Evolutional conservation of molecular structure and antiviral function of a viral RNA receptor, LGP2, in Japanese flounder, Paralichthys olivaceus

Journal of Immunology

Volumn 185, Issue 12, 2010, Pages 7507-7517

  Ohtani, Maki ^a   Jun Ichi, Hikima ^a   Kondo, Hidehiro ^b   Hirono, Ikuo ^b   Tae Sung, Jung ^a   Aoki, Takashi ^a,b  

^a Gyeongsang National University   (South Korea)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; INTERFERON; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG; VIRAL RNA RECEPTOR LGP2; VIRUS RNA;

ANTIVIRAL ACTIVITY; ARTICLE; CHEMICAL STRUCTURE; CYTOKINE PRODUCTION; EMBRYO CELL; FLOUNDER; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY; LEUKOCYTE; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; PARALICHTHYS OLIVACEUS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHABDOVIRUS; SEPTICEMIA;

AMINO ACID SEQUENCE; ANIMALS; DNA, COMPLEMENTARY; FISH PROTEINS; FLOUNDER; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INTERFERON INDUCERS; INTERFERON TYPE I; KIDNEY; MOLECULAR SEQUENCE DATA; NOVIRHABDOVIRUS; POLY I-C; PROTEIN STRUCTURE, TERTIARY; RHABDOVIRIDAE INFECTIONS; RNA HELICASES; RNA, DOUBLE-STRANDED; RNA, MESSENGER; RNA, VIRAL; SEQUENCE DELETION;

EID: 78650674940     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001850     Document Type: Article

References (63)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
2. Kawai, T., and S. Akira. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 1143:1-20.
3. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737.
4. Kang, D. C., R. V. Gopalkrishnan, Q. Wu, E. Jankowsky, A. M. Pyle, and P. B. Fisher. 2002. mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growthsuppressive properties. Proc. Natl. Acad. Sci. USA 99:637-642.
5. Cui, Y., M. Li, K. D. Walton, K. Sun, J. A. Hanover, P. A. Furth, and L. Hennighausen. 2001. The Stat3/5 locus encodes novel endoplasmic reticulum and helicase-like proteins that are preferentially expressed in normal and neoplastic mammary tissue. Genomics 78:129-134.
6. Gee, P., P. K. Chua, J. Gevorkyan, K. Klumpp, I. Najera, D. C. Swinney, and J. Deval. 2008. Essential role of the N-terminal domain in the regulation of RIGI ATPase activity. J. Biol. Chem. 283:9488-9496.
7. Kawai, T., K. Takahashi, S. Sato, C. Coban, H. Kumar, H. Kato, K. J. Ishii, O. Takeuchi, and S. Akira. 2005. IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988.
8. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820.
9. Saito, T., R. Hirai, Y. M. Loo, D. Owen, C. L. Johnson, S. C. Sinha, S. Akira, T. Fujita, and M. Gale, Jr. 2007. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc. Natl. Acad. Sci. USA 104:582-587.
10. Cui, S., K. Eisenächer, A. Kirchhofer, K. Brzózka, A. Lammens, K. Lammens, T. Fujita, K. K. Conzelmann, A. Krug, and K. P. Hopfner. 2008. The C-terminal regulatory domain is the RNA 59-triphosphate sensor of RIG-I. Mol. Cell 29:169-179.
11. Takahasi, K., H. Kumeta, N. Tsuduki, R. Narita, T. Shigemoto, R. Hirai, M. Yoneyama, M. Horiuchi, K. Ogura, T. Fujita, and F. Inagaki. 2009. Solution structures of cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: identification of the RNA recognition loop in RIG-I-like receptors. J. Biol. Chem. 284:17465-17474.
12. Li, X., C. T. Ranjith-Kumar, M. T. Brooks, S. Dharmaiah, A. B. Herr, C. Kao, and P. Li. 2009. The RIG-I-like receptor LGP2 recognizes the termini of doublestranded RNA. J. Biol. Chem. 284:13881-13891.
13. Hornung, V., J. Ellegast, S. Kim, K. Brzózka, A. Jung, H. Kato, H. Poeck, S. Akira, K. K. Conzelmann, M. Schlee, et al. 2006. 59-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
14. Pichlmair, A., O. Schulz, C. P. Tan, T. I. Näslund, P. Liljeström, F. Weber, and C. Reis E Sousa. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 59-phosphates. Science 314:997-1001.
15. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
16. Kato, H., O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, K. Matsushita, A. Hiiragi, T. S. Dermody, T. Fujita, and S. Akira. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205:1601-1610.
17. Yoneyama, M., M. Kikuchi, K. Matsumoto, T. Imaizumi, M. Miyagishi, K. Taira, E. Foy, Y. M. Loo, M. Gale, Jr., S. Akira, et al. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175:2851-2858.
18. Rothenfusser, S., N. Goutagny, G. DiPerna, M. Gong, B. G. Monks, A. Schoenemeyer, M. Yamamoto, S. Akira, and K. A. Fitzgerald. 2005. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 175:5260-5268.
19. Komuro, A., and C. M. Horvath. 2006. RNA-and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J. Virol. 80:12332-12342.
20. Venkataraman, T., M. Valdes, R. Elsby, S. Kakuta, G. Caceres, S. Saijo, Y. Iwakura, and G. N. Barber. 2007. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 178:6444-6455.
21. Gitlin, L., W. Barchet, S. Gilfillan, M. Cella, B. Beutler, R. A. Flavell, M. S. Diamond, and M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103:8459-8464.
22. Satoh, T., H. Kato, Y. Kumagai, M. Yoneyama, S. Sato, K. Matsushita, T. Tsujimura, T. Fujita, S. Akira, and O. Takeuchi. 2010. LGP2 is a positive regulator of RIG-I-and MDA5-mediated antiviral responses. Proc. Natl. Acad. Sci. USA 107:1512-1517.
23. Matsuo, A., H. Oshiumi, T. Tsujita, H. Mitani, H. Kasai, M. Yoshimizu, M. Matsumoto, and T. Seya. 2008. Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J. Immunol. 181:3474-3485.
24. Hirono, I., M. Takami, M. Miyata, T. Miyazaki, H. J. Han, T. Takano, M. Endo, and T. Aoki. 2004. Characterization of gene structure and expression of two tolllike receptors from Japanese flounder, Paralichthys olivaceus. Immunogenetics 56:38-46.
25. Biacchesi, S., M. LeBerre, A. Lamoureux, Y. Louise, E. Lauret, P. Boudinot, and M. Brémont. 2009. Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J. Virol. 83:7815-7827.
26. Su, J., T. Huang, J. Dong, J. Heng, R. Zhang, and L. Peng. 2010. 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. 28:712-718.
27. Huang, T., J. Su, J. Heng, J. Dong, R. Zhang, and H. Zhu. 2010. Identification and expression profiling analysis of grass carp Ctenopharyngodon idella LGP2 cDNA. Fish Shellfish Immunol. 29:349-355.
28. Seppola, M., H. Johnsen, S. Mennen, B. Myrnes, and H. Tveiten. 2009. Maternal transfer and transcriptional onset of immune genes during ontogenesis in Atlantic cod. Dev. Comp. Immunol. 33:1205-1211.
29. Zou, J., M. Chang, P. Nie, and C. J. Secombes. 2009. Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol. Biol. 9:85.
30. Lee, J. Y., I. Hirono, and T. Aoki. 2000. Cloning and analysis of expression of Mx cDNA in Japanese flounder, Paralichthys olivaceus. Dev. Comp. Immunol. 24:407-415. (Pubitemid 30151200)
31. Yasuike, M., H. Kondo, I. Hirono, and T. Aoki. 2010. Identification and characterization of Japanese flounder, Paralichthys olivaceus interferon-stimulated gene 15 (Jf-ISG15). Comp. Immunol. Microbiol. Infect. Dis.
32. Bergan, V., S. Steinsvik, H. Xu, O. Kileng, and B. Robertsen. 2006. Promoters of type I interferon genes from Atlantic salmon contain two main regulatory regions. FEBS J. 273:3893-3906.
33. Chen, J. Y., Y. K. You, J. C. Chen, T. C. Huang, and C. M. Kuo. 2005. Organization and promoter analysis of the zebrafish (Danio rerio) interferon gene. DNA Cell Biol. 24:641-650.
34. Lin, O. E., T. Ohira, I. Hirono, T. Saito-Taki, and T. Aoki. 2005. Immunoanalysis of antiviral Mx protein expression in Japanese flounder (Paralichthys olivaceus) cells. Dev. Comp. Immunol. 29:443-455. (Pubitemid 40222053)
35. Ooi, E. L., I. Hirono, and T. Aoki. 2006. Functional characterisation of the Japanese flounder, Paralichthys olivaceus, Mx promoter. Fish Shellfish Immunol. 21:293-304.
36. Kileng, O., V. Bergan, S. T. Workenhe, and B. Robertsen. 2009. Structural and functional studies of an IRF-7-like gene from Atlantic salmon. Dev. Comp. Immunol. 33:18-27.
37. Holland, J. W., S. Bird, B. Williamson, C. Woudstra, A. Mustafa, T. Wang, J. Zou, S. C. Blaney, B. Collet, and C. J. Secombes. 2008. Molecular characterization of IRF3 and IRF7 in rainbow trout, Oncorhynchus mykiss: functional analysis and transcriptional modulation. Mol. Immunol. 46:269-285.
38. Collet, B., and C. J. Secombes. 2002. Type I-interferon signalling in fish. Fish Shellfish Immunol. 12:389-397.
39. Kasai, H., and M. Yoshimizu. 2001. Establishment of Japanese flounder embryo cell lines. Bulletin of Fisheries Science Hokkaido University 52:67-70.
40. Kimura, T., M. Yoshimizu, and S. Gorie. 1986. A new rhabdovirus isolated in Japan from cultured hirame (Japanese flounder) Paralichthys olivaceus and ayu Plecoglossus altivelis. Dis. Aquat. Org. 1:209-217.
41. Katagiri, T., S. Asakawa, I. Hirono, T. Aoki, and N. Shimizu. 2000. Genomic bacterial artificial chromosome library of the Japanese flounder Paralichthys olivaceus. Mar. Biotechnol. (NY) 2:571-576.
42. Arnold, K., L. Bordoli, J. Kopp, and T. Schwede. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201.
43. Kiefer, F., K. Arnold, M. Künzli, L. Bordoli, and T. Schwede. 2009. The SWISSMODEL Repository and associated resources. Nucleic Acids Res. 37 (Database issue): D387-D392.
44. Peitsch, M. 1995. Protein modeling by e-mail. Nat. Biotechnol. 13:658-660.
45. Bamming, D., and C. M. Horvath. 2009. Regulation of signal transduction by enzymatically inactive antiviral RNA helicase proteins MDA5, RIG-I, and LGP2. J. Biol. Chem. 284:9700-9712.
46. Zapata, A. G., A. Chiba, and A. Varas. 1996. Cells and tissues of the immune system of fish. In The fish immune system. G. Iwama, and T. Nakanishi, eds. Academic Press, San Diego, CA, p. 1-62.
47. Nakamura, H., and A. Shimozawa. 1994. Phagocytotic cells in the fish heart. Arch. Histol. Cytol. 57:415-425.
48. Imaizumi, T., S. Aratani, T. Nakajima, M. Carlson, T. Matsumiya, K. Tanji, K. Ookawa, H. Yoshida, S. Tsuchida, T. M. McIntyre, et al. 2002. Retinoic acidinducible gene-I is induced in endothelial cells by LPS and regulates expression of COX-2. Biochem. Biophys. Res. Commun. 292:274-279.
49. Wang, J., S. Wu, X. Jin, M. Li, S. Chen, J. L. Teeling, V. H. Perry, and J. Gu. 2008. Retinoic acid-inducible gene-I mediates late phase induction of TNF-a by lipopolysaccharide. J. Immunol. 180:8011-8019.
50. Freudenberg, M. A., C. Kalis, Y. Chvatchko, T. Merlin, M. Gumenscheimer, and C. Galanos. 2003. Role of interferons in LPS hypersensitivity. J. Endotoxin Res. 9:308-312.
51. Takeuchi, O., H. Hemmi, and S. Akira. 2004. Interferon response induced by Toll-like receptor signaling. J. Endotoxin Res. 10:252-256.
52. Schumacher, B., D. Bernasconi, U. Schultz, and P. Staeheli. 1994. The chicken Mx promoter contains an ISRE motif and confers interferon inducibility to a reporter gene in chick and monkey cells. Virology 203:144-148.
53. Asano, A., H. K. Jin, and T. Watanabe. 2003. Mouse Mx2 gene: organization, mRNA expression and the role of the interferon-response promoter in its regulation. Gene 306:105-113.
54. Haller, O., and G. Kochs. 2002. Interferon-induced mx proteins: dynamin-like GTPases with antiviral activity. Traffic 3:710-717.
55. Kim, M. J., S. Y. Hwang, T. Imaizumi, and J. Y. Yoo. 2008. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J. Virol. 82:1474-1483
56. Li, Y., C. Li, P. Xue, B. Zhong, A. P. Mao, Y. Ran, H. Chen, Y. Y. Wang, F. Yang, and H. B. Shu. 2009. ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. Proc. Natl. Acad. Sci. USA 106:7945-7950.
57. Au, W. C., P. A. Moore, W. Lowther, Y. T. Juang, and P. M. Pitha. 1995. Identification of a member of the interferon regulatory factor family that binds to the interferon-stimulated response element and activates expression of interferoninduced genes. Proc. Natl. Acad. Sci. USA 92:11657-11661.
58. Grandvaux, N., M. J. Servant, B. tenOever, G. C. Sen, S. Balachandran, G. N. Barber, R. Lin, and J. Hiscott. 2002. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferonstimulated genes. J. Virol. 76:5532-5539.
59. Kileng, O., M. I. Brundtland, and B. Robertsen. 2007. Infectious salmon anemia virus is a powerful inducer of key genes of the type I interferon system of Atlantic salmon, but is not inhibited by interferon. Fish Shellfish Immunol. 23:378-389.
60. Robertsen, B. 2008. Expression of interferon and interferon-induced genes in salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish Shellfish Immunol. 25:351-357.
61. Purcell, M. K., K. J. Laing, J. C. Woodson, G. H. Thorgaard, and J. D. Hansen. 2009. Characterization of the interferon genes in homozygous rainbow trout reveals two novel genes, alternate splicing and differential regulation of duplicated genes. Fish Shellfish Immunol. 26:293-304.
62. Zou, J., C. Tafalla, J. Truckle, and C. J. Secombes. 2007. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J. Immunol. 179:3859-3871.
63. Levraud, J. P., P. Boudinot, I. Colin, A. Benmansour, N. Peyrieras, P. Herbomel, and G. Lutfalla. 2007. Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system. J. Immunol. 178:4385-4394.