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Gene cloning and expression patterns of two prophenoloxidases from Catantops pinguis (Orthoptera: Catantopidae)

Published online by Cambridge University Press:  14 March 2013

Huizhen Zheng ,
Lingshun Li ,
Qi Xu ,
Qi Zou ,
Bin Tang  and
Shigui Wang
Huizhen Zheng
Affiliation:
Hangzhou Key Laboratory of Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou, Zhejiang, 310036, China
Lingshun Li
Affiliation:
Hangzhou Key Laboratory of Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou, Zhejiang, 310036, China
Qi Xu
Affiliation:
Hangzhou Key Laboratory of Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou, Zhejiang, 310036, China
Qi Zou
Affiliation:
Hangzhou Key Laboratory of Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou, Zhejiang, 310036, China
Bin Tang
Affiliation:
Hangzhou Key Laboratory of Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou, Zhejiang, 310036, China
Shigui Wang*
Affiliation:
Hangzhou Key Laboratory of Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou, Zhejiang, 310036, China
*
*Author for correspondence Phone: +86-571-22865077 Fax: +86-571-22865077 E-mail: sgwang@mail.hz.zj.cn
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Abstract

In insect, fat body plays major roles in insect innate immunity. Phenoloxidase (PO) is an important component in insect innate immunity and is necessary for acclimatization. In our study, two prophenoloxidase (PPO) subunits were obtained from fat body of Catantops pinguis (Stål). The full-length cDNA sequence of one PPO (CpPPO1) consisted of 2347 bp with an open reading frame (ORF) of 2187 bp encoding 728 amino acids, while the other subunit (CpPPO2) had a full length of 2445 bp, encoding 691 amino acids. Both the PPO gene products are predicted to possess all the structural features of other PPO members, including two putative tyrosinase copper-binding motifs with six highly conserved histidine residues and a thiolester-like motif. Tissue distribution analysis showed that both PPO mRNAs were abundantly expressed in the fat body among 11 tissues examined, and they were transiently up-regulated after Escherichia coli infection, consistent with them being immune-responsive genes. Total levels of CpPPO1 and CpPPO2 mRNA transcripts were much higher in first instar larvae and adults. A much higher transcript level of CpPPO1 was detected in several months, while there were extremely high mRNA expression levels of CpPPO2 in January, July, October, and December. The above results suggested that PPO from fat body might also bring significant function during the processes of development and acclimatization for C. pinguis.

Keywords

prophenoloxidasecloningexpression patternCatantops pinguis
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 4 , August 2013 , pp. 393 - 405
Copyright
Copyright © Cambridge University Press 2013 

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References

Abril, S., Oliveras, J. & Gómez, C. (2010) Effect of temperature on the development and survival of the Argentine ant, Linepithema humile. Journal of Insect Science 10, 1–13.Google Scholar
Alaux, C., Ducloz, F., Crauser, D. & Le Conte, Y. (2010) Diet effects on honeybee immunocompetence. Biology Letters 6, 562–565.Google Scholar
Amparyup, P., Charoensapsri, W. & Tassanakajon, A. (2009) Two prophenoloxidases are important for the survival of Vibrio harveyi challenged shrimp Penaeus monodon. Developmental and Comparative Immunology 33, 247–256.CrossRefGoogle ScholarPubMed
Antonova, Y., Alvarez, K.S., Kim, Y.J., Kokozak, 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
Arrese, E.L. & Soulages, J.L. (2010) Insect fat body: energy, metabolism and regulation. Annual Review of Entomology 55, 207–225.Google Scholar
Asano, T. & Ashida, M. (2001) Cuticular prophenoloxidase of the silkworm, Bombyx mori purification and demonstration of its transport from hemolymph. Journal of Biological Chemistry 276, 11100–11112.CrossRefGoogle ScholarPubMed
Ashida, M. & Brey, P.T. (1998) Recent advances in research on the insect prophenoloxidase cascade. pp. 135–172in Brey, P.T. & Hultmark, D. (Eds) Molecular Mechanisms of Immune Responses in Insects. London, UK, Chapman and Hall.Google Scholar
Aspan, A., Huang, T.S., Cerenius, L. & Söderhäll, K. (1995) cDNA cloning of prophenoloxidase from the freshwater crayfish Pacifastacus leniusculus and its activation. Proceedings of the National Academy of Sciences of the United States of America 92, 939–943.Google Scholar
Bao, Y.-Y., Lv, Z.-Y., Liu, Z.-B., Xue, J., Xu, Y.-P. & Zhang, C.-X. (2010) Comparative analysis of Bombyx mori nucleopolyhedrovirus responsive genes in fat body and haemocyte of B. mori resistant and susceptible strains. Insect Molecular Biology 19, 347–358.Google Scholar
Cardoso, A.F., Cres, R.L., Moura, A.S., de Almeida, F. & Bijovsky, A.T. (2010) Culex quinquefasciatus vitellogenesis: morphological and biochemical aspects. Memórias do Instituto Oswaldo Cruz 105, 254–262.Google Scholar
Cerenius, L. & Söderhäll, K. (2004) The prophenoloxidase-activating system in invertebrates. Immunological Reviews 198, 116–126.Google Scholar
Cerenius, L., Bangyeekhun, E., Keyser, P., Söderhäll, I. & Söderhäll, K. (2003) Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plague fungus, Aphanomyces astaci. Cellular Microbiology 5, 353–357.Google Scholar
Cerenius, L., Lee, B.L. & Söderhäll, K. (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29, 263–271.Google Scholar
Cho, W.-L., Liu, H.-S., Lee, C.-H., Kuo, C.-C., Chang, T.-Y., Liu, C.-T. & Chen, C.-C. (1998) Molecular cloning, characterization and tissue expression of prophenoloxidase cDNA from the mosquito Armigeres subalbatus inoculated with Dirofilaria immitis microfilariae. Insect Molecular Biology 7, 31–40.Google Scholar
Christensen, B.M., Li, J., Chen, C.-C, Nappi, A.J. (2005) Melanization immune responses in mosquito vectors. Trends in Parasitology 21, 192–199.Google Scholar
Christophides, G.K., Vlachou, D. & Kafatos, F.C. (2004) Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunological Reviews 198, 127–148.Google Scholar
Cui, L., Luckhart, S. & Rosenberg, R. (2000) Molecular characterization of a prophenoloxidase cDNA from the malaria mosquito Anopheles stephensi. Insect Molecular Biology 9, 127–137.Google Scholar
Doucet, D., Béliveau, C., Dowling, A., Simard, J., Feng, Q.L., Krell, P.J. & Cusson, M. (2008) Prophenoloxidases 1 and 2 from the spruce budworm, Choristoneura fumiferana: molecular cloning and assessment of transcriptional regulation by a polydnavirus. Archives of Insect Biochemistry and Physiology 67, 188–201.CrossRefGoogle ScholarPubMed
Eleftherianos, I. & Revenis, C. (2011) Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity 3, 28–33.Google Scholar
Fellous, S. & Lazzaro, B.P. (2010) Larval food quality affects adult (but not larval) immune gene expression independent of effects on general condition. Molecular Ecology 19, 1462–1468.Google Scholar
Feng, C., Huang, J., Song, Q., Stanley, D., Lü, W., Zhang, Y. & Huang, Y. (2011) Parasitization by Macrocentrus cingulum (Hymenoptera: Braconidae) influences expression of prophenoloxidase in Asian corn borer Ostrinia furnacalis. Archives of Insect Biochemistry and Physiology 77, 99–117.Google Scholar
Ferrandon, D., Imler, J.L., Hetru, C. & Hoffmann, J.A. (2007) The Drosophila systemic immune response: sensing and signaling during bacterial and fungal infections. Nature Reviews Immunology 7, 862–874.CrossRefGoogle ScholarPubMed
Fujimoto, K., Okino, N., Kawabata, S., Iwanaga, S. & Ohnishi, E. (1995) Nucleotide sequence of the cDNA encoding the proenzyme of phenoloxidase A1 of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 92, 7769–7773.Google Scholar
Haunerland, N.H. & Shirk, P.D. (1995) Regional and functional differentiation in the insect fat body. Annual Review of Entomology 40, 121–145.Google Scholar
Jiang, H., Wang, Y., Korochkina, S.E., Benes, H. & Kanost, M.R. (1997) Molecular cloning of cDNAs for two prophenoloxidase subunits from the malaria vector, Anopheles gambiae. Insect Biochemistry Molecular Biology 27, 693–699.Google Scholar
Jiravanichpaisal, P., Lee, B.L. & Söderhäll, K. (2006) Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211, 213–236.Google Scholar
Kim, S.R., Yao, R., Han, Q., Christensen, B.M. & Li, J. (2005) Identification and molecular characterization of a prophenoloxidase involved in Aedes aegypti chorion melanization. Insect Molecular Biology 14, 185–194.CrossRefGoogle ScholarPubMed
Leclerc, V., Pelte, N., EI Chamy, L., Martinelli, C., Ligoxygakis, P., Hoffmann, J.A. & Reichhart, J.M. (2006) Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Reports 7, 231–235.CrossRefGoogle Scholar
Lee, W.J., Ahmed, A., della Torra, A., Kobayashi, A., Ashida, M. & Brey, P.T. (1998) Molecular cloning and chromosomal localization of a prophenoloxidase cDNA from the malaria vector Anopheles gambiae. Insect Molecular Biology 7, 41–50.Google Scholar
Li, Y.-C., Wang, Y., Jiang, H.-B. & Deng, J.-P. (2009) Crystal structure of Manduca sexta prophenoloxidase provides insights into the mechanism of type 3 copper enzymes. Proceedings of the National Academy of Sciences of the United States of America 106, 17002–17006.Google Scholar
Ling, E. & Yu, X.-Q. (2005) Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melanization in Manduca sexta. Insect Biochemistry Molecular Biology 35, 1356–1366.Google Scholar
Liu, H., Jiravanichpaisal, P., Cerenius, L., Lee, B.L., Söderhäll, I. & Söderhäll, K. (2007) Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus. Journal of Biological Chemistry 282, 33593–33598.Google Scholar
Lourença, A.P., Zufelato, M.S., Bitondi, M.M. & Simões, Z.L. (2005) Molecular characterization of a cDNA encoding prophenoloxidase and its expression in Apis mellifera. Insect Biochemistry and Molecular Biology 35, 541–552.Google Scholar
Martins, G.F., Serrão, J.E., Ramalho-Ortigão, J.M. & Paolucci-Pimenta, P.F. (2011) A comparative study of fat body morphology in five mosquito species. Memórias do Instituto Oswaldo Cruz 106, 742–747.Google Scholar
Müller, H.M., Dimopoulos, G., Blass, C. & Kafatos, F.C. (1999) A hemocyte-like cell line established from the malaria vector Anopheles gambiae expresses six prophenoloxidase genes. Journal of Biological Chemistry 274, 11727–11735.Google Scholar
Nappi, A.J. & Christensen, B.M. (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology 35, 443–459.Google Scholar
Nappi, A.J. & Ottaviani, E. (2000) Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 22, 469–480.Google Scholar
Park, D.S., Shin, S.W., Kim, M.G., Park, S.S., Lee, W.J., Brey, P.T. & Park, H.Y. (1997) Isolation and characterization of the cDNA encoding the prophenoloxidase of fall webworm, hyphantria cunea. Insect Biochemistry and Molecular Biology 27, 983–992.Google Scholar
Robb, T. & Forbes, M.R. (2006) Age-dependent induction of immunity and subsequent survival costs in males and females of a temperate damselfly. BMC Ecology 6, 15–27.Google Scholar
Roy, S.G. & Raikhel, A.S. (2011) The small GTPase Rheb is a key component linking amino acid signaling and TOR in the nutritional pathway that controls mosquito egg development. Insect Biochemistry and Molecular Biology 41, 62–69.Google Scholar
Schnitger, A.K.D., Kafatos, F.C. & Osta, M.A. (2007) The melanization reaction is not required for survival of Anopheles gambiae mosquitoes after bacterial infections. Journal of Biological Chemistry 282, 21884–21888.Google Scholar
Sezaki, H., Kawamoto, N. & Asada, N. (2001) Effect of ionic concentration on the higher-order structure of prophenol oxidase in Drosophila melanogaster. Biochemical Genetics 39, 83–92.Google Scholar
Sgolastra, F., Bosch, J., Molowny-Horas, R., Maini, S. & Kemp, W.P. (2010) Effect of temperature regime on diapause intensity in an adult-wintering Hymenopteran with obligate diapause. Journal of Insect Physiology 56, 185–194.Google Scholar
Shelby, K.S. & Popham, H.J.R. (2008) Cloning and characterization of the secreted hemocytic prophenoloxidases of Heliothis virescens. Archives of Insect Biochemistry and Physiology 69, 127–142.Google Scholar
Söderhäll, K. & Cerenius, L. (1998) Role of the prophenoloxidase-activating system in invertebrates. Current Opinion in Immunology 10, 23–28.Google Scholar
Sugumaran, M. (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Research 15, 2–9.CrossRefGoogle ScholarPubMed
Taft, A.S., Chen, C.-C., Li, J. & Christensen, B.M. (2001) Molecular cloning of two prophenoloxidase genes from the mosquito Aedes aegypti. Insect Molecular Biology 10, 97–103.Google Scholar
Tamiru, A., Getu, E., Jembere, B. & Bruce, T. (2011) Effect of temperature and relative humidity on the development and fecundity of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae). Bulletin of Entomological Research 7, 1–11.Google Scholar
Tang, H., Kambris, Z., Lemaitre, B. & Hashimoto, C. (2006) Two proteases defining a melanization cascade in the immune system of Drosophila. Journal of Biological Chemistry 281, 28097–28104.Google Scholar
Tian, L., Guo, E.-E., Diao, Y.-P, Zhou, S., Peng, Q., Cao, Y., Ling, E.-J. & Li, S. (2010) Genome-wide regulation of innate immunity by juvenile hormone and 20-hydroxyecdysone in the Bombyx fat body. BMC Genomics 11, 549–559.Google Scholar
Tsao, I.Y., Lin, U.S., Christensen, B.M. & Chen, C.-C. (2009) Armigeres subalbatus prophenoloxidase III: cloning, characterization and potential role in morphogenesis. Insect Biochemistry and Molecular Biology 39, 96–104.Google Scholar
Yamamoto, K., Yakiyama, M., Fujii, H., Kusakabe, T., Koga, K., Aso, Y. & Ishiguro, M. (2000) Expression of prophenoloxidase mRNA during silkworm hemocyte development. Bioscience, Biotechnology and Biochemistry 64, 1197–1202.Google Scholar