Artículo

Parente, J.; Casabuono, A.; Ferrari, M.C.; Paggi, R.A.; De Castro, R.E.; Couto, A.S.; Giménez, M.I. "A rhomboid protease gene deletion affects a novel oligosaccharide N-linked to the S-layer glycoprotein of Haloferax volcanii" (2014) Journal of Biological Chemistry. 289(16):11304-11317
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Abstract:

Background: Rhomboid proteases are ubiquitous, and their role in Archaea has not been explored. Results: We generated a rhomboid deletion mutant that displayed a glycosylation defect. Conclusion: Deletion of a rhomboid protease gene altered S-layer glycoprotein N-glycosylation. Significance: This work provides structural characterization of a novel oligosaccharide bound to H. volcanii S-layer glycoprotein and relates a rhomboid protease with the protein glycosylation process. © 2014 by The American Society for Biochemistry and Molecular Biology, Inc.

Registro:

Documento: Artículo
Título:A rhomboid protease gene deletion affects a novel oligosaccharide N-linked to the S-layer glycoprotein of Haloferax volcanii
Autor:Parente, J.; Casabuono, A.; Ferrari, M.C.; Paggi, R.A.; De Castro, R.E.; Couto, A.S.; Giménez, M.I.
Filiación:Centro de Investigación en Hidratos de Carbono, Departamento de Química Orgánica, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Investigaciones Biológicas, Universidad Nacional de Mar Del Plata-Consejo Nacional, Investigaciones Científicas y Técnicas, Funes 3250 4to nivel, 7600 Mar del Plata, Provincia de Buenos Aires, Argentina
Palabras clave:Esterification; Genes; Glycosylation; Oligosaccharides; Deletion mutants; Gene deletion; Haloferax volcanii; N-Glycosylation; N-linked; Protein glycosylation; S-layers; Structural characterization; Glycoproteins; glycoprotein; oligosaccharide; proteinase; RhoII protease; unclassified drug; article; bacterial gene; bacterial strain; bacterium mutant; carbohydrate analysis; controlled study; enzyme activity; gene deletion; Haloferax volcanii; high performance liquid chromatography; mass spectrometry; nonhuman; priority journal; protein glycosylation; RhoII gene; structure analysis; Archaea; Glycoprotein; Glycosylation; Halophiles; Mass Spectrometry (MS); Rhomboid Protease; Endopeptidases; Gene Knockdown Techniques; Glycosylation; Haloferax volcanii; Membrane Glycoproteins; Oligosaccharides
Año:2014
Volumen:289
Número:16
Página de inicio:11304
Página de fin:11317
DOI: http://dx.doi.org/10.1074/jbc.M113.546531
Título revista:Journal of Biological Chemistry
Título revista abreviado:J. Biol. Chem.
ISSN:00219258
CODEN:JBCHA
CAS:proteinase, 9001-92-7
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219258_v289_n16_p11304_Parente

Referencias:

  • Wolfe, M.S., Kopan, R., Intramembrane proteolysis: Theme and variations (2004) Science, 305, pp. 1119-1123
  • Urban, S., Making the cut: Central roles of intramembrane proteolysis in pathogenic microorganisms (2009) Nat. Rev. Microbiol., 7, pp. 411-423
  • Lee, J.R., Urban, S., Garvey, C.F., Freeman, M., Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila (2001) Cell, 107, pp. 161-171
  • Herlan, M., Vogel, F., Bornhovd, C., Neupert, W., Reichert, A.S., Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA (2003) J. Biol. Chem., 278, pp. 27781-27788
  • McQuibban, G.A., Sand, S., Mitochondrial membrane remodelling regulated by a conserved rhomboid protease (2003) Nature, 423, pp. 537-541. , Freeman, M
  • Baker, R.P., Wijetilaka, R., Urban, S., Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria (2006) PLoS Pathog., 2, pp. e113
  • Baxt, L.A., Baker, R.P., Singh, U., Urban, S., An Entamoeba histolytica rhomboid protease with atypical specificity cleaves a surface lectin involved in phagocytosis and immune evasion (2008) Genes Dev., 22, pp. 1636-1646
  • Stevenson, L.G., Strisovsky, K., Clemmer, K.M., Bhatt, S., Freeman, M., Rather, P.N., Rhomboid protease AarA mediates quorumsensing in Providencia stuartii by activating TatA of the twin-arginine translocase (2007) Proc. Natl. Acad. Sci. U.S.A., 104, pp. 1003-1008
  • Kateete, D.P., Katabazi, F.A., Okeng, A., Okee, M., Musinguzi, C., Asiimwe, B.B., Kyobe, S., Joloba, M.L., Rhomboids of Mycobacteria: Characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis (2012) PloS One, 7, pp. e45741
  • Maupin-Furlow, J.A., Gil, M.A., Humbard, M.A., Kirkland, P.A., Li, W., Reuter, C.J., Wright, A.J., Archaeal proteasomes and other regulatory proteases (2005) Curr. Opin. Microbiol., 8, pp. 720-728
  • Eichler, J., Adams, M.W., Posttranslational protein modification in Archaea (2005) Microbiol. Mol. Biol. Rev., 69, pp. 393-425
  • Jarrell, K.F., Jones, G.M., Nair, D.B., Biosynthesis and role of N-linked glycosylation in cell surface structures of archaea with a focus on flagella and s layers (2010) Int. J. Microbiol., 2010, p. 470138
  • Sumper, M., Berg, E., Mengele, R., Strobel, I., Primary structure and glycosylation of the S-layer protein of Haloferax volcanii (1990) J. Bacteriol., 172, pp. 7111-7118
  • Mengele, R., Sumper, M., Drastic differences in glycosylation of related S-layer glycoproteins from moderate and extreme halophiles (1992) J. Biol. Chem., 267, pp. 8182-8185
  • Abu-Qarn, M., Yurist-Doutsch, S., Giordano, A., Trauner, A., Morris, H.R., Hitchen, P., Medalia, O., Eichler, J., Haloferax volcanii AglB and AglD are involved in N-glycosylation of the S-layer glycoprotein and proper assembly of the surface layer (2007) J. Mol. Biol., 374, pp. 1224-1236
  • Magidovich, H., Yurist-Doutsch, S., Konrad, Z., Ventura, V.V., Dell, A., Hitchen, P.G., Eichler, J., AglP is a S-adenosyl-L-methioninedependent methyltransferase that participates in the N-glycosylation pathway of Haloferax volcanii (2010) Mol. Microbiol., 76, pp. 190-199
  • Calo, D., Kaminski, L., Eichler, J., Protein glycosylation in Archaea: Sweet and extreme (2010) Glycobiology, 20, pp. 1065-1076
  • Tripepi, M., You, J., Temel, S., Önder, O., Brisson, D., Pohlschröder, M., N-Glycosylation of Haloferax volcanii flagellins requires known Agl proteins and is essential for biosynthesis of stable flagella (2012) J. Bacteriol., 194, pp. 4876-4887
  • Guan, Z., Naparstek, S., Calo, D., Eichler, J., Protein glycosylation as an adaptive response in Archaea: Growth at different salt concentrations leads to alterations in Haloferax volcanii S-layer glycoprotein Nglycosylation (2012) Environ. Microbiol., 14, pp. 743-753
  • Kaminski, L., Guan, Z., Yurist-Doutsch, S., Eichler, J., Two distinct N-glycosylation pathways process the Haloferax volcanii S-layer glycoprotein upon changes in environmental salinity (2013) MBio, 4, pp. e00716-e00813
  • Paggi, R.A., Madrid, E.A., D'Alessandro, C.P., Cerletti, M., De Castro, R.E., Growth phase-dependent biosynthesis of Nep, a halolysin-like protease secreted by the alkaliphilic haloarchaeon Natrialba magadii (2010) Lett. Appl. Microbiol., 51, pp. 36-41
  • Sambrook, J., Russell, D.W., (2001) Molecular Cloning: A Laboratory Manual, , Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
  • Strisovsky, K., Sharpe, H.J., Freeman, M., Sequence-specific intramembrane proteolysis: Identification of a recognition motif in rhomboid substrates (2009) Mol. Cell, 36, pp. 1048-1059
  • Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature, 227, pp. 680-685
  • Dubray, G., Bezard, G., A highly sensitive periodic acid-silver stain for 1, 2-diol groups of glycoproteins and polysaccharides in polyacrylamide gels (1982) Anal. Biochem., 119, pp. 325-329
  • Allers, T., Ngo, H.P., Mevarech, M., Lloyd, R.G., Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes (2004) Appl. Environ. Microbiol., 70, pp. 943-953
  • Nieuwlandt, D.T., Palmer, J.R., Armbruster, D.T., Kuo, Y.P., Oda, W., Daniels, C.J., (1995) Archaea: A Laboratory Manual, pp. 161-162. , (Robb, F. T., Place, A. R., Sowers, K. R., Schreier, H. J., DasSarma, S., and Fleischmann, E. M., eds), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
  • Wong, M.L., Medrano, J.F., Real-time PCR for mRNA quantitation (2005) BioTechniques, 39, pp. 75-85
  • Selman, M.H., Hemayatkar, M., Deelder, A.M., Wuhrer, M., Cotton HILIC SPE microtips for microscale purification and enrichment of glycans and glycopeptides (2011) Anal. Chem., 83, pp. 2492-2499
  • Lemberg, M.K., Menendez, J., Misik, A., Garcia, M., Koth, C.M., Freeman, M., Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases (2005) EMBO J., 24, pp. 464-472
  • Lemieux, M.J., Fischer, S.J., Cherney, M.M., Bateman, K.S., James, M.N., The crystal structure of the rhomboid peptidase from Haemophilus influenzae provides insight into intramembrane proteolysis (2007) Proc. Natl. Acad. Sci. U.S.A., 104, pp. 750-754
  • Shlay, J.C., Bartsch, G., Peng, G., Wang, J., Grunfeld, C., Gibert, C.L., Visnegarwala, F., El-Sadr, W.M., Long-term body composition and metabolic changes in antiretroviral naive persons randomized to protease inhibitor-, nonnucleoside reverse transcriptase inhibitor-, or protease inhibitor plus nonnucleoside reverse transcriptase inhibitor-based strategy (2007) J. Acquir. Immune Defic. Syndr., 44, pp. 506-517
  • Baker, R.P., Urban, S., Architectural and thermodynamic principles underlying intramembrane protease function (2012) Nat. Chem. Biol., 8, pp. 759-768
  • Urban, S., Rhomboid proteins: Conserved membrane proteases with divergent biological functions (2006) Genes Dev., 20, pp. 3054-3068
  • Schultz, J., Milpetz, F., Bork, P., Ponting, C.P., SMART, a simple modular architecture research tool: Identification of signaling domains (1998) Proc. Natl. Acad. Sci. U.S.A., 95, pp. 5857-5864
  • Letunic, I., Doerks, T., Bork, P., SMART 6: Recent updates and new developments (2009) Nucleic Acids Res., 37, pp. D229-D232
  • Burroughs, A.M., Iyer, L.M., Aravind, L., Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system (2011) Mol. Biosyst., 7, pp. 2261-2277
  • Zhu, B.C., Drake, R.R., Schweingruber, H., Laine, R.A., Inhibition of glycosylation by amphomycin and sugar nucleotide analogs PP36 and PP55 indicates that Haloferax volcanii β-glucosylates both glycoproteins and glycolipids through lipid-linked sugar intermediates: Evidence for three novel glycoproteins and a novel sulfated dihexosyl-archaeol glycolipid (1995) Arch. Biochem. Biophys., 319, pp. 355-364
  • Konrad, Z., Eichler, J., Protein glycosylation in Haloferax volcanii: Partial characterization of a 98-kDa glycoprotein (2002) FEMS Microbiol. Lett., 209, pp. 197-202
  • Laity, J.H., Lee, B.M., Wright, P.E., Zinc finger proteins: New insights into structural and functional diversity (2001) Curr. Opin. Struct. Biol., 11, pp. 39-46
  • Palmieri, G., Balestrieri, M., Peter-Katalinić, J., Pohlentz, G., Rossi, M., Fiume, I., Pocsfalvi, G., Surface-exposed glycoproteins of hyperthermophilic Sulfolobus solfataricus P2 show a common N-glycosylation profile (2013) J. Proteome Res., 12, pp. 2779-2790
  • Wan, C., Fu, J., Wang, Y., Miao, S., Song, W., Wang, L., Exosome- related multi-pass transmembrane protein TSAP6 is a target of rhomboid protease RHBDD1-induced proteolysis (2012) PloS One, 7, pp. e37452
  • Meyer, B.H., Zolghadr, B., Peyfoon, E., Pabst, M., Panico, M., Morris, H.R., Haslam, S.M., Albers, S.V., Sulfoquinovose synthase: An important enzyme in the N-glycosylation pathway of Sulfolobus acidocaldarius (2011) Mol. Microbiol., 82, pp. 1150-1163
  • Kandiba, L., Aitio, O., Helin, J., Guan, Z., Permi, P., Bamford, D.H., Eichler, J., Roine, E., Diversity in prokaryotic glycosylation: An archaealderived N-linked glycan contains legionaminic acid (2012) Mol. Microbiol., 84, pp. 578-593
  • Allers, T., Barak, S., Liddell, S., Wardell, K., Mevarech, M., Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii (2010) Appl. Environ. Microbiol., 76, pp. 1759-1769
  • Marinus, M.G., Location of DNA methylation genes on the Escherichia coli K-12 genetic map (1973) Mol. Gen. Genet., 127, pp. 47-55

Citas:

---------- APA ----------
Parente, J., Casabuono, A., Ferrari, M.C., Paggi, R.A., De Castro, R.E., Couto, A.S. & Giménez, M.I. (2014) . A rhomboid protease gene deletion affects a novel oligosaccharide N-linked to the S-layer glycoprotein of Haloferax volcanii. Journal of Biological Chemistry, 289(16), 11304-11317.
http://dx.doi.org/10.1074/jbc.M113.546531
---------- CHICAGO ----------
Parente, J., Casabuono, A., Ferrari, M.C., Paggi, R.A., De Castro, R.E., Couto, A.S., et al. "A rhomboid protease gene deletion affects a novel oligosaccharide N-linked to the S-layer glycoprotein of Haloferax volcanii" . Journal of Biological Chemistry 289, no. 16 (2014) : 11304-11317.
http://dx.doi.org/10.1074/jbc.M113.546531
---------- MLA ----------
Parente, J., Casabuono, A., Ferrari, M.C., Paggi, R.A., De Castro, R.E., Couto, A.S., et al. "A rhomboid protease gene deletion affects a novel oligosaccharide N-linked to the S-layer glycoprotein of Haloferax volcanii" . Journal of Biological Chemistry, vol. 289, no. 16, 2014, pp. 11304-11317.
http://dx.doi.org/10.1074/jbc.M113.546531
---------- VANCOUVER ----------
Parente, J., Casabuono, A., Ferrari, M.C., Paggi, R.A., De Castro, R.E., Couto, A.S., et al. A rhomboid protease gene deletion affects a novel oligosaccharide N-linked to the S-layer glycoprotein of Haloferax volcanii. J. Biol. Chem. 2014;289(16):11304-11317.
http://dx.doi.org/10.1074/jbc.M113.546531