The (in) auspicious role of mesenchymal stromal cells in cancer: be it friend or foe

References

• Albini A, Sporn MB. The tumour microenvironment as a target for chemoprevention. Nat Rev Cancer 2007; 7: 139–47
   PubMed Web of Science ®Google Scholar
• Bazzoni G. Signalling pathways and adhesion molecules as targets for antiangiogenesis therapy in tumors. Adv Exp Med Biol 2008; 610: 74–87
   PubMed Web of Science ®Google Scholar
• Hall B, Andreeff M, Marini F. The participation of mesenchymal stem cells in tumor stroma formation and their application as targeted-gene delivery vehicles. Handb Exp Pharmacol 2007:263–83.
   Google Scholar
• Bhowmick NA, Chytil A, Plieth D, et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004; 303: 848–51
   PubMed Web of Science ®Google Scholar
• Kiaris H, Chatzistamou I, Trimis G, et al. Evidence for nonautonomous effect of p53 tumor suppressor in carcinogenesis. Cancer Res 2005; 65: 1627–30
   PubMedGoogle Scholar
• Ries C, Egea V, Karow M, et al. MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines. Blood 2007; 109: 4055–63
   PubMed Web of Science ®Google Scholar
• Silzle T, Randolph GJ, Kreutz M, et al. The fibroblast: sentinel cell and local immune modulator in tumor tissue. Int J Cancer 2004; 108: 173–80
   PubMed Web of Science ®Google Scholar
• Spaeth E, Klopp A, Dembinski J, et al. Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther 2008; 15: 730–8
   PubMed Web of Science ®Google Scholar
• Menon LG, Picinich S, Koneru R, et al. Differential gene expression associated with migration of mesenchymal stem cells to conditioned medium from tumor cells or bone marrow cells. Stem Cells 2007; 25: 520–8
   PubMed Web of Science ®Google Scholar
• Li Y, Yu X, Lin S, et al. Insulin-like growth factor 1 enhances the migratory capacity of mesenchymal stem cells. Biochem Biophys Res Commun 2007; 356: 780–4
   PubMed Web of Science ®Google Scholar
• Mira E, Lacalle RA, Gonzalez MA, et al. A role for chemokine receptor transactivation in growth factor signaling. EMBO Rep 2001; 2: 151–6
   Web of Science ®Google Scholar
• Dwyer RM, Potter-Beirne SM, Harrington KA, et al. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res 2007; 13: 5020–7
   PubMed Web of Science ®Google Scholar
• Sivridis E, Giatromanolaki A, Koukourakis MI. Proliferating fibroblasts at the invading tumour edge of colorectal adenocarcinomas are associated with endogenous markers of hypoxia, acidity, and oxidative stress. J Clin Pathol 2005; 58: 1033–8
   PubMed Web of Science ®Google Scholar
• Kammertoens T, Schuler T, Blankenstein T. Immunotherapy: target the stroma to hit the tumor. Trends Mol Med 2005; 11: 225–31
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143–7
   PubMed Web of Science ®Google Scholar
• Koh SH, Kim KS, Choi MR, et al. Implantation of human umbilical cord-derived mesenchymal stem cells as a neuroprotective therapy for ischemic stroke in rats. Brain Res. 2008
   Google Scholar
• Pijnappels DA, Schalij MJ, Ramkisoensing AA, et al. Forced alignment of mesenchymal stem cells undergoing cardiomyogenic differentiation affects functional integration with cardiomyocyte cultures. Circ Res 2008; 103: 167–76
   PubMed Web of Science ®Google Scholar
• Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007; 110: 3499–506
   PubMed Web of Science ®Google Scholar
• Almeida-Porada G, Porada C, Zanjani ED. Plasticity of human stem cells in the fetal sheep model of human stem cell transplantation. Int J Hematol 2004; 79: 1–6
   Google Scholar
• Allers C, Sierralta WD, Neubauer S, et al. Dynamic of distribution of human bone marrow-derived mesenchymal stem cells after transplantation into adult unconditioned mice. Transplantation 2004; 78: 503–8
   PubMed Web of Science ®Google Scholar
• Erices AA, Allers CI, Conget PA, et al. Human cord blood-derived mesenchymal stem cells home and survive in the marrow of immunodeficient mice after systemic infusion. Cell Transplant 2003; 12: 555–61
   PubMed Web of Science ®Google Scholar
• Natsu K, Ochi M, Mochizuki Y, et al. Allogeneic bone marrow-derived mesenchymal stromal cells promote the regeneration of injured skeletal muscle without differentiation into myofibers. Tissue Eng 2004; 10: 1093–112
   PubMedGoogle Scholar
• Silva GV, Litovsky S, Assad JA, et al. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 2005; 111: 150–6
   PubMed Web of Science ®Google Scholar
• Sato Y, Araki H, Kato J, et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005; 106: 756–63
   PubMed Web of Science ®Google Scholar
• Kurozumi K, Nakamura K, Tamiya T, et al. BDNF gene-modified mesenchymal stem cells promote functional recovery and reduce infarct size in the rat middle cerebral artery occlusion model. Mol Ther 2004; 9: 189–97
   PubMed Web of Science ®Google Scholar
• Phinney DG, Isakova I. Plasticity and therapeutic potential of mesenchymal stem cells in the nervous system. Curr Pharm Des 2005; 11: 1255–65
   PubMed Web of Science ®Google Scholar
• Rojas M, Xu J, Woods CR, et al. Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol 2005; 33: 145–52
   PubMed Web of Science ®Google Scholar
• Chen J, Li Y, Wang L, et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001; 32: 1005–11
   PubMed Web of Science ®Google Scholar
• Barbash IM, Chouraqui P, Baron J, et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 2003; 108: 863–8
   PubMed Web of Science ®Google Scholar
• Mahmood A, Lu D, Lu M , et al. Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery 2003;53:697–702; discussion 3.
   PubMed Web of Science ®Google Scholar
• Ortiz LA, Gambelli F, McBride C, et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 2003; 100: 8407–11
   PubMed Web of Science ®Google Scholar
• Wu GD, Nolta JA, Jin YS, et al. Migration of mesenchymal stem cells to heart allografts during chronic rejection. Transplantation 2003; 75: 679–85
   PubMedGoogle Scholar
• Brooke G, Cook M, Blair C, et al. Therapeutic applications of mesenchymal stromal cells. Semin Cell Dev Biol 2007; 18: 846–58
   PubMed Web of Science ®Google Scholar
• Chiu RC. Stealth immune tolerance’ in stem cell transplantation: potential for ‘universal donors’ in myocardial regenerative therapy. J Heart Lung Transplant 2005; 24: 511–6
   Google Scholar
• Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002; 99: 3838–43
   PubMed Web of Science ®Google Scholar
• Krampera M, Glennie S, Dyson J, et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003; 101: 3722–9
   PubMed Web of Science ®Google Scholar
• Plumas J, Chaperot L, Richard MJ, et al. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 2005; 19: 1597–604
   PubMed Web of Science ®Google Scholar
• Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005; 106: 1755–61
   PubMed Web of Science ®Google Scholar
• Rutella S, Danese S, Leone G. Tolerogenic dendritic cells: cytokine modulation comes of age. Blood 2006; 108: 1435–40
   PubMed Web of Science ®Google Scholar
• Corcione A, Benvenuto F, Ferretti E, et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006; 107: 367–72
   PubMed Web of Science ®Google Scholar
• Sotiropoulou PA, Perez SA, Gritzapis AD, et al. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 2006; 24: 74–85
   PubMed Web of Science ®Google Scholar
• Ringden O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006; 81: 1390–7
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Pittenger M. Mesenchymal stem cells: progress toward promise. Cytotherapy 2005; 7: 36–45
   PubMed Web of Science ®Google Scholar
• Kinnaird T, Stabile E, Burnett MS, et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004; 94: 678–85
   PubMed Web of Science ®Google Scholar
• Potapova IA, Gaudette GR, Brink PR, et al. Mesenchymal stem cells support migration, extracellular matrix invasion, proliferation, and survival of endothelial cells in vitro. Stem Cells 2007; 25: 1761–8
   PubMed Web of Science ®Google Scholar
• Traktuev DO, Merfeld-Clauss S, Li J, et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 2008; 102: 77–85
   PubMed Web of Science ®Google Scholar
• Al-Khaldi A, Eliopoulos N, Martineau D, et al. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther 2003; 10: 621–9
   PubMed Web of Science ®Google Scholar
• Bolontrade M, Worth L, Zhou R, et al. Bone marrow side population cells contribute to neovessel formation in Ewing's sarcoma. Stem Cell Cellular Ther 2003; 1: 14–20
   Google Scholar
• Rajantie I, Ilmonen M, Alminaite A, et al. Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood 2004; 104: 2084–86
   PubMed Web of Science ®Google Scholar
• Dore-Duffy P, Katychev A, Wang X, et al. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 2006; 26: 613–24
   PubMed Web of Science ®Google Scholar
• Ball SG, Shuttleworth CA, Kielty CM. Mesenchymal stem cells and neovascularization: role of platelet-derived growth factor receptors. J Cell Mol Med 2007; 11: 1012–30
   PubMed Web of Science ®Google Scholar
• Roorda BD, Ter Elst A, Kamps WA , et al. 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 2008.
   Google Scholar
• Emura M, Ochiai A, Horino M, et al. Development of myofibroblasts from human bone marrow mesenchymal stem cells cocultured with human colon carcinoma cells and TGF beta 1. In Vitro Cell Dev Biol Anim 2000; 36: 77–80
   Google Scholar
• Mishra PJ, Humeniuk R, Medina DJ, et al. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res 2008; 68: 4331–39
   PubMed Web of Science ®Google Scholar
• Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986; 315: 1650–9
   PubMed Web of Science ®Google Scholar
• Prindull G, Zipori D. Environmental guidance of normal and tumor cell plasticity: epithelial mesenchymal transitions as a paradigm. Blood 2004; 103: 2892–9
   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: 267–74
   PubMed Web of Science ®Google Scholar
• Houghton J, Stoicov C, Nomura S, et al. Gastric cancer originating from bone marrow-derived cells. Science 2004; 306: 1568–71
   PubMed Web of Science ®Google Scholar
• Nakamizo A, Marini F, Amano T, et al. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 2005; 65: 3307–18
   PubMed Web of Science ®Google Scholar
• Studeny M, Marini FC, Champlin RE, et al. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res 2002; 62: 3603–8
   PubMed Web of Science ®Google Scholar
• Studeny M, Marini FC, Dembinski JL, et al. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst 2004; 96: 1593–603
   PubMed Web of Science ®Google Scholar
• De Palma M, Venneri MA, Galli R, et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005; 8: 211–26
   PubMed Web of Science ®Google Scholar
• De Palma M, Venneri MA, Roca C, et al. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 2003; 9: 789–95
   PubMed Web of Science ®Google Scholar
• Hall B, Dembinski J, Sasser AK, et al. Mesenchymal stem cells in cancer: tumor-associated fibroblasts and cell-based delivery vehicles. Int J Hematol 2007; 86: 8–16
   PubMed Web of Science ®Google Scholar
• Wright N, de Lera TL, Garcia-Moruja C, et al. Transforming growth factor-beta1 down-regulates expression of chemokine stromal cell-derived factor-1: functional consequences in cell migration and adhesion. Blood 2003; 102: 1978–84
   PubMed Web of Science ®Google Scholar
• Forbes SJ, Russo FP, Rey V, et al. A significant proportion of myofibroblasts are of bone marrow origin in human liver fibrosis. Gastroenterology 2004; 126: 955–63
   PubMed Web of Science ®Google Scholar
• Ishii G, Sangai T, Oda T, et al. Bone-marrow-derived myofibroblasts contribute to the cancer-induced stromal reaction. Biochem Biophys Res Commun 2003; 309: 232–40
   Google Scholar
• Direkze NC, Hodivala-Dilke K, Jeffery R, et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 2004; 64: 8492–5
   PubMed Web of Science ®Google Scholar
• Roni V, Habeler W, Parenti A, et al. Recruitment of human umbilical vein endothelial cells and human primary fibroblasts into experimental tumors growing in SCID mice. Exp Cell Res 2003; 287: 28–38
   Google Scholar
• Jankowski K, Kucia M, Wysoczynski M, et al. Both hepatocyte growth factor (HGF) and stromal-derived factor-1 regulate the metastatic behavior of human rhabdomyosarcoma cells, but only HGF enhances their resistance to radiochemotherapy. Cancer Res 2003; 63: 7926–35
   PubMed Web of Science ®Google Scholar
• Yoneda T, Hiraga T. Crosstalk between cancer cells and bone microenvironment in bone metastasis. Biochem Biophys Res Commun 2005; 328: 679–87
   PubMed 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: 11687–95
   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: 3837–44
   PubMed Web of Science ®Google Scholar
• Djouad F, Bony C, Apparailly F, et al. Earlier onset of syngeneic tumors in the presence of mesenchymal stem cells. Transplantation 2006; 82: 1060–6
   PubMed Web of Science ®Google Scholar
• Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007; 449: 557–63
   PubMed Web of Science ®Google Scholar
• Yu JM, Jun ES, Bae YC, et al. Mesenchymal stem cells derived from human adipose tissues favor tumor cell growth in vivo. Stem Cells Dev 2008; 17: 463–73
   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: 663–7
   Web of Science ®Google Scholar
• Ohlsson LB, Varas L, Kjellman C, et al. Mesenchymal progenitor cell-mediated inhibition of tumor growth in vivo and in vitro in gelatin matrix. Exp Mol Pathol 2003; 75: 248–55
   PubMed Web of Science ®Google Scholar
• Nakamura K, Ito Y, Kawano Y, et al. Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther 2004; 11: 1155–64
   PubMed Web of Science ®Google Scholar
• Khakoo AY, Pati S, Anderson SA, et al. Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med 2006; 203: 1235–47
   PubMed Web of Science ®Google Scholar
• Markowitz CE. Interferon-beta: mechanism of action and dosing issues. Neurology 2007; 68: S8–11
   PubMed Web of Science ®Google Scholar
• Vannucchi S, Chiantore MV, Mangino G, et al. Perspectives in biomolecular therapeutic intervention in cancer: from the early to the new strategies with type I interferons. Curr Med Chem 2007; 14: 667–79
   Google Scholar
• Hurwitz DR, Kirchgesser M, Merrill W, et al. Systemic delivery of human growth hormone or human factor IX in dogs by reintroduced genetically modified autologous bone marrow stromal cells. Hum Gene Ther 1997; 8: 137–56
   PubMed Web of Science ®Google Scholar
• Evans CH, Robbins PD, Ghivizzani SC, et al. Gene transfer to human joints: progress toward a gene therapy of arthritis. Proc Natl Acad Sci USA 2005; 102: 8698–703
   PubMed Web of Science ®Google Scholar
• Kurozumi K, Nakamura K, Tamiya T, et al. Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model. Mol Ther 2005; 11: 96–104
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Tammik L, Sundberg B, et al. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 2003; 57: 11–20
   PubMed Web of Science ®Google Scholar