Contribution of increased ISG15, ISGylation and deregulated type i IFN signaling in Usp18 mutant mice during the course of bacterial infections

Genes and Immunity

Volumn 15, Issue 5, 2014, Pages 282-292

  Dauphinee, S M ^a   Richer, E ^a   Eva, M M ^a   McIntosh, F ^b   Paquet, M ^c   Dangoor, D ^d   Burkart, C ^d   Zhang, D E ^e   Gruenheid, S ^a   Gros, P ^a   Behr, M ^a   Malo, D ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; ISG15 PROTEIN; PEPTIDASE; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN SPECIFIC PEPTIDASE 18; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; PROTEINASE; CYTOKINE; G1P2 PROTEIN, MOUSE; UBIQUITIN THIOLESTERASE; USP18 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BACTERIAL IMMUNITY; BACTERIAL LOAD; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FEMALE; GENE CONTROL; GENETIC SUSCEPTIBILITY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOREGULATION; INFECTION SENSITIVITY; LUNG; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SIGNAL TRANSDUCTION; SPLEEN; ANIMAL CELL; BACTERIAL INFECTION; GENE; GENE EXPRESSION REGULATION; INFLAMMATION; ISG15 GENE; MUTANT MOUSE STRAIN; SURVIVAL; USP18 GENE; ANIMAL; C57BL MOUSE; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; MYCOBACTERIOSIS; PATHOLOGY;

ANIMALS; AUTOPHAGY; CYTOKINES; INTERFERON TYPE I; INTERLEUKIN-17; INTERLEUKIN-1BETA; LUNG; MICE; MICE, INBRED C57BL; MUTATION; MYCOBACTERIUM INFECTIONS; SALMONELLA INFECTIONS; SIGNAL TRANSDUCTION; SPLEEN; UBIQUITIN THIOLESTERASE; UBIQUITINS;

EID: 84905049001     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2014.17     Document Type: Article

References (56)

1. Crump JA, Mintz ED. Global trends in typhoid and paratyphoid fever. Clin Infect Dis 2010; 50: 241-246.
2. Vidal SM, Malo D, Marquis JF, Gros P. Forward genetic dissection of immunity to infection in the mouse. Annu Rev Immunol 2008; 26: 81-132.
3. Richer E, Prendergast C, Zhang DE, Qureshi ST, Vidal SM, Malo D. N-ethyl-N-nitrosourea-induced mutation in ubiquitin-specific peptidase 18 causes hyper-activation of IFN-alphabeta signaling and suppresses STAT4-induced IFN-gamma production, resulting in increased susceptibility to Salmonella typhimurium. J Immunol 2010; 185: 3593-3601.
4. Malakhova OA, Kim KI, Luo JK, Zou W, Kumar KG, Fuchs SY et al. UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J 2006; 25: 2358-2367.
5. Kim KI, Yan M, Malakhova O, Luo JK, Shen MF, Zou W et al. Ube1L and protein ISGylation are not essential for alpha/beta interferon signaling. Mol Cell Biol 2006; 26: 472-479.
6. Trinchieri G. Type I interferon: friend or foe? J Exp Med 2010; 207: 2053-2063.
7. Decker T, Muller M, Stockinger S. The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol. 2005; 5: 675-687.
8. Rayamajhi M, Humann J, Penheiter K, Andreasen K, Lenz LL. Induction of IFN-alphabeta enables Listeria monocytogenes to suppress macrophage activation by IFN-gamma. J Exp Med 2010; 207: 327-337.
9. Dikopoulos N, Bertoletti A, Kroger A, Hauser H, Schirmbeck R, Reimann J. Type I IFN negatively regulates CD8 + T cell responses through IL-10-producing CD4 + T regulatory 1 cells. J Immunol 2005; 174: 99-109.
10. Brzoza-Lewis KL, Hoth JJ, Hiltbold EM. Type I interferon signaling regulates the composition of inflammatory infiltrates upon infection with Listeria mono-cytogenes. Cell Immunol 2012; 273: 41-51.
11. Khan R, Sancho-Shimizu V, Prendergast C, Roy MF, Loredo-Osti JC, Malo D. Refinement of the genetics of the host response to Salmonella infection in MOLF/Ei: regulation of type 1 IFN and TRP3 pathways by Ity2. Genes Immun 2012; 13: 175-183.
12. Deretic V. Autophagy in immunity and cell-autonomous defense against intra-cellular microbes. Immunol Rev 2011; 240: 92-104.
13. Perrin AJ, Jiang X, Birmingham CL, So NS, Brumell JH. Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr Biol 2004; 14: 806-811.
14. Birmingham CL, Smith AC, Bakowski MA, Yoshimori T, Brumell JH. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem 2006; 281: 11374-11383.
15. Zheng YT, Shahnazari S, Brech A, Lamark T, Johansen T, Brumell JH. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J Immunol 2009; 183: 5909-5916.
16. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR et al. Phosphor-ylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011; 333: 228-233.
17. Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 2009; 10: 1215-1221.
18. Harris J. Autophagy and cytokines. Cytokine 2011; 56: 140-144.
19. Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem 2002; 277: 9976-9981.
20. Zhang D, Zhang DE. Interferon-stimulated gene 15 and the protein ISGylation system. J Interferon Cytokine Res 2011; 31: 119-130.
21. Roy MF, Malo D. Genetic regulation of host responses to Salmonella infection in mice. Genes Immun 2002; 3: 381-393.
22. Sheehan KC, Lai KS, Dunn GP, Bruce AT, Diamond MS, Heutel JD et al. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J Interferon Cytokine Res 2006; 26: 804-819.
23. Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011; 34: 213-223.
24. Finbloom DS, Winestock KD. IL-10 induces the tyrosine phosphorylation of tyk2 and Jak1 and the differential assembly of STAT1 alpha and STAT3 complexes in human T cells and monocytes. J Immunol 1995; 155: 1079-1090.
25. Park HJ, Lee SJ, Kim SH, Han J, Bae J, Kim SJ et al. IL-10 inhibits the starvation induced autophagy in macrophages via class I phosphatidylinositol 3-kinase (PI3K) pathway. Mol Immunol 2011; 48: 720-727.
26. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K et al. Guidelines for the use and interpretation of assays for monitoring autop-hagy. Autophagy 2012; 8: 445-544.
27. Kageyama S, Omori H, Saitoh T, Sone T, Guan JL, Akira S et al. The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol Biol Cell 2011; 22: 2290-2300.
28. Huang J, Canadien V, Lam GY, Steinberg BE, Dinauer MC, Magalhaes MA et al. Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci USA 2009; 106: 6226-6231.
29. Raupach B, Peuschel SK, Monack DM, Zychlinsky A. Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect Immun 2006; 74: 4922-4926.
30. Lee J, Kim HR, Quinley C, Kim J, Gonzalez-Navajas J, Xavier R et al. Autophagy suppresses interleukin-1beta (IL-1beta) signaling by activation of p62 degradation via lysosomal and proteasomal pathways. J Biol Chem 2012; 287: 4033-4040.
31. Peral de Castro C, Jones SA, Ni Cheallaigh C, Hearnden CA, Williams L, Winter J et al. Autophagy regulates IL-23 secretion and innate T cell responses through effects on IL-1 secretion. J Immunol 2012; 189: 4144-4153.
32. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 2009; 31: 331-341.
33. Kim KI, Malakhova OA, Hoebe K, Yan M, Beutler B, Zhang DE. Enhanced antibacterial potential in UBP43-deficient mice against Salmonella typhimurium infection by up-regulating type I IFN signaling. J Immunol 2005; 175: 847-854.
34. Knight Jr. E, Cordova B. IFN-induced 15-kDa protein is released from human lymphocytes and monocytes. J Immunol 1991; 146: 2280-2284.
35. Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D et al. Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 2012; 337: 1684-1688.
36. D'Cunha J, Knight Jr. E, Haas AL, Truitt RL, Borden EC. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc Natl Acad Sci USA 1996; 93: 211-215.
37. Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol 2012; 13: 954-962.
38. Adib-Conquy M, Cavaillon JM. Compensatory anti-inflammatory response syndrome. Thromb Haemost 2009; 101: 36-47.
39. Dokka S, Shi X, Leonard S, Wang L, Castranova V, Rojanasakul Y. Interleukin-10-mediated inhibition of free radical generation in macrophages. Am J Physiol Lung Cell Mol Physiol 2001; 280: L1196-L1202.
40. Bussolati B, Mariano F, Montrucchio G, Piccoli G, Camussi G. Modulatory effect of interleukin-10 on the production of platelet-activating factor and superoxide anions by human leucocytes. Immunology 1997; 90: 440-447.
41. Novikov A, Cardone M, Thompson R, Shenderov K, Kirschman KD, Mayer-Barber KD et al. Mycobacterium tuberculosis triggers host type I IFN signaling to regulate IL-1beta production in human macrophages. J Immunol 2011; 187: 2540-2547.
42. Mayer-Barber KD, Andrade BB, Barber DL, Hieny S, Feng CG, Caspar P et al. Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 2011; 35: 1023-1034.
43. Mayer-Barber KD, Barber DL, Shenderov K, White SD, Wilson MS, Cheever A et al. Caspase-1 independent IL-1beta production is critical for host resistance to Mycobacterium tuberculosis and does not require TLR signaling in vivo. J Immunol 2010; 184: 3326-3330.
44. Liu X, Li H, Zhong B, Blonska M, Gorjestani S, Yan M et al. USP18 inhibits NF-kappaB and NFAT activation during Th17 differentiation by deubiquitinating the TAK1-TAB1 complex. J Exp Med 2013; 210: 1575-1590.
45. Shi CS, Shenderov K, Huang NN, Kabat J, Abu-Asab M, Fitzgerald KA et al. Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 2012; 13: 255-263.
46. Castillo EF, Dekonenko A, Arko-Mensah J, Mandell MA, Dupont N, Jiang S et al. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc Natl Acad Sci USA 2012; 109: E3168-E3176.
47. Bradfute SB, Castillo EF, Arko-Mensah J, Chauhan S, Jiang S, Mandell M et al. Autophagy as an immune effector against tuberculosis. Curr Opin Microbiol 2013; 16: 355-365.
48. Tattoli I, Sorbara MT, Vuckovic D, Ling A, Soares F, Carneiro LA et al. Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe 2012; 11: 563-575.
49. Mesquita FS, Thomas M, Sachse M, Santos AJ, Figueira R, Holden DW. The Salmonella deubiquitinase SseL inhibits selective autophagy of cytosolic aggregates. PLoS Pathogens 2012; 8: e1002743.
50. Schroeder N, Henry T, de Chastellier C, Zhao W, Guilhon AA, Gorvel JP et al. The virulence protein SopD2 regulates membrane dynamics of Salmonella-containing vacuoles. PLoS Pathogens 2010; 6: e1001002.
51. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140: 313-326.
52. 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: 973-977.
53. 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. J Interferon Cytokine Res 2005; 25: 694-701.
54. 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: 1448-1453.
55. Burkart C, Fan JB, Zhang DE. Two independent mechanisms promote expression of an N-terminal truncated USP18 isoform with higher DeISGylation activity in the nucleus. J Biol Chem 2012; 287: 4883-4893.
56. Kim KI, Giannakopoulos NV, Virgin HW, Zhang DE. Interferon-inducible ubiquitin E2, Ubc8, is a conjugating enzyme for protein ISGylation. Mol Cell Biol 2004; 24: 9592-9600.