A toll-like receptor 2 pathway regulates the Ppargc1a/b metabolic co-activators in mice with Staphylococcal aureus sepsis

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Sweeney, Timothy E ^a   Suliman, Hagir B ^a   Hollingsworth, John W ^a   Welty Wolf, Karen E ^a   Piantadosi, Claude A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON RESPONSE FACTOR 3; INTERFERON RESPONSE FACTOR 7; LIVER PROTEIN; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERFERON REPRESSOR PROTEIN, MOUSE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN RECEPTOR; MEMBRANE PROTEIN; PPARGC1A PROTEIN, MOUSE; REPRESSOR PROTEIN; TICAM 1 PROTEIN, MOUSE; TICAM-1 PROTEIN, MOUSE; TIRAP PROTEIN, MOUSE; TIRP PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; INNATE IMMUNITY; LIVER METABOLISM; LIVER MITOCHONDRION; MALE; METABOLIC ACTIVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA GENE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA GENE; PROMOTER REGION; PROTEIN DNA BINDING; SIGNAL TRANSDUCTION; STAPHYLOCOCCAL BACTEREMIA; STAPHYLOCOCCUS AUREUS; ANIMAL; GENETICS; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOGENICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEPSIS; WESTERN BLOTTING;

MUS; STAPHYLOCOCCUS AUREUS;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; FEMALE; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTOR-7; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; PROMOTER REGIONS, GENETIC; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-1; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEPSIS; STAPHYLOCOCCUS AUREUS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TRANS-ACTIVATORS;

EID: 80053151124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025249     Document Type: Article

References (64)

1. Kawai T, Akira S, (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
2. Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen C, et al. (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2: 253-258.
3. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, et al. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412: 346-351.
4. Takeuchi O, Hoshino K, Akira S, (2000) Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol 165: 5392-5396.
5. Fitzgerald KA, Rowe DC, Barnes BJ, Caffrey DR, Visintin A, et al. (2003) LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J Exp Med 198: 1043-1055.
6. Doyle S, Vaidya S, O'Connell R, Dadgostar H, Dempsey P, et al. (2002) IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17: 251-263.
7. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T, (2003) TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 4: 161-167.
8. O'Neill LA, Bowie AG, (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7: 353-364.
9. Barbalat R, Lau L, Locksley RM, Barton GM, (2009) Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 10: 1200-1207.
10. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, et al. (1999) Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11: 443-451.
11. Stenzel W, Soltek S, Sanchez-Ruiz M, Akira S, Miletic H, et al. (2008) Both TLR2 and TLR4 are required for the effective immune response in Staphylococcus aureus-induced experimental murine brain abscess. Am J Pathol 172: 132-145.
12. Murphey ED, Fang G, Sherwood ER, (2008) Pretreatment with the Gram-positive bacterial cell wall molecule peptidoglycan improves bacterial clearance and decreases inflammation and mortality in mice challenged with Staphylococcus aureus. Crit Care Med 36: 3067-3073.
13. Knapp S, von Aulock S, Leendertse M, Haslinger I, Draing C, et al. (2008) Lipoteichoic acid-induced lung inflammation depends on TLR2 and the concerted action of TLR4 and the platelet-activating factor receptor. J Immunol 180: 3478-3484.
14. Inden K, Kaneko J, Miyazato A, Yamamoto N, Mouri S, et al. (2009) Toll-like receptor 4-dependent activation of myeloid dendritic cells by leukocidin of Staphylococcus aureus. Microbes Infect 11: 245-253.
15. Dessing MC, Hirst RA, de Vos AF, van der Poll T, (2009) Role of Toll-like receptors 2 and 4 in pulmonary inflammation and injury induced by pneumolysin in mice. PLoS ONE 4: e7993.
16. Cox KH, Ofek I, Hasty DL, (2007) Enhancement of macrophage stimulation by lipoteichoic acid and the costimulant hemoglobin is dependent on Toll-like receptors 2 and 4. Infect Immun 75: 2638-2641.
17. Lever A, Mackenzie I, (2007) Sepsis: definition, epidemiology, and diagnosis. BMJ 335: 879-883.
18. Crouser ED, (2004) Mitochondrial dysfunction in septic shock and multiple organ dysfunction syndrome. Mitochondrion 4: 729-741.
19. Levy RJ, Vijayasarathy C, Raj NR, Avadhani NG, Deutschman CS, (2004) Competitive and noncompetitive inhibition of myocardial cytochrome C oxidase in sepsis. Shock 21: 110-114.
20. Fink MP, (2001) Cytopathic hypoxia. Mitochondrial dysfunction as mechanism contributing to organ dysfunction in sepsis. Crit Care Clin 17: 219-237.
21. Fredriksson K, Tjader I, Keller P, Petrovic N, Ahlman B, et al. (2008) Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PLoS ONE 3: e3686.
22. Haden DW, Suliman HB, Carraway MS, Welty-Wolf KE, Ali AS, et al. (2007) Mitochondrial biogenesis restores oxidative metabolism during Staphylococcus aureus sepsis. Am J Respir Crit Care Med 176: 768-777.
23. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
24. Wareski P, Vaarmann A, Choubey V, Safiulina D, Liiv J, et al. (2009) PGC-1{alpha} and PGC-1{beta} regulate mitochondrial density in neurons. J Biol Chem 284: 21379-21385.
25. Russell LK, Mansfield CM, Lehman JJ, Kovacs A, Courtois M, et al. (2004) Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ Res 94: 525-533.
26. Scarpulla RC, (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88: 611-638.
27. Koo SH, Satoh H, Herzig S, Lee CH, Hedrick S, et al. (2004) PGC-1 promotes insulin resistance in liver through PPAR-alpha-dependent induction of TRB-3. Nat Med 10: 530-534.
28. Estall JL, Kahn M, Cooper MP, Fisher FM, Wu MK, et al. (2009) Sensitivity of lipid metabolism and insulin signaling to genetic alterations in hepatic peroxisome proliferator-activated receptor-gamma coactivator-1alpha expression. Diabetes 58: 1499-1508.
29. Sweeney TE, Suliman HB, Hollingsworth JW, Piantadosi CA, (2010) Differential regulation of the PGC family of genes in a mouse model of Staphylococcus aureus sepsis. PLoS One 5: e11606.
30. Pierce JW, Schoenleber R, Jesmok G, Best J, Moore SA, et al. (1997) Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem 272: 21096-21103.
31. Dewan MZ, Terashima K, Taruishi M, Hasegawa H, Ito M, et al. (2003) Rapid tumor formation of human T-cell leukemia virus type 1-infected cell lines in novel NOD-SCID/gammac(null) mice: suppression by an inhibitor against NF-kappaB. J Virol 77: 5286-5294.
32. Alvira CM, Abate A, Yang G, Dennery PA, Rabinovitch M, (2007) Nuclear factor-kappaB activation in neonatal mouse lung protects against lipopolysaccharide-induced inflammation. Am J Respir Crit Care Med 175: 805-815.
33. Phelps CB, Sengchanthalangsy LL, Huxford T, Ghosh G, (2000) Mechanism of I kappa B alpha binding to NF-kappa B dimers. J Biol Chem 275: 29840-29846.
34. Miller LS, O'Connell RM, Gutierrez MA, Pietras EM, Shahangian A, et al. (2006) MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus. Immunity 24: 79-91.
35. Kielian T, Phulwani NK, Esen N, Syed MM, Haney AC, et al. (2007) MyD88-dependent signals are essential for the host immune response in experimental brain abscess. J Immunol 178: 4528-4537.
36. Zhang L, Wu L, Hong K, Pagano JS, (2001) Intracellular signaling molecules activated by Epstein-Barr virus for induction of interferon regulatory factor 7. J Virol 75: 12393-12401.
37. Prakash A, Levy DE, (2006) Regulation of IRF7 through cell type-specific protein stability. Biochem Biophys Res Commun 342: 50-56.
38. Sweeney TE, Suliman HB, Hollingsworth JW, Piantadosi CA, (2010) Differential regulation of the PGC family of genes in a mouse model of Staphylococcus aureus sepsis. PLoS ONE 5: e11606.
39. Morin P, Braganca J, Bandu MT, Lin R, Hiscott J, et al. (2002) Preferential binding sites for interferon regulatory factors 3 and 7 involved in interferon-A gene transcription. J Mol Biol 316: 1009-1022.
40. Daffis S, Suthar MS, Szretter KJ, Gale M Jr, Diamond MS, (2009) Induction of IFN-beta and the innate antiviral response in myeloid cells occurs through an IPS-1-dependent signal that does not require IRF-3 and IRF-7. PLoS Pathog 5: e1000607.
41. Demoulins T, Baron ML, Kettaf N, Abdallah A, Sharif-Askari E, et al. (2009) Poly (I:C) induced immune response in lymphoid tissues involves three sequential waves of type I IFN expression. Virology 386: 225-236.
42. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA, (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
43. Oshiumi H, Sasai M, Shida K, Fujita T, Matsumoto M, et al. (2003) TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to toll-like receptor 4 TICAM-1 that induces interferon-beta. J Biol Chem 278: 49751-49762.
44. Kawai T, Takeuchi O, Fujita T, Inoue J, Muhlradt PF, et al. (2001) Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 167: 5887-5894.
45. Jung DY, Lee H, Jung BY, Ock J, Lee MS, et al. (2005) TLR4, but not TLR2, signals autoregulatory apoptosis of cultured microglia: a critical role of IFN-beta as a decision maker. J Immunol 174: 6467-6476.
46. Amit I, Garber M, Chevrier N, Leite AP, Donner Y, et al. (2009) Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 326: 257-263.
47. Zhang H, Tay PN, Cao W, Li W, Lu J, (2002) Integrin-nucleated Toll-like receptor (TLR) dimerization reveals subcellular targeting of TLRs and distinct mechanisms of TLR4 activation and signaling. FEBS Lett 532: 171-176.
48. Lee HK, Dunzendorfer S, Tobias PS, (2004) Cytoplasmic domain-mediated dimerizations of toll-like receptor 4 observed by beta-lactamase enzyme fragment complementation. J Biol Chem 279: 10564-10574.
49. Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, et al. (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115: 2223-2233.
50. Kawai T, Akira S, (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
51. Schagger H, von Jagow G, (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199: 223-231.
52. Wittig I, Braun HP, Schagger H, (2006) Blue native PAGE. Nat Protoc 1: 418-428.
53. Tabeta K, Hoebe K, Janssen EM, Du X, Georgel P, et al. (2006) The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat Immunol 7: 156-164.
54. Kim YM, Brinkmann MM, Paquet ME, Ploegh HL, (2008) UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 452: 234-238.
55. Suliman HB, Sweeney TE, Withers CM, Piantadosi CA, (2010) Co-regulation of nuclear respiratory factor-1 by NF{kappa}B and CREB links LPS-induced inflammation to mitochondrial biogenesis. J Cell Sci 123: 2565-75.
56. Suliman HB, Welty-Wolf KE, Carraway MS, Schwartz DA, Hollingsworth JW, et al. (2005) Toll-like receptor 4 mediates mitochondrial DNA damage and biogenic responses after heat-inactivated E. coli. FASEB J 19: 1531-1533.
57. Lai L, Leone TC, Zechner C, Schaeffer PJ, Kelly SM, et al. (2008) Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev 22: 1948-1961.
58. Dietrich N, Lienenklaus S, Weiss S, Gekara NO, (2010) Murine toll-like receptor 2 activation induces type I interferon responses from endolysosomal compartments. PLoS One 5: e10250.
59. Carre JE, Orban JC, Re L, Felsmann K, Iffert W, et al. (2010) Survival in Critical Illness is Associated with Early Activation of Mitochondrial Biogenesis. Am J Respir Crit Care Med 182: 745-751.
60. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, et al. (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162: 3749-3752.
61. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
62. Yamamoto M, Sato S, Hemmi H, Sanjo H, Uematsu S, et al. (2002) Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420: 324-329.
63. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, et al. (2003) Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301: 640-643.
64. Yamamoto M, Sato S, Hemmi H, Uematsu S, Hoshino K, et al. (2003) TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 4: 1144-1150.