Neutrophil IL-10 suppresses peritoneal inflammatory monocytes during polymicrobial sepsis

Journal of Leukocyte Biology

Volumn 89, Issue 3, 2011, Pages 423-432

  Ocuin, Lee M ^a   Bamboat, Zubin M ^a   Balachandran, Vinod P ^a   Cavnar, Michael J ^a   Obaid, Hebroon ^a   Plitas, George ^a   DeMatteo, Ronald P ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Bacteria; Cecal ligation and puncture; Cytokines; Innate immunity

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL ISOLATION; CELL SELECTION; CELL TRANSFER; CONTROLLED STUDY; FLOW CYTOMETRY; IN VITRO STUDY; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PERITONEUM CELL; PHAGOCYTOSIS; POLYMICROBIAL SEPSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; SURVIVAL;

ANIMALS; INFLAMMATION; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MONOCYTES; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE II; PERITONITIS; SEPSIS; SURVIVAL ANALYSIS; TUMOR NECROSIS FACTOR-ALPHA;

MURINAE; MUS;

EID: 79952205667     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0810479     Document Type: Article

References (49)

1. Riedemann, N. C., Guo, R. F., Ward, P. A. (2003) The enigma of sepsis. J. Clin. Invest. 112, 460-467. (Pubitemid 38056327)
2. Hotchkiss, R. S., Karl, I. E. (2003) The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348, 138-150. (Pubitemid 36056721)
3. Poli-de-Figueiredo, L. F., Garrido, A. G., Nakagawa, N., Sannomiya, P. (2008) Experimental models of sepsis and their clinical relevance. Shock 30 (Suppl. 1), 53-59.
4. Zhang, X., Majlessi, L., Deriaud, E., Leclerc, C., Lo-Man, R. (2009) Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31, 761-771.
5. Smith, J. A. (1994) Neutrophils, host defense, and inflammation: a double-edged sword. J. Leukoc. Biol. 56, 672-686.
6. Perl, M., Chung, C. S., Perl, U., Biffl, W. L., Cioffi, W. G., Ayala, A. (2007) Beneficial versus detrimental effects of neutrophils are determined by the nature of the insult. J. Am. Coll. Surg. 204, 840-852, discussion 852-853.
7. Hoesel, L. M., Neff, T. A., Neff, S. B., Younger, J. G., Olle, E. W., Gao, H., Pianko, M. J., Bernacki, K. D., Sarma, J. V., Ward, P. A. (2005) Harmful and protective roles of neutrophils in sepsis. Shock 24, 40-47. (Pubitemid 40946593)
8. Brown, K. A., Brain, S. D., Pearson, J. D., Edgeworth, J. D., Lewis, S. M., Treacher, D. F. (2006) Neutrophils in development of multiple organ failure in sepsis. Lancet 368, 157-169.
9. Leendertse, M., Willems, R. J., Giebelen, I. A., Roelofs, J. J., Bonten, M. J., van der Poll, T. (2009) Neutrophils are essential for rapid clearance of Enterococcus faecium in mice. Infect. Immun. 77, 485-491.
10. Marks, M., Burns, T., Abadi, M., Seyoum, B., Thornton, J., Tuomanen, E., Pirofski, L. A. (2007) Influence of neutropenia on the course of serotype 8 pneumococcal pneumonia in mice. Infect. Immun. 75, 1586-1597. (Pubitemid 46559422)
11. López, S., Marco, A. J., Prats, N., Czuprynski, C. J. (2000) Critical role of neutrophils in eliminating Listeria monocytogenes from the central nervous system during experimental murine listeriosis. Infect. Immun. 68, 4789-4791. (Pubitemid 30497758)
12. Verdrengh, M., Tarkowski, A. (1997) Role of neutrophils in experimental septicemia and septic arthritis induced by Staphylococcus aureus. Infect. Immun. 65, 2517-2521. (Pubitemid 27264071)
13. Gregory, S. H., Sagnimeni, A. J., Wing, E. J. (1996) Bacteria in the bloodstream are trapped in the liver and killed by immigrating neutrophils. J. Immunol. 157, 2514-2520. (Pubitemid 126450464)
14. Plitas, G., Burt, B. M., Nguyen, H. M., Bamboat, Z. M., DeMatteo, R. P. (2008) Toll-like receptor 9 inhibition reduces mortality in polymicrobial sepsis. J. Exp. Med. 205, 1277-1283. (Pubitemid 351831485)
15. Ayala, A., Chung, C. S., Lomas, J. L., Song, G. Y., Doughty, L. A., Gregory, S. H., Cioffi, W. G., LeBlanc, B. W., Reichner, J., Simms, H. H., Grutkoski, P. S. (2002) Shock-induced neutrophil mediated priming for acute lung injury in mice: divergent effects of TLR-4 and TLR-4/FasL deficiency. Am. J. Pathol. 161, 2283-2294. (Pubitemid 35434872)
16. Fleming, T. J., Fleming, M. L., Malek, T. R. (1993) Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J. Immunol. 151, 2399-2408. (Pubitemid 23264492)
17. Conlan, J. W., North, R. J. (1994) Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J. Exp. Med. 179, 259-268.
18. Daley, J. M., Thomay, A. A., Connolly, M. D., Reichner, J. S., Albina, J. E. (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83, 64-70.
19. Geissmann, F., Jung, S., Littman, D. R. (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71-82. (Pubitemid 36859902)
20. Serbina, N. V., Jia, T., Hohl, T. M., Pamer, E. G. (2008) Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26, 421-452. (Pubitemid 351600381)
21. Serbina, N. V., Hohl, T. M., Cherny, M., Pamer, E. G. (2009) Selective expansion of the monocytic lineage directed by bacterial infection. J. Immunol. 183, 1900-1910.
22. Grivennikov, S. I., Tumanov, A. V., Liepinsh, D. J., Kruglov, A. A., Marakusha, B. I., Shakhov, A. N., Murakami, T., Drutskaya, L. N., Forster, I., Clausen, B. E., Tessarollo, L., Ryffel, B., Kuprash, D. V., Nedospasov, S. A. (2005) Distinct and nonredundant in vivo functions of TNF produced by T cells and macrophages/neutrophils: protective and deleterious effects. Immunity 22, 93-104. (Pubitemid 40143454)
23. Echtenacher, B., Falk, W., Mannel, D. N., Krammer, P. H. (1990) Requirement of endogenous tumor necrosis factor/cachectin for recovery from experimental peritonitis. J. Immunol. 145, 3762-3766.
24. Feldmann, M., Brennan, F. M., Elliott, M. J., Williams, R. O., Maini, R. N. (1995) TNF α is an effective therapeutic target for rheumatoid arthritis. Ann. N. Y. Acad. Sci. 766, 272-278. (Pubitemid 26169107)
25. Beutler, B., Cerami, A. (1989) The biology of cachectin/TNF - a primary mediator of the host response. Annu. Rev. Immunol. 7, 625-655. (Pubitemid 19138027)
26. Cobb, J. P., Hotchkiss, R. S., Swanson, P. E., Chang, K., Qiu, Y., Laubach, V. E., Karl, I. E., Buchman, T. G. (1999) Inducible nitric oxide synthase (iNOS) gene deficiency increases the mortality of sepsis in mice. Surgery 126, 438-442. (Pubitemid 29382815)
27. Moore, K. W., de Waal Malefyt, R., Coffman, R. L., O'Garra, A. (2001) Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765. (Pubitemid 32368050)
28. Standiford, T. J., Strieter, R. M., Lukacs, N. W., Kunkel, S. L. (1995) Neutralization of IL-10 increases lethality in endotoxemia. Cooperative effects of macrophage inflammatory protein-2 and tumor necrosis factor. J. Immunol. 155, 2222-2229.
29. Kato, T., Murata, A., Ishida, H., Toda, H., Tanaka, N., Hayashida, H., Monden, M., Matsuura, N. (1995) Interleukin 10 reduces mortality from severe peritonitis in mice. Antimicrob. Agents Chemother. 39, 1336-1340.
30. Van der Poll, T., Marchant, A., Buurman, W. A., Berman, L., Keogh, C. V., Lazarus, D. D., Nguyen, L., Goldman, M., Moldawer, L. L., Lowry, S. F. (1995) Endogenous IL-10 protects mice from death during septic peritonitis. J. Immunol. 155, 5397-5401. (Pubitemid 3015364)
31. Robben, P. M., LaRegina, M., Kuziel, W. A., Sibley, L. D. (2005) Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J. Exp. Med. 201, 1761-1769. (Pubitemid 41002895)
32. Tracey, K. J., Cerami, A. (1994) Tumor necrosis factor: a pleiotropic cytokine and therapeutic target. Annu. Rev. Med. 45, 491-503.
33. Tracey, K. J., Beutler, B., Lowry, S. F., Merryweather, J., Wolpe, S., Milsark, I. W., Hariri, R. J., Fahey III, T. J., Zentella, A., Albert, J. D., et al. (1986) Shock and tissue injury induced by recombinant human cachectin. Science 234, 470-474. (Pubitemid 17181429)
34. Tracey, K. J., Fong, Y., Hesse, D. G., Manogue, K. R., Lee, A. T., Kuo, G. C., Lowry, S. F., Cerami, A. (1987) Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteremia. Nature 330, 662-664. (Pubitemid 18005583)
35. Beutler, B., Milsark, I. W., Cerami, A. C. (1985) Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 229, 869-871. (Pubitemid 16246587)
36. Omert, L., Tsukada, K., Hierholzer, C., Lyons, V. A., Carlos, T. M., Peitzman, A. B., Billiar, T. R. (1998) A role of neutrophils in the down-regulation of IL-6 and CD14 following hemorrhagic shock. Shock 9, 391-396. (Pubitemid 128463300)
37. Daley, J. M., Reichner, J. S., Mahoney, E. J., Manfield, L., Henry Jr., W. L., Mastrofrancesco, B., Albina, J. E. (2005) Modulation of macrophage phenotype by soluble product(s) released from neutrophils. J. Immunol. 174, 2265-2272. (Pubitemid 40223974)
38. Holub, M., Cheng, C. W., Mott, S., Wintermeyer, P., van Rooijen, N., Gregory, S. H. (2009) Neutrophils sequestered in the liver suppress the proinflammatory response of Kupffer cells to systemic bacterial infection. J. Immunol. 183, 3309-3316.
39. Couper, K. N., Blount, D. G., Riley, E. M. (2008) IL-10: the master regulator of immunity to infection. J. Immunol. 180, 5771-5777.
40. Fadok, V. A., Bratton, D. L., Rose, D. M., Pearson, A., Ezekewitz, R. A., Henson, P. M. (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405, 85-90. (Pubitemid 30321820)
41. Ren, Y., Xie, Y., Jiang, G., Fan, J., Yeung, J., Li, W., Tam, P. K., Savill, J. (2008) Apoptotic cells protect mice against lipopolysaccharide- induced shock. J. Immunol. 180, 4978-4985.
42. Savill, J., Dransfield, I., Gregory, C., Haslett, C. (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975. (Pubitemid 37323217)
43. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101, 890-898. (Pubitemid 28096086)
44. Esmann, L., Idel, C., Sarkar, A., Hellberg, L., Behnen, M., Moller, S., van Zandbergen, G., Klinger, M., Kohl, J., Bussmeyer, U., Solbach, W., Laskay, T. (2010) Phagocytosis of apoptotic cells by neutrophil granulocytes: diminished proinflammatory neutrophil functions in the presence of apoptotic cells. J. Immunol. 184, 391-400.
45. Dardalhon, V., Anderson, A. C., Karman, J., Apetoh, L., Chandwaskar, R., Lee, D. H., Cornejo, M., Nishi, N., Yamauchi, A., Quintana, F. J., Sobel, R. A., Hirashima, M., Kuchroo, V. K. (2010) Tim-3/galectin-9 pathway: regulation of Th1 immunity through promotion of CD11b+Ly-6G+ myeloid cells. J. Immunol. 185, 1383-1392.
46. 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., Al-Quran, S. Z., Swan, R., Chung, C. S., Atkinson, M. A., Ramphal, R., Gabrilovich, D. I., Reeves, W. H., Ayala, A., Phillips, J., Laface, D., Heyworth, P. G., Clare-Salzler, M., Moldawer, L. L. (2007) MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med. 204, 1463-1474. (Pubitemid 46919883)
47. Reichel, C. A., Khandoga, A., Anders, H. J., Schlondorff, D., Luckow, B., Krombach, F. (2006) Chemokine receptors Ccr1, Ccr2, and Ccr5 mediate neutrophil migration to postischemic tissue. J. Leukoc. Biol. 79, 114-122. (Pubitemid 43054256)
48. Souto, F. O., Alves-Filho, J. C., Turato, W. M., Auxiliadora-Martins, M., Basile-Filho, A., Cunha, F. Q. (2010) Essential role of CCR2 in neutrophil tissue infiltration and multiple organ dysfunction in sepsis. Am. J. Respir. Crit. Care Med., Epub ahead of print.
49. Dellinger, R. P., Levy, M. M., Carlet, J. M., Bion, J., Parker, M. M., Jaeschke, R., Reinhart, K., Angus, D. C., Brun-Buisson, C., Beale, R., Calandra, T., Dhainaut, J. F., Gerlach, H., Harvey, M., Marini, J. J., Marshall, J., Ranieri, M., Ramsay, G., Sevransky, J., Thompson, B. T., Townsend, S., Vender, J. S., Zimmerman, J. L., Vincent, J. L. (2008) Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit. Care Med. 36, 296-327.