Studies on the Chitin Binding Property of Novel Cysteine-Rich Peptides from Alternanthera sessilis

Biochemistry

Volumn 54, Issue 43, 2015, Pages 6639-6649

  Kini, Shruthi G ^a   Nguyen, Phuong Q T ^a   Weissbach, Sophie ^b   Mallagaray, Alvaro ^b   Shin, Joon ^a   Yoon, Ho Sup ^a   Tam, James P ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; BINS; BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; CHITIN; COVALENT BONDS; DISSOCIATION; GENE ENCODING; NUCLEAR MAGNETIC RESONANCE; PLANTS (BOTANY); TITRATION;

BINDING INTERACTION; CHITIN BINDING DOMAINS; CHITIN OLIGOSACCHARIDE; DISSOCIATION CONSTANT; ENDOPLASMIC RETICULUM; ENZYMATIC DEGRADATION; ISOLATION AND CHARACTERIZATION; NUCLEAR MAGNETIC RESONANCE(NMR);

PEPTIDES;

ANTIBIOTIC AGENT; CHITIN; CYSTEINE; GLYCINE; HEVEIN; HEVEIN LIKE PEPTIDE; PEPTIDE; PROLINE; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; PROTEIN BINDING; VEGETABLE PROTEIN;

ALTERNANTHERA SESSILIS; ANTIBACTERIAL ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLITORIA TERNATEA; CYSTINE KNOT MOTIF; DRUG PROTEIN BINDING; ENDOPLASMIC RETICULUM; ENZYMATIC DEGRADATION; ENZYME STABILITY; ESCHERICHIA COLI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROGEN BOND; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR CLONING; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; STAPHYLOCOCCUS AUREUS; AMARANTHACEAE; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PLANT GENE; PROTEIN STABILITY; SEQUENCE HOMOLOGY;

AMARANTHACEAE; AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; BINDING SITES; CHITIN; CYSTEINE; GENES, PLANT; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PLANT PROTEINS; PROTEIN BINDING; PROTEIN STABILITY; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84946430124     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00872     Document Type: Article

References (51)

1. Slavokhotova, A. A., Naumann, T. A., Price, N. P. J., Rogozhin, E. A., Andreev, Y. A., Vassilevski, A. A., and Odintsova, T. I. (2014) Novel mode of action of plant defense peptides-hevein-like antimicrobial peptides from wheat inhibit fungal metalloproteases FEBS J. 281, 4754-4764 10.1111/febs.13015
2. Archer, B. L. (1960) The Proteins of Hevea brasiliensis Latex Isolation and Characterization of Crystalline Hevein Biochem. J. 75, 236-240 10.1042/bj0750236
3. Van Parijs, J., Broekaert, W. F., Goldstein, I. J., and Peumans, W. J. (1991) Hevein: an antifungal protein from rubber-tree (Hevea brasiliensis) latex Planta 183, 258-264 10.1007/BF00197797
4. Sanchez-Monge, R., Blanco, C., Perales, A. D., Collada, C., Carrillo, T., Aragoncillo, C., and Salcedo, G. (2000) Class I chitinases, the panallergens responsible for the latex-fruit syndrome, are induced by ethylene treatment and inactivated by heating J. Allergy Clin. Immunol. 106, 190-195 10.1067/mai.2000.107599
5. Blanco, C., Diaz-Perales, A., Collada, C., Sanchez-Monge, R., Carrillo, T., Aragoncillo, C., and Salcedo, G. (2000) Cross-reactions in the latex-fruit syndrome: A relevant role of chitinases but not of cross-reactive carbohydrate determinants J. Allergy Clin. Immunol. 105, S238 10.1016/S0091-6749(00)91133-3
6. Jiménez-Barbero, J., Javier Cañada, F., Asensio, J. L., Aboitiz, N., Vidal, P., Canales, A., Groves, P., Gabius, H.-J., and Siebert, H.-C. (2006) Hevein Domains: An Attractive Model to Study Carbohydrate-Protein Interactions at Atomic Resolution Adv. Carbohydr. Chem. Biochem. 60, 303-354 10.1016/S0065-2318(06)60007-3
7. Peumans, W. J. and Van Damme, E. J. (1998) Plant lectins: specific tools for the identification, isolation, and characterization of O-linked glycans Crit Rev. Biochem Mol. Biol. 33, 209-258
8. Asensio, J. L., Siebert, H. C., von der Lieth, C.-W., Laynez, J., Bruix, M., Soedjanaamadja, U. M., Beintema, J. J., Cañada, F. J., Gabius, H.-J., and Jimenez-Barbero, J. (2000) NMR Investigations of Protein-Carbohydrate Interactions:Studies on the Relevance of Trp/Tyr Variations in Lectin Binding Sites as Deduced from Titration Microcalorimetry and NMR Studies on Hevein Domains. Determination of the NMR Structure of the Complex Between Pseudohevein and N,N′,Na″-Triacetylchitotriose Proteins: Struct., Funct., Genet. 40, 218-236 10.1002/(SICI)1097-0134(20000801)40:2<218::AID-PROT50>3.3.CO;2-G
9. Wright, H. T., Sandrasegaram, G., and Wright, C. S. (1991) Evolution of a family of N-acetylglucosamine binding proteins containing the disulfide-rich domain of wheat germ agglutinin J. Mol. Evol. 33, 283-294 10.1007/BF02100680
10. Drenth, J., Low, B. W., Richardson, J. S., and Wright, C. S. (1980) The Toxin-Agglutinin Fold-a New Group of Small Protein Structures Organized around a 4-Disulfide Core J. Biol. Chem. 255, 2652-2655
11. Lipkin, A., Anisimova, V., Nikonorova, A., Babakov, A., Krause, E., Bienert, M., Grishin, E., and Egorov, T. (2005) An antimicrobial peptide Ar-AMP from amaranth (Amaranthus retroflexus L.) seeds Phytochemistry 66, 2426-2431 10.1016/j.phytochem.2005.07.015
12. Broekaert, W. F., Marien, W., Terras, F. R. G., De Bolle, M. F. C., Proost, P., Van Damme, J., Dillen, L., Claeys, M., and Rees, S. B. (1992) Antimicrobial peptides from Amaranthus caudatus seeds with sequence homology to the cysteine glycine-rich domain of chitin-binding proteins Biochemistry 31, 4308-4314 10.1021/bi00132a023
13. Pallaghy, P. K., Nielsen, K. J., Craik, D. J., and Norton, R. S. (1994) A common structural motif incorporating a cystine knot and a triple-stranded B-sheet in toxic and inhibitory polypeptides Protein Sci. 3, 1833-1839 10.1002/pro.5560031022
14. Nguyen, G. K., Zhang, S., Nguyen, N. T., Nguyen, P. Q., Chiu, M. S., Hardjojo, A., and Tam, J. P. (2011) Discovery and characterization of novel cyclotides originated from chimeric precursors consisting of albumin-1 chain a and cyclotide domains in the Fabaceae family J. Biol. Chem. 286, 24275-24287 10.1074/jbc.M111.229922
15. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of Exchange Processes by 2-Dimensional Nmr-Spectroscopy J. Chem. Phys. 71, 4546-4553 10.1063/1.438208
16. Kumar, A., Ernst, R. R., and Wuthrich, K. (1980) A Two-Dimensional Nuclear Overhauser Enhancement (2d Noe) Experiment for the Elucidation of Complete Proton-Proton Cross-Relaxation Networks in Biological Macromolecules Biochem. Biophys. Res. Commun. 95, 1-6 10.1016/0006-291X(80)90695-6
17. Davis, D. G. and Bax, A. (1985) Assignment of Complex H-1-Nmr Spectra Via Two-Dimensional Homonuclear Hartmann-Hahn Spectroscopy J. Am. Chem. Soc. 107, 2820-2821 10.1021/ja00295a052
18. Bax, A. and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy J. Magn. Reson. 65, 355-360 10.1016/0022-2364(85)90018-6
19. Rance, M., Sørensen, O. W., Bodenhausen, G., Wagner, G., Ernst, R. R., and Wuthrich, K. (1983) Improved spectral resolution in cosy 1H NMR spectra of proteins via double quantum filtering Biochem. Biophys. Res. Commun. 117, 479-485 10.1016/0006-291X(83)91225-1
20. Wuthrich, K., Billeter, M., and Braun, W. (1983) Pseudo-Structures for the 20 Common Amino-Acids for Use in Studies of Protein Conformations by Measurements of Intramolecular Proton Proton Distance Constraints with Nuclear Magnetic-Resonance J. Mol. Biol. 169, 949-961 10.1016/S0022-2836(83)80144-2
21. Liu, M., Mao, X.-A., Ye, C., Huang, H., Nicholson, J., and Lindon, J. (1998) Improved WATERGATE Pulse Sequences for Solvent Suppression in NMR Spectroscopy J. Magn. Reson. 132, 125-129 10.1006/jmre.1998.1405
22. Hwang, T. L. and Shaka, A. J. (1995) Water Suppression That Works. Excitation Sculpting Using Arbitrary Wave-Forms and Pulsed-Field Gradients J. Magn. Reson., Ser. A 112, 275-279 10.1006/jmra.1995.1047
23. Delaglio, F., Grzesiek, S., Vuister, G., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293 10.1007/BF00197809
24. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921 10.1107/S0907444998003254
25. Pardi, A., Billeter, M., and Wüthrich, K. (1984) Calibration of the angular dependence of the amide proton-Cα proton coupling constants, 3JHNα, in a globular protein J. Mol. Biol. 180, 741-751 10.1016/0022-2836(84)90035-4
26. Driscoll, P. C., Gronenborn, A. M., Beress, L., and Clore, G. M. (1989) Determination of the three-dimensional solution structure of the antihypertensive and antiviral protein BDS-I from the sea anemone Anemonia sulcata: a study using nuclear magnetic resonance and hybrid distance geometry-dynamical simulated annealing Biochemistry 28, 2188-2198 10.1021/bi00431a033
27. Nilges, M., Clore, G. M., and Gronenborn, A. M. (1988) Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations FEBS Lett. 229, 317-324 10.1016/0014-5793(88)81148-7
28. Nilges, M., Gronenborn, A., Brünger, A., and Clore, M. (1988) Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2 Protein Eng., Des. Sel. 2, 27-38 10.1093/protein/2.1.27
29. Nilges, M. (1993) A calculation strategy for the structure determination of symmetric demers by 1H NMR Proteins: Struct., Funct., Genet. 17, 297-309 10.1002/prot.340170307
30. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures J. Mol. Graphics 14, 51-55 10.1016/0263-7855(96)00009-4
31. The PyMOL Molecular Graphics System, version 1.7.4 (2014) Schrödinger, LLC, Portland, OR.
32. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291 10.1107/S0021889892009944
33. Williamson, M. P. (2013) Using chemical shift perturbation to characterise ligand binding Prog. Nucl. Magn. Reson. Spectrosc. 73, 1-16 10.1016/j.pnmrs.2013.02.001
34. Doyle, J. J. and Doyle, J. L. (1987) Rapid DNA isolation procedure for small quantities of fresh leaf tissue Phytochem Bull. 19, 11-15
35. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions Nat. Methods 8, 785-786 10.1038/nmeth.1701
36. Hall, T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp. Ser. 41, 95-98
37. Lehrer, R. I., Rosenman, M., Harwig, S. S. S. L., Jackson, R., and Eisenhauer, P. (1991) Ultrasensitive Assays for Endogenous Antimicrobial Polypeptides J. Immunol. Methods 137, 167-173 10.1016/0022-1759(91)90021-7
38. Huang, X. and Miller, W. (1991) A Time-Efficient, Linear-Space Local Similarity Algorithm Adv. Appl. Math 12, 337-357 10.1016/0196-8858(91)90017-D
39. Feeney, J., Batchelor, J. G., Albrand, J. P., and Roberts, G. C. K. (1979) Effects of Intermediate Exchange Processes on the Estimation of Equilibrium-Constants by Nmr J. Magn. Reson. 33, 519-529 10.1016/0022-2364(79)90163-X
40. Lian, L. Y. (1993) Dynamic and exchange processes in macromolecules studied by NMR spectroscopy Method mol biol 17, 169-189 10.1385/0-89603-215-9:169
41. Klaus, K., Nielsen, j. E. N., Madrid, S. M., and Mikkelsen, J. D. (1997) Characterization of a New Antifungal Chitin-Binding Peptide from Sugar Beet Leaves Plant Physiol 113, 83-91 10.1104/pp.113.1.83
42. Jennings, C., West, J., Waine, C., Craik, D., and Anderson, M. (2001) Biosynthesis and insecticidal properties of plant cyclotides: The cyclic knotted proteins from Oldenlandia affinis Proc. Natl. Acad. Sci. U. S. A. 98, 10614-10619 10.1073/pnas.191366898
43. Nguyen, G. K. T., Zhang, S., Wang, W., Wong, C. T. T., Nguyen, N. T. K., and Tam, J. P. (2011) Discovery of a Linear Cyclotide from the Bracelet Subfamily and Its Disulfide Mapping by Top-down Mass Spectrometry J. Biol. Chem. 286, 44833-44844 10.1074/jbc.M111.290296
44. Nguyen, P. Q. T., Luu, T. T., Bai, Y., Nguyen, G. K. T., Pervushin, K., and Tam, J. P. (2015) Allotides: Proline-Rich Cystine Knot α-Amylase Inhibitors from Allamanda cathartica J. Nat. Prod. 78, 695-704 10.1021/np500866c
45. Mergaert, P., Nikovics, K., Kelemen, Z., Maunoury, N., Vaubert, D., Kondorosi, A., and Kondorosi, E. (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs Plant Physiol. 132, 161-173 10.1104/pp.102.018192
46. De Bolle, M. F. C., David, K. M. M., Rees, S. B., Vanderleyden, J., Cammue, B. P., and Broekaert, W. F. (1993) Cloning and characterization of a cDNA encoding an antimicrobial chitin-binding protein from amaranth,Amaranthus caudatus Plant Mol. Biol. 22, 1187-1190 10.1007/BF00028991
47. Andreev, Y. A., Korostyleva, T. V., Slavokhotova, A. A., Rogozhin, E. A., Utkina, L. L., Vassilevski, A. A., Grishin, E. V., Egorov, T. A., and Odintsova, T. I. (2012) Genes encoding hevein-like defense peptides in wheat: distribution, evolution, and role in stress response Biochimie 94, 1009-1016 10.1016/j.biochi.2011.12.023
48. Asensio, J. L., Canada, F. J., Bruix, M., Rodriguezromero, A., and Jimenezbarbero, J. (1995) The Interaction of Hevein with N-Acetylglucosamine-Containing Oligosaccharides-Solution Structure of Hevein Complexed to Chitobiose Eur. J. Biochem. 230, 621-633 10.1111/j.1432-1033.1995.0621h.x
49. Espinosa, J. F., Asensio, J. L., Garcia, J. L., Laynez, J., Bruix, M., Wright, C., Siebert, H.-C., Gabius, H.-J., Cañada, F. J., and Jiménez-Barbero, J. (2000) NMR investigations of protein-carbohydrate interactions binding studies and refined three-dimensional solution structure of the complex between the B domain of wheat germ agglutinin and N,N′,Na″-triacetylchitotriose Eur. J. Biochem. 267, 3965-3978 10.1046/j.1432-1327.2000.01415.x
50. Verheyden, P., Pletinckx, J., Maes, D., Pepermans, H. A. M., Wyns, L., Willem, R., and Martins, J. C. (1995) 1H NMR study of the interaction of triacetyl chitotriose with Ac-AMP2, a sugar binding antimicrobial protein isolated from A.caudatus FEBS Lett. 370, 245-249 10.1016/0014-5793(95)00835-W
51. Asensio, J. L., Cañada, F. J., Siebert, H.-C., Laynez, J., Poveda, A., Nieto, P. M., Soedjanaamadja, U. M., Gabius, H.-J., and Jiménez-Barbero, J. (2000) Structural basis for chitin recognition by defense proteins: GlcNAc residues are bound in a multivalent fashion by extended binding sites in hevein domains Chem. Biol. 7, 529-543 10.1016/S1074-5521(00)00136-8