Structural characterization of two papaya chitinases, a family GH19 of glycosyl hydrolases

Cellular and Molecular Life Sciences

Volumn 63, Issue 24, 2006, Pages 3042-3054

  Huet, J ^a   Wyckmans, J ^a   Wintjens, R ^a   Boussard, P ^a   Raussens, V ^a   Vandenbussche, G ^a   Ruysschaert, J M ^a   Azarkan, M ^a   Looze, Y ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Amino acid sequence; Limited proteolysis; Proline concept; Secondary structure

Indexed keywords

CHITIN; CHITINASE; CHITOSAN; GLYCOSIDASE; POLYPROLINE II; PROLINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; CIRCULAR DICHROISM; INFRARED SPECTROSCOPY; MASS SPECTROMETRY; PAPAYA; PROTEIN DEGRADATION;

CARICA PAPAYA; TETRA;

EID: 33846051365     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-006-6320-3     Document Type: Article

References (52)

1. Henrissat, B. and Bairoch, A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293, 781-788.
2. Terwisscha van Scheltinga, A. C., Hennig, M. and Dijkstra, B. W. (1996) The 1.8 Å resolution structure of hevamine, a plant chitinase/lysozyme, and analysis of the conserved sequence and structure motifs of glycosyl hydrolase family 18. J. Mol. Biol. 262, 243-257.
3. Hart, P. J., Pluger, H. D., Monzingo, A. F., Hollis, T. and Robertus, J. D. (1995) The refined crystal structure of an endochitinase from Hordeum vulgare L. seeds at 1.8 Å resolution. J. Mol. Biol. 248, 402-413.
4. Hahn, M., Hennig, M., Schlesier, B. and Hohne, W. (2000) Structure of jack bean chitinase. Acta Crystallogr. D Biol. Crystallogr. 56, 1096-1099.
5. Iseli, B., Armand, S., Boller, T., Neuhaus, J. M. and Henrissat, B. (1996) Plant chitinases use two different hydrolytic mechanisms. FEBS Lett. 382, 186-188.
6. Durand, A., Hughes, R., Roussel, A., Flatman, R., Henrissat, B. and Juge, N. (2005) Emergence of a subfamily of xylanase inhibitors within glycoside hydrolase family 18. FEBS J. 272, 1745-1755.
7. El Moussaoui, A., Nijs, M., Paul, C., Wintjens, R., Vincentelli, J., Azarkan, M. and Looze, Y. (2001) Revisiting the enzymes stored in the laticifers of Carica papaya in the context of their possible participation in the plant defence mechanism. Cell. Mol. Life Sci. 58, 556-570.
8. Moutim, V., Silva, L. G., Lopes, M. T. P., Wilson Fermandes, G. and Salas, C. E. (1999) Spontaneous processing of peptides during coagulation of latex from Carica papaya. Plant Sci. 142, 115-121.
9. Pinitglang, S., Watts, A. B., Patel, M., Reid, J. D., Nobel, M. A., Gul, S., Bokth, A., Naeem, A., Patel, H., Thomas, E. W., Sreedharan, S. K., Verma, C. and Broklehurst, K. (1997) A classical enzyme active center motif lacks catalytic competence until modified electrostatically. Biochemistry 36, 9968-9982.
10. Song, I., Taylor, M., Baker, K. and Batman, R. C. Jr. (1995) Inhibition of cysteine proteinases by Carica papaya cystatin produced in Escherichia coli. Gene 162, 221-224.
11. Muzzarelli, R. A. A., Tomasetti, M. and Ilari, P. (1994) Depolymerization of chitosans with the aid of papain. Enzyme Microb. Technol. 16, 110-114.
12. Lin, H., Wang, H., Xue, C. and Ye, M. (2002) Preparation of chitosan oligomers by immobilized papain. Enzyme Microb. Technol. 31, 588-592.
13. Muzzarelli, R. A. A., Terbojevich, M., Muzzarelli, C. and Francescangeli, O. (2002) Chitosans depolymerised with the aid of papain and stabilized as glycosylamines. Carbohydr. Polymers 50, 69-78.
14. Azarkan, M., Amrani, A., Nijs, M., Vandermeers, A., Zerhouni, S., Smolders, N. and Looze, Y. (1997) Carica papaya latex is a rich source of a class II chitinase. Phytochemistry 46, 1319-1325.
15. Azarkan, M., Wintjens, R., Looze, Y. and Baeyens-Volant, D. (2004) Detection of three wound-induced proteins in papaya latex. Phytochemistry 65, 525-534.
16. Vishu Kumar A. B. and Tharanathan, R. N. (2004) A comparative study on depolymerisation of chitosan by proteolytic enzymes. Carbohydr. Polymers 58, 275-283.
17. Podoler, H. and Applebaum, S. W. (1971) The α-amylase of the beetle Callosobruchus chinensis. Biochem. J. 121, 321-325.
18. Erlanger, B. F., Kokowsky, N. and Cohen, W. (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95, 271-278.
19. Zhong, H., Marcus, S. L. and Li, L. (2005) Microwave-assisted acid hydrolysis of proteins combined with liquid chromatography MALDI MS/MS for protein identification. J. Am. Soc. Mass Spectrom. 16, 471-481.
20. Eftink, M. R., Jia, Y., Hu, D. and Ghiron, C. A. (1995) Fluorescence studies with tryptophan analogues: excited state interactions involving the side chain amino group. J. Phys. Chem. 99, 5713-5723.
21. Eftink, M. R. and Ghiron, C. A. (1984) Indole fluorescence quenching on proteins and model systems: use of the inefficient quencher succinimide. Biochemistry 23, 3891-3899.
22. Goormaghtigh, E., Raussens, V. and Ruysschaert, J. M. (1999) Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim. Biophys. Acta 1422, 105-185.
23. Oberg, K. A. and Fink, A. L. (1998) A new attenuated total reflectance Fourier transform infrared spectroscopy of proteins in solution. Anal. Biochem. 256, 92-106.
24. Sali, A. and Blundell, T. L. (1993) Comparative protein modeling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815.
25. Laskowski, R. A., Rullmann, J. A., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996) Aqua and Procheck-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486.
26. Novotny, J. and Bruccoleri, R. E. (1987) Correlation among sites of limited proteolysis, enzyme accessibility and segmental mobility. FEBS Lett. 211, 185-189.
27. Novotny, J., Handschumacher, M., Haber, E., Bruccoleri, R. E., Carlson, W. B., Fanning, D. W., Smith, J. A. and Rose, G. D. (1986) Antigenic determinants in proteins coincide with surface regions accessible to large probes (antibody domains). Proc. Natl. Acad. Sci. USA 83, 226-230.
28. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
29. Weber, G. and Young, L. B. (1964) Fragmentation of bovine serum albumin by pepsin. J. Biol. Chem. 239, 1415-1423.
30. Maeda, H., Chatani, E., Koyama, T., Sugiura, M., Izumi, H. and Hayashi, R. (2004) Indiscriminate glycosylation of procarboxypeptidase Y expressed in Pichia Pastoris. Carbohydrate Res. 339, 1041-1045.
31. Azarkan, M., El Moussaoui, A., van Wuytswinkel, D., Dehon, G. and Looze, Y. (2002) Fractionation and purification of the enzymes stored in the latex of Carica papaya. J. Chromatogr. B 790, 229-238.
32. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON and CDSSR methods with an expanded reference set. Anal. Biochem. 287, 252-260.
33. Chotia, C. and Lesk, A. M. (1986) The relation between the divergence of sequence and structure in proteins. EMBO J. 5, 823-826.
34. Howard, J. B. and Glazer, A. N. (1967) Studies of the physicochemical and enzymatic properties of papaya lysozyme. J. Biol. Chem. 242, 5715-5723.
35. Howard, J. B. and Glazer, A. N. (1969) Papaya lysozyme: Terminal sequences and enzymatic properties. J. Biol. Chem. 244, 1399-1409.
36. Subroto, T., Sufiati, S. and Beintema, J. J. (2000) Papaya (Carica papaya) lysozyme is a member of the family 19 (basic, class II) chitinases. J. Mol. Evol. 49, 819-821.
37. Dahlquist, F. W., Borders, C. L., Jacobson, G. and Raftery, M. A. (1969) The stereospecificity of human, hen and papaya lysozymes. Biochemistry, 8, 694-700.
38. Leah, R., Tommerup, H., Svendsen, I. and Mundy, J. (1991) Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J. Biol. Chem. 266, 1564-1573.
39. Hubbard, S. J., Beynon, R. J. and Thornton, J. M. (1998) Assessment of conformational parameters as predictors of limited proteolytic sites in native protein structures. Protein Eng. 11, 349-359.
40. Köditz, J., Ulbrich-Hofmann, R. and Arnold, U. (2004) Probing the unfolding region of ribonuclease A by site directed mutagenesis. Eur. J. Biochem. 272, 4147-4156.
41. Brömme, D., Peters, K., Fink, S. and Fittkan, S. (1986) Enzyme-substrate interactions in the hydrolysis of peptide substrates by thermitase, substilisin BNP', and proteinase. K. Arch. Biochem. Biophys. 244, 439-446.
42. Chiang, C. L., Chang, Y. M., Chang, C. T. and Sung, H. Y. (2005) Characterization of a chitosanase isolated from a commercial ficin preparation. J. Agric. Food Chem. 53, 7579-7585.
43. Hung, T. H., Chang, Y. M., Sung, H. Y. and Chang, C. T. (2002) Purification and characterization of hydrolase with chitinase and chitosanase activity from commercial stem bromelain. J. Agric. Food Chem. 50, 4666-4673.
44. Liao, Y. M., Su, J. L., Chiang, C. L. and Chang, C. T. (2000) Studies on the degradation of chitosan by crude proteolytic enzymes from hog stomach mucosa and Bacillus subtilisis. Taiwanese J. Agric. Chem. Food Sci. 38, 239-247.
45. Yamagami, T. and Funatsu, G. (1996) Limited proteolysis and reduction-carboxymethylation of rye seed chitinase-a: a role of the chitin-binding domain in its chitinase action. Biosci. Biotechnol. Biochem. 60, 1081-1086.
46. Kezuka, Y., Ohishi, M., Itoh, Y., Watanabe, J., Mitsutomi, M., Watanabe, T. and Nonaka, T. (2006) Structural studies of a two-domain chitinase from Streptomyces griseus HUT6037. J. Mol. Biol. 358, 472-484.
47. Kabasch, W. and Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.
48. Cubellis, M. V., Caillez, F., Blundell, T. L. and Lovell, S. C. (2005) Properties of polyproline II, a secondary structure element implicated in protein-protein interactions. Proteins 58, 880-892.
49. Oberg, K. A., Ruysschaert, J. M., Azarkan, M., Smolders, N., Zerhouni, S., Wintjens, R., Amrani, A. and Looze, Y. (1998) Papaya glutamine cyclase, a plant enzyme highly resistant to proteolysis, adopts an all-β conformation. Eur. J. Biochem. 258, 214-214.
50. Parott, I., Huang, P. C. and Khosla, C. (2002) Circular dichroism and nuclear magnetic resonance spectroscopic analysis of immunogenic gluten peptides and their analogs. J. Biol. Chem. 277, 45572-45578.
51. Oberg, K. A., Ruysschaert J.-M. and Goormaghtigh E. (2004) The optimization of protein secondary structure determination with infrared and circular dichroism spectra. Eur. J. Biochem. 271, 2937-2948.
52. Gilbert, S. M., Wellner, N., Belton, P. S., Greenfield, J. A., Siligardi, G., Shewry, P. R. and Tathan, A. S. (2000) Expression and characterization of a highly repetitive peptide derived from a wheat seed storage protein. Biochim. Biophys. Acta 1479, 135-146.