model. J. Cell Mol. Med. 12, 2628 (2008).
45. M. Studeny, F. C. Marini, J. L. Dembinski, C. Zompetta, M. Cabreira-Hansen, B. N. Bekele, R. E. Champlin, and M. Andreeff, Mesenchymal stem cells: Potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J. Natl. Cancer Inst. 96, 1593 (2004).
46. H. Hamada, M. Kobune, K. Nakamura, Y. Kawano, K. Kato, O. Honmou, K. Houkin, T. Matsunaga, and Y. Niitsu, Mesenchymal stem cells (MSC) as therapeutic cytoreagents for gene therapy. Cancer Sci. 96, 149 (2005).
47. A. M. Sonabend, I. V. Ulasov, M. A. Tyler, A. A. Rivera, J. M. Mathis, and M. S. Lesniak, Mesenchymal stem cells effectively deliver an oncolytic adenovirus to intracranial glioma. Stem Cells 26, 831 (2008).