Mitochondria: Sensors and mediators of innate immune receptor signaling

Current Opinion in Microbiology

Volumn 16, Issue 3, 2013, Pages 327-338

  Cloonan, Suzanne M ^a   Choi, Augustine M K ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; FETUIN A; INFLAMMASOME; INTERFERON REGULATORY FACTOR 3; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; SYNAPSIN I; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TRIPARTITE MOTIF PROTEIN 5; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN PROTEIN LIGASE E3;

CYTOKINE PRODUCTION; HUMAN; INFLAMMATORY DISEASE; INNATE IMMUNITY; MEDIATOR; MITOCHONDRION; NONHUMAN; REVIEW; SENSOR;

EUKARYOTA;

EID: 84881548201     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2013.05.005     Document Type: Review

References (101)

1. Cloonan S.M., Choi A.M. Mitochondria: commanders of innate immunity and disease?. Curr Opin Immunol 2012, 24:32-40.
2. Youle R.J., van der Bliek A.M. Mitochondrial fission, fusion, and stress. Science 2012, 337:1062-1065.
3. Tannahill G.M., O'Neill L.A.J. The emerging role of metabolic regulation in the functioning of toll-like receptors and the nod-like receptor nlrp3. FEBS Lett 2011, 585:1568-1572.
4. Koshiba T. Mitochondrial-mediated antiviral immunity. Biochim Biophys Acta 2013, 1833:225-232.
5. Tal M.C., Iwasaki A. Mitoxosome: a mitochondrial platform for cross-talk between cellular stress and antiviral signaling. Immunol Rev 2011, 243:215-234.
6. Koshiba T., Yasukawa K., Yanagi Y., Kawabata S. Mitochondrial membrane potential is required for mavs-mediated antiviral signaling. Sci Signal 2011, 4:ra7.
7. Ishikawa H., Barber G.N. Sting is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008, 455:674-678.
8. Castanier C., Garcin D., Vazquez A., Arnoult D. Mitochondrial dynamics regulate the rig-i-like receptor antiviral pathway. EMBO Rep 2010, 11:133-138.
9. Jenkins K., Khoo J.J., Sadler A., Piganis R., Wang D., Borg N.A., Hjerrild K., Gould J., Thomas B.J., Nagley P., Hertzog P.J., et al. Mitochondrially localised mul1 is a novel modulator of antiviral signaling. Immunol Cell Biol 2013, 91:321-330.
10. Tal M.C., Sasai M., Lee H.K., Yordy B., Shadel G.S., Iwasaki A. Absence of autophagy results in reactive oxygen species-dependent amplification of rlr signaling. Proc Natl Acad Sci U S A 2009, 106:2770-2775.
11. Orvedahl A., Sumpter R., Xiao G., Ng A., Zou Z., Tang Y., Narimatsu M., Gilpin C., Sun Q., Roth M., Forst C.V., et al. Image-based genome-wide sirna screen identifies selective autophagy factors. Nature 2011, 480:113-117.
12. Wang Y., Tong X., Ye X. Ndfip1 negatively regulates rig-i-dependent immune signaling by enhancing e3 ligase smurf1-mediated mavs degradation, Journal of immunology. Journal of immunology (Baltimore, Md: 1950) 2012, 189:5304-5313.
13. Krauss S., Zhang C.Y., Lowell B.B. The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 2005, 6:248-261.
14. Gregoire I.P., Richetta C., Meyniel-Schicklin L., Borel S., Pradezynski F., Diaz O., Deloire A., Azocar O., Baguet J., Le Breton M., Mangeot P.E., et al. Irgm is a common target of rna viruses that subvert the autophagy network. PLoS Pathog 2011, 7:e1002422.
15. Lovett D.H., Mahimkar R., Raffai R.L., Cape L., Maklashina E., Cecchini G., Karliner J.S. A novel intracellular isoform of matrix metalloproteinase-2 induced by oxidative stress activates innate immunity. PLoS ONE 2012, 7:e34177.
16. Lin R., Paz S., Hiscott J. Tom70 imports antiviral immunity to the mitochondria. Cell Res 2010, 20:971-973.
17. Moore C.B., Bergstralh D.T., Duncan J.A., Lei Y., Morrison T.E., Zimmermann A.G., Accavitti-Loper M.A., Madden V.J., Sun L., Ye Z., Lich J.D., et al. Nlrx1 is a regulator of mitochondrial antiviral immunity. Nature 2008, 451:573-577.
18. Xu L., Xiao N., Liu F., Ren H., Gu J. Inhibition of rig-i and mda5-dependent antiviral response by gc1qr at mitochondria. Proc Natl Acad Sci U S A 2009, 106:1530-1535.
19. Shi H.X., Liu X., Wang Q., Tang P.P., Liu X.Y., Shan Y.F., Wang C. Mitochondrial ubiquitin ligase march5 promotes tlr7 signaling by attenuating tank action. PLoS Pathog 2011, 7:e1002057.
20. Kondo T., Watanabe M., Hatakeyama S. Trim59 interacts with ECSIT and negatively regulates nf-kappab and irf-3/7-mediated signal pathways. Biochem Biophys Res Commun 2012, 422:501-507.
21. Andreyev A.Y., Fahy E., Guan Z., Kelly S., Li X., McDonald J.G., Milne S., Myers D., Park H., Ryan A., Thompson B.M., et al. Subcellular organelle lipidomics in tlr-4-activated macrophages. J Lipid Res 2010, 51:2785-2797.
22. Sampey B.P., Freemerman A.J., Zhang J., Kuan P.F., Galanko J.A., O'Connell T.M., Ilkayeva O.R., Muehlbauer M.J., Stevens R.D., Newgard C.B., Brauer H.A., et al. Metabolomic profiling reveals mitochondrial-derived lipid biomarkers that drive obesity-associated inflammation. PLoS ONE 2012, 7:e38812.
23. Coletta D.K., Mandarino L.J. Mitochondrial dysfunction and insulin resistance from the outside-in: extracellular matrix, the cytoskeleton, and mitochondria. Am J Physiol Endocrinol Metab 2011, 301:E749-E755.
24. Eguchi K., Manabe I., Oishi-Tanaka Y., Ohsugi M., Kono N., Ogata F., Yagi N., Ohto U., Kimoto M., Miyake K., Tobe K., et al. Saturated fatty acid and tlr signaling link beta cell dysfunction and islet inflammation. Cell Metab 2012, 15:518-533.
25. Wang Z., Liu D., Wang F., Liu S., Zhao S., Ling E.A., Hao A. Saturated fatty acids activate microglia via toll-like receptor 4/nf-kappab signalling. Br J Nutr 2012, 107:229-241.
26. Erridge C., Samani N.J. Saturated fatty acids do not directly stimulate toll-like receptor signaling. Arterioscler Thromb Vasc Biol 2009, 29:1944-1949.
27. Schaeffler A., Gross P., Buettner R., Bollheimer C., Buechler C., Neumeier M., Kopp A., Schoelmerich J., Falk W. Fatty acid-induced induction of toll-like receptor-4/nuclear factor-kappab pathway in adipocytes links nutritional signalling with innate immunity. Immunology 2009, 126:233-245.
28. Pal D., Dasgupta S., Kundu R., Maitra S., Das G., Mukhopadhyay S., Ray S., Majumdar S.S., Bhattacharya S. Fetuin-a acts as an endogenous ligand of tlr4 to promote lipid-induced insulin resistance. Nat Med 2012, 18:1279-1285.
29. Ahmad S., White C.W., Chang L.Y., Schneider B.K., Allen C.B. Glutamine protects mitochondrial structure and function in oxygen toxicity. Am J Physiol Lung Cell Mol Physiol 2001, 280:L779-L791.
30. Kessel A., Toubi E., Pavlotzky E., Mogilner J., Coran A.G., Lurie M., Karry R., Sukhotnik I. Treatment with glutamine is associated with down-regulation of toll-like receptor-4 and myeloid differentiation factor 88 expression and decrease in intestinal mucosal injury caused by lipopolysaccharide endotoxaemia in a rat. Clin Exp Immunol 2008, 151:341-347.
31. Hu Y.M., Pai M.H., Yeh C.L., Hou Y.C., Yeh S.L. Glutamine administration ameliorates sepsis-induced kidney injury by downregulating the high-mobility group box protein-1-mediated pathway in mice. Am J Physiol Renal Physiol 2012, 302:F150-F158.
32. Hou Y.C., Chu C.C., Ko T.L., Yeh C.L., Yeh S.L. Effects of alanyl-glutamine dipeptide on the expression of colon-inflammatory mediators during the recovery phase of colitis induced by dextran sulfate sodium. Eur J Nutr 2013, 52:1089-1098.
33. Den Hond E., Hiele M., Peeters M., Ghoos Y., Rutgeerts P. Effect of long-term oral glutamine supplements on small intestinal permeability in patients with crohn's disease. JPEN J Parenter Enteral Nutr 1999, 23:7-11.
34. Benjamin J., Makharia G., Ahuja V., Anand Rajan K.D., Kalaivani M., Gupta S.D., Joshi Y.K. Glutamine and whey protein improve intestinal permeability and morphology in patients with crohn's disease: a randomized controlled trial. Dig Dis Sci 2012, 57:1000-1012.
35. Perez-Barcena J., Crespi C., Regueiro V., Marse P., Raurich J.M., Ibanez J., Garcia de Lorenzo-Mateos A., Bengoechea J.A. Lack of effect of glutamine administration to boost the innate immune system response in trauma patients in the intensive care unit. Crit Care 2010, 14:R233.
36. Slotwinski R., Slotwinska S., Kedziora S., Balan B.J. Innate immunity signaling pathways: Links between immunonutrition and responses to sepsis. Arch Immunol Ther Exp (Warsz) 2011, 59:139-150.
37. Garedew A., Henderson S.O., Moncada S. Activated macrophages utilize glycolytic atp to maintain mitochondrial membrane potential and prevent apoptotic cell death. Cell Death Differ 2010, 17:1540-1550.
38. Infantino V., Convertini P., Cucci L., Panaro M.A., Di Noia M.A., Calvello R., Palmieri F., Iacobazzi V. The mitochondrial citrate carrier: a new player in inflammation. Biochem J 2011, 438:433-436.
39. Bauerfeld C.P., Rastogi R., Pirockinaite G., Lee I., Huttemann M., Monks B., Birnbaum M.J., Franchi L., Nunez G., Samavati L. Tlr4-mediated akt activation is myd88/trif dependent and critical for induction of oxidative phosphorylation and mitochondrial transcription factor a in murine macrophages. Journal of immunology (Baltimore, Md: 1950) 2012, 188:2847-2857.
40. Tannahill G.M.C.A., Adamik J., Palsson-McDermott E.M., McGettrick A.F., Goel G.F.C., Bernard N.J., Kelly B., Foley N.H., Zheng L., Gardet A., Tong Z., Jany S.S.C.S., Haneklaus M., Caffery B.E., Pierce K., Walmsley S., Beasley F.C., Cummins E.N.V., Whyte M., Taylor C.T., Lin H., Masters S.L., Gottlieb E., Kelly V.C.C., Auron P.E., Xavier R.J., O'Neill L.A.J. Succinate is a danger signal that induces il-1β via hif-1α. Nature 2013, 496:238-242.
41. Djafarzadeh S., Vuda M., Takala J., Ochs M., Jakob S.M. Toll-like receptor-3-induced mitochondrial dysfunction in cultured human hepatocytes. Mitochondrion 2011, 11:83-88.
42. Panneerselvam P., Singh L.P., Selvarajan V., Chng W.J., Ng S.B., Tan N.S., Ho B., Chen J., Ding J.L. T-cell death following immune activation is mediated by mitochondria-localized sarm. Cell Death Differ 2013, 20:478-489.
43. Piantadosi C.A., Suliman H.B. Transcriptional control of mitochondrial biogenesis and its interface with inflammatory processes. Biochim Biophys Acta 2012, 1820:532-541.
44. Richardson W.M., Sodhi C.P., Russo A., Siggers R.H., Afrazi A., Gribar S.C., Neal M.D., Dai S., Prindle T., Branca M., Ma C., et al. Nucleotide-binding oligomerization domain-2 inhibits toll-like receptor-4 signaling in the intestinal epithelium. Gastroenterology 2010, 139:904-917. 917 e901-906.
45. Nakahira K., Haspel J.A., Rathinam V.A., Lee S.J., Dolinay T., Lam H.C., Englert J.A., Rabinovitch M., Cernadas M., Kim H.P., Fitzgerald K.A., et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the nalp3 inflammasome. Nat Immunol 2011, 12:222-230.
46. Subramanian N., Natarajan K., Clatworthy M.R., Wang Z., Germain R.N. The adaptor mavs promotes nlrp3 mitochondrial localization and inflammasome activation. Cell 2013, 153:348-361.
47. Misawa T., Takahama M., Kozaki T., Lee H., Zou J., Saitoh T., Akira S. Microtubule-driven spatial arrangement of mitochondria promotes activation of the nlrp3 inflammasome. Nat Immunol 2013, 14:454-460.
48. Juliana C., Fernandes-Alnemri T., Kang S., Farias A., Qin F., Alnemri E.S. Non-transcriptional priming and deubiquitination regulate nlrp3 inflammasome activation. J Biol Chem 2012, 287:36617-36622.
49. Zhou R., Yazdi A.S., Menu P., Tschopp J. A role for mitochondria in nlrp3 inflammasome activation. Nature 2011, 469:221-225.
50. Zhou R., Tardivel A., Thorens B., Choi I., Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 2010, 11:136-140.
51. Akundi R.S., Huang Z., Eason J., Pandya J.D., Zhi L., Cass W.A., Sullivan P.G., Bueler H. Increased mitochondrial calcium sensitivity and abnormal expression of innate immunity genes precede dopaminergic defects in pink1-deficient mice. PLoS ONE 2011, 6:e16038.
52. Lei Y., Wen H., Yu Y., Taxman D.J., Zhang L., Widman D.G., Swanson K.V., Wen K.W., Damania B., Moore C.B., Giguere P.M., et al. The mitochondrial proteins nlrx1 and tufm form a complex that regulates type i interferon and autophagy. Immunity 2012, 36:933-946.
53. Reynolds C.M., McGillicuddy F.C., Harford K.A., Finucane O.M., Mills K.H., Roche H.M. Dietary saturated fatty acids prime the nlrp3 inflammasome via tlr4 in dendritic cells-implications for diet-induced insulin resistance. Mol Nutr Food Res 2012, 56:1212-1222.
54. Wen H., Gris D., Lei Y., Jha S., Zhang L., Huang M.T., Brickey W.J., Ting J.P. Fatty acid-induced nlrp3-asc inflammasome activation interferes with insulin signaling. Nat Immunol 2011, 12:408-415.
55. Hu Q.H., Zhang X., Pan Y., Li Y.C., Kong L.D. Allopurinol, quercetin and rutin ameliorate renal nlrp3 inflammasome activation and lipid accumulation in fructose-fed rats. Biochem Pharmacol 2012, 84:113-125.
56. Lee G.S., Subramanian N., Kim A.I., Aksentijevich I., Goldbach-Mansky R., Sacks D.B., Germain R.N., Kastner D.L., Chae J.J. The calcium-sensing receptor regulates the nlrp3 inflammasome through ca2+ and camp. Nature 2012, 492:123-127.
57. Shimada K., Crother T.R., Karlin J., Dagvadorj J., Chiba N., Chen S., Ramanujan V.K., Wolf A.J., Vergnes L., Ojcius D.M., Rentsendorj A., et al. Oxidized mitochondrial DNA activates the nlrp3 inflammasome during apoptosis. Immunity 2012, 36:401-414.
58. Pelletier M., Lepow T.S., Billingham L.K., Murphy M.P., Siegel R.M. New tricks from an old dog: mitochondrial redox signaling in cellular inflammation. Semin Immunol 2012, 24:384-392.
59. Lenaz G. The mitochondrial production of reactive oxygen species: Mechanisms and implications in human pathology. IUBMB Life 2001, 52:159-164.
60. Gonzalez-Dosal R., Horan K.A., Paludan S.R. Mitochondria-derived reactive oxygen species negatively regulates immune innate signaling pathways triggered by a DNA virus, but not by an rna virus. Biochem Biophys Res Commun 2012, 418:806-810.
61. Maitra U., Deng H., Glaros T., Baker B., Capelluto D.G., Li Z., Li L. Molecular mechanisms responsible for the selective and low-grade induction of proinflammatory mediators in murine macrophages by lipopolysaccharide. Journal of immunology (Baltimore, Md: 1950) 2012, 189:1014-1023.
62. Murakami T., Ockinger J., Yu J., Byles V., McColl A., Hofer A.M., Horng T. Critical role for calcium mobilization in activation of the nlrp3 inflammasome. Proc Natl Acad Sci U S A 2012, 109:11282-11287.
63. Givvimani S., Munjal C., Tyagi N., Sen U., Metreveli N., Tyagi S.C. Mitochondrial division/mitophagy inhibitor (mdivi) ameliorates pressure overload induced heart failure. PLoS ONE 2012, 7:e32388.
64. Lopez-Armada M.J., Riveiro-Naveira R.R., Vaamonde-Garcia C., Valcarcel-Ares M.N. Mitochondrial dysfunction and the inflammatory response. Mitochondrion 2013, 13:106-118.
65. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., Akira S. Ips-1, an adaptor triggering rig-i- and mda5-mediated type i interferon induction. Nat Immunol 2005, 6:981-988.
66. Csak T., Dolganiuc A., Kodys K., Nath B., Petrasek J., Bala S., Lippai D., Szabo G. Mitochondrial antiviral signaling protein defect links impaired antiviral response and liver injury in steatohepatitis in mice. Hepatology 2011, 53:1917-1931.
67. West A.P., Shadel G.S., Ghosh S. Mitochondria in innate immune responses. Nat Rev Immunol 2011, 11:389-402.
68. Deng L., Dai P., Parikh T., Cao H., Bhoj V., Sun Q., Chen Z., Merghoub T., Houghton A., Shuman S. Vaccinia virus subverts a mitochondrial antiviral signaling protein-dependent innate immune response in keratinocytes through its double-stranded rna binding protein, e3. J Virol 2008, 82:10735-10746.
69. Bhoj V.G., Sun Q., Bhoj E.J., Somers C., Chen X., Torres J.P., Mejias A., Gomez A.M., Jafri H., Ramilo O., Chen Z.J. Mavs and myd88 are essential for innate immunity but not cytotoxic t lymphocyte response against respiratory syncytial virus. Proc Natl Acad Sci U S A 2008, 105:14046-14051.
70. Dong X., Feng P. Murine gamma herpesvirus 68 hijacks mavs and ikkbeta to abrogate nfkappab activation and antiviral cytokine production. PLoS Pathog 2011, 7:e1002336.
71. Pothlichet J., Niewold T.B., Vitour D., Solhonne B., Crow M.K., Si-Tahar M. A loss-of-function variant of the antiviral molecule mavs is associated with a subset of systemic lupus patients. EMBO Mol Med 2011, 3:142-152.
72. Li X.D., Chiu Y.H., Ismail A.S., Behrendt C.L., Wight-Carter M., Hooper L.V., Chen Z.J. Mitochondrial antiviral signaling protein (mavs) monitors commensal bacteria and induces an immune response that prevents experimental colitis. Proc Natl Acad Sci U S A 2011, 108:17390-17395.
73. Jin R., Zhu W., Cao S., Chen R., Jin H., Liu Y., Wang S., Wang W., Xiao G. Japanese encephalitis virus activates autophagy as a viral immune evasion strategy. PLoS ONE 2013, 8:e52909.
74. Le Goffic R., Pothlichet J., Vitour D., Fujita T., Meurs E., Chignard M., Si-Tahar M. Cutting edge: influenza a virus activates tlr3-dependent inflammatory and rig-i-dependent antiviral responses in human lung epithelial cells. Journal of Immunology (Baltimore, Md: 1950) 2007, 178:3368-3372.
75. Kang M.J., Lee C.G., Lee J.Y., Dela Cruz C.S., Chen Z.J., Enelow R., Elias J.A. Cigarette smoke selectively enhances viral pamp- and virus-induced pulmonary innate immune and remodeling responses in mice. J Clin Invest 2008, 118:2771-2784.
76. West A.P., Brodsky I.E., Rahner C., Woo D.K., Erdjument-Bromage H., Tempst P., Walsh M.C., Choi Y., Shadel G.S., Ghosh S. Tlr signalling augments macrophage bactericidal activity through mitochondrial ros. Nature 2011, 472:476-480.
77. Petkova D.S., Viret C., Faure M. Irgm in autophagy and viral infections. Front Immunol 2012, 3:426.
78. Zhang Q., Raoof M., Chen Y., Sumi Y., Sursal T., Junger W., Brohi K., Itagaki K., Hauser C.J. Circulating mitochondrial damps cause inflammatory responses to injury. Nature 2010, 464:104-107.
79. Lundberg A.M., Ketelhuth D.F., Johansson M.E., Gerdes N., Liu S., Yamamoto M., Akira S., Hansson G.K. Toll-like receptor 3 and 4 signalling through the trif and tram adaptors in hematopoietic cells promotes atherosclerosis. Cardiovasc Res 2013, [Epub ahead of print].
80. Sobenin I.A., Sazonova M.A., Postnov A.Y., Bobryshev Y.V., Orekhov A.N. Changes of mitochondria in atherosclerosis: possible determinant in the pathogenesis of the disease. Atherosclerosis 2010, 16:76-86.
81. Beltran B., Nos P., Dasi F., Iborra M., Bastida G., Martinez M., O'Connor J.E., Saez G., Moret I., Ponce J. Mitochondrial dysfunction, persistent oxidative damage, and catalase inhibition in immune cells of naive and treated crohn's disease. Inflamm Bowel Dis 2010, 16:76-86.
82. Abarca-Rojano E., Rosas-Medina P., Zamudio-Cortez P., Mondragon-Flores R., Sanchez-Garcia F.J. Mycobacterium tuberculosis virulence correlates with mitochondrial cytochrome c release in infected macrophages. Scand J Immunol 2003, 58:419-427.
83. Moreno-Altamirano M.M., Paredes-Gonzalez I.S., Espitia C., Santiago-Maldonado M., Hernandez-Pando R., Sanchez-Garcia F.J. Bioinformatic identification of mycobacterium tuberculosis proteins likely to target host cell mitochondria: virulence factors?. Microb Inform Exp 2012, 2:9.
84. Perl A., Hanczko R., Doherty E. Assessment of mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Methods Mol Biol 2012, 900:61-89.
85. Baez A., Lo Presti M.S., Rivarola H.W., Mentesana G.G., Pons P., Fretes R., Paglini-Oliva P. Mitochondrial involvement in chronic chagasic cardiomyopathy. Trans R Soc Trop Med Hyg 2011, 105:239-246.
86. Soler-Lopez M., Badiola N., Zanzoni A., Aloy P. Towards alzheimer's root cause: ECSIT as an integrating hub between oxidative stress, inflammation and mitochondrial dysfunction. Hypothetical role of the adapter protein ECSIT in familial and sporadic alzheimer's disease pathogenesis. Bioessays 2012, 34:532-541.
87. Nicholas S.A., Coughlan K., Yasinska I., Lall G.S., Gibbs B.F., Calzolai L., Sumbayev V.V. Dysfunctional mitochondria contain endogenous high-affinity human toll-like receptor 4 (tlr4) ligands and induce tlr4-mediated inflammatory reactions. Int J Biochem Cell Biol 2011, 43:674-681.
88. Heneka M.T., Kummer M.P., Stutz A., Delekate A., Schwartz S., Vieira-Saecker A., Griep A., Axt D., Remus A., Tzeng T.C., Gelpi E., et al. Nlrp3 is activated in alzheimer's disease and contributes to pathology in app/ps1 mice. Nature 2013, 493:674-678.
89. Oka T., Hikoso S., Yamaguchi O., Taneike M., Takeda T., Tamai T., Oyabu J., Murakawa T., Nakayama H., Nishida K., Akira S., et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012, 485:251-255.
90. Goulopoulou S., Matsumoto T., Bomfim G.F., Webb R.C. Toll-like receptor 9 activation: A novel mechanism linking placenta-derived mitochondrial DNA and vascular dysfunction in pre-eclampsia. Clin Sci (Lond) 2012, 123:429-435.
91. Malik A.N., Czajka A. Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction?. Mitochondrion 2012, pii: S1567-7249(12)00232-2.
92. Kaneto H., Katakami N., Matsuhisa M., Matsuoka T.A. Role of reactive oxygen species in the progression of type 2 diabetes and atherosclerosis. Mediators Inflamm 2010, 2010:453892.
93. Puente-Maestu L., Tejedor A., Lazaro A., de Miguel J., Alvarez-Sala L., Gonzalez-Aragoneses F., Simon C., Agusti A. Site of mitochondrial reactive oxygen species production in skeletal muscle of chronic obstructive pulmonary disease and its relationship with exercise oxidative stress. Am J Respir Cell Mol Biol 2012, 47:358-362.
94. Rolo A.P., Teodoro J.S., Palmeira C.M. Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic Biol Med 2012, 52:59-69.
95. Reale M., Pesce M., Priyadarshini M., Kamal M.A., Patruno A. Mitochondria as an easy target to oxidative stress events in parkinson's disease. CNS Neurol Disord Drug Targets 2012, 11:430-438.
96. Tarallo V., Hirano Y., Gelfand B.D., Dridi S., Kerur N., Kim Y., Cho W.G., Kaneko H., Fowler B.J., Bogdanovich S., Albuquerque R.J., et al. Dicer1 loss and alu rna induce age-related macular degeneration via the nlrp3 inflammasome and myd88. Cell 2012, 149:847-859.
97. Emre Y., Hurtaud C., Nubel T., Criscuolo F., Ricquier D., Cassard-Doulcier A.M. Mitochondria contribute to lps-induced mapk activation via uncoupling protein ucp2 in macrophages. Biochem J 2007, 402:271-278.
98. Bulua A.C., Simon A., Maddipati R., Pelletier M., Park H., Kim K.Y., Sack M.N., Kastner D.L., Siegel R.M. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in tnfr1-associated periodic syndrome (traps). J Exp Med 2011, 208:519-533.
99. Machado M.V., Ferreira D.M., Castro R.E., Silvestre A.R., Evangelista T., Coutinho J., Carepa F., Costa A., Rodrigues C.M., Cortez-Pinto H. Liver and muscle in morbid obesity: the interplay of fatty liver and insulin resistance. PLoS ONE 2012, 7:e31738.
100. Zhang Q., Yu J.T., Wang P., Chen W., Wu Z.C., Jiang H., Tan L. Mitochondrial transcription factor a (tfam) polymorphisms and risk of late-onset alzheimer's disease in han chinese. Brain Res 2011, 1368:355-360.
101. Shin D.M., Jeon B.Y., Lee H.M., Jin H.S., Yuk J.M., Song C.H., Lee S.H., Lee Z.W., Cho S.N., Kim J.M., Friedman R.L., et al. Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog 2010, 6:e1001230.