Artículo

El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Proteins may adopt diverse conformations during their folding in vivo, ranging from extended chains when they emerge from the ribosome to compact intermediates near the end of the folding process. Accordingly, a variety of chaperones and folding assisting enzymes have evolved to deal with this diversity. Chaperone selection by a particular substrate depends on the structural features of its folding intermediates. In addition, this process may be modulated by competitive effects between chaperones. Here we address this issue by using TcrCATL as model substrate. TcrCATL is an abundant Trypanosoma cruzi lysosomal protease and it was the first identified endogenous UDP-Glc:glycoprotein glucosyltransferase (UGGT) substrate. We found that TcrCATL associated sequentially with BiP and calreticulin (CRT) during its folding process. Early, extended conformations were bound to BiP, while more advanced and compact folding intermediates associated to CRT. The interaction between TcrCATL and CRT was impeded by deletion of the UGGT-encoding gene but, similarly to what was observed in wild type cells, in mutant cells TcrCATL associated to BiP only when displaying extended conformations. The absence of TcrCATL-CRT interactions in UGGT null cells resulted in a drastic reduction of TcrCATL folding efficiency and triggered the aggregation of TcrCATL through intermolecular disulfide bonds. These observations show that BiP and CRT activities complement each other to supervise a complete and efficient TcrCATL folding process. The present report provides further evidence on the early evolutionary acquisition of the basic tenets of the N-glycan dependent quality control mechanism of glycoprotein folding. © 2010 Elsevier B.V. All rights reserved.

Registro:

Documento: Artículo
Título:Functional cooperation between BiP and calreticulin in the folding maturation of a glycoprotein in Trypanosoma cruzi
Autor:Labriola, C.A.; Giraldo, A.M.V.; Parodi, A.J.; Caramelo, J.J.
Filiación:Laboratories of Glycobiology, Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires (IIBBA-CONICET), Avenida Patricias Argentinas 435, C1405BWE Buenos Aires, Argentina
Structural Cell Biology Laboratory, Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires (IIBBA-CONICET), Avenida Patricias Argentinas 435, C1405BWE Buenos Aires, Argentina
Department of Biological Chemistry, School of Sciences, University of Buenos Aires, 1428 Buenos Aires, Argentina
Palabras clave:BiP; Calreticulin; Glycoprotein folding quality control; Trypanosome cruzi; calreticulin; glucose regulated protein 78; glycoprotein; proteinase; unclassified drug; uridine diphosphate glc:glycoprotein glucosyltransferase; article; lysosome; molecular interaction; mutant; nonhuman; priority journal; protein conformation; protein folding; Trypanosoma cruzi; Calreticulin; Cysteine Endopeptidases; HSP70 Heat-Shock Proteins; Models, Biological; Models, Chemical; Protein Folding; Protozoan Proteins; Trypanosoma cruzi; Trypanosoma cruzi
Año:2011
Volumen:175
Número:2
Página de inicio:112
Página de fin:117
DOI: http://dx.doi.org/10.1016/j.molbiopara.2010.10.002
Título revista:Molecular and Biochemical Parasitology
Título revista abreviado:Mol. Biochem. Parasitol.
ISSN:01666851
CODEN:MBIPD
CAS:proteinase, 9001-92-7; Calreticulin; Cysteine Endopeptidases, 3.4.22.-; HSP70 Heat-Shock Proteins; Protozoan Proteins; cruzain, Trypanosoma cruzi, 3.4.22.-
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01666851_v175_n2_p112_Labriola

Referencias:

  • Gragerov, A., Nudler, E., Komissarova, N., Gaitanaris, G.A., Gottesman, M.E., Nikiforov, V., Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli (1992) Proc Natl Acad Sci USA, 89 (21), pp. 10341-10344
  • Gaitanaris, G.A., Vysokanov, A., Hung, S.C., Gottesman, M.E., Gragerov, A., Successive action of Escherichia coli chaperones in vivo (1994) Mol Microbiol, 14 (5), pp. 861-869
  • Naylor, D.J., Hartl, F.U., Contribution of molecular chaperones to protein folding in the cytoplasm of prokaryotic and eukaryotic cells (2001) Biochem Soc Symp, 68, pp. 45-68
  • Michalak, M., Corbett, E.F., Mesaeli, N., Nakamura, K., Opas, M., Calreticulin: One protein, one gene, many functions (1999) Biochem J, 344 (PART 2), pp. 281-292
  • Caramelo, J.J., Parodi, A.J., Getting in and out from calnexin/calreticulin cycles (2008) J Biol Chem, 283, pp. 10221-10225
  • Jessop, C.E., Tavender, T.J., Watkins, R.H., Chambers, J.E., Bulleid, N.J., Substrate specificity of the oxidoreductase ERp57 is determined primarily by its interaction with calnexin and calreticulin (2009) J Biol Chem, 284, pp. 2194-2202
  • Hammond, C., Braakman, I., Helenius, A., Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control (1994) Proc Natl Acad Sci USA, 91, pp. 913-917
  • Caramelo, J.J., Castro, O.A., Alonso, L.G., De Prat-Gay, G., Parodi, A.J., UDP-Glc:glycoprotein glucosyltransferase recognizes structured and solvent accessible hydrophobic patches in molten globule-like folding intermediates (2003) Proc Natl Acad Sci USA, 100, pp. 86-91
  • Caramelo, J.J., Castro, O.A., De Prat-Gay, G., Parodi, A.J., The endoplasmic reticulum glucosyltransferase recognizes nearly native glycoprotein folding intermediates (2004) J Biol Chem, 279, pp. 46280-46285
  • Ritter, C., Helenius, A., Recognition of local glycoprotein misfolding by the ER folding sensor UDP-glucose:glycoprotein glucosyltransferase (2000) Nat Struct Biol, 7, pp. 278-280
  • Ritter, C., Quirin, K., Kowarik, M., Helenius, A., Minor folding defects trigger local modification of glycoproteins by the ER folding sensor GT (2005) EMBO J, 24, pp. 1730-1738
  • Keith, N., Parodi, A.J., Caramelo, J.J., Glycoprotein tertiary and quaternary structures are monitored by the same quality control mechanism (2005) J Biol Chem, 280, pp. 18138-18141
  • Misselwitz, B., Staeck, O., Rapoport, T.A., J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences (1998) Mol Cell, 2, pp. 593-603
  • Hammond, C., Helenius, A., Folding of VSV G protein: Sequential interaction with BiP and calnexin (1994) Science, 266, pp. 456-458
  • Kim, P.S., Arvan, P., Calnexin and BiP act as sequential molecular chaperones during thyroglobulin folding in the endoplasmic reticulum (1995) J Cell Biol, 128, pp. 29-38
  • Melnick, J., Dul, J.L., Argon, Y., Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum (1994) Nature, 370, pp. 373-375
  • Molinari, M., Helenius, A., Chaperone selection during glycoprotein translocation into the endoplasmic reticulum (2000) Science, 288, pp. 331-333
  • Parodi, A.J., Lederkremer, G.Z., Mendelzon, D.H., Protein glycosylation in Trypanosoma cruzi. the mechanism of glycosylation and structure of protein-bound oligosaccharides (1983) J Biol Chem, 258, pp. 5589-5595
  • Bosch, M., Trombetta, S., Engstrom, U., Parodi, A.J., Characterization of dolichol diphosphate oligosaccharide:protein oligosaccharyltransferase and of glycoprotein processing glucosidases occurring in trypanosomatids (1988) J Biol Chem, 263, pp. 17360-17365
  • Conte, I., Labriola, C., Cazzulo, J.J., Docampo, R., Parodi, A.J., The interplay between folding-facilitating mechanisms in Trypanosoma cruzi endoplasmic reticulum (2003) Mol Biol Cell, 14, pp. 3529-3540
  • Labriola, C., Cazzulo, J.J., Parodi, A.J., Trypanosoma cruzi calreticulin is a lectin that binds monoglucosylated oligosaccharides but not protein moieties of glycoproteins (1999) Mol Biol Cell, 10, pp. 1381-1394
  • Izquierdo, L., Atrih, A., Rodrigues, J.A., Jones, D.C., Ferguson, M.A.J., Trypanosoma brucei UDP-Glc:glycoprotein glucosyltransferase has unusual substrate specificity and protects the parasite from stress (2009) Eukaryot Cell, 8, pp. 230-240
  • Banerjee, S., Vishwanath, P., Cui, J., The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation (2007) Proc Natl Acad Sci USA, 104, pp. 11676-11681
  • Parodi, A.J., Quesada-Allué, L.A., Protein glycosylation in Trypanosoma cruzi. I. Characterization of dolichol-bound monosaccharides and oligosaccharides synthesized in vivo (1982) J Biol Chem, 257, pp. 7637-7640
  • Parodi, A.J., N-glycosylation in trypanosomatid protozoa (1993) Glycobiology, 3, pp. 193-199
  • Caffrey, C.R., Steverding, D., Kinetoplastid papain-like cysteine peptidases (2009) Mol Biochem Parasitol, 167, pp. 12-19
  • Bangs, J.D., Uyetake, J., Brickman, M.J., Balber, A.E., Boothroyd, J.C., Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei. Divergent ER retention signals in a lower eukaryote (1993) J Cell Sci, 105, pp. 1101-1113
  • Cazzulo, J.J., Franke De Cazzulo, B.M., Engel, J.C., Cannata, J.J., End products and enzyme levels of aerobic glucose fermentation in trypanosomatids (1985) Mol Biochem Parasitol, 16, pp. 329-343
  • Labriola, C., Cazzulo, J.J., Parodi, A.J., Retention of glucose units added by the UDP-Glc:glycoprotein glucosyltransferase delays exit of glycoproteins from the endoplasmic reticulum (1995) J Cell Biol, 130, pp. 771-779
  • Parodi, A.J., Labriola, C., Cazzulo, J.J., The presence of complex-type oligosaccharides at the C-terminal domain glycosylation site of some molecules of cruzipain (1995) Mol Biochem Parasitol, 69, pp. 247-255
  • Cazzulo, J.J., Martínez, J., Parodi, A.J.A., Wernstedt, C., Hellman, U., On the post-translational modifications at the C-terminal domain of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi (1992) FEMS Microbiol Lett, 100, pp. 411-416
  • Campetella, O., Henriksson, J., Aslund, L., Frasch, A.C.C., Petersson, U., Cazzulo, J.J., The major cysteine proteinase (cruzipain) from Trypanosome cruzi is encoded by multiple polymorphic tandemly organized genes locates on different chromosomes (1992) Mol Biol Parasitol, 50, pp. 225-234
  • Martínez, J., Cazzulo, J.J., Anomalous electrophoretic behaviour of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi in relation to its apparent molecular mass (1992) FEMS Microbiol Lett, 95, pp. 225-230
  • Francis, E., Daniels, R., Hebert, D.N., Analysis of protein folding and oxidation in the endoplasmic reticulum (2002) Curr Protoc Cell Biol
  • Pearse, B.R., Gabriel, L., Wang, N., Hebert, D.N., A cell-based reglucosylation assay demonstrates the role of GT1 in the quality control of a maturing glycoprotein (2008) J Cell Biol, 181, pp. 309-320
  • Pearse, B.R., Tamura, T., Sunryd, C.J., Grabowski, G.A., Kaufman, R.J., Hebert, D.N., The role of UDP-Glc:glycoprotein glucosyltransferase 1 in the maturation of an obligate substrate prosaposin (2010) J Cell Biol, 189, pp. 829-841
  • Field, M.C., Sergeenko, T., Wang, Y.N., Böhm, S., Carrington, M., Chaperone requirements for biosynthesis of the trypanosome variant surface glycoprotein (2010) PLoS One, 5 (1), p. 8468

Citas:

---------- APA ----------
Labriola, C.A., Giraldo, A.M.V., Parodi, A.J. & Caramelo, J.J. (2011) . Functional cooperation between BiP and calreticulin in the folding maturation of a glycoprotein in Trypanosoma cruzi. Molecular and Biochemical Parasitology, 175(2), 112-117.
http://dx.doi.org/10.1016/j.molbiopara.2010.10.002
---------- CHICAGO ----------
Labriola, C.A., Giraldo, A.M.V., Parodi, A.J., Caramelo, J.J. "Functional cooperation between BiP and calreticulin in the folding maturation of a glycoprotein in Trypanosoma cruzi" . Molecular and Biochemical Parasitology 175, no. 2 (2011) : 112-117.
http://dx.doi.org/10.1016/j.molbiopara.2010.10.002
---------- MLA ----------
Labriola, C.A., Giraldo, A.M.V., Parodi, A.J., Caramelo, J.J. "Functional cooperation between BiP and calreticulin in the folding maturation of a glycoprotein in Trypanosoma cruzi" . Molecular and Biochemical Parasitology, vol. 175, no. 2, 2011, pp. 112-117.
http://dx.doi.org/10.1016/j.molbiopara.2010.10.002
---------- VANCOUVER ----------
Labriola, C.A., Giraldo, A.M.V., Parodi, A.J., Caramelo, J.J. Functional cooperation between BiP and calreticulin in the folding maturation of a glycoprotein in Trypanosoma cruzi. Mol. Biochem. Parasitol. 2011;175(2):112-117.
http://dx.doi.org/10.1016/j.molbiopara.2010.10.002