Artículo

Medus, M.L.; Gomez, G.E.; Zacchi, L.F.; Couto, P.M.; Labriola, C.A.; Labanda, M.S.; Bielsa, R.C.; Clérico, E.M.; Schulz, B.L.; Caramelo, J.J. "N-glycosylation Triggers a Dual Selection Pressure in Eukaryotic Secretory Proteins" (2017) Scientific Reports. 7(1)
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Nearly one third of the eukaryotic proteome traverses the secretory pathway and most of these proteins are N-glycosylated in the lumen of the endoplasmic reticulum. N-glycans fulfill multiple structural and biological functions, and are crucial for productive folding of many glycoproteins. N-glycosylation involves the attachment of an oligosaccharide to selected asparagine residues in the sequence N-X-S/T (X P), a motif known as an N-glycosylation'sequon'. Mutations that create novel sequons can cause disease due to the destabilizing effect of a bulky N-glycan. Thus, an analogous process must have occurred during evolution, whenever ancestrally cytosolic proteins were recruited to the secretory pathway. Here, we show that during evolution N-glycosylation triggered a dual selection pressure on secretory pathway proteins: while sequons were positively selected in solvent exposed regions, they were almost completely eliminated from buried sites. This process is one of the sharpest evolutionary signatures of secretory pathway proteins, and was therefore critical for the evolution of an efficient secretory pathway. © 2017 The Author(s).

Registro:

Documento: Artículo
Título:N-glycosylation Triggers a Dual Selection Pressure in Eukaryotic Secretory Proteins
Autor:Medus, M.L.; Gomez, G.E.; Zacchi, L.F.; Couto, P.M.; Labriola, C.A.; Labanda, M.S.; Bielsa, R.C.; Clérico, E.M.; Schulz, B.L.; Caramelo, J.J.
Filiación:Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires (IIBBA-CONICET), Buenos Aires, 1405, Argentina
Universidad de Buenos Aires. CONICET. Facultad de Farmacia y Bioquímica, Departamento de Química Biológica, Instituto de Química y Fisicoquímica Biológicas (IQUIFIB), Buenos Aires, 1113, Argentina
School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, QLD 4072, Australia
Department of Biochemistry and Molecular Biology, Life Sciences Laboratories, University of Massachusetts, Amherst, MA 01003, United States
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Química Biológica, Buenos Aires, 1428, Argentina
ARC Training Centre for Biopharmaceutical Innovation, University of Queensland, St. Lucia, QLD 4072, Australia
Palabras clave:glycoprotein; membrane protein; protein binding; animal; biology; chemistry; Chlorocebus aethiops; CV-1 cell line; endoplasmic reticulum; eukaryotic cell; genetic disorder; genetic selection; genetics; glycosylation; human; metabolism; molecular model; procedures; protein conformation; Animals; Cercopithecus aethiops; Computational Biology; COS Cells; Endoplasmic Reticulum; Eukaryotic Cells; Genetic Diseases, Inborn; Glycoproteins; Glycosylation; Humans; Membrane Proteins; Models, Molecular; Protein Binding; Protein Conformation; Selection, Genetic
Año:2017
Volumen:7
Número:1
DOI: http://dx.doi.org/10.1038/s41598-017-09173-6
Título revista:Scientific Reports
Título revista abreviado:Sci. Rep.
ISSN:20452322
CAS:Glycoproteins; Membrane Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_20452322_v7_n1_p_Medus

Referencias:

  • Braakman, I., Hebert, D.N., Protein folding in the endoplasmic reticulum (2013) Cold Spring Harb. Perspect. Biol, 5, p. a013201
  • Caramelo, J.J., Parodi, A.J., A sweet code for glycoprotein folding (2015) FEBS Lett, 589, pp. 3379-3387
  • Hebert, D.N., Lamriben, L., Powers, E.T., Kelly, J.W., The intrinsic and extrinsic effects of n-linked glycans on glycoproteostasis (2014) Nat. Chem. Biol, 10, pp. 902-910
  • Imperiali, B., O'Connor, S.E., Effect of n-linked glycosylation on glycopeptide and glycoprotein structure (1999) Curr. Opin. Chem. Biol, 3, pp. 643-649
  • Mitra, N., Sinha, S., Ramya, T.N., Surolia, A., N-linked oligosaccharides as outfitters for glycoprotein folding, form and function (2006) Trends Biochem. Sci, 31, pp. 156-163
  • Shental-Bechor, D., Levy, Y., Folding of glycoproteins: Toward understanding the biophysics of the glycosylation code (2009) Curr. Opin. Struct. Biol, 19, pp. 524-533
  • Hebert, D.N., Molinari, M., Flagging and docking: Dual roles for n-glycans in protein quality control and cellular proteostasis (2012) Trends Biochem. Sci, 37, pp. 404-410
  • Shrimal, S., Cherepanova, N.A., Gilmore, R., Cotranslational and posttranslocational n-glycosylation of proteins in the endoplasmic reticulum (2015) Sem. Cell Dev. Biol, 41, pp. 71-78
  • Williams, R., Encoding asymmetry of the n-glycosylation motif facilitates glycoprotein evolution (2014) Plos ONE, 9, p. e86088
  • Kelleher, D.J., Gilmore, R., An evolving view of the eukaryotic oligosaccharyltransferase (2006) Glycobiology, 16, pp. 47R-62R
  • Mohorko, E., Glockshuber, R., Aebi, M., Oligosaccharyltransferase: The central enzyme of n-linked protein glycosylation (2011) J. Inherit. Metab. Dis, 34, pp. 869-878
  • Vogt, G., Gains of glycosylation comprise an unexpectedly large group of pathogenic mutations (2005) Nature Gen, 37, pp. 692-700
  • Lin, S.W., Lin, S.R., Shen, M.C., Characterization of genetic defects of hemophilia a in patients of Chinese origin (1993) Genomics, 18, pp. 496-504
  • Bunge, S., Identification of 31 novel mutations in the n-Acetylgalactosamine-6-sulfatase gene reveals excessive allelic heterogeneity among patients with morquio a syndrome (1997) Hum. Mutat, 10, pp. 223-232
  • Cui, J., Smith, T., Robbins, P.W., Samuelson, J., Darwinian selection for sites of asn-linked glycosylation in phylogenetically disparate eukaryotes and viruses (2009) Proc. Natl. Acad. Sci. USA, 106, pp. 13421-13426
  • Apweiler, R., Hermjakob, H., Sharon, N., On the frequency of protein glycosylation, as deduced from analysis of the swiss-prot database (1999) Bioch. Biophys. Acta, 1473, pp. 4-8
  • Zacchi, L.F., Schulz, B.L., N-glycoprotein macroheterogeneity: Biological implications and proteomic characterization (2016) Glycoconj. J, 33, pp. 359-376
  • Schulz, B.L., (2012) Beyond the Sequon: Sites of N-Glycosylation, , InTech
  • Schulz, B.L., Aebi, M., Analysis of glycosylation site occupancy reveals a role for ost3p and ost6p in site-specific n-glycosylation efficiency (2009) Mol. Cell. Prot, 8, pp. 357-364
  • Schulz, B.L., Oxidoreductase activity of oligosaccharyltransferase subunits ost3p and ost6p defines site-specific glycosylation efficiency (2009) Proc. Natl. Acad. Sci. USA, 106, pp. 11061-11066
  • Shrimal, S., Trueman, S.F., Gilmore, R., Extreme c-terminal sites are posttranslocationally glycosylated by the stt3b isoform of the ost (2013) J. Cell Biol, 201, pp. 81-95
  • Kasturi, L., Eshleman, J.R., Wunner, W.H., Shakin-Eshleman, S.H., The hydroxy amino acid in an asn-x-ser/thr sequon can influence n-linked core glycosylation efficiency and the level of expression of a cell surface glycoprotein (1995) J. Biol. Chem, 270, pp. 14756-14761
  • Shakin-Eshleman, S.H., Spitalnik, S.L., Kasturi, L., The amino acid at the x position of an asn-x-ser sequon is an important determinant of n-linked core-glycosylation efficiency (1996) J. Biol. Chem, 271, pp. 6363-6366
  • Mellquist, J.L., Kasturi, L., Spitalnik, S.L., Shakin-Eshleman, S.H., The amino acid following an asn-x-ser/thr sequon is an important determinant of n-linked core glycosylation efficiency (1998) Biochemistry, 37, pp. 6833-6837
  • Petrescu, A.J., Milac, A.L., Petrescu, S.M., Dwek, R.A., Wormald, M.R., Statistical analysis of the protein environment of nglycosylation sites: Implications for occupancy, structure, and folding (2004) Glycobiology, 14, pp. 103-114
  • Holst, B., Bruun, A.W., Kielland-Brandt, M.C., Winther, J.R., Competition between folding and glycosylation in the endoplasmic reticulum (1996) EMBO J, 15, pp. 3538-3546
  • Losfeld, M.E., Soncin, F., Ng, B.G., Singec, I., Freeze, H.H., A sensitive green fluorescent protein biomarker of n-glycosylation site occupancy (2012) FASEB J, 26, pp. 4210-4217
  • Benyair, R., Ogen-Shtern, N., Lederkremer, G.Z., Glycan regulation of er-Associated degradation through compartmentalization (2015) Semin. Cell Dev. Biol, 41, pp. 99-109
  • Park, C., Zhang, J., Genome-wide evolutionary conservation of n-glycosylation sites (2011) Mol. Biol. Evol, 28, pp. 2351-2357
  • Sato, T., Stt3b-dependent posttranslational n-glycosylation as a surveillance system for secretory protein (2012) Mol. Cell, 47, pp. 99-110
  • Carrington, D.M., Auffret, A., Hanke, D.E., Polypeptide ligation occurs during post-translational modification of concanavalin a (1985) Nature, 313, pp. 64-67
  • Kityk, R., Kopp, J., Sinning, I., Mayer, M.P., Structure and dynamics of the atp-bound open conformation of hsp70 chaperones (2012) Mol. Cell, 48, pp. 863-874
  • Gidalevitz, T., Stevens, F., Argon, Y., Orchestration of secretory protein folding by er chaperones (2013) Bioch. Biophys. Acta, 1833, pp. 2410-2424
  • Vembar, S.S., Jonikas, M.C., Hendershot, L.M., Weissman, J.S., Brodsky, J.L., J domain co-chaperone specificity defines the role of bip during protein translocation (2010) J. Biol. Chem, 285, pp. 22484-22494
  • Gardner, B.M., Pincus, D., Gotthardt, K., Gallagher, C.M., Walter, P., Endoplasmic reticulum stress sensing in the unfolded protein response (2013) Cold Spring Harbor Persp. Biol, 5, p. a013169
  • Bushkin, G.G., Suggestive evidence for darwinian selection against asparagine-linked glycans of plasmodium falciparum and toxoplasma gondii (2010) Eukaryotic Cell, 9, pp. 228-241
  • Murray, P.J., Watowich, S.S., Lodish, H.F., Young, R.A., Hilton, D.J., Epitope tagging of the human endoplasmic reticulum hsp70 protein, bip, to facilitate analysis of bip-substrate interactions (1995) Analytical Bioch, 229, pp. 170-179
  • Kimata, Y., Genetic evidence for a role of bip/kar2 that regulates ire1 in response to accumulation of unfolded proteins (2003) Mol. Biol. Cell, 14, pp. 2559-2569
  • Yang, J., Nune, M., Zong, Y., Zhou, L., Liu, Q., Close and allosteric opening of the polypeptide-binding site in a human hsp70 chaperone bip (2015) Structure, 23, pp. 2191-2203
  • Emanuelsson, O., Brunak, S., Von Heijne, G., Nielsen, H., Locating proteins in the cell using targetp signalp and related tools (2007) Nature Prot, 2, pp. 953-971
  • Pettersen, E.F., Ucsf chimera-A visualization system for exploratory research and analysis (2004) J. Comp. Chem, 25, pp. 1605-1612
  • Sali, A., Blundell, T.L., Comparative protein modelling by satisfaction of spatial restraints (1993) J. Mol. Biol, 234, pp. 779-815
  • Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., Pease, L.R., Site-directed mutagenesis by overlap extension using the polymerase chain reaction (1989) Gene, 77, pp. 51-59
  • Donoso, G., Herzog, V., Schmitz, A., Misfolded bip is degraded by a proteasome-independent endoplasmic-reticulum-Associated degradation pathway (2005) Biochem. J, 387, pp. 897-903
  • Wang, J., Pareja, K.A., Kaiser, C.A., Sevier, C.S., Redox signaling via the molecular chaperone bip protects cells against endoplasmic reticulum-derived oxidative stress (2014) ELife, 3, p. e03496
  • Imai, Y., Matsushima, Y., Sugimura, T., Terada, M., A simple and rapid method for generating a deletion by PCR (1991) Nucl. Acids Res, 19, p. 2785
  • Zacchi, L.F., The bip molecular chaperone plays multiple roles during the biogenesis of torsina, an aaa+ atpase associated with the neurological disease early-onset torsion dystonia (2014) J. Biol. Chem, 289, pp. 12727-12747

Citas:

---------- APA ----------
Medus, M.L., Gomez, G.E., Zacchi, L.F., Couto, P.M., Labriola, C.A., Labanda, M.S., Bielsa, R.C.,..., Caramelo, J.J. (2017) . N-glycosylation Triggers a Dual Selection Pressure in Eukaryotic Secretory Proteins. Scientific Reports, 7(1).
http://dx.doi.org/10.1038/s41598-017-09173-6
---------- CHICAGO ----------
Medus, M.L., Gomez, G.E., Zacchi, L.F., Couto, P.M., Labriola, C.A., Labanda, M.S., et al. "N-glycosylation Triggers a Dual Selection Pressure in Eukaryotic Secretory Proteins" . Scientific Reports 7, no. 1 (2017).
http://dx.doi.org/10.1038/s41598-017-09173-6
---------- MLA ----------
Medus, M.L., Gomez, G.E., Zacchi, L.F., Couto, P.M., Labriola, C.A., Labanda, M.S., et al. "N-glycosylation Triggers a Dual Selection Pressure in Eukaryotic Secretory Proteins" . Scientific Reports, vol. 7, no. 1, 2017.
http://dx.doi.org/10.1038/s41598-017-09173-6
---------- VANCOUVER ----------
Medus, M.L., Gomez, G.E., Zacchi, L.F., Couto, P.M., Labriola, C.A., Labanda, M.S., et al. N-glycosylation Triggers a Dual Selection Pressure in Eukaryotic Secretory Proteins. Sci. Rep. 2017;7(1).
http://dx.doi.org/10.1038/s41598-017-09173-6