Two specific membrane-bound aminopeptidase N isoforms from Aedes aegypti larvae serve as functional receptors for the Bacillus thuringiensis Cry4Ba toxin implicating counterpart specificity

Biochemical and Biophysical Research Communications

Volumn 461, Issue 2, 2015, Pages 300-306

  Aroonkesorn, Aratee ^a   Pootanakit, Kusol ^a   Katzenmeier, Gerd ^a   Angsuthanasombat, Chanan ^a,b  

^a MAHIDOL UNIVERSITY   (Thailand)

^b Laboratory of Molecular Biophysics and Structural Biochemistry   (Thailand)

Author keywords

APN structure; Baculovirus expression system Cry; Cytotoxicity assay; Double immunolocalization; Membrane bound APN; endotoxin

Indexed keywords

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECT PROTEIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; ISOPROTEIN; MICROSOMAL AMINOPEPTIDASE;

AEDES; AMINO ACID SEQUENCE; ANIMAL; BACILLUS THURINGIENSIS; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; HOST PATHOGEN INTERACTION; LARVA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ALIGNMENT;

AEDES; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD13; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; CELL LINE; ENDOTOXINS; HEMOLYSIN PROTEINS; HOST-PATHOGEN INTERACTIONS; INSECT PROTEINS; LARVA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT;

EID: 84937762462     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2015.04.026     Document Type: Article

References (32)

1. E. Schnepf, N. Crickmore, J. Van Rie, D. Lereclus, J. Baum, J. Feitelson, D.R. Zeigler, and D.H. Dean Bacillus thuringiensis and its pesticidal crystal proteins Microbiol. Mol. Biol. Rev. 62 1998 775 806
2. C. Angsuthanasombat Structural basis of pore formation by mosquito-larvicidal proteins from Bacillus thuringiensis Open Toxinol J. 2010 119 125
3. E. Ben-Dov Bacillus thuringiensis subsp. israelensis and its dipteran-specific toxins Toxins 6 2014 1222 1243
4. J. Carroll, M.G. Wolfersberger, and D.J. Ellar The Bacillus thuringiensis Cry1Ac toxin-induced permeability change in Manduca sexta midgut brush border membrane vesicles proceeds by more than one mechanism J. Cell. Sci. 110 1997 3099 3104
5. P. Boonserm, P. Davis, D.J. Ellar, and J. Li Crystal structure of the mosquito-larvicidal toxin Cry4Ba and its biological implications J. Mol. Biol. 348 2005 363 382
6. S. Visitsattapongse, S. Sakdee, S. Leetacheewa, and C. Angsuthanasombat Single-reversal charge in the β10-β11 receptor-binding loop of Bacillus thuringiensis Cry4Aa and Cry4Ba toxins reflects their different toxicity against Culex spp. larvae Biochem. Biophys. Res. Commun. 450 2014 948 952
7. C.R. Pigott, and D.J. Ellar Role of receptors in Bacillus thuringiensis crystal toxin activity Microbiol. Mol. Biol. Rev. 71 2007 255 281
8. J. Chen, K.G. Aimanova, L.E. Fernandez, A. Bravo, M. Soberon, and S.S. Gill Aedes aegypti cadherin serves as a putative receptor of the Cry11Aa toxin from Bacillus thuringiensis subsp. israelensis Biochem. J. 424 2009 191 200
9. G. Hua, R. Zhang, M.A. Abdullah, and M.J. Adang Anopheles gambiae cadherin AgCad1 binds the Cry4Ba toxin of Bacillus thuringiensis israelensis and a fragment of AgCad1 synergizes toxicity Biochemistry 47 2008 5101 5110
10. L.E. Fernandez, K.G. Aimanova, S.S. Gill, A. Bravo, and M. Soberon A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae Biochem. J. 394 2006 77 84
11. L.E. Fernandez, C. Martinez-Anaya, E. Lira, J. Chen, A. Evans, S. Hernandez-Martinez, H. Lanz-Mendoza, A. Bravo, S.S. Gill, and M. Soberon Cloning and epitope mapping of Cry11Aa-binding sites in the Cry11Aa-receptor alkaline phosphatase from Aedes aegypti Biochemistry 48 2009 8899 8907
12. M. Dechklar, K. Tiewsiri, C. Angsuthanasombat, and K. Pootanakit Functional expression in insect cells of glycosylphosphatidylinositol-linked alkaline phosphatase from Aedes aegypti larval midgut: a Bacillus thuringiensis Cry4Ba toxin receptor Insect Biochem. Mol. Biol. 41 2011 159 166
13. G. Hua, R. Zhang, K. Bayyareddy, and M.J. Adang Anopheles gambiae alkaline phosphatase is a functional receptor of Bacillus thuringiensis jegathesan Cry11Ba toxin Biochemistry 48 2009 9785 9793
14. S. Saengwiman, A. Aroonkesorn, P. Dedvisitsakul, S. Sakdee, S. Leetachewa, C. Angsuthanasombat, and K. Pootanakit In vivo identification of Bacillus thuringiensis Cry4Ba toxin receptors by RNA interference knockdown of glycosylphosphatidylinositol-linked aminopeptidase N transcripts in Aedes aegypti larvae Biochem. Biophys. Res. Commun. 407 2011 708 713
15. J. Chen, K.G. Aimanova, S. Pan, and S.S. Gill Identification and characterization of Aedes aegypti aminopeptidase N as a putative receptor of Bacillus thuringiensis Cry11A toxin Insect Biochem. Mol. Biol. 39 2009 688 696
16. M.A. Abdullah, A.P. Valaitis, and D.H. Dean Identification of a Bacillus thuringiensis Cry11Ba toxin-binding aminopeptidase from the mosquito, Anopheles quadrimaculatus BMC Biochem. 7 2006 16
17. R. Zhang, G. Hua, T.M. Andacht, and M.J. Adang A 106-kDa aminopeptidase is a putative receptor for Bacillus thuringiensis Cry11Ba toxin in the mosquito Anopheles gambiae Biochemistry 47 2008 11263 11272
18. C. Lailak, T. Khaokhiew, C. Promptmas, B. Promdonkoy, K. Pootanakit, and C. Angsuthanasombat Bacillus thuringiensis Cry4Ba toxin employs two receptor-binding loops for synergistic interactions with Cyt2Aa2 Biochem. Biophys. Res. Commun. 435 2013 216 221
19. N.M. Hooper Families of zinc metalloproteases FEBS Lett. 354 1994 1 6
20. G. Kochan, T. Krojer, D. Harvey, R. Fischer, L. Chen, M. Vollmar, F. von Delft, K.L. Kavanagh, M.A. Brown, P. Bowness, P. Wordsworth, B.M. Kessler, and U. Oppermann Crystal structures of the endoplasmic reticulum aminopeptidase-1 (ERAP1) reveal the molecular basis for N-terminal peptide trimming Proc. Natl. Acad. Sci. U. S. A. 108 2011 7745 7750
21. T.T. Nguyen, S.-C. Chang, I. Evnouchidou, I.A. York, C. Zikos, K.L. Rock, A.L. Goldberg, E. Stratikos, and L.J. Stern Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1 Nat. Struct. Mol. Biol. 18 2011 604 613
22. N. Thamwiriyasati, S. Sakdee, P. Chuankhayan, G. Katzenmeier, C.J. Chen, and C. Angsuthanasombat Crystallization and preliminary X-ray crystallographic analysis of a full-length active form of the Cry4Ba toxin from Bacillus thuringiensis Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 66 2010 721 724
23. P. Benkert, S.C. Tosatto, and D. Schomburg QMEAN: a comprehensive scoring function for model quality assessment Proteins 71 2008 261 277
24. S.C. Lovell, I.W. Davis, W.B. Arendall 3rd, P.I. de Bakker, J.M. Word, M.G. Prisant, J.S. Richardson, and D.C. Richardson Structure validation by Cα geometry: phi,psi and Cβ deviation Proteins 50 2003 437 450
25. S. Atsumi, E. Mizuno, H. Hara, K. Nakanishi, M. Kitami, N. Miura, H. Tabunoki, A. Watanabe, and R. Sato Location of the Bombyx mori aminopeptidase N type 1 binding site on Bacillus thuringiensis Cry1Aa toxin Appl. Environ. Microbiol. 71 2005 3966 3977
26. S.S. Gill, E.A. Cowles, and V. Francis Identification, isolation, and cloning of a Bacillus thuringiensis CryIAc toxin-binding protein from the midgut of the lepidopteran insect Heliothis virescens J. Biol. Chem. 270 1995 27277 27282
27. C.M. Crava, Y. Bel, S.F. Lee, B. Manachini, D.G. Heckel, and B. Escriche Study of the aminopeptidase N gene family in the lepidopterans Ostrinia nubilalis (Hubner) and Bombyx mori (L.): sequences, mapping and expression Insect Biochem. Mol. Biol. 40 2010 506 515
28. P.J. Knight, J. Carroll, and D.J. Ellar Analysis of glycan structures on the 120 kDa aminopeptidase N of Manduca sexta and their interactions with Bacillus thuringiensis Cry1Ac toxin Insect Biochem. Mol. Biol. 34 2004 101 112
29. A. Thammasittirong, M. Dechklar, S. Leetachewa, K. Pootanakit, and C. Angsuthanasombat Aedes aegypti membrane-bound alkaline phosphatase expressed in Escherichia coli retains high-affinity binding for Bacillus thuringiensis Cry4Ba toxin Appl. Environ. Microbiol. 77 2011 6836 6840
30. L. Portugal, J.L. Gringorten, G.F. Caputo, M. Soberon, C. Munoz-Garay, and A. Bravo Toxicity and mode of action of insecticidal Cry1A proteins from Bacillus thuringiensis in an insect cell line, CF-1 Peptides 53 2014 292 299
31. K.J. Garner, S. Hiremath, K. Lehtoma, and A.P. Valaitis Cloning and complete sequence characterization of two gypsy moth aminopeptidase-N cDNAs, including the receptor for Bacillus thuringiensis Cry1Ac toxin Insect Biochem. Mol. Biol. 29 1999 527 535
32. P.J. Knight, B.H. Knowles, and D.J. Ellar Molecular cloning of an insect aminopeptidase N that serves as a receptor for Bacillus thuringiensis CryIA(c) toxin J. Biol. Chem. 270 1995 17765 17770