Structural features of free N-glycans occurring in plants and functional features of de-N-glycosylation enzymes, ENGase, and PNGase: The presence of unusual plant complex type N-glycans

Frontiers in Plant Science

Volumn 5, Issue SEP, 2014, Pages

  Maeda, Megumi ^a   Kimura, Yoshinobu ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

ENGase; Free N glycans; Glycochaperone; Knockout plant; PNGase

Indexed keywords

EID: 84908181407     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00429     Document Type: Review

References (52)

1. Alisi, C., Afferni, C., Iacovacci, P., Barletta, B., Tinghino, R., Butteroni, C.,et al. (2001). Rapid isolation, characterization, and glycan analysis of Cup a 1, the major allergen of Arizona cypress (Cupressus arizonica) pollen. Allergy 56, 978-984. doi: 10.1034/j.1398-9995.2001.103125.x
2. Altmann, F., Paschinger, K., Dalik, T., and Vorauer, K. (1998). Characterisation of peptide-N4-(N-acetyl-β-glucosaminyl)asparagine amidase A and its N-glycans. Eur. J. Biochem. 252, 118-123. doi: 10.1046/j.1432-1327.1998.2520118.x
3. Boisson, M., Gomord, V., Audran, C., Berger, N., Dubreucq, D., Granier, F.,et al. (2001). Arabidopsis glucosidase Imutants reveal a critical role of N-glycan trimming in seed development. EMBO J. 20, 1010-1019. doi: 10.1093/emboj/20.5.1010
4. Chang, T., Kuo, M. C., Khoo, K. H., Inoue, S., and Inoue, Y. (2000). Developmentally regulated expression of a peptide:N-glycanase during germination of rice seeds (Oryza sativa) and its purification and characterization. J. Biol. Chem. 275, 129-134. doi: 10.1074/jbc.275.1.129
5. Diepold, A., Li, G., Lennarz, W. J., Nürnberger, T., and Brunner, F. (2007). The Arabidopsis AtPNG1 gene encodes a peptide:N-glycanase. Plant J. 52, 94-104. doi: 10.1111/j.1365-313X.2007.03215.x
6. Faugeron, C., Lhernould, S., Lemoine, J., Costa, G., and Morvan, H. (1997a). Identification of unconjugated N-glycans in strawberry plants. Plant Physiol. Biochem. 35, 891-895.
7. Faugeron, C., Lhernould, S., Maes, E., Lerouge, P., Strecker, G., and Morvan, H. (1997b). Tomato plant leaves also contain unconjugated N-glycans. Plant Physiol. Biochem. 35, 73-79.
8. Fichette-Lainè, A. C., Gomord, V., Cabanes, M., Michalski, J. C., Macary, M. S., Foucher, B.,et al. (1997). N-glycans harboring the Lewis a epitope are expressed at the surface of plant cells. Plant J. 12, 1411-1417. doi: 10.1046/j.1365-313x.1997.12061411.x
9. Fischl, R. M., Stadlmann, J., Grass, J., Altman F., and Léonard, R. (2011). The two endo-β-N-acetylglucosaminidase genes from Arabidopsis thaliana encode cytoplasmic enzymes controlling free N-glycan levels. Plant Mol. Biol. 77, 275-284. doi: 10.1007/s11103-011-9808-7
10. Gillmor, S. C., Poindexter, P., Lorieau, J., Palcic, M. M., and Somerville, C. (2002). α-Glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. J. Cell. Biol. 156, 1003-1013. doi: 10.1083/jcb.200111093
11. Hossain, M. A., Nakano, R., Nakamura, K., Hossain, M. T., and Kimura, Y. (2010a). 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. doi: 10.1093/jb/mvq094
12. Hossain, M. A., Nakano, R., Nakamura, K., and Kimura, Y. (2010b). Molecular identification and characterization of an acidic peptide:N-glycanase (PNGase) from tomato (Lycopersicum esculentum) fruits. J. Biochem. 147, 157-165. doi: 10.1093/jb/mvp157
13. Ishizuka, A., Hashimoto, Y., Naka, R., Kinoshita, M., Kakehi, K., Seino, J.,et al. (2008). Accumulation of free complex-type N-glycans in MKN7 and MKN45 stomach cancer cells. Bichem. J. 413, 227-237. doi: 10.1042/BJ20071562
14. Jitsuhara, Y., Toyoda, T., Itai, T., and Yamaguchi, H. (2002). Chaperone-like functions of high-mannose type and complex-type N-glycans and their molecular basis. J. Biochem. 132, 803-811. doi: 10.1093/oxfordjournals.jbchem.a003290
15. Kang, J. S., Frank, J., Kang, C. H., Kajiura, H., Vikram, M., Ueda, A.,et al. (2008). Salt tolerance of Arabidopsis thaliana requires mutation of N-glycosylated proteins in the Golgi apparatus. Proc. Natl. Acad. Sci. U.S.A. 105, 5933-5938. doi: 10.1073/pnas.0800237105
16. Kato, T., Fujita, K., Takeuchi, M., Kobayashi, K., Natsuka, S., Ikura, K.,et al. (2002). Identification of an endo-β-N-acetylglucosaminidase gene in Caenorhabditis elegans and its expression in Escherichia coli. Glycobiology 12, 581-587. doi: 10.1093/glycob/cwf073
17. Kato, T., Hatanaka, K., Mega, T., and Hase, S. (1997). Purification and characterization of endo-β-N-acetylglucosaminidase from hen oviduct. J. Biochem. 122, 1167-1173. doi: 10.1093/oxfordjournals.jbchem.a021877
18. Kimura, N., Uchida, M., Nishimura, S., and Yamaguchi, H. (1998). Promotion of polypeptide folding by interactions with Asn-Glycans. J. Biochem. 124, 857-862. doi: 10.1093/oxfordjournals.jbchem.a022190
19. Kimura, Y. (2007). "Structural and functional features of plant glycoprotein glycans," in Comprehensive Glycoscience-From Chemistry to Systems Biology, Vol. 3, ed. H. Kamerling (Oxford: Elsevier), 61-76.
20. Kimura, Y., Hess, D., and Strum, A. (1999). The N-glycans of jack bean α-mannosidase. Structure, topology and function. Eur. J. Biochem. 264, 168-175. doi: 10.1046/j.1432-1327.1999.00598.x
21. Kimura, Y., Kamamoto, M., Maeda, M., Okano, M., Yokoyama, M., and Kino, K. (2005). Occurrence of Lewis a epitope in N-glycans of a glycoallergen, Jun a 1, from mountain cedar (Juniperus ashei) pollen. Biosci. Biotechnol. Biochem. 69, 137-144. doi: 10.1271/bbb.69.137
22. Kimura, Y., and Kitahara, E. (2000). Structural analysis of free N-glycans occurring in soybean seedlings. Biosci. Biotechnol. Biochem. 64, 1847-1855. doi: 10.1271/bbb.64.1847
23. Kimura, Y., and Matsuo, S. (2000). Free N-glycans already occur at an early stage of seed development. J. Biochem. 127, 1013-1019. doi: 10.1093/oxfordjournals.jbchem.a022692
24. Kimura, Y., Matsuo, S., Tsurusaki, S., Kimura, M., Nishimura-Hara, I., and Nishimura, M. (2002). Subcellular localization of endo-β-N-acetylglucosaminidase and high-mannose type free N-glycans in plant cell. Biochim. Biophys. Acta 1570, 38-46. doi: 10.1016/S0304-4165(02)00149-6
25. Kimura, Y., and Ohno, A. (1998). A new peptide-N4-(acetyl-β-glucosaminyl)asparagine amidase from soybean (Glycime max) seeds: purification and substrate specificity. Biosci. Biotech. Biochem. 62, 412-418. doi: 10.1271/bbb.62.412
26. Kimura, Y., Takagi, S., and Shiraishi, T. (1997). Occurrence of free N-glycans in pea (Pisum sativum L.) seedlings. Biosci. Biotechnol. Biochem. 61, 924-926. doi: 10.1271/bbb.61.924
27. Kimura, Y., Takeoka, Y., Inoue, M., Maeda, M., and Fujiyama, K. (2011). Double-knockout of putative endo-β-N-acetylglucosaminidase (ENGase) genes in Arabidopsis thaliana: loss of ENGase activity induced accumulation of high-mannose type free N-glycans bearing N,N′-acetylchitobiosyl unit. Biosci. Biotech. Biochem. 75, 1019-1021. doi: 10.1271/bbb.110148
28. Kobata, A. (2007). "Glycoprotein glycan structures," in Comprehensive GlycoscienceFrom Chemistry to Systems Biology, ed. H. Kamerling (Oxford: Elsevier), 1, 39-72.
29. Lerouge, P., Cabanes-Macheteau, M., Rayon, C., Fischette-Lainé, A. C., Gomord, V., and Faye, L. (1998). N-Glycoprotein biosynthesis in plants: recent developments and future trends. Plant. Mol. Biol. 38, 31-48. doi: 10.1023/A:1006012005654
30. Lhernould, S., Karamanos, Y., Lerouge, P., and Morvan, H. (1995). Characterization of the peptide-N4-(N-acetylglucosaminyl) asparagine amidase (PNGase Se) from Silene alba cells. Glycoconjugate J. 12, 94-98. doi: 10.1007/BF00731874
31. Maeda, M., Kamamoto, M., Yamamoto, S., Kimura, M., Okano, M., and Kimura, Y. (2005). Glycoform analysis of Japanese cedar pollen allergen, Cry j1. Biosci. Biotechnol. Biochem. 69, 1700-1705. doi: 10.1271/bbb.69.1700
32. Maeda, M., Kimura, M., and Kimura, Y. (2010). Intracellular and extracellular free N-glycans produced by plant cells: occurrence of unusual plant complex-type free N-glycans in extracellular spaces. J. Biochem. 148, 681-692. doi: 10.1093/jb/mvq102
33. Masahara-Negishi, Y., Hosomi, A., Della Mea, M., Serafini-Fracassini, D., and Suzuki, T. (2012). A plant peptide: N-glycanase orthologue facilitates glycoprotein ER-associated degradation in yeast. Biochim. Biphys. Acta 1820, 1457-1462. doi: 10.1016/j.bbagen.2012.05.009
34. Meli, V. S., Ghosh, S., Prabha, T. N., Chakraborty, N., Chakraborty, S., and Datta, A. (2010). Enhancement of fruit shelf life by suppressing N-glycan processing enzymes. Proc. Natl. Acad. Sci. U.S.A. 107, 2413-2418. doi: 10.1073/pnas.0909329107
35. Nakamura, K., Inoue, M., Nakano, R., Hosoi K., and Kimura, Y. (2009). Molecular cloning and gene expression analysis of tomato endo-β-N-acetylglucosaminidase, an endoglycosidase involved in the production of high-mannose type free N-glycans during tomato fruit ripening. Biosci. Biotechnol. Biochem. 73, 461-464. doi: 10.1271/bbb.80889
36. Nakamura, K., Inoue, M., Yoshiie, T., Hosoi, K., and Kimura, Y. (2008). Changes in structural features of free N-glycan and endoglycosidase activity during tomato fruit ripening. Biosci. Biotechnol. Biochem. 72, 2936-2945. doi: 10.1271/bbb.80414
37. Priem, B., Gitti, R., Bush, C. A., and Gross, K. C. (1993). Structure of ten free N-glycans in ripening tomato fruit. Arabinose is a constituent of a plant N-glycan. Plant Physiol. 102, 445-458. doi: 10.1104/pp.102.2.445
38. Priem, B., and Gross, K. C. (1992). Mannosyl- and xylosyl-containing glycans promote tomato (Lycopersicon esculentum Mill.) fruit ripening. Plant Physiol. 98, 399-401. doi: 10.1104/pp.98.1.399
39. Priem, B., Morvan, H., Hafez, A. M. A., and Morvan, C. (1990a). Influence d'un xylmannoside d'origine vegetale sur l'elongation de l'hypocotyle de Lin. C. R. Acad. Sci. Paris. 311, 411-416.
40. Priem, B., Solokwan, J., Wieruszeski, J. M., Strecker, G., Nazih, H., and Morvan, H. (1990b). Isolation and characterization of free glycans of the oligomannoside type from the extracellular medium of a plant cell suspension. Glycoconjugate J. 7, 121-132. doi: 10.1007/BF01050375
41. Suzuki, T., and Funakoshi, Y. (2006). Free N-linked oligosaccharide chains: formation and degradation. Glycoconjugate J. 23, 291-302. doi: 10.1007/s10719-006-6975-x
42. Suzuki, T., Park, H., Hollingsworth, N. M., Sternglanz, R., and Lennarz, W. J. (2000). PNG1, a yeast gene encoding a highly conserved peptide:N-glycanase. J. Cell. Biol. 29, 1039-1052. doi: 10.1083/jcb.149.5.1039
43. Suzuki, T., Park, H., Kwofie, M. A., and Lennarz, W. J. (2001). Rad23 provides a link between the Png1 deglycosylating enzyme and the 26 S proteasome in yeast. J. Biol. Chem. 276, 21601-21607. doi: 10.1074/jbc.M100826200
44. Suzuki, T., Tanabe, K., and Funakoshi, Y. (2007). "Folding and quality control of glycoproteins," in Comprehensive Glycoscience-From Chemistry to Systems Biology, Vol. 3, ed. H. Kamerling (Oxford: Elsevier), 129-149.
45. Suzuki, T., Yano, K., Sugimoto, S., Kitajima, K., Lennarz, W. J., Inoue, S.,et al. (2002). Endo-β-N-acetylglucosaminidase, an enzyme involved in processing of free oligosaccharides in the cytosol. Proc. Natl. Acad. Sci. U.S.A. 99, 9691-9696. doi: 10.1073/pnas.152333599
46. Takahashi, N. (1977). Demonstration of a new amidase acting on glycopeptides. Biochem. Biophys. Res. Commun.76, 1194-1201. doi: 10.1016/0006-291X(77)90982-2
47. Takahashi, N., and Nishibe, H. (1978). Some characteristics of a new glycopeptidase acting on aspartylglycosylamine linkages. J. Biochem. 84, 1467-1473.
48. Vitale, A., and Chrispeels, M. J. (1984). Transient N-acetylglucosamine in the biosynthesis of phytohemagglutinin: attachment in the golgi apparatus and removal in protein bodies. J. Cell Biol. 99, 133-140. doi: 10.1083/jcb.99.1.133
49. Wilson, I. B. H., Zeleny, R., Kolarich, D., Staudacher, E., Stroop, C. J. M., Kamerling, J. P.,et al. (2001). Analysis of Asn linked glycans from vegetable foodstuffs: widespread occurrence of Lewis a, core α1,3-linked fucose and xylose substitutions. Glycobiology 11, 261-274. doi: 10.1093/glycob/11.4.261
50. Yamamoto, K. (2006). "Endoglycosidases that relate to N-glycans," in Endoglycosidase, eds M. Endo, S. Hase, K. Yamamoto, and K. Takagaki (Tokyo: Kodansha-Springer), 55-74.
51. Yamamoto, K. (2012). Biological analysis of the microbial metabolism of hetero-oligosaccharides in application to glycotechnology. Biosci. Biotechnol. Biochem. 76, 1815-1827. doi: 10.1271/bbb.120401
52. Yunovitz, H., and Gross, K. C. (1994). Delay of tomato fruit ripening by an oligosaccharide N-glycan. Interactions with IAA, galactose and lectins. Physiol. Plantarum 90, 152-156. doi: 10.1111/j.1399-3054.1994.tb02205.x