SOCS1 regulates the immune modulatory properties of mesenchymal stem cells by inhibiting nitric oxide production

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Zhang, Lei ^a,b   Dang, Rui Jie ^c   Li, Hong ^a   Li, Ping ^c   Yang, Yan Mei ^c   Guo, Xi Min ^a   Wang, Xiao Yan ^a   Fang, Nan Zhu ^b   Mao, Ning ^a   Wen, Ning ^c   Jiang, Xiao Xia ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b YANBIAN UNIVERSITY   (China)

^c CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; SUPPRESSOR OF CYTOKINE SIGNALING 1; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; IMMUNOLOGIC FACTOR; NITRIC OXIDE; SIGNAL PEPTIDE; SUPPRESSOR OF CYTOKINE SIGNALING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; DOWN REGULATION; ENZYME INHIBITION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; MELANOMA; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; T LYMPHOCYTE; TUMOR GROWTH; ANIMAL; C57BL MOUSE; CELL LINE; CELL PROLIFERATION; GENETICS; IMMUNOSUPPRESSIVE TREATMENT; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CYTOKINES; HUMANS; IMMUNOLOGIC FACTORS; IMMUNOSUPPRESSION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES;

EID: 84901363364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097256     Document Type: Article

References (36)

1. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147. (Pubitemid 29282067)
2. Jiang YH, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, et al. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49. (Pubitemid 34742565)
3. Zhang Y, Li CD, Jiang XX, Zhang SX, Wu Y, et al. (2004) Human placenta-derived mesenchymal progenitor cells support culture expansion of long-term culture-initiating cells from cord blood CD34(+) cells. Experimental hematology 32, 657-664. (Pubitemid 38891535)
4. Chamberlain G, Fox J, Ashton B, Middleton J (2007) Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. Stem cells 25, 2739-2749. (Pubitemid 350127858)
5. Caplan AI (2007) Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. Journal of cellular physiology 213, 341-347.
6. Le Blanc K, Rasmusson I, Sundberg B, Gotherstrom C, Hassan M, et al. (2004) Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363, 1439-1441. (Pubitemid 38586721)
7. Ren GW, Zhang LY, Zhao X, Xu GW, Zhang YY, et al. (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell stem cell 2, 141-150. (Pubitemid 351181031)
8. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, et al. (2007) Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109, 228-234. (Pubitemid 46053063)
9. Asari S, Itakura S, Ferreri K, Liu CP, Kuroda Y, et al. (2009) Mesenchymal stem cells suppress B-cell terminal differentiation. Experimental hematology 37, 604-615.
10. Chatterjee D, Hass R, Marquardt N, Kasper C, Schmidt RE, et al. (2012) Human mesenchymal stem cell mediated suppression of NK cell effector functions. Immunology 137, 92-92.
11. Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, et al. (2005) Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105, 4120-4126. (Pubitemid 40656164)
12. Shi YF, Su JJ, Roberts AI, Shou PS, Rabson AB, et al. (2012) How mesenchymal stem cells interact with tissue immune responses. Trends in immunology 33, 136-143.
13. Li W, Ren G, Huang Y, Su J, Han Y, et al. (2012) Mesenchymal stem cells: a double-edged sword in regulating immune responses. Cell death and differentiation 19, 1505-1513.
14. Kubo M, Hanada T, Yoshimura A (2003) Suppressors of cytokine signaling and immunity. Nature immunology 4, 1169-1176. (Pubitemid 37540685)
15. Waiboci LW, Ahmed CM, Mujtaba MG, Flowers LO, Martin JP, et al. (2007) Both the suppressor of cytokine signaling 1 (SOCS-1) kinase inhibitory region and SOCS-1 mimetic bind to JAK2 autophosphorylation site: Implications for the development of a SOCS-1 antagonist. Journal of immunology 178, 5058-5068. (Pubitemid 46595289)
16. Sayama K, Dai X, Tohyama M, Yamasaki K, Shirakata Y, et al. (2004) SOCS-1 negative feedback mechanism of STAT1 activation is a key pathway in the dsRNA-induced innate immune response of human keratinocytes. J Invest Dermatol 122, A132-A132.
17. Yahata Y, Yamasaki K, Shirakata Y, Tohyama M, Sayama K, et al. (2004) SOCS1 is a negative regulator of the MyD88-independent signaling pathway of the LPS-induced TLR4 natural immune response in HDMEC. J Invest Dermatol 122, A2-A2.
18. Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annual review of immunology 21, 685-711. (Pubitemid 37174545)
19. Shen L, Evel-Kabler K, Strube R, Chen SY (2004) Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific anti-tumor immunity. Nature biotechnology 22, 1546-1553. (Pubitemid 40039457)
20. Martinez FO, Sica A, Mantovani A, Locati M (2008) Macrophage activation and polarization. Front Biosci-Landmrk 13, 453-461. (Pubitemid 351599757)
21. Wilson HM (2010) Macrophages heterogeneity in atherosclerosis - implications for therapy. Journal of cellular and molecular medicine 14, 2055-2065.
22. Whyte CS, Bishop ET, Ruckerl D, Gaspar-Pereira S, Barker RN, et al. (2011) Suppressor of cytokine signaling (SOCS)1 is a key determinant of differential macrophage activation and function. Journal of leukocyte biology 90, 845-854.
23. Yang YM, Li H, Zhang L, Dang RJ, Li P, et al. (2013) [A new method for isolating and culturing mouse bone marrow mesenchymal stem cells]. Zhongguo shi yan xue ye xue za zhi/Zhongguo bing li sheng li xue hui = Journal of experimental hematology/Chinese Association of Pathophysiology 21, 1563-1567.
24. Alexander WS, Starr R, Fenner JE, Scott CL, Handman E, et al. (1999) SOCS1 is a critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98, 597-608. (Pubitemid 29418951)
25. Chinen T, Kobayashi T, Ogata H, Takaesu G, Takaki H, et al. (2006) Suppressor of cytokine signaling-1 regulates inflammatory bowel disease in which both IFNgamma and IL-4 are involved. Gastroenterology 130, 373-388. (Pubitemid 43202037)
26. Ryo A, Suizu F, Yoshida Y, Perrem K, Liou YC, et al. (2003) Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitinmediated proteolysis of p65/RelA. Molecular cell 12, 1413-1426. (Pubitemid 38037011)
27. Fenner JE, Starr R, Cornish AL, Zhang JG, Metcalf D, et al. (2006) Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon activity. Nature immunology 7, 33-39. (Pubitemid 41823866)
28. Hanada T, Tanaka K, Matsumura Y, Yamauchi M, Nishinakamura H, et al. (2005) Induction of hyper Th1 cell-type immune responses by dendritic cells lacking the suppressor of cytokine signaling-1 gene. Journal of immunology 174, 4325-4332. (Pubitemid 40396015)
29. Kinjyo I, Hanada T, Inagaki-Ohara K, Mori H, Aki D, et al. (2002) SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 17, 583-591. (Pubitemid 35351504)
30. Jorgensen C (2010) Mesenchymal stem cells in arthritis: role of bone marrow microenvironment. Arthritis research & therapy 12, 135.
31. Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G (2007) Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis and rheumatism 56, 1175-1186. (Pubitemid 46608642)
32. Djouad F, Fritz V, Apparailly F, Louis-Plence P, Bony C, et al. (2005) Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis and rheumatism 52, 1595-1603. (Pubitemid 40663952)
33. Clancy RM, Amin AR, Abramson SB (1998) The role of nitric oxide in inflammation and immunity. Arthritis and rheumatism 41, 1141-1151. (Pubitemid 28313414)
34. Sahin G, Guler H, Sezgin M, Incel NA, Polat G (2006) The effect of circulating nitric oxide level on axial bone mineral density in postmenopausal Turkish women with rheumatoid arthritis: A preliminary report. Rheumatology international 26, 805-809. (Pubitemid 43881807)
35. Su J, Chen X, Huang Y, Li W, Li J, et al. (2014) Phylogenetic distinction of iNOS and IDO function in mesenchymal stem cell-mediated immunosuppression in mammalian species. Cell death and differentiation 21, 388-396.
36. Ma S, Xie N, Li W, Yuan B, Shi Y, et al. (2014) Immunobiology of mesenchymal stem cells. Cell death and differentiation 21, 216-225.