1887

Abstract

Immunomodulatory cellular subsets, including myeloid-derived suppressor cells (MDSCs) and T regulatory cells (Tregs), contribute to the immunosuppressive tumour microenvironment and are targets of immunotherapy, but their role in retroviral-associated immunosuppression is less well understood. Due to known crosstalk between Tregs and MDSCs in the tumour microenvironment, and also their hypothesized involvement during human immunodeficiency virus/simian immunodeficiency virus infection, studying the interplay between these immune cells during LP-BM5 retrovirus-induced murine AIDS is of interest. IL-10-producing FoxP3 Tregs expanded after LP-BM5 infection. Following adoptive transfer of natural Treg (nTreg)-depleted CD4T-cells, and subsequent LP-BM5 retroviral infection, enriched monocytic MDSCs (M-MDSCs) from these nTreg-depleted mice displayed altered phenotypic subsets. In addition, M-MDSCs from LP-BM5-infected nTreg-depleted mice exhibited increased suppression of T-cell, but not B-cell, responses, compared with M-MDSCs derived from non-depleted LP-BM5-infected controls. Additionally, LP-BM5-induced M-MDSCs modulated the production of IL-10 by FoxP3 Tregs . These collective data highlight and for the first time, to the best of our knowledge, reciprocal modulation between retroviral-induced M-MDSCs and Tregs, and may provide insight into the immunotherapeutic targeting of such regulatory cells during retroviral infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000260
2016-02-01
2020-04-07
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/2/509.html?itemId=/content/journal/jgv/10.1099/jgv.0.000260&mimeType=html&fmt=ahah

References

  1. Allers K., Loddenkemper C., Hofmann J., Unbehaun A., Kunkel D., Moos V., Kaup F.-J., Stahl-Hennig C., Sauermann U., other authors. 2010; Gut mucosal FOXP3+ regulatory CD4+T cells and nonregulatory CD4+T cells are differentially affected by simian immunodeficiency virus infection in rhesus macaques. J Virol84:3259–3269 [CrossRef][PubMed]
    [Google Scholar]
  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 Dis205:1495–1500 [CrossRef][PubMed]
    [Google Scholar]
  3. Apoil P. A., Puissant B., Roubinet F., Abbal M., Massip P., Blancher A.. 2005; FOXP3 mRNA levels are decreased in peripheral blood CD4+ lymphocytes from HIV-positive patients. J Acquir Immune Defic Syndr39:381–385 [CrossRef][PubMed]
    [Google Scholar]
  4. Baecher-Allan C., Wolf E., Hafler D. A.. 2005; Functional analysis of highly defined, FACS-isolated populations of human regulatory CD4+ CD25+T cells. Clin Immunol115:10–18 [CrossRef][PubMed]
    [Google Scholar]
  5. Bandera A., Ferrario G., Saresella M., Marventano I., Soria A., Zanini F., Sabbatini F., Airoldi M., Marchetti G., other authors. 2010; CD4+T cell depletion, immune activation and increased production of regulatory T cells in the thymus of HIV-infected individuals. PLoS One5:e10788 [CrossRef][PubMed]
    [Google Scholar]
  6. Beilharz M. W., Sammels L. M., Paun A., Shaw K., van Eeden P., Watson M. W., Ashdown M. L.. 2004; Timed ablation of regulatory CD4+T cells can prevent murine AIDS progression. J Immunol172:4917–4925 [CrossRef][PubMed]
    [Google Scholar]
  7. Bi X., Suzuki Y., Gatanaga H., Oka S.. 2009; High frequency and proliferation of CD4+ FOXP3+ Treg in HIV-1-infected patients with low CD4 counts. Eur J Immunol39:301–309 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathog10:e1003993 [CrossRef][PubMed]
    [Google Scholar]
  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 Med171:315–320 [CrossRef][PubMed]
    [Google Scholar]
  10. Chase A. J., Yang H.-C., Zhang H., Blankson J. N., Siliciano R. F.. 2008; Preservation of FoxP3+ regulatory T cells in the peripheral blood of human immunodeficiency virus type 1-infected elite suppressors correlates with low CD4+T-cell activation. J Virol82:8307–8315 [CrossRef][PubMed]
    [Google Scholar]
  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 Immunol166:134–142 [CrossRef][PubMed]
    [Google Scholar]
  12. Chevalier M. F., Weiss L.. 2013; The split personality of regulatory T cells in HIV infection. Blood121:29–37 [CrossRef][PubMed]
    [Google Scholar]
  13. Chevalier M. F., Didier C., Petitjean G., Karmochkine M., Girard P.-M., Barré-Sinoussi F., Scott-Algara D., Weiss L.. 2015; Phenotype alterations in regulatory T-cell subsets in primary HIV infection and identification of Tr1-like cells as the main interleukin 10-producing CD4+T cells. J Infect Dis211:769–779 [CrossRef][PubMed]
    [Google Scholar]
  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-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med207:2439–2453 [CrossRef][PubMed]
    [Google Scholar]
  15. Daley-Bauer L. P., Wynn G. M., Mocarski E. S.. 2012; Cytomegalovirus impairs antiviral CD8+T cell immunity by recruiting inflammatory monocytes. Immunity37:122–133 [CrossRef][PubMed]
    [Google Scholar]
  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 Invest115:3623–3633 [CrossRef][PubMed]
    [Google Scholar]
  17. Delano M. J., Scumpia P. O., Weinstein J. S., Coco D., Nagaraj S., Kelly-Scumpia K. M., O'Malley K. A., Wynn J. L., Antonenko S., other authors. 2007; MyD88-dependent expansion of an immature GR-1+CD11b+ population induces T cell suppression and Th2 polarization in sepsis. J Exp Med204:1463–1474 [CrossRef][PubMed]
    [Google Scholar]
  18. Dietze K. K., Zelinskyy G., Gibbert K., Schimmer S., Francois S., Myers L., Sparwasser T., Hasenkrug K. J., Dittmer U.. 2011; Transient depletion of regulatory T cells in transgenic mice reactivates virus-specific CD8+T cells and reduces chronic retroviral set points. Proc Natl Acad Sci U S A108:2420–2425 [CrossRef][PubMed]
    [Google Scholar]
  19. Dittmer U., He H., Messer R. J., Schimmer S., Olbrich A. R. M., Ohlen C., Greenberg P. D., Stromnes I. M., Iwashiro M., other authors. 2004; Functional impairment of CD8+T cells by regulatory T cells during persistent retroviral infection. Immunity20:293–303 [CrossRef][PubMed]
    [Google Scholar]
  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 Res73:3591–3603 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathog5:e1000295 [CrossRef][PubMed]
    [Google Scholar]
  22. Fortin C., Huang X., Yang Y.. 2012; NK cell response to vaccinia virus is regulated by myeloid-derived suppressor cells. J Immunol189:1843–1849 [CrossRef][PubMed]
    [Google Scholar]
  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 Dermatol132:1239–1246 [CrossRef][PubMed]
    [Google Scholar]
  24. Gabrilovich D. I., Nagaraj S.. 2009; Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol9:162–174 [CrossRef][PubMed]
    [Google Scholar]
  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 Dis209:441–451 [CrossRef][PubMed]
    [Google Scholar]
  26. Gazzinelli R. T., Makino M., Chattopadhyay S. K., Snapper C. M., Sher A., Hügin A. W., Morse H. C. III. 1992; CD4+ subset regulation in viral infection. Preferential activation of Th2 cells during progression of retrovirus-induced immunodeficiency in mice. J Immunol148:182–188[PubMed]
    [Google Scholar]
  27. Giordanengo L., Guiñazú 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 Immunol32:1003–1011 [CrossRef][PubMed]
    [Google Scholar]
  28. Goñi O., Alcaide P., Fresno M.. 2002; Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1+)CD11b+ immature myeloid suppressor cells. Int Immunol14:1125–1134 [CrossRef][PubMed]
    [Google Scholar]
  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 Virol70:2569–2575[PubMed]
    [Google Scholar]
  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. Virology241:260–268 [CrossRef][PubMed]
    [Google Scholar]
  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 Virol75:3581–3589 [CrossRef][PubMed]
    [Google Scholar]
  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 Virol76:13106–13110 [CrossRef][PubMed]
    [Google Scholar]
  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 down-modulatory role in LP-BM5 retrovirus-induced murine immunodeficiency syndrome. J Virol82:2456–2469 [CrossRef][PubMed]
    [Google Scholar]
  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 Virol87:2058–2071 [CrossRef][PubMed]
    [Google Scholar]
  35. Hamann A.. 2012; Regulatory T cells stay on course. Immunity36:161–163 [CrossRef][PubMed]
    [Google Scholar]
  36. Huang B., Pan P.-Y., Li Q., Sato A. I., Levy D. E., Bromberg J., Divino C. M., Chen S.-H.. 2006; 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 Res66:1123–1131 [CrossRef][PubMed]
    [Google Scholar]
  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. Blood120:3030–3038 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathog9:e1003319 [CrossRef][PubMed]
    [Google Scholar]
  39. Jenabian M.-A., Patel M., Kema I., Vyboh K., Kanagaratham C., Radzioch D., Thébault 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 Immunol178:102–111 [CrossRef][PubMed]
    [Google Scholar]
  40. Jiang Q., Zhang L., Wang R., Jeffrey J., Washburn M. L., Brouwer D., Barbour S., Kovalev G. I., Unutmaz D., Su L.. 2008; FoxP3+CD4+ regulatory T cells play an important role in acute HIV-1 infection in humanized Rag2− / − (C− / −  mice in vivo. Blood112:2858–2868 [CrossRef][PubMed]
    [Google Scholar]
  41. Kinter A., McNally J., Riggin L., Jackson R., Roby G., Fauci A. S.. 2007; Suppression of HIV-specific T cell activity by lymph node CD25+ regulatory T cells from HIV-infected individuals. Proc Natl Acad Sci U S A104:3390–3395 [CrossRef][PubMed]
    [Google Scholar]
  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 Immunol140:1123–1131[PubMed]
    [Google Scholar]
  43. Klinman D. M., Morse H. C. III. 1989; Characteristics of B cell proliferation and activation in murine AIDS. J Immunol142:1144–1149[PubMed]
    [Google Scholar]
  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 Res15:2148–2157 [CrossRef][PubMed]
    [Google Scholar]
  45. Li W., Green W. R.. 2006; The role of CD4 T cells in the pathogenesis of murine AIDS. J Virol80:5777–5789 [CrossRef][PubMed]
    [Google Scholar]
  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?. Virology360:58–71 [CrossRef][PubMed]
    [Google Scholar]
  47. Li W., Green W. R.. 2011; Immunotherapy of murine retrovirus-induced acquired immunodeficiency by CD4 T regulatory cell depletion and PD-1 blockade. J Virol85:13342–13353 [CrossRef][PubMed]
    [Google Scholar]
  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 Invest114:1640–1649 [CrossRef][PubMed]
    [Google Scholar]
  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 set-point levels and of disease progression in HIV-1 infection. PLoS One7:e46143 [CrossRef][PubMed]
    [Google Scholar]
  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-1α-dependent glycolysis. Cancer Res74:727–737 [CrossRef][PubMed]
    [Google Scholar]
  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-α. Nat Med21:638–646 [CrossRef][PubMed]
    [Google Scholar]
  52. Maynard C. L., Harrington L. E., Janowski K. M., Oliver J. R., Zindl C. L., Rudensky A. Y., Weaver C. T.. 2007; Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3 −  precursor cells in the absence of interleukin 10.. Nat Immunol8:931–941 [CrossRef][PubMed]
    [Google Scholar]
  53. Mencacci A., Montagnoli C., Bacci A., Cenci E., Pitzurra L., Spreca A., Kopf M., Sharpe A. H., Romani L.. 2002; CD80+Gr-1+ myeloid cells inhibit development of antifungal Th1 immunity in mice with candidiasis. J Immunol169:3180–3190 [CrossRef][PubMed]
    [Google Scholar]
  54. Moir S., Fauci A. S.. 2008; Pathogenic mechanisms of B-lymphocyte dysfunction in HIV disease. J Allergy Clin Immunol122:12–19 quiz 2021 [CrossRef][PubMed]
    [Google Scholar]
  55. Moreno-Fernandez M. E., Presicce P., Chougnet C. A.. 2012; Homeostasis and function of regulatory T cells in HIV/SIV infection. J Virol86:10262–10269 [CrossRef][PubMed]
    [Google Scholar]
  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 Immunol143:844–850[PubMed]
    [Google Scholar]
  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 Med161:766–784 [CrossRef][PubMed]
    [Google Scholar]
  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 Med165:1737–1742 [CrossRef][PubMed]
    [Google Scholar]
  59. Niedbala W., Cai B., Liu H., Pitman N., Chang L., Liew F. Y.. 2007; Nitric oxide induces CD4+CD25+ Foxp3 regulatory T cells from CD4+CD25 T cells via p53, IL-2, and OX40.. Proc Natl Acad Sci U S A104:15478–15483 [CrossRef][PubMed]
    [Google Scholar]
  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-1α, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med211:781–790 [CrossRef][PubMed]
    [Google Scholar]
  61. O'Connor M. A., Green W. R.. 2013; The role of indoleamine 2,3-dioxygenase in LP-BPM5 murine retroviral disease progression. Virol J10:154 [CrossRef][PubMed]
    [Google Scholar]
  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 Virol88:2349–2353 [CrossRef][PubMed]
    [Google Scholar]
  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. Virology485:263–273[CrossRef]
    [Google Scholar]
  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 Res70:99–108 [CrossRef][PubMed]
    [Google Scholar]
  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 Immunol5:681[PubMed]
    [Google Scholar]
  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 Virol87:1477–1490 [CrossRef][PubMed]
    [Google Scholar]
  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 Med4:34ra62[PubMed]
    [Google Scholar]
  68. Redpath S. A., van der Werf N., Cervera A. M., MacDonald A. S., Gray D., Maizels R. M., Taylor M. D.. 2013; ICOS controls Foxp3+ regulatory T-cell expansion, maintenance and IL-10 production during helminth infection. Eur J Immunol43:705–715 [CrossRef][PubMed]
    [Google Scholar]
  69. Robertson S. J., Messer R. J., Carmody A. B., Hasenkrug K. J.. 2006; In vitro suppression of CD8+T cell function by Friend virus-induced regulatory T cells. J Immunol176:3342–3349 [CrossRef][PubMed]
    [Google Scholar]
  70. Schulze zur Wiesch J., Thomssen A., Hartjen P., Tóth I., Lehmann C., Meyer-Olson D., Colberg K., Frerk S., Babikir D., other authors. 2011; Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of FoxP3+T regulatory cells correlates with progressive disease. J Virol85:1287–1297 [CrossRef][PubMed]
    [Google Scholar]
  71. Serafini P., Mgebroff S., Noonan K., Borrello I.. 2008; Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res68:5439–5449 [CrossRef][PubMed]
    [Google Scholar]
  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 Virol71:3013–3022[PubMed]
    [Google Scholar]
  73. Simonetta F., Lecuroux C., Girault I., Goujard C., Sinet M., Lambotte O., Venet A., Bourgeois C.. 2012; Early and long-lasting alteration of effector CD45RA− Foxp3high regulatory T-cell homeostasis during HIV infection. J Infect Dis205:1510–1519 [CrossRef][PubMed]
    [Google Scholar]
  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 One5:e11762 [CrossRef][PubMed]
    [Google Scholar]
  75. Sui Y., Hogg A., Wang Y., Frey B., Yu H., Xia Z., Venzon D., McKinnon K., Smedley J., other authors. 2014; Vaccine-induced myeloid cell population dampens protective immunity to SIV. J Clin Invest124:2538–2549 [CrossRef][PubMed]
    [Google Scholar]
  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 Immunol172:4410–4417 [CrossRef][PubMed]
    [Google Scholar]
  77. Taieb J., Chaput N., Schartz N., Roux S., Novault S., Ménard C., Ghiringhelli F., Terme M., Carpentier A. F., other authors. 2006; Chemoimmunotherapy of tumors: cyclophosphamide synergizes with exosome based vaccines. J Immunol176:2722–2729 [CrossRef][PubMed]
    [Google Scholar]
  78. Talmadge J. E., Gabrilovich D. I.. 2013; History of myeloid-derived suppressor cells. Nat Rev Cancer13:739–752 [CrossRef][PubMed]
    [Google Scholar]
  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 Med11:148 [CrossRef][PubMed]
    [Google Scholar]
  80. Terrazas L. I., Walsh K. L., Piskorska D., McGuire E., Harn D. A. Jr. 2001; The schistosome oligosaccharide lacto-N-neotetraose expands Gr1+ cells that secrete anti-inflammatory cytokines and inhibit proliferation of naive CD4+ cells: a potential mechanism for immune polarization in helminth infections. J Immunol167:5294–5303 [CrossRef][PubMed]
    [Google Scholar]
  81. Tseng C.-W., Hung C.-F., Alvarez R. D., Trimble C., Huh W. K., Kim D., Chuang C.-M., Lin C.-T., Tsai Y.-C., other authors. 2008; Pretreatment with cisplatin enhances E7-specific CD8+T-cell-mediated antitumor immunity induced by DNA vaccination. Clin Cancer Res14:3185–3192 [CrossRef][PubMed]
    [Google Scholar]
  82. Uehara S., Hitoshi Y., Numata F., Makino M., Howard M., Mizuochi T., Takatsu K.. 1994; An IFN-γ-dependent pathway plays a critical role in the pathogenesis of murine immunodeficiency syndrome induced by LP-BM5 murine leukemia virus. Int Immunol6:1937–1947 [CrossRef][PubMed]
    [Google Scholar]
  83. Voisin M.-B., Buzoni-Gatel D., Bout D., Velge-Roussel F.. 2004; Both expansion of regulatory GR1+ CD11b+ myeloid cells and anergy of T lymphocytes participate in hyporesponsiveness of the lung-associated immune system during acute toxoplasmosis. Infect Immun72:5487–5492 [CrossRef][PubMed]
    [Google Scholar]
  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. AIDS26:F31–F37 [CrossRef][PubMed]
    [Google Scholar]
  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 Cancer1:10 [CrossRef][PubMed]
    [Google Scholar]
  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 Immunol32:2680–2686 [CrossRef][PubMed]
    [Google Scholar]
  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 Sci66:2603–2622 [CrossRef][PubMed]
    [Google Scholar]
  88. Yang R., Cai Z., Zhang Y., Yutzy W. H. IV. Roby K F & Roden R B S 2006; CD80 in immune suppression by mouse ovarian carcinoma-associated Gr-1+CD11b+ myeloid cells.. Cancer Res66:6807–6815 [CrossRef][PubMed]
    [Google Scholar]
  89. Zelinskyy G., Kraft A. R. M., Schimmer S., Arndt T., Dittmer U.. 2006; Kinetics of CD8+ effector T cell responses and induced CD4+ regulatory T cell responses during Friend retrovirus infection. Eur J Immunol36:2658–2670 [CrossRef][PubMed]
    [Google Scholar]
  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. Blood114:3199–3207 [CrossRef][PubMed]
    [Google Scholar]
  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 Immunol10:1000–1007 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000260
Loading
/content/journal/jgv/10.1099/jgv.0.000260
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error