Multipotent human mesenchymal stromal cells mediate expansion of myeloid-derived suppressor cells via hepatocyte growth factor/c-Met and STAT3

Stem Cell Reports

Volumn 1, Issue 2, 2013, Pages 139-151

  Yen, B Linju ^a,b   Yen, Men Luh ^c   Hsu, Pei Ju ^a   Liu, Ko Jiunn ^a,d   Wang, Chia Jen ^f   Bai, Chyi Huey ^e   Sytwu, Huey Kang ^f  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b CATHAY GENERAL HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^f NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; SCATTER FACTOR; STAT3 PROTEIN; HGF PROTEIN, HUMAN; HGF PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; SCATTER FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL EXPANSION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; REGULATORY T LYMPHOCYTE; SECRETION (PROCESS); SUPPRESSOR CELL; WILD TYPE; ANIMAL; BONE MARROW CELL; CELL CULTURE; CYTOLOGY; FEMALE; GENETICS; IMMUNOLOGY; LIVER; METABOLISM; PLACENTA; PREGNANCY;

MUS;

ANIMALS; ANTIGENS, CD; BONE MARROW CELLS; CELLS, CULTURED; FEMALE; GENE KNOCKDOWN TECHNIQUES; HEPATOCYTE GROWTH FACTOR; HUMANS; LIVER; MESENCHYMAL STROMAL CELLS; MICE; MYELOID CELLS; PLACENTA; PREGNANCY; PROTO-ONCOGENE PROTEINS C-MET; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY;

EID: 84881337812     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2013.06.006     Document Type: Article

References (56)

1. R. Abdi, P. Fiorina, C.N. Adra, M. Atkinson, and M.H. Sayegh Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes Diabetes 57 2008 1759 1767
2. B. Almand, J.I. Clark, E. Nikitina, J. van Beynen, N.R. English, S.C. Knight, D.P. Carbone, and D.I. Gabrilovich Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer J. Immunol. 166 2001 678 689 (Pubitemid 32038493)
3. M. Benkhoucha, M.L. Santiago-Raber, G. Schneiter, M. Chofflon, H. Funakoshi, T. Nakamura, and P.H. Lalive Hepatocyte growth factor inhibits CNS autoimmunity by inducing tolerogenic dendritic cells and CD25+Foxp3+ regulatory T cells Proc. Natl. Acad. Sci. USA 107 2010 6424 6429
4. S.K. Bunt, L. Yang, P. Sinha, V.K. Clements, J. Leips, and S. Ostrand-Rosenberg Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression Cancer Res. 67 2007 10019 10026 (Pubitemid 47621253)
5. F. Cecchi, D.C. Rabe, and D.P. Bottaro Targeting the HGF/Met signalling pathway in cancer Eur. J. Cancer 46 2010 1260 1270
6. C.J. Chang, M.L. Yen, Y.C. Chen, C.C. Chien, H.I. Huang, C.H. Bai, and B.L. Yen Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma Stem Cells 24 2006 2466 2477 (Pubitemid 44674307)
7. J.G. Christensen, R. Schreck, J. Burrows, P. Kuruganti, E. Chan, P. Le, J. Chen, X. Wang, L. Ruslim, and R. Blake A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes in vitro and exhibits cytoreductive antitumor activity in vivo Cancer Res. 63 2003 7345 7355 (Pubitemid 37413476)
8. M. Di Nicola, C. Carlo-Stella, M. Magni, M. Milanesi, P.D. Longoni, P. Matteucci, S. Grisanti, and A.M. Gianni Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli Blood 99 2002 3838 3843 (Pubitemid 34534559)
9. F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, J. Sany, D. Noël, and C. Jorgensen Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals Blood 102 2003 3837 3844 (Pubitemid 37409409)
10. F. Djouad, C. Bouffi, S. Ghannam, D. Noël, and C. Jorgensen Mesenchymal stem cells: innovative therapeutic tools for rheumatic diseases Nat. Rev. Rheumatol. 5 2009 392 399
11. M. Dominici, K. Le Blanc, I. Mueller, I. Slaper-Cortenbach, F. Marini, D. Krause, R. Deans, A. Keating, Dj. Prockop, and E. Horwitz Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement Cytotherapy 8 2006 315 317 (Pubitemid 44269669)
12. A.S. Dugast, T. Haudebourg, F. Coulon, M. Heslan, F. Haspot, N. Poirier, R. Vuillefroy de Silly, C. Usal, H. Smit, and B. Martinet Myeloid-derived suppressor cells accumulate in kidney allograft tolerance and specifically suppress effector T cell expansion J. Immunol. 180 2008 7898 7906
13. L. Elzaouk, K. Moelling, and J. Pavlovic Anti-tumor activity of mesenchymal stem cells producing IL-12 in a mouse melanoma model Exp. Dermatol. 15 2006 865 874 (Pubitemid 44473325)
14. I. Fricke, N. Mirza, J. Dupont, C. Lockhart, A. Jackson, J.H. Lee, J.A. Sosman, and D.I. Gabrilovich Vascular endothelial growth factor-trap overcomes defects in dendritic cell differentiation but does not improve antigen-specific immune responses Clin. Cancer Res. 13 2007 4840 4848 (Pubitemid 47298146)
15. A.J. Friedenstein Precursor cells of mechanocytes Int. Rev. Cytol. 47 1976 327 359
16. D.I. Gabrilovich, and S. Nagaraj Myeloid-derived suppressor cells as regulators of the immune system Nat. Rev. Immunol. 9 2009 162 174
17. D.I. Gabrilovich, S. Ostrand-Rosenberg, and V. Bronte Coordinated regulation of myeloid cells by tumours Nat. Rev. Immunol. 12 2012 253 268
18. M. Gordin, M. Tesio, S. Cohen, Y. Gore, F. Lantner, L. Leng, R. Bucala, and I. Shachar c-Met and its ligand hepatocyte growth factor/scatter factor regulate mature B cell survival in a pathway induced by CD74 J. Immunol. 185 2010 2020 2031
19. I. Guleria, and M.H. Sayegh Maternal acceptance of the fetus: true human tolerance J. Immunol. 178 2007 3345 3351 (Pubitemid 46417596)
20. B. Huang, P.Y. Pan, Q. Li, A.I. Sato, D.E. Levy, J. Bromberg, C.M. Divino, and S.H. Chen Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host Cancer Res. 66 2006 1123 1131 (Pubitemid 43165981)
21. S.C. Hung, R.R. Pochampally, S.C. Chen, S.C. Hsu, and D.J. Prockop Angiogenic effects of human multipotent stromal cell conditioned medium activate the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis Stem Cells 25 2007 2363 2370 (Pubitemid 47480496)
22. A. Keating Mesenchymal stromal cells: new directions Cell Stem Cell 10 2012 709 716
23. A.H. Klopp, A. Gupta, E. Spaeth, M. Andreeff, and F. Marini 3rd Concise review: dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29 2011 11 19
24. M. Kinoshita, T. Uchida, A. Sato, M. Nakashima, H. Nakashima, S. Shono, Y. Habu, H. Miyazaki, S. Hiroi, and S. Seki Characterization of two F4/80-positive Kupffer cell subsets by their function and phenotype in mice J. Hepatol. 53 2010 903 910
25. S.H. Lee, P. Crocker, and S. Gordon Macrophage plasma membrane and secretory properties in murine malaria. Effects of Plasmodium yoelii blood-stage infection on macrophages in liver, spleen, and blood J. Exp. Med. 163 1986 54 74 (Pubitemid 16189510)
26. K. Le Blanc, and D. Mougiakakos Multipotent mesenchymal stromal cells and the innate immune system Nat. Rev. Immunol. 12 2012 383 396
27. K. Le Blanc, L. Tammik, B. Sundberg, S.E. Haynesworth, and O. Ringdén Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex Scand. J. Immunol. 57 2003 11 20 (Pubitemid 38019084)
28. K. Le Blanc, F. Frassoni, L. Ball, F. Locatelli, H. Roelofs, I. Lewis, E. Lanino, B. Sundberg, M.E. Bernardo, M. Remberger Developmental Committee of the European Group for Blood and Marrow Transplantation. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study Lancet 371 2008 1579 1586 (Pubitemid 351626841)
29. K.J. Liu, C.J. Wang, C.J. Chang, H.I. Hu, P.J. Hsu, Y.C. Wu, C.H. Bai, H.K. Sytwu, and B.L. Yen Surface expression of HLA-G is involved in mediating immunomodulatory effects of placenta-derived multipotent cells (PDMCs) towards natural killer lymphocytes Cell Transplant. 20 2011 1721 1730
30. A.L. Mellor, and D.H. Munn IDO expression by dendritic cells: tolerance and tryptophan catabolism Nat. Rev. Immunol. 4 2004 762 774 (Pubitemid 39336293)
31. M.M. Mueller, and N.E. Fusenig Friends or foes - bipolar effects of the tumour stroma in cancer Nat. Rev. Cancer 4 2004 839 849 (Pubitemid 39472951)
32. J. Nemunaitis, D.F. Andrews, D.Y. Mochizuki, M.B. Lilly, and J.W. Singer Human marrow stromal cells: response to interleukin-6 (IL-6) and control of IL-6 expression Blood 74 1989 1929 1935 (Pubitemid 19269091)
33. A.C. Ochoa, A.H. Zea, C. Hernandez, and P.C. Rodriguez Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma Clin. Cancer Res. 13 2007 721s 726s
34. S. Ostrand-Rosenberg, and P. Sinha Myeloid-derived suppressor cells: linking inflammation and cancer J. Immunol. 182 2009 4499 4506
35. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig, and D.R. Marshak Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147 (Pubitemid 29282067)
36. I. Poschke, and R. Kiessling On the armament and appearances of human myeloid-derived suppressor cells Clin. Immunol. 144 2012 250 268
37. D.J. Prockop Marrow stromal cells as stem cells for nonhematopoietic tissues Science 276 1997 71 74 (Pubitemid 27161245)
38. G.A. Rabinovich, D. Gabrilovich, and E.M. Sotomayor Immunosuppressive strategies that are mediated by tumor cells Annu. Rev. Immunol. 25 2007 267 296 (Pubitemid 46697910)
39. P.C. Rodríguez, and A.C. Ochoa Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives Immunol. Rev. 222 2008 180 191 (Pubitemid 351430370)
40. S. Sakaguchi, M. Ono, R. Setoguchi, H. Yagi, S. Hori, Z. Fehervari, J. Shimizu, T. Takahashi, and T. Nomura Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease Immunol. Rev. 212 2006 8 27 (Pubitemid 44116697)
41. P. Serafini, R. Carbley, K.A. Noonan, G. Tan, V. Bronte, and I. Borrello High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells Cancer Res. 64 2004 6337 6343 (Pubitemid 39129439)
42. K. Sheth, and P. Bankey The liver as an immune organ Curr. Opin. Crit. Care 7 2001 99 104 (Pubitemid 32411398)
43. F. Shojaei, X. Wu, A.K. Malik, C. Zhong, M.E. Baldwin, S. Schanz, G. Fuh, H.P. Gerber, and N. Ferrara Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells Nat. Biotechnol. 25 2007 911 920 (Pubitemid 47236916)
44. P. Sinha, V.K. Clements, and S. Ostrand-Rosenberg Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease J. Immunol. 174 2005 636 645 (Pubitemid 40094255)
45. P. Sinha, V.K. Clements, A.M. Fulton, and S. Ostrand-Rosenberg Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells Cancer Res. 67 2007 4507 4513 (Pubitemid 46815102)
46. M. Studeny, F.C. Marini, R.E. Champlin, C. Zompetta, I.J. Fidler, and M. Andreeff Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors Cancer Res. 62 2002 3603 3608 (Pubitemid 34728832)
47. M. Swiecki, and M. Colonna Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance Immunol. Rev. 234 2010 142 162
48. K. Takai, J. Hara, K. Matsumoto, G. Hosoi, Y. Osugi, A. Tawa, S. Okada, and T. Nakamura Hepatocyte growth factor is constitutively produced by human bone marrow stromal cells and indirectly promotes hematopoiesis Blood 89 1997 1560 1565 (Pubitemid 27097448)
49. L. Trusolino, A. Bertotti, and P.M. Comoglio MET signalling: principles and functions in development, organ regeneration and cancer Nat. Rev. Mol. Cell Biol. 11 2010 834 848
50. A. Uccelli, L. Moretta, and V. Pistoia Mesenchymal stem cells in health and disease Nat. Rev. Immunol. 8 2008 726 736
51. K. Wing, and S. Sakaguchi Regulatory T cells exert checks and balances on self tolerance and autoimmunity Nat. Immunol. 11 2010 7 13
52. H. Xin, M. Kanehira, H. Mizuguchi, T. Hayakawa, T. Kikuchi, T. Nukiwa, and Y. Saijo Targeted delivery of CX3CL1 to multiple lung tumors by mesenchymal stem cells Stem Cells 25 2007 1618 1626 (Pubitemid 47121838)
53. B.L. Yen, and M.L. Yen Mesenchymal stem cells and cancer: for better or for worse? J. Cancer Mol. 4 2008 5 9 (Pubitemid 351902828)
54. B.L. Yen, H.I. Huang, C.C. Chien, H.Y. Jui, B.S. Ko, M. Yao, C.T. Shun, M.L. Yen, M.C. Lee, and Y.C. Chen Isolation of multipotent cells from human term placenta Stem Cells 23 2005 3 9 (Pubitemid 40105287)
55. M.R. Young, and M.A. Wright Myelopoiesis-associated immune suppressor cells in mice bearing metastatic Lewis lung carcinoma tumors: gamma interferon plus tumor necrosis factor alpha synergistically reduces immune suppressor and tumor growth-promoting activities of bone marrow cells and diminishes tumor recurrence and metastasis Cancer Res. 52 1992 6335 6340
56. H. Yu, D. Pardoll, and R. Jove STATs in cancer inflammation and immunity: a leading role for STAT3 Nat. Rev. Cancer 9 2009 798 809