Non-hematopoietic stem cells as factories for in vivo therapeutic protein production

Gene Therapy

Volumn 19, Issue 1, 2012, Pages 1-7

  Sanz, L ^a   Compte, M ^a   Guijarro Muoz I ^a   Alvarez Vallina L ^a  

^a HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

Author keywords

cell factory; cell based gene delivery; endothelial progenitor cell; mesenchymal stem cell; neural stem cell

Indexed keywords

ALPHA INTERFERON; BETA GLUCURONIDASE; BETA INTERFERON; BLOOD CLOTTING FACTOR; BLOOD CLOTTING FACTOR 8; CYTOSINE DEAMINASE; ENDOSTATIN; ERYTHROPOIETIN; FRACTALKINE; HEMOPEXIN; INSULIN; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 7; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VASCULOTROPIN RECEPTOR 2;

ADULT STEM CELL; ALLOGENEIC STEM CELL TRANSPLANTATION; ANEMIA; AUTOLOGOUS STEM CELL TRANSPLANTATION; BLOOD LEVEL; BREAST CANCER; BURKITT LYMPHOMA; CANCER GENE THERAPY; CANCER INHIBITION; CELL DIFFERENTIATION; CELL PROLIFERATION; COLON CARCINOMA; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DIABETES MELLITUS; ENDOTHELIAL PROGENITOR CELL; ENGRAFTMENT; EX VIVO STUDY; GENE DELIVERY SYSTEM; GLIOBLASTOMA; GLIOMA; HELA CELL; HEMOPHILIA; HEMOPHILIA A; HUMAN; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VIVO STUDY; LIFESPAN; LUNG CARCINOMA; LUNG METASTASIS; MELANOMA; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MUCOPOLYSACCHARIDOSIS TYPE 7; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; STEM CELL TRANSPLANTATION; TUMOR ENGRAFTMENT; TUMOR LOCALIZATION; TUMOR VASCULARIZATION; UTERINE CERVIX CARCINOMA;

ANIMALS; CYTOKINES; GENE TARGETING; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; IMMUNE SYSTEM; MESENCHYMAL STEM CELLS; MICE; NEOPLASMS; RECOMBINANT PROTEINS; STEM CELL TRANSPLANTATION; TRANSPLANTATION, HOMOLOGOUS;

EID: 84855438776     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2011.68     Document Type: Review

References (74)

1. Seow Y, Wood MJ. Biological gene delivery vehicles: beyond viral vectors. Mol Ther 2009; 17: 767-777.
2. Bessis N, GarciaCozar FJ, Boissier MC. Immune responses to gene therapy vectors: influence on vector function and effector mechanisms. Gene Therapy 2004; 11: S10-S17. (Pubitemid 39359442)
3. Nayak S, Herzog RW. Progress and prospects: immune responses to viral vectors. Gene Therapy 2010; 17: 295-304.
4. Harrington K, Alvarez-Vallina L, Crittenden M, Gough M, Chong H, Diaz RM et al. Cells as vehicles for cancer gene therapy: the missing link between targeted vectors and systemic delivery? Hum Gene Ther 2002; 13: 1263-1280. (Pubitemid 35034507)
5. Roth JC, Curiel DT, Pereboeva L. Cell vehicle targeting strategies. Gene Therapy 2008; 15: 716-729. (Pubitemid 351627355)
6. Aboody KS, Najbauer J, Danks MK. Stem and progenitor cell-mediated tumor selective gene therapy. Gene Therapy 2008; 15: 739-752. (Pubitemid 351627357)
7. Bexell D, Scheding S, Bengzon J. Toward brain tumor gene therapy using multipotent mesenchymal stromal cell vectors. Mol Ther 2010; 18: 1067-1075.
8. Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W et al. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 2000; 97: 12846-12851.
9. Benedetti S, Pirola B, Pollo B, Magrassi L, Bruzzone MG, Rigamonti D et al. Gene therapy of experimental brain tumors using neural progenitor cells. Nat Med 2000; 6: 447-450. (Pubitemid 30208163)
10. Muller FJ, Snyder EY, Loring JF. Gene therapy: can neural stem cells deliver? Nat Rev Neurosci 2006; 7: 75-84. (Pubitemid 41828933)
11. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007; 109: 1801-1809. (Pubitemid 46348173)
12. 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 Therapy 2004; 11: 1155-1164. (Pubitemid 39117311)
13. Gunnarsson S, Bexell D, Svensson A, Siesjo P, Darabi A, Bengzon J. Intratumoral IL-7 delivery by mesenchymal stromal cells potentiates IFNgamma-transduced tumor cell immunotherapy of experimental glioma. J Neuroimmunol 2010; 218: 140-144.
14. Xu G, Jiang XD, Xu Y, Zhang J, Huang FH, Chen ZZ et al. Adenoviral-mediated interleukin-18 expression in mesenchymal stem cells effectively suppresses the growth of glioma in rats. Cell Biol Int 2009; 33: 466-474.
15. Nakamizo A, Marini F, Amano T, Khan A, Studeny M, Gumin J et al. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 2005; 65: 3307-3318. (Pubitemid 40524615)
16. Kim SM, Lim JY, Park SI, Jeong CH, Oh JH, Jeong M et al. Gene therapy using TRAILsecreting human umbilical cord blood-derived mesenchymal stem cells against intracranial glioma. Cancer Res 2008; 68: 9614-9623.
17. Sasportas LS, Kasmieh R, Wakimoto H, Hingtgen S, van de Water JA, Mohapatra G et al. Assessment of therapeutic efficacy and fate of engineered human mesenchymal stem cells for cancer therapy. Proc Natl Acad Sci USA 2009; 106: 4822-4827.
18. Ehtesham M, Kabos P, Kabosova A, Neuman T, Black KL, Yu JS. The use of interleukin 12-secreting neural stem cells for the treatment of intracranial glioma. Cancer Res 2002; 62: 5657-5763.
19. Kim SK, Cargioli TG, Machluf M, Yang W, Sun Y, Al-Hashem R et al. PEX-producing human neural stem cells inhibit tumor growth in a mouse glioma model. Clin Cancer Res 2005; 11: 5965-5970. (Pubitemid 41170327)
20. Ehtesham M, Kabos P, Gutierrez MA, Chung NH, Griffith TS, Black KL et al. Induction of glioblastoma apoptosis using neural stem cell-mediated delivery of tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res 2002; 62: 7170-7174. (Pubitemid 36025232)
21. Menon LG, Kelly K, Yang HW, Kim SK, Black PM, Carroll RS. Human bone marrowderived mesenchymal stromal cells expressing S-TRAIL as a cellular delivery vehicle for human glioma therapy. Stem Cells 2009; 27: 2320-2330.
22. Hong X, Miller C, Savant-Bhonsale S, Kalkanis SN. Antitumor treatment using interleukin-12-secreting marrow stromal cells in an invasive glioma model. Neurosurgery 2009; 64: 1139-1146.
23. Yuan X, Hu J, Belladonna ML, Black KL, Yu JS. Interleukin-23-expressing bone marrow-derived neural stem-like cells exhibit antitumor activity against intracranial glioma. Cancer Res 2006; 66: 2630-2638.
24. Bexell D, Gunnarsson S, Tormin A, Darabi A, Gisselsson D, Roybon L et al. Bone marrow multipotent mesenchymal stroma cells act as pericyte-like migratory vehicles in experimental gliomas. Mol Ther 2009; 17: 183-190.
25. Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 2003; 108: 863-868. (Pubitemid 37022130)
26. Fischer UM, Harting MT, Jimenez F, Monzon-Posadas WO, Xue H, Savitz SI et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev 2009; 18: 683-692.
27. 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. (Pubitemid 32437040)
28. Harting MT, Jimenez F, Xue H, Fischer UM, Baumgartner J, Dash PK et al. Intravenous mesenchymal stem cell therapy for traumatic brain injury. J Neurosurg 2009; 110: 1189-1197.
29. Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009; 5: 54-63.
30. Wang H, Cao F, De A, Cao Y, Contag C, Gambhir SS et al. Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells 2009; 27: 1548-1558.
31. Smits PA, Kleppe LS, Witt TA, Mueske CS, Vile RG, Simari RD. Distribution of circulation-derived endothelial progenitors following systemic delivery. Endothelium 2007; 14: 1-5. (Pubitemid 46978764)
32. Studeny M, Marini FC, Champlin RE, Zompetta C, Fidler IJ, Andreeff M. Bone marrowderived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res 2002; 62: 3603-3608. (Pubitemid 34728832)
33. Studeny M, Marini FC, Dembinski JL, Zompetta C, Cabreira-Hansen M, Bekele BN et al. Mesenchymal stem cells: potential precursors for tumor stroma and targeteddelivery vehicles for anticancer agents. J Natl Cancer Inst 2004; 96: 1593-1603. (Pubitemid 39534883)
34. 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 Therapy 2008; 15: 1446-1453.
35. Ren C, Kumar S, Chanda D, Chen J, Mountz JD, Ponnazhagan S. Therapeutic potential of mesenchymal stem cells producing interferon-alpha in a mouse melanoma lung metastasis model. Stem Cells 2008; 26: 2332-2338.
36. Kanehira M, Xin H, Hoshino K, Maemondo M, Mizuguchi H, Hayakawa T et al. Targeted delivery of NK4 to multiple lung tumors by bone marrow-derived mesenchymal stem cells. Cancer Gene Ther 2007; 14: 894-903. (Pubitemid 47557220)
37. Xin H, Kanehira M, Mizuguchi H, Hayakawa T, Kikuchi T, Nukiwa T et al. Targeted delivery of CX3CL1 to multiple lung tumors by mesenchymal stem cells. Stem Cells 2007; 25: 1618-1626. (Pubitemid 47121838)
38. 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. (Pubitemid 44473325)
39. Frank RT, Edmiston M, Kendall SE, Najbauer J, Cheung CW, Kassa T et al. Neural stem cells as a novel platform for tumor-specific delivery of therapeutic antibodies. PLoS One 2009; 4: e8314.
40. Chen X, Lin X, Zhao J, Shi W, Zhang H, Wang Y et al. A tumor-selective biotherapy with prolonged impact on established metastases based on cytokine gene-engineered MSCs. Mol Ther 2008; 16: 749-756. (Pubitemid 351426177)
41. Duan X, Guan H, Cao Y, Kleinerman ES. Murine bone marrow-derived mesenchymal stem cells as vehicles for interleukin-12 gene delivery into Ewing sarcoma tumors. Cancer 2009; 115: 13-22.
42. Grisendi G, Bussolari R, Cafarelli L, Petak I, Rasini V, Veronesi E et al. Adipose-derived mesenchymal stem cells as stable source of tumor necrosis factor-related apoptosisinducing ligand delivery for cancer therapy. Cancer Res 2010; 70: 3718-3729.
43. Dudek AZ, Bodempudi V, Welsh BW, Jasinski P, Griffin RJ, Milbauer L et al. Systemic inhibition of tumour angiogenesis by endothelial cell-based gene therapy. Br J Cancer 2007; 97: 513-522. (Pubitemid 47258448)
44. Prockop DJ. Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther 2009; 17: 939-946.
45. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenasemediated tryptophan degradation. Blood 2004; 103: 4619-4621. (Pubitemid 38745993)
46. Sanz L, Santos-Valle P, Alonso-Camino V, Salas C, Serrano A, Vicario JL et al. Long-term in vivo imaging of human angiogenesis: critical role of bone marrow-derived mesenchymal stem cells for the generation of durable blood vessels. Microvasc Res 2008; 75: 308-314.
47. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 2007; 109: 228-234. (Pubitemid 46053063)
48. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GWet al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007; 449: 557-563. (Pubitemid 47525152)
49. Chuah MK, Van DA, Zwinnen H, Goovaerts I, Vanslembrouck V, Collen D et al. Longterm persistence of human bone marrow stromal cells transduced with factor VIIIretroviral vectors and transient production of therapeutic levels of human factor VIII in nonmyeloablated immunodeficient mice. Hum Gene Ther 2000; 11: 729-738. (Pubitemid 30180277)
50. Eliopoulos N, Al-Khaldi A, Crosato M, Lachapelle K, Galipeau J. A neovascularized organoid derived from retrovirally engineered bone marrow stroma leads to prolonged in vivo systemic delivery of erythropoietin in nonmyeloablated, immunocompetent mice. Gene Therapy 2003; 10: 478-489. (Pubitemid 36395265)
51. Eliopoulos N, Lejeune L, Martineau D, Galipeau J. Human-compatible collagen matrix for prolonged and reversible systemic delivery of erythropoietin in mice from genemodified marrow stromal cells. Mol Ther 2004; 10: 741-748. (Pubitemid 39272863)
52. Eliopoulos N, Gagnon RF, Francois M, Galipeau J. Erythropoietin delivery by genetically engineered bone marrow stromal cells for correction of anemia in mice with chronic renal failure. J Am Soc Nephrol 2006; 17: 1576-1584. (Pubitemid 43794660)
53. Compte M, Cuesta AM, Sanchez-Martin D, Alonso-Camino V, Vicario JL, Sanz L et al. Tumor immunotherapy using gene-modified human mesenchymal stem cells loaded into synthetic extracellular matrix scaffolds. Stem Cells 2009; 27: 753-760.
54. Frank RT, Najbauer J, Aboody KS. Concise review: stem cells as an emerging platform for antibody therapy of cancer. Stem Cells 2010; 28: 2084-2087.
55. Wang N, Fallavollita L, Nguyen L, Burnier J, Rafei M, Galipeau J et al. Autologous bone marrow stromal cells genetically engineered to secrete an igf-I receptor decoy prevent the growth of liver metastases. Mol Ther 2009; 17: 1241-1249.
56. Stagg J, Lejeune L, Paquin A, Galipeau J. Marrow stromal cells for interleukin-2 delivery in cancer immunotherapy. Hum Gene Ther 2004; 15: 597-608. (Pubitemid 41071207)
57. Eliopoulos N, Francois M, Boivin MN, Martineau D, Galipeau J. Neo-organoid of marrow mesenchymal stromal cells secreting interleukin-12 for breast cancer therapy. Cancer Res 2008; 68: 4810-4818.
58. Van Damme A, Thorrez L, Ma L, Vandenburgh H, Eyckmans J, Dell'Accio F et al. Efficient lentiviral transduction and improved engraftment of human bone marrow mesenchymal cells. Stem Cells 2006; 24: 896-907. (Pubitemid 44464723)
59. Lin Y, Chang L, Solovey A, Healey JF, Lollar P, Hebbel RP. Use of blood outgrowth endothelial cells for gene therapy for hemophilia A. Blood 2002; 99: 457-462. (Pubitemid 34533079)
60. Matsui H, Shibata M, Brown B, Labelle A, Hegadorn C, Andrews C et al. Ex vivo gene therapy for hemophilia A that enhances safe delivery and sustained in vivo factor VIII expression from lentivirally engineered endothelial progenitors. Stem Cells 2007; 25: 2660-2669. (Pubitemid 47582759)
61. Coutu DL, Cuerquis J, El AR, Forner KA, Roy R, Francois M et al. Hierarchical scaffold design for mesenchymal stem cell-based gene therapy of hemophilia B. Biomaterials 2011; 32: 295-305.
62. Rameshwar P. Casting doubt on the safety of 'off-the-shelf' mesenchymal stem cells for cell therapy. Mol Ther 2009; 17: 216-218.
63. Campeau PM, Rafei M, Francois M, Birman E, Forner KA, Galipeau J. Mesenchymal stromal cells engineered to express erythropoietin induce anti-erythropoietin antibodies and anemia in allorecipients. Mol Ther 2009; 17: 369-372.
64. Chen NK, Tan SY, Udolph G, Kon OL. Insulin expressed from endogenously active glucose-responsive EGR1 promoter in bone marrow mesenchymal stromal cells as diabetes therapy. Gene Therapy 2010; 17: 592-605.
65. Meyerrose TE, Roberts M, Ohlemiller KK, Vogler CA, Wirthlin L, Nolta JA et al. Lentiviral-transduced human mesenchymal stem cells persistently express therapeutic levels of enzyme in a xenotransplantation model of human disease. Stem Cells 2008; 26: 1713-1722.
66. Orive G, Hernandez RM, Gascon AR, Calafiore R, Chang TM, De VP et al. Cell encapsulation: promise and progress. Nat Med 2003; 9: 104-107. (Pubitemid 36098269)
67. Goren A, Dahan N, Goren E, Baruch L, Machluf M. Encapsulated human mesenchymal stem cells: a unique hypoimmunogenic platform for long-term cellular therapy. FASEB J 2010; 24: 22-31.
68. Conrad C, Gupta R, Mohan H, Niess H, Bruns CJ, Kopp R et al. Genetically engineered stem cells for therapeutic gene delivery. Curr Gene Ther 2007; 7: 249-260. (Pubitemid 47232957)
69. Karp JM, Leng Teo GS. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009; 4: 206-216.
70. Coutu DL, Yousefi AM, Galipeau J. Three-dimensional porous scaffolds at the crossroads of tissue engineering and cell-based gene therapy. J Cell Biochem 2009; 108: 537-546.
71. Fritz V, Noel D, Bouquet C, Opolon P, Voide R, Apparailly F et al. Antitumoral activity and osteogenic potential of mesenchymal stem cells expressing the urokinase-type plasminogen antagonist amino-terminal fragment in a murine model of osteolytic tumor. Stem Cells 2008; 26: 2981-2990.
72. Hu M, Yang JL, Teng H, Jia YQ, Wang R, Zhang XW et al. Anti-angiogenesis therapy based on the bone marrow-derived stromal cells genetically engineered to express sFlt-in mouse tumor model. BMC Cancer 2008; 8: 306.
73. Kyriakou CA, Yong KL, Benjamin R, Pizzey A, Dogan A, Singh N et al. Human mesenchymal stem cells (hMSCs) expressing truncated soluble vascular endothelial growth factor receptor (tsFlk-1) following lentiviral-mediated gene transfer inhibit growth of Burkitt's lymphoma in a murine model. J Gene Med 2006; 8: 253-264.
74. Loebinger MR, Eddaoudi A, Davies D, Janes SM. Mesenchymal stem cell delivery of TRAIL can eliminate metastatic cancer. Cancer Res 2009; 69: 4134-4142.