N-glycosylation at non-canonical Asn-X-Cys sequence of an insect recombinant cathepsin B-like counter-defense protein

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 156, Issue 1, 2010, Pages 40-47

  Chi, Yong Hun ^a,b   Koo, Yoon Duck ^a   Dai, Susie Y ^a,c   Ahn, Ji Eun ^a   Yun, Dae Jin ^b   Lee, Sang Yeol ^b   Zhu Salzman, Keyan ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b Gyeongsang National University   (South Korea)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Cathepsin B; Counter defense; N glycosylation; Pichia; Site directed mutagenesis

Indexed keywords

CARBOHYDRATE; CATHEPSIN B LIKE CYSTEINE PROTEASE; CYSTEINE PROTEINASE; GLYCOSIDASE; MUTANT PROTEIN; PEPTIDE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME CHEMISTRY; ENZYME DEGRADATION; ENZYME MODIFICATION; ENZYME STABILITY; INSECT GENETICS; MOLECULAR WEIGHT; NONHUMAN; PICHIA PASTORIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; SITE DIRECTED MUTAGENESIS;

BRUCHINAE; HEXAPODA; PICHIA; PICHIA PASTORIS;

EID: 77950863798     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.01.017     Document Type: Article

References (47)

1. Ahn J.E., Salzman R.A., Braunagel S.C., Koiwa H., Zhu-Salzman K. Functional roles of specific bruchid protease isoforms in adaptation to a soybean protease inhibitor. Insect Mol. Biol. 2004, 13:649-657.
2. Ahn J.E., Zhu-Salzman K. CmCatD, a cathepsin D-like protease has a potential role in insect defense against a phytocystatin. J. Insect Physiol. 2009, 55:678-685.
3. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
4. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22:195-201.
5. Bayes A., Comellas-Bigler M., de la Vega M.R., Maskos K., Bode W., Aviles F.X., Jongsma M.A., Beekwilder J., Vendrell J. Structural basis of the resistance of an insect carboxypeptidase to plant protease inhibitors. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:16602-16607.
6. Bordoli L., Kiefer F., Arnold K., Benkert P., Battey J., Schwede T. Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc. 2009, 4:1-13.
7. Bown D.P., Wilkinson H.S., Gatehouse J.A. Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigara, are members of complex multigene families. Insect Biochem. Mol. Biol. 1997, 27:625-638.
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
9. Bretthauer R.K., Castellino F.J. Glycosylation of Pichia pastoris-derived proteins. Biotechnol. Appl. Biochem. 1999, 30:193-200.
10. Broadway R.M. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J. Insect Physiol. 1997, 43:855-874.
11. Brunelle F., Cloutier C., Michaud D. Colorado potato beetles compensate for tomato cathepsin D inhibitor expressed in transgenic potato. Arch. Insect Biochem. Physiol. 2004, 55:103-113.
12. Chi Y.H., Salzman R.A., Balfe S., Ahn J.E., Sun W., Moon J., Yun D.J., Lee S.Y., Higgins T.J., Pittendrigh B., Murdock L.L., Zhu-Salzman K. Cowpea bruchid midgut transcriptome response to a soybean cystatin-costs and benefits of counter-defence. Insect Mol. Biol. 2009, 18:97-110.
13. Cloutier C., Jean C., Fournier M., Yelle S., Michaud D. Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch. Insect Biochem. Physiol. 2000, 44:69-81.
14. De Leo F., Bonade-Bottino M.A., Ceci L.R., Gallerani R., Jouanin L. Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiol. 1998, 118:997-1004.
15. Delroisse J.M., Dannau M., Gilsoul J.J., El Mejdoub T., Destain J., Portetelle D., Thonart P., Haubruge E., Vandenbol M. Expression of a synthetic gene encoding a Tribolium castaneum carboxylesterase in Pichia pastoris. Protein Expr. Purif. 2005, 42:286-294.
16. Grinnell B.W., Walls J.D., Gerlitz B. Glycosylation of human protein C affects its secretion, processing, functional activities, and activation by thrombin. J. Biol. Chem. 1991, 266:9778-9785.
17. Hasnain S., Hirama T., Tam A., Mort J.S. Characterization of recombinant rat cathepsin-B and nonglycosylated mutants expressed in yeast-new insights into the pH-dependence of cathepsin B-catalyzed hydrolyses. J. Biol. Chem. 1992, 267:4713-4721.
18. Ishii T.M., Zerr P., Xia X.M., Bond C.T., Maylie J., Adelman J.P. Site-directed mutagenesis. Method Enzymol. 1998, 293:53-71.
19. Jongsma M.A., Bakker P.L., Peters J., Bosch D., Stiekema W.J. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:8041-8045.
20. Jongsma M.A., Bolter C. The adaptation of insects to plant protease inhibitors. J. Insect Physiol. 1997, 43:885-895.
21. Kiefer F., Arnold K., Kunzli M., Bordoli L., Schwede T. The SWISS-MODEL Repository and associated resources. Nucleic Acids Res. 2009, 37:D387-D392.
22. Kirschke H., Barrett A.J., Rawlings N.D. Proteinases 1. Lysosomal cysteine proteinases. Protein Profile 1995, 2:1587-1643.
23. Koo Y.D., Ahn J.E., Salzman R.A., Moon J., Chi Y.H., Yun D.J., Lee S.Y., Koiwa H., Zhu-Salzman K. Functional expression of an insect cathepsin B-like counter-defence protein. Insect Mol. Biol. 2008, 17:235-245.
24. Kopp J., Schwede T. The SWISS-MODEL repository: new features and functionalities. Nucleic Acids Res. 2006, 34:D315-D318.
25. Liu Y.L., Salzman R.A., Pankiw T., Zhu-Salzman K. Transcriptional regulation in southern corn rootworm larvae challenged by soyacystatin N. Insect Biochem. Mol. Biol. 2004, 34:1069-1077.
26. Marshall R.D. Glycoproteins. Annu. Rev. Biochem. 1972, 41:673-702.
27. Mazumdar-Leighton S., Broadway R.M. Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochem. Mol. Biol. 2001, 31:645-657.
28. Miletich J.P., Broze G.J. Beta-protein C is not glycosylated at asparagine-329-the rate of translation may influence the frequency of usage at asparagine-X-cysteine sites. J. Biol. Chem. 1990, 265:11397-11404.
29. Moon J., Salzman R.A., Ahn J.E., Koiwa H., Zhu-Salzman K. Transcriptional regulation in cowpea bruchid guts during adaptation to a plant defence protease inhibitor. Insect Mol. Biol. 2004, 13:283-291.
30. Murdock L.L., Brookhart G., Dunn P.E., Foard D.E., Kelley S., Kitch L., Shade R.E., Shukle R.H., Wolfson J.L. Cysteine digestive proteinases in coleoptera. Comp. Biochem. Physiol. 1987, 87B:783-787.
31. Musil D., Zucic D., Turk D., Engh R.A., Mayr I., Huber R., Popovic T., Turk V., Towatari T., Katunuma N., Bode W. The refined 2.15-a X-ray crystal structure of human liver cathepsin B-the structural basis for its specificity. EMBO J. 1991, 10:2321-2330.
32. Nakahara M., Koyama T., Nakazawa F., Nishio M., Shibamiya A., Hirosawa S. Gradually glycosylated protein C mutants (Arg178Gln and Cys331Arg) are degraded by proteasome after mannose trimming. Thromb. Haemost. 2004, 92:1284-1290.
33. Philip J.M., Fitches E., Harrison R.L., Bonning B., Gatehouse J.A. Characterisation of functional and insecticidal properties of a recombinant cathepsin L-like proteinase from flesh fly (Sarcophaga peregrina), which plays a role in differentiation of imaginal discs. Insect Biochem. Mol. Biol. 2007, 37:589-600.
34. Podobnik M., Kuhelj R., Turk V., Turk D. Crystal structure of the wild-type human procathepsin B at 2.5A resolution reveals the native active site of a papain-like cysteine protease zymogen. J. Mol. Biol. 1997, 271:774-788.
35. Sato C., Kim J.H., Abe Y., Saito K., Yokoyama S., Kohda D. Characterization of the N-oligosaccharides attached to the atypical Asn-X-Cys sequence of recombinant human epidermal growth factor receptor. J. Biochem. 2000, 127:65-72.
36. Schwede T., Kopp J., Guex N., Peitsch M.C. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 2003, 31:3381-3385.
37. Sebban-Kreuzer C., Deprez-Beauclair P., Berton A., Crenon I. High-level expression of nonglycosylated human pancreatic lipase-related protein 2 in Pichia pastoris. Protein Expr. Purif. 2006, 49:284-291.
38. Stack C.M., Dalton J.P., Cunneen M., Donnelly S. De-glycosylation of Pichia pastoris-produced Schistosoma mansoni cathepsin B eliminates non-specific reactivity with IgG in normal human serum. J. Immunol. Methods 2005, 304:151-157.
39. Takahashi T., Dehdarani A.H., Schmidt P.G., Tang J. Cathepsins B and H from porcine spleen. Purification, polypeptide chain arrangements, and carbohydrate content. J. Biol. Chem. 1984, 259:9874-9882.
40. Vance B.A., Bennett M.J., Ward Y., Gress R.G., Kearse K.P. Distinct but dispensable N-glycosylation of human CD69 proteins. Arch. Biochem. Biophys. 1999, 368:214-220.
41. Vance B.A., Wu W., Ribaudo R.K., Segal D.M., Kearse K.P. Multiple dimeric forms of human CD69 result from differential addition of N-glycans to typical (Asn-X-Ser/Thr) and atypical (Asn-X-cys) glycosylation motifs. J. Biol. Chem. 1997, 272:23117-23122.
42. Wang J.X., Zhao X.F., Liang Y.L., Li L., Zhang W., Ren Q., Wang L.C., Wang L.Y. Molecular characterization and expression of the antimicrobial peptide defensin from the housefly (Musca domestica). Cell. Mol. Life Sci. 2006, 63:3072-3082.
43. Weiner M.P., Costa G.L., Schoettlin W., Cline J., Mathur E., Bauer J.C. Site-directed mutagenesis of double-stranded DNA by the polymerase chain reaction. Gene 1994, 151:119-123.
44. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 2008, 9:40.
45. Zhang Y. I-TASSER: fully automated protein structure prediction in CASP8. Proteins 2009, 77(Suppl 9):100-113.
46. Zhang Y., Skolnick J. Automated structure prediction of weakly homologous proteins on a genomic scale. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:7594-7599.
47. Zhu-Salzman K., Koiwa H., Salzman R.A., Shade R.E., Ahn J.E. Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol. Biol. 2003, 12:135-145.