The methyltransferase Setdb2 mediates virus-induced susceptibility to bacterial superinfection

Nature Immunology

Volumn 16, Issue 1, 2015, Pages 67-74

  Schliehe, Christopher ^a   Flynn, Elizabeth K ^b,j   Vilagos, Bojan ^a   Richson, Udochuku ^a   Swaminathan, Savitha ^c   Bosnjak, Berislav ^d   Bauer, Lisa ^a   Kandasamy, Richard K ^a   Griesshammer, Isabel M ^a,j   Kosack, Lindsay ^a   Schmitz, Frank ^c   Litvak, Vladimir ^e   Sissons, James ^c   Lercher, Alexander ^a   Bhattacharya, Anannya ^a   Khamina, Kseniya ^a   Trivett, Anna L ^b   Tessarollo, Lino ^b   Mesteri, Ildiko ^f   Hladik, Anastasiya ^a,f   Merkler, Doron ^g,h   Kubicek, Stefan ^a   Knapp, Sylvia ^a,f   Epstein, Michelle M ^d   Symer, David E ^b,i   Aderem, Alan ^c   Bergthaler, Andreas ^a   more..

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b NATIONAL CANCER INSTITUTE   (United States)

^c SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^d Universitatsklinik fur Dermatologie   (Austria)

^e UNIVERSITY OF MASSACHUSETTS   (United States)

^f MEDICAL UNIVERSITY OF VIENNA   (Austria)

^g GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^h UNIVERSITY OF GÖTTINGEN   (Germany)

ⁱ OHIO STATE UNIVERSITY   (United States)

^j GENEDX   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; HISTONE H3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 2; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 10; INTERLEUKIN 6; METHYLTRANSFERASE; PROTEIN SETDB2; STAT1 PROTEIN; UNCLASSIFIED DRUG; CXCL1 PROTEIN, MOUSE; HISTONE LYSINE METHYLTRANSFERASE; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL SUPERINFECTION; CONTROLLED STUDY; DISEASE EXACERBATION; FEMALE; GENE EXPRESSION; GENE REPRESSION; HISTONE METHYLATION; IMMUNOMODULATION; INFECTION SENSITIVITY; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; LUNG ALVEOLUS MACROPHAGE; MOUSE; NEUTROPHILIA; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; VIRUS PNEUMONIA; ANIMAL; C57BL MOUSE; CHEMISTRY; DISEASE PREDISPOSITION; DNA MICROARRAY; ENZYMOLOGY; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; MICROBIOLOGY; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRUS INFECTION; PNEUMONIA; SUPERINFECTION; VIROLOGY;

ANIMALS; CHEMOKINE CXCL1; DISEASE SUSCEPTIBILITY; FEMALE; HISTONE-LYSINE N-METHYLTRANSFERASE; INTERFERON TYPE I; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA; REAL-TIME POLYMERASE CHAIN REACTION; RNA; SPECIFIC PATHOGEN-FREE ORGANISMS; SUPERINFECTION;

EID: 84923304136     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3046     Document Type: Article

References (50)

1. Morens, D.M., Taubenberger, J.K., Fauci, A.S. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J. Infect. Dis. 198, 962-970 (2008).
2. Molinari, N.A. et al. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25, 5086-5096 (2007).
3. van der Sluijs, K.F., van der Poll, T., Lutter, R., Juffermans, N.P., Schultz, M.J. Bench-to-bedside review: bacterial pneumonia with influenza-pathogenesis and clinical implications. Crit. Care 14, 219 (2010).
4. McCullers, J.A. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat. Rev. Microbiol. 12, 252-262 (2014).
5. Kawai, T., Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384 (2010).
6. Taniguchi, T., Ogasawara, K., Takaoka, A., Tanaka, N. IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 19, 623-655 (2001).
7. Sadler, A.J., Williams, B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8, 559-568 (2008).
8. Schoggins, J.W. et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505, 691-695 (2014).
9. Oeckinghaus, A., Ghosh, S. The NF-B family of transcription factors and its regulation. Cold Spring Harb. Perspect. Biol. 1, a000034 (2009).
10. Medzhitov, R., Schneider, D.S., Soares, M.P. Disease tolerance as a defense strategy. Science 335, 936-941 (2012).
11. Litvak, V. et al. A FOXO3-IRF7 gene regulatory circuit limits inflammatory sequelae of antiviral responses. Nature 490, 421-425 (2012).
12. Rouse, B.T., Sehrawat, S. Immunity and immunopathology to viruses: what decides the outcome Nat. Rev. Immunol. 10, 514-526 (2010).
13. Navarini, A.A. et al. Increased susceptibility to bacterial superinfection as a consequence of innate antiviral responses. Proc. Natl. Acad. Sci. USA 103, 15535-15539 (2006).
14. Nakamura, S., Davis, K.M., Weiser, J.N. Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice. J. Clin. Invest. 121, 3657-3665 (2011).
15. Shahangian, A. et al. Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J. Clin. Invest. 119, 1910-1920 (2009).
16. Foster, S.L., Hargreaves, D.C., Medzhitov, R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447, 972-978 (2007).
17. Fang, T.C. et al. Histone H3 lysine 9 di-methylation as an epigenetic signature of the interferon response. J. Exp. Med. 209, 661-669 (2012).
18. Satoh, T. et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol. 11, 936-944 (2010).
19. Allan, R.S. et al. An epigenetic silencing pathway controlling T helper 2 cell lineage commitment. Nature 487, 249-253 (2012).
20. Dillon, S.C., Zhang, X., Trievel, R.C., Cheng, X. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol. 6, 227 (2005).
21. Matsui, T. et al. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464, 927-931 (2010).
22. Ceol, C.J. et al. The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 471, 513-517 (2011).
23. Xu, P.F. et al. Setdb2 restricts dorsal organizer territory and regulates left-right asymmetry through suppressing fgf8 activity. Proc. Natl. Acad. Sci. USA 107, 2521-2526 (2010).
24. Falandry, C. et al. CLLD8/KMT1F is a lysine methyltransferase that is important for chromosome segregation. J. Biol. Chem. 285, 20234-20241 (2010).
25. Hogarth, C.A., Mitchell, D., Evanoff, R., Small, C., Griswold, M. Identification and expression of potential regulators of the mammalian mitotic-to-meiotic transition. Biol. Reprod. 84, 34-42 (2011).
26. Richon, V.M. et al. Chemogenetic analysis of human protein methyltransferases. Chem. Biol. Drug Des. 78, 199-210 (2011).
27. Takaoka, A. et al. Cross talk between interferon-and-/signaling components in caveolar membrane domains. Science 288, 2357-2360 (2000).
28. Black, J.C., Van Rechem, C., Whetstine, J.R. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol. Cell 48, 491-507 (2012).
29. Mantovani, A., Cassatella, M.A., Costantini, C., Jaillon, S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531 (2011).
30. McNamee, L.A., Harmsen, A.G. Both influenza-induced neutrophil dysfunction and neutrophil-independent mechanisms contribute to increased susceptibility to a secondary Streptococcus pneumoniae infection. Infect. Immun. 74, 6707-6721 (2006).
31. Cai, S., Batra, S., Lira, S.A., Kolls, J.K., Jeyaseelan, S. CXCL1 regulates pulmonary host defense to Klebsiella Infection via CXCL2, CXCL5, NF-B, and MAPKs. J. Immunol. 185, 6214-6225 (2010).
32. Levy, D. et al. Lysine methylation of the NF-B subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-B signaling. Nat. Immunol. 12, 29-36 (2011).
33. Zhang, Y. et al. Positional cloning of a quantitative trait locus on chromosome 13q14 that influences immunoglobulin E levels and asthma. Nat. Genet. 34, 181-186 (2003).
34. Ruthenburg, A.J., Li, H., Patel, D.J., Allis, C.D. Multivalent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cell Biol. 8, 983-994 (2007).
35. Marazzi, I. et al. Suppression of the antiviral response by an influenza histone mimic. Nature 483, 428-433 (2012).
36. Nauseef, W.M., Borregaard, N. Neutrophils at work. Nat. Immunol. 15, 602-611 (2014).
37. Raquil, M.A., Anceriz, N., Rouleau, P., Tessier, P.A. Blockade of antimicrobial proteins S100A8 and S100A9 inhibits phagocyte migration to the alveoli in streptococcal pneumonia. J. Immunol. 180, 3366-3374 (2008).
38. Arredouani, M. et al. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J. Exp. Med. 200, 267-272 (2004).
39. Dela Cruz, C.S. et al. Chitinase 3-like-1 promotes Streptococcus pneumoniae killing and augments host tolerance to lung antibacterial responses. Cell Host Microbe 12, 34-46 (2012).
40. Jamieson, A.M. et al. Role of tissue protection in lethal respiratory viral-bacterial coinfection. Science 340, 1230-1234 (2013).
41. Helin, K., Dhanak, D. Chromatin proteins and modifications as drug targets. Nature 502, 480-488 (2013).
42. Müller, U. et al. Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921 (1994).
43. Honda, K. et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434, 772-777 (2005).
44. Durbin, J.E., Hackenmiller, R., Simon, M.C., Levy, D.E. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84, 443-450 (1996).
45. Takeuchi, O. et al. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11, 443-451 (1999).
46. Febbraio, M. et al. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Invest. 105, 1049-1056 (2000).
47. Lee, E.C. et al. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73, 56-65 (2001).
48. Sheehan, K.C. et al. Blocking monoclonal antibodies specific for mouse IFN-/receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J. Interferon Cytokine Res. 26, 804-819 (2006).
49. Kratz, P.A., Bottcher, B., Nassal, M. Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc. Natl. Acad. Sci. USA 96, 1915-1920 (1999).
50. Schebesta, A. et al. Transcription factor Pax5 activates the chromatin of key genes involved in B cell signaling, adhesion, migration, and immune function. Immunity 27, 49-63 (2007).