A rhomboid protease gene deletion affects a novel oligosaccharide N-linked to the S-layer glycoprotein of Haloferax volcanii

Journal of Biological Chemistry

Volumn 289, Issue 16, 2014, Pages 11304-11317

  Parente, Juliana ^a   Casabuono, Adriana ^a   Ferrari, María Celeste ^b   Paggi, Roberto Alejandro ^b   De Castro, Rosana Esther ^b   Couto, Alicia Susana ^a   Giménez, María Inés ^b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

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;

EID: 84899029290     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.546531     Document Type: Article

References (46)

1. Wolfe, M. S., and Kopan, R. (2004) Intramembrane proteolysis: theme and variations. Science 305, 1119-1123
2. Urban, S. (2009) Making the cut: central roles of intramembrane proteolysis in pathogenic microorganisms. Nat. Rev. Microbiol. 7, 411-423
3. Lee, J. R., Urban, S., Garvey, C. F., and Freeman, M. (2001) Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107, 161-171
4. Herlan, M., Vogel, F., Bornhovd, C., Neupert, W., and Reichert, A. S. (2003) Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J. Biol. Chem. 278, 27781-27788
5. McQuibban, G. A., Saurya, S., and Freeman, M. (2003) Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 423, 537-541
6. Baker, R. P., Wijetilaka, R., and Urban, S. (2006) Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathog. 2, e113
7. Baxt, L. A., Baker, R. P., Singh, U., and Urban, S. (2008) An Entamoeba histolytica rhomboid protease with atypical specificity cleaves a surface lectin involved in phagocytosis and immune evasion. Genes Dev. 22, 1636-1646
8. Stevenson, L. G., Strisovsky, K., Clemmer, K. M., Bhatt, S., Freeman, M., and Rather, P. N. (2007) Rhomboid protease AarA mediates quorumsensing in Providencia stuartii by activating TatA of the twin-arginine translocase. Proc. Natl. Acad. Sci. U.S.A. 104, 1003-1008
9. Kateete, D. P., Katabazi, F. A., Okeng, A., Okee, M., Musinguzi, C., Asiimwe, B. B., Kyobe, S., Asiimwe, J., Boom, W. H., and Joloba, M. L. (2012) Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis. PloS One 7, e45741
10. Maupin-Furlow, J. A., Gil, M. A., Humbard, M. A., Kirkland, P. A., Li, W., Reuter, C. J., and Wright, A. J. (2005) Archaeal proteasomes and other regulatory proteases. Curr. Opin. Microbiol. 8, 720-728
11. Eichler, J., and Adams, M. W. (2005) Posttranslational protein modification in Archaea. Microbiol. Mol. Biol. Rev. 69, 393-425
12. Jarrell, K. F., Jones, G. M., and Nair, D. B. (2010) Biosynthesis and role of N-linked glycosylation in cell surface structures of archaea with a focus on flagella and s layers. Int. J. Microbiol. 2010, 470138
13. Sumper, M., Berg, E., Mengele, R., and Strobel, I. (1990) Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J. Bacteriol. 172, 7111-7118
14. Mengele, R., and Sumper, M. (1992) Drastic differences in glycosylation of related S-layer glycoproteins from moderate and extreme halophiles. J. Biol. Chem. 267, 8182-8185
15. Abu-Qarn, M., Yurist-Doutsch, S., Giordano, A., Trauner, A., Morris, H. R., Hitchen, P., Medalia, O., Dell, A., and Eichler, J. (2007) Haloferax volcanii AglB and AglD are involved in N-glycosylation of the S-layer glycoprotein and proper assembly of the surface layer. J. Mol. Biol. 374, 1224-1236
16. Magidovich, H., Yurist-Doutsch, S., Konrad, Z., Ventura, V. V., Dell, A., Hitchen, P. G., and Eichler, J. (2010) AglP is a S-adenosyl-L- methioninedependent methyltransferase that participates in the N-glycosylation pathway of Haloferax volcanii. Mol. Microbiol. 76, 190-199
17. Calo, D., Kaminski, L., and Eichler, J. (2010) Protein glycosylation in Archaea: sweet and extreme. Glycobiology 20, 1065-1076
18. Tripepi, M., You, J., Temel, S., Önder, Ö., Brisson, D., and Pohlschröder, M. (2012)N-Glycosylation of Haloferax volcanii flagellins requires known Agl proteins and is essential for biosynthesis of stable flagella. J. Bacteriol. 194, 4876-4887
19. Guan, Z., Naparstek, S., Calo, D., and Eichler, J. (2012) Protein glycosylation as an adaptive response in Archaea: growth at different salt concentrations leads to alterations in Haloferax volcanii S-layer glycoprotein Nglycosylation. Environ. Microbiol. 14, 743-753
20. Kaminski, L., Guan, Z., Yurist-Doutsch, S., and Eichler, J. (2013) Two distinct N-glycosylation pathways process the Haloferax volcanii S-layer glycoprotein upon changes in environmental salinity. MBio 4, e00716-13
21. Paggi, R. A., Madrid, E. A., D'Alessandro, C. P., Cerletti, M., and De Castro, R. E. (2010) Growth phase-dependent biosynthesis of Nep, a halolysin-like protease secreted by the alkaliphilic haloarchaeon Natrialba magadii. Lett. Appl. Microbiol. 51, 36-41
22. Sambrook, J., Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
23. Strisovsky, K., Sharpe, H. J., and Freeman, M. (2009) Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates. Mol. Cell 36, 1048-1059
24. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
25. Dubray, G., and Bezard, G. (1982) A highly sensitive periodic acid-silver stain for 1, 2-diol groups of glycoproteins and polysaccharides in polyacrylamide gels. Anal. Biochem. 119, 325-329
26. Allers, T., Ngo, H. P., Mevarech, M., and Lloyd, R. G. (2004) Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl. Environ. Microbiol. 70, 943-953
27. Nieuwlandt, D. T., Palmer, J. R., Armbruster, D. T., Kuo, Y. P., Oda, W., and Daniels, C. J. (1995) in Archaea: A Laboratory Manual (Robb, F. T., Place, A. R., Sowers, K. R., Schreier, H. J., DasSarma, S., and Fleischmann, E. M., eds) pp. 161-162, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
28. Wong, M. L., and Medrano, J. F. (2005) Real-time PCR for mRNA quantitation. BioTechniques 39, 75-85
29. Selman, M. H., Hemayatkar, M., Deelder, A. M., and Wuhrer, M. (2011) Cotton HILIC SPE microtips for microscale purification and enrichment of glycans and glycopeptides. Anal. Chem. 83, 2492-2499
30. Lemberg, M. K., Menendez, J., Misik, A., Garcia, M., Koth, C. M., and Freeman, M. (2005) Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases. EMBO J. 24, 464-472
31. Lemieux, M. J., Fischer, S. J., Cherney, M. M., Bateman, K. S., and James, M. N. (2007) The crystal structure of the rhomboid peptidase from Haemophilus influenzae provides insight into intramembrane proteolysis. Proc. Natl. Acad. Sci. U.S.A. 104, 750-754
32. Shlay, J. C., Bartsch, G., Peng, G., Wang, J., Grunfeld, C., Gibert, C. L., Visnegarwala, F., Raghavan, S. S., Xiang, Y., Farrough, M., Perry, H. E., Kotler, D., and El-Sadr, W. M. (2007) 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. J. Acquir. Immune Defic. Syndr. 44, 506-517
33. Baker, R. P., and Urban, S. (2012) Architectural and thermodynamic principles underlying intramembrane protease function. Nat. Chem. Biol. 8, 759-768
34. Urban, S. (2006) Rhomboid proteins: conserved membrane proteases with divergent biological functions. Genes Dev. 20, 3054-3068
35. Schultz, J., Milpetz, F., Bork, P., and Ponting, C. P. (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U.S.A. 95, 5857-5864
36. Letunic, I., Doerks, T., and Bork, P. (2009) SMART 6: recent updates and new developments. Nucleic Acids Res. 37, D229-D232
37. Burroughs, A. M., Iyer, L. M., and Aravind, L. (2011) Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system. Mol. Biosyst. 7, 2261-2277
38. Zhu, B. C., Drake, R. R., Schweingruber, H., and Laine, R. A. (1995) 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. Arch. Biochem. Biophys. 319, 355-364
39. Konrad, Z., and Eichler, J. (2002) Protein glycosylation in Haloferax volcanii: partial characterization of a 98-kDa glycoprotein. FEMS Microbiol. Lett. 209, 197-202
40. Laity, J. H., Lee, B. M., and Wright, P. E. (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11, 39-46
41. Palmieri, G., Balestrieri, M., Peter-Katalinić, J., Pohlentz, G., Rossi, M., Fiume, I., and Pocsfalvi, G. (2013) Surface-exposed glycoproteins of hyperthermophilic Sulfolobus solfataricus P2 show a common N-glycosylation profile. J. Proteome Res. 12, 2779-2790
42. Wan, C., Fu, J., Wang, Y., Miao, S., Song, W., and Wang, L. (2012) Exosome- related multi-pass transmembrane protein TSAP6 is a target of rhomboid protease RHBDD1-induced proteolysis. PloS One 7, e37452
43. Meyer, B. H., Zolghadr, B., Peyfoon, E., Pabst, M., Panico, M., Morris, H. R., Haslam, S. M., Messner, P., Schäffer, C., Dell, A., and Albers, S. V. (2011) Sulfoquinovose synthase: an important enzyme in the N-glycosylation pathway of Sulfolobus acidocaldarius. Mol. Microbiol. 82, 1150-1163
44. Kandiba, L., Aitio, O., Helin, J., Guan, Z., Permi, P., Bamford, D. H., Eichler, J., and Roine, E. (2012) Diversity in prokaryotic glycosylation: an archaealderived N-linked glycan contains legionaminic acid. Mol. Microbiol. 84, 578-593
45. Allers, T., Barak, S., Liddell, S., Wardell, K., and Mevarech, M. (2010) Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii. Appl. Environ. Microbiol. 76, 1759-1769
46. Marinus, M. G. (1973) Location of DNA methylation genes on the Escherichia coli K-12 genetic map. Mol. Gen. Genet. 127, 47-55 Técnicas Técnicas