Therapeutic potential of mesenchymal stem cells in gastrointestinal cancers – current evidence

References

• Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–147.
   PubMed Web of Science ®Google Scholar
• Zvaifler NJ, Marinova-Mutafchieva L, Adams G, et al. Mesenchymal precursor cells in the blood of normal individuals. Arthritis Res. 2000; 2(6):477–488.
   PubMedGoogle Scholar
• Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7(2):211–228.
   PubMedGoogle Scholar
• Corsten MF, Shah K. Therapeutic stem-cells for cancer treatment: hopes and hurdles in tactical warfare. Lancet Oncol. 2008;9(4):376–384.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276(5309):71–74.
   PubMed Web of Science ®Google Scholar
• Jackson WM, Nesti LJ, Tuan RS. Concise review: clinical translation of wound healing therapies based on mesenchymal stem cells. Stem Cells Transl Med. 2012;1(1):44–50.
   PubMed Web of Science ®Google Scholar
• Meuleman N, Tondreau T, Ahmad I, et al. Infusion of mesenchymal stromal cells can aid hematopoietic recovery following allogeneic hematopoietic stem cell myeloablative transplant: a pilot study. Stem Cells Dev. 2009;18(9):1247–1252.
   PubMed Web of Science ®Google Scholar
• Kornblit B, Leisenring WM, Santos EB, et al. Safety of treatment with DLA-identical or unrelated mesenchymal stromal cells in DLA-identical canine bone marrow transplantation. Chimerism. 2013;4(3):95–101.
   PubMedGoogle Scholar
• Perico N, Casiraghi F, Introna M, et al. Autologous mesenchymal stromal cells and kidney transplantation: a pilot study of safety and clinical feasibility. Clin J Am Soc Nephrol. 2011;6(2):412–422.
   PubMed Web of Science ®Google Scholar
• Reinders ME, de Fijter JW, Roelofs H, et al. Autologous bone marrow-derived mesenchymal stromal cells for the treatment of allograft rejection after renal transplantation: results of a phase I study. Stem Cells Transl Med. 2013;2(2):107–111.
   PubMed Web of Science ®Google Scholar
• Teo AK, Vallier L. Emerging use of stem cells in regenerative medicine. Biochem J. 2010;428(1):11–23.
   Google Scholar
• Roobrouck VD, Clavel C, Jacobs SA, et al. Differentiation potential of human postnatal mesenchymal stem cells, mesoangioblasts, and multipotent adult progenitor cells reflected in their transcriptome and partially influenced by the culture conditions. Stem Cells. 2011;29(5):871–882.
   Web of Science ®Google Scholar
• Roobrouck VD, Vanuytsel K, Verfaillie CM. Concise review: culture mediated changes in fate and/or potency of stem cells. Stem Cells. 2011; 29(4):583–589.
   Web of Science ®Google Scholar
• Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–317.
   PubMed Web of Science ®Google Scholar
• Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9(5):641–650.
   PubMed Web of Science ®Google Scholar
• Sacchetti B, Funari A, Michienzi S, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131(2):324–336.
   PubMed Web of Science ®Google Scholar
• Zhang D, Fan GC, Zhou X, et al. Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. J Mol Cell Cardiol. 2008;44(2):281–292.
   PubMed Web of Science ®Google Scholar
• Zhuang Y, Chen X, Xu M, et al. Chemokine stromal cell-derived factor 1/CXCL12 increases homing of mesenchymal stem cells to injured myocardium and neovascularization following myocardial infarction. Chin Med J (Engl). 2009;122(2):183–187.
   Web of Science ®Google Scholar
• Ryu CH, Park SA, Kim SM, et al. Migration of human umbilical cord blood mesenchymal stem cells mediated by stromal cell-derived factor-1/CXCR4 axis via Akt, ERK, and p38 signal transduction pathways. Biochem Biophys Res Commun. 2010;398(1):105–110.
   Web of Science ®Google Scholar
• Kortesidis A, Zannettino A, Isenmann S, et al. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood. 2005;105(10):3793–3801.
   Web of Science ®Google Scholar
• Honczarenko M, Le Y, Swierkowski M, et al. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells. 2006;24(4):1030–1041.
   PubMed Web of Science ®Google Scholar
• Rombouts WJ, Ploemacher RE. Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia. 2003;17(1):160–170.
   PubMed Web of Science ®Google Scholar
• Shi M, Li J, Liao L, et al. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice. Haematologica. 2007;92(7):897–904.
   PubMed Web of Science ®Google Scholar
• Ponte AL, Marais E, Gallay N, et al. The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells. 2007;25(7):1737–1745.
   PubMed Web of Science ®Google Scholar
• Fan H, Zhao G, Liu L, et al. Pre-treatment with IL-1beta enhances the efficacy of MSC transplantation in DSS-induced colitis. Cell Mol Immunol. 2012;9(6):473–481.
   Web of Science ®Google Scholar
• Klopp AH, Spaeth EL, Dembinski JL, et al. Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res. 2007;67(24):11687–11695.
   PubMed Web of Science ®Google Scholar
• Mishra PJ, Mishra PJ, Glod JW, et al. Mesenchymal stem cells: flip side of the coin. Cancer Res. 2009;69(4):1255–1258.
   Web of Science ®Google Scholar
• François S, Bensidhoum M, Mouiseddine M, et al. Local irradiation not only induces homing of human mesenchymal stem cells at exposed sites but promotes their widespread engraftment to multiple organs: a study of their quantitative distribution after irradiation damage. Stem Cells. 2006;24(4):1020–1029.
   Web of Science ®Google Scholar
• Dwyer RM, Khan S, Barry FP, et al. Advances in mesenchymal stem cell-mediated gene therapy for cancer. Stem Cell Res Ther. 2010;1(3):25.
   Google Scholar
• Kidd S, Caldwell L, Dietrich M, et al. Mesenchymal stromal cells alone or expressing interferon-β suppress pancreatic tumors in vivo, an effect countered by anti-inflammatory treatment. Cytotherapy. 2010;12(5):615–625.
   PubMed Web of Science ®Google Scholar
• Maestroni GJ, Hertens E, Galli P. Factor(s) from nonmacrophage bone marrow stromal cells inhibit Lewis lung carcinoma and B16 melanoma growth in mice. Cell Mol Life Sci. 1999;55(4):663–667.
   Web of Science ®Google Scholar
• Qiao L, Xu Z, Zhao T, et al. Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res. 2008;18(4):500–507.
   PubMed Web of Science ®Google Scholar
• Qiao L, Zhao TJ, Wang FZ, et al. NF-κB downregulation may be involved the depression of tumor cell proliferation mediated by human mesenchymal stem cells. Acta Pharmacol Sin. 2008;29(3):333–340.
   Web of Science ®Google Scholar
• Wong RS. Mesenchymal stem cells: angels or demons? J Biomed Biotechnol. 2011;2011:459510.
   PubMedGoogle Scholar
• Conrad C, Husemann Y, Niess H, et al. Linking transgene expression of engineered mesenchymal stem cells and angiopoietin-1-induced differentiation to target cancer angiogenesis. Ann Surg. 2011;253(3):566–571.
   Web of Science ®Google Scholar
• Zischek C, Niess H, Ischenko I, et al. Targeting tumor stroma using engineered mesenchymal stem cells reduces the growth of pancreatic carcinoma. Ann Surg. 2009;250(5):747–753.
   PubMed Web of Science ®Google Scholar
• Niess H, Bao Q, Conrad C, et al. Selective targeting of genetically engineered mesenchymal stem cells to tumor stroma microenvironments using tissue-specific suicide gene expression suppresses growth of hepatocellular carcinoma. Ann Surg. 2011;254(5):767–774; discussion 774–775.
   PubMed Web of Science ®Google Scholar
• Zhu W, Xu W, Jiang R, et al. Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp Mol Pathol. 2006;80(3):267–274.
   PubMed Web of Science ®Google Scholar
• Djouad F, Plence P, Bony C, et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003;102(10):3837–3844.
   PubMed Web of Science ®Google Scholar
• Li GC, Ye QH, Xue YH, et al. Human mesenchymal stem cells inhibit metastasis of a hepatocellular carcinoma model using the MHCC97-H cell line. Cancer Sci. 2010;101(12):2546–2553.
   Web of Science ®Google Scholar
• Tian LL, Yue W, Zhu F, et al. Human mesenchymal stem cells play a dual role on tumor cell growth in vitro and in vivo. J Cell Physiol. 2011;226(7):1860–1867.
   Web of Science ®Google Scholar
• Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression? Trends Immunol. 2007;28(5):219–226.
   PubMed Web of Science ®Google Scholar
• Ashkenazi A, Pai RC, Fong S, et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest. 1999;104(2):155–162.
   PubMed Web of Science ®Google Scholar
• Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol. 2003;3(2):133–146.
   PubMed Web of Science ®Google Scholar
• Gately MK, Renzetti LM, Magram J, et al. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol. 1998;16:495–521.
   PubMed Web of Science ®Google Scholar
• Chen XC, Wang R, Zhao X, et al. Prophylaxis against carcinogenesis in three kinds of unestablished tumor models via IL12-gene-engineered MSCs. Carcinogenesis. 2006;27(12):2434–2441.
   Web of Science ®Google Scholar
• Klebanoff CA, Finkelstein SE, Surman DR, et al. IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc Natl Acad Sci U S A. 2004;101(7):1969–1974.
   PubMed Web of Science ®Google Scholar
• Watkins SK, Egilmez NK, Suttles J, et al. IL-12 rapidly alters the functional profile of tumor-associated and tumor-infiltrating macrophages in vitro and in vivo. J Immunol. 2007;178(3):1357–1362.
   PubMed Web of Science ®Google Scholar
• Watkins SK, Li B, Richardson KS, et al. Rapid release of cytoplasmic IL-15 from tumor-associated macrophages is an initial and critical event in IL-12-initiated tumor regression. Eur J Immunol. 2009;39(8):2126–2135.
   Web of Science ®Google Scholar
• Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol. 2006;6(8):595–601.
   PubMed Web of Science ®Google Scholar
• Sneller MC, Kopp WC, Engelke KJ, et al. IL-15 administered by continuous infusion to rhesus macaques induces massive expansion of CD8+ T effector memory population in peripheral blood. Blood. 2011;118(26):6845–6848.
   PubMed Web of Science ®Google Scholar
• Weiss JM, Back TC, Scarzello AJ, et al. Successful immunotherapy with IL-2/anti-CD40 induces the chemokine-mediated mitigation of an immunosuppressive tumor microenvironment. Proc Natl Acad Sci U S A. 2009;106(46):19455–19460.
   PubMed Web of Science ®Google Scholar
• Jing W, Chen Y, Lu L, et al. Human umbilical cord blood-derived mesenchymal stem cells producing IL15 eradicate established pancreatic tumor in syngeneic mice. Mol Cancer Ther. 2014;13(8):2127–2137.
   Web of Science ®Google Scholar
• Jonasch E, Haluska FG. Interferon in oncological practice: review of interferon biology, clinical applications, and toxicities. Oncologist. 2001;6(1):34–55.
   PubMed Web of Science ®Google Scholar
• Kirkwood JM, Ernstoff MS. Interferons in the treatment of human cancer. J Clin Oncol. 1984;2(4):336–352.
   PubMed Web of Science ®Google Scholar
• Fang JY, Al-Suwayeh SA. Nanoparticles as delivery carriers for anticancer prodrugs. Expert Opin Drug Deliv. 2012;9(6):657–669.
   PubMed Web of Science ®Google Scholar
• You MH, Kim WJ, Shim W, et al. Cytosine deaminase-producing human mesenchymal stem cells mediate an antitumor effect in a mouse xenograft model. J Gastroenterol Hepatol. 2009;24(8):1393–1400.
   Web of Science ®Google Scholar
• Moolten FL. Tumor chemosensitivity conferred by inserted herpes thymidine kinase genes: paradigm for a prospective cancer control strategy. Cancer Res. 1986;46(10):5276–5281.
   PubMed Web of Science ®Google Scholar
• Rubsam LZ, Davidson BL, Shewach DS. Superior cytotoxicity with ganciclovir compared with acyclovir and 1-beta-D-arabinofuranosylthymine in herpes simplex virus-thymidine kinase-expressing cells: a novel paradigm for cell killing. Cancer Res. 1998;58(17):3873–3882.
   Web of Science ®Google Scholar
• Craperi D, Vicat JM, Nissou MF, et al. Increased bax expression is associated with cell death induced by ganciclovir in a herpes thymidine kinase gene-expressing glioma cell line. Hum Gene Ther. 1999;10(4):679–688.
   Web of Science ®Google Scholar
• Ishii-Morita H, Agbaria R, Mullen CA, et al. Mechanism of ‘bystander effect’ killing in the herpes simplex thymidine kinase gene therapy model of cancer treatment. Gene Ther. 1997;4(3):244–251.
   PubMed Web of Science ®Google Scholar
• Mesnil M, Piccoli C, Tiraby G, et al. Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins. Proc Natl Acad Sci U S A. 1996;93(5):1831–1835.
   PubMed Web of Science ®Google Scholar
• Mueller LP, Luetzkendorf J, Widder M, et al. TRAIL-transduced multipotent mesenchymal stromal cells (TRAIL-MSC) overcome TRAIL resistance in selected CRC cell lines in vitro and in vivo. Cancer Gene Ther. 2011;18(4):229–239.
   PubMed Web of Science ®Google Scholar
• Luetzkendorf J, Mueller LP, Mueller T, et al. Growth inhibition of colorectal carcinoma by lentiviral TRAIL-transgenic human mesenchymal stem cells requires their substantial intratumoral presence. J Cell Mol Med. 2010;14(9):2292–2304.
   Web of Science ®Google Scholar
• Grisendi G, Bussolari R, Cafarelli L, et al. Adipose-derived mesenchymal stem cells as stable source of tumor necrosis factor-related apoptosis-inducing ligand delivery for cancer therapy. Cancer Res. 2010;70(9):3718–3729.
   PubMed Web of Science ®Google Scholar
• Moniri MR, Sun XY, Rayat J, et al. TRAIL-engineered pancreas-derived mesenchymal stem cells: characterization and cytotoxic effects on pancreatic cancer cells. Cancer Gene Ther. 2012;19(9):652–658.
   PubMed Web of Science ®Google Scholar
• Deng Q, Zhang Z, Feng X, et al. TRAIL-secreting mesenchymal stem cells promote apoptosis in heat-shock-treated liver cancer cells and inhibit tumor growth in nude mice. Gene Ther. 2014;21(3):317–327.
   PubMed Web of Science ®Google Scholar
• Yan C, Yang M, Li Z, et al. Suppression of orthotopically implanted hepatocarcinoma in mice by umbilical cord-derived mesenchymal stem cells with sTRAIL gene expression driven by AFP promoter. Biomaterials. 2014;35(9):3035–3043.
   PubMed Web of Science ®Google Scholar
• Sun XY, Nong J, Qin K, et al. MSC(TRAIL)-mediated HepG2 cell death in direct and indirect co-cultures. Anticancer Res. 2011;31(11):3705–3712.
   PubMed Web of Science ®Google Scholar
• Xin L, Xu R, Zhang Q, et al. Kringle 1 of human hepatocyte growth factor inhibits bovine aortic endothelial cell proliferation stimulated by basic fibroblast growth factor and causes cell apoptosis. Biochem Biophys Res Commun. 2000;277(1):186–190.
   PubMed Web of Science ®Google Scholar
• Kuba K, Matsumoto K, Ohnishi K, et al. Kringle 1–4 of hepatocyte growth factor inhibits proliferation and migration of human microvascular endothelial cells. Biochem Biophys Res Commun. 2000;279(3):846–852.
   Web of Science ®Google Scholar
• Zhu Y, Cheng M, Yang Z, et al. Mesenchymal stem cell-based NK4 gene therapy in nude mice bearing gastric cancer xenografts. Drug Des Devel Ther. 2014;8:2449–2462.
   PubMed Web of Science ®Google Scholar
• Francois A, Milliat F, Guipaud O, et al. Inflammation and immunity in radiation damage to the gut mucosa. Biomed Res Int. 2013;2013:123241.
   PubMed Web of Science ®Google Scholar
• Chapel A, Bertho JM, Bensidhoum M, et al. Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J Gene Med. 2003;5(12):1028–1038.
   PubMed Web of Science ®Google Scholar
• Zielske SP, Livant DL, Lawrence TS. Radiation increases invasion of gene-modified mesenchymal stem cells into tumors. Int J Radiat Oncol Biol Phys. 2009;75(3):843–853.
   PubMed Web of Science ®Google Scholar
• Knoop K, Kolokythas M, Klutz K, et al. Image-guided, tumor stroma-targeted 131I therapy of hepatocellular cancer after systemic mesenchymal stem cell-mediated NIS gene delivery. Mol Ther. 2011;19(9):1704–1713.
   Web of Science ®Google Scholar
• Chen MF, Lin CT, Chen WC, et al. The sensitivity of human mesenchymal stem cells to ionizing radiation. Int J Radiat Oncol Biol Phys. 2006;66(1):244–253.
   PubMed Web of Science ®Google Scholar