The Mechanism for Type I Interferon Induction by Mycobacterium tuberculosis is Bacterial Strain-Dependent

PLoS Pathogens

Volumn 12, Issue 8, 2016, Pages

  Wiens, Kirsten E ^a   Ernst, Joel D ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CELL NUCLEUS DNA; CYCLIC GMP; INTERFERON; MITOCHONDRIAL DNA;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSCRIPTION; HOST PATHOGEN INTERACTION; IMMUNOBLOTTING; MITOCHONDRION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHYLOGENY; PROTEIN INDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUBERCULOSIS; ANIMAL; BIOSYNTHESIS; BONE MARROW CELL; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; MACROPHAGE;

ANIMALS; BONE MARROW CELLS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOBLOTTING; INTERFERON TYPE I; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MYCOBACTERIUM TUBERCULOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUBERCULOSIS;

EID: 84984848329     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005809     Document Type: Article

References (53)

1. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A, Type I interferons in infectious disease. Nature reviews Immunology. 2015;15(2):87–103. doi: 10.1038/nri378725614319.
2. Maertzdorf J, Ota M, Repsilber D, Mollenkopf HJ, Weiner J, Hill PC, et al. Functional correlations of pathogenesis-driven gene expression signatures in tuberculosis. Plos One. 2011;6(10):e26938. Epub 2011/11/03. doi: 10.1371/journal.pone.002693822046420; PubMed Central PMCID: PMC3203931.
3. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature. 2010;466(7309):973–7. Epub 2010/08/21. doi: 10.1038/nature0924720725040; PubMed Central PMCID: PMC3492754.
4. Teles RM, Graeber TG, Krutzik SR, Montoya D, Schenk M, Lee DJ, et al. Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science. 2013;339(6126):1448–53. Epub 2013/03/02. doi: 10.1126/science.123366523449998; PubMed Central PMCID: PMC3653587.
5. Mayer-Barber KD, Andrade BB, Oland SD, Amaral EP, Barber DL, Gonzales J, et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature. 2014;511(7507):99–103. doi: 10.1038/nature1348924990750.
6. Desvignes L, Wolf AJ, Ernst JD, Dynamic roles of type I and type II IFNs in early infection with Mycobacterium tuberculosis. J Immunol. 2012;188(12):6205–15. Epub 2012/05/09. doi: 10.4049/jimmunol.120025522566567; PubMed Central PMCID: PMC3370955.
7. Stanley SA, Johndrow JE, Manzanillo P, Cox JS, The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol. 2007;178(5):3143–52. Epub 2007/02/22. 17312162.
8. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, Brosch R, et al. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS pathogens. 2012;8(2):e1002507. Epub 2012/02/10. doi: 10.1371/journal.ppat.100250722319448; PubMed Central PMCID: PMC3271072.
9. Dey B, Dey RJ, Cheung LS, Pokkali S, Guo H, Lee JH, et al. A bacterial cyclic dinucleotide activates the cytosolic surveillance pathway and mediates innate resistance to tuberculosis. Nature medicine. 2015;21(4):401–6. doi: 10.1038/nm.381325730264; PubMed Central PMCID: PMCPMC4390473.
10. Collins AC, Cai H, Li T, Franco LH, Li XD, Nair VR, et al. Cyclic GMP-AMP Synthase Is an Innate Immune DNA Sensor for Mycobacterium tuberculosis. Cell host & microbe. 2015;17(6):820–8. doi: 10.1016/j.chom.2015.05.00526048137; PubMed Central PMCID: PMCPMC4499468.
11. Wassermann R, Gulen MF, Sala C, Perin SG, Lou Y, Rybniker J, et al. Mycobacterium tuberculosis Differentially Activates cGAS- and Inflammasome-Dependent Intracellular Immune Responses through ESX-1. Cell host & microbe. 2015;17(6):799–810. doi: 10.1016/j.chom.2015.05.00326048138.
12. Watson RO, Bell SL, MacDuff DA, Kimmey JM, Diner EJ, Olivas J, et al. The Cytosolic Sensor cGAS Detects Mycobacterium tuberculosis DNA to Induce Type I Interferons and Activate Autophagy. Cell host & microbe. 2015;17(6):811–9. doi: 10.1016/j.chom.2015.05.00426048136; PubMed Central PMCID: PMCPMC4466081.
13. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS, Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell host & microbe. 2012;11(5):469–80. Epub 2012/05/23. doi: 10.1016/j.chom.2012.03.00722607800.
14. Bold TD, Davis DC, Penberthy KK, Cox LM, Ernst JD, de Jong BC, Impaired fitness of Mycobacterium africanum despite secretion of ESAT-6. The Journal of infectious diseases. 2012;205(6):984–90. Epub 2012/02/04. doi: 10.1093/infdis/jir88322301632; PubMed Central PMCID: PMC3282571.
15. de Jong BC, Hill PC, Aiken A, Awine T, Antonio M, Adetifa IM, et al. Progression to active tuberculosis, but not transmission, varies by Mycobacterium tuberculosis lineage in The Gambia. The Journal of infectious diseases. 2008;198(7):1037–43. Epub 2008/08/16. doi: 10.1086/59150418702608; PubMed Central PMCID: PMC2597014.
16. Steenken W, Jr.Gardner LU, History of H37 strain of tubercle bacillus. Am Rev Tuberc. 1946;54:62–6. 20995860.
17. Kato-Maeda M, Kim EY, Flores L, Jarlsberg LG, Osmond D, Hopewell PC, Differences among sublineages of the East-Asian lineage of Mycobacterium tuberculosis in genotypic clustering. The international journal of tuberculosis and lung disease: the official journal of the International Union against Tuberculosis and Lung Disease. 2010;14(5):538–44. Epub 2010/04/16. 20392345; PubMed Central PMCID: PMC3625672.
18. Kato-Maeda M, Shanley CA, Ackart D, Jarlsberg LG, Shang S, Obregon-Henao A, et al. Beijing sublineages of Mycobacterium tuberculosis differ in pathogenicity in the guinea pig. Clinical and vaccine immunology: CVI. 2012;19(8):1227–37. Epub 2012/06/22. doi: 10.1128/CVI.00250-1222718126; PubMed Central PMCID: PMC3416080.
19. Houben D, Demangel C, van Ingen J, Perez J, Baldeon L, Abdallah AM, et al. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cellular microbiology. 2012;14(8):1287–98. doi: 10.1111/j.1462-5822.2012.01799.x22524898.
20. Wong KW, Jacobs WR, JrCritical role for NLRP3 in necrotic death triggered by Mycobacterium tuberculosis. Cellular microbiology. 2011;13(9):1371–84. Epub 2011/07/12. doi: 10.1111/j.1462-5822.2011.01625.x21740493; PubMed Central PMCID: PMC3257557.
21. Ray K, Bobard A, Danckaert A, Paz-Haftel I, Clair C, Ehsani S, et al. Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time. Cellular microbiology. 2010;12(4):545–56. Epub 2010/01/15. doi: 10.1111/j.1462-5822.2010.01428.x20070313.
22. Wu J, Sun L, Chen X, Du F, Shi H, Chen C, et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science. 2013;339(6121):826–30. doi: 10.1126/science.122996323258412; PubMed Central PMCID: PMCPMC3855410.
23. Sun L, Wu J, Du F, Chen X, Chen ZJ, Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science. 2013;339(6121):786–91. doi: 10.1126/science.123245823258413; PubMed Central PMCID: PMCPMC3863629.
24. Caielli S, Athale S, Domic B, Murat E, Chandra M, Banchereau R, et al. Oxidized mitochondrial nucleoids released by neutrophils drive type I interferon production in human lupus. The Journal of experimental medicine. 2016;213(5):697–713. doi: 10.1084/jem.2015187627091841; PubMed Central PMCID: PMCPMC4854735.
25. Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, Chen S, et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity. 2012;36(3):401–14. doi: 10.1016/j.immuni.2012.01.00922342844; PubMed Central PMCID: PMCPMC3312986.
26. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nature immunology. 2011;12(3):222–30. doi: 10.1038/ni.198021151103; PubMed Central PMCID: PMCPMC3079381.
27. Bronner DN, Abuaita BH, Chen X, Fitzgerald KA, Nunez G, He Y, et al. Endoplasmic Reticulum Stress Activates the Inflammasome via NLRP3- and Caspase-2-Driven Mitochondrial Damage. Immunity. 2015;43(3):451–62. doi: 10.1016/j.immuni.2015.08.00826341399; PubMed Central PMCID: PMCPMC4582788.
28. West AP, Khoury-Hanold W, Staron M, Tal MC, Pineda CM, Lang SM, et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature. 2015;520(7548):553–7. doi: 10.1038/nature1415625642965; PubMed Central PMCID: PMCPMC4409480.
29. Rongvaux A, Jackson R, Harman CC, Li T, West AP, de Zoete MR, et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell. 2014;159(7):1563–77. doi: 10.1016/j.cell.2014.11.03725525875; PubMed Central PMCID: PMCPMC4272443.
30. Lood C, Blanco LP, Purmalek MM, Carmona-Rivera C, De Ravin SS, Smith CK, et al. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nature medicine. 2016;22(2):146–53. doi: 10.1038/nm.402726779811; PubMed Central PMCID: PMCPMC4742415.
31. Carroll EC, Jin L, Mori A, Munoz-Wolf N, Oleszycka E, Moran HB, et al. The Vaccine Adjuvant Chitosan Promotes Cellular Immunity via DNA Sensor cGAS-STING-Dependent Induction of Type I Interferons. Immunity. 2016. doi: 10.1016/j.immuni.2016.02.00426944200.
32. West AP, Shadel GS, Ghosh S, Mitochondria in innate immune responses. Nature reviews Immunology. 2011;11(6):389–402. doi: 10.1038/nri297521597473; PubMed Central PMCID: PMCPMC4281487.
33. Murphy MP, How mitochondria produce reactive oxygen species. Biochem J. 2009;417(1):1–13. doi: 10.1042/BJ2008138619061483; PubMed Central PMCID: PMCPMC2605959.
34. Weinberg SE, Sena LA, Chandel NS, Mitochondria in the regulation of innate and adaptive immunity. Immunity. 2015;42(3):406–17. doi: 10.1016/j.immuni.2015.02.00225786173; PubMed Central PMCID: PMCPMC4365295.
35. Collins LV, Hajizadeh S, Holme E, Jonsson IM, Tarkowski A, Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J Leukoc Biol. 2004;75(6):995–1000. doi: 10.1189/jlb.070332814982943.
36. Murphy MP, Smith RA, Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu Rev Pharmacol Toxicol. 2007;47:629–56. doi: 10.1146/annurev.pharmtox.47.120505.10511017014364.
37. Galluzzi L, Kepp O, Kroemer G, Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol. 2012;13(12):780–8. doi: 10.1038/nrm347923175281.
38. Lee HM, Sugino H, Aoki C, Nishimoto N, Underexpression of mitochondrial-DNA encoded ATP synthesis-related genes and DNA repair genes in systemic lupus erythematosus. Arthritis Res Ther. 2011;13(2):R63. doi: 10.1186/ar331721496236; PubMed Central PMCID: PMCPMC3132058.
39. Lee HT, Lin CS, Chen WS, Liao HT, Tsai CY, Wei YH, Leukocyte mitochondrial DNA alteration in systemic lupus erythematosus and its relevance to the susceptibility to lupus nephritis. Int J Mol Sci. 2012;13(7):8853–68. doi: 10.3390/ijms1307885322942739; PubMed Central PMCID: PMCPMC3430270.
40. Pascual V, Farkas L, Banchereau J, Systemic lupus erythematosus: all roads lead to type I interferons. Curr Opin Immunol. 2006;18(6):676–82. doi: 10.1016/j.coi.2006.09.01417011763.
41. Rudel T, Kepp O, Kozjak-Pavlovic V, Interactions between bacterial pathogens and mitochondrial cell death pathways. Nature reviews Microbiology. 2010;8(10):693–705. doi: 10.1038/nrmicro242120818415.
42. Bentley SD, Comas I, Bryant JM, Walker D, Smith NH, Harris SR, et al. The genome of Mycobacterium africanum West African 2 reveals a lineage-specific locus and genome erosion common to the M. tuberculosis complex. PLoS neglected tropical diseases. 2012;6(2):e1552. Epub 2012/03/06. doi: 10.1371/journal.pntd.000155222389744; PubMed Central PMCID: PMC3289620.
43. Watanabe S, Zimmermann M, Goodwin MB, Sauer U, Barry CE, 3rdBoshoff HI, Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS pathogens. 2011;7(10):e1002287. doi: 10.1371/journal.ppat.100228721998585; PubMed Central PMCID: PMCPMC3188519.
44. Wynosky-Dolfi MA, Snyder AG, Philip NH, Doonan PJ, Poffenberger MC, Avizonis D, et al. Oxidative metabolism enables Salmonella evasion of the NLRP3 inflammasome. The Journal of experimental medicine. 2014;211(4):653–68. doi: 10.1084/jem.2013062724638169; PubMed Central PMCID: PMCPMC3978275.
45. Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, Musser JM, et al. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta. Proc Natl Acad Sci U S A. 2001;98(10):5752–7. Epub 2001/04/26. doi: 10.1073/pnas.09109699811320211; PubMed Central PMCID: PMC33285.
46. Manca C, Tsenova L, Freeman S, Barczak AK, Tovey M, Murray PJ, et al. Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research. 2005;25(11):694–701. Epub 2005/12/02. doi: 10.1089/jir.2005.25.69416318583.
47. Parwati I, van Crevel R, van Soolingen D, Possible underlying mechanisms for successful emergence of the Mycobacterium tuberculosis Beijing genotype strains. The Lancet infectious diseases. 2010;10(2):103–11. doi: 10.1016/S1473-3099(09)70330-520113979.
48. de Jong BC, Antonio M, Gagneux S, Mycobacterium africanum—review of an important cause of human tuberculosis in West Africa. PLoS neglected tropical diseases. 2010;4(9):e744. Epub 2010/10/12. doi: 10.1371/journal.pntd.000074420927191; PubMed Central PMCID: PMC2946903.
49. Winglee K, Manson McGuire A, Maiga M, Abeel T, Shea T, Desjardins CA, et al. Whole Genome Sequencing of Mycobacterium africanum Strains from Mali Provides Insights into the Mechanisms of Geographic Restriction. PLoS neglected tropical diseases. 2016;10(1):e0004332. doi: 10.1371/journal.pntd.000433226751217.
50. Gehre F, Kumar S, Kendall L, Ejo M, Secka O, Ofori-Anyinam B, et al. A Mycobacterial Perspective on Tuberculosis in West Africa: Significant Geographical Variation of M. africanum and Other M. tuberculosis Complex Lineages. PLoS neglected tropical diseases. 2016;10(3):e0004408. doi: 10.1371/journal.pntd.000440826964059.
51. Mayer-Barber K, Andrade BdB, Sher A, Barber DL, Treatment and prevention of diseases mediated by microorganisms via drug-mediated manipulation of the eicosanoid balance. Google Patents; 2014.
52. Holden P, Horton WA, Crude subcellular fractionation of cultured mammalian cell lines. BMC Res Notes. 2009;2:243. doi: 10.1186/1756-0500-2-24320003239; PubMed Central PMCID: PMCPMC2802353.
53. Faurobert M, Pelpoir E, Chaib J, Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues. Methods Mol Biol. 2007;355:9–14. doi: 10.1385/1-59745-227-0:917093297.