Subpopulations of M-MDSCs from mice infected by an immunodeficiency-causing retrovirus and their differential suppression of T- vs B-cell responses

Virology

Volumn 485, Issue , 2015, Pages 263-273

  O'Connor, Megan A ^a   Fu, Whitney W ^a   Green, Kathy A ^a   Green, William R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

LP BM5; Myeloid derived suppressor cells; Retrovirus

Indexed keywords

CD11B ANTIGEN; CELL PROTEIN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR CXCR4; F4 80 PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LYMPHOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN 6C; NITRIC OXIDE; UNCLASSIFIED DRUG; CHEMOKINE RECEPTOR; DIFFERENTIATION ANTIGEN; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; MONOCYTE-MACROPHAGE DIFFERENTIATION ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CELL DENSITY; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CELL SELECTION; CONTROLLED STUDY; IMMUNE DEFICIENCY; MONOCYTIC MYELOID DERIVED SUPPRESSOR CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RETROVIRUS INFECTION; SUPPRESSOR CELL; T LYMPHOCYTE SUBPOPULATION; ANIMAL; BONE MARROW CELL; GENE EXPRESSION; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOPHENOTYPING; METABOLISM; RETROVIRIDAE; T LYMPHOCYTE; VIROLOGY;

MURINAE; MUS;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, DIFFERENTIATION; ANTIGENS, LY; B-LYMPHOCYTES; GENE EXPRESSION; IMMUNOMODULATION; IMMUNOPHENOTYPING; MICE; MYELOID CELLS; RECEPTORS, CHEMOKINE; RETROVIRIDAE; RETROVIRIDAE INFECTIONS; T-LYMPHOCYTES;

EID: 84940056780     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.07.020     Document Type: Article

References (67)

1. Auffray C., Fogg D., Garfa M., Elain G., Join-Lambert O., Kayal S., Sarnacki S., Cumano A., Lauvau G., Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007, 317:666-670.
2. Aziz DC., Hanna Z., Jolicoeur P. Severe immunodeficiency disease induced by a defective murine leukaemia virus. Nature 1989, 338:505-508.
3. Bowers NL., Helton ES., Huijbregts RPH., Goepfert PA., Heath SL., Hel Z. Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog. 2014, 10:e1003993.
4. Brandau S., Trellakis S., Bruderek K., Schmaltz D., Steller G., Elian M., Suttmann H., Schenck M., Welling J., Zabel P., Lang S. Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J. Leukoc. Biol. 2011, 89:311-317.
5. Bronte V., Zanovello P. Regulation of immune responses by l-arginine metabolism. Nat. Rev. Immunol. 2005, 5:641-654.
6. Cerny A., Hügin AW., Hardy RR., Hayakawa K., Zinkernagel RM., Makino M., Morse HC. B cells are required for induction of T cell abnormalities in a murine retrovirus-induced immunodeficiency syndrome. J. Exp. Med. 1990, 171:315-320.
7. Chen M-F., Kuan F-C., Yen T-C., Lu M-S., Lin P-Y., Chung Y-H., Chen W-C., Lee K-D. IL-6-stimulated CD11b+ CD14+ HLA-DR- myeloid-derived suppressor cells, are associated with progression and poor prognosis in squamous cell carcinoma of the esophagus. Oncotarget 2014, 5:8716-8728.
8. Condamine T., Gabrilovich DI. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 2011, 32:19-25.
9. Connelly L., Jacobs AT., Palacios-Callender M., Moncada S., Hobbs AJ. Macrophage endothelial nitric-oxide synthase autoregulates cellular activation and pro-inflammatory protein expression. J. Biol. Chem. 2003, 278:26480-26487.
10. Crook KR., Jin M., Weeks MF., Rampersad RR., Baldi RM., Glekas AS., Shen Y., Esserman DA., Little P., Schwartz TA., Liu P. Myeloid-derived suppressor cells regulate T cell and B cell responses during autoimmune disease. J. Leukoc. Biol. 2015, 97:573-582.
11. Daley-Bauer LP., Wynn GM., Mocarski ES. Cytomegalovirus impairs antiviral CD8+ T cell immunity by recruiting inflammatory monocytes. Immunity 2012, 37:122-133.
12. Gabrilovich DI., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
13. Gallina G., Dolcetti L., Serafini P., De Santo C., Marigo I., Colombo MP., Basso G., Brombacher F., Borrello I., Zanovello P., Bicciato S., Bronte V. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 2006, 116:2777-2790.
14. Garg A., Spector SA. HIV type 1 gp120-induced expansion of myeloid derived suppressor cells is dependent on interleukin 6 and suppresses immunity. J. Infect. Dis. 2014, 209:441-451.
15. Gazzinelli RT., Makino M., Chattopadhyay SK., Snapper CM., Sher A., Hügin AW., Morse HC. CD4+ subset regulation in viral infection. Preferential activation of Th2 cells during progression of retrovirus-induced immunodeficiency in mice. J. Immunol. (Baltimore, Md.: 1950) 1992, 148:182-188.
16. Goh C., Narayanan S., Hahn YS. Myeloid-derived suppressor cells: the dark knight or the joker in viral infections?. Immunol. Rev. 2013, 255:210-221.
17. Gordon S., Hamann J., Lin H-H., Stacey M. F4/80 and the related adhesion-GPCRs. Eur. J. Immunol. 2011, 41:2472-2476.
18. Green KA., Crassi KM., Laman JD., Schoneveld A., Strawbridge RR., Foy TM., Noelle RJ., Green WR. Antibody to the ligand for CD40 (gp39) inhibits murine AIDS-associated splenomegaly, hypergammaglobulinemia, and immunodeficiency in disease-susceptible C57BL/6 mice. J. Virol. 1996, 70:2569-2575.
19. Green KA., Noelle RJ., Green WR. Evidence for a continued requirement for CD40/CD40 ligand (CD154) interactions in the progression of LP-BM5 retrovirus-induced murine AIDS. Virology 1998, 241:260-268.
20. Green KA., Noelle RJ., Durell BG., Green WR. Characterization of the CD154-positive and CD40-positive cellular subsets required for pathogenesis in retrovirus-induced murine immunodeficiency. J. Virol. 2001, 75:3581-3589.
21. Green KA., Cook WJ., Sharpe AH., Green WR. The CD154/CD40 interaction required for retrovirus-induced murine immunodeficiency syndrome is not mediated by upregulation of the CD80/CD86 costimulatory molecules. J. Virol. 2002, 76:13106-13110.
22. Green KA., Ahonen CL., Cook WJ., Green WR. CD40-associated TRAF 6 signaling is required for disease induction in a retrovirus-induced murine immunodeficiency. J. Virol. 2004, 78:6055-6060.
23. Green KA., Cook WJ., Green WR. 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. 2013, 87:2058-2071.
24. Griffith JW., Sokol CL., Luster AD. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 2014, 32:659-702.
25. Hart KM., Usherwood EJ., Berwin BL. CX3CR1 delineates temporally and functionally distinct subsets of myeloid-derived suppressor cells in a mouse model of ovarian cancer. Immunol. Cell Biol. 2014, 92:499-508.
26. Highfill SL., Cui Y., Giles AJ., Smith JP., Zhang H., Morse E., Kaplan RN., Mackall CL. Disruption of CXCR2-mediated MDSC tumor trafficking enhances anti-PD1 efficacy. Sci. Transl. Med. 2014, 6. 237ra67.
27. Huang B., Pan P-Y., Li Q., Sato AI., Levy DE., Bromberg J., Divino CM., Chen S-H. 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. 2006, 66:1123-1131.
28. Huang B., Lei Z., Zhao J., Gong W., Liu J., Chen Z., Liu Y., Li D., Yuan Y., Zhang G-M., Feng Z-H. CCL2/CCR2 pathway mediates recruitment of myeloid suppressor cells to cancers. Cancer Lett. 2007, 252:86-92.
29. Jayaraman P., Parikh F., Lopez-Rivera E., Hailemichael Y., Clark A., Ma G., Cannan D., Ramacher M., Kato M., Overwijk WW., Chen S-H., Umansky VY., Sikora AG. Tumor-expressed inducible nitric oxide synthase controls induction of functional myeloid-derived suppressor cells through modulation of vascular endothelial growth factor release. J. Immunol. (Baltimore, Md.: 1950) 2012, 188:5365-5376.
30. Jolicoeur P. Murine acquired immunodeficiency syndrome (MAIDS): an animal model to study the AIDS pathogenesis. FASEB J. 1991, 5:2398-2405. Off Publ Fed Am Soc Exp Biol.
31. Klinken SP., Fredrickson TN., Hartley JW., Yetter RA., Morse HC. Evolution of B cell lineage lymphomas in mice with a retrovirus-induced immunodeficiency syndrome, MAIDS. J. Immunol. 1988, 140:1123-1131.
32. Klinman DM., Morse HC. Characteristics of B cell proliferation and activation in murine AIDS. J. Immunol. 1989, 142:1144-1149.
33. Lee PY., Wang J-X., Parisini E., Dascher CC., Nigrovic PA. Ly6 family proteins in neutrophil biology. J. Leukoc. Biol. 2013, 94:585-594.
34. Lesokhin AM., Hohl TM., Kitano S., Cortez C., Hirschhorn-Cymerman D., Avogadri F., Rizzuto GA., Lazarus JJ., Pamer EG., Houghton AN., Merghoub T., Wolchok JD. Monocytic CCR2(+) myeloid-derived suppressor cells promote immune escape by limiting activated CD8 T-cell infiltration into the tumor microenvironment. Cancer Res. 2012, 72:876-886.
35. Li W., Green WR. The role of CD4 T Cells in the pathogenesis of murine AIDS. J. Virol. 2006, 80:5777-5789.
36. Li W., Green WR. Murine AIDS requires CD154/CD40L expression by the CD4 T cells that mediate retrovirus-induced disease: is CD4 T cell receptor ligation needed?. Virology 2007, 360.
37. Lin H-H., Faunce DE., Stacey M., Terajewicz A., Nakamura T., Zhang-Hoover J., Kerley M., Mucenski ML., Gordon S., Stein-Streilein J. The macrophage F4/80 receptor is required for the induction of antigen-specific efferent regulatory T cells in peripheral tolerance. J. Exp. Med. 2005, 201:1615-1625.
38. Lin H-H., Stacey M., Stein-Streilein J., Gordon S. F4/80: the macrophage-specific adhesion-GPCR and its role in immunoregulation. Adv. Exp. Med. Biol. 2010, 706:149-156.
39. Luther SA., Cyster JG. Chemokines as regulators of T cell differentiation. Nat. Immunol. 2001, 2:102-107.
40. Marigo I., Dolcetti L., Serafini P., Zanovello P., Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev. 2008, 222:162-179.
41. Morse HC., Yetter RA., Via CS., Hardy RR., Cerny A., Hayakawa K., Hugin AW., Miller MW., Holmes KL., Shearer GM. Functional and phenotypic alterations in T cell subsets during the course of MAIDS, a murine retrovirus-induced immunodeficiency syndrome. J. Immunol. 1989, 143:844-850.
42. Mosier DE., Yetter RA., Morse HC. Retroviral induction of acute lymphoproliferative disease and profound immunosuppression in adult C57BL/6 mice. J. Exp. Med. 1985, 161:766-784.
43. Movahedi K., Guilliams M., Van den Bossche J., Van den Bergh R., Gysemans C., Beschin A., De Baetselier P., Van Ginderachter JA. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008, 111:4233-4244.
44. Obermajer N., Muthuswamy R., Odunsi K., Edwards RP., Kalinski P. PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res. 2011, 71:7463-7470.
45. Ostrand-Rosenberg S., Sinha P., Beury DW., Clements VK. Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin. Cancer Biol. 2012, 22:275-281.
46. O'Connor MA., Green WR. The role of indoleamine 2,3-dioxygenase in LP-BM5 murine retroviral disease progression. Virol. J. 2013, 10:154.
47. O'Connor MA., Green WR. Use of IRF-3 and/or IRF-7 knockout mice to study viral pathogenesis: lessons from a murine retrovirus-induced AIDS model. J. Virol. 2013, 88:2349-2353.
48. Qin A., Cai W., Pan T., Wu K., Yang Q., Wang N., Liu Y., Yan D., Hu F., Guo P., Chen X., Chen L., Zhang H., Tang X., Zhou J. Expansion of monocytic myeloid-derived suppressor cells dampens T cell function in HIV-1-seropositive individuals. J. Virol. 2013, 87:1477-1490.
49. Rath M., Müller I., Kropf P., Closs EI., Munder M. Metabolism via arginase or nitric oxide synthase: two competing arginine pathways in macrophages. Front. Immunol. 2014, 5:532.
50. Rodriguez PC., Zea AH., DeSalvo J., Culotta KS., Zabaleta J., Quiceno DG., Ochoa JB., Ochoa AC. l-Arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J. Immunol. (Baltimore, Md.: 1950) 2003, 171:1232-1239.
51. Sawanobori Y., Ueha S., Kurachi M., Shimaoka T., Talmadge JE., Abe J., Shono Y., Kitabatake M., Kakimi K., Mukaida N., Matsushima K. Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood 2008, 111:5457-5466.
52. Schaller E., Macfarlane AJ., Rupec RA., Gordon S., McKnight AJ., Pfeffer K. Inactivation of the F4/80 glycoprotein in the mouse germ line. Mol. Cell. Biol. 2002, 22:8035-8043.
53. Schlecker E., Stojanovic A., Eisen C., Quack C., Falk CS., Umansky V., Cerwenka A. Tumor-infiltrating monocytic myeloid-derived suppressor cells mediate CCR5-dependent recruitment of regulatory T cells favoring tumor growth. J. Immunol. (Baltimore, Md.: 1950) 2012, 189:5602-5611.
54. Shi C., Pamer EG. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 2011, 11:762-774.
55. Sica A., Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 2007, 117:1155-1166.
56. Simard C., Klein SJ., Mak T., Jolicoeur P. Studies of the susceptibility of nude, CD4 knockout, and SCID mutant mice to the disease induced by the murine AIDS defective virus. J. Virol. 1997, 71:3013-3022.
57. Solito S., Marigo I., Pinton L., Damuzzo V., Mandruzzato S., Bronte V. Myeloid-derived suppressor cell heterogeneity in human cancers. Ann. N.Y. Acad. Sci. 2014, 1319:47-65.
58. Sui Y., Hogg A., Wang Y., Frey B., Yu H., Xia Z., Venzon D., McKinnon K., Smedley J., Gathuka M., Klinman D., Keele BF., Langermann S., Liu L., Franchini G., Berzofsky JA. Vaccine-induced myeloid cell population dampens protective immunity to SIV. J. Clin. Invest. 2014, 124:2538-2549.
59. Tacke RS., Lee H-C., Goh C., Courtney J., Polyak SJ., Rosen HR., Hahn YS. Myeloid suppressor cells induced by hepatitis C virus suppress T-cell responses through the production of reactive oxygen species. Hepatology 2012, 55:343-353.
60. Talmadge JE., Gabrilovich DI. History of myeloid-derived suppressor cells. Nat. Rev. Cancer 2013, 13:739-752.
61. Umemura N., Saio M., Suwa T., Kitoh Y., Bai J., Nonaka K., Ouyang G-F., Okada M., Balazs M., Adany R., Shibata T., Takami T. Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. J. Leukoc. Biol. 2008, 83:1136-1144.
62. Vollbrecht T., Stirner R., Tufman A., Roider J., Huber RM., Bogner JR., Lechner A., Bourquin C., Draenert R. Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS 2012, 26:F31-37.
63. Wang W., Jiao Z., Duan T., Liu M., Zhu B., Zhang Y., Xu Q., Wang R., Xiong Y., Xu H., Lu L. Functional characterization of myeloid-derived suppressor cell subpopulations during the development of experimental arthritis. Eur. J. Immunol. 2015, 45:464-473.
64. Yamanaka N., O'Connor MB. Nitric oxide directly regulates gene expression during Drosophila development: need some gas to drive into metamorphosis?. Genes Dev. 2011, 25:1459-1463.
65. Youn J-I., Nagaraj S., Collazo M., Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. (Baltimore, Md.: 1950) 2008, 181:5791-5802.
66. Zhao W., Xu Y., Xu J., Wu D., Zhao B., Yin Z., Wang X. Subsets of myeloid-derived suppressor cells in hepatocellular carcinoma express chemokines and chemokine receptors differentially. Int. Immunopharmacol. 2015, 26:314-321.
67. Zhu K., Zhang N., Guo N., Yang J., Wang J., Yang C., Yang C., Zhu L., Xu C., Deng Q., Zhu R., Wang H., Chen X., Shi Y., Li Y., Leng Q. SSC(high)CD11b(high)Ly-6C(high)Ly-6G(low) myeloid cells curtail CD4 T cell response by inducible nitric oxide synthase in murine hepatitis. Int. J. Biochem. Cell Biol. 2014, 54:89-97.