A Deletion in the Golgi Alpha-mannosidase II Gene of Caenorhabditis Elegans Results in Unexpected Non-wild-type N-glycan Structures

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2006 Jul 26

PMID 16864579

Citations 30

Authors

Katharina Paschinger

Matthias Hackl

Martin Gutternigg

Dorothea Kretschmer-Lubich

Ute Stemmer

Verena Jantsch

Gunter Lochnit

Iain B H Wilson

Affiliations

Soon will be listed here.

Abstract

The processing of N-linked oligosaccharides by alpha-mannosidases in the endoplasmic reticulum and Golgi is a process conserved in plants and animals. After the transfer of a GlcNAc residue to Asn-bound Man(5)GlcNAc(2) by N-acetylglucosaminyltransferase I, an alpha-mannosidase (EC 3.2.1.114) removes one alpha1,3-linked and one alpha1,6-linked mannose residue. In this study, we have identified the relevant alpha-mannosidase II gene (aman-2; F58H1.1) from Caenorhabditis elegans and have detected its activity in both native and recombinant forms. For comparative studies, the two other cDNAs encoding class II mannosidases aman-1 (F55D10.1) and aman-3 (F48C1.1) were cloned; the corresponding enzymes are, respectively, a putative lysosomal alpha-mannosidase and a Co(II)-activated alpha-mannosidase. The analysis of the N-glycan structures of an aman-2 mutant strain demonstrates that the absence of alpha-mannosidase II activity results in a shift to structures not seen in wild-type worms (e.g. N-glycans with the composition Hex(5-7)HexNAc(2-3)Fuc(2)Me) and an accumulation of hybrid oligosaccharides. Paucimannosidic glycans are almost absent from aman-2 worms, indicative also of a general lack of alpha-mannosidase III activity. We hypothesize that there is a tremendous flexibility in the glycosylation pathway of C. elegans that does not impinge, under standard laboratory conditions, on the viability of worms with glycotypes very unlike the wild-type pattern.

Citing Articles

Genome architecture and selective signals compensatorily shape plastic response to a new environment.

Li A, Zhao M, Zhang Z, Wang C, Zhang K, Zhang X Innovation (Camb). 2023; 4(4):100464.

PMID: 37485076 PMC: 10362523. DOI: 10.1016/j.xinn.2023.100464.

Synthesis, α-mannosidase inhibition studies and molecular modeling of 1,4-imino-ᴅ-lyxitols and their C-5-altered -arylalkyl derivatives.

Kalnik M, Sestak S, Kona J, Bella M, Polakova M Beilstein J Org Chem. 2023; 19:282-293.

PMID: 36925565 PMC: 10012049. DOI: 10.3762/bjoc.19.24.

Increasing Complexity of the N-Glycome During Caenorhabditis Development.

Wilson I, Yan S, Jin C, Dutkiewicz Z, Rendic D, Palmberger D Mol Cell Proteomics. 2023; 22(3):100505.

PMID: 36717059 PMC: 7614267. DOI: 10.1016/j.mcpro.2023.100505.

1,4-Dideoxy-1,4-imino-D- and L-lyxitol-based inhibitors bind to Golgi α-mannosidase II in different protonation forms.

Kona J, Sestak S, Wilson I, Polakova M Org Biomol Chem. 2022; 20(45):8932-8943.

PMID: 36322142 PMC: 7614232. DOI: 10.1039/d2ob01545e.

Specific N-glycans regulate an extracellular adhesion complex during somatosensory dendrite patterning.

Rahman M, Ramirez-Suarez N, Diaz-Balzac C, Bulow H EMBO Rep. 2022; 23(7):e54163.

PMID: 35586945 PMC: 9253746. DOI: 10.15252/embr.202154163.

References

Kaji H, Saito H, Yamauchi Y, Shinkawa T, Taoka M, Hirabayashi J . Lectin affinity capture, isotope-coded tagging and mass spectrometry to identify N-linked glycoproteins. Nat Biotechnol. 2003; 21(6):667-72. DOI: 10.1038/nbt829. View

Altmann F, Schwihla H, Staudacher E, Glossl J, Marz L . Insect cells contain an unusual, membrane-bound beta-N-acetylglucosaminidase probably involved in the processing of protein N-glycans. J Biol Chem. 1995; 270(29):17344-9. DOI: 10.1074/jbc.270.29.17344. View

Haslam S, Dell A . Hallmarks of Caenorhabditis elegans N-glycosylation: complexity and controversy. Biochimie. 2003; 85(1-2):25-32. DOI: 10.1016/s0300-9084(03)00041-5. View

Kawar Z, Karaveg K, Moremen K, Jarvis D . Insect cells encode a class II alpha-mannosidase with unique properties. J Biol Chem. 2001; 276(19):16335-40. PMC: 3633600. DOI: 10.1074/jbc.M100119200. View

Henrissat B, Bairoch A . New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1993; 293 ( Pt 3):781-8. PMC: 1134435. DOI: 10.1042/bj2930781. View

Paschinger K, Staudacher E, Stemmer U, Fabini G, Wilson I . Fucosyltransferase substrate specificity and the order of fucosylation in invertebrates. Glycobiology. 2004; 15(5):463-74. DOI: 10.1093/glycob/cwi028. View

Numao S, He S, Evjen G, Howard S, Tollersrud O, Withers S . Identification of Asp197 as the catalytic nucleophile in the family 38 alpha-mannosidase from bovine kidney lysosomes. FEBS Lett. 2000; 484(3):175-8. DOI: 10.1016/s0014-5793(00)02148-7. View

Ioffe E, Stanley P . Mice lacking N-acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc Natl Acad Sci U S A. 1994; 91(2):728-32. PMC: 43022. DOI: 10.1073/pnas.91.2.728. View

von Schaewen A, Sturm A, ONeill J, Chrispeels M . Isolation of a mutant Arabidopsis plant that lacks N-acetyl glucosaminyl transferase I and is unable to synthesize Golgi-modified complex N-linked glycans. Plant Physiol. 1993; 102(4):1109-18. PMC: 158895. DOI: 10.1104/pp.102.4.1109. View

10.

Bischoff J, Moremen K, Lodish H . Isolation, characterization, and expression of cDNA encoding a rat liver endoplasmic reticulum alpha-mannosidase. J Biol Chem. 1990; 265(28):17110-7. View

11.

Cipollo J, Awad A, Costello C, Robbins P, Hirschberg C . Biosynthesis in vitro of Caenorhabditis elegans phosphorylcholine oligosaccharides. Proc Natl Acad Sci U S A. 2004; 101(10):3404-8. PMC: 373474. DOI: 10.1073/pnas.0400384101. View

12.

Strasser R, Schoberer J, Jin C, Glossl J, Mach L, Steinkellner H . Molecular cloning and characterization of Arabidopsis thaliana Golgi alpha-mannosidase II, a key enzyme in the formation of complex N-glycans in plants. Plant J. 2006; 45(5):789-803. DOI: 10.1111/j.1365-313X.2005.02648.x. View

13.

Heikinheimo P, Helland R, Leiros H, Leiros I, Karlsen S, Evjen G . The structure of bovine lysosomal alpha-mannosidase suggests a novel mechanism for low-pH activation. J Mol Biol. 2003; 327(3):631-44. DOI: 10.1016/s0022-2836(03)00172-4. View

14.

Zhu S, Hanneman A, Reinhold V, Spence A, Schachter H . Caenorhabditis elegans triple null mutant lacking UDP-N-acetyl-D-glucosamine:alpha-3-D-mannoside beta1,2-N-acetylglucosaminyltransferase I. Biochem J. 2004; 382(Pt 3):995-1001. PMC: 1133976. DOI: 10.1042/BJ20040793. View

15.

Zhang W, Cao P, Chen S, Spence A, Zhu S, Staudacher E . Synthesis of paucimannose N-glycans by Caenorhabditis elegans requires prior actions of UDP-N-acetyl-D-glucosamine:alpha-3-D-mannoside beta1,2-N-acetylglucosaminyltransferase I, alpha3,6-mannosidase II and a specific membrane-bound.... Biochem J. 2003; 372(Pt 1):53-64. PMC: 1223384. DOI: 10.1042/BJ20021931. View

16.

DEWALD B, Touster O . A new alpha-D-mannosidase occurring in Golgi membranes. J Biol Chem. 1973; 248(20):7223-33. View

17.

Akama T, Nakagawa H, Wong N, Sutton-Smith M, Dell A, Morris H . Essential and mutually compensatory roles of {alpha}-mannosidase II and {alpha}-mannosidase IIx in N-glycan processing in vivo in mice. Proc Natl Acad Sci U S A. 2006; 103(24):8983-8. PMC: 1474017. DOI: 10.1073/pnas.0603248103. View

18.

Altmann F, Fabini G, Ahorn H, Wilson I . Genetic model organisms in the study of N-glycans. Biochimie. 2001; 83(8):703-12. DOI: 10.1016/s0300-9084(01)01297-4. View

19.

Hase S, Ibuki T, Ikenaka T . Reexamination of the pyridylamination used for fluorescence labeling of oligosaccharides and its application to glycoproteins. J Biochem. 1984; 95(1):197-203. DOI: 10.1093/oxfordjournals.jbchem.a134585. View

20.

Rabouille C, Kuntz D, Lockyer A, Watson R, Signorelli T, Rose D . The Drosophila GMII gene encodes a Golgi alpha-mannosidase II. J Cell Sci. 1999; 112 ( Pt 19):3319-30. DOI: 10.1242/jcs.112.19.3319. View