Heterogonous expression and characterization of a plant class IV chitinase from the pitcher of the carnivorous plant Nepenthes alata

Glycobiology

Volumn 22, Issue 3, 2012, Pages 345-351

  Ishisaki, Kana ^a   Honda, Yuji ^a   Taniguchi, Hajime ^a   Hatano, Naoya ^b,c   Hamada, Tatsuro ^a  

^a ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^b RIKEN SPring 8 Center   (Japan)

^c KOBE UNIVERSITY   (Japan)

Author keywords

carnivorous plant; chitinase; class IV; GH family 19; Nepenthes

Indexed keywords

ACETIC ACID; CHITINASE; CLASS IV CHITINASE; GLYCOSIDASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CARNIVOROUS PLANT; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ESCHERICHIA COLI; HYDROLYSIS; NEPENTHES ALATA; NONHUMAN; NORWAY SPRUCE; PH; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TEMPERATURE;

ACETYLGLUCOSAMINE; AMINO ACID SEQUENCE; CARYOPHYLLACEAE; CATALYTIC DOMAIN; CHITINASE; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLONING, MOLECULAR; GENE EXPRESSION; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; KINETICS; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

ESCHERICHIA COLI; NEPENTHES; NEPENTHES ALATA; PICEA ABIES;

EID: 84856301036     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwr142     Document Type: Article

References (46)

1. Amagase S, Mori M, Nakayama S. 1972. Digestive enzymes in insectivorous plants. IV. Enzymatic digestion of insects by Nepenthes secretion and Drosera peltata extract: Proteolytic and chitinolytic activities. J Biochem. 72:765-767.
2. Andersen MD, Jensen A, Robertus JD, Leah R, Skriver K. 1997. Heterologous expression and characterization of wild-type and mutant forms of a 26 kDa endochitinase from barley (Hordeum vulgare L.). Biochem J. 322 (Pt 3):815-822. (Pubitemid 27135629)
3. Armand S, Tomita H, Heyraud A, Gey C, Watanabe T, Henrissat B. 1994. Stereochemical course of the hydrolysis reaction catalyzed by chitinases A1 and D from Bacillus circulans WL-12. FEBS Lett. 343:177-180.
4. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes database (CAZy): An expert resource for glycogenomics. Nucleic Acids Res. 37:D233-D238.
5. Chen YT, Hsu LH, Huang IP, Tsai TC, Lee GC, Shaw JF. 2007. Gene cloning and characterization of a novel recombinant antifungal chitinase from papaya (Carica papaya). J Agric Food Chem. 55:714-722.
6. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K. 1993. Plant chitinases. Plant J. 3:31-40.
7. Dixon M, Webb EC. 1979. Inhibition by High Substrate Concentrations. Enzymes. London: Longman Group. p. 126-133.
8. Eilenberg H, Pnini-Cohen S, Schuster S, Movtchan A, Zilberstein A. 2006. Isolation and characterization of chitinase genes from pitchers of the carnivorous plant Nepenthes khasiana. J Exp Bot. 57:2775-2784. (Pubitemid 44290308)
9. Fukamizo T, Koga D, Goto S. 1995. Comparative biochemistry of chitinases-anomeric form of the reaction products. Biosci Biotech Biochem. 59:311-313.
10. Fung K-L, Zhao K-J, He Z-M, Chye M-L. 2002. Tobacco-expressed Brassica juncea chitinase BjCHI1 shows antifungal activity in vitro. Plant Mol Biol. 50:283-294. (Pubitemid 38458821)
11. Hahn M, Hennig M, Schlesier B, Hohne W. 2000. Structure of jack bean chitinase. Acta Crystallogr D Biol Crystallogr. 56:1096-1099.
12. Hart PJ, Pfluger HD, Monzingo AF, Hollis T, Robertus JD. 1995. The refined crystal structure of an endochitinase from Hordeum vulgare L. seeds at 1.8 A resolution. J Mol Biol. 248:402-413.
13. Hatano N, Hamada T. 2008. Proteome analysis of pitcher fluid of the carnivorous plant Nepenthes alata. J Proteome Res. 7:809-816. (Pubitemid 351294045)
14. Hollis T, Honda Y, Fukamizo T, Marcotte E, Day PJ, Robertus JD. 1997. Kinetic analysis of barley chitinase. Arch Biochem Biophys. 344:335-342. (Pubitemid 27344070)
15. Honda Y, Kitaoka M, Hayashi K. 2004. Kinetic evidence related to substrate-assisted catalysis of family 18 chitinases. FEBS Lett. 567:307-310. (Pubitemid 38748411)
16. Huet J, Rucktooa P, Clantin B, Azarkan M, Looze Y, Villeret V, Wintjens R. 2008. X-ray structure of papaya chitinase reveals the substrate binding mode of glycosyl hydrolase family 19 chitinases. Biochemistry. 47:8283-8291.
17. Imoto T, Yagishita K. 1971. Simple activity measurement of lysozyme. Agric Biol Chem. 35:1154-1156.
18. Iseli B, Boller T, Neuhaus JM. 1993. The N-terminal cysteine-rich domain of tobacco class I chitinase is essential for chitin binding but not for catalytic or antifungal activity. Plant Physiol. 103:221-226.
19. Kaomek M, Mizuno K, Fujimura T, Sriyotha P, Cairns JRK. 2003. Cloning, expression, and characterization of an antifungal chitinase from Leucaena leucocephala de Wit. Biosci Biotechnol Biochem. 67:667-676. (Pubitemid 39251893)
20. Kawase T, Yokokawa S, Saito A, Fujii T, Nikaidou N, Miyashita K, Watanabe T. 2006. Comparison of enzymatic and antifungal properties between family 18 and 19 chitinases from S. coelicolor A3(2). Biosci Biotechnol Biochem. 70:988-998.
21. Kezuka Y, Ohishi M, Itoh Y, Watanabe J, Mitsutomi M, Watanabe T, Nonaka T. 2006. Structural studies of a two-domain chitinase from Streptomyces griseus HUT6037. J Mol Biol. 358:472-484.
22. Koga D, Yoshioka T, Arakane Y. 1998. HPLC analysis of anomeric formation and cleavage pattern by chitinolytic enzyme. Biosci Biotechnol Biochem. 62:1643-1646. (Pubitemid 128475106)
23. Kramer KJ, Muthukrishnan S. 2009. Chitin metabolism in insects. In: Amsterdam LIG, editor. Insect Development: Morphogenesis, Molting and Metamorphosis. Boston: Academic Press. p. 497-530.
24. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
25. Melchers LS, Groot MA-d, Van Der Knaap JA, Ponstein AS, Sela-Buurlage MB, Bol JF, Cornelissen BJC, Van Den Elzen PJM, Linthorst HJM. 1994. A new class of tobacco chitinases homologous to bacterial exo-chitinases displays antifungal activity. Plant J. 5:469-480.
26. Mithöfer A. 2011. Carnivorous pitcher plants: Insights in an old topic. Phytochemistry. 72:1678-1682.
27. Mizuno R, Fukamizo T, Sugiyama S, Nishizawa Y, Kezuka Y, Nonaka T, Suzuki K, Watanabe T. 2008. Role of the loop structure of the catalytic domain in rice class I chitinase. J Biochem. 143:487-495. (Pubitemid 351451774)
28. Moran JA, Clarke CM. 2010. The carnivorous syndrome in Nepenthes pitcher plants: Current state of knowledge and potential future directions. Plant Signal Behav. 5:644-648.
29. Nishimura S-I, Kuzuhara H, Takiguchi Y, Shimahara K. 1989. Peracetylated chitobiose: Preparation by specific degradations of chitin, and chemical manipulations. Carbohydr Res. 194:223-231.
30. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T. 1995. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4:2411-2423.
31. Shibuya N, Minami E. 2001. Oligosaccharide signalling for defence responses in plant. Physiol Mol Plant Pathol. 59:223-233. (Pubitemid 34018124)
32. Shinshi H, Neuhaus J-M, Ryals J, Meins F. 1990. Structure of a tobacco endochitinase gene: Evidence that different chitinase genes can arise by transposition of sequences encoding a cysteine-rich domain. Plant Mol Biol. 14:357-368.
33. Slack A. 2000. Carnivorous Plants. Cambridge: The MIT Press.
34. Taira T. 2010. Structures and antifungal activity of plant chitinases. J Appl Glycosci. 57:167-176.
35. Taira T, Mahoe Y, Kawamoto N, Onaga S, Iwasaki H, Ohnuma T, Fukamizo T. 2011. Cloning and characterization of a small family 19 chitinase from moss (Bryum coronatum). Glycobiology. 21:644-654.
36. Taira T, Ohdomari A, Nakama N, Shimoji M, Ishihara M. 2005. Characterization and antifungal activity of gazyumaru (Ficus microcarpa) latex chitinases: Both the chitin-binding and the antifungal activities of class I chitinase are reinforced with increasing ionic strength. Biosci Biotechnol Biochem. 69:811-818. (Pubitemid 40793788)
37. Taira T, Toma N, Ishihara M. 2005. Purification, characterization, and antifungal activity of chitinases from pineapple (Ananas comosus) leaf. Biosci Biotechnol Biochem. 69:189-196. (Pubitemid 40383499)
38. Terwisscha van Scheltinga AC, Armand S, Kalk KH, Isogai A, Henrissat B, Dijkstra BW. 1995. Stereochemistry of chitin hydrolysis by a plant chitinase/lysozyme and X-ray structure of a complex with allosamidin: Evidence for substrate assisted catalysis. Biochemistry. 34:15619-15623.
39. Tews I, Terwisscha van Scheltinga AC, Perrakis A, Wilson KS, Dijkstra BW. 1997. Substrate-assisted catalysis unifies two families of chitinolytic enzymes. J Am Chem Soc. 119:7954-7959. (Pubitemid 27380255)
40. Theis T, Stahl U. 2004. Antifungal proteins: Targets, mechanisms and prospective applications. Cell Mol Life Sci. 61:437-455. (Pubitemid 38316580)
41. Truong NH, Park SM, Nishizawa Y, Watanabe T, Sasaki T, Itoh Y. 2003. Structure, heterologous expression, and properties of rice (Oryza sativa L.) family 19 chitinases. Biosci Biotechnol Biochem. 67:1063-1070. (Pubitemid 39251865)
42. Ubhayasekera W. 2011. Structure and function of chitinases from glycoside hydrolase family 19. Polymer International. 60:890-896.
43. Ubhayasekera W, Rawat R, Ho S, Wiweger M, Von Arnold S, Chye M-L, Mowbray S. 2009. The first crystal structures of a family 19 class IV chitinase: The enzyme from Norway spruce. Plant Mol Biol. 71:277-289.
44. Ubhayasekera W, Tang CM, Ho SW, Berglund G, Bergfors T, Chye ML, Mowbray SL. 2007. Crystal structures of a family 19 chitinase from Brassica juncea show flexibility of binding cleft loops. FEBS J. 274:3695-3703. (Pubitemid 47052411)
45. van Loon LC, Rep M, Pieterse CM. 2006. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol. 44:135-162. (Pubitemid 44435701)
46. Vogelsang R, Barz W. 1993. Purification, characterization and differential hormonal regulation of a β-1,3-glucanase and two chitinases from chickpea (Cicer arietinum L.). Planta. 189:60-69.