Purification and characterization of Arabidopsis thaliana oligosaccharyltransferase complexes from the native host: a protein super-expression system for structural studies

Plant Journal

Volumn 94, Issue 1, 2018, Pages 131-145

  Jeong, In Sil ^a,b   Lee, Sangmin ^c   Bonkhofer, Florian ^d   Tolley, Jordan ^a   Fukudome, Akihito ^a   Nagashima, Yukihiro ^a   May, Kimberly ^a   Rips, Stephan ^d   Lee, Sang Y ^e   Gallois, Patrick ^f   Russell, William K ^g   Jung, Hyun Suk ^c   von Schaewen, Antje ^d   Koiwa, Hisashi ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b Catholic Kwandong University   (South Korea)

^c Kangwon National University   (South Korea)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e Gyeongsang National University   (South Korea)

^f UNIVERSITY OF MANCHESTER   (United Kingdom)

^g University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Arabidopsis thaliana; oligosaccharyltransferase complex; protein N glycosylation; ribosome; tandem affinity purification; transmission electron microscopy

Indexed keywords

CELL MEMBRANES; ELECTRON AFFINITY; ELECTRON MICROSCOPY; GENE ENCODING; GLYCOSYLATION; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; MACROMOLECULES; MASS SPECTROMETRY; PLANTS (BOTANY); PURIFICATION; RECOMBINANT PROTEINS; TRANSMISSION ELECTRON MICROSCOPY;

ARABIDOPSIS THALIANA; N-GLYCOSYLATION; OLIGOSACCHARYLTRANSFERASE; RIBOSOME; TANDEM AFFINITY PURIFICATION;

PROTEINS;

ANALYSIS; ELECTRON MICROSCOPY; MACROMOLECULES; PLANTS; PROTEINS; PURIFICATION; SPECTROMETERS; TRANSMISSION ELECTRON MICROSCOPY;

ARABIDOPSIS PROTEIN; DOLICHYL-DIPHOSPHOOLIGOSACCHARIDE - PROTEIN GLYCOTRANSFERASE; GLYCOSYLTRANSFERASE; MEMBRANE PROTEIN;

ARABIDOPSIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; RIBOSOME; TRANSMISSION ELECTRON MICROSCOPY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; HEXOSYLTRANSFERASES; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; RIBOSOMES; TANDEM AFFINITY PURIFICATION;

EID: 85043458460     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13847     Document Type: Article

References (52)

1. Aoki, Y., Okamura, Y., Tadaka, S., Kinoshita, K. and Obayashi, T. (2016) ATTED-II in 2016: a plant coexpression database towards lineage-specific coexpression. Plant Cell Physiol. 57, e5.
2. Brach, T., Soyk, S., Muller, C., Hinz, G., Hell, R., Brandizzi, F. and Meyer, A.J. (2009) Non-invasive topology analysis of membrane proteins in the secretory pathway. Plant J. 57, 534–541.
3. Buren, S., Ortega-Villasante, C., Blanco-Rivero, A., Martinez-Bernardini, A., Shutova, T., Shevela, D., Messinger, J., Bako, L., Villarejo, A. and Samuelsson, G. (2011) Importance of post-translational modifications for functionality of a chloroplast-localized carbonic anhydrase (CAH1) in Arabidopsis thaliana. PLoS ONE, 6, e21021.
4. Butaye, K.M., Goderis, I.J., Wouters, P.F., Pues, J.M., Delaure, S.L., Broekaert, W.F., Depicker, A., Cammue, B.P. and De Bolle, M.F. (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutants and matrix attachment regions. Plant J. 39, 440–449.
5. Chi, J.H., Roos, J. and Dean, N. (1996) The OST4 gene of Saccharomyces cerevisiae encodes an unusually small protein required for normal level of oligosaccharyltransferase activity. J. Biol. Chem. 271, 3132–3140.
6. Curtis, M.D. and Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469.
7. Danon, A., Rotari, V.I., Gordon, A., Mailhac, N. and Gallois, P. (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and defender against apoptotic death. J. Biol. Chem. 279, 779–787.
8. Doelling, J.H. and Pikaard, C.S. (1993) Transient expression in Arabidopsis thaliana protoplasts derived from rapidly established cell suspension cultures. Plant Cell Rep. 12, 241–244.
9. Farid, A., Malinovsky, F.G., Veit, C., Schoberer, J., Zipfel, C. and Strasser, R. (2013) Specialized roles of the conserved subunit OST3/6 of the oligosaccharyltransferase complex in innate immunity and tolerance to abiotic stresses. Plant Physiol. 162, 24–38.
10. Frank, J., Kaulfurst-Soboll, H., Rips, S., Koiwa, H. and von Schaewen, A. (2008) Comparative analyses of Arabidopsis cgl1 (complex glycan 1) mutants and genetic interaction with stt3a (staurosporin & temperature-sensitive 3a). Plant Physiol. 148, 1354–1367.
11. Freeze, H.H. (2013) Understanding human glycosylation disorders: biochemistry leads the charge. J. Biol. Chem. 288, 6936–6945.
12. Fukudome, A., Aksoy, E., Wu, X., Kumar, K., Jeong, I.S., May, K., Russell, W.K. and Koiwa, H. (2014) Arabidopsis CPL4 is an essential C-terminal domain phosphatase that suppresses xenobiotic stress responses. Plant J. 80, 27–39.
13. Gallois, P., Makishima, T., Hecht, V., Despres, B., Laudie, M., Nishimoto, T. and Cooke, R. (1997) An Arabidopsis thaliana cDNA complementing a hamster apoptosis suppressor mutant. Plant J. 11, 1325–1331.
14. Gehl, C., Kaufholdt, D., Hamisch, D., Bikker, R., Kudla, J., Mendel, R.R. and Hansch, R. (2011) Quantitative analysis of dynamic protein-protein interactions in planta by a floated-leaf luciferase complementation imaging (FLuCI) assay using binary Gateway vectors. Plant J. 67, 542–553.
15. Hanson, G.T., Aggeler, R., Oglesbee, D., Cannon, M., Capaldi, R.A., Tsien, R.Y. and Remington, S.J. (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J. Biol. Chem. 279, 13044–13053.
16. Harada, Y., Li, H., Li, H. and Lennarz, W.J. (2009) Oligosaccharyltransferase directly binds to ribosome at a location near the translocon-binding site. Proc. Natl Acad. Sci. USA, 106, 6945–6949.
17. Häweker, H., Rips, S., Koiwa, H., Salomon, S., Saijo, Y., Chinchilla, D., Robatzek, S. and von Schaewen, A. (2010) Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285, 4629–4636.
18. Helenius, A. and Aebi, M. (2001) Intracellular functions of N-linked glycans. Science, 291, 2364–2369.
19. Jeong, I.S., Fukudome, A., Aksoy, E. et al. (2013) Regulation of abiotic stress signalling by Arabidopsis C-terminal domain phosphatase-like 1 requires interaction with a K-homology domain-containing protein. PLoS ONE, 8, e80509.
20. Johnson, M.A., von Besser, K., Zhou, Q., Smith, E., Aux, G., Patton, D., Levin, J.Z. and Preuss, D. (2004) Arabidopsis hapless mutations define essential gametophytic functions. Genetics, 168, 971–982.
21. Kang, J.S., Frank, J., Kang, C.H. et al. (2008) Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc. Natl Acad. Sci. USA, 105, 5933–5938.
22. Karaoglu, D., Kelleher, D.J. and Gilmore, R. (1997) The highly conserved Stt3 protein is a subunit of the yeast oligosaccharyltransferase and forms a subcomplex with Ost3p and Ost4p. J. Biol. Chem. 272, 32513–32520.
23. Kasajima, I., Ide, Y., Ohkama-Ohtsu, N., Hayashi, H., Yoneyama, T. and Fujiwara, T. (2004) A protocol for rapid DNA extraction fromArabidopsis thaliana for PCR analysis. Plant Mol. Biol. Rep. 22, 49–52.
24. Kelleher, D.J. and Gilmore, R. (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology, 16, 47R–62R.
25. Kelleher, D.J., Kreibich, G. and Gilmore, R. (1992) Oligosaccharyltransferase activity is associated with a protein complex composed of ribophorins I and II and a 48 kd protein. Cell, 69, 55–65.
26. Klodmann, J., Sunderhaus, S., Nimtz, M., Jänsch, L. and Braun, H.-P. (2010) Internal architecture of mitochondrial complex I from Arabidopsis thaliana. Plant Cell, 22, 797–810.
27. Knauer, R. and Lehle, L. (1999) The oligosaccharyltransferase complex from yeast. Biochim. Biophys. Acta, 1426, 259–273.
28. Koiwa, H., Li, F., McCully, M.G. et al. (2003) The STT3a subunit isoform of the Arabidopsis thaliana oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell, 15, 2273–2284.
29. Kouřil, R., Zygadlo, A., Arteni, A.A., de Wit, C.D., Dekker, J.P., Jensen, P.E., Scheller, H.V. and Boekema, E.J. (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry, 44, 10935–10940.
30. Lee, S., Chung, J.M., Yun, H.J., Won, J. and Jung, H.S. (2016) New insight into multifunctional role of peroxiredoxin family protein: determination of DNA protection properties of bacterioferritin comigratory protein under hyperthermal and oxidative stresses. Biochem. Biophys. Res. Commun. 469, 1028–1033.
31. Lehtimaki, N., Koskela, M.M. and Mulo, P. (2015) Posttranslational modifications of chloroplast proteins: an emerging field. Plant Physiol. 168, 768–775.
32. Lerouxel, O., Mouille, G., Andeme-Onzighi, C., Bruyant, M.P., Seveno, M., Loutelier-Bourhis, C., Driouich, A., Hofte, H. and Lerouge, P. (2005) Mutants in DEFECTIVE GLYCOSYLATION, an Arabidopsis homolog of an oligosaccharyltransferase complex subunit, show protein underglycosylation and defects in cell differentiation and growth. Plant J. 42, 455–468.
33. Ludtke, S.J., Baldwin, P.R. and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82–97.
34. Ma, J., Wang, D., She, J., Li, J., Zhu, J.K. and She, Y.M. (2016) Endoplasmic reticulum-associated N-glycan degradation of cold-upregulated glycoproteins in response to chilling stress in Arabidopsis. New Phytol. 212, 282–296.
35. Mitsuhara, I., Ugaki, M., Hirochika, H. et al. (1996) Efficient promoter casettes for enhanced expresion of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol. 37, 49–59.
36. Muller, L.M., Lindner, H., Pires, N.D., Gagliardini, V. and Grossniklaus, U. (2016) A subunit of the oligosaccharyltransferase complex is required for interspecific gametophyte recognition in Arabidopsis. Nat. Commun. 7, 10826.
37. Nelson, B.K., Cai, X. and Nebenfuhr, A. (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126–1136.
38. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H. and Kinoshita, K. (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987–D991.
39. de Oliveira, M.V.V., Xu, G., Li, B. et al. (2016) Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nat. Plants, 2, 15218.
40. Onate-Sanchez, L. and Vicente-Carbajosa, J. (2008) DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res. Notes, 1, 93.
41. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612.
42. Rips, S., Bentley, N., Jeong, I.S., Welch, J.L., von Schaewen, A. and Koiwa, H. (2014) Multiple N-glycans cooperate in the subcellular targeting and functioning of Arabidopsis KORRIGAN1. Plant Cell, 26, 3792–3808.
43. Ruiz-Canada, C., Kelleher, D.J. and Gilmore, R. (2009) Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms. Cell, 136, 272–283.
44. Shrimal, S., Ng, B.G., Losfeld, M.-E., Gilmore, R. and Freeze, H.H. (2013) Mutations in STT3A and STT3B cause two congenital disorders of glycosylation. Hum. Mol. Genet. 22, 4638–4645.
45. Silberstein, S. and Gilmore, R. (1996) Biochemistry, molecular biology, and genetics of the oligosaccharyltransferase. FASEB J. 10, 849–858.
46. Snowden, C.J., Leborgne-Castel, N., Wootton, L.J., Hadlington, J.L. and Denecke, J. (2007) In vivo analysis of the lumenal binding protein (BiP) reveals multiple functions of its ATPase domain. Plant J. 52, 987–1000.
47. Stanley, P. (2016) What have we learned from glycosyltransferase knockouts in mice? J. Mol. Biol. 428, 3166–3182.
48. Strasser, R. (2016) Plant protein glycosylation. Glycobiology, 26, 926–939.
49. Van Leene, J., Witters, E., Inze, D. and De Jaeger, G. (2008) Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci. 13, 517–520.
50. Walter, P., Gilmore, R., Muller, M. and Blobel, G. (1982) The protein translocation machinery of the endoplasmic reticulum. Philos. Trans. R. Soc. Lond. B Biol. Sci. 300, 225–228.
51. Wilson, C.M. and High, S. (2007) Ribophorin I acts as a substrate-specific facilitator of N-glycosylation. J. Cell Sci. 120, 648–657.
52. Zhang, Q., Sun, T. and Zhang, Y. (2015) ER quality control components UGGT and STT3a are required for activation of defense responses in bir1-1. PLoS ONE, 10, e0120245.