Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T11:47:34.805Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional analysis of a NF-κB transcription factor in the immune defense of Oriental fruit fly, Bactrocera dorsalis Hendel (Diptera: Tephritidae)

Published online by Cambridge University Press:  22 November 2016

Z. Shi ,
H. Liang  and
Y. Hou
Z. Shi
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture & Forestry University (FAFU), Fuzhou, China
H. Liang
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture & Forestry University (FAFU), Fuzhou, China
Y. Hou*
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture & Forestry University (FAFU), Fuzhou, China
*
*Author for correspondence Phone: +86-591-83768654 Fax: +86-591-83768654 E-mail: ymhou@fafu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Although some novel antimicrobial peptides (AMP) have been successfully isolated from Bactrocera dorsalis Hendel, the mechanisms underlying the induction of these peptides are still elusive. The homolog of NF-κB transcription factor Relish, designated as BdRelish, was cloned from B. dorsalis. The full length cDNA of BdRelish is 3954 bp with an open reading frame that encodes 1013 amino acids. Similar to Drosophila Relish and the mammalian p100, it is a compound protein containing a conserved Rel homology domain, an IPT (Ig-like, plexins, transcription factors) domain and an IκB-like domain (four ankyrin repeats), the nuclear localization signal RKRRR is also detected at the residues 449–453, suggesting that it has homology to Relish and it is a member of the Rel family of transcription activator proteins. Reverse transcription quantitative polymerase chain reaction analysis reveals that BdRelish mRNAs are detected in different quantities from various tissues and the highest transcription level of BdRelish is determined in fat body. The injection challenge of Escherichia coli and Staphylococcus aureas significantly upregulated the expression of BdRelish. The injection of BdRelish dsRNA markedly reduced the expression of BdRelish and decreased the transcription magnitude of antimicrobial peptides. Individuals injected BdRelish dsRNA died at a significantly faster rate compared with the control groups. Therefore, BdRelish is vital for the transcription of AMPs to attack the invading bacteria.

Keywords

insect immunityRelishantimicrobial peptideBactrocera dorsalis
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 2 , April 2017 , pp. 251 - 260
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Antonova, Y., Alvarez, K.S., Kim, Y.J., Kokoza, V. & Raikhel, A.S. (2009) The role of NF-κB factor REL2 in the Aedes aegypti immune response. Insect Biochemistry and Molecular Biology 39, 303–314.CrossRefGoogle ScholarPubMed
Barroga, C.F., Stevenson, J.K., Schwarz, E.M. & Verma, I.M. (1995) Constitutive phosphorylation of IκBα by casein kinase II. Proceedings of the National Academy of Sciences of the United States of America 92, 7637–7641.Google Scholar
Baud, V. & Derudder, E. (2011) Control of NF-κB activity by proteolysis. Current Topics in Microbiology and Immunology 349, 97–114.Google ScholarPubMed
Bonnay, F., Nguyen, X.H., Cohen-Berros, E., Troxler, L., Batsche, E., Camonis, J., Takeuchi, O., Reichhart, J. & Matt, N. (2014) Akirin specifies NF-κB selectivity of Drosophila innate immune response via chromatin remodeling. EMBO Journal 33, 2349–2362.CrossRefGoogle ScholarPubMed
Clarke, A.R., Armstrong, K.F., Carmichael, A.E., Milne, J.R., Raghu, S., Roderick, G.K. & Yeates, D.K. (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annual Review of Entomology 50, 293–319.Google Scholar
Dang, X.L., Tian, J.H., Yi, H.Y., Wang, W.X., Zheng, M., Li, Y.F., Cao, Y. & Wen, S.Y. (2006) Inducing and isolation of antibacterial peptides from oriental fruit fly, Bactrocera dorsalis Hendel. Insect Science 13, 257–262.Google Scholar
Dang, X.L., Tian, J.H., Yang, W.Y., Wang, W.X., Ishibashi, J., Asaoka, A., Yi, H.Y., Li, Y.F., Cao, Y., Yamakawa, M. & Wen, S.Y. (2009) Bactrocerin-1: a novel inducible antimicrobial peptide from pupae of Oriental fruit fly Bactrocera dorsalis Hendel. Archives of Insect Biochemistry and Physiology 13, 257–262.Google Scholar
Dushay, M.S., Åsling, B. & Hultmark, D. (1996) Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila . Proceedings of the National Academy of Sciences of the United States of America 93, 10343–10347.Google Scholar
Fan, Z.H., Wang, X.W., Lu, J., Ho, B. & Ding, J.L. (2008) Elucidating the function of an ancient NF-κB p100 homologue, CrRelish, in antibacterial defense. Infection and Immunity 76, 664–670.Google Scholar
Ghosh, G., Wang, V.Y., Huang, D.B. & Fusco, A. (2012) NF-κB regulation: lessons from structures. Immunological Reviews 246, 36–58.Google Scholar
Ghosh, S., May, M.J. & Kopp, E.B. (1998) NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annual Review of Immunology 16, 225–260.Google Scholar
Gilmore, T.D. & Wolenski, F.S. (2012) NF-κB: where did it come from and why? Immunological Reviews 246, 14–35.Google Scholar
Goto, A., Fukuyama, H., Imler, J.L. & Hoffmann, J.A. (2014) The chromatin regulator DMAP1 modulates activity of the nuclear factor κB (NF-κB) transcription factor Relish in the Drosophila innate immune response. Journal of Biological Chemistry 289, 20470–20476.Google Scholar
Hedengren, M., Asling, B., Dushay, M.S., Ando, I., Ekengren, S., Wihlborg, M. & Hultmark, D. (1999) Relish, a central factor in the control of humoral but not cellular immunity in Drosophila . Molecular Cell 4, 827–837.CrossRefGoogle Scholar
Hetru, C. & Hoffmann, J.A. (2009) NF-κB in the immune response of Drosophila . Cold Spring Harbor Perspectives in Biology 1, a000232.Google Scholar
Hoffmann, A., Natoli, G. & Ghosh, G. (2006) Transcriptional regulation via the NF-kappa signaling module. Oncogene 25, 6706–6716.Google Scholar
Hoffmann, J.A. (2003) The immune response of Drosophila . Nature 426, 33–38.Google Scholar
Hsu, J.C. & Feng, H.T. (2006) Development of resistance to spinosad in oriental fruit fly (Diptera: Tephritidae) in laboratory selection and cross-resistance. Journal of Economic Entomology 99, 931–936.Google Scholar
Hsu, J.C., Chien, T.Y., Hu, C.C., Chen, M.J., Wu, W.J., Feng, H.T., Haymer, D.S. & Chen, C.Y. (2012) Discovery of genes related to insecticide resistance in Bactrocera dorsalis by functional genomic analysis of a de novo assembled transcriptome. PLoS ONE 7, e40950.Google Scholar
Huang, X.D., Liu, W.G., Guan, Y.Y., Shi, Y., Wang, Q., Zhao, M., Wu, S.Z. & He, M.X. (2012) Molecular cloning and characterization of class I NF-κB transcription factor from pearl oyster (Pinctada fucata). Fish and Shellfish Immunology 33, 659–666.CrossRefGoogle Scholar
Hultmark, D. (2003) Drosophila immunity: paths and patterns. Current Opinion in Immunology 15, 12–19.Google Scholar
Imler, J.L. & Bulet, P. (2005) Antimicrobial peptides and activation of immune responses in Drosophila: structures, activities and gene regulation. Chemical Immunology and Allergy 86, 1–21.Google Scholar
Jin, T., Zeng, L., Lin, Y.Y., Lu, Y.Y. & Liang, G.W. (2011) Insecticide resistance of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in mainland China. Pest Management Sciences 67, 370–376.Google Scholar
Lemaitre, B. & Hoffmann, J.A. (2007) The host defense of Drosophila melanogaster . Annual Review of Immunology 25, 697–743.Google Scholar
Leulier, F., Rodriguez, A., Khush, R.S., Abrams, J.M. & Lemaitre, B. (2000) The Drosophila caspase Dredd is required to resist gram-negative bacterial infection. EMBO Reports 1, 353–358.Google Scholar
Li, F.H., Yan, H., Wang, D.D., Priya, T.A.J., Li, S.H., Wang, B., Zhang, J.Q. & Xiang, J.H. (2009) Identification of a novel relish homolog in Chinese shrimp Fenneropenaeus chinensis and its function in regulating the transcription of antimicrobial peptides. Developmental and Comparative Immunology 33, 1093–1101.Google Scholar
Meister, S., Kanzok, S.M., Zheng, X.L., Luna, C., Li, T.R., Hoa, N.T., Clayton, J.R., White, K.P., Kafatos, F.C., Christophides, G.K. & Zheng, L.B. (2005) Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae . Proceedings of the National Academy of Sciences of the United States of America 102, 11420–11425.Google Scholar
Minakhina, S. & Steward, R. (2006) Nuclear factor-kappa B pathways in Drosophila . Oncogene 25, 6749–6757.Google Scholar
Myllymäki, H., Valanne, S. & Rämet, M. (2014) The Drosophila Imd signaling pathway. Journal of Immunology 192, 83455–83462.Google Scholar
Rogers, S., Wells, R. & Rechsteiner, M. (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234, 364–368.Google Scholar
Shumway, S.D., Maki, M. & Miyamoto, S. (1999) The PEST domain of IκBα is necessary and sufficient for in vitro degradation by μ−Calpain. Journal of Biological Chemistry 274, 30874–30881.Google Scholar
Stöven, S., Ando, I., Kadalayil, L., Engström, Y. & Hultmark, D. (2000) Activation of the Drosophila NF-κB factor Relish by rapid endoproteolytic cleavage. EMBO Reports 1, 347–352.Google Scholar
Stöven, S., Silverman, N., Junell, A., Hendengren-Olcott, M., Erturk, D., Engström, Y., Maniatis, T. & Hultmark, D. (2003) Caspase-mediated processing of the Drosophila NF-κB factor Relish. Proceedings of the National Academy of Sciences of the United States of America 100, 5991–5996.Google Scholar
Tanaka, H., Matsuki, H., Furukawa, S., Sagisaka, A., Kotani, E., Mori, H. & Yamakawa, M. (2007) Identification and functional analysis of Relish homologs in the silkworm, Bombyx mori . Biochimica Biophysica Acta 1769, 559–568.Google Scholar
Tanji, T., Yun, E. & Tony Ip, Y. (2010) Heterodimers of NF-κB transcription factors DIF and Relish regulate antimicrobial peptide genes in Drosophila . Proceedings of the National Academy of Sciences of the United States of America 107, 14715–14720.Google Scholar
Thornberry, N.A., Rano, T.A., Peterson, E.P., Rasper, D.M., Timkey, T., Garcia-Calva, M., Houtzager, V.M., Nordstrom, P.A., Roy, S., Vaillancourt, J.P., Chapman, K.T. & Nicholson, D.W. (1997) A combinatorial approach defines specificities of members of the Caspase family and Granzyme B: functional relationships established for key mediators of apoptosis. Journal of Biological Chemistry 272, 17907–17911.Google Scholar
Vargas, R.I., Ramadan, M., Hussain, T., Mochizuki, N., Bautista, R.C. & Stark, J.D. (2002) Comparative demography of six fruit fly (Diptera: Tephritidae) parasitoids (Hymenoptera: Braconidae). Biological Control 25, 30–40.Google Scholar
Wang, H., Jin, L. & Zhang, H. (2011) Comparison of the diversity of the bacterial communities in the intestinal tract of adult Bactrocera dorsalis from three different populations. Journal of Applied Microbiology 110, 1390–1401.Google Scholar
Wiklund, M., Steinert, S., Junell, A., Hultmark, D. & Stöven, S. (2009) The N-terminal half of the Drosophila Rel/NF-κB factor Relish, REL-68, constitutively activates transcription of specific Relish target genes. Developmental and Comparative Immunology 33, 690–695.CrossRefGoogle ScholarPubMed
Xue, Y., Liu, Z.X., Cao, J., Ma, Q., Gao, X.J., Wang, Q.Q., Jin, C.J., Zhou, Y.H., Wen, L.Q. & Ren, J. (2011) GPS 2.1: enhanced prediction of kinase-specific phosphorylation sites with an algorithm of motif length selection. Protein Engineering, Design and Selection 24, 255–260.Google Scholar
Yang, W.J., Yuan, G.R., Cong, L., Xie, Y.F. & Wang, J.J. (2014) De novo cloning and annotation of genes associated with immunity, detoxification and energy metabolism from the fat body of the Oriental fruit fly Bactrocera dorsalis . PLoS ONE 9, e94470.Google Scholar
Zhong, X., Rao, X.J., Yi, H.Y., Lin, X.Y., Huang, X.H. & Yu, X.Q. (2016) Co-expression of Dorsal and Rel2 negatively regulates antimicrobial peptide expression in the tobacco hornworm Manduca sexta . Scientific Reports 6, 20654.Google Scholar