Mesenchymal stem cells - A new hope for radiotherapy-induced tissue damage?

Cancer Letters

Volumn 366, Issue 2, 2015, Pages 133-140

  Nicolay, Nils H ^a,b,c   Lopez Perez, Ramon ^b,c   Debus, Juergen ^a,b   Huber, Peter E ^a,b,c  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b Heidelberg Institute for Radiation Oncology (HIRO)   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Acute radiation injury; Fibrosis; Mesenchymal stem cell; Radiotherapy; Side effect

Indexed keywords

BONE INJURY; BONE MARROW DISEASE; CANCER RADIOTHERAPY; CARCINOGENICITY; CELL DIFFERENTIATION; CELL FUNCTION; HUMAN; INTESTINE INJURY; IONIZING RADIATION; LIVER INJURY; LUNG INJURY; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; RADIATION INJURY; RADIATION PROTECTION; RADIOSENSITIVITY; SALIVARY GLAND DISEASE; SHORT SURVEY; SKIN INJURY; STANDARDIZATION; TISSUE INJURY; TISSUE REGENERATION; TISSUE SPECIFICITY; WHOLE BODY RADIATION; BONE; BONE MARROW; CELL PROLIFERATION; FUNCTIONS OF THE SKIN AND ITS APPENDAGES; INTESTINE; LIVER; LUNG; MESENCHYMAL STROMA CELL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIATION INJURIES; RADIATION RESPONSE; REGENERATION; SALIVARY GLAND;

ANIMALIA;

BONE AND BONES; BONE MARROW; CELL PROLIFERATION; HUMANS; INTESTINES; LIVER; LUNG; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; RADIATION INJURIES; REGENERATION; SALIVARY GLANDS; SKIN PHYSIOLOGICAL PHENOMENA;

EID: 84937825529     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.06.012     Document Type: Review

References (130)

1. Friedenstein A.J., Deriglasova U.F., Kulagina N.N., et al. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp. Hematol 1974, 2:83-92.
2. Pittenger M.F., Mackay A.M., Beck S.C., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
3. Ho A.D., Wagner W., Franke W. Heterogeneity of mesenchymal stromal cell preparations. Cytotherapy 2008, 10:320-330.
4. Morikawa S., Mabuchi Y., Kubota Y., et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med 2009, 206:2483-2496.
5. Tolar J., Nauta A.J., Osborn M.J., et al. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 2007, 25:371-379.
6. Chen B.Y., Wang X., Chen L.W., et al. Molecular targeting regulation of proliferation and differentiation of the bone marrow-derived mesenchymal stem cells or mesenchymal stromal cells. Curr. Drug Targets 2012, 13:561-571.
7. 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, 8:315-317.
8. Nicolay N.H., Lopez Perez R., Saffrich R., et al. Radio-resistant mesenchymal stem cells - mechanisms of resistance and potential implications for the clinic. Oncotarget 2015.
9. Nicolay N.H., Liang Y., Lopez Perez R., et al. Mesenchymal stem cells are resistant to carbon ion radiotherapy. Oncotarget. 2015, 6:2076-2087.
10. Nicolay N.H., Sommer E., Lopez R., et al. Mesenchymal stem cells retain their defining stem cell characteristics after exposure to ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys 2013, 87:1171-1178.
11. Nicolay N.H., Sommer E., Perez R.L., et al. Mesenchymal stem cells are sensitive to treatment with kinase inhibitors and ionizing radiation. Strahlenther. Onkol 2014, 190:1037-1045.
12. Chen M.F., Lin C.T., Chen W.C., et al. The sensitivity of human mesenchymal stem cells to ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys 2006, 66:244-253.
13. Sugrue T., Lowndes N.F., Ceredig R. Mesenchymal stromal cells: radio-resistant members of the bone marrow. Immunol. Cell Biol 2013, 91:5-11.
14. Singh S., Kloss F.R., Brunauer R., et al. Mesenchymal stem cells show radioresistance in vivo. J. Cell. Mol. Med 2012, 16:877-887.
15. Sugrue T., Brown J.A., Lowndes N.F., et al. Multiple facets of the DNA damage response contribute to the radio-resistance of mouse mesenchymal stromal cell lines. Stem Cells 2012.
16. Chow A., Lucas D., Hidalgo A., et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J. Exp. Med 2011, 208:261-271.
17. Schraufstatter I.U., Discipio R.G., Khaldoyanidi S. Mesenchymal stem cells and their microenvironment. Front. Biosci 2011, 16:2271-2288.
18. Anthony B.A., Link D.C. Regulation of hematopoietic stem cells by bone marrow stromal cells. Trends Immunol 2014, 35:32-37.
19. Gomez-Gaviro M.V., Lovell-Badge R., Fernandez-Aviles F., et al. The vascular stem cell niche. J. Cardiovasc. Transl. Res. 2012, 5:618-630.
20. Leeman K.T., Fillmore C.M., Kim C.F. Lung stem and progenitor cells in tissue homeostasis and disease. Curr. Top. Dev. Biol 2014, 107:207-233.
21. Shi C., Lv T., Xiang Z., et al. Role of Wnt/beta-catenin signaling in epithelial differentiation of lung resident mesenchymal stem cells. J. Cell. Biochem 2015, 116:1532-1539.
22. Alimperti S., You H., George T., et al. Cadherin-11 regulates both mesenchymal stem cell differentiation into smooth muscle cells and the development of contractile function in vivo. J. Cell Sci 2014, 127:2627-2638.
23. Nedeau A.E., Bauer R.J., Gallagher K., et al. A CXCL5- and bFGF-dependent effect of PDGF-B-activated fibroblasts in promoting trafficking and differentiation of bone marrow-derived mesenchymal stem cells. Exp. Cell Res 2008, 314:2176-2186.
24. Kalinina N.I., Sysoeva V.Y., Rubina K.A., et al. Mesenchymal stem cells in tissue growth and repair. Acta Naturae 2011, 3:30-37.
25. Ulivi V., Tasso R., Cancedda R., et al. Mesenchymal stem cell paracrine activity is modulated by platelet lysate: induction of an inflammatory response and secretion of factors maintaining macrophages in a proinflammatory phenotype. Stem Cells Dev 2014, 23:1858-1869.
26. Linero I., Chaparro O. Paracrine effect of mesenchymal stem cells derived from human adipose tissue in bone regeneration. PLoS ONE 2014, 9. e107001.
27. Liang X., Ding Y., Zhang Y., et al. Paracrine mechanisms of mesenchymal stem cell-based therapy: current status and perspectives. Cell Transplant 2014, 23:1045-1059.
28. Granero-Molto F., Myers T.J., Weis J.A., et al. Mesenchymal stem cells expressing insulin-like growth factor-I (MSCIGF) promote fracture healing and restore new bone formation in Irs1 knockout mice: analyses of MSCIGF autocrine and paracrine regenerative effects. Stem Cells 2011, 29:1537-1548.
29. Zhang Y., Liang X., Lian Q., et al. Perspective and challenges of mesenchymal stem cells for cardiovascular regeneration. Expert Rev. Cardiovasc. Ther 2013, 11:505-517.
30. Wilson J.G., Liu K.D., Zhuo H., et al. Mesenchymal stem (stromal) cells for treatment of ARDS: a phase 1 clinical trial. Lancet Respir. Med 2015, 3:24-32.
31. Jo C.H., Lee Y.G., Shin W.H., et al. Intra-articular injection of mesenchymal stem cells for the treatment of osteoarthritis of the knee: a proof-of-concept clinical trial. Stem Cells 2014, 32:1254-1266.
32. Williams A.R., Hare J.M. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ. Res 2011, 109:923-940.
33. van Bekkum D.W. Radiation sensitivity of the hemopoietic stem cell. Radiat. Res 1991, 128:S4-S8.
34. Adkins D.R., DiPersio J.F. Total body irradiation before an allogeneic stem cell transplantation: is there a magic dose?. Curr. Opin. Hematol 2008, 15:555-560.
35. Cosset J.M., Socie G., Dubray B., et al. Single dose versus fractionated total body irradiation before bone marrow transplantation: radiobiological and clinical considerations. Int. J. Radiat. Oncol. Biol. Phys 1994, 30:477-492.
36. Abdel-Mageed A.S., Senagore A.J., Pietryga D.W., et al. Intravenous administration of mesenchymal stem cells genetically modified with extracellular superoxide dismutase improves survival in irradiated mice. Blood 2009, 113:1201-1203.
37. Hu K.X., Sun Q.Y., Guo M., et al. The radiation protection and therapy effects of mesenchymal stem cells in mice with acute radiation injury. Br. J. Radiol 2010, 83:52-58.
38. Lange C., Brunswig-Spickenheier B., Cappallo-Obermann H., et al. Radiation rescue: mesenchymal stromal cells protect from lethal irradiation. PLoS ONE 2011, 6. e14486.
39. Konoplyannikov A.G., Petriev V.M., Konoplyannikova O.A., et al. Effects of (60)co whole-body gamma-irradiation in different doses on the distribution of (188)Re-labeled autologous mesenchymal stem cells in wistar rats after intravenous (systemic) transplantation during different periods after exposure. Bull. Exp. Biol. Med 2008, 145:520-525.
40. Francois 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, 24:1020-1029.
41. Mouiseddine M., Francois S., Semont A., et al. Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model. Br. J. Radiol 2007, 80(Spec No 1):S49-S55.
42. Chapel A., Bertho J.M., 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, 5:1028-1038.
43. Drouet M., Mourcin F., Grenier N., et al. Mesenchymal stem cells rescue CD34+ cells from radiation-induced apoptosis and sustain hematopoietic reconstitution after coculture and cografting in lethally irradiated baboons: is autologous stem cell therapy in nuclear accident settings hype or reality?. Bone Marrow Transplant 2005, 35:1201-1209.
44. Yang X., Balakrishnan I., Torok-Storb B., et al. Marrow stromal cell infusion rescues hematopoiesis in lethally irradiated mice despite rapid clearance after infusion. Adv. Hematol. 2012, 2012:142530.
45. Liu S., Hu P., Hou Y., et al. The additive effect of mesenchymal stem cells and bone morphogenetic protein 2 on gamma-irradiated bone marrow in mice. Cell Biochem. Biophys 2011, 61:539-550.
46. Nemeth K., Leelahavanichkul A., Yuen P.S., et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med 2009, 15:42-49.
47. Chapel A., Francois S., Douay L., et al. Fifteen years of preclinical and clinical experiences about biotherapy treatment of lesions induced by accidental irradiation and radiotherapy. World J. Stem Cells 2013, 5:68-72.
48. Dawson L.A., Normolle D., Balter J.M., et al. Analysis of radiation-induced liver disease using the Lyman NTCP model. Int. J. Radiat. Oncol. Biol. Phys 2002, 53:810-821.
49. Mouiseddine M., Francois S., Souidi M., et al. Intravenous human mesenchymal stem cells transplantation in NOD/SCID mice preserve liver integrity of irradiation damage. Methods Mol. Biol 2012, 826:179-188.
50. Francois S., Mouiseddine M., Allenet-Lepage B., et al. Human mesenchymal stem cells provide protection against radiation-induced liver injury by antioxidative process, vasculature protection, hepatocyte differentiation, and trophic effects. Biomed Res. Int 2013, 2013:151679.
51. Huang C.K., Lee S.O., Luo J., et al. A mouse model of liver injury to evaluate paracrine and endocrine effects of bone marrow mesenchymal stem cells. Methods Mol. Biol 2014, 1213:69-79.
52. Shao C.H., Chen S.L., Dong T.F., et al. Transplantation of bone marrow-derived mesenchymal stem cells after regional hepatic irradiation ameliorates thioacetamide-induced liver fibrosis in rats. J. Surg. Res 2014, 186:408-416.
53. Zhang J., Zhou S., Zhou Y., et al. Hepatocyte growth factor gene-modified adipose-derived mesenchymal stem cells ameliorate radiation induced liver damage in a rat model. PLoS ONE 2014, 9. e114670.
54. Chapel A., Francois S., Douay L., et al. New insights for pelvic radiation disease treatment: multipotent stromal cell is a promise mainstay treatment for the restoration of abdominopelvic severe chronic damages induced by radiotherapy. World J. Stem Cells 2013, 5:106-111.
55. Kudo K., Liu Y., Takahashi K., et al. Transplantation of mesenchymal stem cells to prevent radiation-induced intestinal injury in mice. J. Radiat. Res. (Tokyo) 2010, 51:73-79.
56. Chang P., Qu Y., Liu Y., et al. Multi-therapeutic effects of human adipose-derived mesenchymal stem cells on radiation-induced intestinal injury. Cell Death Dis 2013, 4:e685.
57. Semont A., Francois S., Mouiseddine M., et al. Mesenchymal stem cells increase self-renewal of small intestinal epithelium and accelerate structural recovery after radiation injury. Adv. Exp. Med. Biol 2006, 585:19-30.
58. Saha S., Bhanja P., Kabarriti R., et al. Bone marrow stromal cell transplantation mitigates radiation-induced gastrointestinal syndrome in mice. PLoS ONE 2011, 6. e24072.
59. Semont A., Mouiseddine M., Francois A., et al. Mesenchymal stem cells improve small intestinal integrity through regulation of endogenous epithelial cell homeostasis. Cell Death Differ 2010, 17:952-961.
60. Zhang J., Gong J.F., Zhang W., et al. Effects of transplanted bone marrow mesenchymal stem cells on the irradiated intestine of mice. J. Biomed. Sci 2008, 15:585-594.
61. Gao Z., Zhang Q., Han Y., et al. Mesenchymal stromal cell-conditioned medium prevents radiation-induced small intestine injury in mice. Cytotherapy 2012, 14:267-273.
62. Francois M., Birman E., Forner K.A., et al. Adoptive transfer of mesenchymal stromal cells accelerates intestinal epithelium recovery of irradiated mice in an interleukin-6-dependent manner. Cytotherapy 2012, 14:1164-1170.
63. Roeder F., Friedrich J., Timke C., et al. Correlation of patient-related factors and dose-volume histogram parameters with the onset of radiation pneumonitis in patients with small cell lung cancer. Strahlenther. Onkol 2010, 186:149-156.
64. Flechsig P., Dadrich M., Bickelhaupt S., et al. LY2109761 attenuates radiation-induced pulmonary murine fibrosis via reversal of TGF-beta and BMP-associated proinflammatory and proangiogenic signals. Clin. Cancer Res. 2012, 18:3616-3627.
65. Li M., Abdollahi A., Grone H.J., et al. Late treatment with imatinib mesylate ameliorates radiation-induced lung fibrosis in a mouse model. Radiat. Oncol. 2009, 4:66.
66. Abdollahi A., Li M., Ping G., et al. Inhibition of platelet-derived growth factor signaling attenuates pulmonary fibrosis. J. Exp. Med 2005, 201:925-935.
67. Wang R., Zhu C.Z., Qiao P., et al. Experimental treatment of radiation pneumonitis with human umbilical cord mesenchymal stem cells. Asian Pac. J. Trop. Med 2014, 7:262-266.
68. Yan X., Liu Y., Han Q., et al. Injured microenvironment directly guides the differentiation of engrafted Flk-1(+) mesenchymal stem cell in lung. Exp. Hematol 2007, 35:1466-1475.
69. Xue J., Li X., Lu Y., et al. Gene-modified mesenchymal stem cells protect against radiation-induced lung injury. Mol. Ther 2013, 21:456-465.
70. Wang H., Yang Y.F., Zhao L., et al. Hepatocyte growth factor gene-modified mesenchymal stem cells reduce radiation-induced lung injury. Hum. Gene Ther 2013, 24:343-353.
71. Kursova L.V., Konoplyannikov A.G., Pasov V.V., et al. Possibilities for the use of autologous mesenchymal stem cells in the therapy of radiation-induced lung injuries. Bull. Exp. Biol. Med 2009, 147:542-546.
72. Graham M.V., Pajak T.E., Herskovic A.M., et al. Phase I/II study of treatment of locally advanced (T3/T4) non-oat cell lung cancer with concomitant boost radiotherapy by the Radiation Therapy Oncology Group (RTOG 83-12): long-term results. Int. J. Radiat. Oncol. Biol. Phys 1995, 31:819-825.
73. Chen J., Wang C., Wong Y., et al. Osteoradionecrosis of mandible bone in oral cancer patients - associated factors and treatment outcomes. Head Neck 2014.
74. Zhang W.B., Zheng L.W., Chua D.T., et al. Treatment of irradiated mandibles with mesenchymal stem cells transfected with bone morphogenetic protein 2/7. J. Oral Maxillofac. Surg. 2012, 70:1711-1716.
75. Xu J., Zheng Z., Fang D., et al. Mesenchymal stromal cell-based treatment of jaw osteoradionecrosis in Swine. Cell Transplant 2012, 21:1679-1686.
76. Phulpin B., Dolivet G., Marie P.Y., et al. Feasibility of treating irradiated bone with intramedullary delivered autologous mesenchymal stem cells. J. Biomed. Biotechnol. 2011, 2011:560257.
77. Mendonca J.J., Juiz-Lopez P. Regenerative facial reconstruction of terminal stage osteoradionecrosis and other advanced craniofacial diseases with adult cultured stem and progenitor cells. Plast. Reconstr. Surg 2010, 126:1699-1709.
78. Eisbruch A., Ten Haken R.K., Kim H.M., et al. Dose, volume, and function relationships in parotid salivary glands following conformal and intensity-modulated irradiation of head and neck cancer. Int. J. Radiat. Oncol. Biol. Phys 1999, 45:577-587.
79. Lim J.Y., Ra J.C., Shin I.S., et al. Systemic transplantation of human adipose tissue-derived mesenchymal stem cells for the regeneration of irradiation-induced salivary gland damage. PLoS ONE 2013, 8. e71167.
80. Lim J.Y., Yi T., Choi J.S., et al. Intraglandular transplantation of bone marrow-derived clonal mesenchymal stem cells for amelioration of post-irradiation salivary gland damage. Oral Oncol 2013, 49:136-143.
81. Schwarz S., Huss R., Schulz-Siegmund M., et al. Bone marrow-derived mesenchymal stem cells migrate to healthy and damaged salivary glands following stem cell infusion. Int. J. Oral Sci 2014, 6:154-161.
82. Lin C.Y., Chang F.H., Chen C.Y., et al. Cell therapy for salivary gland regeneration. J. Dent. Res 2011, 90:341-346.
83. Lombaert I.M., Wierenga P.K., Kok T., et al. Mobilization of bone marrow stem cells by granulocyte colony-stimulating factor ameliorates radiation-induced damage to salivary glands. Clin. Cancer Res. 2006, 12:1804-1812.
84. Deng W., Han Q., Liao L., et al. Engrafted bone marrow-derived flk-(1+) mesenchymal stem cells regenerate skin tissue. Tissue Eng 2005, 11:110-119.
85. Francois S., Mouiseddine M., Mathieu N., et al. Human mesenchymal stem cells favour healing of the cutaneous radiation syndrome in a xenogenic transplant model. Ann. Hematol 2007, 86:1-8.
86. Riccobono D., Agay D., Scherthan H., et al. Application of adipocyte-derived stem cells in treatment of cutaneous radiation syndrome. Health Phys 2012, 103:120-126.
87. Agay D., Scherthan H., Forcheron F., et al. Multipotent mesenchymal stem cell grafting to treat cutaneous radiation syndrome: development of a new minipig model. Exp. Hematol 2010, 38:945-956.
88. Horton J.A., Hudak K.E., Chung E.J., et al. Mesenchymal stem cells inhibit cutaneous radiation-induced fibrosis by suppressing chronic inflammation. Stem Cells 2013, 31:2231-2241.
89. Kim W.S., Park B.S., Sung J.H. The wound-healing and antioxidant effects of adipose-derived stem cells. Expert Opin. Biol. Ther 2009, 9:879-887.
90. Guo M., Dong Z., Qiao J., et al. Severe acute radiation syndrome: treatment of a lethally 60Co-source irradiated accident victim in China with HLA-mismatched peripheral blood stem cell transplantation and mesenchymal stem cells. J. Radiat. Res. (Tokyo) 2014, 55:205-209.
91. Houghton J., Stoicov C., Nomura S., et al. Gastric cancer originating from bone marrow-derived cells. Science 2004, 306:1568-1571.
92. Tirode F., Laud-Duval K., Prieur A., et al. Mesenchymal stem cell features of Ewing tumors. Cancer Cell 2007, 11:421-429.
93. Matushansky I., Hernando E., Socci N.D., et al. Derivation of sarcomas from mesenchymal stem cells via inactivation of the Wnt pathway. J. Clin. Invest 2007, 117:3248-3257.
94. Torsvik A., Bjerkvig R. Mesenchymal stem cell signaling in cancer progression. Cancer Treat. Rev 2013, 39:180-188.
95. Rubio D., Garcia-Castro J., Martin M.C., et al. Spontaneous human adult stem cell transformation. Cancer Res 2005, 65:3035-3039.
96. Rosland G.V., Svendsen A., Torsvik A., et al. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res 2009, 69:5331-5339.
97. Torsvik A., Rosland G.V., Svendsen A., et al. Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: putting the research field on track - letter. Cancer Res 2010, 70:6393-6396.
98. de la Fuente R., Bernad A., Garcia-Castro J., et al. Retraction: spontaneous human adult stem cell transformation. Cancer Res 2010, 70:6682.
99. Kim E.K., Kim H.J., Yang Y.I., et al. Endogenous gastric-resident mesenchymal stem cells contribute to formation of cancer stroma and progression of gastric cancer. Korean J. Pathol 2013, 47:507-518.
100. Ke C.C., Liu R.S., Suetsugu A., et al. In vivo fluorescence imaging reveals the promotion of mammary tumorigenesis by mesenchymal stromal cells. PLoS ONE 2013, 8. e69658.
101. Ljujic B., Milovanovic M., Volarevic V., et al. Human mesenchymal stem cells creating an immunosuppressive environment and promote breast cancer in mice. Sci. Rep 2013, 3:2298.
102. Lin J.T., Wang J.Y., Chen M.K., et al. Colon cancer mesenchymal stem cells modulate the tumorigenicity of colon cancer through interleukin 6. Exp. Cell Res 2013, 319:2216-2229.
103. De Boeck A., Pauwels P., Hensen K., et al. Bone marrow-derived mesenchymal stem cells promote colorectal cancer progression through paracrine neuregulin 1/HER3 signalling. Gut 2013, 62:550-560.
104. Eterno V., Zambelli A., Pavesi L., et al. Adipose-derived Mesenchymal Stem Cells (ASCs) may favour breast cancer recurrence via HGF/c-Met signaling. Oncotarget. 2014, 5:613-633.
105. Wang L., Zhao Y., Liu Y., et al. IFN-gamma and TNF-alpha synergistically induce mesenchymal stem cell impairment and tumorigenesis via NFkappaB signaling. Stem Cells 2013, 31:1383-1395.
106. Tian K., Yang S., Ren Q., et al. p38 MAPK contributes to the growth inhibition of leukemic tumor cells mediated by human umbilical cord mesenchymal stem cells. Cell. Physiol. Biochem 2010, 26:799-808.
107. Zhu Y., Sun Z., Han Q., et al. Human mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1. Leukemia 2009, 23:925-933.
108. Qiao L., Xu Z., Zhao T., et al. Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res 2008, 18:500-507.
109. Ahn J.O., Coh Y.R., Lee H.W., et al. Human adipose tissue-derived mesenchymal stem cells inhibit melanoma growth in vitro and in vivo. Anticancer Res 2015, 35:159-168.
110. Bianchi G., Morandi F., Cilli M., et al. Close interactions between mesenchymal stem cells and neuroblastoma cell lines lead to tumor growth inhibition. PLoS ONE 2012, 7. e48654.
111. Ahn J.O., Chae J.S., Coh Y.R., et al. Human adipose tissue-derived mesenchymal stem cells inhibit T-cell lymphoma growth in vitro and in vivo. Anticancer Res 2014, 34:4839-4847.
112. Atsuta I., Liu S., Miura Y., et al. Mesenchymal stem cells inhibit multiple myeloma cells via the Fas/Fas ligand pathway. Stem Cell Res. Ther. 2013, 4:111.
113. Yang H.Y., Qu R.M., Lin X.S., et al. IGF-1 from adipose-derived mesenchymal stem cells promotes radioresistance of breast cancer cells. Asian Pac J Cancer Prev. 2014, 15:10115-10119.
114. Klopp A.H., Spaeth E.L., Dembinski J.L., et al. Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res 2007, 67:11687-11695.
115. Sensebe L., Gadelorge M., Fleury-Cappellesso S. Production of mesenchymal stromal/stem cells according to good manufacturing practices: a review. Stem Cell Res. Ther. 2013, 4:66.
116. Verbeek R. Generation of mesenchymal stem cells as a medicinal product in organ transplantation. Curr. Opin. Organ Transplant. 2013, 18:65-70.
117. Pytlik R., Stehlik D., Soukup T., et al. The cultivation of human multipotent mesenchymal stromal cells in clinical grade medium for bone tissue engineering. Biomaterials 2009, 30:3415-3427.
118. Capelli C., Gotti E., Morigi M., et al. Minimally manipulated whole human umbilical cord is a rich source of clinical-grade human mesenchymal stromal cells expanded in human platelet lysate. Cytotherapy 2011, 13:786-801.
119. Bieback K., Schallmoser K., Kluter H., et al. Clinical protocols for the isolation and expansion of mesenchymal stromal cells. Transfus. Med. Hemother 2008, 35:286-294.
120. Aghayan H.R., Goodarzi P., Arjmand B. GMP-compliant human adipose tissue-derived mesenchymal stem cells for cellular therapy. Methods Mol. Biol 2015, 1283:93-107.
121. Bieback K. Platelet lysate as replacement for fetal bovine serum in mesenchymal stromal cell cultures. Transfus. Med. Hemother 2013, 40:326-335.
122. Rojewski M.T., Fekete N., Baila S., et al. GMP-compliant isolation and expansion of bone marrow-derived MSCs in the closed, automated device quantum cell expansion system. Cell Transplant 2013, 22:1981-2000.
123. Kinzebach S., Bieback K. Expansion of Mesenchymal Stem/Stromal cells under xenogenic-free culture conditions. Adv. Biochem. Eng. Biotechnol. 2013, 129:33-57.
124. Caruso S.R., Orellana M.D., Mizukami A., et al. Growth and functional harvesting of human mesenchymal stromal cells cultured on a microcarrier-based system. Biotechnol. Prog 2014, 30:889-895.
125. Dos Santos F., Campbell A., Fernandes-Platzgummer A., et al. A xenogeneic-free bioreactor system for the clinical-scale expansion of human mesenchymal stem/stromal cells. Biotechnol. Bioeng 2014, 111:1116-1127.
126. Mizukami A., Orellana M.D., Caruso S.R., et al. Efficient expansion of mesenchymal stromal cells in a disposable fixed bed culture system. Biotechnol. Prog 2013, 29:568-572.
127. Weber C., Freimark D., Portner R., et al. Expansion of human mesenchymal stem cells in a fixed-bed bioreactor system based on non-porous glass carrier-part A: inoculation, cultivation, and cell harvest procedures. Int. J. Artif. Organs 2010, 33:512-525.
128. Sensebe L., Bourin P., Tarte K. Good manufacturing practices production of mesenchymal stem/stromal cells. Hum. Gene Ther 2011, 22:19-26.
129. Sensebe L. Clinical grade production of mesenchymal stem cells. Biomed Mater. Eng 2008, 18:S3-S10.
130. Torre M.L., Lucarelli E., Guidi S., et al. Ex vivo expanded mesenchymal stromal cell minimal quality requirements for clinical application. Stem Cells Dev 2015, 24:677-685.