Recurrent Exposure to Subclinical Lipopolysaccharide Increases Mortality and Induces Cardiac Fibrosis in Mice

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Lew, Wilbur Y W ^a   Bayna, Evelyn ^a   Molle, Erminia Dalle ^a   Dalton, Nancy D ^a   Lai, N Chin ^a   Bhargava, Valmik ^a   Mendiola, Vincent ^a   Clopton, Paul ^a   Tang, Tong ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; COLLAGEN IIIALPHA1; GELATINASE A; GELATINASE B; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LOSARTAN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CELL COUNT; BLOOD CHEMISTRY; BLOOD PRESSURE MEASUREMENT; CARDIOVASCULAR MORTALITY; COLLAGEN IALPHA1 GENE; COLLAGEN IIIALPHA1 GENE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; GENE; GENE EXPRESSION; HEART ARRHYTHMIA; HEART HEMODYNAMICS; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE FIBROSIS; HEART RATE; IMMUNOHISTOCHEMISTRY; MALE; MMP2 GENE; MMP9 GENE; MOUSE; MYOFIBROBLAST; NONHUMAN; PERIOSTIN GENE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYSTOLIC BLOOD PRESSURE; TELEMETRY; TIMP1 GENE;

ANIMALS; BIOLOGICAL MARKERS; BLOOD PRESSURE; CELLS, CULTURED; COLLAGEN; COLLAGENASES; FIBROBLASTS; FIBROSIS; HEART RATE; HEMODYNAMICS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MYOCARDIUM; SURVIVAL ANALYSIS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; VENTRICULAR FUNCTION, LEFT;

MUS;

EID: 84876014283     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061057     Document Type: Article

References (39)

1. Beutler B, Rietschel ET, (2003) Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 3: 169-176.
2. Erridge C, Attina T, Spickett CM, Webb DJ, (2007) A high-fat meal induces low-grade endotoxemia: evidence of a novel mechanism of postprandial inflammation. Am J Clin Nutr 86: 1286-1292.
3. Ghanim H, Abuaysheh S, Sia CL, Korzeniewski K, Chaudhuri A, et al. (2009) Increase in plasma endotoxin concentrations and the expression of Toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal: implications for insulin resistance. Diabetes Care 32: 2281-2287.
4. Wiedermann CJ, Kiechl S, Dunzendorfer S, Schratzberger P, Egger G, et al. (1999) Association of endotoxemia with carotid atherosclerosis and cardiovascular disease: prospective results from the Bruneck Study. J Am Coll Cardiol 34: 1975-1981.
5. Selkirk GA, McLellan TM, Wright HE, Rhind SG, (2008) Mild endotoxemia, NF-kappaB translocation, and cytokine increase during exertional heat stress in trained and untrained individuals. Am J Physiol Regul Integr Comp Physiol 295: R611-R623.
6. Pussinen PJ, Tuomisto K, Jousilahti P, Havulinna AS, Sundvall J, et al. (2007) Endotoxemia, immune response to periodontal pathogens, and systemic inflammation associate with incident cardiovascular disease events. Arterioscler Thromb Vasc Biol 27: 1433-1439.
7. Creely SJ, McTernan PG, Kusminski CM, Fisher M, da Silva NF, et al. (2007) Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 292: E740-E747.
8. Niebauer J, Volk HD, Kemp M, Dominguez M, Schumann RR, et al. (1999) Endotoxin and immune activation in chronic heart failure: a prospective cohort study. Lancet 353: 1838-1842.
9. Manco M, Putignani L, Bottazzo GF, (2010) Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev 31: 817-844.
10. Stoll LL, Denning GM, Weintraub NL, (2006) Endotoxin, TLR4 signaling and vascular inflammation: potential therapeutic targets in cardiovascular disease. Curr Pharm Des 12: 4229-4245.
11. Beck JD, Elter JR, Heiss G, Couper D, Mauriello SM, et al. (2001) Relationship of periodontal disease to carotid artery intima-media wall thickness: the atherosclerosis risk in communities (ARIC) study. Arterioscler Thromb Vasc Biol 21: 1816-1822.
12. Desvarieux M, Demmer RT, Rundek T, Boden-Albala B, Jacobs DR Jr, et al. (2005) Periodontal microbiota and carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Circulation 111: 576-582.
13. Amar S, Gokce N, Morgan S, Loukideli M, Van Dyke TE, et al. (2003) Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation. Arterioscler Thromb Vasc Biol 23: 1245-1249.
14. Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, et al. (2007) Treatment of periodontitis and endothelial function. N Engl J Med 356: 911-920.
15. Frantz S, Kobzik L, Kim YD, Fukazawa R, Medzhitov R, et al. (1999) Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest 104: 271-280.
16. Mann DL, (2011) The emerging role of innate immunity in the heart and vascular system: for whom the cell tolls. Circ Res 108: 1133-1145.
17. Yasuda S, Lew WYW, (1997) Lipopolysaccharide depresses cardiac contractility and β-adrenergic contractile response by decreasing myofilament response to Ca2+ in cardiac myocytes. Circ Res 81: 1011-1020.
18. Li HL, Suzuki J, Bayna E, Zhang FM, Dalle ME, et al. (2002) Lipopolysaccharide induces apoptosis in adult rat ventricular myocytes via cardiac AT1 receptors. Am J Physiol Heart Circ Physiol 283: H461-H467.
19. Suzuki J, Bayna E, Li HL, Molle ED, Lew WYW, (2007) Lipopolysaccharide activates calcineurin in ventricular myocytes. J Am Coll Cardiol 49: 491-499.
20. Mehta PK, Griendling KK, (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292: C82-C97.
21. Roth DM, Drumm JD, Bhargava V, Swaney JS, Gao MH, et al. (2003) Cardiac-directed expression of adenylyl cyclase and heart rate regulation. Basic Res Cardiol 98: 380-387.
22. Dobaczewski M, Bujak M, Li N, Gonzalez-Quesada C, Mendoza LH, et al. (2010) Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ Res 107: 418-428.
23. Haudek SB, Xia Y, Huebener P, Lee JM, Carlson S, et al. (2006) Bone marrow-derived fibroblast precursors mediate ischemic cardiomyopathy in mice. Proc Natl Acad Sci U S A 103: 18284-18289.
24. Warren HS, Fitting C, Hoff E, Adib-Conquy M, Beasley-Topliffe L, et al. (2010) Resilience to bacterial infection: difference between species could be due to proteins in serum. J Infect Dis 201: 223-232.
25. Copeland S, Warren HS, Lowry SF, Calvano SE, Remick D, (2005) Acute inflammatory response to endotoxin in mice and humans. Clin Diagn Lab Immunol 12: 60-67.
26. Seki E, De MS, Osterreicher CH, Kluwe J, Osawa Y, et al. (2007) TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 13: 1324-1332.
27. Pulskens WP, Rampanelli E, Teske GJ, Butter LM, Claessen N, et al. (2010) TLR4 promotes fibrosis but attenuates tubular damage in progressive renal injury. J Am Soc Nephrol 21: 1299-1308.
28. Blyszczuk P, Kania G, Dieterle T, Marty RR, Valaperti A, et al. (2009) Myeloid differentiation factor-88/interleukin-1 signaling controls cardiac fibrosis and heart failure progression in inflammatory dilated cardiomyopathy. Circ Res 105: 912-920.
29. Suzuki J, Bayna E, Dalle ME, Lew WYW, (2003) Nicotine inhibits cardiac apoptosis induced by lipopolysaccharide in rats. J Am Coll Cardiol 41: 482-488.
30. Sciarretta S, Paneni F, Palano F, Chin D, Tocci G, et al. (2009) Role of the renin-angiotensin-aldosterone system and inflammatory processes in the development and progression of diastolic dysfunction. Clin Sci (Lond) 116: 467-477.
31. Brown RD, Ambler SK, Mitchell MD, Long CS, (2005) The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol 45: 657-687.
32. Spinale FG, (2007) Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev 87: 1285-1342.
33. Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, et al. (2007) Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 101: 313-321.
34. O'Reilly S, Ciechomska M, Cant R, Hugle T, van Laar JM, (2012) Interleukin-6, its role in fibrosing conditions. Cytokine Growth Factor Rev 23: 99-107.
35. Melendez GC, McLarty JL, Levick SP, Du Y, Janicki JS, et al. (2010) Interleukin 6 mediates myocardial fibrosis, concentric hypertrophy, and diastolic dysfunction in rats. Hypertension 56: 225-231.
36. Amar J, Burcelin R, Ruidavets JB, Cani PD, Fauvel J, et al. (2008) Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr 87: 1219-1223.
37. Mehta NN, McGillicuddy FC, Anderson PD, Hinkle CC, Shah R, et al. (2010) Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 59: 172-181.
38. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, et al. (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772.
39. Geerts SO, Nys M, De MP, Charpentier J, Albert A, et al. (2002) Systemic release of endotoxins induced by gentle mastication: association with periodontitis severity. J Periodontol 73: 73-78.