Deficiency of α-glucosidase I alters glycoprotein glycosylation and lifespan in Caenorhabditis elegans

Glycobiology

Volumn 23, Issue 10, 2013, Pages 1142-1151

  Katoh, Toshihiko ^a   Takase, Juri ^a   Tani, Yasushi ^b   Amamoto, Ryuta ^b   Aoshima, Naofumi ^b   Tiemeyer, Michael ^a   Yamamoto, Kenji ^c   Ashida, Hisashi ^a,d  

^a UNIVERSITY OF GEORGIA   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^d KINKI UNIVERSITY   (Japan)

Author keywords

glucosidase I; Caenorhabditis elegans; Congenital disorder of glycosylation; Free oligosaccharide; N glycan

Indexed keywords

ALPHA GLUCOSIDASE; CALNEXIN; CALRETICULIN; COMPLEMENTARY DNA; GLYCOPROTEIN; OLIGOSACCHARIDE;

AGL 1 GENE; ARTICLE; CAENORHABDITIS ELEGANS; CELL SURFACE; CHO CELL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME GLYCOSYLATION; GENE; GENE SILENCING; LIFESPAN; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA INTERFERENCE; UPREGULATION; WESTERN BLOTTING; WILD TYPE;

CAENORHABDITIS ELEGANS; CONGENITAL DISORDER OF GLYCOSYLATION; FREE OLIGOSACCHARIDE; N-GLYCAN; Α-GLUCOSIDASE I;

ALPHA-GLUCOSIDASES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; CRICETINAE; ENDOPLASMIC RETICULUM STRESS; GLYCOPROTEINS; GLYCOSYLATION; LONGEVITY; OLIGOSACCHARIDES; PROTEOLYSIS; RNA, SMALL INTERFERING;

EID: 84887928744     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt051     Document Type: Article

References (64)

1. Research Resources (P41RR018502) and the National Institute of General Medical Sciences (P41GM103490) from the National Institutes of Health, USA.
2. Alonzi DS, Neville DC, Lachmann R.H., Dwek RA, Butters TD 2008. Glucosylated free oligosaccharides are biomarkers of endoplasmic-reticulum α-glucosidase inhibition. Biochem J. 409: 571-580.
3. Altmann F, Fabini G, Ahorn H., Wilson IB 2001. Genetic model organisms in the study of N-glycans. Biochimie. 83: 703-712.
4. Anumula KR, Spiro RG 1983. Release of glucose-containing polymannose oli-gosaccharides during glycoprotein biosynthesis. Studies with thyroid microsomal enzymes and slices. J Biol Chem. 258: 15274-15282.
5. Anumula KR, Taylor PB 1992. A comprehensive procedure for preparation of partially methylated alditol acetates from glycoprotein carbohydrates. Anal Biochem. 203: 101-108.
6. Aoki K, Perlman M, Lim J.M., Cantu R., Wells L, Tiemeyer M. 2007. Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo. J Biol Chem. 282: 9127-9142.
7. n. Anal Chem. 77: 6250-6262.
8. Belard M, Cacan R, Verbert A. 1988. Characterization of an oligosaccharide-pyrophosphodolichol pyrophosphatase activity in yeast. Biochem J. 255: 235-242.
9. Bernales S, McDonald KL, Walter P. 2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4: e423.
10. Blom D, Hirsch C, Stern P., Tortorella D, Ploegh HL 2004. A glycosylated type I membrane protein becomes cytosolic when peptide: N-glycanase is compromised. EMBO J. 23: 650-658.
11. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77: 71-94.
12. Calfon M, Zeng H, Urano F., Till JH, Hubbard SR, Harding HP, Clark S.G., Ron D. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 415: 92-96.
13. Casarejos MJ, Solano RM, Gomez A, Perucho J., de Yebenes JG, Mena MA 2011. The accumulation of neurotoxic proteins, induced by proteasome inhibition, is reverted by trehalose, an enhancer of autophagy, in human neuro-blastoma cells. Neurochem Int. 58: 512-520.
14. Chantret I, Moore SE 2008. Free oligosaccharide regulation during mammalian protein N-glycosylation. Glycobiology. 18: 210-224.
15. Cipollo JF, Awad AM, Costello C.E., Hirschberg CB 2005. N-Glycans of Caenorhabditis elegans are specific to developmental stages. J Biol Chem. 280: 26063-26072.
16. Cipollo JF, Costello CE, Hirschberg CB 2002. The fine structure of Caenorhabditis elegans N-glycans. J Biol Chem. 277: 49143-49157.
17. Clerc S, Hirsch C, Oggier D.M., Deprez P., Jakob C, Sommer T, Aebi M. 2009. Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum. J Cell Biol. 184: 159-172.
18. Cox JS, Walter P. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell. 87: 391-404.
19. De Praeter C.M., Gerwig GJ, Bause E, Nuytinck L.K., Vliegenthart JF, Breuer W, Kamerling JP, Espeel M.F., Martin JJ, De Paepe AM, et al 2000. A novel disorder caused by defective biosynthesis of N-linked oligosaccharides due to glucosidase I deficiency. Am J Hum Genet. 66: 1744-1756.
20. Durrant C, Moore SE 2002. Perturbation of free oligosaccharide trafficking in endoplasmic reticulum glucosidase I-deficient and castanospermine-treated cells. Biochem J. 365: 239-247.
21. Hanneman AJ, Rosa JC, Ashline D, Reinhold VN 2006. Isomer and glycomer complexities of core GlcNAcs in Caenorhabditis elegans. Glycobiology. 16: 874-890.
22. Haslam SM, Dell A. 2003. Hallmarks of Caenorhabditis elegans N-glycosylation: Complexity and controversy. Biochimie. 85: 25-32.
23. Helenius A, Aebi M. 2001. Intracellular functions of N-linked glycans. Science. 291: 2364-2369.
24. Helenius A, Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem. 73: 1019-1049.
25. Hirayama H, Seino J, Kitajima T., Jigami Y, Suzuki T. 2010. Free oligosaccharides to monitor glycoprotein endoplasmic reticulum-associated degradation in Saccharomyces cerevisiae. J Biol Chem. 285: 12390-12404.
26. Hong Y, Sundaram S, Shin D.J., Stanley P. 2004. The Lec23 Chinese hamster ovary mutant is a sensitive host for detecting mutations in α-glucosidase I that give rise to congenital disorder of glycosylation IIb (CDG IIb). J Biol Chem. 279: 49894-49901.
27. Hosokawa N, Tremblay LO, Sleno B, Kamiya Y., Wada I, Nagata K, Kato K., Herscovics A. 2010. EDEM1 accelerates the trimming of α1,2-linked mannose on the C branch of N-glycans. Glycobiology. 20: 567-575.
28. Kalz-Fuller B., Bieberich E, Bause E. 1995. Cloning and expression of glucosidase I from human hippocampus. Eur J Biochem. 231: 344-351.
29. Kamath RS, Martinez-Campos M, Zipperlen P., Fraser AG, Ahringer J. 2000. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2: research0002.1-research0002.10.
30. Kato T, Kawahara A, Ashida H., Yamamoto K. 2007. Unique peptide: N-glycanase of Caenorhabditis elegans has activity of protein disulphide reductase as well as of deglycosylation. J Biochem. 142: 175-181.
31. Kato T, Kitamura K, Maeda M., Kimura Y, Katayama T, Ashida H., Yamamoto K. 2007. Free oligosaccharides in the cytosol of Caenorhabditis elegans are generated through endoplasmic reticulum-golgi trafficking. J Biol Chem. 282: 22080-22088.
32. Kimura KD, Tissenbaum HA, Liu Y.X., Ruvkun G. 1997. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 277: 942-946.
33. Lin K, Dorman JB, Rodan A, Kenyon C. 1997. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science. 278: 1319-1322.
34. Liu YL, Lu WC, Brummel T.J., Yuh CH, Lin PT, Kao TY, Li F.Y., Liao PC, Benzer S, Wang HD 2009. Reduced expression of α-1,2-mannosidase I extends lifespan in Drosophila melanogaster and Caenorhabditis elegans. Aging Cell. 8: 370-379.
35. Maattanen P, Gehring K, Bergeron J.J., Thomas DY 2010. Protein quality control in the ER: The recognition of misfolded proteins. Semin Cell Dev Biol. 21: 500-511.
36. Melendez A, Talloczy Z, Seaman M., Eskelinen EL, Hall DH, Levine B. 2003. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science. 301: 1387-1391.
37. Mellor HR, Neville DC, Harvey D.J., Platt FM, Dwek RA, Butters TD 2004. Cellular effects of deoxynojirimycin analogues: Inhibition of N-linked oligosaccharide processing and generation of free glucosylated oligosaccharides. Biochem J. 381: 867-875.
38. Moore SE, Spiro RG 1994. Intracellular compartmentalization and degradation of free polymannose oligosaccharides released during glycoprotein biosynthesis. J Biol Chem. 269: 12715-12721.
39. Mori K. 2000. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell. 101: 451-454.
40. Morris JZ, Tissenbaum HA, Ruvkun G. 1996. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature. 382: 536-539.
41. Natsuka S, Adachi J, Kawaguchi M., Nakakita S, Hase S, Ichikawa A., Ikura K. 2002. Structural analysis of N-linked glycans in Caenorhabditis elegans. J Biochem. 131: 807-813.
42. Ogg S, Paradis S, Gottlieb S., Patterson GI, Lee L, Tissenbaum HA, Ruvkun G. 1997. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature. 389: 994-999.
43. Paschinger K, Gutternigg M, Rendic D., Wilson IB 2008. The N-glycosylation pattern of Caenorhabditis elegans. Carbohydr Res. 343: 2041-2049.
44. Paschinger K, Rendic D, Lochnit G., Jantsch V, Wilson IB 2004. Molecular basis of anti-horseradish peroxidase staining in Caenorhabditis elegans. J Biol Chem. 279: 49588-49598.
45. Paschinger K, Rendic D, Wilson IB 2009. Revealing the anti-HRP epitope in Drosophila and Caenorhabditis. Glycoconj J. 26: 385-395.
46. Patel T, Bruce J, Merry A., Bigge C, Wormald M, Jaques A., Parekh R. 1993. Use of hydrazine to release in intact and unreduced form both N- and O-linked oligosaccharides from glycoproteins. Biochemistry. 32: 679-693.
47. Ray MK, Yang J, Sundaram S., Stanley P. 1991. A novel glycosylation phenotype expressed by Lec23, a Chinese hamster ovary mutant deficient in α-glucosidase I. J Biol Chem. 266: 22818-22825.
48. Ruddock LW, Molinari M. 2006. N-Glycan processing in ER quality control. J Cell Sci. 119: 4373-4380.
49. Saint-Pol A., Codogno P, Moore SE 1999. Cytosol-to-lysosome transport of free polymannose-type oligosaccharides. Kinetic and specificity studies using rat liver lysosomes. J Biol Chem. 274: 13547-13555.
50. Sarkar S, Davies JE, Huang Z, Tunnacliffe A., Rubinsztein DC 2007. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and α-synuclein. J Biol Chem. 282: 5641-5652.
51. Sarkar M, Iliadi KG, Leventis P.A., Schachter H., Boulianne GL 2010. Neuronal expression of Mgat1 rescues the shortened life span of Drosophila Mgat1 null mutants and increases life span. Proc Natl Acad Sci USA. 107: 9677-9682.
52. Sarkar M, Leventis PA, Silvescu C.I., Reinhold VN, Schachter H, Boulianne GL 2006. Null mutations in Drosophila N-acetylglucosaminyltransferase I produce defects in locomotion and a reduced life span. J Biol Chem. 281: 12776-12785.
53. Schachter H. 2009. Paucimannose N-glycans in Caenorhabditis elegans and Drosophila melanogaster. Carbohydr Res. 344: 1391-1396.
54. Shintani T, Yamazaki F, Katoh T., Umekawa M, Matahira Y, Hori S., Kakizuka A, Totani K, Yamamoto K., Ashida H. 2010. Glucosamine induces autophagy via an mTOR-independent pathway. Biochem Bioph Res Commun. 391: 1775-1779.
55. Sidrauski C, Cox JS, Walter P. 1996. tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell. 87: 405-413.
56. Sousa MC, Ferrero-Garcia MA, Parodi AJ 1992. Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Glc: glycoprotein glucosyltransferase. Biochemistry. 31: 97-105.
57. Suzuki T. 2007. Cytoplasmic peptide: N-glycanase and catabolic pathway for free N-glycans in the cytosol. Semin Cell Dev Biol. 18: 762-769.
58. Suzuki T, Hara I, Nakano M., Shigeta M, Nakagawa T, Kondo A., Funakoshi Y, Taniguchi N. 2006. Man2C1, an α-mannosidase, is involved in the trimming of free oligosaccharides in the cytosol. Biochem J. 400: 33-41.
59. Suzuki T, Park H, Hollingsworth N.M., Sternglanz R., Lennarz WJ 2000. PNG1, a yeast gene encoding a highly conserved peptide: N-glycanase. J Cell Biol. 149: 1039-1052.
60. Volker C, De Praeter CM, Hardt B, Breuer W, Kalz-Fuller B, Van Coster RN, Bause E. 2002. Processing of N-linked carbohydrate chains in a patient with glucosidase I deficiency (CDG type IIb). Glycobiology. 12: 473-483.
61. Xie W, Ng DT 2010. ERAD substrate recognition in budding yeast. Semin Cell Dev Biol. 21: 533-539.
62. Yorimitsu T, Nair U, Yang Z., Klionsky DJ 2006. Endoplasmic reticulum stress triggers autophagy. J Biol Chem. 281: 30299-30304.
63. Zapun A, Darby NJ, Tessier D.C., Michalak M., Bergeron JJ, Thomas DY 1998. Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J Biol Chem. 273: 6009-6012.
64. Zhu S, Hanneman A, Reinhold V.N., Spence AM, Schachter H. 2004. Caenorhabditis elegans triple null mutant lacking UDP-N-acetyl-d-glucosamine: α-3-d-mannoside β1,2-N-acetylglucosaminyltransferase I. Biochem J. 382: 995-1001.