Study of the aminopeptidase N gene family in the lepidopterans Ostrinia nubilalis (Hübner) and Bombyx mori (L.): Sequences, mapping and expression

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 7, 2010, Pages 506-515

  Crava, Cristina M ^a   Bel, Yolanda ^a   Lee, Siu Fai ^b   Manachini, Barbara ^c   Heckel, David G ^d   Escriche, Baltasar ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF PALERMO   (Italy)

^d MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Bt toxin binding proteins; Larval development expression; Midgut APN; Puromycin sensitive aminopeptidase; Quantitative PCR

Indexed keywords

INSECT PROTEIN; ISOENZYME; MESSENGER RNA; MICROSOMAL AMINOPEPTIDASE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGY; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETIC LINKAGE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MOTH; MULTIGENE FAMILY; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SILKWORM; BOMBYX;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD13; BOMBYX; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; INSECT PROTEINS; ISOENZYMES; LARVA; LINKAGE (GENETICS); MOLECULAR SEQUENCE DATA; MOTHS; MULTIGENE FAMILY; PHYLOGENY; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, NUCLEIC ACID; GENETIC LINKAGE;

BACILLUS THURINGIENSIS; BOMBYX MORI; LEPIDOPTERA; OSTRINIA NUBILALIS; ZEA MAYS;

EID: 77953911945     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.04.010     Document Type: Article

References (43)

1. Albiston A.L., Ye S., Chai S.Y. Membrane bound members of the M1 family more than aminopeptidases. Protein Pept. Lett. 2004, 11:491-500.
2. Angelucci C., Barrett-Wilt G.A., Hunt D.F., Akhurst E.J., East P.D., Gordon K.H., Campbell P.M. Diversity of aminopeptidases, derived from four lepidopteran gene duplications, and polycalins expressed in the midgut of Helicoverpa armigera: identification of proteins binding the δ-endotoxin, Cry1Ac of Bacillus thuringiensis. Insect Biochem. Mol. Biol. 2008, 38:685-696.
3. Baxter S.W., Zhao J.Z., Shelton A.M., Vogel H., Heckel D.G. Genetic mapping of Bt-toxin binding proteins in a Cry1A-toxin resistant strain of diamondback moth Plutella xylostella. Insect Biochem. Mol. Biol. 2008, 38:125-135.
4. Bel Y., Escriche B. Common genomic structure for the Lepidoptera cadherin-like genes. Gene 2006, 381:71-80.
5. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
6. Bravo A., Gill S.S., Soberon M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 2007, 49:423-435.
7. Budatha M., Meur G., Dutta-Gupta A. A novel aminopeptidase in the fat body of the moth Achaea janata as a receptor for Bacillus thuringiensis Cry toxins and its comparison with midgut aminopeptidase. Biochem. J. 2007, 405:287-297.
8. Chang W.X., Gahan L.J., Tabashnik B.E., Heckel D.G. A new aminopeptidase from diamondback moth provides evidence for a gene duplication event in Lepidoptera. Insect Mol. Biol. 1999, 8:171-177.
9. Chougule N.P., Giri A.P., Mohini N.S., Gupta V.S. Gene expression patterns of Helicoverpa armigera gut proteases. Insect Biochem. Mol. Biol. 2005, 35:355-367.
10. Coates B.S., Sumerford D.V., Hellmich R.L., Lewis L.C. Mining an Ostrinia nubilalis midgut expressed sequence tag (EST) library for candidate genes and single nucleotide polymorphisms (SNPs). Insect Mol. Biol. 2008, 17:607-620.
11. Duan J., Li R., Cheng D., Fan W., Zha X., Cheng T., Wu Y., Wang J., Mita K., Xiang Z., Xia Q. SilkDB v2.0 a platform for silkworm (Bombyx mori) genome biology. Nucleic Acids Res. 2009, 38:D453-D456.
12. Emmerling M., Chandler D., Sandeman M. Molecular cloning of three cDNAs encoding aminopeptidases from the midgut if Helicoverpa punctigera, the Australian native budworm. Insect Biochem. Mol. Biol. 2001, 31:899-907.
13. Ferré J., Van Rie J. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 2002, 47:501-533.
14. Flanagan R.D., Cao-Guo Y., Mathis J.P., Meyer T.E., Shi X.M., Siquiera H.A.A., Siegfried B.D. Identification, cloning and expression of a Cry1Ab cadherin receptor of European corn borer Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae). Insect Biochem. Mol. Biol. 2005, 35:33-40.
15. Garczynski S.F., Adang M.J. Bacillus thuringiensis CrylA(c) δ-endotoxin binding APN in the Manduca sexta midgut has a glycosyl-phosphatidylinositol anchor. Insect Biochem. Mol. Biol. 1995, 25:409-415.
16. Gill M., Ellar D.J. Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1. Insect Mol. Biol. 2002, 11:619-625.
17. Herrero S., Gechev T., Bakker P.L., Moar W.J., de Maagd R.A. Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four aminopeptidases N genes. BMC Genomics 2005, 6:96.
18. Hooper N.M. Families of zinc metalloproteases. FEBS Lett. 1994, 354:1-6.
19. Hua G., Masson L., Jurat-Fuentes J.L., Schwab G., Adang M.J. Binding analysis of Bacillus thuringiensis Cry δ-endotoxins using brush border membrane vesicles of Ostrinia nubilalis. Appl. Environ. Microbiol. 2001, 67:872-879.
20. Ibiza-Palacios M.S., Ferré J., Higurashi S., Miyamoto K., Sato R., Escriche B. Selective inhibition of binding of Bacillus thuringiensis Cry1Ab toxin to cadherin-like and aminopeptidase proteins in brush-border membranes and dissociated epithelial cells from Bombyx mori. Biochem. J. 2008, 409:215-221.
21. Jurat-Fuentes J.L., Adang M.J. Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur. J. Biochem. 2004, 271:3127-3135.
22. Khajuria C., Zhu Y.C., Chen M.S., Buschman L.L., Higgins R.A., Yao J., Crespo A.L.B., Siegfried B.D., Muthukrishnan S., Zhu K.Y. Expressed sequence tags from larval gut of the European corn borer (Ostrinia nubilalis): exploring candidate genes potentially involved in Bacillus thuringiensis toxicity and resistance. BMC Genomics 2009, 10:286.
23. Knight P.J., Crickmore N., Ellar D.J. The receptor for Bacillus thuringiensis CrylA(c) delta-endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N. Mol. Microbiol. 1994, 11:429-436.
24. Koziel M.G., Beland G.L., Bowman C., Carozzi N.B., Crenshaw R., Crossland L., Dawson J., Desai N., Hill M., Kadwell S., Launis K., Lewis K., Maddox D., McPherson K., Meghji M.R., Merlin E., Rhodes R., Warren G.W., Wright M., Evola S.V. Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Biotechnology 1993, 11:194-200.
25. Lee, Siu Fai, 2006. Genome mapping in Lepidoptera. PhD Thesis, Department of Genetics, University of Melbourne, Melbourne, Australia.
26. Nakanishi K., Yaoi K., Nagino Y., Hara H., KitamiAtsumi S., Miura N., Sato R. Aminopeptidase N isoforms from the midgut of Bombyx mori and Plutella xylostella - their classification and the factors that determine their binding specificity to Bacillus thuringiensis Cry1A toxin. FEBS Lett. 2002, 9:215-220.
27. Ogutcu A., Suludere Z., Uzunhisarcikli M., Kalender Y. Effects of Bacillus thuringiensis on Malpighian tubule cells of Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae) larvae. Folia Biol. (Krakow) 2005, 53:7-11.
28. ©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
29. Piggot C.R., Ellar D.J. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 2007, 71:255-281.
30. Rajagopal R., Sivakumar S., Agrawal N., Malhotra P.M., Bhatnagar R.K. Silencing of midgut aminopeptidase N of Spodoptera litura by double stranded RNA establishes its role as Bacillus thuringiensis receptor. J. Biol. Chem. 2002, 277:46849-46851.
31. Schulz C., Perezgasga L., Fuller M.T. Genetic analysis of dPsa, the Drosophila orthologous of puromycin-sensitive aminopeptidase, suggests redundancy of aminopeptidases. Dev. Genes Evol. 2001, 211:581-588.
32. Simpson R.M., Poulton J., Markwick N.P. Expression levels of aminopeptidase-N genes in the lightbrown apple moth, Epiphyas postvittana. Insect Sci. 2008, 15:505-512.
33. Shimomura M., Minami H., Suetsugu Y., Ohyanagi H., Satoh C., Antonio B., Nagamura Y., Kadono-Okuda K., Kajiwara H., Sezutsu H., Nagaraju J., Goldsmith M.R., Xia Q., Yamamoto K., Mita K. KAIKObase: an integrated silkworm genome database and data mining tools. BMC Genomics 2009, 10:486.
34. Terra W.R., Ferreira C. Insect digestive enzymes: properties compartmentalization and function. Comp. Biochem. Phys. 1994, 109:1-62.
35. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
36. Thompson M.W., Tobler A., Fontana A., Hersh L.B. Cloning and analysis of the gene for the human puromycin-sensitive aminopeptidase. Biochem. Biophys. Res. Commun. 1999, 258:234-240.
37. Tobler A.R., Constam D.B., Schmitt-Graff A., Malipiero U., Schlapbach R., Fontana A. Cloning the human puromycin-sensitive aminopeptidase and evidence for expression in neurons. J. Neurochem. 1997, 68:889-897.
38. Vlahovic P., Stefanovic V. Kidney ectopeptidases. Structure, functions and clinical significance. Pathol. Biol. 1998, 46:779-786.
39. Vos P., Hogers R., Bleeker M., Reijans M., van de Lee T., Hornes M., Frijters A., Pot J., Peleman J., Kuiper M., Zabeu M. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995, 23:4407-4414.
40. Wang P., Zhang X., Zhang J. Molecular characterization of four midgut aminopeptidase N isozymes from the cabbage looper, Trichoplusia ni. Insect Biochem. Mol. Biol. 2005, 35:611-620.
41. Wyniger R. Insektenzucht. Methoden der Zucht und Haltung von Insekten und Milben im Laboratorium 1974, Verlag Eugen Ulmer, Stuttgart, Germany.
42. Xia Q., Cheng D., Duan J., Wang G., Cheng T., Zha X., Liu C., Zhao P., Dai F., Zhang Z., He N., Zhang L., Xiang Z. Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol. 2007, 8:R162.
43. Zhang S., Cheng H., Gao Y., Wang G., Liang G., Wu K. Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochem. Mol. Biol. 2009, 39:421-429.