The shrimp IKK-NF-κB signaling pathway regulates antimicrobial peptide expression and may be subverted by white spot syndrome virus to facilitate viral gene expression

Cellular and Molecular Immunology

Volumn 10, Issue 5, 2013, Pages 423-436

  Wang, Pei Hui ^a   Gu, Zhi Hua ^a   Wan, Ding Hui ^a   Liu, Bo Du ^a   Huang, Xian De ^a   Weng, Shao Ping ^a   Yu, Xiao Qiang ^b   He, Jian Guo ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Antimicrobial peptide; IKK NF kB; Innate immunity; Litopenaeus vannamei; WSSV

Indexed keywords

DOUBLE STRANDED RNA; I KAPPA B KINASE BETA; I KAPPA B KINASE EPSILON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSOZYME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CELL STRAIN HEK293; CONTROLLED STUDY; DNA VIRUS INFECTION; DROSOPHILA; GENE ACTIVATION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GILL; HEPATOPANCREAS; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; IN VITRO STUDY; IN VIVO STUDY; INTESTINE; LITOPENAEUS VANNAMEI; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; REPORTER GENE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION; WHITE SPOT SYNDROME VIRUS; WHITE SPOT SYNDROME VIRUS INFECTION; WSSV051 GENE; WSSV059 GENE; WSSV069 GENE; WSSV083 GENE; WSSV090 GENE; WSSV107 GENE; WSSV244 GENE; WSSV303 GENE; WSSV371 GENE; WSSV445 GENE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE; CLONING, MOLECULAR; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION, VIRAL; GENE SILENCING; GENES, REPORTER; HOST-PATHOGEN INTERACTIONS; HUMANS; I-KAPPA B KINASE; LUCIFERASES; MURAMIDASE; NF-KAPPA B; PENAEIDAE; PROMOTER REGIONS, GENETIC; RECOMBINANT PROTEINS; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; WHITE SPOT SYNDROME VIRUS 1;

EID: 84883405832     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2013.30     Document Type: Article

References (46)

1. Kawai T, Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol 2009; 21: 317-337.
2. Kumar H, Kawai T, Akira S. Toll-like receptors and innate immunity. Biochem Biophys Res Commun 2009; 388: 621-625.
3. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140: 805-820.
4. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
5. Takeuchi O, Akira S. Innate immunity to virus infection. Immunol Rev 2009; 227: 75-86.
6. Hacker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006; 2006: re13.
7. Kumar H, Kawai T, Akira S. Pathogen recognition in the innate immune response. Biochem J 2009; 420: 1-16.
8. Ferrandon D, Imler JL, Hetru C, Hoffmann JA. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 2007; 7: 862-874.
9. Hoffmann JA. The immune response of Drosophila. Nature 2003; 426: 33-38.
10. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol 2007; 25: 697-743.
11. Sabin LR, Hanna SL, Cherry S. Innate antiviral immunity in Drosophila. Curr Opin Immunol 2010; 22: 4-9.
12. Kemp C, Imler JL. Antiviral immunity in Drosophila. Curr Opin Immunol 2009; 21: 3-9.
13. Erturk-Hasdemir D, Broemer M, Leulier F, Lane WS, Paquette N, Hwang D et al. Two roles for the Drosophila IKK complex in the activation of Relish and the induction of antimicrobial peptide genes. Proc Natl Acad Sci USA 2009; 106: 9779-9784.
14. Ganesan S, Aggarwal K, Paquette N, Silverman N. NF-kappaB/Rel proteins and the humoral immune responses of Drosophila melanogaster. Curr Top Microbiol Immunol 2011; 349: 25-60.
15. Dubin-Bar D, Bitan A, Bakhrat A, Kaiden-Hasson R, Etzion S, Shaanan B et al. The Drosophila IKK-related kinase (Ik2) and Spindle-F proteins are part of a complex that regulates cytoskeleton organization during oogenesis. BMC Cell Biol 2008; 9: 51.
16. Kuranaga E, Kanuka H, Tonoki A, Takemoto K, Tomioka T, Kobayashi M et al. Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 2006; 126: 583-596.
17. de Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J 2002; 21: 2568-2579.
18. Wang PH, Liang JP, Gu ZH, Wan DH, Zhu WB, Qiu W et al. Molecular cloning, characterization and expression analysis of two novel Tolls (LvToll2 and LvToll3) and three putative Spatzle-like Toll ligands (LvSpz1-3) from Litopenaeus vannamei. Dev Comp Immunol 2012; 36: 359-371.
19. Huang XD, Yin ZX, Jia XT, Liang JP, Ai HS, Yang LS et al. Identification and functional study of a shrimp Dorsal homologue. Dev Comp Immunol 2010; 34: 107-113.
20. Huang XD, Yin ZX, Liao JX, Wang PH, Yang LS, Ai HS et al. Identification and functional study of a shrimp Relish homologue. Fish Shellfish Immunol 2009; 27: 230-238.
21. Wang PH, Gu ZH, Huang XD, Liu BD, Deng XX, Ai HS et al. An immune deficiency homolog from the white shrimp, Litopenaeus vannamei, activates antimicrobial peptide genes. Mol Immunol 2009; 46: 1897-1904.
22. de Lorgeril J, Gueguen Y, Goarant C, Goyard E, Mugnier C, Fievet J et al. A relationship between antimicrobial peptide gene expression and capacity of a selected shrimp line to survive a Vibrio infection. Mol Immunol 2008; 45: 3438-3445.
23. Wang PH, Wan DH, Gu ZH, Deng XX, Weng SP, Yu XQ et al. Litopenaeus vannamei tumor necrosis factor receptor-associated factor 6 (TRAF6) responds to Vibrio alginolyticus and white spot syndrome virus (WSSV) infection and activates antimicrobial peptide genes. Dev Comp Immunol 2011; 35: 105-114.
24. Wang PH, Wan DH, Pang LR, Gu ZH, Qiu W, Weng SP et al. Molecular cloning, characterization and expression analysis of the tumor necrosis factor (TNF) superfamily gene, TNF receptor superfamily gene and lipopolysaccharide-induced TNF-alpha factor (LITAF) gene from Litopenaeus vannamei. Dev Comp Immunol 2012; 36: 39-50.
25. Wang PH, Gu ZH, Wan DH, Zhang MY, Weng SP, Yu XQ et al. The shrimp NF-kappaB pathway is activated by white spot syndrome virus (WSSV) 449 to facilitate the expression of WSSV069 (ie1), WSSV303 and WSSV371. PloS ONE 2011; 6: e24773.
26. Wang PH, Wan DH, Gu ZH, Deng XX, Weng SP, Yu XQ et al. Litopenaeus vannamei tumor necrosis factor receptor-associated factor 6 (TRAF6) responds to Vibrio alginolyticus and white spot syndrome virus (WSSV) infection and activates antimicrobial peptide genes. Dev Comp Immunol 2011; 35: 105-114.
27. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29: e45.
28. Ho SH, Song YL. Cloning of penaeidin gene promoter in tiger shrimp (Penaeus monodon). Fish Shellfish Immunol 2009; 27: 73-77.
29. Li F, Wang D, Li S, Yan H, Zhang J, Wang B et al. A Dorsal homolog (FcDorsal) in the Chinese shrimp Fenneropenaeus chinensis is responsive to both bacteria and WSSV challenge. Dev Comp Immunol 2010; 34: 874-883.
30. O'Leary NA, Gross PS. Genomic structure and transcriptional regulation of the penaeidin gene family from Litopenaeus vannamei. Gene 2006; 371: 75-83.
31. Huang XD, Zhao L, Zhang HQ, Xu XP, Jia XT, Chen YH et al. Shrimp NFkappaB binds to the immediate-early gene ie1 promoter of white spot syndrome virus and upregulates its activity. Virology 2010; 406: 176-180.
32. Wang PH, Gu ZH, Wan DH, Zhu WB, Qiu W, Weng SP et al. Litopenaeus vannamei sterile-alpha and armadillo motif containing protein (LvSARM) is involved in regulation of penaeidins and antilipopolysaccharide factors. PloS ONE 2013; 8: e52088.
33. Vallabhapurapu S, Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 2009; 27: 693-733.
34. Zhi H, Yang L, Kuo YL, Ho YK, Shih HM, Giam CZ. NF-kappaB hyperactivation by HTLV-1 tax induces cellular senescence, but can be alleviated by the viral anti-sense protein HBZ. PLoS Pathog 2011; 7: e1002025.
35. Wang PH, Gu ZH, Wan DH, Zhang MY, Weng SP, Yu XQ et al. Litopenaeus vannamei Toll-interacting protein (LvTollip) is a potential negative regulator of the shrimp Toll pathway involved in the regulation of the shrimp antimicrobial peptide gene penaeidin-4 (PEN4). Dev Comp Immunol 2013; 40: 266-277.
36. Kadalayil L, Petersen UM, Engstrom Y. Adjacent GATA and kappa Blike motifs regulate the expression of a Drosophila immune gene. Nucleic Acids Res 1997; 25: 1233-1239.
37. Valanne S, Wang JH, Ramet M. The Drosophila Toll signaling pathway. J Immunol 2011; 186: 649-656.
38. Hiscott J, Nguyen TL, Arguello M, Nakhaei P, Paz S. Manipulation of the nuclear factor-kappaB pathway and the innate immune response by viruses. Oncogene 2006; 25: 6844-6867.
39. Li F, Yan H, Wang D, Priya TA, Li S, Wang B et al. Identification of a novel relish homolog in Chinese shrimp Fenneropenaeus chinensis and its function in regulating the transcription of antimicrobial peptides. Dev Comp Immunol 2009; 33: 1093-1101.
40. Zhang S, Li CZ, Yan H, Qiu W, Chen YG, Wang PH et al. Identification and function of myeloid differentiation factor 88 (MyD88) in Litopenaeus vannamei. PloS ONE 2012; 7: e47038.
41. Li C, Chen YX, Zhang S, Lü L, Chen YH, Chai J et al. Identification, characterization, and function analysis of the Cactus gene from Litopenaeus vannamei. PloS ONE 2012; 7: e49711.
42. Santoro MG, Rossi A, Amici C. NF-kappaB and virus infection: who controls whom. EMBO J 2003; 22: 2552-2560.
43. Liu WJ, Chang YS, Wang CH, Kou GH, Lo CF. Microarray and RT-PCR screening for white spot syndrome virus immediate-early genes in cycloheximide-treated shrimp. Virology 2005; 334: 327-341.
44. Li F, Li M, Ke W, Ji Y, Bian X, Yan X. Identification of the immediateearly genes of white spot syndrome virus. Virology 2009; 385: 267-274.
45. Liu WJ, Chang YS, Wang HC, Leu JH, Kou GH, Lo CF. Transactivation, dimerization, and DNA-binding activity of white spot syndrome virus immediate-early protein IE1. J Virol 2008; 82: 11362-11373.
46. Liu WJ, Chang YS, Wang AH, Kou GH, Lo CF. White spot syndrome virus annexes a shrimp STAT to enhance expression of the immediateearly gene ie1. J Virol 2007; 81: 1461-1471.