Potential implications of mesenchymal stem cells in cancer therapy

Cancer Letters

Volumn 305, Issue 1, 2011, Pages 8-20

  Dai, Long Jun ^a   Moniri, Mani R ^a   Zeng, Zhi Rong ^b   Zhou, Jeff X ^c   Rayat, Jarrett ^a   Warnock, Garth L ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b THE FIRST AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^c NINGBO UNIVERSITY   (China)

Author keywords

Cancer; Cytotherapy; Gene therapy; Mesenchymal stem cells

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; PROTEIN KINASE B; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; WNT PROTEIN;

ANTINEOPLASTIC ACTIVITY; ANTITUMOR GENE; APOPTOSIS; AUTOLOGOUS STEM CELL TRANSPLANTATION; BREAST CANCER; CANCER INHIBITION; CANCER TRANSPLANTATION; CARCINOGENICITY; CELL DIFFERENTIATION; CELL HOMING; CELL RENEWAL; CELL SELECTION; CELL TYPE; CELLULAR DISTRIBUTION; CLONOGENESIS; COLONY FORMING UNIT; COLORECTAL CARCINOMA; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE DELIVERY SYSTEM; GENETIC ENGINEERING; GLIOMA; GRAFT VERSUS HOST REACTION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOSURVEILLANCE; LEUKEMIA; LIVER CELL CARCINOMA; LUNG CARCINOMA; LYMPHOCYTE PROLIFERATION; MALIGNANT TRANSFORMATION; MELANOMA; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METASTASIS; MULTIPOTENT STEM CELL; NONHUMAN; PANCREAS CANCER; PERSONALIZED MEDICINE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SHORT SURVEY; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

EID: 79953187914     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.02.012     Document Type: Review

References (129)

1. Friedenstein A.J., Piatetzky S., Petrakova K.V. Osteogenesis in transplants of bone marrow cells. J. Embryol. Exp. Morphol. 1966, 16:381-390.
2. Friedenstein A.J., Petrakova K.V., Kurolesova A.I., Frolova G.P. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968, 6:230-247.
3. Caplan A.I. Mesenchymal stem cells. J. Orthop. Res. 1991, 9:641-650.
4. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science (New York, NY) 1999, 284:143-147.
5. Le Blanc K., Pittenger M. Mesenchymal stem cells: progress toward promise. Cytotherapy 2005, 7:36-45.
6. Fiorina P., Jurewicz M., Augello A., Vergani A., Dada S., La Rosa S., Selig M., Godwin J., Law K., Placidi C., Smith R.N., Capella C., Rodig S., Adra C.N., Atkinson M., Sayegh M.H., Abdi R. Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J. Immunol. 2009, 183:993-1004.
7. Nauta A.J., Fibbe W.E. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007, 110:3499-3506.
8. Loebinger M.R., Janes S.M. Stem cells as vectors for antitumour therapy. Thorax 2010, 65:362-369.
9. Vaananen H.K. Mesenchymal stem cells. Ann. Med. 2005, 37:469-479.
10. Ohyabu Y., Kaul Z., Yoshioka T., Inoue K., Sakai S., Mishima H., Uemura T., Kaul S.C., Wadhwa R. Stable and nondisruptive in vitro/in vivo labeling of mesenchymal stem cells by internalizing quantum dots. Hum. Gene Ther. 2009, 20:217-224.
11. Anjos-Afonso F., Siapati E.K., Bonnet D. In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J. Cell Sci. 2004, 117:5655-5664.
12. da Silva Meirelles L., Chagastelles P.C., Nardi N.B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 2006, 119:2204-2213.
13. Crisan M., Casteilla L., Lehr L., Carmona M., Paoloni-Giacobino A., Yap S., Sun B., Leger B., Logar A., Penicaud L., Schrauwen P., Cameron-Smith D., Russell A.P., Peault B., Giacobino J.P. A reservoir of brown adipocyte progenitors in human skeletal muscle. Stem Cells 2008, 26:2425-2433.
14. Short B., Brouard N., Occhiodoro-Scott T., Ramakrishnan A., Simmons P.J. Mesenchymal stem cells. Arch. Med. Res. 2003, 34:565-571.
15. Caplan A.I. Why are MSCs therapeutic? New data: new insight. J. Pathol. 2009, 217:318-324.
16. Sakaguchi Y., Sekiya I., Yagishita K., Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum. 2005, 52:2521-2529.
17. Stewart K., Monk P., Walsh S., Jefferiss C.M., Letchford J., Beresford J.N. STRO-1, HOP-26 (CD63), CD49a and SB-10 (CD166) as markers of primitive human marrow stromal cells and their more differentiated progeny: a comparative investigation in vitro. Cell Tissue Res. 2003, 313:281-290.
18. Pittenger M.F., Martin B.J. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ. Res. 2004, 95:9-20.
19. Delorme B., Ringe J., Gallay N., Le Vern Y., Kerboeuf D., Jorgensen C., Rosset P., Sensebe L., Layrolle P., Haupl T., Charbord P. Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood 2008, 111:2631-2635.
20. Uccelli A., Moretta L., Pistoia V. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 2008.
21. Giordano A., Galderisi U., Marino I.R. From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. J. Cell. Physiol. 2007, 211:27-35.
22. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
23. Owen M.E., Cave J., Joyner C.J. Clonal analysis in vitro of osteogenic differentiation of marrow CFU-F. J. Cell Sci. 1987, 87(Pt. 5):731-738.
24. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
25. Majumdar M.K., Keane-Moore M., Buyaner D., Hardy W.B., Moorman M.A., McIntosh K.R., Mosca J.D. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J. Biomed. Sci. 2003, 10:228-241.
26. Chen S.L., Fang W.W., Ye F., Liu Y.H., Qian J., Shan S.J., Zhang J.J., Chunhua R.Z., Liao L.M., Lin S., Sun J.P. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol. 2004, 94:92-95.
27. Choi Y.H., Kurtz A., Stamm C. Mesenchymal stem cells for cardiac cell therapy. Hum. Gene Ther. 2011, 22:3-17.
28. Qu C., Mahmood A., Lu D., Goussev A., Xiong Y., Chopp M. Treatment of traumatic brain injury in mice with marrow stromal cells. Brain Res. 2008, 1208:234-239.
29. Chopp M., Li Y. Treatment of neural injury with marrow stromal cells. Lancet Neurol. 2002, 1:92-100.
30. Zhang Z.X., Guan L.X., Zhang K., Zhang Q., Dai L.J. A combined procedure to deliver autologous mesenchymal stromal cells to patients with traumatic brain injury. Cytotherapy 2008, 10:134-139.
31. Dezawa M., Hoshino M., Ide C. Treatment of neurodegenerative diseases using adult bone marrow stromal cell-derived neurons. Expert Opin. Biol. Ther. 2005, 5:427-435.
32. Li D.S., Warnock G.L., Tu H.J., Ao Z., He Z., Lu H., Dai L.J. Do immunotherapy and beta cell replacement play a synergistic role in the treatment of type 1 diabetes?. Life Sci. 2009, 85:549-556.
33. Dai L.J., Li H.Y., Guan L.X., Ritchie G., Zhou J.X. The therapeutic potential of bone marrow-derived mesenchymal stem cells on hepatic cirrhosis. Stem Cell Res. 2009, 2:16-25.
34. Jemal A., Siegel R., Xu J., Ward E. Cancer statistics. CA Cancer J. Clin. 2010.
35. Albini A., Sporn M.B. The tumour microenvironment as a target for chemoprevention. Nat. Rev. 2007, 7:139-147.
36. Zischek C., Niess H., Ischenko I., Conrad C., Huss R., Jauch K.W., Nelson P.J., Bruns C. Targeting tumor stroma using engineered mesenchymal stem cells reduces the growth of pancreatic carcinoma. Ann. Surg. 2009, 250:747-753.
37. Dvorak H.F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. New Engl. J. Med. 1986, 315:1650-1659.
38. Loebinger M.R., Kyrtatos P.G., Turmaine M., Price A.N., Pankhurst Q., Lythgoe M.F., Janes S.M. Magnetic resonance imaging of mesenchymal stem cells homing to pulmonary metastases using biocompatible magnetic nanoparticles. Cancer Res. 2009, 69:8862-8867.
39. Sasportas L.S., Kasmieh R., Wakimoto H., Hingtgen S., van de Water J.A., Mohapatra G., Figueiredo J.L., Martuza R.L., Weissleder R., Shah K. Assessment of therapeutic efficacy and fate of engineered human mesenchymal stem cells for cancer therapy. Proc. Natl. Acad. Sci. USA 2009, 106:4822-4827.
40. Sonabend A.M., Ulasov I.V., Tyler M.A., Rivera A.A., Mathis J.M., Lesniak M.S. Mesenchymal stem cells effectively deliver an oncolytic adenovirus to intracranial glioma. Stem Cells (Dayton, Ohio) 2008, 26:831-841.
41. Yang B., Wu X., Mao Y., Bao W., Gao L., Zhou P., Xie R., Zhou L., Zhu J. Dual-targeted antitumor effects against brainstem glioma by intravenous delivery of tumor necrosis factor-related, apoptosis-inducing, ligand-engineered human mesenchymal stem cells. Neurosurgery 2009, 65:610-624. (Discussion 624).
42. Khakoo A.Y., Pati S., Anderson S.A., Reid W., Elshal M.F., Rovira, Nguyen A.T., Malide D., Combs C.A., Hall G., Zhang J., Raffeld M., Rogers T.B., Stetler-Stevenson W., Frank J.A., Reitz M., Finkel T. Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J. Exp. Med. 2006, 203:1235-1247.
43. Patel S.A., Meyer J.R., Greco S.J., Corcoran K.E., Bryan M., Rameshwar P. Mesenchymal stem cells protect breast cancer cells through regulatory T cells: role of mesenchymal stem cell-derived TGF-beta. J. Immunol. 2010, 184:5885-5894.
44. Kidd S., Spaeth E., Dembinski J.L., Dietrich M., Watson K., Klopp A., Battula V.L., Weil M., Andreeff M., Marini F.C. Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells (Dayton, Ohio) 2009, 27:2614-2623.
45. Menon L.G., Picinich S., Koneru R., Gao H., Lin S.Y., Koneru M., Mayer-Kuckuk P., Glod J., Banerjee D. Differential gene expression associated with migration of mesenchymal stem cells to conditioned medium from tumor cells or bone marrow cells. Stem Cells (Dayton, Ohio) 2007, 25:520-528.
46. S. Kidd, L. Caldwell, M. Dietrich, I. Samudio, E.L. Spaeth, K. Watson, Y. Shi, J. Abbruzzese, M. Konopleva, M. Andreeff, F.C. Marini, Mesenchymal stromal cells alone or expressing interferon-beta suppress pancreatic tumors in vivo, an effect countered by anti-inflammatory treatment. Cytotherapy 12 (2010) 615-625.
47. Studeny M., Marini F.C., Champlin R.E., Zompetta C., Fidler I.J., Andreeff M. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res. 2002, 62:3603-3608.
48. Dwyer R.M., Potter-Beirne S.M., Harrington K.A., Lowery A.J., Hennessy E., Murphy J.M., Barry F.P., O'Brien T., Kerin M.J. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin. Cancer Res. 2007, 13:5020-5027.
49. Son B.R., Marquez-Curtis L.A., Kucia M., Wysoczynski M., Turner A.R., Ratajczak J., Ratajczak M.Z., Janowska-Wieczorek A. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells (Dayton, Ohio) 2006, 24:1254-1264.
50. Imitola J., Raddassi K., Park K.I., Mueller F.J., Nieto M., Teng Y.D., Frenkel D., Li J., Sidman R.L., Walsh C.A., Snyder E.Y., Khoury S.J. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc. Natl. Acad. Sci. USA 2004, 101:18117-18122.
51. Schmidt N.O., Przylecki W., Yang W., Ziu M., Teng Y., Kim S.U., Black P.M., Aboody K.S., Carroll R.S. Brain tumor tropism of transplanted human neural stem cells is induced by vascular endothelial growth factor. Neoplasia (New York, NY) 2005, 7:623-629.
52. Nakamizo A., Marini F., Amano T., Khan A., Studeny M., Gumin J., Chen J., Hentschel S., Vecil G., Dembinski J., Andreeff M., Lang F.F. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res. 2005, 65:3307-3318.
53. H. Motaln, C. Schichor, T.T. Lah, Human mesenchymal stem cells and their use in cell-based therapies. Cancer 116 (2010) 2519-2530.
54. Von Luttichau I., Notohamiprodjo M., Wechselberger A., Peters C., Henger A., Seliger C., Djafarzadeh R., Huss R., Nelson P.J. Human adult CD34-progenitor cells functionally express the chemokine receptors CCR1, CCR4, CCR7, CXCR5, and CCR10 but not CXCR4. Stem Cells Dev. 2005, 14:329-336.
55. Klopp A.H., Spaeth E.L., Dembinski J.L., Woodward W.A., Munshi A., Meyn R.E., Cox J.D., Andreeff M., Marini F.C. Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res. 2007, 67:11687-11695.
56. H.K. Salem, C. Thiemermann, Mesenchymal stromal cells: current understanding and clinical status. Stem Cells (Dayton, Ohio) 28 (2010) 585-596.
57. Kemp K.C., Hows J., Donaldson C. Bone marrow-derived mesenchymal stem cells. Leuk. Lymphoma 2005, 46:1531-1544.
58. Honczarenko M., Le Y., Swierkowski M., Ghiran I., Glodek A.M., Silberstein L.E. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells 2006, 24:1030-1041.
59. De Becker A., Van Hummelen P., Bakkus M., Vande Broek I., De Wever J., De Waele M., Van Riet I. Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3. Haematologica 2007, 92:440-449.
60. Luetzkendorf J., Mueller L.P., Mueller T., Caysa H., Nerger K., Schmoll H.J. Growth inhibition of colorectal carcinoma by lentiviral TRAIL-transgenic human mesenchymal stem cells requires their substantial intratumoral presence. J. Cell. Mol. Med. 2010, 14:2292-2304.
61. Li H., Fan X., Houghton J. Tumor microenvironment: the role of the tumor stroma in cancer. J. Cell. Biochem. 2007, 101:805-815.
62. Zhu W., Xu W., Jiang R., Qian H., Chen M., Hu J., Cao W., Han C., Chen Y. Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp. Mol. Pathol. 2006, 80:267-274.
63. Karnoub A.E., Dash A.B., Vo A.P., Sullivan A., Brooks M.W., Bell G.W., Richardson A.L., Polyak K., Tubo R., Weinberg R.A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007, 449:557-563.
64. Lis R., Touboul C., Mirshahi P., Ali F., Mathew S., Nolan D.J., Maleki T.M., Abdalla S.A., Raynaud C.M., Querleu D., Al-Azwani E., Malek J., Mirshahi M., Rafii A. Tumor associated mesenchymal stem cells protects ovarian cancer cells from hyperthermia through CXCL12. Int. J. Cancer 2010.
65. Okumura T., Wang S.S., Takaishi S., Tu S.P., Ng V., Ericksen R.E., Rustgi A.K., Wang T.C. Identification of a bone marrow-derived mesenchymal progenitor cell subset that can contribute to the gastric epithelium. Lab. Invest. 2009, 89:1410-1422.
66. Djouad F., Plence P., Bony C., Tropel P., Apparailly F., Sany J., Noel D., Jorgensen C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003, 102:3837-3844.
67. Ghannam S., Bouffi C., Djouad F., Jorgensen C., Noel D. Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Stem Cell Res. Ther. 2010, 1:2.
68. Shi Y., Hu G., Su J., Li W., Chen Q., Shou P., Xu C., Chen X., Huang Y., Zhu Z., Huang X., Han X., Xie N., Ren G. Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Res. 2010, 20:510-518.
69. Ren G., Zhang L., Zhao X., Xu G., Zhang Y., Roberts A.I., Zhao R.C., Shi Y. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008, 2:141-150.
70. Polchert D., Sobinsky J., Douglas G., Kidd M., Moadsiri A., Reina E., Genrich K., Mehrotra S., Setty S., Smith B., Bartholomew A. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur. J. Immunol. 2008, 38:1745-1755.
71. Noel D., Djouad F., Bouffi C., Mrugala D., Jorgensen C. Multipotent mesenchymal stromal cells and immune tolerance. Leuk. Lymphoma 2007, 48:1283-1289.
72. Glennie S., Soeiro I., Dyson P.J., Lam E.W., Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005, 105:2821-2827.
73. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., Grisanti S., Gianni A.M. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002, 99:3838-3843.
74. 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-dioxygenase-mediated tryptophan degradation. Blood 2004, 103:4619-4621.
75. Aggarwal S., Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005, 105:1815-1822.
76. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., Risso M., Gualandi F., Mancardi G.L., Pistoia V., Uccelli A. Human mesenchymal stem cells modulate B-cell functions. Blood 2006, 107:367-372.
77. Reichert T.E., Strauss L., Wagner E.M., Gooding W., Whiteside T.L. Signaling abnormalities, apoptosis, and reduced proliferation of circulating and tumor-infiltrating lymphocytes in patients with oral carcinoma. Clin. Cancer Res. 2002, 8:3137-3145.
78. Whiteside T.L. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008, 27:5904-5912.
79. + T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica 2005, 90:516-525.
80. Patel S.A., Meyer J.R., Greco S.J., Corcoran K.E., Bryan M., Rameshwar P. Mesenchymal stem cells protect breast cancer cells through regulatory T cells: role of mesenchymal stem cell-derived TGF-beta. J. Immunol. 2010, 184:5885-5894.
81. + regulatory T cells upon mesenchymal stem cell-lymphocyte interaction. Haematologica 2007, 92:881-888.
82. Bergmann C., Strauss L., Zeidler R., Lang S., Whiteside T.L. Expansion of human T regulatory type 1 cells in the microenvironment of cyclooxygenase 2 overexpressing head and neck squamous cell carcinoma. Cancer Res. 2007, 67:8865-8873.
83. +CD25highFoxp3+ T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin. Cancer Res. 2007, 13:4345-4354.
84. Woo E.Y., Chu C.S., Goletz T.J., Schlienger K., Yeh H., Coukos G., Rubin S.C., Kaiser L.R., June C.H. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 2001, 61:4766-4772.
85. Banerjee D.K., Dhodapkar M.V., Matayeva E., Steinman R.M., Dhodapkar K.M. Expansion of FOXP3high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood 2006, 108:2655-2661.
86. Zhou G., Drake C.G., Levitsky H.I. Amplification of tumor-specific regulatory T cells following therapeutic cancer vaccines. Blood 2006, 107:628-636.
87. Kinnaird T., Stabile E., Burnett M.S., Lee C.W., Barr S., Fuchs S., Epstein S.E. 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, 94:678-685.
88. Al-Khaldi A., Eliopoulos N., Martineau D., Lejeune L., Lachapelle K., Galipeau J. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther. 2003, 10:621-629.
89. Sun B., Zhang S., Ni C., Zhang D., Liu Y., Zhang W., Zhao X., Zhao C., Shi M. Correlation between melanoma angiogenesis and the mesenchymal stem cells and endothelial progenitor cells derived from bone marrow. Stem Cells Dev. 2005, 14:292-298.
90. Valdes F., Alvarez A.M., Locascio A., Vega S., Herrera B., Fernandez M., Benito M., Nieto M.A., Fabregat I. The epithelial mesenchymal transition confers resistance to the apoptotic effects of transforming growth factor Beta in fetal rat hepatocytes. Mol Cancer Res. 2002, 1:68-78.
91. Klymkowsky M.W., Savagner P. Epithelial-mesenchymal transition: a cancer researcher's conceptual friend and foe. Am. J. Pathol. 2009, 174:1588-1593.
92. Iwatsuki M., Mimori K., Yokobori T., Ishi H., Beppu T., Nakamori S., Baba H., Mori M. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci. 2010, 101:293-299.
93. Martin F.T., Dwyer R.M., Kelly J., Khan S., Murphy J.M., Curran C., Miller N., Hennessy E., Dockery P., Barry F.P., O'Brien T., Kerin M.J. Potential role of mesenchymal stem cells (MSCs) in the breast tumour microenvironment: stimulation of epithelial to mesenchymal transition (EMT). Breast Cancer Res. Treat. 2010.
94. Turley E.A., Veiseh M., Radisky D.C., Bissell M.J. Mechanisms of disease: epithelial-mesenchymal transition - does cellular plasticity fuel neoplastic progression?. Nat. Clin. Pract. Oncol. 2008, 5:280-290.
95. Lepperdinger G., Brunauer R., Jamnig A., Laschober G., Kassem M. Controversial issue: is it safe to employ mesenchymal stem cells in cell-based therapies?. Exp. Gerontol. 2008, 43:1018-1023.
96. Bernardo M.E., Zaffaroni N., Novara F., Cometa A.M., Avanzini M.A., Moretta A., Montagna D., Maccario R., Villa R., Daidone M.G., Zuffardi O., Locatelli F. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res. 2007, 67:9142-9149.
97. Wang Y., Huso D.L., Harrington J., Kellner J., Jeong D.K., Turney J., McNiece I.K. Outgrowth of a transformed cell population derived from normal human BM mesenchymal stem cell culture. Cytotherapy 2005, 7:509-519.
98. Rubio D., Garcia S., Paz M.F., De la Cueva T., Lopez-Fernandez L.A., Lloyd A.C., Garcia-Castro J., Bernad A. Molecular characterization of spontaneous mesenchymal stem cell transformation. PLoS One 2008, 3:e1398.
99. Houghton J., Stoicov C., Nomura S., Rogers A.B., Carlson J., Li H., Cai X., Fox J.G., Goldenring J.R., Wang T.C. Gastric cancer originating from bone marrow-derived cells. Science 2004, 306:1568-1571.
100. Centeno C.J., Schultz J.R., Cheever M., Robinson B., Freeman M., Marasco W. Safety and complications reporting on the re-implantation of culture-expanded mesenchymal stem cells using autologous platelet lysate technique. Curr. Stem Cell Res. Ther. 2010, 5:81-93.
101. Maestroni G.J., 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, 55:663-667.
102. Ohlsson L.B., Varas L., Kjellman C., Edvardsen K., Lindvall M. Mesenchymal progenitor cell-mediated inhibition of tumor growth in vivo and in vitro in gelatin matrix. Exp. Mol. Pathol. 2003, 75:248-255.
103. Kidd S., Caldwell L., Dietrich M., Samudio I., Spaeth E.L., Watson K., Shi Y., Abbruzzese J., Konopleva M., Andreeff M., Marini F.C. Mesenchymal stromal cells alone or expressing interferon-beta suppress pancreatic tumors in vivo, an effect countered by anti-inflammatory treatment. Cytotherapy 2010.
104. Qiao L., Xu Z., Zhao T., Zhao Z., Shi M., Zhao R.C., Ye L., Zhang X. Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res. 2008, 18:500-507.
105. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
106. Reya T., Clevers H. Wnt signalling in stem cells and cancer. Nature 2005, 434:843-850.
107. Duncan A.W., Rattis F.M., DiMascio L.N., Congdon K.L., Pazianos G., Zhao C., Yoon K., Cook J.M., Willert K., Gaiano N., Reya T. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 2005, 6:314-322.
108. Androutsellis-Theotokis A., Leker R.R., Soldner F., Hoeppner D.J., Ravin R., Poser S.W., Rueger M.A., Bae S.K., Kittappa R., McKay R.D. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006, 442:823-826.
109. Chen G., Shukeir N., Potti A., Sircar K., Aprikian A., Goltzman D., Rabbani S.A. Up-regulation of Wnt-1 and beta-catenin production in patients with advanced metastatic prostate carcinoma: potential pathogenetic and prognostic implications. Cancer 2004, 101:1345-1356.
110. Moon R.T., Kohn A.D., De Ferrari G.V., Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 2004, 5:691-701.
111. Li Z., Tan F., Liewehr D.J., Steinberg S.M., Thiele C.J. In vitro and in vivo inhibition of neuroblastoma tumor cell growth by AKT inhibitor perifosine. J. Natl. Cancer Inst. 2010, 102:758-770.
112. Lu Y.R., Yuan Y., Wang X.J., Wei L.L., Chen Y.N., Cong C., Li S.F., Long D., Tan W.D., Mao Y.Q., Zhang J., Li Y.P., Cheng J.Q. The growth inhibitory effect of mesenchymal stem cells on tumor cells in vitro and in vivo. Cancer Biol. Ther. 2008, 7:245-251.
113. Sun B., Roh K.H., Park J.R., Lee S.R., Park S.B., Jung J.W., Kang S.K., Lee Y.S., Kang K.S. Therapeutic potential of mesenchymal stromal cells in a mouse breast cancer metastasis model. Cytotherapy 2009, 11:289-298. 281 p (following 298).
114. Ren C., Kumar S., Chanda D., Chen J., Mountz J.D., Ponnazhagan S. Therapeutic potential of mesenchymal stem cells producing interferon-alpha in a mouse melanoma lung metastasis model. Stem Cells 2008, 26:2332-2338.
115. Li X., Lu Y., Huang W., Xu H., Chen X., Geng Q., Fan H., Tan Y., Xue G., Jiang X. In vitro effect of adenovirus-mediated human Gamma Interferon gene transfer into human mesenchymal stem cells for chronic myelogenous leukemia. Hematol. Oncol. 2006, 24:151-158.
116. Nakamura K., Ito Y., Kawano Y., Kurozumi K., Kobune M., Tsuda H., Bizen A., Honmou O., Niitsu Y., Hamada H. Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther. 2004, 11:1155-1164.
117. Chen X., Lin X., Zhao J., Shi W., Zhang H., Wang Y., Kan B., Du L., Wang B., Wei Y., Liu Y., Zhao X. A tumor-selective biotherapy with prolonged impact on established metastases based on cytokine gene-engineered MSCs. Mol. Ther. 2008, 16:749-756.
118. Kanehira M., Xin H., Hoshino K., Maemondo M., Mizuguchi H., Hayakawa T., Matsumoto K., Nakamura T., Nukiwa T., Saijo Y. Targeted delivery of NK4 to multiple lung tumors by bone marrow-derived mesenchymal stem cells. Cancer Gene Ther. 2007, 14:894-903.
119. Loebinger M.R., Eddaoudi A., Davies D., Janes S.M. Mesenchymal stem cell delivery of TRAIL can eliminate metastatic cancer. Cancer Res. 2009, 69:4134-4142.
120. Kim S.M., Lim J.Y., Park S.I., Jeong C.H., Oh J.H., Jeong M., Oh W., Park S.H., Sung Y.C., Jeun S.S. Gene therapy using TRAIL-secreting human umbilical cord blood-derived mesenchymal stem cells against intracranial glioma. Cancer Res. 2008, 68:9614-9623.
121. Grisendi G., Bussolari R., Cafarelli L., Petak I., Rasini V., Veronesi E., De Santis G., Spano C., Tagliazzucchi M., Barti-Juhasz H., Scarabelli L., Bambi F., Frassoldati A., Rossi G., Casali C., Morandi U., Horwitz E.M., Paolucci P., Conte P., Dominici M. Adipose-derived mesenchymal stem cells as stable source of tumor necrosis factor-related apoptosis-inducing ligand delivery for cancer therapy. Cancer Res. 2010, 70:3718-3729.
122. Johnstone R.W., Frew A.J., Smyth M.J. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat. Rev. Cancer 2008, 8:782-798.
123. Jeong M., Kwon Y.S., Park S.H., Kim C.Y., Jeun S.S., Song K.W., Ko Y., Robbins P.D., Billiar T.R., Kim B.M., Seol D.W. Possible novel therapy for malignant gliomas with secretable trimeric TRAIL. PLoS One 2009, 4:e4545.
124. Krampera M., Cosmi L., Angeli R., Pasini A., Liotta F., Andreini A., Santarlasci V., Mazzinghi B., Pizzolo G., Vinante F., Romagnani P., Maggi E., Romagnani S., Annunziato F. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006, 24:386-398.
125. Spaggiari G.M., Capobianco A., Abdelrazik H., Becchetti F., Mingari M.C., Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 2008, 111:1327-1333.
126. +CD25highFOXP3+ regulatory T cells. Stem Cells 2008, 26:212-222.
127. Morandi F., Raffaghello L., Bianchi G., Meloni F., Salis A., Millo E., Ferrone S., Barnaba V., Pistoia V. Immunogenicity of human mesenchymal stem cells in HLA-class I-restricted T-cell responses against viral or tumor-associated antigens. Stem Cells 2008, 26:1275-1287.
128. Bian L., Guo Z.K., Wang H.X., Wang J.S., Wang H., Li Q.F., Yang Y.F., Xiao F.J., Wu C.T., Wang L.S. In vitro and in vivo immunosuppressive characteristics of hepatocyte growth factor-modified murine mesenchymal stem cells. In Vivo 2009, 23:21-27.
129. Ding Y., Xu D., Feng G., Bushell A., Muschel R.J., Wood K.J. Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and -9. Diabetes 2009, 58:1797-1806.