Characterisation of class i and II α-mannosidases from Drosophila melanogaster

Glycoconjugate Journal

Volumn 30, Issue 9, 2013, Pages 899-909

  Nemčovičová, Ivana ^a,c   Šesták, Sergej ^a   Rendić, Dubravko ^b   Plšková, Margita ^a   Mucha, Ján ^a   Wilson, Iain B H ^b  

^a Oddelenie glykobiotechnológie   (Slovakia)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^c Slovenská Akadémia Vied Bratislava   (Slovakia)

Author keywords

Insect; Mannosidase; N glycans

Indexed keywords

ALPHA MANNOSIDASE; ALPHA MANNOSIDASE I; ALPHA MANNOSIDASE II; NITROPHENOL; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME LOCALIZATION; ENZYME PURIFICATION; ENZYME SUBSTRATE; GENETIC DISTANCE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY;

DROSOPHILA MELANOGASTER; HEXAPODA; PICHIA PASTORIS;

ALPHA-MANNOSIDASE; AMINO ACID SEQUENCE; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; KINETICS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; SUBSTRATE SPECIFICITY;

EID: 84887997730     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-013-9495-5     Document Type: Article

References (49)

1. Henrissat, B., Bairoch, A.: New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293, 781-788 (1993)
2. Winchester, B.: Role of α-D-mannosidases in the biosynthesis and catabolism of glycoproteins. Biochem. Soc. Trans. 12, 522-524 (1984)
3. Herscovics, A.: Importance of glycosidases in mammalian glycoprotein biosynthesis. Biochim. Biophys. Acta 1473, 96-107 (1999)
4. Tollersrud, O.-K., Berg, T., Healy, P., Evjen, G., Ramachandran, U., Nilssen, Ø.: Purification of bovine α-mannosidase, characterisation of its gene and determination of two mutations that cause α-mannosidosis. Eur. J. Biochem. 246, 410-419 (1997)
5. Berg, T., Tollersrud, O.K., Walkley, S.U., Siegel, D., Nilssen, O.: Purification of feline lysosomal α-mannosidase, determination of its cDNA sequence and identification of a mutation causing α-mannosidosis in Persian cats. Biochem. J. 328, 863-870 (1997)
6. Nilssen, Ø., Berg, T., Riise, H.M.F., Ramachandran, U., Evjen, G., Hansen, G.M., Malm, D., Tranebjaerg, L., Tollersrud, O.-K.: α-Mannosidosis: functional cloning of the lysosomal α-mannosidase cDNA and identification of a mutation in two affected siblings. Hum. Mol. Genet. 6, 717-726 (1997)
7. x in N-glycan processing in vivo in mice. Proc. Natl. Acad. Sci. U. S. A. 103, 8983-8988 (2006)
8. Gauss, R., Kanehara, K., Carvalho, P., Ng, D.T., Aebi, M.: A complex of Pdi1p and the mannosidase Htm1p initiates clearance of unfolded glycoproteins from the endoplasmic reticulum. Mol. Cell 42, 782-793 (2011)
9. Kerscher, S., Albert, S., Wucherpfennig, D., Heisenberg, M., Schneuwly, S.: Molecular and genetic analysis of the Drosophila mas-1 (mannosidase-1) gene which encodes a glycoprotein processing α1,2-mannosidase. Dev. Biol. 168, 613-626 (1995)
10. Liu, Y.L., Lu, W.C., Brummel, T.J., Yuh, C.H., Lin, P.T., Kao, T.Y., Li, F.Y., Liao, P.C., Benzer, S., Wang, H.D.: Reduced expression of α-1,2-mannosidase I extends lifespan in Drosophila melanogaster and Caenorhabditis elegans. Aging Cell 8, 370-379 (2009)
11. Roberts, D.B., Mulvany, W.J., Dwek, R.A., Rudd, P.M.: Mutant analysis reveals an alternative pathway for N-linked glycosylation in Drosophila melanogaster. Eur. J. Biochem. 253, 494-498 (1998)
12. Rose, D.R.: Structure, mechanism and inhibition of Golgi α-mannosidase II. Curr. Opin. Struct. Biol. 22, 558-562 (2012)
13. Rabouille, C., Kuntz, D.A., Lockyer, A., Watson, R., Signorelli, T., Rose, D.R., van den Heuvel, M., Roberts, D.B.: The Drosophila GMII gene encodes a Golgi α-mannosidase II. J. Cell Sci. 112, 3319-3330 (1999)
14. van den Elsen, J.M., Kuntz, D.A., Rose, D.R.: Structure of Golgi α-mannosidase II: a target for inhibition of growth and metastasis of cancer cells. EMBO J. 20, 3008-3017 (2001)
15. Kawatkar, S.P., Kuntz, D.A., Woods, R.J., Rose, D.R., Boons, G.J.: Structural basis of the inhibition of Golgi α-mannosidase II by mannostatin A and the role of the thiomethyl moiety in ligand-protein interactions. J. Am. Chem. Soc. 128, 8310-8319 (2006)
16. Kumar, N.S., Kuntz, D.A., Wen, X., Pinto, B.M., Rose, D.R.: Binding of sulfonium-ion analogues of di-epi-swainsonine and 8-epi-lentiginosine to Drosophila Golgi α-mannosidase II: the role of water in inhibitor binding. Proteins 71, 1484-1496 (2008)
17. Kuntz, D.A., Tarling, C.A., Withers, S.G., Rose, D.R.: Structural analysis of Golgi α-mannosidase II inhibitors identified from a focused glycosidase inhibitor screen. Biochemistry 47, 10058-10068 (2008)
18. Kuntz, D.A., Zhong, W., Guo, J., Rose, D.R., Boons, G.J.: The molecular basis of inhibition of Golgi α-mannosidase II by mannostatin A. Chembiochem 10, 268-277 (2008)
19. Shah, N., Kuntz, D.A., Rose, D.R.: Golgi α-mannosidase II cleaves two sugars sequentially in the same catalytic site. Proc. Natl. Acad. Sci. U. S. A. 105, 9570-9575 (2008)
20. Zhong, W., Kuntz, D.A., Ember, B., Singh, H., Moremen, K.W., Rose, D.R., Boons, G.J.: Probing the substrate specificity of Golgi α-mannosidase II by use of synthetic oligosaccharides and a catalytic nucleophile mutant. J. Am. Chem. Soc. 130, 8975-8983 (2008)
21. Lukacsovich, T., Asztalos, Z., Awano, W., Baba, K., Kondo, S., Niwa, S., Yamamoto, D.: Dual-tagging gene trap of novel genes in Drosophila melanogaster. Genetics 157, 727-742 (2001)
22. Landis, G., Bhole, D., Lu, L., Tower, J.: High-frequency generation of conditional mutants affecting Drosophila melanogaster development and life span. Genetics 158, 1167-1176 (2001)
23. Wilson, I.B.H.: The class I α1,2-mannosidases of Caenorhabditis elegans. Glycoconj. J. 29, 173-179 (2012)
24. Paschinger, K., Hackl, M., Gutternigg, M., Kretschmer-Lubich, D., Stemmer, U., Jantsch, V., Lochnit, G., Wilson, I.B.H.: A deletion in the Golgi α-mannosidase II gene of Caenorhabditis elegans results in unexpected non-wild type N-glycan structures. J. Biol. Chem. 281, 28265-28277 (2006)
25. Šafář, P., Žúžiová, J., Marchalín, S., Prónayová, N., Švorc, L., Vrábel, V., Šesták, S., Rendić, D., Tognetti, V., Joubert, L., Daïch, A.: Combined Chemical, Biological and Theoretical DFT-QTAIM Study of Potent Glycosidase Inhibitors Based on Quaternary Indolizinium Salts. Eur. J. Org. Chem., 5498-5514 (2012)
26. Nemčovičová, I., Nemčovic, M., Šesták, S., Plškova, M., Wilson, I.B.H., Mucha, J.: Expression, purification and preliminary crystallographic analysis of Drosophila melanogaster lysosomal α-mannosidase. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68, 965-970 (2012)
27. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W. Z., Lopez, R., McWilliam, H., Remmert, M., Soding, J., Thompson, J. D., Higgins, D. G.: Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011)
28. Goujon, M., McWilliam, H., Li, W.Z., Valentin, F., Squizzato, S., Paern, J., Lopez, R.: A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38, W695-W699 (2010)
29. Page, R.D.M.: TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357-358 (1996)
30. Both, P., Sobczak, L., Breton, C., Hann, S., Nobauer, K., Paschinger, K., Kozmon, S., Mucha, J., Wilson, I.B.H.: Distantly-related plant and nematode core α1,3-fucosyltransferases display similar trends in structure-function relationships. Glycobiology 21, 1401-1415 (2011)
31. Lineweaver, H., Burk, D.: The determination of enzyme dissociation constants. J. Am. Chem. Soc. 56, 658-666 (1934)
32. Dixon, M.: The determination of enzyme inhibitor constants. Biochem. J. 55, 170-171 (1953)
33. Park, C., Meng, L., Stanton, L.H., Collins, R.E., Mast, S.W., Yi, X., Strachan, H., Moremen, K.W.: Characterization of a human core-specific lysosomal α1,6-mannosidase involved in N-glycan catabolism. J. Biol. Chem. 280, 37204-37216 (2005)
34. Numao, S., He, S., Evjen, G., Howard, S., Tollersrud, O.-K., Withers, S.G.: Identification of Asp197 as the catalytic nucleophile in the family 38 α-mannosidase from bovine kidney microsomes. FEBS Lett. 484, 175-178 (2000)
35. Kawar, Z., Karaveg, K., Moremen, K.W., Jarvis, D.L.: Insect cells encode a class II α-mannosidase with unique properties. J. Biol. Chem. 276, 16335-16340 (2001)
36. Heikinheimo, P., Helland, R., Schrøder Leiros, H.-K., Leiros, I., Karlsen, S., Evjen, G., Ravelli, R., Schoehn, G., Ruigrok, R., Tollersrud, O.-K., McSweeney, S., Hough, E.: The structure of bovine lysosomal α-mannosidase suggests a novel mechanism for low-pH activation. J. Mol. Biol. 327, 631-644 (2003)
37. Hossain, M.A., Nakano, R., Nakamura, K., Hossain, M.T., Kimura, Y.: Molecular characterization of plant acidic α-mannosidase, a member of glycosylhydrolase family 38, involved in the turnover of N-glycans during tomato fruit ripening. J. Biochem. 148, 603-616 (2010)
38. Suzuki, T., Hara, I., Nakano, M., Shigeta, M., Nakagawa, T., Kondo, A., Funakoshi, Y., Taniguchi, N.: Man2C1, an α-mannosidase is involved in the trimming of free oligosaccharides in the cytosol. Biochem. J. 400, 33-41 (2006)
39. Venkatesan, M., Kuntz, D.A., Rose, D.R.: Human lysosomal α-mannosidases exhibit different inhibition and metal binding properties. Protein Sci. 18, 2242-2251 (2009)
40. Woo, K.K., Miyazaki, M., Hara, S., Kimura, M., Kimura, Y.: Purification and characterization of a Co(II)-sensitive α-mannosidase from Ginkgo biloba seeds. Biosci. Biotechnol. Biochem. 68, 2547-2556 (2004)
41. Elbein, A.D., Solf, R., Dorling, P.R., Vosbeck, K.: Swainsonine: an inhibitor of glycoprotein processing. Proc. Natl. Acad. Sci. U. S. A. 78, 7393-7397 (1981)
42. Tropea, J.E., Kaushal, G.P., Pastuszak, I., Mitchell, M., Aoyagi, T., Molyneux, R.J., Elbein, A.D.: Mannostatin A, a new glycoprotein-processing inhibitor. Biochemistry 29, 10062-10069 (1990)
43. Li, B., Kawatkar, S.P., George, S., Strachan, H., Woods, R.J., Siriwardena, A., Moremen, K.W., Boons, G.J.: Inhibition of Golgi mannosidase II with mannostatin A analogues: synthesis, biological evaluation, and structure-activity relationship studies. Chembiochem 5, 1220-1227 (2004)
44. Schutzbach, J.S., Forsee, W.T.: Calcium ion activation of rabbit liver α1,2-mannosidase. J. Biol. Chem. 265, 2546-2549 (1990)
45. Tempel, W., Karaveg, K., Liu, Z.J., Rose, J., Wang, B.C., Moremen, K.W.: Structure of mouse Golgi α-mannosidase IA reveals the molecular basis for substrate specificity among class 1 (family 47 glycosylhydrolase) α1,2-mannosidases. J. Biol. Chem. 279, 29774-29786 (2004)
46. 2. Anal. Biochem. 193, 90-100 (1991)
47. al Daher, S., de Gasperi, R., Daniel, P., Hall, N., Warren, C.D., Winchester, B.: The substrate-specificity of human lysosomal α-D-mannosidase in relation to genetic α-mannosidosis. Biochem. J. 277, 743-751 (1991)
48. Michalski, J.C., Haeuw, J.F., Wieruszeski, J.M., Montreuil, J., Strecker, G.: In vitro hydrolysis of oligomannosyl oligosaccharides by the lysosomal α-D-mannosidases. Eur. J. Biochem. 189, 369-379 (1990)
49. Numao, S., Kuntz, D.A., Withers, S.G., Rose, D.R.: Insights into the mechanism of Drosophila melanogaster Golgi α-mannosidase II through the structural analysis of covalent reaction intermediates. J. Biol. Chem. 278, 48074-48083 (2003)