Ukr.Biochem.J. 2014; Volume 86, Issue 6, Nov-Dec, pp. 5-17

doi: https://doi.org/10.15407/ubj86.06.005

“Three sources and three component parts” of free oligosaccharides

I. U. Pismenetskaya1, T. D. Butters2

1SI Dnepropetrovsk Medical Academy, Ukraine;
2Oxford Glycobiology Institute, University of Oxford, UK;
e-mail: pismenetskaya@yahoo.com

Metabolism of glycoproteins and glycolipids is accompanied by the appearance of unbound structural analogues of the carbohydrate portion of glycoconjugates or so called free oligosaccharides. There are their several sources inside the cell: 1) multistep pathways of N-glycosylation, 2) the cell quality control and ER-associated degradation of misglycosylated and /or misfolded glycoproteins, 3) lysosomal degradation of mature glycoconjugates. In this review the information about the ways of free oligosaccharides appearance in different cell compartments and details of their structures depending on the source is summarized. In addition, extracellular free oligosaccharides, their structures and changes under normal and pathological conditions are discussed.

Keywords: , , , , ,


References:

  1. Varki A. (ed.) Essentials of Glycobiology. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 2009. 784 p.
  2. Donoso G, Herzog V, Schmitz A. Misfolded BiP is degraded by a proteasome-independent endoplasmic-reticulum-associated degradation pathway. Biochem J. 2005 May 1;387(Pt 3):897-903. PubMed, PubMedCentral, CrossRef
  3. Moore SE. Oligosaccharide transport: pumping waste from the ER into lysosomes. Trends Cell Biol. 1999 Nov;9(11):441-6. Review. PubMed, CrossRef
  4. Alonzi DS, Neville DC, Lachmann RH, Dwek RA, Butters TD. Glucosylated free oligosaccharides are biomarkers of endoplasmic- reticulum alpha-glucosidase inhibition. Biochem J. 2008 Jan 15;409(2):571-80. PubMed, CrossRef
  5. Vleugels W, Keldermans L, Jaeken J, Butters TD, Michalski JC, Matthijs G, Foulquier F. Quality control of glycoproteins bearing truncated glycans in an ALG9-defective (CDG-IL) patient. Glycobiology. 2009 Aug;19(8):910-7. PubMed, CrossRef
  6. Alonzi DS, Su YH, Butters TD. Urinary glycan markers for disease. Biochem Soc Trans. 2011 Jan;39(1):393-8. Review. PubMed, CrossRef
  7. Pismenetskaya I. U., Butters T. D. Chromatographic profile changes of plasma free oligosaccharides in subleukemic myelosis. “Scientific Notes of Taurida V. Vernadsky National University”. Series: Biology, Chemistry. 2013;26(65), N 1:153-160. (in Russian).
  8. Jones MB, Rosenberg JN, Betenbaugh MJ, Krag SS. Structure and synthesis of polyisoprenoids used in N-glycosylation across the three domains of life. Biochim Biophys Acta. 2009 Jun;1790(6):485-94. Review. PubMed, PubMedCentral, CrossRef
  9. Rush JS, Gao N, Lehrman MA, Waechter CJ. Recycling of dolichyl monophosphate to the cytoplasmic leaflet of the endoplasmic reticulum after the cleavage of dolichyl pyrophosphate on the lumenal monolayer. J Biol Chem. 2008 Feb 15;283(7):4087-93. PubMed, CrossRef
  10. Schenk B, Fernandez F, Waechter CJ. The ins(ide) and out(side) of dolichyl phosphate biosynthesis and recycling in the endoplasmic reticulum. Glycobiology. 2001 May;11(5):61R-70R. Review. PubMed, CrossRef
  11. Peric D, Durrant-Arico C, Delenda C, Dupré T, De Lonlay P, de Baulny HO, Pelatan C, Bader-Meunier B, Danos O, Chantret I, Moore SE. The compartmentalisation of phosphorylated free oligosaccharides in cells from a CDG Ig patient reveals a novel ER-to-cytosol translocation process. PLoS One. 2010;5(7);e11675. PubMed, PubMedCentral, CrossRef
  12. Anumula KR, Spiro RG. Release of glucose-containing polymannose oligosaccharides during glycoprotein biosynthesis. Studies with thyroid microsomal enzymes and slices. J Biol Chem. 1983 Dec 25;258(24):15274-82. PubMed
  13. Rosenwald AG, Stoll J, Krag SS. Regulation of glycosylation. Three enzymes compete for a common pool of dolichyl phosphate in vivo. J Biol Chem. 1990 Aug 25;265(24):14544-53. PubMed
  14. Hsu AF, Baynes JW, Heath EC. The role of a dolichol-oligosaccharide as an intermediate in glycoprotein biosynthesis. Proc Natl Acad Sci USA. 1974 Jun;71(6):2391-5. PubMed, PubMedCentral, CrossRef
  15. Hoflack B, Cacan R, Verbert A. Dolichol pathway in lymphocytes from rat spleen. Influence of the glucosylation on the cleavage of dolichyl diphosphate oligosaccharides into phosphooligosaccharides. Eur J Biochem. 1981 Jul;117(2):285-90. PubMed, CrossRef
  16. Chantret I, Moore SE. Free oligosaccharide regulation during mammalian protein N-glycosylation. Glycobiology. 2008 Mar;18(3):210-24. Review. PubMed, CrossRef
  17. Belard M, Cacan R, Verbert A. Characterization of an oligosaccharide-pyrophosphodolichol pyrophosphatase activity in yeast. Biochem J. 1988 Oct 1;255(1):235-42. PubMed, PubMedCentral
  18. Cacan R, Villers C, Bélard M, Kaiden A, Krag SS, Verbert A. Different fates of the oligosaccharide moieties of lipid intermediates. Glycobiology. 1992 Apr;2(2):127-36. PubMed, CrossRef
  19. Grunewald S, Matthijs G, Jaeken J. Congenital disorders of glycosylation: a review. Pediatr Res. 2002 Nov;52(5):618-24. Review. PubMed, CrossRef
  20. Vleugels W, Duvet S, Peanne R, Mir AM, Cacan R, Michalski JC, Matthijs G, Foulquier F. Identification of phosphorylated oligosaccharides in cells of patients with a congenital disorders of glycosylation (CDG-I). Biochimie. 2011 May;93(5):823-33. PubMed, CrossRef
  21. Oliver GJ, Harrison J, Hemming FW. The mannosylation of dolichol diphosphate oligosaccharides and the formation of oligosaccharides and glycoproteins in pig liver microsomal preparations. Biochem Soc Trans. 1975;3(5):666-8. PubMed, CrossRef
  22. Hanover JA, Lennarz WJ. Transmembrane assembly of membrane and secretory glycoproteins. Arch Biochem Biophys. 1981 Oct 1;211(1):1-19. Review. PubMed, CrossRef
  23. Harada Y, Buser R, Ngwa EM, Hirayama H, Aebi M, Suzuki T. Eukaryotic oligosaccharyltransferase generates free oligosaccharides during N-glycosylation. J Biol Chem. 2013 Nov 8;288(45):32673-84. PubMed, PubMedCentral, CrossRef
  24. Spiro MJ, Spiro RG. Potential regulation of N-glycosylation precursor through oligosaccharide-lipid hydrolase action and glucosyltransferase-glucosidase shuttle. J Biol Chem. 1991 Mar 15;266(8):5311-7. PubMed
  25. Gao N, Shang J, Lehrman MA. Analysis of glycosylation in CDG-Ia fibroblasts by fluorophore-assisted carbohydrate electrophoresis: implications for extracellular glucose and intracellular mannose 6-phosphate. J Biol Chem. 2005 May 6;280(18):17901-9. PubMed, PubMedCentral, CrossRef
  26. Kukushkin N. V., Alonzi D. S., Dwek R. A., Butters T. D. Demonstration that endoplasmic reticulum-associated degradation of glyco­proteins can occur downstream of processing by endomannosidase.  Biochem J. 2011 Aug 15;438(1):133-42. PubMed, CrossRef
  27. Alonzi DS, Kukushkin NV, Allman SA, Hakki Z, Williams SJ, Pierce L, Dwek RA, Butters TD. Glycoprotein misfolding in the endoplasmic reticulum: identification of released oligosaccharides reveals a second ER-associated degradation pathway for Golgi-retrieved proteins. Cell Mol Life Sci. 2013 Aug;70(15):2799-814. Epub 2013 Mar 16. PubMed, CrossRef
  28. Araki K, Nagata K. Protein folding and quality control in the ER. Cold Spring Harb Perspect Biol. 2011 Nov 1;3(11):a007526. Review. PubMed, PubMedCentral, CrossRef
  29. Hoseki J, Ushioda R, Nagata K. Mechanism and components of endoplasmic reticulum-associated degradation. J Biochem. 2010 Jan;147(1):19-25. Review. PubMed, CrossRef
  30. Olzmann JA, Kopito RR, Christianson JC. The mammalian endoplasmic reticulum-associated degradation system. Cold Spring Harb Perspect Biol. 2013 Sep 1;5(9). pii: a013185. Review. PubMed, PubMedCentral, CrossRef
  31. Avezov E, Frenkel Z, Ehrlich M, Herscovics A, Lederkremer GZ. Endoplasmic reticulum (ER) mannosidase I is compartmentalized and required for N-glycan trimming to Man5-6GlcNAc2 in glycoprotein ER-associated degradation. Mol Biol Cell. 2008 Jan;19(1):216-25. PubMed, PubMedCentral, CrossRef
  32. Bosis E, Nachliel E, Cohen T, Takeda Y, Ito Y, Bar-Nun S, Gutman M. Endoplasmic reticulum glucosidase II is inhibited by its end products. Biochemistry. 2008 Oct 14;47(41):10970-80. Epub 2008 Sep 20. PubMed, CrossRef
  33. Ito Y, Takeda Y. Deciphering the roles of glycan processing in glycoprotein quality control through organic synthesis. Biosci Biotechnol Biochem. 2013;77(12):2331-8. Review. PubMed, CrossRef
  34. D’Alessio C, Caramelo JJ, Parodi AJ. UDP-GlC:glycoprotein glucosyltransferase-glucosidase II, the ying-yang of the ER quality control. Semin Cell Dev Biol. 2010 Jul;21(5):491-9. Review. PubMed, PubMedCentral, CrossRef
  35. Roth J, Yam GH, Fan J, Hirano K, Gaplovska-Kysela K, Le Fourn V, Guhl B, Santimaria R, Torossi T, Ziak M, Zuber C. Protein quality control: the who’s who, the where’s and therapeutic escapes. Histochem Cell Biol. 2008 Feb;129(2):163-77. Review. PubMed, PubMedCentral, CrossRef
  36. Pan S, Cheng X, Sifers RN. Golgi-situated endoplasmic reticulum α-1, 2-mannosidase contributes to the retrieval of ERAD substrates through a direct interaction with γ-COP. Mol Biol Cell. 2013 Apr;24(8):1111-21. PubMed, PubMedCentral, CrossRef
  37. Rymen D, Peanne R, Millón MB, Race V, Sturiale L, Garozzo D, Mills P, Clayton P, Asteggiano CG, Quelhas D, Cansu A, Martins E, Nassogne MC, Gonçalves-Rocha M, Topaloglu H, Jaeken J, Foulquier F, Matthijs G. MAN1B1 deficiency: an unexpected CDG-II. PLoS Genet. 2013;9(12):e1003989.  PubMed, PubMedCentral, CrossRef
  38. Anelli T, Sitia R. Protein quality control in the early secretory pathway. EMBO J. 2008 Jan 23;27(2):315-27. Review. PubMed, PubMedCentral, CrossRef
  39. Spiro RG. Role of N-linked polymannose oligosaccharides in targeting glycoproteins for endoplasmic reticulum-associated degradation. Cell Mol Life Sci. 2004 May;61(9):1025-41. Review. PubMed, CrossRef
  40. Cacan R, Duvet S, Labiau O, Verbert A, Krag SS. Monoglucosylated oligomannosides are released during the degradation process of newly synthesized glycoproteins. J Biol Chem. 2001 Jun 22;276(25):22307-12. Epub 2001 Apr 6. PubMed, CrossRef
  41. Hebert DN, Bernasconi R, Molinari M. ERAD substrates: which way out? Semin Cell Dev Biol. 2010 Jul;21(5):526-32. Epub 2009 Dec 22. Review. PubMed, CrossRef
  42. Verbert A, Cacan R. Trafficking of oligomannosides released during N-glycosylation: a clearing mechanism of the rough endoplasmic reticulum. Biochim Biophys Acta. 1999 Dec 6;1473(1):137-46. Review. PubMed, CrossRef
  43. Cacan R, Dengremont C, Labiau O, Kmiécik D, Mir AM, Verbert A. Occurrence of a cytosolic neutral chitobiase activity involved in oligomannoside degradation: a study with Madin-Darby bovine kidney (MDBK) cells. Biochem J. 1996 Jan 15;313 ( Pt 2):597-602. PubMed, PubMedCentral, CrossRef
  44. Kato T, Hatanaka K, Mega T, Hase S. Purification and characterization of endo-beta-N-acetylglucosaminidase from hen oviduct. J Biochem. 1997 Dec;122(6):1167-73. PubMed, CrossRef
  45. Suzuki T, Yano K, Sugimoto S, Kitajima K, Lennarz WJ, Inoue S, Inoue Y, Emori Y. Endo-beta-N-acetylglucosaminidase, an enzyme involved in processing of free oligosaccharides in the cytosol. Proc Natl Acad Sci USA. 2002 Jul 23;99(15):9691-6. PubMed, PubMedCentral, CrossRef
  46. Hirsch C, Blom D, Ploegh HL. A role for N-glycanase in the cytosolic turnover of glycoproteins. EMBO J. 2003 Mar 3;22(5):1036-46. PubMed, PubMedCentral, CrossRef
  47. Ohashi S, Iwai K, Mega T, Hase S. Quantitation and isomeric structure analysis of free oligosaccharides present in the cytosol fraction of mouse liver: detection of a free disialobiantennary oligosaccharide and glucosylated oligomannosides. J Biochem. 1999 Nov;126(5):852-8. PubMed, CrossRef
  48. Mellor HR, Neville DC, Harvey DJ, Platt FM, Dwek RA, Butters TD. Cellular effects of deoxynojirimycin analogues: inhibition of N-linked oligosaccharide processing and generation of free glucosylated oligosaccharides. Biochem J. 2004 Aug 1;381(Pt 3):867-75. PubMed, PubMedCentral, CrossRef
  49. Saint-Pol A, Codogno P, Moore SE. Cytosol-to-lysosome transport of free polymannose-type oligosaccharides. Kinetic and specificity studies using rat liver lysosomes. J Biol Chem. 1999 May 7;274(19):13547-55. PubMed, CrossRef
  50. Bernon C, Carré Y, Kuokkanen E, Slo­mianny MC, Mir AM, Krzewinski F, Cacan R, Heikinheimo P, Morelle W, Michalski JC, Foulquier F, Duvet S. Overexpression of Man2C1 leads to protein underglycosylation and upregulation of endoplasmic reticulum-associated degradation pathway. Glycobiology. 2011;21(3):363-375. PubMed, CrossRef
  51. Yamashita K, Tachibana Y, Mihara K, Okada S, Yabuuchi H, Kobata A. Urinary oligosaccharides of mannosidosis. J Biol Chem. 1980 Jun 10;255(11):5126-33. PubMed
  52. Winchester B. Lysosomal metabolism of glycoproteins. Glycobiology. 2005 Jun;15(6):1R-15R. Review. PubMed, CrossRef
  53. Johnson SW, Alhadeff JA. Mammalian alpha-L-fucosidases. Comp Biochem Physiol B. 1991;99(3):479-88. Review. PubMed, CrossRef
  54. Barker C, Dell A, Rogers M, Alhadeff JA, Winchester B. Canine alpha-L-fucosidase in relation to the enzymic defect and storage products in canine fucosidosis. Biochem J. 1988 Sep 15;254(3):861-8. PubMed, PubMedCentral, CrossRef
  55. Saarela J, Laine M, Oinonen C, von Schantz C, Jalanko A, Rouvinen J, Peltonen L. Molecular pathogenesis of a disease: structural consequences of aspartyglucosaminuria mutations. Hum Mol Genet. 2001;10(9):983-995. PubMed, CrossRef
  56. Goldberg DE, Kornfeld S. The phosphorylation of beta-glucuronidase oligosaccharides in mouse P388D1 cells. J Biol Chem. 1981 Dec 25;256(24):13060-7. PubMed
  57. Do H, Lee WS, Ghosh P, Hollowell T, Canfield W, Kornfeld S. Human mannose 6-phosphate-uncovering enzyme is synthesized as a proenzyme that is activated by the endoprotease furin. J Biol Chem. 2002 Aug 16;277(33):29737-44.  PubMed, CrossRef
  58. Yang L, Tredget EE, Ghahary A. Activation of latent transforming growth factor-beta1 is induced by mannose 6-phosphate/insulin-like growth factor-II receptor. Wound Repair Regen. 2000 Nov-Dec;8(6):538-46. PubMed, CrossRef
  59. Barnes J, Lim JM, Godard A, Blanchard F, Wells L, Steet R. Extensive mannose phosphorylation on leukemia inhibitory factor (LIF) controls its extracellular levels by multiple mechanisms. J Biol Chem. 2011 Jul 15;286(28):24855-64. PubMed, PubMedCentral, CrossRef
  60. Lazzarino DA, Gabel CA. Mannose processing is an important determinant in the assembly of phosphorylated high mannose-type oligosaccharides. J Biol Chem. 1989 Mar 25;264(9):5015-23. PubMed
  61. Nordén NE, Lundblad A, Svensson S, Ockerman PA, Autio S. A mannose-containing trisaccharide isolated from urines of three patients with mannosidosis. J Biol Chem. 1973 Sep 10;248(17):6210-5. PubMed
  62. Peelen GO, de Jong JG, Wevers RA. HPLC analysis of oligosaccharides in urine from oligosaccharidosis patients. Clin Chem. 1994 Jun;40(6):914-21. PubMed
  63. Sowell J, Wood T. Towards a selected reaction monitoring mass spectrometry fingerprint approach for the screening of oligosaccharidoses. Anal Chim Acta. 2011 Feb 7;686(1-2):102-6.  PubMed, PubMedCentral, CrossRef
  64. Xia B, Asif G, Arthur L, Pervaiz MA, Li X, Liu R, Cummings RD, He M. Oligosaccharide analysis in urine by maldi-tof mass spectrometry for the diagnosis of lysosomal storage diseases. Clin Chem. 2013 Sep;59(9):1357-68. PubMed, CrossRef
  65. Kobata A. Exo- and endoglycosidases revisited. Proc Jpn Acad Ser B Phys Biol Sci. 2013;89(3):97-117. Review. PubMed, PubMedCentral, CrossRef
  66. Saint-Pol A, Bauvy C, Codogno P, Moore SE. Transfer of free polymannose-type oligosaccharides from the cytosol to lysosomes in cultured human hepatocellular carcinoma HepG2 cells. J Cell Biol. 1997 Jan 13;136(1):45-59. PubMed, PubMedCentral, CrossRef
  67. Durrant C, Moore SE. Perturbation of free oligosaccharide trafficking in endoplasmic reticulum glucosidase I-deficient and castanospermine-treated cells. Biochem J. 2002 Jul 1;365(Pt 1):239-47. PubMed, PubMedCentral, CrossRef
  68. Chantret I, Fasseu M, Zaoui K, Le Bizec C, Sadou YH, Dupre T, Moore SHE. Identification of Roles for Peptide: N-Glycanase and Endo-b-NAcetylglucosaminidase (Engase1p) during Protein N-Glycosylation in Human HepG2 Cells. PLoS ONE. 2010;5(7):e11734. PubMed, PubMedCentral, CrossRef
  69. Thibodeau MS, Giardina C, Knecht DA, Helble J, Hubbard AK. Silica-induced apoptosis in mouse alveolar macrophages is initiated by lysosomal enzyme activity. Toxicol Sci. 2004 Jul;80(1):34-48. PubMed, CrossRef
  70. Pupyshev AB. Lysosomal membrane permeabilization as apoptogenic factor. Tsitologiia. 2011;53(4):313-24. Review. Russian. PubMed
  71. Bidère N, Lorenzo HK, Carmona S, Laforge M, Harper F, Dumont C, Senik A. Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem. 2003 Aug 15;278(33):31401-11. PubMed, CrossRef
  72. Ishizuka A, Hashimto Y, Naka R, Kinoshita M, Kakehi K, Seino J, Funakoshi Y, Suzuki T, Kameyama A, Narimatsu H. Accumulation of free complex-type N-glycans in MKN7 and MKN45 stomach cancer cells. Biochem J. 2008 Jul 15;413(2):227-37. PubMed, CrossRef
  73. Pismenetskaya IU. Spectra detailing of blood plasma free oligosaccharides of healthy volunteers.“Visnyk of the Lviv University” Series Biology. 2012;60:105-110. (in Ukrainian).
  74. Pismenetskaya IU, Butters TD. Free oligosaccharides of human plasma as a new hunting field for disease biomarkers. Abstract book of 7th Lviv-Lublin conference of Experimental and Clinical Biochemistry. Lviv, Ukraine, 2013. P. 152.

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.