Flagellin treatment prevents increased susceptibility to systemic bacterial infection after injury by inhibiting anti-inflammatory IL-10+ IL-12- neutrophil polarization

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Neely, Crystal J ^a   Kartchner, Laurel B ^a   Mendoza, April E ^b   Linz, Brandon M ^a   Frelinger, Jeffrey A ^a   Wolfgang, Matthew C ^a   Maile, Robert ^a,b   Cairns, Bruce A ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; INTERLEUKIN 10; INTERLEUKIN 12; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL INFECTION; BACTERIAL STRAIN; BURN; CELL POPULATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; INNATE IMMUNITY; INOCULATION; MACROPHAGE; MORTALITY; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; POLARIZATION; PROTEIN EXPRESSION; PROTEIN TARGETING; PSEUDOMONAS AERUGINOSA; SALMONELLA TYPHIMURIUM; SPLEEN CELL;

ANIMALS; BURNS; CELL POLARITY; FEMALE; FLAGELLIN; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; INTERLEUKIN-10; INTERLEUKIN-12; MACROPHAGES; MICE; MICE, INBRED C57BL; NEUTROPHILS; PSEUDOMONAS INFECTIONS; SEPSIS; TOLL-LIKE RECEPTORS;

EID: 84898622817     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085623     Document Type: Article

References (62)

1. Centers for Disease Control and Prevention (2012) Web-based Injury Statistics Query and Reporting System
2. Papia G, McLellan BA, El-Helou P, Louie M, Rachlis A, et al. (1999) Infection in hospitalized trauma patients: incidence, risk factors, and complications. J Trauma 47: 923-927
3. Niven DJ, Fick GH, Kirkpatrick AW, Grant V, Laupland KB (2010) Cost and outcomes of nosocomial bloodstream infections complicating major traumatic injury. J Hosp Infect 76: 296-299
4. Glance LG, Stone PW, Mukamel DB, Dick AW (2011) Increases in mortality, length of stay, and cost associated with hospital-acquired infections in trauma patients. Arch Surg 146: 794-801
5. Patel JC, Mollitt DL, Tepas JJ (2000) Infectious complications in critically injured children. J Pediatr Surg 35: 1174-1178 (Pubitemid 30640205)
6. Fukuzuka K, Edwards CK , Clare-Salzer M, Copeland EM 3rd, Moldawer LL, et al. (2000) Glucocorticoid and Fas ligand induced mucosal lymphocyte apoptosis after burn injury. J Trauma 49: 710-716
7. Pellegrini JD, De AK, Kodys K, Puyana JC, Furse RK, et al. (2000) Relationships between T lymphocyte apoptosis and anergy following trauma. J Surg Res 88: 200-206 (Pubitemid 30085853)
8. Maile R, Barnes CM, Nielsen AI, Meyer AA, Frelinger JA, et al. (2006) Lymphopenia-induced homeostatic proliferation of CD8(+) T cells is a mechanism for effective allogeneic skin graft rejection following burn injury. Journal of Immunology 176: 6717-6726 (Pubitemid 43791968)
9. Cairns BA, Maile R, Buchanan I, Pilati D, Deserres S, et al. (2001) CD8 T cells express a T-helper 1-like phenotype after burn injury. Surgery 130: 210-216 (Pubitemid 32721671)
10. Guo Z, Kavanagh E, Zang Y, Dolan SM, Kriynovich SJ, et al. (2003) Burn injury promotes antigen-driven Th2-type responses in vivo. J Immunol 171: 3983-3990 (Pubitemid 37238672)
11. Kovacs EJ, Duffner LA, Plackett TP (2004) Immunosuppression after injury in aged mice is associated with a TH1-TH2 shift, which can be restored by estrogen treatment. Mech Ageing Dev 125: 121-123 (Pubitemid 38177571)
12. Zedler S, Bone RC, Baue AE, von Donnersmarck GH, Faist E (1999) T-cell reactivity and its predictive role in immunosuppression after burns. Crit Care Med 27: 66-72 (Pubitemid 29052816)
13. MacConmara MP, Maung AA, Fujimi S, McKenna AM, Delisle A, et al. (2006) increased CD4+ CD25+ T regulatory cell activity in trauma patients depresses protective Th1 immunity. Ann Surg 244: 514-523
14. Choileain NN, Macconmara M, Zang Y, Murphy TJ, Mannick JA, et al. (2006) Enhanced Regulatory T Cell Activity Is an Element of the Host Response to Injury. J Immunol 176: 225-236 (Pubitemid 43023267)
15. Scumpia PO, Delano MJ, Kelly KM, O'Malley KA, Efron PA, 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 (Pubitemid 44846310)
16. Nordenfelt P, Tapper H (2011) Phagosome dynamics during phagocytosis by neutrophils. J Leukoc Biol 90: 271-284
17. Borregaard N (1997) Development of neutrophil granule diversity. Ann N Y Acad Sci 832: 62-68 (Pubitemid 28045304)
18. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535 (Pubitemid 38314426)
19. Fujiwara N, Kobayashi K (2005) Macrophages in inflammation. Curr Drug Targets Inflamm Allergy 4: 281-286 (Pubitemid 40873112)
20. Savina A, Amigorena S (2007) Phagocytosis and antigen presentation in dendritic cells. Immunol Rev 219: 143-156 (Pubitemid 47390005)
21. Lien E, Ingalls RR (2002) Toll-like receptors. Crit Care Med 30: S1-11
22. van Putten JP, Bouwman LI, de Zoete MR (2010) Unraveling bacterial interactions with toll-like receptors. Immunol Lett 128: 8-11
23. Harter L, Mica L, Stocker R, Trentz O, Keel M (2004) Increased expression of toll-like receptor-2 and -4 on leukocytes from patients with sepsis. Shock 22: 403-409 (Pubitemid 39472563)
24. Martins PS, Brunialti MK, Martos LS, Machado FR, Assuncao MS, et al. (2008) Expression of cell surface receptors and oxidative metabolism modulation in the clinical continuum of sepsis. Crit Care 12: R25
25. Hotchkiss RS, Coopersmith CM, McDunn JE, Ferguson TA (2009) The sepsis seesaw: tilting toward immunosuppression. Nat Med 15: 496-497
26. Qin H, Holdbrooks AT, Liu Y, Reynolds SL, Yanagisawa LL, et al. (2012) SOCS3 deficiency promotes M1 macrophage polarization and inflammation. J Immunol 189: 3439-3448
27. Kasten KR, Muenzer JT, Caldwell CC (2010) Neutrophils are significant producers of IL-10 during sepsis. Biochem Biophys Res Commun 393: 28-31
28. Biswas SK, Chittezhath M, Shalova IN, Lim JY (2012) Macrophage polarization and plasticity in health and disease. Immunol Res 53: 11-24
29. Zhang X, Mosser DM (2008) Macrophage activation by endogenous danger signals. J Pathol 214: 161-178 (Pubitemid 351160154)
30. Cairns BA, Barnes CM, Mlot S, Meyer AA, Maile R (2008) Toll-like receptor 2 and 4 ligation results in complex altered cytokine profiles early and late after burn injury. J Trauma 64: 1069-1077; discussion 1077-1068
31. Cohen MJ, Carroll C, He LK, Muthu K, Gamelli RL, et al. (2007) Severity of burn injury and sepsis determines the cytokine responses of bone marrow progenitor-derived macrophages. J Trauma 62: 858-867 (Pubitemid 46624202)
32. Noel G, Wang Q, Schwemberger S, Hanson C, Giacalone N, et al. (2011) Neutrophils, not monocyte/macrophages, are the major splenic source of postburn IL-10. Shock 36: 149-155
33. Schwacha MG, Chaudry IH, Alexander M (2003) Regulation of macrophage IL-10 production postinjury via beta2 integrin signaling and the P38 MAP kinase pathway. Shock 20: 529-535
34. Kalechman Y, Gafter U, Gal R, Rushkin G, Yan D, et al. (2002) Anti-IL-10 therapeutic strategy using the immunomodulator AS101 in protecting mice from sepsis-induced death: dependence on timing of immunomodulating intervention. J Immunol 169: 384-392
35. Kahlke V, Dohm C, Mees T, Brotzmann K, Schreiber S, et al. (2002) Early interleukin-10 treatment improves survival and enhances immune function only in males after hemorrhage and subsequent sepsis. Shock 18: 24-28
36. Steinhauser ML, Hogaboam CM, Kunkel SL, Lukacs NW, Strieter RM, et al. (1999) IL-10 is a major mediator of sepsis-induced impairment in lung antibacterial host defense. J Immunol 162: 392-399 (Pubitemid 29018946)
37. Yamaguchi T, Hirakata Y, Izumikawa K, Miyazaki Y, Maesaki S, et al. (2000) Prolonged survival of mice with Pseudomonas aeruginosa-induced sepsis by rIL- 12 modulation of IL-10 and interferon-gamma. J Med Microbiol 49: 701-707 (Pubitemid 30623902)
38. Sun L, Guo RF, Newstead MW, Standiford TJ, Macariola DR, et al. (2009) Effect of IL-10 on neutrophil recruitment and survival after Pseudomonas aeruginosa challenge. Am J Respir Cell Mol Biol 41: 76-84
39. Jones SW, Zhou H, Ortiz-Pujols SM, Maile R, Herbst M, et al. (2013) Bronchoscopy-Derived Correlates of Lung Injury following Inhalational Injuries: A Prospective Observational Study. PLoS One 8: e64250
40. Cuenca AG, Delano MJ, Kelly-Scumpia KM, Moreno C, Scumpia PO, et al. (2011) A paradoxical role for myeloid-derived suppressor cells in sepsis and trauma. Mol Med 17: 281-292
41. Noel JG, Osterburg A, Wang Q, Guo X, Byrum D, et al. (2007) Thermal injury elevates the inflammatory monocyte subpopulation in multiple compartments. Shock 28: 684-693 (Pubitemid 350135473)
42. Cuenca AG, Moldawer LL (2012) Myeloid-derived suppressor cells in sepsis: friend or foe? Intensive Care Med 38: 928-930
43. Wolfgang MC, Lee VT, Gilmore ME, Lory S (2003) Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 4: 253-263 (Pubitemid 36221801)
44. Maung AA, Fujimi S, Miller ML, MacConmara MP, Mannick JA, et al. (2005) Enhanced TLR4 reactivity following injury is mediated by increased p38 activation. J Leukoc Biol 78: 565-573 (Pubitemid 41061328)
45. Hajjar AM, Ernst RK, Tsai JH, Wilson CB, Miller SI (2002) Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat Immunol 3: 354-359 (Pubitemid 34308623)
46. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, et al. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51
47. Balloy V, Verma A, Kuravi S, Si-Tahar M, Chignard M, et al. (2007) The role of flagellin versus motility in acute lung disease caused by Pseudomonas aeruginosa. J Infect Dis 196: 289-296 (Pubitemid 47047469)
48. Schwacha MG (2003) Macrophages and post-burn immune dysfunction. Burns 29: 1-14 (Pubitemid 36132258)
49. Smith RS, Wolfgang MC, Lory S (2004) An adenylate cyclase-controlled signaling network regulates Pseudomonas aeruginosa virulence in a mouse model of acute pneumonia. Infect Immun 72: 1677-1684 (Pubitemid 38263791)
50. Vicente-Suarez I, Takahashi Y, Cheng F, Horna P, Wang HW, et al. (2007) Identification of a novel negative role of flagellin in regulating IL-10 production. Eur J Immunol 37: 3164-3175 (Pubitemid 350131295)
51. Mendoza AE, Neely CJ, Charles AG, Kartchner LB, Brickey WJ, et al. (2012) Radiation combined with thermal injury induces immature myeloid cells. Shock 38: 532-542
52. Cairns B, Maile R, Barnes CM, Frelinger JA, Meyer AA (2006) Increased Tolllike receptor 4 expression on T cells may be a mechanism for enhanced T cell response late after burn injury. Journal of Trauma-Injury Infection and Critical Care 61: 293-298; discussion 298-299
53. Hart KM, Byrne KT, Molloy MJ, Usherwood EM, Berwin B (2011) IL-10 immunomodulation of myeloid cells regulates a murine model of ovarian cancer. Front Immunol 2: 29
54. Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, et al. (2008) Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111: 4233-4244
55. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI (2008) Subsets of myeloidderived suppressor cells in tumor-bearing mice. J Immunol 181: 5791-5802
56. Mosmann TR, Sad S (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17: 138-146
57. Sica A, Larghi P, Mancino A, Rubino L, Porta C, et al. (2008) Macrophage polarization in tumour progression. Semin Cancer Biol 18: 349-355
58. Jeannin P, Duluc D, Delneste Y (2011) IL-6 and leukemia-inhibitory factor are involved in the generation of tumor-associated macrophage: regulation by IFNgamma. Immunotherapy 3: 23-26
59. Martinez FO, Sica A, Mantovani A, Locati M (2008) Macrophage activation and polarization. Front Biosci 13: 453-461 (Pubitemid 351599757)
60. Ambarus CA, Santegoets KC, van Bon L, Wenink MH, Tak PP, et al. (2012) Soluble immune complexes shift the TLR-induced cytokine production of distinct polarized human macrophage subsets towards IL-10. PLoS One 7: e35994
61. Shigematsu K, Asai A, Kobayashi M, Herndon DN, Suzuki F (2009) Enterococcus faecalis translocation in mice with severe burn injury: a pathogenic role of CCL2 and alternatively activated macrophages (M2aMphi and M2cMphi). J Leukoc Biol 86: 999-1005
62. Csontos C, Foldi V, Palinkas L, Bogar L, Roth E, et al. (2010) Time course of pro- and anti-inflammatory cytokine levels in patients with burns-prognostic value of interleukin-10. Burns 36: 483-494