Injury primes the innate immune system for enhanced Toll-like receptor reactivity

Journal of Immunology

Volumn 171, Issue 3, 2003, Pages 1473-1483

  Paterson, Hugh M ^a   Murphy, Thomas J ^a   Purcell, Elizabeth J ^a   Shelley, Odhran ^a   Kriynovich, Sara J ^a   Lien, Egil ^b,c   Mannick, John A ^a   Lederer, James A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; INTERLEUKIN 1BETA; INTERLEUKIN 6; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNE SYSTEM; INFLAMMATION; INJURY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL;

EID: 0041344362     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.3.1473     Document Type: Article

References (69)

1. Lederer, J. A., M. L, Rodrick, and J. A. Mannick. 1999. The effects of injury on the adaptive immune response. Shock 11:153.
2. Baker, C. C., C. L. Miller, and D. D. Trunkey. 1979. Predicting fatal sepsis in bum patients. J. Trauma 19:641.
3. Miller, C. L., and D. D. Trunkey. 1977. Thermal injury: defects in immune response induction. J. Surg. Res. 22:621.
4. Barlow, Y. 1994. T lymphocytes and immunosuppression in the burned patient: a review. Burns 20:487.
5. 2 and immunomodulation with indomethacin. J. Immunol. 151:2142.
6. 2 by LPS-stimulated rat bone marrow macrophages after thermal injury: effect of indomethacin. Inflammation 18:175.
7. Flach, R., M. Majetschak, T. Heukamp, V. Jennissen, S. Flohe, J. Borgermann, U. Obertacke, and F. U. Schade. 1999. Relation of ex vivo sfimulated blood cytokine synthesis to post-traumatic sepsis. Cytokine 11:173.
8. Kelly, J. L., C. O'Sullivan. M. O'Riordain, D. O'Riordain, A. Lyons, J. Doherty, J. A. Mannick, and M. L. Rodrick. 1997. Is circulating endotoxin the trigger for the systemic inflammatory response syndrome seen after injury? Ann. Surg. 225:530.
9. Kell, M. R., E. G. Kavanaugh, A. Goebel, C. C. Soberg, and J. A. Lederer. 1999. Injury primes the immune system for an enhanced and lethal T-cell response against bacterial superantigen. Shock 12:139.
10. Bang, R. L., R. K. Gang, S. C. Sanyal, E. Mokaddas, and M. K. Ebrahim. 1998. Bum septicaemia: an analysis of 79 patients. Burns 24:354.
11. Bone, R. C. 1992. Toward an epidemiology and natural history of SIRS (systemic inflammatory response syndrome). J. Am. Med. Assoc. 268:3452.
12. Baue, A. E., R. Durham, and E. Faist. 1998. Systemic inflammatory response syndrome (SIRS), multiple organ dysfunction syndrome (MODS). multiple organ failure (MOF): are we winning the battle? Shock 10:79.
13. Shahbazian, L. M., M. Jeevanandam, and S. R. Petersen. 1999. Release of proinflammatory cytokines by mitogen-stimulated peripheral blood mononuclear cells from critically ill multiple-trauma victims. Metabolism 48:1397.
14. Jeevanandam, M., L. M. Shahbazian, and S. R. Petersen. 1999. Proinflammatory cytokine production by mitogen-stimulated peripheral blood mononuclear cells (PBMCs) in trauma patients fed immune-enhancing enteral diets. Nutrition 15:842.
15. Wu. J. Z., C. K. Ogle, J. X. Mao, K. Szczur, J. E. Fischer, and J. D. Ogle. 1995. The increased potential for the production of inflammatory cytokines by Kupffer cells and splenic macrophages eight days after thermal injury. Inflammation 19:529.
16. Williams, J. G., P. Bankey, J. P. Minei. K. McIntyre, and T. Turbeville. 1994. Burn injury enhances alveolar macrophage endotoxin sensitivity. J. Burn Care Rehabil. 15:493.
17. 2: contribution to the enhancement of inducible nitric oxide synthase activity. J. Leukocyte Biol. 64:740.
18. Schwacha, M. G., C. P. Schneider, K. I. Rland, and I. H. Chaudry. 2001. Resistance of macrophages to the suppressive effect of interleukin-10 following thermal injury. Am. J. Physiol. 281:C1180.
19. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394.
20. Janeway, C. A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20:197.
21. Kaisho, T., and S. Akira. 2000. Critical roles of Toll-like receptors in host defense. Crit. Rev. Immunol. 20:393.
22. Chow, J. C., D. W. Young, D. T. Golenbock, W. J. Christ, and F. Gusovsky. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274:10689.
23. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyperesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162:3749.
24. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. V. Huffel, X. Du. D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085.
25. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135.
26. Schwandner, R., R. Dziarski, H. Wesche, M. Rothe, and C. J. Kirschning. 1999. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J. Biol. Chem. 274:17406.
27. Yoshimura, A., E. Lien, R. R. Ingalls, E. Tuomanen, R. Dziarski, and D. Golenbock. 1999. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163:1.
28. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740.
29. Michelsen, K. S., A. Aicher. M. Mohaupt, T. Hartung, S. Dimmeler, C. J. Kirschning, and R. R. Schumann. 2001. The role of Toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCs): peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J. Biol. Chem. 276:25680.
30. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11:443.
31. Moss, N. M., D. B. Gough, A. L. Jordan, J. T. Grbic, J. J. Wood, M. L. Rodrick, and J. A. Mannick. 1988. Temporal correlation of impaired immune response after thermal injury with susceptibility to infection in a murine model. Surgery 104:882.
32. Akashi, S., R. Shimazu, H. Ogata, Y. Nagai, K. Takeda, M. Kimoto, and K. Miyake. 2000. Cutting edge: cell surface expression and lipopolysaccharide signaling via the Toll-like receptor 4-MD-2 complex on mouse peritoneal macrophages. J. Immunol. 164:3471.
33. Ohashi, K., V. Burkart, S. Flohe, and H. Kolb. 2000. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J. Immunol. 164:558.
34. Vabulas, R. M., P. Ahmad-Nejad, S. Ghose, C. J. Kirschning, R. D. Issels, and H. Wagner. 2002. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277:15107.
35. Dybdahl, B., A. Wahba, E. Lien, T. H. Flo, A. Waage, N. Qureshi, O. F. Sellevold, T. Espevik, and A. Sundan. 2002. Inflammatory response after open heart surgery: release of heat-shock protein 70 and signaling through Toll-like receptor-4. Circulation 105:685.
36. Okamura, Y., M. Watari, E. S. Jerud, D. W. Young, S. T. Ishizaka, J. Rose, J. C. Chow, and J. F. Strauss III. 2001. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276:10229.
37. Rassa, J. C., J. L. Meyers, Y. Zhang, R. Kudaravalli, and S. R. Ross. 2002. Murine retroviruses activate B cells via interaction with Toll-like receptor 4. Proc. Natl. Acad. Sci. USA 99:2281.
38. Beutler, B., and A. Poltorak. 2001. Sepsis and evolution of the innate immune response. Crit. Care Med. 29:S2.
39. Wang, J. E., A. Warris, E. A. Ellingsen, P. F. Jorgensen, T. H. Flo, T. Espevik, R. Solberg, P. E. Verweij, and A. O. Aasen. 2001. Involvement of CD14 and Toll-like receptors in activation of human monocytes by Aspergillus fumigatus hyphae. Infect. Immun. 69:2402.
40. Hirschfeld, M., C. J. Kirschning, R. Schwandner, H. Wesche, J. H. Weis, R. M. Wooten, and J. J. Weis. 1999. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by Toll-like receptor 2. J. Immunol. 163:2382.
41. Underhill, D. M., A. Ozinsky, K. D. Smith, and A. Aderem. 1999. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 96:14459.
42. Flo, T. H., O. Halaas, E. Lien, L. Ryan, G. Teti, D. T. Golenbock, A. Sundan, and T. Espevik. 2000. Human Toll-like receptor 2 mediates monocyte activation by Listeria monocytogenes, but not by group B streptococci or lipopolysaccharide. J. Immunol. 164:2064.
43. Lien, E., T. K. Means, H. Heine, A. Yoshimura, S. Kusumoto, K. Fukase, M. J. Fenton, M. Oikawa, N. Qureshi, B. Monks, et al. 2000. Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J. Clin. Invest. 105:497.
44. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison, 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431.
45. Shimazu, R., S. Akashi, H. Ogata, Y. Nagai, K. Fukudome, K. Miyake, and M. Kimoto. 1999. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 189:1777.
46. Hirschfeld, M., Y. Ma, J. H. Weis, S. N. Vogel, and J. J. Weis. 2000. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J. Immunol. 165:618.
47. Hajjar, A. M., D. S. O'Mahony, A. Ozinsky, D. M. Underhill, A. Aderem, S. J. Klebanoff, and C. B. Wilson. 2001. Cutting edge: functional interactions between Toll-like receptor (TLR)2 and TLRI or TLR6 in response to phenol-soluble modulin. J. Immunol. 166:15.
48. Ozinsky, A., D. M. Underhill, J. D. Fontenot. A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA 97:13766.
49. Jones, B. W., T. K. Means, K. A. Heldwein, M. A. Keen, P. J. Hill, J. T. Belisle, and M. J. Fenton. 2001. Different Toll-like receptor agonists induce distinct macrophage responses. J. Leukocyte Biol. 69:1036.
50. Apte, R. N., C. Galanos, and D. H. Pluznik. 1976. Lipid A, the active part of bacterial endotoxins in inducing serum colony stimulating activity and proliferation of splenic granulocyte/macrophage progenitor cells. J. Cell. Physiol. 87:71.
51. Doe, W. F., S. T. Yang, D. C. Morrison, S. J. Betz, and P. M. Henson. 1978. Macrophage stimulation by bacterial lipopolysaccharides. II. Evidence for differentiation signals delivered by lipid A and by a protein rich fraction of lipopolysaccharides. J. Exp. Med. 148:557.
52. Netea, M. G., M. van Deuren, B. J. Kullberg, J. M. Cavaillon, and J. W. Van der Meer. 2002. Does the shape of lipid A determine the interaction of LPS with Toll-like receptors? Trends Immunol. 23:135.
53. Li, M., D. F. Carpio, Y. Zheng, P. Bruzzo, V. Singh, F. Ouaaz, R. M. Medzhitov, and A. A. Beg. 2001. An essential role of the NF-κB/Toll-like receptor pathway in induction of inflammatory and tissue-repair gene expression by necrotic cells. J. Immunol. 166:7128.
54. Smiley, S. T., J. A. King, and W. W. Hancock. 2001. Fibrinogen stimulates macrophage chemokine secretion through Toll-like receptor 4. J. Immunol. 167:2887.
55. Matzinger, P. 1994. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12:991.
56. Kobayashi, K., L. D. Hernandez, J. E. Galan, C. A. Janeway, Jr., R. Medzhitov, and R. A. Flavell. 2002. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110:191.
57. Fan, J., A. Kapus, P. A. Marsden, Y. H. Li, G. Oreopoulos, J. C. Marshall, S. Frantz, R. A. Kelly, R. Medzhitov, and O. D. Rotstein. 2002. Regulation of Toll-like receptor 4 expression in the lung following hemorrhagic shock and lipopolysaccharide. J. Immunol. 168:5252.
58. Rajnik, M., C. A. Salkowski, K. E. Thomas, Y. Y. Li, F. M. Rollwagen, and S. N. Vogel. 2002. Induction of early inflammatory gene expression in a murine model of nonresuscitated, fixed-volume hemorrhage. Shock 17:322.
59. Minei, J. P., J. G. Williams, S. J. Hill, K. McIntyre, and P. E. Bankey. 1994. Augmented tumor necrosis factor response to lipopolysaccharide after thermal injury is regulated posttranscriptionally. Arch. Surg. 129:1198.
60. Gamelli, R. L., H. Liu, L. K. He, and C. A. Hofmann. 1996. Augmentations of glucose uptake and glucose transporter-1 in macrophages following thermal injury and sepsis in mice. J. Leukocyte Biol. 59:639.
61. Ogle, C. K., J. F. Valente, X. Guo, B. G. Li, J. D. Ogle, and J. W. Alexander. 1997. Thermal injury induces the development of inflammatory macrophages from nonadherent bone marrow cells. Inflammation 21:569.
62. Schwacha, M. G., and S. D. Somers. 1998. Thermal injury induces macrophage hyperactivity through pertussis toxin-sensitive and -insensitive pathways. Shock 9:249.
63. Zhu, X. L., R. Zellweger, X. H. Zhu, A. Ayala, and I. H. Chaudry. 1995. Cytokine gene expression in splenic macrophages and Kupffer cells following haemorrhage. Cytokine 7:8.
64. McCarter, M. D., V. E. Mack, J. M. Daly, H. A. Naama, and S. E. Calvano. 1998. Trauma-induced alterations in macrophage function. Surgery 123:96.
65. Zallen, G., E. E. Moore, J. L. Johnson, D. Y. Tamura, J. Aiboshi, W. L. Biffl, and C. C. Silliman. 1999. Circulating postinjury neutrophils are primed for the release of proinflammatory cytokines. J. Trauma 46:42.
66. Dobrovolskaia, M. A., and S. N. Vogel. 2002. Toll receptors, CD14, and macrophage activation and deactivation by LPS. Microbes Infect. 4:903.
67. West, M. A., and W. Heagy. 2002. Endotoxin tolerance: a review. Crit. Care Med. 30:S64.
68. Matzinger, P. 2002. The danger model: a renewed sense of self. Science 296:301.
69. Mannick, J. A., M. L. Rodrick, and J. A. Lederer. 2001. The immunologic response to injury. J. Am. Coll. Surg. 193:237.