Activation of toll-like receptor 4 is necessary for trauma hemorrhagic shock-induced gut injury and polymorphonuclear neutrophil priming

Shock

Volumn 38, Issue 1, 2012, Pages 107-114

  Reino, Diego C ^a   Palange, David ^a   Feketeova, Elenora ^a   Bonitz, Robert P ^a   Xu, Da Zhong ^a   Lu, Qi ^a   Sheth, Sharvil U ^a   Peña, Geber ^a   Ulloa, Luis ^a   De Maio, Antonio ^b   Feinman, Rena ^a   Deitch, Edwin A ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

danger model; hemorrhage; Mesenteric lymph; MODS; shock

Indexed keywords

BACTERIAL DNA; ENDOTOXIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HIGH MOBILITY GROUP B1 PROTEIN; HYALURONIC ACID; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HEMORRHAGIC SHOCK; INTESTINE INJURY; MALE; MOUSE; NEUTROPHIL; NONHUMAN; REPERFUSION INJURY; RESPIRATORY BURST;

ACUTE LUNG INJURY; ANIMALS; INTESTINAL DISEASES; INTESTINES; LIGANDS; LYMPH; MALE; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; NEUTROPHIL ACTIVATION; PERMEABILITY; RATS; RESPIRATORY BURST; SHOCK, HEMORRHAGIC; SIGNAL TRANSDUCTION; SWINE; SWINE, MINIATURE; TOLL-LIKE RECEPTOR 4; WOUNDS AND INJURIES;

EID: 84862755182     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0b013e318257123a     Document Type: Article

References (57)

1. Matzinger P: The danger model: a renewed sense of self. Science 296:301-305, 2002. (Pubitemid 34303674)
2. Bianchi ME: DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81:1-5, 2007. (Pubitemid 46028489)
3. Kono H, Rock KL: How dying cells alert the immune system to danger. Nat Rev Immunol 8:279-289, 2008. (Pubitemid 351432799)
4. Paterson HM, Murphy TJ, Purcell EJ, Shelley O, Kriynovich SJ, Lien E, Mannick JA, Lederer JA: Injury primes the innate immune system for enhanced toll-like receptor reactivity. J Immunol 171:1473-1483, 2003. (Pubitemid 36900082)
5. Mollen K, Anand R, Tsung A, Prince J, Levy R, Billiar T: Emerging paradigm: toll-like receptor 4-sentinel for the detection of tissue damage. Shock 26:430-437, 2006. (Pubitemid 44632271)
6. Fan J, Kapus A, Marsden PA, Li YH, Oreopoulos G, Marshall JC, Frantz S, Kelly RA, Medzhitov R, Rotstein OD: Regulation of toll-like receptor 4 expression in the lung following hemorrhagic shock and lipopolysaccharide. J Immunol 168:5252-5259, 2002. (Pubitemid 34495993)
7. Reino DC, Pisarenko V, Palange D, Doucet D, Bonitz RP, Lu Q, Colorado I, Sheth SU, Chandler B, Kannan KB, et al.: Trauma hemorrhagic shockYinduced lung injury involves a gut-lymph-induced TLR4 pathway in mice. PLoS One 6:e14829, 2011.
8. Prince JM, Levy RM, Yang R, Mollen KP, Fink MP, Vodovotz Y, Billiar TR: Toll-like receptor-4 signaling mediates hepatic injury and systemic inflammation in hemorrhagic shock. J Am Coll Surg 202:407-417, 2006. (Pubitemid 43356214)
9. Chen C, Wang Y, Zhang Z, Wang C, Peng M: Toll-like receptor 4 regulates heme oxygenase-1 expression after hemorrhagic shock induced acute lung injury in mice: requirement of p38 mitogen-activated protein kinase activation. Shock 31:486-492, 2009.
10. Fan J: TLR cross-talk mechanism of hemorrhagic shockYprimed pulmonary neutrophil infiltration. Open Crit Care Med J 2:1-8, 2010.
11. Deitch EA, Xu D, Lu Q: Gut lymph hypothesis of early shock and traumainduced multiple organ dysfunction: a new look at gut origin of sepsis. J Org Dys 2:70, 2006.
12. Senthil M, Watkins A, Barlos D, Xu D, Lu Q, Abungu B, Caputo F, Feinman R, Deitch EA: Intravenous injection of trauma-hemorrhagic shock mesenteric lymph causes lung injury that is dependent upon activation of the inducible nitric oxide synthase pathway. Ann Surg 246:822-830, 2007. (Pubitemid 350035659)
13. Condon M, Senthil M, Xu D, Mason L, Sheth S, Spolarics Z, Feketova E, Machiedo G, Deitch EA: Intravenous injection of mesenteric lymph produced during hemorrhagic shock decreases RBC deformability in the rat. J Trauma 70:489-495, 2011.
14. Abraham E: Neutrophils and acute lung injury. Crit Care Med 31:S195-S199, 2003. (Pubitemid 36458167)
15. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S: Targeted disruption of the MyD88 gene results in loss of IL-1Y and IL-18Ymediated function. Immunity 9:143-150, 1998. (Pubitemid 28361303)
16. Poltorak A, He X, Smirnova I, Liu M-Y, Huffel CV, Du X, Birdwell D, Alejos E, Silva M, Galanos C, et al.: Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088, 1998. (Pubitemid 29001265)
17. Senthil M, Brown M, Xu D, Lu Q, Feketeova E, Deitch EA: Gut-lymph hypothesis of systemic inflammatory response syndrome/multiple-organ dysfunction syndrome: validating studies in a porcine model. J Trauma 60:958-965, 2006. (Pubitemid 43778621)
18. Caputo F, Rupani B, Watkins A, Barlos D, Vega D, Senthil M, Deitch EA: Pancreatic duct ligation abrogates the trauma hemorrhageYinduced gut barrier failure and the subsequent production of biologically active intestinal lymph. Shock 28:441-446, 2007. (Pubitemid 47415255)
19. Doucet DR, Bonitz RP, Feinman R, Colorado I, Ramanathan M, Feketeova E, Condon M, Machiedo GW, Hauser CJ, Xu DZ, et al.: Estrogenic hormone modulation abrogates changes in red blood cell deformability and neutrophil activation in trauma hemorrhagic shock. J Trauma 68:35-41, 2010.
20. Magnotti L, Upperman J, Xu D, Lu Q, Deitch EA: Gut-derived mesenteric lymph but not portal blood increases endothelial permeability and potentiates lung injury following hemorrhagic shock. Ann Surg 228:518-527, 1998. (Pubitemid 30194395)
21. Ulloa L, Ochani M, Yang H, Tanovic M, Halperin D, Yang R, Czura CJ, Fink MP, Tracey KJ: Ethyl pyruvate prevents lethality in mice with established lethal sepsis and systemic inflammation. Proc Natl Acad Sci USA 99:12351-12356, 2002.
22. Vega V, Charles W, De Maio A: A new feature of the stress response: increase in endocytosis mediated by HSP70. Cell Stress Chaperones 15:517-527, 2010.
23. Lindqvist U, Chichibu K, Delpech B, Goldberg RL, Knudson W, Poole AR, Laurent TC: Seven different assays of hyaluronan compared for clinical utility. Clin Chem 38:127-132, 1992.
24. Wang H, Yang H, Czura C, Sama A, Tracey K: HMGB1 as a late mediator of lethal systemic inflammation. Am J Respir Crit Care Med 164:1768-1773, 2001. (Pubitemid 33152308)
25. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, et al.: HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248-251, 1999. (Pubitemid 29329996)
26. Piccinini AM, Midwood KS: DAMPening inflammation by modulating TLR signalling. Mediat Inflamm 2010. pii: 672395. Epub 2010 Jul 13.
27. Moore E, Moore F, Franciose R, Kim F, Biffl W, Banerjee A: The postischemic gut serves as a priming bed for circulating neutrophils that provoke multiple organ failure. J Trauma 37:881-887, 1994.
28. Abraham E, Carmody A, Shenkar R, Arcaroli J: PMNs as early immunologic effectors in hemorrhage-or endotoxemia-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 279:L1137-L1145, 2000. (Pubitemid 32009500)
29. Mantovani A, Cassatella MA, Costantini C, Jaillon S: Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11:519-531, 2011.
30. Leaphart CL, Tepas JJ III: The gut is a motor of organ system dysfunction. Surgery 141:563-569, 2007. (Pubitemid 46621132)
31. Caruso JMFE, Dayal SD, Hauser CJ, Deitch EA: Factors in intestinal lymph after shock increase neutrophil adhesion molecule expression and pulmonary leukosequestration. J Trauma 55:727-733, 2003. (Pubitemid 37322616)
32. Zallen G, Moore E, Johnson J, Tamura D, Ciesla D, Silliman C: Posthemorrhagic shock mesenteric lymph primes circulating neutrophils and provokes lung injury. J Surg Res 83:83-88, 1999. (Pubitemid 29391611)
33. Deitch EA, Forsythe R, Anjaria D, Livingston D, Lu Q, Xu D, Redl H: The role of lymph factors in lung injury, bone marrow suppression, and endothelial cell dysfunction in a primate model of trauma-hemorrhagic shock. Shock 22:221-228, 2004. (Pubitemid 39468986)
34. Deitch EA, Feketeova E, Adams J, Forsythe R, Xu D, Itagaki K, Redl H: Lymph from a primate baboon trauma hemorrhagic shock model activates human neutrophils. Shock 25:460-463, 2006.
35. Dayal S, Hauser C, Feketeova E, Fekete Z, Adams J, Lu Q, Xu D, Zaets S, Deitch EA: Shock mesenteric lymph-induced rat polymorphonuclear neutrophil activation and endothelial cell injury is mediated by aqueous factors. J Trauma 52:1048-1055, 2002. (Pubitemid 34664370)
36. Deitch EA, Feketeova E, Lu Q, Zaets S, Berezina T, Machiedo G, Hauser C, Livingston D, Xu D: Resistance of the female, as opposed to the male, intestine to ischemia reperfusion-mediated injury is associated with increased resistance to gut-induced distant organ injury. Shock 29:78-83, 2008.
37. Davidson MT, Deitch EA, Lu Q, Osband A, Feketeova E, Németh ZH, Haskó G, Xu DZ: A study of the biologic activity of trauma-hemorrhagic shock mesenteric lymph over time and the relative role of cytokines. Surgery 136: 32-41, 2004. (Pubitemid 38834217)
38. Levy RM, Prince JM, Yang R, Mollen KP, Liao H, Watson GA, Fink MP, Vodovotz Y, Billiar TR: Systemic inflammation and remote organ damage following bilateral femur fracture requires toll-like receptor 4. Am J Physiol Regul Integr Comp Physiol 291:R970-R976, 2006. (Pubitemid 44498437)
39. Mollen KP, Levy RM, Prince JM, Hoffman RA, Scott MJ, Kaczorowski DJ, Vallabhaneni R, Vodovotz Y, Billiar TR: Systemic inflammation and end organ damage following trauma involves functional TLR4 signaling in both bone marrow-derived cells and parenchymal cells. J Leukoc Biol 83:80-88, 2008.
40. Breslin J, Wu M, Guo M, Reynoso R, Yuan S: Toll-like receptor 4 contributes to microvascular inflammation and barrier dysfunction in thermal injury. Shock 29:197-216, 2008.
41. Feng Y, Zhao H, Xu X, Buys ES, Raher MJ, Bopassa JC, Thibault H, Scherrer-Crosbie M, Schmidt U, Chao W: Innate immune adaptor MyD88 mediates PMN recruitment and myocardial injury after ischemia-reperfusion in mice. Am J Physiol Heart Circ Physiol 295:H1311-H1318, 2008.
42. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, van Loo G, Ermolaeva M, Veldhuizen R, Leung YHC, Wang H, et al.: Identification of oxidative stress and toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133:235-249, 2008. (Pubitemid 351512299)
43. Simpson R, Alon R, Kobzik L, Valeri CR, Shepro D, Hechtman HB: Neutrophil and non-neutrophil-mediated injury in intestinal ischemia-reperfusion. Ann Surg 218:444-454, 1993. (Pubitemid 23312398)
44. Hill J, Lindsay T, Valeri CR, Shepro D, Hechtman HB: A CD18 antibody prevents lung injury but not hypotension after intestinal ischemia-reperfusion. J Appl Physiol 74:659-664, 1993. (Pubitemid 23078158)
45. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE: Use of ly6gspecific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83:64-70, 2008.
46. Adams J, Charles A., Xu DZ, Lu Q, Deitch EA: Factors larger than 100 kd in post-hemorrhagic shock mesenteric lymph are toxic for endothelial cells. Surgery 129:351-363, 2001.
47. Kaiser V, Sifri Z, Dikdan G, Berezina T, Zaets S, Lu Q, Xu D, Deitch EA: Trauma-hemorrhagic shock mesenteric lymph from rat contains a modified form of albumin that is implicated in endothelial cell toxicity. Shock 23:417-425, 2005. (Pubitemid 40571664)
48. Gonzalez R, Moore E, Biffl W, Ciesla D, Silliman C: The lipid fraction of post-hemorrhagic shock mesenteric lymph (PHSML) inhibits neutrophil apoptosis and enhances cytotoxic potential. Shock 14:404-448, 2002.
49. Deitch EA, Qin X, Sheth S, Tiesi G, Palange D, Dong W, Lu Q, Xu D, Feketeova E, Feinman R: Anticoagulants influence the in vitro activity and composition of shock lymph but not its in vivo activity. Shock 36:177-183, 2011.
50. Cai B, Deitch EA, Grande D, Ulloa L: Anti-inflammatory resuscitation improves survival in hemorrhage with trauma. J Trauma 66:1632-1640, 2009.
51. Peltz E, Moore E, Eckels P, Damle S, Tsuruta Y, Johnson J, Sauaia A, Silliman C, Banerjee A, Abraham E: HMGB1 is markedly elevated within 6 hours of mechanical trauma in humans. Shock 32:17-22, 2009.
52. Peltz ED, Moore EE, Zurawel AA, Jordan JR, Damle SS, Redzic JS, Masuno T, Eun J, Hansen KC, Banerjee A: Proteome and system ontology of hemorrhagic shock: exploring early constitutive changes in postshock mesenteric lymph. Surgery 146:347-357, 2009.
53. Fang J, Shih L, Yuan K, Fang K, Hwang T, Hsieh S: Proteomic analysis of posthemorrhagic shock mesenteric lymph. Shock 34:291-298, 2010.
54. Mittal A, Middleditch M, Ruggiero K, Loveday B, Delahunt B, Jü llig M, Cooper G, Windsor J, Phillips A: Changes in the mesenteric lymph proteome induced by hemorrhagic shock. Shock 34:140-149, 2010.
55. Mittal A, Phillips A, Middleditch M, Ruggiero K, Loveday B, Delahunt B, Cooper G, Windsor J: The proteome of mesenteric lymph during acute pancreatitis and implications for treatment. JOP 10:130-142, 2009.
56. Dzieciatkowska M, Wohlauer M, Moore E, Damle S, Peltz E, Campsen J, Kelher M, Silliman C, Banerjee A, Hansen K: Proteomic analysis of human mesenteric lymph. Shock 35:331-338, 2011.
57. De Maio A: Extracellular heat shock proteins, cellular export vesicles, and the stress observation system: a form of communication during injury, infection, and cell damage. Cell Stress Chaperones 16:235-249, 2011.