Reciprocal relationship of T regulatory cells and monocytic myeloid-derived suppressor cells in LP-BM5 murine retrovirus-induced immunodeficiency

Journal of General Virology

Volumn 97, Issue 2, 2016, Pages 509-522

  O’Connor, Megan A ^a   Vella, Jennifer L ^a   Green, William R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MONOCYTIC MYELOID DERIVED SUPPRESSOR CELL; MOUSE; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RETROVIRIDAE; RETROVIRUS INDUCED IMMUNODEFICIENCY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SUPPRESSOR CELL; T LYMPHOCYTE; TUMOR MICROENVIRONMENT; ANIMAL; C57BL MOUSE; IMMUNOLOGY; MONOCYTE; PATHOLOGY; PHYSIOLOGY; RETROVIRUS INFECTION; VIROLOGY;

ANIMALS; IMMUNOLOGIC DEFICIENCY SYNDROMES; MICE, INBRED C57BL; MONOCYTES; RETROVIRIDAE; RETROVIRIDAE INFECTIONS; T-LYMPHOCYTES, REGULATORY;

EID: 84959120733     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000260     Document Type: Article

References (91)

1. +T cells are differentially affected by simian immunodeficiency virus infection in rhesus macaques. J Virol 84, 3259-3269.
2. Angin, M., Kwon, D. S., Streeck, H., Wen, F., King, M., Rezai, A., Law, K., Hongo, T. C., Pyo, A. & other authors (2012). Preserved function of regulatory T cells in chronic HIV-1 infection despite decreased numbers in blood and tissue. J Infect Dis 205, 1495-1500.
3. + lymphocytes from HIV-positive patients. J Acquir Immune Defic Syndr 39, 381-385.
4. +T cells. Clin Immunol 115, 10-18.
5. +T cell depletion, immune activation and increased production of regulatory T cells in the thymus of HIV-infected individuals. PLoS One 5, e10788.
6. +T cells can prevent murine AIDS progression. J Immunol 172, 4917-4925.
7. + Treg in HIV-1-infected patients with low CD4 counts. Eur J Immunol 39, 301-309.
8. Bowers, N. L., Helton, E. S., Huijbregts, R. P. H., Goepfert, P. A., Heath, S. L. & Hel, Z. (2014). Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog 10, e1003993.
9. Cerny, A., Hügin, A. W., Hardy, R. R., Hayakawa, K., Zinkernagel, R. M., Makino, M. & Morse, H. C., III (1990). B cells are required for induction of T cell abnormalities in a murine retrovirus-induced immunodeficiency syndrome. J Exp Med 171, 315-320.
10. +T-cell activation. J Virol 82, 8307-8315.
11. Chen, S., Akbar, S. M. F., Abe, M., Hiasa, Y. & Onji, M. (2011). 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.
12. Chevalier, M. F. & Weiss, L. (2013). The split personality of regulatory T cells in HIV infection. Blood 121, 29-37.
13. +T cells. J Infect Dis 211, 769-779.
14. Corzo, C. A., Condamine, T., Lu, L., Cotter, M. J., Youn, J.-I., Cheng, P., Cho, H.-I., Celis, E., Quiceno, D. G. & other authors (2010). HIF-1a regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 207, 2439-2453.
15. +T cell immunity by recruiting inflammatory monocytes. Immunity 37, 122-133.
16. Dannull, J., Su, Z., Rizzieri, D., Yang, B. K., Coleman, D., Yancey, D., Zhang, A., Dahm, P., Chao, N. & other authors (2005). Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 115, 3623-3633.
17. + population induces T cell suppression and Th2 polarization in sepsis. J Exp Med 204, 1463-1474.
18. +T cells and reduces chronic retroviral set points. Proc Natl Acad Sci U S A 108, 2420-2425.
19. +T cells by regulatory T cells during persistent retroviral infection. Immunity 20, 293-303.
20. Duraiswamy, J., Kaluza, K. M., Freeman, G. J. & Coukos, G. (2013). Dual blockade of PD-1 and CTLA-4 combined with tumor vaccine effectively restores T-cell rejection function in tumors. Cancer Res 73, 3591-3603.
21. Favre, D., Lederer, S., Kanwar, B., Ma, Z.-M., Proll, S., Kasakow, Z., Mold, J., Swainson, L., Barbour, J. D. & other authors (2009). Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog 5, e1000295.
22. Fortin, C., Huang, X. & Yang, Y. (2012). NK cell response to vaccinia virus is regulated by myeloid-derived suppressor cells. J Immunol 189, 1843-1849.
23. Fujimura, T., Ring, S., Umansky, V., Mahnke, K. & Enk, A. H. (2012). Regulatory T cells stimulate B7-H1 expression in myeloid-derived suppressor cells in ret melanomas. J Invest Dermatol 132, 1239-1246.
24. Gabrilovich, D. I. & Nagaraj, S. (2009). Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9, 162-174.
25. Garg, A. & Spector, S. A. (2014). HIV type 1 gp120-induced expansion of myeloid derived suppressor cells is dependent on interleukin 6 and suppresses immunity. J Infect Dis 209, 441-451.
26. + subset regulation in viral infection. Preferential activation of Th2 cells during progression of retrovirus-induced immunodeficiency in mice. J Immunol 148, 182-188.
27. Giordanengo, L., Guiñ azu´, N., Stempin, C., Fretes, R., Cerbán, F. & Gea, S. (2002). Cruzipain, a major Trypanosoma cruzi antigen, conditions the host immune response in favor of parasite. Eur J Immunol 32, 1003-1011.
28. + immature myeloid suppressor cells. Int Immunol 14, 1125-1134.
29. Green, K. A., Crassi, K. M., Laman, J. D., Schoneveld, A., Strawbridge, R. R., Foy, T. M., Noelle, R. J. & Green, W. R. (1996). Antibody to the ligand for CD40 (gp39) inhibits murine AIDS-associated splenomegaly, hypergammaglobulinemia, and immunodeficiency in disease-susceptible C57BL/6 mice. J Virol 70, 2569-2575.
30. Green, K. A., Noelle, R. J. & Green, W. R. (1998). Evidence for a continued requirement for CD40/CD40 ligand (CD154) interactions in the progression of LP-BM5 retrovirus-induced murine AIDS. Virology 241, 260-268.
31. Green, K. A., Noelle, R. J., Durell, B. G. & Green, W. R. (2001). Characterization of the CD154-positive and CD40-positive cellular subsets required for pathogenesis in retrovirus-induced murine immunodeficiency. J Virol 75, 3581-3589.
32. Green, K. A., Cook, W. J., Sharpe, A. H. & Green, W. R. (2002). The CD154/CD40 interaction required for retrovirus-induced murine immunodeficiency syndrome is not mediated by upregulation of the CD80/CD86 costimulatory molecules. J Virol 76, 13106-13110.
33. Green, K. A., Okazaki, T., Honjo, T., Cook, W. J. & Green, W. R. (2008). The programmed death-1 and interleukin-10 pathways play a downmodulatory role in LP-BM5 retrovirus-induced murine immunodeficiency syndrome. J Virol 82, 2456-2469.
34. Green, K. A., Cook, W. J. & Green, W. R. (2013). Myeloid-derived suppressor cells in murine retrovirus-induced AIDS inhibit T-and B-cell responses in vitro that are used to define the immunodeficiency. J Virol 87, 2058-2071.
35. Hamann, A. (2012). Regulatory T cells stay on course. Immunity 36, 161-163.
36. + immature myeloid suppressor cells mediate the development of tumorinduced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 66, 1123-1131.
37. Huang, J., Jochems, C., Talaie, T., Anderson, A., Jales, A., Tsang, K. Y., Madan, R. A., Gulley, J. L. & Schlom, J. (2012). Elevated serum soluble CD40 ligand in cancer patients may play an immunosuppressive role. Blood 120, 3030-3038.
38. Jenabian, M.-A., Seddiki, N., Yatim, A., Carriere, M., Hulin, A., Younas, M., Ghadimi, E., Kök, A., Routy, J.-P. & other authors (2013). Regulatory T cells negatively affect IL-2 production of effector T cells through CD39/adenosine pathway in HIV infection. PLoS Pathog 9, e1003319.
39. Jenabian, M.-A., Patel, M., Kema, I., Vyboh, K., Kanagaratham, C., Radzioch, D., Thé bault, P., Lapointe, R., Gilmore, N. & other authors (2014). Soluble CD40-ligand (sCD40L, sCD154) plays an immunosuppressive role via regulatory T cell expansion in HIV infection. Clin Exp Immunol 178, 102-111.
40. + regulatory T cells play an important role in acute HIV-1 infection in humanized Rag22/2C2/2 mice in vivo. Blood 112, 2858-2868.
41. + regulatory T cells from HIV-infected individuals. Proc Natl Acad Sci U S A 104, 3390-3395.
42. Klinken, S. P., Fredrickson, T. N., Hartley, J. W., Yetter, R. A. & Morse, H. C., III (1988). Evolution of B cell lineage lymphomas in mice with a retrovirus-induced immunodeficiency syndrome, MAIDS. J Immunol 140, 1123-1131.
43. Klinman, D. M. & Morse, H. C., III (1989). Characteristics of B cell proliferation and activation in murine AIDS. J Immunol 142, 1144-1149.
44. Ko, J. S., Zea, A. H., Rini, B. I., Ireland, J. L., Elson, P., Cohen, P., Golshayan, A., Rayman, P. A., Wood, L. & other authors (2009). Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res 15, 2148-2157.
45. Li, W. & Green, W. R. (2006). The role of CD4 T cells in the pathogenesis of murine AIDS. J Virol 80, 5777-5789.
46. Li, W. & Green, W. R. (2007). Murine AIDS requires CD154/CD40L expression by the CD4 T cells that mediate retrovirus-induced disease: is CD4 T cell receptor ligation needed? Virology 360, 58-71.
47. Li, W. & Green, W. R. (2011). Immunotherapy of murine retrovirusinduced acquired immunodeficiency by CD4 T regulatory cell depletion and PD-1 blockade. J Virol 85, 13342-13353.
48. Lim, H. W., Hillsamer, P. & Kim, C. H. (2004). Regulatory T cells can migrate to follicles upon T cell activation and suppress GC-Th cells and GC-Th cell-driven B cell responses. J Clin Invest 114, 1640-1649.
49. Liovat, A.-S., Rey-Cuillé, M.-A., Lécuroux, C., Jacquelin, B., Girault, I., Petitjean, G., Zitoun, Y., Venet, A., Barré-Sinoussi, F. & other authors (2012). Acute plasma biomarkers of T cell activation setpoint levels and of disease progression in HIV-1 infection. PLoS One 7, e46143.
50. Liu, G., Bi, Y., Shen, B., Yang, H., Zhang, Y., Wang, X., Liu, H., Lu, Y., Liao, J. & other authors (2014). SIRT1 limits the function and fate of myeloid-derived suppressor cells in tumors by orchestrating HIF-1adependent glycolysis. Cancer Res 74, 727-737.
51. Mascanfroni, I. D., Takenaka, M. C., Yeste, A., Patel, B., Wu, Y., Kenison, J. E., Siddiqui, S., Basso, A. S., Otterbein, L. E. & other authors (2015). Metabolic control of type 1 regulatory T cell differentiation by AHR and HIF1-a. Nat Med 21, 638-646.
52. + and Foxp32 precursor cells in the absence of interleukin 10. Nat Immunol 8, 931-941.
53. + myeloid cells inhibit development of antifungal Th1 immunity in mice with candidiasis. J Immunol 169, 3180-3190.
54. Moir, S. & Fauci, A. S. (2008). Pathogenic mechanisms of B-lymphocyte dysfunction in HIV disease. J Allergy Clin Immunol 122, 12-19 quiz 20-21.
55. Moreno-Fernandez, M. E., Presicce, P. & Chougnet, C. A. (2012). Homeostasis and function of regulatory T cells in HIV/SIV infection. J Virol 86, 10262-10269.
56. Morse, H. C., III, Yetter, R. A., Via, C. S., Hardy, R. R., Cerny, A., Hayakawa, K., Hugin, A. W., Miller, M. W., Holmes, K. L. & Shearer, G. M. (1989). Functional and phenotypic alterations in T cell subsets during the course of MAIDS, a murine retrovirus-induced immunodeficiency syndrome. J Immunol 143, 844-850.
57. Mosier, D. E., Yetter, R. A. & Morse, H. C., III (1985). Retroviral induction of acute lymphoproliferative disease and profound immunosuppression in adult C57BL/6 mice. J Exp Med 161, 766-784.
58. Mosier, D. E., Yetter, R. A. & Morse, H. C., III (1987). Functional T lymphocytes are required for a murine retrovirus-induced immunodeficiency disease (MAIDS). J Exp Med 165, 1737-1742.
59. +CD25 T cells via p53, IL-2, and OX40. Proc Natl Acad Sci U S A 104, 15478-15483.
60. Noman, M. Z., Desantis, G., Janji, B., Hasmim, M., Karray, S., Dessen, P., Bronte, V. & Chouaib, S. (2014). PD-L1 is a novel direct target of HIF-1a, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med 211, 781-790.
61. O’Connor, M. A. & Green, W. R. (2013). The role of indoleamine 2,3-dioxygenase in LP-BPM5 murine retroviral disease progression. Virol J 10, 154.
62. O’Connor, M. A. & Green, W. R. (2014). Use of IRF-3 and/or IRF-7 knockout mice to study viral pathogenesis: lessons from a murine retrovirus-induced AIDS model. J Virol 88, 2349-2353.
63. O’Connor, M. A., Fu, W. W., Green, K. A. & Green, W. R. (2015). Subpopulations of M-MDSCs from mice infected by an immunodeficiency-causing retrovirus and their differential suppression of T-vs B-cell responses. Virology 485, 263-273.
64. Pan, P.-Y., Ma, G., Weber, K. J., Ozao-Choy, J., Wang, G., Yin, B., Divino, C. M. & Chen, S.-H. (2010). Immune stimulatory receptor CD40 is required for T-cell suppression and T regulatory cell activation mediated by myeloid-derived suppressor cells in cancer. Cancer Res 70, 99-108.
65. Phetsouphanh, C., Xu, Y. & Zaunders, J. (2014). CD4 T cells mediate both positive and negative regulation of the immune response to HIV infection: complex role of T follicular helper cells and regulatory T cells in pathogenesis. Front Immunol 5, 681.
66. Qin, A., Cai, W., Pan, T., Wu, K., Yang, Q., Wang, N., Liu, Y., Yan, D., Hu, F. & other authors (2013). Expansion of monocytic myeloid-derived suppressor cells dampens T cell function in HIV-1-seropositive individuals. J Virol 87, 1477-1490.
67. Rech, A. J., Mick, R., Martin, S., Recio, A., Aqui, N. A., Powell, D. J. Jr., Colligon, T. A., Trosko, J. A., Leinbach, L. I. & other authors (2012). CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients. Sci Transl Med 4, 34ra62.
68. + regulatory T-cell expansion, maintenance and IL-10 production during helminth infection. Eur J Immunol 43, 705-715.
69. +T cell function by Friend virus-induced regulatory T cells. J Immunol 176, 3342-3349.
70. +T regulatory cells correlates with progressive disease. J Virol 85, 1287-1297.
71. Serafini, P., Mgebroff, S., Noonan, K. & Borrello, I. (2008). Myeloidderived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res 68, 5439-5449.
72. Simard, C., Klein, S. J., Mak, T. & Jolicoeur, P. (1997). Studies of the susceptibility of nude, CD4 knockout, and SCID mutant mice to the disease induced by the murine AIDS defective virus. J Virol 71, 3013-3022.
73. Simonetta, F., Lecuroux, C., Girault, I., Goujard, C., Sinet, M., Lambotte, O., Venet, A. & Bourgeois, C. (2012). Early and longlasting alteration of effector CD45RA2Foxp3high regulatory T-cell homeostasis during HIV infection. J Infect Dis 205, 1510-1519.
74. Suchard, M. S., Mayne, E., Green, V. A., Shalekoff, S., Donninger, S. L., Stevens, W. S., Gray, C. M. & Tiemessen, C. T. (2010). FOXP3 expression is upregulated in CD4T cells in progressive HIV-1 infection and is a marker of disease severity. PLoS One 5, e11762.
75. Sui, Y., Hogg, A., Wang, Y., Frey, B., Yu, H., Xia, Z., Venzon, D., McKinnon, K., Smedley, J. & other authors (2014). Vaccineinduced myeloid cell population dampens protective immunity to SIV. J Clin Invest 124, 2538-2549.
76. Sunderkötter, C., Nikolic, T., Dillon, M. J., Van Rooijen, N., Stehling, M., Drevets, D. A. & Leenen, P. J. M. (2004). Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 172, 4410-4417.
77. Taieb, J., Chaput, N., Schartz, N., Roux, S., Novault, S., Mé nard, C., Ghiringhelli, F., Terme, M., Carpentier, A. F. & other authors (2006). Chemoimmunotherapy of tumors: cyclophosphamide synergizes with exosome based vaccines. J Immunol 176, 2722-2729.
78. Talmadge, J. E. & Gabrilovich, D. I. (2013). History of myeloidderived suppressor cells. Nat Rev Cancer 13, 739-752.
79. Tan, C., Reddy, V., Dannull, J., Ding, E., Nair, S. K., Tyler, D. S., Pruitt, S. K. & Lee, W. T. (2013). Impact of anti-CD25 monoclonal antibody on dendritic cell-tumor fusion vaccine efficacy in a murine melanoma model. J Transl Med 11, 148.
80. + cells: a potential mechanism for immune polarization in helminth infections. J Immunol 167, 5294-5303.
81. + T-cellmediated antitumor immunity induced by DNA vaccination. Clin Cancer Res 14, 3185-3192.
82. Uehara, S., Hitoshi, Y., Numata, F., Makino, M., Howard, M., Mizuochi, T. & Takatsu, K. (1994). An IFN-c-dependent pathway plays a critical role in the pathogenesis of murine immunodeficiency syndrome induced by LP-BM5 murine leukemia virus. Int Immunol 6, 1937-1947.
83. + myeloid cells and anergy of T lymphocytes participate in hyporesponsiveness of the lung-associated immune system during acute toxoplasmosis. Infect Immun 72, 5487-5492.
84. Vollbrecht, T., Stirner, R., Tufman, A., Roider, J., Huber, R. M., Bogner, J. R., Lechner, A., Bourquin, C. & Draenert, R. (2012). Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS 26, F31-F37.
85. Wesolowski, R., Markowitz, J. & Carson, W. E., III (2013). Myeloid derived suppressor cells-a new therapeutic target in the treatment of cancer. J Immunother Cancer 1, 10.
86. Witsch, E. J., Peiser, M., Hutloff, A., Büchner, K., Dorner, B. G., Jonuleit, H., Mages, H. W. & Kroczek, R. A. (2002). ICOS and CD28 reversely regulate IL-10 on re-activation of human effector T cells with mature dendritic cells. Eur J Immunol 32, 2680-2686.
87. Workman, C. J., Szymczak-Workman, A. L., Collison, L. W., Pillai, M. R. & Vignali, D. A. A. (2009). The development and function of regulatory T cells. Cell Mol Life Sci 66, 2603-2622.
88. + myeloid cells. Cancer Res 66, 6807-6815.
89. + regulatory T cell responses during Friend retrovirus infection. Eur J Immunol 36, 2658-2670.
90. Zelinskyy, G., Dietze, K. K., Hüsecken, Y. P., Schimmer, S., Nair, S., Werner, T., Gibbert, K., Kershaw, O., Gruber, A. D. & other authors (2009). The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood 114, 3199-3207.
91. Zhou, X., Bailey-Bucktrout, S. L., Jeker, L. T., Penaranda, C., Martínez-Llordella, M., Ashby, M., Nakayama, M., Rosenthal, W. & Bluestone, J. A. (2009). Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol 10, 1000-1007.