Human mesenchymal stem cells creating an immunosuppressive environment and promote breast cancer in mice

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Ljujic, Biljana ^a   Milovanovic, Marija ^a   Volarevic, Vladislav ^a   Murray, Bridgid ^b   Bugarski, Diana ^c   Przyborski, Stefan ^b   Arsenijevic, Nebojsa ^a   Lukic, Miodrag L ^a   Stojkovic, Miodrag ^a  

^a University of Kragujevac Medical Faculty   (Serbia)

^b DURHAM UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ANIMAL; ARTICLE; BREAST TUMOR; CELL MOTION; CELL TRANSFORMATION; CYTOTOXICITY; FEMALE; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; METASTASIS; MOUSE; NATURAL KILLER CELL; NATURAL KILLER T CELL; PATHOLOGY; SPLEEN; T LYMPHOCYTE SUBPOPULATION; TUMOR MICROENVIRONMENT; TUMOR VOLUME;

ANIMALS; BREAST NEOPLASMS; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; NATURAL KILLER T-CELLS; NEOPLASM METASTASIS; SPLEEN; T-LYMPHOCYTE SUBSETS; TUMOR BURDEN; TUMOR MICROENVIRONMENT;

EID: 84881188594     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep02298     Document Type: Article

References (59)

1. Meirelles, D. L., Chagastelles, P. C. & Nardi, N. B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci. 119, 2204-2213 (2006). (Pubitemid 43960310)
2. Pittenger, M. F. et al. Multilineage potential ofadult human mesenchymal stem cells. Science. 284, 143-147 (1999). (Pubitemid 29282067)
3. Stagg, J. Mesenchymal stem cells in cancer. Stem Cell Rev. 4, 119-124 (2008).
4. Roorda, B. D., Ter Elst, A., Kamps, W. A. & de Bont, E. S. 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. 69, 187-198 (2009).
5. Li,n S. Y. et al. The isolation of novel mesenchymal stromal cell chemotactic factors from the conditioned medium of tumor cells. Exp Cell Res. 314, 3107-3117 (2008).
6. Uccelli, A.,Moretta, L.&Pistoia, V. Mesenchymal stem cells in health and disease. Nat Rev. 8, 726-736 (2008).
7. Ramasamy, R., Lam, E. W., Soeiro, I., Tisato, V., Bonnet, D. & Dazzi, F. Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth. Leukemia. 21, 304-310 (2007). (Pubitemid 46158124)
8. Yu, J. M., Jun, E. S. & Bae, Y. C. Mesenchymal stem cells derived from human adipose tissues favour tumor cell growth in vivo. Stem Cells Dev. 17, 463-473 (2008). (Pubitemid 351948199)
9. Kucerova, L.,Matuskova, M., Hlubinova, K., Altanerova, V. & Altaner, C. Tumor cell behaviour modulation by mesenchymal stromal cells. Mol Cancer. 9, 1-15 (2010).
10. Secchiero, P. et al. Human bone marrow mesenchymal stem cells display anticancer activity in SCID mice bearing disseminated non-Hodgkin's lymphoma xenografts. Plos One. 16, 5-6 (2010).
11. Ling, X. et al. Mesenchymal Stem Cells Overexpressing IFN-b Inhibit Breast Cancer Growth and Metastases through Stat3 Signaling in a Syngeneic Tumor Model. Cancer Microenviron. 3, 83-95 (2010).
12. Rasmusson, I., Ringden, O., Sundberg, B. & Le Blanc, K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation. 76, 1208-1213 (2003). (Pubitemid 37339646)
13. Raffaghello, L. et al. Human mesenchymal stem cells inhibit neutrophil apoptosis: a model for neutrophil preservation in the bone marrow niche. Stem Cells. 26, 151-162 (2008).
14. Djouad, F. et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 102, 3837-3844 (2003). (Pubitemid 37409409)
15. Ning, H. et al. The correlation between cotransplantation of mesenchymal stem cells and higher recurrence rate in hematologic malignancy patients: outcome of a pilot clinical study. Leukemia. 22, 593-599 (2008). (Pubitemid 351386730)
16. Aggarwal, S. & Pittenger, M. F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 105, 1815-1822 (2005). (Pubitemid 40223708)
17. Selmani, Z. et al. Human leukocyte antigen-G5 secretion by humanmesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4 1 CD25 high FOXP31 regulatory T cells. Stem Cells. 26, 212-222 (2008).
18. Fernandez, M. A. et al. T regulatory cells contribute to the attenuated primary CD81 and CD41 T cell responses to herpes simplex virus type 2 in neonatal mice. J Immunol. 180, 1556-1564 (2008).
19. Vasir, B. et al. Fusions of dendritic cells with breast carcinoma stimulate the expansion of regulatory T cells while concomitant exposure to IL-12, CpG oligodeoxynucleotides, and anti-CD3/CD28 promotes the expansion of activated tumor reactive cells. J Immunol. 181, 808-821 (2008).
20. Studeny, M. et al. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst. 96, 1593-1603 (2004). (Pubitemid 39534883)
21. Annacker, O. et al. A CD25 1CD41 T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J Immunol. 166, 3008-3018 (2001). (Pubitemid 33117296)
22. Awasthi, A. et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol. l8, 1380-1389 (2007). (Pubitemid 350131175)
23. Ammirante, M., Luo, J. L., Grivennikov, S., Nedospasov, S. & Karin, M. B-cell derived lymphotoxin promotes castration-resistant prostate cancer. Nature. 464, 302-305 (2010).
24. Rafei, M. et al. A granulocyte-macrophage colony-stimulating factor and interleukin-15 fusokine induces a regulatory B cell population with immune suppressive properties. Nat Med. 15, 1038-1045 (2009).
25. Carpentier, A. F. & Meng, Y. Recent advances in immunotherapy for human glioma. Curr Opin Oncol. 18, 631-636 (2006). (Pubitemid 44427639)
26. Lizee, G., Radvanyi, L. G., Overwijk, W. W. & Hwu, P. Improving antitumor immune responses by circumventing immunoregulatory cells and mechanisms. Clin Cancer Res. 12, 4794-4803 (2006). (Pubitemid 44338563)
27. Olkhanud, P. B. et al. Tumor-Evoked Regulatory B Cells Promote Breast Cancer Metastasis by Converting Resting CD41 T Cells to T-Regulatory Cells. Cancer Res. 71, 3505-3515 (2011).
28. Patel, S. A. et al. Mesenchymal stem cells protect breast cancer cells through regulatory T cells: role of mesenchymal stem cell-derived TGF-beta. J Immunol. 184, 5885-5894 (2010).
29. Oreffo, R. O., Cooper, C., Mason, C. & Clements, M. Mesenchymal stem cells: lineage, plasticity, and skeletal therapeutic potential. Stem Cell Rev. 1, 169-178 (2005). (Pubitemid 43074202)
30. Parekkadan, B. et al. Immunomodulation of activated hepatic stellate cells by mesenchymal stem cells. Biochem Biophys Res Commun. 363, 247-252 (2007). (Pubitemid 47484321)
31. Dvorak, H. F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and woundhealing. N Engl J Med. 315, 1650-1659 (1986). (Pubitemid 17052899)
32. Karnoub, A. E. et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 449, 557-563 (2007). (Pubitemid 47525152)
33. Studeny, M. et al. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res. 62, 3603-3608 (2002). (Pubitemid 34728832)
34. Kidd, S. et al. Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells. 27, 2614-2623 (2009).
35. Lin, Y. T. et al. Human mesenchymal stem cells prolong survival and ameliorate motor deficit through trophic support in Huntington's disease mouse models. Plos One. 6, 8-e22924 (2011).
36. Eggenhofer, E. et al. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front Immunol. 3, 297 (2012).
37. Khakoo, A. Y. et al. Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med. 203, 1235-1247 (2006). (Pubitemid 43736593)
38. Li, G. C. et al. Human mesenchymal stem cells inhibit metastasis of a hepatocellular carcinoma model using the MHCC97-H cell line. Cancer Sci. 101, 2546-2553 (2010).
39. 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. 75, 248-255 (2003). (Pubitemid 37373711)
40. Wang, H. et al. Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells. 27, 1548-1558 (2009).
41. Djouad, F. et al. Earlier onset of syngeneic tumors in the presence of mesenchymal stem cells. Transplantation. 82, 1060-1066 (2006). (Pubitemid 44632122)
42. Muehlberg, F. L. et al. Tissue resident stem cells promote breast cancer growth and metastasis. Carcinogenesis. 30, 589-597 (2009).
43. Krampera,M. et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood. 101, 3722-3729 (2003).
44. Rutella, S., Danese, S. & Leone, G. Tolerogenic dendritic cells: Cytokine modulation comes of age. Blood. 108, 1435-1440 (2006). (Pubitemid 44316106)
45. Corcione, A. et al. Human mesenchymal stem cells modulate B-cell functions. Blood. 107, 367-372 (2006). (Pubitemid 43053565)
46. Sotiropoulou, P. A., Perez, S. A., Gritzapis, A. D., Baxevanis, C. N. & Papamichail, M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells. 24, 74-85 (2006).
47. Spaggiari, G. M. et al. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3- dioxygenase and prostaglandin E2. Blood. 111, 1327-1333 (2008). (Pubitemid 351213419)
48. Minguell, J. J., Erices, A. & Conget, P. Mesenchymal stem cells. Exp Biol Med. 226, 507-520 (2001). (Pubitemid 32524497)
49. Joshi, P. C., Zhou, X., Cuchens, M.&Jones, Q. Prostaglandin E2 suppressed IL-15- mediated human NK cell function through down-regulation of common c-chain. J Immunol. 166, 885-891 (2001). (Pubitemid 32060242)
50. Swann, J., Crowe, N. Y., Hayakawa, Y., Godfrey, D. I. & Smyth, M. J. Regulation of antitumour immunity by CD1d-restricted NKT cells. Immunol Cell Biol. 82, 323-331 (2004). (Pubitemid 38870027)
51. Yanagisawa, K. et al. Impaired proliferative response ofValpha 24 NKT cells from cancer patients against alpha-galactosylceramide. J Immunol. 168, 6494-6499 (2002). (Pubitemid 34620075)
52. Dhodapkar, M. V. et al. A reversible defect in natural killer T cell function characterizes the progression of premalignant to malignant multiple myeloma. J Exp Med. 197, 1667-1676 (2003). (Pubitemid 36745342)
53. Molling, J. W. et al. Low levels of circulating invariant natural killer T cells predict poor clinical outcome in patients with head and neck squamous cell carcinoma. J Clin Oncol. 25, 862-868 (2007). (Pubitemid 350002887)
54. Ghiringhelli, F., Ménard, C.,Martin, F. & Zitvogel, L. The role of regulatory T cells in the control of natural killer cells: relevance during tumor progression. Immunol Rev. 214, 229-238 (2006). (Pubitemid 44707914)
55. Casiraghi, F. et al. Pretransplant infusion of mesenchymal stem cells prolongs the survival of a semiallogeneic heart transplant through the generation of regulatory T cells. J Immunol. 181, 3933-3946 (2008).
56. Batten, P. et al. Human mesenchymal stem cells induce T cell anergy and downregulate T cell alloresponses via the TH2 pathway: relevance to tissue engineering human heart valves. Tissue Eng. 12, 2263-2273 (2006). (Pubitemid 44734984)
57. Trivanovic, D. et al. Mesenchymal stem cells isolated from peripheral blood and umbilical cord Wharton's jelly. Srp Arh Celok Lek. 141, 178-186 (2013).
58. Carlsson, G., Ekelund, E., Stigsson, L. & Hafstrom, L. Vascularization and tumour volume estimations of solitary liver tumours in rats. Ann Chir Gynaecol. 72, 187-191 (1983).
59. Jonjic, B. M. et al. Innate direct anticancer effector function of human immature dendritic cells. I. Involvement of an apoptosis-inducing pathway. J Immunol. 168, 1823-1830 (2002).