Monocytic myeloid-derived suppressor cells from females, but not males, alleviate CVB3-induced myocarditis by increasing regulatory and CD4+ IL-10+ T cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Su, Nan ^a   Yue, Yan ^a   Xiong, Sidong ^a  

^a SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IL10 PROTEIN, MOUSE; INTERLEUKIN 10;

ANIMAL; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; CHEMISTRY; COXSACKIE VIRUS INFECTION; DISEASE MODEL; ENTEROVIRUS B; FEMALE; IMMUNOLOGY; MALE; MYELOID-DERIVED SUPPRESSOR CELL; MYOCARDITIS; SEX FACTOR; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; COXSACKIEVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; ENTEROVIRUS B, HUMAN; FEMALE; INTERLEUKIN-10; MALE; MICE, INBRED BALB C; MYELOID-DERIVED SUPPRESSOR CELLS; MYOCARDITIS; SEX FACTORS; T-LYMPHOCYTE SUBSETS;

EID: 84960424448     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22658     Document Type: Article

References (49)

1. Mason, J. W. Myocarditis and dilated cardiomyopathy: an inflammatory link. Cardiovasc Res 60, 5-10 (2003).
2. Pollack, A., Kontorovich, A. R., Fuster, V. & Dec, G. W. Viral myocarditis-diagnosis, treatment options, and current controversies. Nat Rev Cardiol 12, 670-680, (2015).
3. Gupta, S., Markham, D. W., Drazner, M. H. & Mammen, P. P. Fulminant myocarditis. Nat Clin Pract Cardiovasc Med 5, 693-706 (2008).
4. Calabrese, F. et al. Molecular diagnosis of myocarditis and dilated cardiomyopathy in children: clinicopathologic features and prognostic implications. Diagn Mol Pathol 11, 212-221 (2002).
5. Leonard, E. G. Viral myocarditis. Pediatr Infect Dis J 23, 665-666 (2004).
6. Godeny, E. K. & Gauntt, C. J. Involvement of natural killer cells in coxsackievirus B3-induced murine myocarditis. J Immunol 137, 1695-1702 (1986).
7. Coronado, M. J. et al. Testosterone and interleukin-1beta increase cardiac remodeling during coxsackievirus B3 myocarditis via serpin A 3n. Am J Physiol Heart Circ Physiol 302, H1726-1736 (2012).
8. Frisancho-Kiss, S. et al. Sex differences in coxsackievirus B3-induced myocarditis: IL-12Rbeta1 signaling and IFN-gamma increase inflammation in males independent from STAT4. Brain research 1126, 139-147, (2006).
9. Koenig, A., Sateriale, A., Budd, R. C., Huber, S. A. & Buskiewicz, I. A. The role of sex differences in autophagy in the heart during coxsackievirus B3-induced myocarditis. J Cardiovasc Transl Res 7, 182-191, (2014).
10. Woodruff, J. F. Viral myocarditis. A review. Am J Pathol 101, 425-484 (1980).
11. Frisancho-Kiss, S. et al. Cutting edge: cross-regulation by TLR4 and T cell Ig mucin-3 determines sex differences in inflammatory heart disease. J Immunol 178, 6710-6714 (2007).
12. Papageorgiou, A. P. et al. Thrombospondin-2 prevents cardiac injury and dysfunction in viral myocarditis through the activation of regulatory T-cells. Cardiovasc Res 94, 115-124, (2012).
13. He, F. et al. Inhibition of IL-2 inducible T-cell kinase alleviates T-cell activation and murine myocardial inflammation associated with CVB3 infection. Mol Immunol 59, 30-38 (2014).
14. Huber, S. A. & Pfaeffle, B. Differential Th1 and Th2 cell responses in male and female BALB/c mice infected with coxsackievirus group B type 3. J Virol 68, 5126-5132 (1994).
15. Liu, L., Yue, Y. & Xiong, S. NK-derived IFN-gamma/IL-4 triggers the sexually disparate polarization of macrophages in CVB3- induced myocarditis. J Mol Cell Cardiol 76, 15-25 (2014).
16. Li, K. et al. Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ Res 105, 353-364 (2009).
17. Gabrilovich, D. I. & Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9, 162-174 (2009).
18. Ding, Z. C. et al. Immunosuppressive myeloid cells induced by chemotherapy attenuate antitumor CD4+ T-cell responses through the PD-1-PD-L1 axis. Cancer Res 74, 3441-3453 (2014).
19. Nagaraj, S. & Gabrilovich, D. I. Tumor escape mechanism governed by myeloid-derived suppressor cells. Cancer Res 68, 2561-2563 (2008).
20. Vollbrecht, T. et al. Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS 26, F31-37, (2012).
21. Brudecki, L., Ferguson, D. A., McCall, C. E. & El Gazzar, M. Myeloid-derived suppressor cells evolve during sepsis and can enhance or attenuate the systemic inflammatory response. Infect Immun 80, 2026-2034 (2012).
22. Skabytska, Y. et al. Cutaneous Innate Immune Sensing of Toll-like Receptor 2-6 Ligands Suppresses T Cell Immunity by Inducing Myeloid-Derived Suppressor Cells. Immunity 41, 762-775 (2014).
23. Youn, J. I. & Gabrilovich, D. I. The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol 40, 2969-2975 (2010).
24. Tacke, R. S. et al. Myeloid suppressor cells induced by hepatitis C virus suppress T-cell responses through the production of reactive oxygen species. Hepatology 55, 343-353 (2012).
25. Fortin, C., Huang, X. & Yang, Y. NK cell response to vaccinia virus is regulated by myeloid-derived suppressor cells. Journal of immunology (Baltimore, Md.: 1950) 189, 1843-1849 (2012).
26. De Santo, C. et al. Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid-derived suppressor cells in mice and humans. J Clin Invest 118, 4036-4048 (2008).
27. Derive, M., Bouazza, Y., Alauzet, C. & Gibot, S. Myeloid-derived suppressor cells control microbial sepsis. Intensive Care Med 38, 1040-1049 (2012).
28. Pereira, W. F. et al. Myeloid-derived suppressor cells help protective immunity to Leishmania major infection despite suppressed T cell responses. J Leukoc Biol 90, 1191-1197 (2011).
29. Cuervo, H. et al. Myeloid-derived suppressor cells infiltrate the heart in acute Trypanosoma cruzi infection. J Immunol 187, 2656-2665 (2011).
30. Dong, G. et al. 17beta-estradiol contributes to the accumulation of myeloid-derived suppressor cells in blood by promoting TNFalpha secretion. Acta Biochim Biophys Sin (Shanghai) 47, 620-629 (2015).
31. Fletcher, M. et al. L-Arginine depletion blunts anti-tumor T cell responses by inducing myeloid-derived suppressor cells. Cancer Res 75, 275-83 (2015).
32. Jeisy-Scott, V. et al. Increased MDSC accumulation and Th2 biased response to influenza A virus infection in the absence of TLR7 in mice. PLoS One 6, e25242 (2011).
33. Chen, S., Akbar, S. M., Abe, M., Hiasa, Y. & Onji, M. Immunosuppressive functions of hepatic myeloid-derived suppressor cells of normal mice and in a murine model of chronic hepatitis B virus. Clin Exp Immunol 166, 134-142 (2011).
34. Huang, A. et al. Myeloid-Derived Suppressor Cells Regulate Immune Response in Patients with Chronic Hepatitis B Virus Infection through PD-1-Induced IL-10. J Immunol 193, 5461-5469 (2014).
35. Shirota, Y., Shirota, H. & Klinman, D. M. Intratumoral injection of CpG oligonucleotides induces the differentiation and reduces the immunosuppressive activity of myeloid-derived suppressor cells. J Immunol 188, 1592-1599 (2012).
36. Fujita, M. et al. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res 71, 2664-2674 (2011).
37. Youn, J. I., Nagaraj, S., Collazo, M. & Gabrilovich, D. I. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 181, 5791-5802 (2008).
38. Lan, X., Qu, H., Yao, W. & Zhang, C. Granulocyte-colony stimulating factor inhibits neuronal apoptosis in a rat model of diabetic cerebral ischemia. Tohoku J Exp Med 216, 117-126 (2008).
39. Greifenberg, V., Ribechini, E., Rossner, S. & Lutz, M. B. Myeloid-derived suppressor cell activation by combined LPS and IFNgamma treatment impairs DC development. Eur J Immunol 39, 2865-2876 (2009).
40. Morales, J. K., Kmieciak, M., Knutson, K. L., Bear, H. D. & Manjili, M. H. GM-CSF is one of the main breast tumor-derived soluble factors involved in the differentiation of CD11b-Gr1- bone marrow progenitor cells into myeloid-derived suppressor cells. Breast Cancer Res Treat 123, 39-49 (2010).
41. Zhu, B. et al. CD11b+ Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J Immunol 179, 5228-5237 (2007).
42. Dardalhon, V. et al. Tim-3/galectin-9 pathway: regulation of Th1 immunity through promotion of CD11b+ Ly-6G+ myeloid cells. J Immunol 185, 1383-1392 (2010).
43. Corzo, C. A. et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 207, 2439-2453 (2010).
44. Shi, Y. et al. Regulatory T cells protect mice against coxsackievirus-induced myocarditis through the transforming growth factor beta-coxsackie-adenovirus receptor pathway. Circulation 121, 2624-2634 (2010).
45. Watanabe, K. et al. Protection against autoimmune myocarditis by gene transfer of interleukin-10 by electroporation. Circulation 104, 1098-1100 (2001).
46. Li, Z., Yue, Y. & Xiong, S. Distinct Th17 inductions contribute to the gender bias in CVB3-induced myocarditis. Cardiovasc Pathol 22, 373-382 (2013).
47. Gallina, G. et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 116, 2777-2790 (2006).
48. Maeda, A. et al. Monocytic MDSCs regulate macrophage-mediated xenogenic cytotoxicity. Transpl Immunol 33, 140-145 (2015).
49. Li, Z., Yue, Y. & Xiong, S. Distinct Th17 inductions contribute to the gender bias in CVB3-induced myocarditis. Cardiovasc Pathol 22, 373-82 (2013).