Article

You have full text access to this OnlineOpen article

Human lysosomal α-mannosidases exhibit different inhibition and metal binding properties

  1. Meenakshi Venkatesan1,
  2. Douglas A. Kuntz1,
  3. David R. Rose1,2,†,*

Article first published online: 31 AUG 2009

DOI: 10.1002/pro.235

Issue

Protein Science

Protein Science

Volume 18, Issue 11, pages 2242–2251, November 2009

Additional Information

How to Cite

Venkatesan, M., Kuntz, D. A. and Rose, D. R. (2009), Human lysosomal α-mannosidases exhibit different inhibition and metal binding properties. Protein Science, 18: 2242–2251. doi: 10.1002/pro.235

Author Information

  1. 1

    Ontario Cancer Institute, Division of Cancer Genomics and Proteomics, Toronto, Ontario M5G 1L7, Canada

  2. 2

    Department of Medical Biophysics, University of Toronto, Canada

  1. †

    Department of Biology, University ofWaterloo,Waterloo, Ontario N2L 3G1, Canada

*Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, Ontario N2L 3G1, Canada

Publication History

  1. Issue published online: 23 OCT 2009
  2. Article first published online: 31 AUG 2009
  3. Accepted manuscript online: 31 AUG 2009 12:00AM EST
  4. Manuscript Revised: 18 AUG 2009
  5. Manuscript Accepted: 18 AUG 2009
  6. Manuscript Received: 29 JUN 2009

Funded by

  • Ontario Cancer Institute
  • George Knudson Fellowship; Canadian Institutes of Health Research. Grant Number: MOP79312
  • Mizutani Foundation. Grant Number: 080032

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (343K)

References

  • 1
    Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B ( 2009) The Carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucl Acids Res 37: D233–D238.
  • 2
    Crawley AC, Walkley SU ( 2007) Developmental analysis of CNS pathology in the lysosomal storage disease α-mannosidosis. J Neuropathol Exp Neurol 66: 687–697.
  • 3
    Novikoff PM, Touster O, Novikoff AB, Tulsiani DP ( 1985) Effects of swainsonine on rat liver and kidney: biochemical and morphological studies. J Cell Biol 101: 339–349.
  • 4
    Tulsiani DR, Touster O ( 1983) Swainsonine, a potent mannosidase inhibitor, elevates rat liver and brain lysosomal α-D-mannosidase, decreases Golgi α-D-mannosidase II, and increases the plasma levels of several acid hydrolases. Arch Biochem Biophys 224: 594–600.
  • 5
    Daniel PF, Evans JE, De Gasperi R, Winchester B, Warren CD ( 1992) A human lysosomal α(1–6)-mannosidase active on the branched trimannosyl core of complex glycans. Glycobiology 2: 327–336.
  • 6
    De Gasperi R, Daniel PF, Warren CD ( 1992) A human lysosomal α-mannosidase specific for the core of complex glycans. J Biol Chem 267: 9706–9712.
  • 7
    Haeuw JF, Grard T, Alonso C, Strecker G, Michalski JC ( 1994) The core-specific lysosomal α(1–6)-mannosidase activity depends on aspartamidohydrolase activity. Biochem J 297: 463–466.
  • 8
    Okamura N, Dacheux F, Venien A, Onoe S, Huet JC, Dacheux JL ( 1992) Localization of a maturation-dependent epididymal sperm surface antigen recognized by a monoclonal antibody raised against a 135-kilodalton protein in porcine epididymal fluid. Biol Reprod 47: 1040–1052.
  • 9
    Okamura N, Tamba M, Liao HJ, Onoe S, Sugita Y, Dacheux F, Dacheux JL ( 1995) Cloning of complementary DNA encoding a 135-kilodalton protein secreted from porcine corpus epididymis and its identification as an epididymis-specific α-mannosidase. Mol Reprod Dev 42: 141–148.
  • 10
    Park C, Meng L, Stanton LH, Collins RE, Mast SW, Yi X, Strachan H, Moremen KW ( 2005) Characterization of a human core-specific lysosomal α1,6-mannosidase involved in N-glycan catabolism. J Biol Chem 280: 37204–37216.
  • 11
    Dennis JW, Granovsky M, Warren CE ( 1999) Protein glycosylation in development and disease. Bioessays 21: 412–421.
  • 12
    Humphries MJ, Matsumoto K, White SL, Molyneux RJ, Olden K ( 1988) Augmentation of murine natural killer cell activity by swainsonine, a new antimetastatic immunomodulator. Cancer Res 48: 1410–1415.
  • 13
    Tulsiani DR, Broquist HP, Touster O ( 1985) Marked differences in the swainsonine inhibition of rat liver lysosomal α-D-mannosidase, rat liver Golgi mannosidase II, and jack bean α-D-mannosidase. Arch Biochem Biophys 236: 427–434.
  • 14
    Van Den Elsen JM, Kuntz DA, Rose DR ( 2001) Structure of Golgi α-mannosidase II: a target for inhibition of growth and metastasis of cancer cells. EMBO J 20: 3008–3017.
  • 15
    Berg T, King B, Meikle PJ, Nilssen O, Tollersrud OK, Hopwood JJ ( 2001) Purification and characterization of recombinant human lysosomal α-mannosidase. Mol Genet Metab 73: 18–29.
  • 16
    Liao YF, Lal A, Moremen KW ( 1996) Cloning, expression, purification, and characterization of the human broad specificity lysosomal acid α-mannosidase. J Biol Chem 271: 28348–28358.
  • 17
    Heikinheimo P, Helland R, Leiros HK, Leiros I, Karlsen S, Evjen G, Ravelli R, Schoehn G, Ruigrok R, Tollersrud OK, McSweeney S, Hough E ( 2003) The structure of bovine lysosomal α-mannosidase suggests a novel mechanism for low-pH activation. J Mol Biol 327: 631–644.
  • 18
    Fujita T, Nagasawa H, Uto Y, Hashimoto T, Asakawa Y, Hori H ( 2004) Synthesis of the new mannosidase inhibitors, diversity-oriented 5-substituted swainsonine analogues, via stereoselective Mannich reaction. Org Lett 6: 827–830.
  • 19
    Hauser H, Wagner R ( 1997) Mammalian cell biotechnology in protein production. Berlin: Walter de Gruyter & Co.
  • 20
    Tollersrud OK, Berg T, Healy P, Evjen G, Ramachandran U, Nilssen O ( 1997) Purification of bovine lysosomal α-mannosidase, characterization of its gene and determination of two mutations that cause α-mannosidosis. Eur J Biochem 246: 410–419.
  • 21
    Berg T, Tollersrud OK, Walkley SU, Siegel D, Nilssen O ( 1997) 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.
  • 22
    Von Heijne G ( 1985) Signal sequences. The limits of variation. J Mol Biol 184: 99–105.
  • 23
    Bendtsen JD, Nielsen H, Von Heijne G, Brunak S ( 2004) Improved prediction of signal peptides: signalP 3.0. J Mol Biol 340: 783–795.
  • 24
    Gupta R, Brunak S ( 2002) Prediction of glycosylation across the human proteome and the correlation to protein function. Pac Symp Biocomput 7: 310–322.
  • 25
    Kawatkar SP, Kuntz DA, Woods RJ, Rose DR, Boons GJ ( 2006) 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.
  • 26
    Fiaux H, Kuntz DA, Hoffman D, Janzer RC, Gerber-Lemaire S, Rose DR, Juillerat-Jeanneret L ( 2008) Functionalized pyrrolidine inhibitors of human type II α-mannosidases as anti-cancer agents: optimizing the fit to the active site. Bioorg Med Chem 16: 7337–7346.
  • 27
    Englebienne P, Fiaux H, Kuntz DA, Corbeil CR, Gerber-Lemaire S, Rose DR, Moitessier N ( 2007) Evaluation of docking programs for predicting binding of Golgi α-mannosidase II inhibitors: a comparison with crystallography. Proteins 69: 160–176.
  • 28
    Johansen H, Van Der Straten A, Sweet R, Otto E, Maroni G, Rosenberg M ( 1989) Regulated expression at high copy number allows production of a growth-inhibitory oncogene product in Drosophila Schneider cells. Genes Dev 3: 882–889.
  • 29
    Aldecoa A, Gujer R, Fischer JA, Born W ( 2000) Mammalian calcitonin receptor-like receptor/receptor activity modifying protein complexes define calcitonin gene-related peptide and adrenomedullin receptors in Drosophila Schneider 2 cells. FEBS Lett 471: 156–160.
  • 30
    Rossi EJ, Sim L, Kuntz DA, Hahn D, Johnston BD, Ghavami A, Szczepina MG, Kumar NS, Sterchi EE, Nichols BL, Pinto BM, Rose DR ( 2006) Inhibition of recombinant human maltase glucoamylase by salacinol and derivatives. FEBS J 273: 2673–2683.
  • 31
    Scotter AJ, Kuntz DA, Saul M, Graham LA, Davies PL, Rose DR ( 2006) Expression and purification of sea raven type II antifreeze protein from Drosophila melanogaster S2 cells. Protein Expr Purif 47: 374–383.
  • 32
    Yamashiro K, Itoh H, Yamagishi M, Natsuka S, Mega T, Hase S ( 1997) Purification and characterization of neutral α-mannosidase from hen oviduct: studies on the activation mechanism of Co2+. J Biochem 122: 1174–1181.
  • 33
    Haeuw JF, Strecker G, Wieruszeski JM, Montreuil J, Michalski JC ( 1991) Substrate specificity of rat liver cytosolic α-D-mannosidase. Novel degradative pathway for oligomannosidic type glycans. Eur J Biochem 202: 1257–1268.
  • 34
    Shah N, Kuntz DA, Rose DR ( 2008) Golgi α-mannosidase II cleaves two sugars sequentially in the same catalytic site. Proc Natl Acad Sci USA 105: 9570–9575.
  • 35
    Lopez-Torres E, Mendiola MA, Pastor CJ ( 2006) Crystal structures of triazine-3-thione derivatives by reaction with copper and cobalt salts. Inorg Chem 45: 3103–3112.
  • 36
    Chen HP, Marsh EN ( 1997) How enzymes control the reactivity of adenosylcobalamin: effect on coenzyme binding and catalysis of mutations in the conserved histidine-aspartate pair of glutamate mutase. Biochemistry 36: 7884–7889.
  • 37
    Liptak MD, Datta S, Matthews RG, Brunold TC ( 2008) Spectroscopic study of the cobalamin-dependent methionine synthase in the activation conformation: effects of the Y1139 residue and S-adenosylmethionine on the B12 cofactor. J Am Chem Soc 130: 16374–16381.
  • 38
    Garau G, Bebrone C, Anne C, Galleni M, Frere JM, Dideberg O ( 2005) A metallo-β-lactamase enzyme in action: crystal structures of the monozinc carbapenemase CphA and its complex with biapenem. J Mol Biol 345: 785–795.
  • 39
    Miyanaga A, Fushinobu S, Ito K, Wakagi T ( 2001) Crystal structure of cobalt-containing nitrile hydratase. Biochem Biophys Res Commun 288: 1169–1174.
  • 40
    Bessey OA, Lowry OH, Brock MJ ( 1946) A method for the rapid determination of alkaline phosphatase with five cubic millimeters of serum. J Biol Chem 164: 321–329.
  • 41
    Segel IH ( 1975) Enzyme kinetics: behaviour and analysis of rapid equilibrium and steady state enzyme systems. New York: John Wiley & Sons.
  • 42
    Leatherbarrow RJ ( 1998) GraFit Version 4.0, Erithacus Software Ltd., Staines, UK.
View Full Article with Supporting Information (HTML) Get PDF (343K)