Enzymatic characterization and molecular modeling of an evolutionarily interesting fungal β-N-acetylhexosaminidase

FEBS Journal

Volumn 278, Issue 14, 2011, Pages 2469-2484

  Ryšlavá, Helena ^a   Kalendová, Alžběta ^a   Doubnerová, Veronika ^a   Skočdopol, Přemysl ^a   Kumar, Vinay ^a,b   Kukačka, Zdeněk ^a   Pompach, Petr ^a,c   Vaněk, Ondřej ^a   Slámová, Kristýna ^c   Bojarová, Pavla ^c   Kulik, Natallia ^d   Ettrich, Rudiger ^d   Křen, Vladimír ^c   Bezouška, Karel ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b TULANE UNIVERSITY   (United States)

^c INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^d UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

deglycosylation; enzyme kinetics; hexosaminidase; molecular dynamics; molecular modeling

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; ENDOGLYCOSIDASE H; GLYCOSIDASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CHEMISTRY; ENZYME GLYCOSYLATION; ENZYME ISOLATION; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME STRUCTURE; MOLECULAR CLONING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR MODEL; MOLECULAR WEIGHT; NONHUMAN; PENICILLIUM; PENICILLIUM OXALICUM; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; BETA-N-ACETYLHEXOSAMINIDASES; CATALYTIC DOMAIN; CONSERVED SEQUENCE; ENZYME PRECURSORS; ENZYME STABILITY; FUNGAL PROTEINS; GLYCOSYLATION; HYDROGEN-ION CONCENTRATION; KINETICS; MANNOSYL-GLYCOPROTEIN ENDO-BETA-N-ACETYLGLUCOSAMINIDASE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PENICILLIUM; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TEMPERATURE;

PENICILLIUM OXALICUM;

EID: 79960003545     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08173.x     Document Type: Article

References (40)

1. Slámová K, Bojarová P, Petrásková L, &, Křen V, (2010) β-N-Acetylhexosaminidase: what's in a name? Biotechnol Adv 28, 682-693.
2. Proia RL, (1988) Gene encoding the human β-hexosaminidase β-chain-extensive homology of intron placement in the α-chain and β-chain genes. Proc Natl Acad Sci USA 85, 1883-1887. (Pubitemid 24315788)
3. Knapp S, Vocadlo D, Gao ZN, Kirk B, Lou JP, &, Withers SG, (1996) NAG-thiazoline, an N-acetyl-β-hexosaminidase inhibitor that implicates acetamido participation. J Am Chem Soc 118, 6804-6805. (Pubitemid 26248188)
4. Tews I, Perrakis A, Oppenheim A, Dauter Z, Wilson KS, &, Vorgias CE, (1996) Bacterial chitobiase structure provides insight into catalytic mechanism and the basis of Tay-Sachs disease. Nat Struct Biol 3, 638-648. (Pubitemid 26239213)
5. Gooday GW, Zhu WY, &, Odonnell RW, (1992) What are the roles of chitinases in the growing fungus? FEMS Microbiol Lett 100, 387-391. (Pubitemid 23008549)
6. Reyes F, Calatayud J, Vazquez C, &, Martinez MJ, (1989) β-N-Acetylglucosaminidase from Aspergillus nidulans which degrades chitin oligomers during autolysis. FEMS Microbiol Lett 65, 83-87. (Pubitemid 19285747)
7. Křen V, &, Martínková L, (2001) Glycosides in medicine: the role of glycosidic residue in biological activity. Curr Med Chem 8, 1303-1328. (Pubitemid 32791798)
8. Bojarová P, &, Křen V, (2009) Glycosidases: a key to tailored carbohydrates. Trends Biotechnol 27, 199-209.
9. Plíhal O, Sklenář J, Kmoníčková J, Man P, Pompach P, Havlíček V, Křen V, &, Bezouška K, (2004) N-Glycosylated catalytic unit meets O-glycosylated propeptide: complex protein architecture in a fungal hexosaminidase. Biochem Soc Trans 32, 764-765. (Pubitemid 39524373)
10. Plíhal O, Sklenář J, Hofbauerová K, Novák P, Man P, Pompach P, Kavan D, Ryšlavá H, Weignerová L, Charvátova-Pišvejcová A, et al. (2007) Large propeptides of fungal β-N-acetylhexosaminidases are novel enzyme regulators that must be intracellularly processed to control activity, dimerization, and secretion into the extracellular environment. Biochemistry 46, 2719-2734. (Pubitemid 46417912)
11. Weignerová L, Vavrušková P, Pišvejcová A, Thiem J, &, Křen V, (2003) Fungal β-N-acetylhexosaminidases with high β-N-acetylgalactosaminidase activity and their use for synthesis of β-GalNAc-containing oligosaccharides. Carbohydr Res 338, 1003-1008. (Pubitemid 36398021)
12. Fialová P, Weignerová L, Rauvolfová J, Přikrylová V, Pišvejcová A, Ettrich R, Kuzma M, Sedmera P, &, Křen V, (2004) Hydrolytic and transglycosylation reactions of N-acyl modified substrates catalysed by β-N- acetylhexosaminidases. Tetrahedron 60, 693-701. (Pubitemid 38045380)
13. Fialová P, Namdjou DJ, Ettrich R, Přikrylová W, Rauvolfová J, Křenek K, Kuzma M, Elling L, Bezouška K, &, Křen V, (2005) Combined application of galactose oxidase and β-N-acetylhexosaminidase in the synthesis of complex immunoactive N-acetyl-D-galactos-aminides. Adv Synth Catal 347, 997-1006. (Pubitemid 40840020)
14. Hušáková L, Riva S, Casali M, Nicotra S, Kuzma M, Huňková Z, &, Křen V, (2001) Enzymatic glycosylation using 6-O-acylated sugar donors and acceptors: β-N-acetylhexosaminidase- catalysed synthesis of 6-O,N,N'-triacetylchitobiose and 6′-O,N,N'- triacetylchitobiose. Carbohydr Res 331, 143-148. (Pubitemid 32226394)
15. Slámová K, Gažák R, Bojarová P, Kulik N, Ettrich R, Pelantová H, Sedmera P, &, Křen V, (2010) 4-Deoxy-substrates for β-N-acetylhexosaminidases: how to make use of their loose specificity. Glycobiology 20, 1002-1009.
16. Di Giambattista R, Federici F, Petruccioli M, &, Fenice M, (2001) The chitinolytic activity of Penicillium janthinellum P9: purification, partial characterization and potential applications. J Appl Microbiol 91, 498-505. (Pubitemid 34205762)
17. Diez B, Rodriguez-Saiz M, de la Fuente JL, Moreno MA, &, Barredo JL, (2005) The nagA gene of Penicillium chrysogenum encoding β-N- acetylglucosaminidase. FEMS Microbiol Lett 242, 257-264. (Pubitemid 40038397)
18. Rodriguez J, Copapatino JL, Reyes F, &, Perezleblic MI, (1994) A β-N-acetylhexosaminidase from Penicillium oxalicum implicated in its cell-wall degradation. Lett Appl Microbiol 19, 217-220.
19. Yamamoto K, Lee KM, Kumagai H, &, Tochikura T, (1985) Purification and characterization of β-N-acetylhexosaminidase from Penicillium oxalicum. Agric Biol Chem 49, 611-619.
20. Huňková Z, Křen V, Åčigelová M, Weignerová L, Scheel O, &, Thiem J, (1996) Induction of β-N-acetylhexosaminidase in Aspergillus oryzae. Biotechnol Lett 18, 725-730.
21. Laemmli UK, (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227, 680-685.
22. Lee DH, &, Lee CB, (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159, 75-85.
23. Peterbauer CK, Brunner K, Mach RL, &, Kubicek CP, (2002) Identification of the N-acetyl-D-glucosamine-inducible element in the promoter of the Trichoderma atroviride nag1 gene encoding N-acetyl-glucosaminidase. Mol Gen Genomics 267, 162-170. (Pubitemid 34437991)
24. Pompach P, Man P, Kavan D, Hofbauerová K, Kumar V, Bezouška K, Havlíček V, &, Novak P, (2009) Modified electrophoretic and digestion conditions allow a simplified mass spectrometric evaluation of disulfide bonds. J Mass Spectrom 44, 1571-1578.
25. Ettrich R, Kopecký V, Hofbauerová K, Baumruk V, Novák P, Pompach P, Man P, Plíhal O, Kutý M, Kulik N, et al. (2007) Structure of the dimeric N-glycosylated form of fungal β-N-acetylhexosaminidase revealed by computer modeling, vibrational spectroscopy, and biochemical studies. BMC Struct Biol 7, 32.
26. Schuck P, (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal Biochem 320, 104-124. (Pubitemid 36937072)
27. Fisher A, Do RK, &, Sali A, (2000) Modeling of loops in protein structures. Protein Sci 9, 1753-1773.
28. Intra J, Pavesi G, &, Horner DS, (2008) Phylogenetic analyses suggest multiple changes of substrate specificity within the glycosyl hydrolase 20 family. BMC Evol Biol 8, 214.
29. Gutternigg M, Rendič D, Voglauer R, Iskratsch TI, &, Wilson IBN, (2009) Mammalian cells contain a second nucleocytoplasmic hexosaminidase. Biochem J 419, 83-90.
30. Prag G, Papanikolau Y, Tavlas G, Vorgias CE, Petratos K, &, Oppenheim AB, (2000) Structures of chitobiase mutants complexed with the substrate di-N-acetyl-D-glucosamine: the catalytic role of the conserved acidic pair, aspartate 539 and glutamate 540. J Mol Biol 300, 611-617.
31. Goodsell DS, &, Olson AJ, (1990) Automated docking of substrates to proteins by simulated annealing. Proteins 8, 195-202. (Pubitemid 20363304)
32. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, &, Olson AJ, (1998) Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J Comput Chem 19, 1639-1662. (Pubitemid 128590223)
33. Mark BL, Mahuran DJ, Cherney MM, Zhao DL, Knapp S, &, James MNG, (2003) Crystal structure of human β-hexosaminidase B: understanding the molecular basis of Sandhoff and Tay-Sachs disease. J Mol Biol 327, 1093-1109. (Pubitemid 36363715)
34. Brumer H, Sims PFG, &, Sinnott ML, (1999) Lignocellulose degradation by Phanerochaete chrysosporium: purification and characterization of the main α-galactosidase. Biochem J 339, 43-53. (Pubitemid 29179289)
35. Notredame C, Higgins DG, &, Heringa J, (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302, 205-217.
36. Krieger E, Darden T, Nabuurs SB, Finkelstein A, &, Vriend G, (2004) Making optimal use of empirical energy functions: force-field parameterization in crystal space. Proteins 57, 678-683. (Pubitemid 39626989)
37. Sali A, &, Blundell TL, (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234, 779-815. (Pubitemid 24007801)
38. Laskowski RA, Macarthur MW, Moss DS, &, Thornton JM, (1993) Procheck-a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283-291.
39. Sippl MJ, (1993) Recognition of errors in three-dimensional structures of proteins. Proteins 17, 355-362. (Pubitemid 23358545)
40. Bohne-Lang A, &, von der Lieth CW, (2005) GlyProt: in silico glycosylation of proteins. Nucleic Acids Res 33, W214-W219. (Pubitemid 44529911)