LGP2 plays extensive roles in modulating innate immune responses in Ctenopharyngodon idella kidney (CIK) cells

Developmental and Comparative Immunology

Volumn 49, Issue 1, 2015, Pages 138-148

  Chen, Xiaohui ^a   Yang, Chunrong ^a   Su, Jianguo ^a   Rao, Youliang ^a   Gu, Tianle ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

CIK cells; Grass carp (Ctenopharyngodon idella); Grass carp reovirus; LGP2; RLR pathway

Indexed keywords

MESSENGER RNA; DEAD BOX PROTEIN; FISH PROTEIN; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CIIPS 1 GENE; CILGP2 GENE; CIMDA5 GENE; CIRIG I GENE; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC VARIABILITY; GRASS CARP; IMMUNE RESPONSE; INNATE IMMUNITY; KIDNEY CELL; NONHUMAN; REOVIRUS; UPREGULATION; VIRUS REPLICATION; ANIMAL; CARP; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KIDNEY; PHYSIOLOGY; REOVIRIDAE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

BACTERIA (MICROORGANISMS); CTENOPHARYNGODON; CTENOPHARYNGODON IDELLA; DSRNA VIRUSES; GRASS CARP REOVIRUS; PISCES;

ANIMALS; CARPS; CELL LINE; DEAD-BOX RNA HELICASES; FISH PROTEINS; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; KIDNEY; LIPOPOLYSACCHARIDES; REOVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84919391360     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2014.10.012     Document Type: Article

References (46)

1. Biacchesi S., LeBerre M., Lamoureux A., Louise Y., Lauret E., Boudinot P., et al. Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J. Virol 2009, 83:7815-7827.
2. Bruns A.M., Horvath C.M. Antiviral RNA recognition and assembly by RLR family innate immune sensors. Cytokine Growth Factor Rev 2014, 25:507-512.
3. Bruns A.M., Pollpeter D., Hadizadeh N., Myong S., Marko J.F., Horvath C.M. ATP hydrolysis enhances RNA recognition and antiviral signal transduction by the innate immune sensor, laboratory of genetics and physiology 2 (LGP2). J. Biol. Chem 2013, 288:938-946.
4. Bruns A.M., Leser G.P., Lamb R.A., Horvath C.M. The innate immune sensor LGP2 activates antiviral signaling by regulating MDA5-RNA interaction and filament assembly. Mol. Cell 2014, 55:771-781.
5. Chang M., Collet B., Nie P., Lester K., Campbell S., Secombes C.J., et al. Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in Rainbow trout (Oncorhynchus mykiss). J. Virol 2011, 85:8403-8412.
6. Chen L., Su J., Yang C., Peng L., Wan Q., Wang L. Functional characterizations of RIG-I to GCRV and viral/bacterial PAMPs in grass carp Ctenopharyngodon idella. PLoS ONE 2012, 7. e42182.
7. Childs K., Randall R., Goodbourn S. Paramyxovirus V proteins interact with the RNA helicase LGP2 to inhibit RIG-I-dependent interferon induction. J. Virol 2012, 86:3411-3421.
8. Childs K., Randall R., Goodbourn S. LGP2 plays a critical role in sensitizing mda-5 to activation by double-stranded RNA. PLoS ONE 2013, 8. e64202.
9. De Arras L., Alper S. Limiting of the innate immune response by SF3A-dependent control of MyD88 alternative mRNA splicing. PLoS Genet 2013, 9. e1003855.
10. Goodbourn S., Randall R.E. The regulation of type I interferon production by paramyxoviruses. J. Interferon Cytokine Res 2009, 29:539-547.
11. Heine H. TLRs, NLRs and RLRs: innate sensors and their impact on allergic diseases - a current view. Immunol. Lett 2011, 139:14-24.
12. Huang T., Su J., Heng J., Dong J., Zhang R., Zhu H. Identification and expression profiling analysis of grass carp Ctenopharyngodon idella LGP2 cDNA. Fish Shellfish Immunol 2010, 29:349-355.
13. Kato H., Takeuchi O., Mikamo-Satoh E., Hirai R., Kawai T., Matsushita K., et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med 2008, 205:1601-1610.
14. Komuro A., Horvath C.M. RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J. Virol 2006, 80:12332-12342.
15. Kowalinski E., Lunardi T., McCarthy A.A., Louber J., Brunel J., Grigorov B., et al. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 2011, 147:423-435.
16. Kumar H., Bot A. Innate immune recognition mechanisms and translational opportunities. Int. Rev. Immunol 2013, 32:113-115.
17. Kumar H., Kawai T., Kato H., Sato S., Takahashi K., Coban C., et al. Essential role of IPS-1 in innate immune responses against RNA viruses. J. Exp. Med 2006, 203:1795-1803.
18. Levy D.E., Marie I.J., Durbin J.E. Induction and function of type I and III interferon in response to viral infection. Curr. Opin. Virol 2011, 1:476-486.
19. Loo Y.M., Gale M. Immune signaling by RIG-I-like receptors. Immunity 2011, 34:680-692.
20. Malur M., Gale M., Krug R.M. LGP2 downregulates interferon production during infection with seasonal human influenza A viruses that activate interferon regulatory factor 3. J. Virol 2012, 86:10733-10738.
21. Moresco E.M., Beutler B. LGP2: positive about viral sensing. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1261-1262.
22. Ohtani M., Hikima J., Kondo H., Hirono I., Jung T.S., Aoki T. Evolutional conservation of molecular structure and antiviral function of a viral RNA receptor, LGP2, in Japanese flounder, Paralichthys olivaceus. J. Immunol 2010, 185:7507-7517.
23. Peng L., Yang C., Su J. Protective roles of grass carp Ctenopharyngodon idella Mx isoforms against grass carp reovirus. PLoS ONE 2012, 7. e52142.
24. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., Weber F., et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006, 314:997-1001.
25. Pichlmair A., Schulz O., Tan C.P., Rehwinkel J., Kato H., Takeuchi O., et al. Activation of MDA5 requires higher-order RNA structures generated during virus infection. J. Virol 2009, 83:10761-10769.
26. Pollpeter D., Komuro A., Barber G.N., Horvath C.M. Impaired cellular responses to cytosolic DNA or infection with Listeria monocytogenes and vaccinia virus in the absence of the murine LGP2 protein. PLoS ONE 2011, 6. e18842.
27. Rajendran K.V., Zhang J., Liu S., Peatman E., Kucuktas H., Wang X., et al. Pathogen recognition receptors in channel catfish: II. Identification, phylogeny and expression of retinoic acid-inducible gene I (RIG-I)-like receptors (RLRs). Dev. Comp. Immunol 2012, 37:381-389.
28. Reikine S., Nguyen J.B., Modis Y. Pattern recognition and signaling mechanisms of RIG-I and MDA5. Front. Immunol 2014, 5.
29. Rodriguez K.R., Horvath C.M. Amino acid requirements for MDA5 and LGP2 recognition by paramyxovirus V proteins: a single arginine distinguishes MDA5 from RIG-I. J. Virol 2013, 87:2974-2978.
30. Rodriguez K.R., Bruns A.M., Horvath C.M. MDA5 and LGP2: accomplices and antagonists of antiviral signal transduction. J. Virol 2014, 88:8194-8200.
31. Rothenfusser S., Goutagny N., DiPerna G., Gong M., Monks B.G., Schoenemeyer A., et al. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol 2005, 175:5260-5268.
32. Saito T., Hirai R., Loo Y.M., Owen D., Johnson C.L., Sinha S.C., et al. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:582-587.
33. Satoh T., Kato H., Kumagai Y., Yoneyama M., Sato S., Matsushita K., et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1512-1517.
34. Schlee M., Roth A., Hornung V., Hagmann C.A., Wimmenauer V., Barchet W., et al. Recognition of 5' triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 2009, 31:25-34.
35. Shang X., Su J., Wan Q., Su J., Feng X. CpG methylation in the 5'-flanking region of LGP2 gene lacks association with resistance/susceptibility to GCRV but contributes to the differential expression between muscle and spleen tissues in grass carp, Ctenopharyngodon idella. Fish Shellfish Immunol 2014, 40:154-163.
36. Su J., Huang T., Dong J., Heng J., Zhang R., Peng L. Molecular cloning and immune responsive expression of MDA5 gene, a pivotal member of the RLR gene family from grass carp Ctenopharyngodon idella. Fish Shellfish Immunol 2010, 28:712-718.
37. Su J., Zhang R., Dong J., Yang C. Evaluation of internal control genes for qRT-PCR normalization in tissues and cell culture for antiviral studies of grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 2011, 30:830-835.
38. Sun F., Zhang Y.B., Liu T.K., Shi J., Wang B., Gui J.F. Fish MITA serves as a mediator for distinct fish IFN gene activation dependent on IRF3 or IRF7. J. Immunol 2011, 187:2531-2539.
39. Venkataraman T., Valdes M., Elsby R., Kakuta S., Caceres G., Saijo S., et al. Loss of DExDH box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol 2007, 178:6444-6455.
40. Wan Q., Wang L., Su J., Yang C., Peng L., Chen L. Genetic structure, polymorphism identification of LGP2 gene and their relationship with the resistance/susceptibility to GCRV in grass carp, Ctenopharyngodon idella. Gene 2013, 521:166-175.
41. Yang C., Su J., Huang T., Zhang R., Peng L. Identification of a retinoic acid-inducible gene I from grass carp (Ctenopharyngodon idella) and expression analysis in vivo and in vitro. Fish Shellfish Immunol 2011, 30:936-943.
42. Yang C., Peng L., Su J. Two HMGB1 genes from grass carp Ctenopharyngodon idella mediate immune responses to viral/bacterial PAMPs and GCRV challenge. Dev. Comp. Immunol 2013, 39:133-146.
43. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol 2004, 5:730-737.
44. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol 2005, 175:2851-2858.
45. Zhu Z., Zhang X., Wang G., Zheng H. The laboratory of genetics and physiology 2: emerging insights into the controversial functions of this RIG-I-like receptor. Biomed. Res. Int 2014, 2014. 960190.
46. Zuo W., Qian H., Xu Y., Du S., Yang X. A cell line derived from the kidney of grass carp (Ctenopharyngodon idellus). J. Fish. China 1986, 10:11-17. In Chinese with English abstract.