Role of rhomboid proteases in bacteria

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 12, 2013, Pages 2849-2854

  Rather, Philip ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

AarA; GlpG; Rhomboid protease; Twin arginine transport

Indexed keywords

AARA PROTEIN; BACTERIAL ENZYME; BACTERIAL PROTEIN; CEFOTAXIME; GLPG PROTEIN; PROTEINASE; RHOMBOID PROTEASE; RHOMBOSORTASE; TATA PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; YQGP PROTEIN;

AARA GENE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIUM COLONY; BIOFILM; CELL DIVISION; ENZYME ANALYSIS; ENZYME SUBSTRATE; ESCHERICHIA COLI; GLPG GENE; GLUCOSE TRANSPORT; MSMEG 4904 GENE; MSMEG 5036 GENE; MUTATIONAL ANALYSIS; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FAMILY; PROTEIN FUNCTION; PROVIDENCIA STUARTII; REVIEW;

AARA; GLPG; RHOMBOID PROTEASE; TWIN-ARGININE TRANSPORT;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; ENDOPEPTIDASES; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MYCOBACTERIUM SMEGMATIS; PROTEOLYSIS; PROVIDENCIA; QUORUM SENSING; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

BACILLUS SUBTILIS; ESCHERICHIA COLI; MYCOBACTERIUM SMEGMATIS; PROVIDENCIA STUARTII;

EID: 84885181836     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.03.012     Document Type: Review

References (58)

1. S. Urban, J.R. Lee, and M. Freeman Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases Cell 107 2001 173 182 (Pubitemid 33035944)
2. J.R. Lee, S. Urban, C.F. Garvey, and M. Freeman Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila Cell 107 2001 161 171 (Pubitemid 33035943)
3. S. Urban, and M. Freeman Intramembrane proteolysis controls diverse signaling pathways throughout evolution Curr. Opin. Genet. Dev. 12 2002 512 518 (Pubitemid 35013532)
4. T. Reddy, and J.K. Rainey The multifaceted substrate capture scheme of a rhomboid protease J. Phys. Chem. 116 2012 8942 8954
5. Y. Zhou, S.M. Moin, S. Urban, and Y. Zhang An internal water retention site in the rhomboid intramembrane protease GlpG ensures catalytic efficiency Structure 20 2012 1255 1263
6. M.K. Lemberg, J. Menendez, A. Misik, M. Garcia, C.M. Koth, and M. Freeman Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases EMBO J. 24 2005 464 472 (Pubitemid 40343249)
7. S. Urban, and M. Freeman Substrate specificity of rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain Mol. Cell 11 2003 1425 1434 (Pubitemid 36776530)
8. S. Urban, and M.S. Wolfe Reconstitution of intramembrane proteolysis in vitro reveals that pure rhomboid is sufficient for catalysis and specificity Proc. Natl. Acad. Sci. U.S.A. 102 2005 1883 1888 (Pubitemid 40261981)
9. Y. Xue, S. Chowdhury, X. Liu, Y. Akiyama, J. Ellman, and Y. Ha Conformational change in the rhomboid protease GlpG induced by inhibitor binding to its S′ substrates Biochemistry 51 2012 3723 3731
10. Y. Wang, Y. Zhang, and Y. Ha Crystal structure of a rhomboid family intramembrane protease Nature 444 2006 179 180
11. A. Ben-Shem, D. Fass, and E. Bibi Structural basis for intramembrane proteolysis by rhomboid serine proteases Proc. Natl. Acad. Sci. U.S.A. 104 2007 462 466 (Pubitemid 46123048)
12. S. Maegawa, K. Ito, and Y. Akiyama Proteolytic action of GlpG, a rhomboid protease in the Escherichia coli cytoplasmic membrane Biochemistry 44 2005 13543 13552 (Pubitemid 41443681)
13. Z. Wu, N. Yan, L. Feng, A. Oberstein, H. Yan, R.P. Baker, L. Gu, P.D. Jeffrey, S. Urban, and Y. Shi Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry Nat. Struct. Mol. Biol. 13 2006 1084 1091 (Pubitemid 44885918)
14. Y. Wang, and Y. Ha Open cap conformation of intramembrane protease GlpG Proc. Natl. Acad. Sci. U.S.A. 104 2007 2098 2102 (Pubitemid 46391358)
15. R.P. Baker, K. Young, L. Feng, Y. Shi, and S. Urban Enzymatic analysis of a rhomboid intramembrane protease implicates transmembrane helix 5 as the lateral substrate gate Proc. Natl. Acad. Sci. U.S.A. 104 2007 8257 8262 (Pubitemid 47175475)
16. C. Lazero-Saez, C.L. Brooks, and M.J. Lemieux Structural comparison of substrate entry gate for rhomboid intramembrane peptidases Biochem. Cell Biol. 89 2011 216 223
17. K.R. Vinothkumar, K. Strisovsky, A. Andreeva, Y. Christova, S. Verhelst, and M. Freeman The structural basis for catalysis and substrate specificity of a rhomboid protease EMBO J. 29 2010 3793 3801
18. S. Urban, and R.P. Baker In vivo analysis reveals substrate gating mutants of a rhomboid intramembrane protease display increased activity in living cells Biol. Chem. 389 2008 1107 1115
19. P. Sampathkumar, M.W. Mak, S.J. Fischer-Witholt, E. Guigard, C.M. Kay, and M.J. Lemieux Oligomeric state study of prokaryotic rhomboid proteases Biochim. Biophys. Acta 1818 2012 3090 3097
20. A. Del Rio, K. Dutta, J. Chavez, I. Ubarretxena-Belandia, and R. Ghose Solution structure and dynamics of the N-terminal cytosolic domain of rhomboid intramembrane protease from Pseudomonas aeruginosa: insights into a functional role in intramembrane proteolysis J. Mol. Biol. 365 2006 109 122 (Pubitemid 44821200)
21. Y. Akiyama, and S. Maegawa Sequence features of substrates required for cleavage by GlpG, an Escherichia coli rhomboid protease Mol. Microbiol. 64 2007 1028 1037 (Pubitemid 46743969)
22. K. Strisovsky, H.J. Sharpe, and M. Freeman Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates Mol Cell 36 2009 1048 1059
23. L.G. Stevenson, K. Strisovsky, K.M. Clemmer, S. Bhatt, M. Freeman, and P.N. Rather The rhomboid protease AarA mediates quorum sensing in Providencia stuartii by activating TatA of the twin arginine translocase Proc. Natl. Acad. Sci. U.S.A. 104 2007 1003 1008 (Pubitemid 46154726)
24. P.N. Rather, and E. Orosz Characterization of aarA, a pleiotrophic negative regulator of the 2′-N-acetyltransferase in Providencia stuartii J. Bacteriol. 176 1994 5140 5144 (Pubitemid 24253759)
25. M.J. Fritsch, M. Krehenbrink, M.J. Tarry, B.C. Berks, and T. Palmer Processing by rhomboid protease is required for Providencia stuartii TatA to interact with TatC and form functional homo-oligomeric complexes Mol. Microbiol. 84 2012 1108 1123
26. P.N. Rather, M.M. Parojcic, and M.R. Paradise An extracellular factor regulating expression of the chromosomal aminoglycoside 2′-N- acetyltransferase in Providencia stuartii Antimicrob. Agents Chemother. 41 1997 1749 1754 (Pubitemid 27339880)
27. P.N. Rather, X. Ding, R.R. Baca-DeLancey, and S. Sidduqui Providencia stuartii genes activated by cell-cell signaling and identification of a gene required for the production or activity of an extracellular factor J. Bacteriol. 181 1999 7185 7191
28. L.R. Mesak, F.M. Mesak, and M.K. Dahl Expression of a novel gene gluP is essential for normal Bacillus subtilis cell division and contributes to glucose transport BMC Microbiol. 4 2004 13
29. D.P. Kateete, F.A. Katabazi, A. Okeng, M. Okee, C. Musinguzi, B.B. Asiimwe, S. Kyobe, J. Asiimwe, W.H. Boom, and M.L. Joloba Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis PLoS One 7 2012 9e45741
30. E. Erez, and E. Bibi Cleavage of a multispanning membrane protein by an intramembrane serine protease Biochemistry 48 2009 12314 12322
31. D.H. Haft, and N. Varghese Gly-Gly CTERM and rhombosortase: a C-terminal protein processing signal in a many to one pairing with a rhomboid family intramembrane serine protease PLoS One 6 12 2011 e28886
32. S. Urban, D. Schlieper, and M. Freeman Conservation of intramembrane proteolytic activity and substrate specificity in prokaryotic and eukaryotic rhomboids Curr. Biol. 12 2002 1507 1512 (Pubitemid 35036649)
33. B. Yang, and T.J. Larson Multiple promoters are responsible for transcription of the glpEGR operon of Escherichia coli Biochim. Biophys. Acta 1396 1998 114 126 (Pubitemid 28131451)
34. W.K. Ray, G. Zeng, M.B. Potters, A.M. Mansuri, and T.J. Larson Characterization of a 12 kilodalton rhodanese encoded by glpE of Escherichia coli and its interaction with thioredoxin J. Bacteriol. 182 2000 2277 2284 (Pubitemid 30183548)
35. H. Schweizer, W. Boos, and T.J. Larson Repressor for the sn-glycerol-3-phosphateregulon of Escherichia coli K12: cloning of the glpR gene and identification of its product J. Bacteriol. 161 1985 563 566 (Pubitemid 15168912)
36. K.M. Clemmer, G.M. Sturgill, A. Veenstra, and P.N. Rather Functional characterization of Escherichia coli GlpG and additional rhomboid proteins using an aarA mutant of Providencia stuartii J. Bacteriol. 188 2006 3415 3419
37. P.N. Rather, E. Orosz, R. Hare, G. Miller, and K. Shaw Characterization and transcriptional regulation of the 2′-N-acetyltransferase gene of Providencia stuartii J. Bacteriol. 175 1993 6492 6498 (Pubitemid 23315481)
38. P.N. Rather, and D.R. Macinga The chromosomal 2′-N- acetyltransferase of Providencia stuartii: physiological functions and genetic regulation Front. Biosci. 4 1999 132 140
39. K.G. Payie, P.N. Rather, and A.J. Clarke Contribution of gentamicin 2′-N-acetyltransferase to the O-acetylation of peptidoglycan in Providencia stuartii J. Bacteriol. 177 1995 4303 4310
40. N.R. Stanley, K. Findlay, B.C. Berks, and T. Palmer Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotrophic defects in the cell envelope J. Bacteriol. 183 2001 139 144 (Pubitemid 32003117)
41. M. Gallio, and P. Kylsten Providencia may help find a function for a novel widespread protein family Curr. Biol. 10 2000 693 694
42. M. Gallio, G. Sturgill, P.N. Rather, and P. Kylsten A common mechanism for extracellular signaling in eukaryotes and prokaryotes Proc. Natl. Acad. Sci. U.S.A. 99 2002 12208 12213
43. M.A. Sturtevant, M. Roark, and E. Bier The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway Genes Dev. 7 1993 961 973 (Pubitemid 23170821)
44. C.L. Santini, B. Ize, A. Chanal, M. Muller, G. Giordano, and L.F. Wu A novel sec-independent periplasmic protein translocation pathway in Escherichia coli EMBO J. 17 1998 101 112 (Pubitemid 28041052)
45. F. Sargent, E.G. Bogsch, N.R. Stanley, M. Wexler, C. Robinson, B.C. Berks, and T. Palmer Overlapping functions of components of a bacterial Sec-independent protein export pathway EMBO J. 17 1998 3640 3650 (Pubitemid 28327382)
46. J.H. Weiner, P.T. Bilous, G.M. Shaw, S.P. Lubitz, L. Frost, G.H. Thomas, J.A. Cole, and R.J. Turner A novel and ubiquitous system for membrane targeting and secretion of cofactor containing proteins Cell 93 1998 93 101 (Pubitemid 28173555)
47. T. Palmer, F. Sargent, and B.C. Berks Export of complex cofactor-containing proteins by the bacterial Tat pathway Trends Microbiol. 13 2005 175 180 (Pubitemid 40463319)
48. M. Wexler, F. Sargent, R.L. Jack, N.R. Stanley, E.G. Bogsch, C. Robinson, B.C. Berks, and T. Palmer TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in sec-independent protein export J. Biol. Chem. 275 2000 16717 16722 (Pubitemid 30398902)
49. T.G. Bernhardt, and P.A.J. de Boer The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway Mol. Microbiol. 48 2003 1171 1182 (Pubitemid 36718214)
50. B. Ize, N.R. Stanley, G. Buchanan, and T. Palmer Role of the Escherichia coli Tat pathway in outer membrane integrity Mol. Microbiol. 48 2003 1183 1193 (Pubitemid 36718215)
51. C. Heidrich, M.F. Templin, A. Ursinus, M. Merdanovic, J. Berger, and H. Schwarz Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli Mol. Microbiol. 41 2001 167 178 (Pubitemid 32660992)
52. C. Heidrich, A. Ursinus, J. Berger, H. Schwarz, and J.V. Holtje Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli J. Bacteriol. 184 2002 6093 6099 (Pubitemid 35265888)
53. A. Bolhuis, E.G. Bogsch, and C. Robinson Subunit interactions in the twin arginine translocase complex of Escherichia coli FEBS Lett. 472 2000 88 92 (Pubitemid 30224592)
54. E. de Leeuw, T. Granjon, I. Porcelli, M. Alami, S.B. Carr, M. Mueller, F. Sargent, T. Palmer, and B.C. Berks Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes J. Mol. Biol. 322 2002 1135 1146 (Pubitemid 35266517)
55. I. Porcelli, E. de Leeuw, R. Wallis, E. van den Brink-van, B. der Laan, B.A. de Kruijff, T. Wallace, and B.C. Berks Palmer Characterization and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system Biochemistry 41 2002 13690 13697 (Pubitemid 35332706)
56. F. Sargent, U. Gohlke, E. de Leeuw, N.R. Stanley, T. Palmer, H.R. Saibil, and B.C. Berks Purified components of the Escherichia coli Tat protein transport system form a double layered ring structure Eur. J. Biochem. 268 2001 3361 3367 (Pubitemid 32862927)
57. U. Gohlke, L. Pullan, C.A. McDevitt, I. Porcelli, E. de Leeuw, T. Palmer, H.R. Saibil, and B.C. Berks The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter Proc. Natl. Acad. Sci. U.S.A. 102 2005 10482 10486 (Pubitemid 41061580)
58. R. Priyadarshini, D.L. Popham, and K.D. Young Daughter cell separation by penicillin-binding proteins and peptidoglycan amidases in Escherichia coli J. Bacteriol. 188 2006 5345 5355 (Pubitemid 44157290)