Bacterial flagellin triggers cardiac innate immune responses and acute contractile dysfunction

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-13

  Rolli, Joelle ^a   Rosenblatt Velin, Nathalie ^a   Li, Jianhui ^a,c   Loukili, Noureddine ^a   Levrand, Sandra ^a   Pacher, Pal ^b   Waeber, Bernard ^a   Feihl, François ^a   Ruchat, Patrick ^a   Liaudet, Lucas ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN MIP 2; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HEART CONTRACTION; HEART DILATATION; HEART EJECTION FRACTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MALE; MOUSE; MYOCARDIAL DISEASE; MYOCARDITIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SYSTOLE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL LINE; GENETICS; HEART; HEART MUSCLE; IMMUNOLOGY; MICROBIOLOGY; MOUSE MUTANT; MYOBLAST; PATHOPHYSIOLOGY; SALMONELLA; SALMONELLOSIS; SEPTIC SHOCK;

BACTERIA (MICROORGANISMS); MAMMALIA; MUS; RATTUS; RODENTIA;

ANIMALS; CELL LINE; CELLS, CULTURED; CYTOKINES; FLAGELLIN; HEART; HUMANS; IMMUNITY, INNATE; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MYOBLASTS, CARDIAC; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; NF-KAPPA B; RATS; SALMONELLA; SALMONELLA INFECTIONS; SHOCK, SEPTIC; TOLL-LIKE RECEPTOR 5;

EID: 77958525928     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012687     Document Type: Article

References (38)

1. Russell JA (2006) Management of sepsis. N Engl J Med 355: 1699-1713.
2. Trinchieri G, Sher A (2007) Cooperation of Toll-like receptor signals in innate immune defence. Nat Rev Immunol 7: 179-190.
3. Dowling D, Hamilton CM, O'Neill SM (2008) A comparative analysis of cytokine responses, cell surface marker expression and MAPKs in DCs matured with LPS compared with a panel of TLR ligands. Cytokine 41: 254-262.
4. Zhang Z, Reenstra W, Weiner DJ, Louboutin JP, Wilson JM (2007) The p38 mitogen-activated protein kinase signaling pathway is coupled to Toll-like receptor 5 to mediate gene regulation in response to Pseudomonas aeruginosa infection in human airway epithelial cells. Infect Immun 75: 5985-5992.
5. Parker MM, Shelhamer JH, Bacharach SL, Green MV, Natanson C, et al. (1984) Profound but reversible myocardial depression in patients with septic shock. Ann Intern Med 100: 483-490.
6. Rudiger A, Singer M (2007) Mechanisms of sepsis-induced cardiac dysfunction. Crit Care Med 35: 1599-1608.
7. Merx MW, Weber C (2007) Sepsis and the heart. Circulation 116: 793-802.
8. Flierl MA, Rittirsch D, Huber-Lang MS, Sarma JV, Ward PA (2008) Molecular events in the cardiomyopathy of sepsis. Mol Med 14: 327-336.
9. Knuefermann P, Nemoto S, Misra A, Nozaki N, Defreitas G, et al. (2002) CD14-deficient mice are protected against lipopolysaccharide-induced cardiac inflammation and left ventricular dysfunction. Circulation 106: 2608-2615.
10. Nemoto S, Vallejo JG, Knuefermann P, Misra A, Defreitas G, et al. (2002) Escherichia coli LPS-induced LV dysfunction: role of toll-like receptor-4 in the adult heart. Am J Physiol Heart Circ Physiol 282: H2316-2323.
11. Constable PD (1999) Acute endotoxemia increases left ventricular contractility and diastolic stiffness in calves. Shock 12: 391-401.
12. Pinsky MR, Rico P (2000) Cardiac contractility is not depressed in early canine endotoxic shock. Am J Respir Crit Care Med 161: 1087-1093.
13. Eaves-Pyles T, Murthy K, Liaudet L, Virag L, Ross G, et al. (2001) Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J Immunol 166: 1248-1260.
14. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
15. Andersen-Nissen E, Hawn TR, Smith KD, Nachman A, Lampano AE, et al. (2007) Cutting edge: Tlr5-/- mice are more susceptible to Escherichia coli urinary tract infection. J Immunol 178: 4717-4720.
16. Feuillet V, Medjane S, Mondor I, Demaria O, Pagni PP, et al. (2006) Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci U S A 103: 12487-12492.
17. Liaudet L, Murthy KG, Mabley JG, Pacher P, Soriano FG, et al. (2002) Comparison of inflammation, organ damage, and oxidant stress induced by Salmonella enterica serovar Muenchen flagellin and serovar Enteritidis lipopolysaccharide. Infect Immun 70: 192-198.
18. Liaudet L, Szabo C, Evgenov OV, Murthy KG, Pacher P, et al. (2003) Flagellin from gram-negative bacteria is a potent mediator of acute pulmonary inflammation in sepsis. Shock 19: 131-137.
19. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167: 1882-1885.
20. Loukili N, Rosenblatt-Velin N, Rolli J, Levrand S, Feihl F, et al. (2010) Oxidants positively or negatively regulate nuclear factor kappa B in a context-dependent manner. J Biol Chem 285: 15746-15752.
21. Levrand S, Pesse B, Feihl F, Waeber B, Pacher P, et al. (2005) Peroxynitrite is a potent inhibitor of NF-{kappa}B activation triggered by inflammatory stimuli in cardiac and endothelial cell lines. J Biol Chem 280: 34878-34887.
22. Levrand S, Vannay-Bouchiche C, Pesse B, Pacher P, Feihl F, et al. (2006) Peroxynitrite is a major trigger of cardiomyocyte apoptosis in vitro and in vivo. Free Radic Biol Med 41: 886-895.
23. Murakami Y, Kohsaka H, Kitasato H, Akahoshi T (2007) Lipopolysaccharideinduced up-regulation of triggering receptor expressed on myeloid cells-1 expression on macrophages is regulated by endogenous prostaglandin E2. J Immunol 178: 1144-1150.
24. Knuefermann P, Sakata Y, Baker JS, Huang CH, Sekiguchi K, et al. (2004) Tolllike receptor 2 mediates Staphylococcus aureus-induced myocardial dysfunction and cytokine production in the heart. Circulation 110: 3693-3698.
25. Knuefermann P, Schwederski M, Velten M, Krings P, Ehrentraut H, et al. (2008) Bacterial DNA induces myocardial inflammation and reduces cardiomyocyte contractility: role of Toll-like receptor 9. Cardiovasc Res 78: 26-35.
26. Boyd JH, Mathur S, Wang Y, Bateman RM, Walley KR (2006) Toll-like receptor stimulation in cardiomyoctes decreases contractility and initiates an NF-kappaB dependent inflammatory response. Cardiovasc Res 72: 384-393.
27. Peng T, Lu X, Lei M, Moe GW, Feng Q (2003) Inhibition of p38 MAPK decreases myocardial TNF-alpha expression and improves myocardial function and survival in endotoxemia. Cardiovasc Res 59: 893-900.
28. Yang M, Wu J, Martin CM, Kvietys PR, Rui T (2008) Important role of p38 MAP kinase/NF-{kappa}B signaling pathway in the sepsis-induced conversion of cardiac myocytes to a proinflammatory phenotype. Am J Physiol Heart Circ Physiol 294: H994-H1001.
29. Zhang H, Wang HY, Bassel-Duby R, Maass DL, Johnston WE, et al. (2007) Role of interleukin-6 in cardiac inflammation and dysfunction after burn complicated by sepsis. Am J Physiol Heart Circ Physiol 292: H2408-2416.
30. Neviere RR, Cepinskas G, Madorin WS, Hoque N, Karmazyn M, et al. (1999) LPS pretreatment ameliorates peritonitis-induced myocardial inflammation and dysfunction: role of myocytes. Am J Physiol 277: H885-892.
31. Suga H, Sagawa K (1974) Instantaneous pressure-volume relationships and their ratio in the excised, supported canine left ventricle. Circ Res 35: 117-126.
32. Natanson C, Fink MP, Ballantyne HK, MacVittie TJ, Conklin JJ, et al. (1986) Gram-negative bacteremia produces both severe systolic and diastolic cardiac dysfunction in a canine model that simulates human septic shock. J Clin Invest 78: 259-270.
33. Hescheler J, Meyer R, Plant S, Krautwurst D, Rosenthal W, et al. (1991) Morphological, biochemical, and electrophysiological characterization of a clonal cell (H9c2) line from rat heart. Circ Res 69: 1476-1486.
34. Levrand S, Pacher P, Pesse B, Rolli J, Feihl F, et al. (2007) Homocysteine induces cell death in H9C2 cardiomyocytes through the generation of peroxynitrite. Biochem Biophys Res Commun 359: 445-450.
35. Uematsu S, Jang MH, Chevrier N, Guo Z, Kumagai Y, et al. (2006) Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 7: 868-874.
36. Rosenblatt-Velin N, Lepore MG, Cartoni C, Beermann F, Pedrazzini T (2005) FGF-2 controls the differentiation of resident cardiac precursors into functional cardiomyocytes. J Clin Invest 115: 1724-1733.
37. Waeckel L, Bignon J, Liu JM, Markovits D, Ebrahimian TG, et al. (2006) Tetrapeptide AcSDKP induces postischemic neovascularization through monocyte chemoattractant protein-1 signaling. Arterioscler Thromb Vasc Biol 26: 773-779.
38. Pacher P, Liaudet L, Bai P, Mabley JG, Kaminski PM, et al. (2003) Potent metalloporphyrin peroxynitrite decomposition catalyst protects against the development of doxorubicin-induced cardiac dysfunction. Circulation 107: 896-904.