Regulated intramembrane proteolysis in the control of extracytoplasmic function sigma factors

Research in Microbiology

Volumn 160, Issue 9, 2009, Pages 696-703

  Heinrich, Janine ^a   Wiegert, Thomas ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Extracytoplasmic function; Proteolysis; Sigma factors; Transmembrane signaling processes

Indexed keywords

ANTIBIOTIC AGENT; ESCHERICHIA COLI PROTEIN; PEPTIDE DERIVATIVE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN PRSW; PROTEIN RASP; PROTEIN RSIW; SIGMA FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BINDING AFFINITY; BIOFILM; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL COMMUNICATION; CELL COMPARTMENTALIZATION; CELL DIVISION; CELL STIMULATION; CELL STRESS; CRYSTAL STRUCTURE; CYTOPLASM; EUKARYOTE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; REGULON; SIGNAL TRANSDUCTION;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOCATALYSIS; CELL MEMBRANE; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-NEGATIVE BACTERIA; SIGMA FACTOR; STRESS, PHYSIOLOGICAL;

EID: 71749105254     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2009.08.019     Document Type: Article

References (82)

1. E in Esche-richia coli. Curr. Opin. Microbiol. 7 (2004) 157-162
2. E envelope stress response. Curr. Opin. Microbiol. 11 (2008) 535-540
3. E-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev. 13 (1999) 2449-2461
4. Akiyama Y., Kanehara K., and Ito K. RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences. EMBO J. 23 (2004) 4434-4442
5. E-dependent envelope stress response. Mol. Microbiol. 52 (2004) 613-619
6. E-dependent extracytoplasmic stress response. Genes Dev. 16 (2002) 2156-2168
7. An F.Y., Sulavik M.C., and Clewell D.B. Identification and characterization of a determinant (eep) on the Enterococcus faecalis chromosome that is involved in production of the peptide sex pheromone cAD1. J. Bacteriol. 181 (1999) 5915-5921
8. E, and its anti-sigma factor, ChrR. J. Mol. Biol. 341 (2004) 345-360
9. Asai K., Ishiwata K., Matsuzaki K., and Sadaie Y. A viable Bacillus subtilis strain without functional extracytoplasmic function sigma genes. J. Bacteriol. 190 (2008) 2633-2636
10. Bramkamp M., Weston L., Daniel R.A., and Errington J. Regulated intramembrane proteolysis of FtsL protein and the control of cell division in Bacillus subtilis. Mol. Microbiol. 62 (2006) 580-591
11. Brooks B.E., and Buchanan S.K. Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors. Biochim. Biophys. Acta 1778 (2008) 1930-1945
12. Brown M.S., Ye J., Rawson R.B., and Goldstein J.L. Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100 (2000) 391-398
13. Browning D.F., Whitworth D.E., and Hodgson D.A. Light-induced carotenogenesis in Myxococcus xanthus: functional characterization of the ECF sigma factor CarQ and antisigma factor CarR. Mol. Microbiol. 48 (2003) 237-251
14. W-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol. Microbiol. 60 (2006) 765-782
15. Butcher B.G., Mascher T., and Helmann J.D. Environmental sensing and the role of extracytoplasmic function sigma factors. In: El-Sharoud W. (Ed). Bacterial Physiology: a Molecular Approach (2008) 233-261 (Chapter 8)
16. E with the cytoplasmic domain of its anti-sigma RseA. Mol. Cell 11 (2003) 1067-1078
17. M regulons. Mol. Microbiol. 45 (2002) 1267-1276
18. Cezairliyan B.O., and Sauer R.T. Inhibition of regulated proteolysis by RseB. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 3771-3776
19. Cezairliyan B.O., and Sauer R.T. Control of Pseudomonas aeruginosa AlgW protease cleavage of MucA by peptide signals and MucB. Mol. Microbiol. 72 (2009) 368-379
20. E-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction. Genes Dev. 21 (2007) 124-136
21. Chen J.C., Viollier P.H., and Shapiro L. A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant. Mol. Microbiol. 55 (2005) 1085-1103
22. E, is required for intracellular survival of nontypeable Haemophilus influenzae in J774 macrophages. Infect. Immun. 70 (2002) 708-715
23. E is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides. Mol. Microbiol. 56 (2005) 789-799
24. E. Mol. Microbiol. 24 (1997) 373-385
25. DeVries C.A., and Ohman D.E. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J. Bacteriol. 176 (1994) 6677-6687
26. Ehrmann M., and Clausen T. Proteolysis as a regulatory mechanism. Annu. Rev. Genet. 38 (2004) 709-724
27. Ellermeier C.D., and Losick R. Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis. Genes Dev. 20 (2006) 1911-1922
28. Erez E., Fass D., and Bibi E. How intramembrane proteases bury hydrolytic reactions in the membrane. Nature 459 (2009) 371-378
29. E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. Genes Dev. 3 (1989) 1462-1471
30. Flynn J.M., Levchenko I., Sauer R.T., and Baker T.A. Modulating substrate choice: the SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev. 18 (2004) 2292-2301
31. Flynn J.M., Neher S.M., Kim Y.-I., Sauer R.T., and Baker T.A. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell 11 (2003) 671-683
32. E envelope stress response relies on multiple mechanisms to inhibit signal-independent proteolysis of the transmembrane anti-sigma factor, RseA. Genes Dev. 18 (2004) 2686-2697
33. E stress response by DegS: how the PDZ domain keeps the protease inactive in the resting state and allows integration of different OMP-derived stress signals upon folding stress. Genes Dev. 21 (2007) 2659-2670
34. Heinrich J., Lunden T., Kontinen V.P., and Wiegert T. The Bacillus subtilis ABC transporter EcsAB influences intramembrane proteolysis through RasP. Microbiology 154 (2008) 1989-1997
35. Heinrich J., and Wiegert T. YpdC determines site-1 degradation in regulated intramembrane proteolysis of the RsiW anti-sigma factor of Bacillus subtilis. Mol. Microbiol. 62 (2006) 566-579
36. Helmann J.D. The extracytoplasmic function (ECF) sigma factors. Adv. Microbiol. Physiol. 46 (2002) 47-110
37. W protein and intrinsic resistance to antimicrobial compounds. Sci. Prog. 89 (2006) 243-266
38. E, is critically important for the virulence of Salmonella typhimurium. Infect. Immun. 67 (1999) 1560-1568
39. Inaba K., Suzuki M., Maegawa K., Akiyama S., Ito K., and Akiyama Y. A pair of circularly permutated PDZ domains control RseP, the S2P family intramembrane protease of Escherichia coli. J. Biol. Chem. 283 (2008) 35042-35052
40. Jin K.S., Kim D.Y., Rho Y., Le V.B., Kwon E., Kim K.K., and Ree M. Solution structures of RseA and its complex with RseB. J. Synchrotron. Radiat. 15 (2008) 219-222
41. Jordan S., Hutchings M.I., and Mascher T. Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol. Rev. 32 (2008) 107-146
42. E, RseA. Genes Dev. 16 (2002) 2147-2155
43. Kanehara K., Ito K., and Akiyama Y. YaeL proteolysis of RseA is controlled by the PDZ domain of YaeL and a Gln-rich region of RseA. EMBO J. 22 (2003) 6389-6398
44. Kang J.G., Paget M.S., Seok Y.J., Hahn M.Y., Bae J.B., Hahn J.S., Kleanthous C., Buttner M.J., and Roe J.H. RsrA, an anti-sigma factor regulated by redox change. EMBO J. 18 (1999) 4292-4298
45. Kim D.Y., Jin K.S., Kwon E., Ree M., and Kim K.K. Crystal structure of RseB and a model of its binding mode to RseA. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 8779-8784
46. King-Lyons N.D., Smith K.F., and Connell T.D. Expression of hurP, a gene encoding a prospective site 2 protease, is essential for heme-dependent induction of bhuR in Bordetella bronchiseptica. J. Bacteriol. 189 (2007) 6266-6275
47. Koide K., Ito K., and Akiyama Y. Substrate recognition and binding by RseP, an Escherichia coli intramembrane protease. J. Biol. Chem. 283 (2008) 9562-9570
48. E plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect. Immun. 70 (2002) 5355-5362
49. Kunst F., Ogasawara N., Moszer I., Albertini A.M., Alloni G., Azevedo V., Bertero M.G., Bessieres P., Bolotin A., Borchert S., Borriss R., Boursier L., Brans A., Braun M., Brignell S.C., Bron S., Brouillet S., Bruschi C.V., Caldwell B., Capuano V., Carter N.M., Choi S.K., Codani J.J., Connerton I.F., and Danchin A. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390 (1997) 249-256
50. Lonetto M.A., Brown K.L., Rudd K.E., and Buttner M.J. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase σ factors involved in the regulation of extracytoplasmic functions. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 7573-7577
51. Makinoshima H., and Glickman M.S. Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis. Nature 436 (2005) 406-409
52. Makinoshima H., and Glickman M.S. Site-2 proteases in prokaryotes: regulated intramembrane proteolysis expands to microbial pathogenesis. Microbes Infect. 8 (2006) 1882-1888
53. E and stress response. J. Bacteriol. 176 (1994) 6688-6696
54. Martinez-Argudo I., Ruiz-Vazquez R.M., and Murillo F.J. The structure of an ECF-sigma-dependent, light-inducible promoter from the bacterium Myxococcus xanthus. Mol. Microbiol. 30 (1998) 883-893
55. E regulon through an OmpU-dependent signalling pathway. Mol. Microbiol. 63 (2007) 848-858
56. Matson J.S., and DiRita V.J. Degradation of the membrane-localized virulence activator TcpP by the YaeL protease in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 16403-16408
57. E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7 (1993) 2618-2628
58. E (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol. Microbiol. 24 (1997) 355-371
59. Noone D., Howell A., and Devine K.M. Expression of ykdA, encoding a Bacillus subtilis homologue of HtrA, is heat shock inducible and negatively autoregulated. J. Bacteriol. 182 (2000) 1592-1599
60. Pei J., and Grishin N.V. Type II CAAX prenyl endopeptidases belong to a novel superfamily of putative membrane-bound metalloproteases. Trends Biochem. Sci. 26 (2001) 275-277
61. Petersohn A., Brigulla M., Haas S., Hoheisel J.D., Völker U., and Hecker M. Global analysis of the general stress response of Bacillus subtilis. J. Bacteriol. 183 (2001) 5617-5631
62. Pietiäinen M., Gardemeister M., Mecklin M., Leskela S., Sarvas M., and Kontinen V.P. Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems. Microbiology 151 (2005) 1577-1592
63. Qiu D., Eisinger V.M., Head N.E., Pier G.B., and Yu H.D. ClpXP proteases positively regulate alginate overexpression and mucoid conversion in Pseudomonas aeruginosa. Microbiology 154 (2008) 2119-2130
64. Qiu D., Eisinger V.M., Rowen D.W., and Yu H.D. Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A (2007)
65. Raivio T.L., and Silhavy T.J. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55 (2001) 591-624
66. Ramsey D.M., and Wozniak D.J. Understanding the control of Pseudomonas aeruginosa alginate synthesis and the prospects for management of chronic infections in cystic fibrosis. Mol. Microbiol. 56 (2005) 309-322
67. Rudner D.Z., Fawcett P., and Losick R. A family of membrane-embedded metalloproteases involved in regulated proteolysis of membrane-associated transcription factors. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 14765-14770
68. W anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol. Microbiol. 52 (2004) 1091-1105
69. S, a novel component of the Staphylococcus aureus stress and virulence responses. PLoS One 3 (2008) e3844
70. Sohn J., Grant R.A., and Sauer R.T. Allosteric activation of DegS, a stress sensor PDZ protease. Cell 131 (2007) 572-583
71. Sohn J., and Sauer R.T. OMP peptides modulate the activity of DegS protease by differential binding to active and inactive conformations. Mol. Cell 33 (2009) 64-74
72. Stevenson L.G., Strisovsky K., Clemmer K.M., Bhatt S., Freeman M., and Rather P.N. 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
73. E controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol. Microbiol. 43 (2002) 771-782
74. Urban S. Making the cut: central roles of intramembrane proteolysis in pathogenic microorganisms. Nat. Rev. Microbiol. 7 (2009) 411-423
75. Urban S., and Freeman M. Intramembrane proteolysis controls diverse signalling pathways throughout evolution. Curr. Opin. Genet. Dev. 12 (2002) 512-518
76. Urban S., and Shi Y. Core principles of intramembrane proteolysis: comparison of rhomboid and site-2 family proteases. Curr. Opin. Struct. Biol. 18 (2008) 432-441
77. Weihofen A., and Martoglio B. Intramembrane-cleaving proteases: controlled liberation of proteins and bioactive peptides. Trends Cell Biol. 13 (2003) 71-78
78. W regulon. Mol. Microbiol. 41 (2001) 59-71
79. Wolfe M.S., and Kopan R. Intramembrane proteolysis: theme and variations. Science 305 (2004) 1119-1123
80. Wollmann P., and Zeth K. The structure of RseB: a sensor in periplasmic stress response of E. coli. J. Mol. Biol. 372 (2007) 927-941
81. Yu Y.T., and Kroos L. Evidence that SpoIVFB is a novel type of membrane metalloprotease governing intercompartmental communication during Bacillus subtilis sporulation. J. Bacteriol. 182 (2000) 3305-3309
82. W stress response. Mol. Microbiol. 61 (2006) 1569-1582