Mammalian cells lacking either the cotranslational or posttranslocational oligosaccharyltransferase complex display substrate-dependent defects in asparagine linked glycosylation

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Cherepanova, Natalia A ^a   Gilmore, Reid ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; CATION TRANSPORT PROTEIN; GLYCOSYLTRANSFERASE; MAGT1 PROTEIN, HUMAN; MEMBRANE PROTEIN; N33 PROTEIN, HUMAN; STT3A PROTEIN, HUMAN; STT3B PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL; CELL LINE; CHEMISTRY; CRISPR CAS SYSTEM; DEFICIENCY; ENZYME SPECIFICITY; GENETIC ENGINEERING; GENETIC TRANSFECTION; GENETICS; GLYCOSYLATION; HEK293 CELL LINE; HELA CELL LINE; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; PLASMID; PROTEIN PROCESSING; PROTEIN SYNTHESIS;

ANIMALS; ASPARAGINE; BASE SEQUENCE; CATION TRANSPORT PROTEINS; CELL LINE; CRISPR-CAS SYSTEMS; GENETIC ENGINEERING; GLYCOSYLATION; HEK293 CELLS; HELA CELLS; HEXOSYLTRANSFERASES; HUMANS; MEMBRANE PROTEINS; PLASMIDS; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SUBSTRATE SPECIFICITY; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84959259856     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20946     Document Type: Article

References (43)

1. Aebi, M. N-linked protein glycosylation in the ER. Biochim. Biophys. Acta 1833, 2430-2437 (2013).
2. Zielinska, D. F., Gnad, F., Wisniewski, J. R. & Mann, M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907 (2010).
3. Shrimal, S., Cherepanova, N. A. & Gilmore, R. Cotranslational and posttranslocational N-glycosylation of proteins in the endoplasmic reticulum. Semin. Cell Dev. Biol. 41, 71-78 (2015).
4. Kelleher, D. J., Karaoglu, D., Mandon, E. C. & Gilmore, R. Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol. Cell 12, 101-111 (2003).
5. Cherepanova, N. A., Shrimal, S. & Gilmore, R. Oxidoreductase activity is necessary for N-glycosylation of cysteine-proximal acceptor sites in glycoproteins. J. Cell Biol. 206, 525-539 (2014).
6. Shibatani, T., David, L. L., McCormack, A. L., Frueh, K. & Skach, W. R. Proteomic analysis of mammalian oligosaccharyltransferase reveals multiple subcomplexes that contain Sec61, TRAP, and two potential new subunits. Biochemistry 44, 5982-5992 (2005).
7. Roboti, P. & High, S. Keratinocyte-associated protein 2 is a bona fide subunit of the mammalian oligosaccharyltransferase. J. Cell Sci. 125, 220-232 (2012).
8. Roboti, P. & High, S. The oligosaccharyltransferase subunits OST48, DAD1 and KCP2 function as ubiquitous and selective modulators of mammalian N-glycosylation. J. Cell Sci. 125, 3474-3484 (2012).
9. Conti, B. J., Devaraneni, P. K., Yang, Z., David, L. L. & Skach, W. R. Cotranslational stabilization of Sec62/63 within the ER Sec61 translocon is controlled by distinct substrate-driven translocation events. Mol Cell 58, 269-83 (2015).
10. Nilsson, I. et al. Photocross-linking of nascent chains to the STT3 subunit of the oligosaccharyltransferase complex. J. Cell Biol. 161, 715-725 (2003).
11. Ruiz-Canada, C., Kelleher, D. J. & Gilmore, R. Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms. Cell 136, 272-283 (2009).
12. Shrimal, S., Ng, B. G., Losfeld, M. E., Gilmore, R. & Freeze, H. H. Mutations in STT3A and STT3B cause two congenital disorders of glycosylation. Hum. Mol. Genet. 22, 4638-4645 (2013).
13. Kelleher, D. J. & Gilmore, R. An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16, 47-62 (2006).
14. Karaoglu, D., Kelleher, D. J. & Gilmore, R. 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 (1997).
15. Knauer, R. & Lehle, L. The oligosaccharyltransferase complex from Saccharomyces cerevisiae. Isolation of the OST6 gene, its synthetic interaction with OST3, and analysis of the native complex. J. Biol. Chem. 274, 17249-17256. (1999).
16. Spirig, U., Bodmer, D., Wacker, M., Burda, P. & Aebi, M. The 3.4 kDa Ost4 protein is required for the assembly of two distinct oligosaccharyltransferase complexes in yeast. Glycobiology 15, 1396-1406 (2005).
17. Schulz, B. L. et al. Oxidoreductase activity of oligosaccharyltransferase subunits Ost3p and Ost6p defines site-specific glycosylation efficiency. Proc. Natl. Acad. Sci. USA 106, 11061-11066 (2009).
18. Mohorko, E. et al. Structural basis of substrate specificity of human oligosaccharyl transferase subunit N33/Tusc3 and its role in regulating protein N-glycosylation. Structure 22, 590-601 (2014).
19. Li, F. Y. et al. Second messenger role for Mg2+ revealed by human T-cell immunodeficiency. Nature 475, 471-476 (2011).
20. Piton, A., Redin, C. & Mandel, J. L. XLID-causing mutations and associated genes challenged in light of data from large-scale human exome sequencing. Am. J. Hum. Genet. 93, 368-383 (2013).
21. Molinari, F. et al. Oligosaccharyltransferase-subunit mutations in nonsyndromic mental retardation. Am. J. Hum. Genet. 82, 1150-1157 (2008).
22. Garshasbi, M. et al. A defect in the TUSC3 gene is associated with autosomal recessive mental retardation. Am. J. Hum. Genet. 82, 1158-1164 (2008).
23. Garshasbi, M. et al. A novel nonsense mutation in TUSC3 is responsible for non-syndromic autosomal recessive mental retardation in a consanguineous Iranian family. Am. J. Med. Genet. A. 155A, 1976-1980 (2011).
24. Shrimal, S., Trueman, S. F. & Gilmore, R. Extreme C-terminal sites are posttranslocationally glycosylated by the STT3B isoform of the OST. J. Cell Biol. 201, 81-95 (2013).
25. Shrimal, S. & Gilmore, R. Glycosylation of closely spaced acceptor sites in human glycoproteins. J. Cell Sci. 126, 5513-5523 (2013).
26. Malaby, H. L. & Kobertz, W. R. The middle x residue influences cotranslational N-glycosylation consensus site skipping. Biochemistry 53, 4884-4893 (2014).
27. Shrimal, S. & Gilmore, R. Reduced expression of the oligosaccharyltransferase exacerbates protein hypoglycosylation in cells lacking the fully assembled oligosaccharide donor. Glycobiology 25, 774-783 (2015).
28. Tsao, Y. S., Ivessa, N. E., Adesnik, M., Sabatini, D. D. & Kreibich, G. Carboxy terminally truncated forms of ribophorin I are degraded in pre-Golgi compartments by a calcium-dependent process. J. Cell Biol. 116, 57-67 (1992).
29. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-23 (2013).
30. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-6 (2013).
31. Zhang, F., Wen, Y. & Guo, X. CRISPR/Cas9 for genome editing: progress, implications and challenges. Hum Mol Genet 23, R40-6 (2014).
32. Zhou, H. & Clapham, D. E. Mammalian MagT1 and TUSC3 are required for cellular magnesium uptake and vertebrate embryonic development. Proc. Natl. Acad. Sci. USA 106, 15750-15755 (2009).
33. Lin, Y. C. et al. Genome dynamics of the human embryonic kidney 293 lineage in response to cell biology manipulations. Nat. Commun. 5, 4767 (2014).
34. Canver, M. C. et al. Characterization of genomic deletion efficiency mediated by clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 nuclease system in mammalian cells. J Biol Chem 289, 21312-24 (2014).
35. Fu, Y. et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31, 822-6 (2013).
36. Schroder, M. & Kaufman, R. J. ER stress and the unfolded protein response. Mutat. Res. 569, 29-63 (2005).
37. Bocchinfuso, W. P., Ma, K. L., Lee, W. M., Warmels-Rodenhiser, S. & Hammond, G. L. Selective removal of glycosylation sites from sex hormone-binding globulin by site-directed mutagenesis. Endocrinology 131, 2331-2336 (1992).
38. Bause, E. Model studies on N-glycosylation of proteins. Biochem. Soc. Trans. 12, 514-517 (1984).
39. Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013).
40. Hsu, P. D. et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832 (2013).
41. Yu, Y., Sabatini, D. D. & Kreibich, G. Antiribophorin antibodies inhibit the targeting to the ER membrane of ribosomes containing secretory polypeptides. J. Cell Biol. 111, 1335-1342 (1990).
42. Kelleher, D. J. & Gilmore, R. DAD1, the defender against apoptotic cell death, is a subunit of the mammalian oligosaccharyltransferase. Proc. Natl. Acad. Sci. USA 94, 4994-4999 (1997).
43. Song, W., Raden, D., Mandon, E. C. & Gilmore, R. Role of Sec61alpha in the regulated transfer of the ribosome-nascent chain complex from the signal recognition particle to the translocation channel. Cell 100, 333-343 (2000).