MyD88-dependent expansion of an immature GR-1 +CD11b+ population induces T cell suppression and Th2 polarization in sepsis

Journal of Experimental Medicine

Volumn 204, Issue 6, 2007, Pages 1463-1474

  Delano, Matthew J ^a   Scumpia, Philip O ^a   Weinstein, Jason S ^a   Coco, Dominique ^a   Nagaraj, Srinivas ^b   Kelly Scumpia, Kindra M ^a   O'Malley, Kerri A ^a   Wynn, James L ^a   Antonenko, Svetlana ^c   Al Quran, Samer Z ^a   Swan, Ryan ^d   Chung, Chun Shiang ^d   Atkinson, Mark A ^a   Ramphal, Reuben ^a   Gabrilovich, Dmitry I ^b   Reeves, Wesley H ^a   Ayala, Alfred ^d   Phillips, Joseph ^c   LaFace, Drake ^c   Heyworth, Paul G ^c   Clare Salzler, Michael ^a   Moldawer, Lyle L ^a   more..

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

^d BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; BETA INTERFERON; BETA INTERFERON RECEPTOR; CD11B ANTIGEN; CHEMOKINE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANTIBODY PRODUCTION; ANTIGEN SPECIFICITY; ARTICLE; BONE MARROW; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL; CELL COUNT; CELL HETEROGENEITY; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GR 1 CELL; LYMPH NODE; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; SEPSIS; SPLEEN; T LYMPHOCYTE; TH2 CELL;

ANIMALS; ANTIGENS, CD11B; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; CYTOKINES; FLOW CYTOMETRY; IMMUNE TOLERANCE; LYMPHOID TISSUE; MICE; MICE, INBRED C57BL; MYELOID DIFFERENTIATION FACTOR 88; MYELOID PROGENITOR CELLS; RECEPTORS, CHEMOKINE; SEPSIS; SIGNAL TRANSDUCTION; TH2 CELLS;

EID: 34250359119     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20062602     Document Type: Article

References (33)

1. Hotchkiss, R.S., and I.E. Karl. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348:138-150.
2. Riedemann, N.C., R.F. Guo, and P.A. Ward. 2003. The enigma of sepsis. J. Clin. Invest. 112:460-467.
3. Hotchkiss, R.S., K.W. Tinsley, P.E. Swanson, R.E. Schmieg Jr., J.J. Hui, K.C. Chang, D.F. Osborne, B.D. Freeman, J.P. Cobb, T.G. Buchman, and I.E. Karl. 2001. Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans. J. Immunol. 166:6952-6963.
4. Oberholzer, C., A. Oberholzer, F.R. Bahjat, R.M. Minter, C.L. Tannahill, A. Abouhamze, D. LaFace, B. Hutchins, M.J. Clare-Salzler, and L.L. Moldawer. 2001. Targeted adenovirus-induced expression of IL-10 decreases thymic apoptosis and improves survival in murine sepsis. Proc. Natl. Acad. Sci. USA. 98:11503-11508.
5. Murphey, E.D., C.Y. Lin, R.W. McGuire, T. Toliver-Kinsky, D.N. Herndon, and E.R. Sherwood. 2004. Diminished bacterial clearance is associated with decreased IL-12 and interferon-gamma production but a sustained proinflammatory response in a murine model of postseptic immunosuppression. Shock. 21:415-425.
6. McDunn, J.E., I.R. Turnbull, A.D. Polpitiya, A. Tong, S.K. MacMillan, D.F. Osborne, R.S. Hotchkiss, M. Colonna, and J.P. Cobb. 2006. Splenic CD4+ T cells have a distinct transcriptional response six hours after the onset of sepsis. J. Am. Coll. Surg. 203:365-375.
7. Ferguson, N.R., H.F. Galley, and N.R. Webster. 1999. T helper cell subset ratios in patients with severe sepsis. Intensive Care Med. 25:106-109.
8. Bronte, V., E. Apolloni, A. Cabrelle, R. Ronca, P. Serafini, P. Zamboni, N.P. Restifo, and P. Zanovello. 2000. Identification of a CD11b(+)/ Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood. 96:3838-3846.
9. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5:641-654.
10. Ezernitchi, A.V., I. Vaknin, L. Cohen-Daniel, O. Levy, E. Manaster, A. Halabi, E. Pikarsky, L. Shapira, and M. Baniyash. 2006. TCR zeta down-regulation under chronic inflammation is mediated by myeloid suppressor cells differentially distributed between various lymphatic organs. J. Immunol. 177:4763-4772.
11. Gabrilovich, D.I., M.P. Velders, E.M. Sotomayor, and W.M. Kast. 2001. Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J. Immunol. 166:5398-5406.
12. Kusmartsev, S., F. Cheng, B. Yu, Y. Nefedova, E. Sotomayor, R. Lush, and D. Gabrilovich. 2003. All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination. Cancer Res. 63:4441-4449.
13. Kusmartsev, S., and D.I. Gabrilovich. 2003. Inhibition of myeloid cell differentiation in cancer: the role of reactive oxygen species. J. Leukoc. Biol. 74:186-196.
14. Kusmartsev, S., S. Nagaraj, and D.I. Gabrilovich. 2005. Tumor-associated CD8+ T cell tolerance induced by bone marrow-derived immature myeloid cells. J. Immunol. 175:4583-4592.
15. Kusmartsev, S., Y. Nefedova, D. Yoder, and D.I. Gabrilovich. 2004. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172:989-999.
16. Jordan, M.B., D.M. Mills, J. Kappler, P. Marrack, and J.C. Cambier. 2004. Promotion of B cell immune responses via an alum-induced myeloid cell population. Science. 304:1808-1810.
17. Ling, V., D. Luxenberg, J. Wang, E. Nickbarg, P.J. Leenen, S. Neben, and M. Kobayashi. 1997. Structural identification of the hematopoietic progenitor antigen ER-MP12 as the vascular endothelial adhesion molecule PECAM-1 (CD31). Eur. J. Immunol. 27:509-514.
18. Biermann, H., B. Pietz, R. Dreier, K.W. Schmid, C. Sorg, and C. Sunderkotter. 1999. Murine leukocytes with ring-shaped nuclei include granulocytes, monocytes, and their precursors. J. Leukoc. Biol. 65:217-231.
19. Sherr, D.H., and M.E. Dorf. 1984. Characterization of anti-idiotypic suppressor T cells (Tsid) induced after antigen priming. J. Immunol. 133:1142-1150.
20. Monneret, G., A.L. Debard, F. Venet, J. Bohe, O. Hequet, J. Bienvenu, and A. Lepape. 2003. Marked elevation of human circulating CD4+CD25+ regulatory T cells in sepsis-induced immunoparalysis. Crit. Care Med. 31:2068-2071.
21. Venet, F., A. Pachot, A.L. Debard, J. Bohe, J. Bienvenu, A. Lepape, and G. Monneret. 2004. Increased percentage of CD4+CD25+ regulatory T cells during septic shock is due to the decrease of CD4+CD25? lymphocytes. Crit. Care Med. 32:2329-2331.
22. Scumpia, P.O., M.J. Delano, K.M. Kelly, K.A. O'Malley, P.A. Efron, P.F. McAuliffe, T. Brusko, R. Ungaro, T. Barker, J.L. Wynn, et al. 2006. Increased natural CD4+CD25+ regulatory T cells and their suppressor activity do not contribute to mortality in murine polymicrobial sepsis. J. Immunol. 177:7943-7949.
23. Wisnoski, N., C.-S. Chung, Y. Chen, X. Huang, and A. Ayala. 2007. The contribution of CD4+CD25+ T regulatory cells to immune suppression in sepsis. Shock. 27:251-257.
24. Makarenkova, V.P., V. Bansal, B.M. Matta, L.A. Perez, and J.B. Ochoa. 2006. CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J. Immunol. 176:2085-2094.
25. Hotchkiss, R.S., P.E. Swanson, C.M. Knudson, K.C. Chang, J.P. Cobb, D.F. Osborne, K.M. Zollner, T.G. Buchman, S.J. Korsmeyer, and I.E. Karl. 1999. Overexpression of Bcl-2 in transgenic mice decreases apoptosis and improves survival in sepsis. J. Immunol. 162:4148-4156.
26. Hotchkiss, R.S., K.W. Tinsley, P.E. Swanson, K.C. Chang, J.P. Cobb, T.G. Buchman, S.J. Korsmeyer, and I.E. Karl. 1999. Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc. Natl. Acad. Sci. USA. 96:14541-14546.
27. Efron, P.A., A. Martins, D. Minnich, K. Tinsley, R. Ungaro, F.R. Bahjat, R. Hotchkiss, M. Clare-Salzler, and L.L. Moldawer. 2004. Characterization of the systemic loss of dendritic cells in murine lymph nodes during polymicrobial sepsis. J. Immunol. 173:3035-3043.
28. Mirza, N., M. Fishman, I. Fricke, M. Dunn, A.M. Neuger, T.J. Frost, R.M. Lush, S. Antonia, and D.I. Gabrilovich. 2006. All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res. 66:9299-9307.
29. Gabrilovich, D.I., V. Bronte, S.H. Chen, M.P. Colombo, A. Ochoa, S. Ostrand-Rosenberg, and H. Schreiber. 2007. The terminology issue for myeloid-derived suppressor cells. Cancer Res. 67:425.
30. Danna, E.A., P. Sinha, M. Gilbert, V.K. Clements, B.A. Pulaski, and S. Ostrand-Rosenberg. 2004. Surgical removal of primary tumor reverses tumor-induced immunosuppression despite the presence of metastatic disease. Cancer Res. 64:2205-2211.
31. McMasters, K.M., J.C. Peyton, D.J. Hadjiminas, and W.G. Cheadle. 1994. Endotoxin and tumour necrosis factor do not cause mortality from caecal ligation and puncture. Cytokine. 6:530-536.
32. Scumpia, P.O., P.F. McAuliffe, K.A. O'Malley, R. Ungaro, T. Uchida, T. Matsumoto, D.G. Remick, M.J. Clare-Salzler, L.L. Moldawer, and P.A. Efron. 2005. CD11c+ dendritic cells are required for survival in murine polymicrobial sepsis. J. Immunol. 175:3282-3286.
33. Hurov, J.B., T.S. Stappenbeck, C.M. Zmasek, L.S. White, S.H. Ranganath, J.H. Russell, A.C. Chan, K.M. Murphy, and H. Piwnica-Worms. 2001. Immune system dysfunction and autoimmune disease in mice lacking Emk (Par-1) protein kinase. Mol. Cell. Biol. 21:3206-3219.