Activation of nucleotide oligomerization domain 2 (NOD2) by human cytomegalovirus initiates innate immune responses and restricts virus Replication

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Kapoor, Arun ^a   Forman, Michael ^b   Arav Boger, Ravit ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CASPASE RECRUITMENT DOMAIN PROTEIN 15; GLYCOPROTEIN B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 8; PHOSPHOTRANSFERASE; PROTEIN RIPK2; UNCLASSIFIED DRUG; AUTACOID; CYTOKINE; GLYCOPROTEIN B, SIMPLEXVIRUS; INTERFERON; MESSENGER RNA; MUTANT PROTEIN; NOD2 PROTEIN, HUMAN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CELL NUCLEUS; COLITIS; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE RESPONSE; DISEASE ASSOCIATION; DISEASE SEVERITY; GLIOMA CELL LINE; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; INNATE IMMUNITY; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; U373 CELL LINE; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS REPLICATION; CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; FIBROBLAST; GENE SILENCING; GENETICS; HERPESVIRIDAE; IMMUNOLOGY; KINETICS; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; ULTRAVIOLET RADIATION; VIROLOGY; VIRUS INACTIVATION;

CELL LINE; CYTOKINES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HERPESVIRIDAE; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; INTERFERONS; KINETICS; MALE; MUTANT PROTEINS; NF-KAPPA B; NOD2 SIGNALING ADAPTOR PROTEIN; RNA, MESSENGER; ULTRAVIOLET RAYS; VIRAL ENVELOPE PROTEINS; VIRUS INACTIVATION; VIRUS REPLICATION;

EID: 84899922475     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092704     Document Type: Article

References (49)

1. Staras SA, Dollard SC, Radford KW, Flanders WD, Pass RF, et al. (2006) Seroprevalence of cytomegalovirus infection in the United States, 1988-1994. Clin Infect Dis 43: 1143-1151. (Pubitemid 44632796)
2. Kenneson A, Cannon MJ (2007) Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol 17: 253-276. (Pubitemid 47066638)
3. Yow MD, Demmler GJ (1992) Congenital cytomegalovirus disease-20 years is long enough. N Engl J Med 326: 702-703.
4. Griffiths PD, Clark DA, Emery VC (2000) Betaherpesviruses in transplant recipients. J Antimicrob Chemother 45 Suppl T3: 29-34.
5. Cooke GS, Hill AV (2001) Genetics of susceptibility to human infectious disease. Nat Rev Genet 2: 967-977. (Pubitemid 33691093)
6. Hill AV (2001) The genomics and genetics of human infectious disease susceptibility. Annu Rev Genomics Hum Genet 2: 373-400.
7. Molvig J, Baek L, Christensen P, Manogue KR, Vlassara H, et al. (1988) Endotoxin-stimulated human monocyte secretion of interleukin 1, tumour necrosis factor alpha, and prostaglandin E2 shows stable interindividual differences. Scand J Immunol 27: 705-716.
8. Westendorp RG, Langermans JA, Huizinga TW, Elouali AH, Verweij CL, et al. (1997) Genetic influence on cytokine production and fatal meningococcal disease. Lancet 349: 170-173. (Pubitemid 27039197)
9. Casanova JL, Abel L, Quintana-Murci L (2011) Human TLRs and IL-1Rs in host defense: natural insights from evolutionary, epidemiological, and clinical genetics. Annu Rev Immunol 29: 447-491.
10. Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, et al. (2003) Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Tolllike receptor 2. J Virol 77: 4588-4596. (Pubitemid 36402808)
11. Boehme KW, Guerrero M, Compton T (2006) Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J Immunol 177: 7094-7102. (Pubitemid 44715077)
12. Kijpittayarit S, Eid AJ, Brown RA, Paya CV, Razonable RR (2007) Relationship between Toll-like receptor 2 polymorphism and cytomegalovirus disease after liver transplantation. Clin Infect Dis 44: 1315-1320. (Pubitemid 46717293)
13. Paludan SR, Bowie AG, Horan KA, Fitzgerald KA (2011) Recognition of herpesviruses by the innate immune system. Nat Rev Immunol 11: 143-154.
14. DeFilippis VR, Alvarado D, Sali T, Rothenburg S, Fruh K (2010) Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J Virol 84: 585-598.
15. Gariano GR, Dell'Oste V, Bronzini M, Gatti D, Luganini A, et al. (2012) The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog 8: e1002498.
16. Kuenzel S, Till A, Winkler M, Hasler R, Lipinski S, et al. (2010) The nucleotide-binding oligomerization domain-like receptor NLRC5 is involved in IFN-dependent antiviral immune responses. J Immunol 184: 1990-2000.
17. Kanneganti TD, Lamkanfi M, Nunez G (2007) Intracellular NOD-like receptors in host defense and disease. Immunity 27: 549-559. (Pubitemid 47615512)
18. Shaw MH, Reimer T, Kim YG, Nunez G (2008) NOD-like receptors (NLRs): bona fide intracellular microbial sensors. Curr Opin Immunol 20: 377-382.
19. Shaw MH, Kamada N, Warner N, Kim YG, Nunez G (2011) The ever-expanding function of NOD2: autophagy, viral recognition, and T cell activation. Trends Immunol 32: 73-79.
20. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, et al. (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603-606. (Pubitemid 32531409)
21. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, et al. (2005) Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307: 731-734. (Pubitemid 40194644)
22. Hysi P, Kabesch M, Moffatt MF, Schedel M, Carr D, et al. (2005) NOD1 variation, immunoglobulin E and asthma. Hum Mol Genet 14: 935-941. (Pubitemid 40533104)
23. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, et al. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5: 1166-1174. (Pubitemid 39549631)
24. Watanabe T, Asano N, Fichtner-Feigl S, Gorelick PL, Tsuji Y, et al. (2010) NOD1 contributes to mouse host defense against Helicobacter pylori via induction of type I IFN and activation of the ISGF3 signaling pathway. J Clin Invest 120: 1645-1662.
25. Watanabe T, Asano N, Kitani A, Fuss IJ, Chiba T, et al. (2011) Activation of type I IFN signaling by NOD1 mediates mucosal host defense against Helicobacter pylori infection. Gut Microbes 2: 61-65.
26. Deshmukh HS, Hamburger JB, Ahn SH, McCafferty DG, Yang SR, et al. (2009) Critical role of NOD2 in regulating the immune response to Staphylococcus aureus. Infect Immun 77: 1376-1382.
27. Shimada K, Chen S, Dempsey PW, Sorrentino R, Alsabeh R, et al. (2009) The NOD/RIP2 pathway is essential for host defenses against Chlamydophila pneumoniae lung infection. PLoS Pathog 5: e1000379.
28. Opitz B, Puschel A, Schmeck B, Hocke AC, Rosseau S, et al. (2004) Nucleotide-binding oligomerization domain proteins are innate immune receptors for internalized Streptococcus pneumoniae. J Biol Chem 279: 36426-36432. (Pubitemid 39128982)
29. Sabbah A, Chang TH, Harnack R, Frohlich V, Tominaga K, et al. (2009) Activation of innate immune antiviral responses by Nod2. Nat Immunol 10: 1073-1080.
30. Lupfer C, Thomas PG, Anand PK, Vogel P, Milasta S, et al. (2013) Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat Immunol 14: 480-488.
31. Xu Y, Ahn JH, Cheng M, apRhys CM, Chiou CJ, et al. (2001) Proteasome-independent disruption of PML oncogenic domains (PODs), but not covalent modification by SUMO-1, is required for human cytomegalovirus immediate-early protein IE1 to inhibit PML-mediated transcriptional repression. J Virol 75: 10683-10695. (Pubitemid 33031538)
32. He R, Sandford G, Hayward GS, Burns WH, Posner GH, et al. (2011) Recombinant Luciferase-Expressing Human Cytomegalovirus (CMV) for evaluation of CMV inhibitors. Virol J 8: 40.
33. Child SJ, Jarrahian S, Harper VM, Geballe AP (2002) Complementation of vaccinia virus lacking the double-stranded RNA-binding protein gene E3L by human cytomegalovirus. J Virol 76: 4912-4918. (Pubitemid 34441697)
34. Kapoor A, He R, Venkatadri R, Forman M, Arav-Boger R (2013) Wnt modulating agents inhibit human cytomegalovirus replication. Antimicrob Agents Chemother 57: 2761-2767.
35. Tiscornia G, Singer O, Ikawa M, Verma IM (2003) A general method for gene knockdown in mice by using lentiviral vectors expressing small interfering RNA. Proc Natl Acad Sci U S A 100: 1844-1848. (Pubitemid 36254536)
36. Tanaka Y, Kanda Y, Kami M, Mori S, Hamaki T, et al. (2002) Monitoring cytomegalovirus infection by antigenemia assay and two distinct plasma realtime PCR methods after hematopoietic stem cell transplantation. Bone Marrow Transplant 30: 315-319.
37. Rosner M, Hengstschlager M (2008) Cytoplasmic and nuclear distribution of the protein complexes mTORC1 and mTORC2: rapamycin triggers dephosphorylation and delocalization of the mTORC2 components rictor and sin1. Hum Mol Genet 17: 2934-2948.
38. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, et al. (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869-8872. (Pubitemid 36800360)
39. Browne EP, Wing B, Coleman D, Shenk T (2001) Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J Virol 75: 12319-12330. (Pubitemid 33115904)
40. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, et al. (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603. (Pubitemid 32531408)
41. Kobayashi K, Inohara N, Hernandez LD, Galan JE, Nunez G, et al. (2002) RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416: 194-199. (Pubitemid 34246479)
42. Hsu YM, Zhang Y, You Y, Wang D, Li H, et al. (2007) The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat Immunol 8: 198-205. (Pubitemid 46152651)
43. Pandey AK, Yang Y, Jiang Z, Fortune SM, Coulombe F, et al. (2009) NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog 5: e1000500.
44. Homer CR, Richmond AL, Rebert NA, Achkar JP, McDonald C (2010) ATG16L1 and NOD2 interact in an autophagy-dependent antibacterial pathway implicated in Crohn's disease pathogenesis. Gastroenterology 139: 1630-41, 1641.
45. Travassos LH, Carneiro LA, Girardin S, Philpott DJ (2010) Nod proteins link bacterial sensing and autophagy. Autophagy 6: 409-411.
46. Rahbar A, Bostrom L, Lagerstedt U, Magnusson I, Soderberg-Naucler C, et al. (2003) Evidence of active cytomegalovirus infection and increased production of IL-6 in tissue specimens obtained from patients with inflammatory bowel diseases. Inflamm Bowel Dis 9: 154-161. (Pubitemid 36592445)
47. Kim JJ, Simpson N, Klipfel N, Debose R, Barr N, et al. (2010) Cytomegalovirus infection in patients with active inflammatory bowel disease. Dig Dis Sci 55: 1059-1065.
48. Matsuoka K, Iwao Y, Mori T, Sakuraba A, Yajima T, et al. (2007) Cytomegalovirus is frequently reactivated and disappears without antiviral agents in ulcerative colitis patients. Am J Gastroenterol 102: 331-337. (Pubitemid 46160547)
49. Borm ME, van Bodegraven AA, Mulder CJ, Kraal G, Bouma G (2008) The effect of NOD2 activation on TLR2-mediated cytokine responses is dependent on activation dose and NOD2 genotype. Genes Immun 9: 274-278. (Pubitemid 351584196)