Function of site-2 proteases in bacteria and bacterial pathogens

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 12, 2013, Pages 2808-2814

  Schneider, Jessica S ^a,c   Glickman, Michael S ^a,b,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Division of Infectious Diseases   (United States)

^c Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

Bacterial signal transduction; Site two protease

Indexed keywords

BACTERIAL ENZYME; CHOLESTEROL; FATTY ACID; MEMBRANE PROTEIN; METALLOPROTEINASE; PHEROMONE; RIP1 PROTEIN; SIGMA FACTOR; SIGMA FACTOR E; SITE 2 PROTEASE; SPOIVFB PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

BACILLUS SUBTILIS; BACTERIAL VIRULENCE; BACTERIUM; BORDETELLA BRONCHISEPTICA; CAULOBACTER CRESCENTUS; CHOLESTEROL SYNTHESIS; CYANOBACTERIUM; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; FATTY ACID SYNTHESIS; LIPOGENESIS; MEMBRANE; METABOLIC REGULATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; REGULON; REVIEW; SALMONELLA ENTERICA; SIGNAL TRANSDUCTION; SPOROGENESIS; TRANSCRIPTION REGULATION;

BACTERIAL SIGNAL TRANSDUCTION; SITE TWO PROTEASE;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; LIPID METABOLISM; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MUTATION; PHEROMONES; PROTEOLYSIS; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS; VIRULENCE FACTORS;

EID: 84885087118     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.04.019     Document Type: Review

References (79)

1. L.N. Kinch, K. Ginalski, and N.V. Grishin Site-2 protease regulated intramembrane proteolysis: sequence homologs suggest an ancient signaling cascade Protein science: a publication of the Protein Society 15 2006 84 93 (Pubitemid 43004236)
2. D.Z. Rudner, P. Fawcett, and R. Losick 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 (Pubitemid 30019714)
3. J. Heinrich, and T. Wiegert Regulated intramembrane proteolysis in the control of extracytoplasmic function sigma factors Res. Microbiol. 160 2009 696 703
4. F.H. Damron, and J.B. Goldberg Proteolytic regulation of alginate overproduction in Pseudomonas aeruginosa Mol. Microbiol. 84 2012 595 607
5. S. Urban Making the cut: central roles of intramembrane proteolysis in pathogenic microorganisms Nat. Rev. Microbiol. 7 2009 411 423
6. T.D. Ho, and C.D. Ellermeier Extra cytoplasmic function sigma factor activation Curr. Opin. Microbiol. 15 2012 182 188
7. J.D. Helmann The extracytoplasmic function (ECF) sigma factors Adv. Microb. Physiol. 46 2002 47 110
8. M.A. Lonetto, K.L. Brown, K.E. Rudd, and M.J. Buttner Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions Proc. Natl. Acad. Sci. U.S.A. 91 1994 7573 7577 (Pubitemid 24238227)
9. D. Missiakas, and S. Raina The extracytoplasmic function sigma factors: role and regulation Mol. Microbiol. 28 1998 1059 1066 (Pubitemid 28293532)
10. R. Chaba, B.M. Alba, M.S. Guo, J. Sohn, N. Ahuja, R.T. Sauer, and C.A. Gross Signal integration by DegS and RseB governs the σ E-mediated envelope stress response in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 108 2011 2106 2111
11. J. Sohn, and R.T. Sauer OMP peptides modulate the activity of DegS protease by differential binding to active and inactive conformations Mol. Cell 33 2009 64 74
12. J. Sohn, R.A. Grant, and R.T. Sauer Allosteric activation of DegS, a stress sensor PDZ protease Cell 131 2007 572 583 (Pubitemid 350007693)
13. N.P. Walsh, B.M. Alba, B. Bose, C.A. Gross, and R.T. Sauer OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain Cell 113 2003 61 71 (Pubitemid 36411960)
14. S.E. Ades, L.E. Connolly, B.M. Alba, and C.A. Gross The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor Genes Dev. 13 1999 2449 2461 (Pubitemid 29453615)
15. K. Koide, K. Ito, and Y. Akiyama Substrate recognition and binding by RseP, an Escherichia coli intramembrane protease J. Biol. Chem. 283 2008 9562 9570
16. Y. Akiyama, K. Kanehara, and K. Ito RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences EMBO J. 23 2004 4434 4442 (Pubitemid 39601968)
17. K. Kanehara, K. Ito, and Y. Akiyama YaeL (EcfE) activates the sigma(E) pathway of stress response through a site-2 cleavage of anti-sigma(E), RseA Genes Dev. 16 2002 2147 2155
18. Y. Hizukuri, and Y. Akiyama PDZ domains of RseP are not essential for sequential cleavage of RseA or stress-induced sigma(E) activation in vivo Mol. Microbiol. 86 2012 1232 1245
19. X. Li, B. Wang, L. Feng, H. Kang, Y. Qi, J. Wang, and Y. Shi Cleavage of RseA by RseP requires a carboxyl-terminal hydrophobic amino acid following DegS cleavage Proc. Natl. Acad. Sci. U.S.A. 106 2009 14837 14842
20. J.M. Flynn, I. Levchenko, R.T. Sauer, and T.A. Baker 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 (Pubitemid 39209577)
21. V.A. Rhodius, W.C. Suh, G. Nonaka, J. West, and C.A. Gross Conserved and variable functions of the sigmaE stress response in related genomes PLoS Biol. 4 2006 e2
22. T.L. Raivio, and T.J. Silhavy Periplasmic stress and ECF sigma factors Annu. Rev. Microbiol. 55 2001 591 624 (Pubitemid 32978117)
23. J. Heinrich, and T. Wiegert YpdC determines site-1 degradation in regulated intramembrane proteolysis of the RsiW anti-sigma factor of Bacillus subtilis Mol. Microbiol. 62 2006 566 579 (Pubitemid 44477242)
24. C.D. Ellermeier, and R. Losick Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis Genes Dev. 20 2006 1911 1922 (Pubitemid 44079328)
25. J. Heinrich, K. Hein, and T. Wiegert Two proteolytic modules are involved in regulated intramembrane proteolysis of Bacillus subtilis RsiW Mol. Microbiol. 74 2009 1412 1426
26. S. Schobel, S. Zellmeier, W. Schumann, and T. Wiegert The Bacillus subtilis sigmaW anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC Mol. Microbiol. 52 2004 1091 1105 (Pubitemid 38916176)
27. T.D. Ho, and C.D. Ellermeier PrsW is required for colonization, resistance to antimicrobial peptides, and expression of extracytoplasmic function sigma factors in Clostridium difficile Infect. Immun. 79 2011 3229 3238
28. M. Cao, T. Wang, R. Ye, and J.D. Helmann Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis sigma(W) and sigma(M) regulons Mol. Microbiol. 45 2002 1267 1276 (Pubitemid 35015351)
29. T. Wiegert, G. Homuth, S. Versteeg, and W. Schumann Alkaline shock induces the Bacillus subtilis sigma(W) regulon Mol. Microbiol. 41 2001 59 71 (Pubitemid 32660983)
30. M. Cao, P.A. Kobel, M.M. Morshedi, M.F. Wu, C. Paddon, and J.D. Helmann Defining the Bacillus subtilis sigma(W) regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches J. Mol. Biol. 316 2002 443 457 (Pubitemid 34729233)
31. A.W. Kingston, C. Subramanian, C.O. Rock, and J.D. Helmann A sigmaW-dependent stress response in Bacillus subtilis that reduces membrane fluidity Mol. Microbiol. 81 2011 69 79
32. M. Bramkamp, L. Weston, R.A. Daniel, and J. Errington Regulated intramembrane proteolysis of FtsL protein and the control of cell division in Bacillus subtilis Mol. Microbiol. 62 2006 580 591 (Pubitemid 44477243)
33. V. Guariglia-Oropeza, and J.D. Helmann Bacillus subtilis sigma(V) confers lysozyme resistance by activation of two cell wall modification pathways, peptidoglycan O-acetylation and d-alanylation of teichoic acids J. Bacteriol. 193 2011 6223 6232
34. T.D. Ho, J.L. Hastie, P.J. Intile, and C.D. Ellermeier The Bacillus subtilis extracytoplasmic function sigma factor sigma(V) is induced by lysozyme and provides resistance to lysozyme J. Bacteriol. 193 2011 6215 6222
35. Y.T. Yu, and L. Kroos Evidence that SpoIVFB is a novel type of membrane metalloprotease governing intercompartmental communication during Bacillus subtilis sporulation J. Bacteriol. 182 2000 3305 3309 (Pubitemid 30326954)
36. O. Resnekov, S. Alper, and R. Losick Subcellular localization of proteins governing the proteolytic activation of a developmental transcription factor in Bacillus subtilis Genes to cells: devoted to molecular & cellular mechanisms 1 1996 529 542 (Pubitemid 126673147)
37. S. Cutting, A. Driks, R. Schmidt, B. Kunkel, and R. Losick Forespore-specific transcription of a gene in the signal transduction pathway that governs pro-sigma K processing in Bacillus subtilis Genes Dev. 5 1991 456 466 (Pubitemid 21905968)
38. M. Gomez, S. Cutting, and P. Stragier Transcription of spoIVB is the only role of sigma G that is essential for pro-sigma K processing during spore formation in Bacillus subtilis J. Bacteriol. 177 1995 4825 4827
39. S. Cutting, V. Oke, A. Driks, R. Losick, S. Lu, and L. Kroos A forespore checkpoint for mother cell gene expression during development in B. subtilis Cell 62 1990 239 250
40. D.Z. Rudner, and R. Losick A sporulation membrane protein tethers the pro-sigmaK processing enzyme to its inhibitor and dictates its subcellular localization Genes Dev. 16 2002 1007 1018 (Pubitemid 34408549)
41. N. Campo, and D.Z. Rudner A branched pathway governing the activation of a developmental transcription factor by regulated intramembrane proteolysis Mol. Cell 23 2006 25 35 (Pubitemid 43963443)
42. N. Campo, and D.Z. Rudner SpoIVB and CtpB are both forespore signals in the activation of the sporulation transcription factor sigmaK in Bacillus subtilis J. Bacteriol. 189 2007 6021 6027 (Pubitemid 47236154)
43. R. Zhou, and L. Kroos Serine proteases from two cell types target different components of a complex that governs regulated intramembrane proteolysis of pro-sigmaK during Bacillus subtilis development Mol. Microbiol. 58 2005 835 846 (Pubitemid 41532479)
44. H. Prince, R. Zhou, and L. Kroos Substrate requirements for regulated intramembrane proteolysis of Bacillus subtilis pro-sigmaK J. Bacteriol. 187 2005 961 971 (Pubitemid 40189770)
45. R. Zhou, C. Cusumano, D. Sui, R.M. Garavito, and L. Kroos Intramembrane proteolytic cleavage of a membrane-tethered transcription factor by a metalloprotease depends on ATP Proc. Natl. Acad. Sci. U.S.A. 106 2009 16174 16179
46. D.H. Green, and S.M. Cutting Membrane topology of the Bacillus subtilis pro-sigma(K) processing complex J. Bacteriol. 182 2000 278 285 (Pubitemid 30030109)
47. A.J. Hinz, D.E. Larson, C.S. Smith, and Y.V. Brun The Caulobacter crescentus polar organelle development protein PodJ is differentially localized and is required for polar targeting of the PleC development regulator Mol. Microbiol. 47 2003 929 941 (Pubitemid 36232792)
48. P.H. Viollier, N. Sternheim, and L. Shapiro Identification of a localization factor for the polar positioning of bacterial structural and regulatory proteins Proc. Natl. Acad. Sci. U.S.A. 99 2002 13831 13836 (Pubitemid 35215466)
49. J.C. Chen, A.K. Hottes, H.H. McAdams, P.T. McGrath, P.H. Viollier, and L. Shapiro Cytokinesis signals truncation of the PodJ polarity factor by a cell cycle-regulated protease EMBO J. 25 2006 377 386 (Pubitemid 43152858)
50. J.C. Chen, P.H. Viollier, and L. Shapiro A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant Mol. Microbiol. 55 2005 1085 1103 (Pubitemid 40299179)
51. H. Makinoshima, and M.S. Glickman Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis Nature 436 2005 406 409 (Pubitemid 41059051)
52. J.G. Sklar, H. Makinoshima, J.S. Schneider, and M.S. Glickman M. tuberculosis intramembrane protease Rip1 controls transcription through three anti-sigma factor substrates Mol. Microbiol. 77 2010 605 617
53. P. Mukherjee, K. Sureka, P. Datta, T. Hossain, S. Barik, K.P. Das, M. Kundu, and J. Basu Novel role of Wag31 in protection of mycobacteria under oxidative stress Mol. Microbiol. 73 2009 103 119
54. V. Deretic, M.J. Schurr, J.C. Boucher, and D.W. Martin Conversion of Pseudomonas aeruginosa to mucoidy in cystic fibrosis: environmental stress and regulation of bacterial virulence by alternative sigma factors J. Bacteriol. 176 1994 2773 2780 (Pubitemid 24152919)
55. C.E. Chitnis, and D.E. Ohman Genetic analysis of the alginate biosynthetic gene cluster of Pseudomonas aeruginosa shows evidence of an operonic structure Mol. Microbiol. 8 1993 583 593
56. C.A. DeVries, and D.E. Ohman 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 (Pubitemid 24338083)
57. D.W. Martin, B.W. Holloway, and V. Deretic Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor J. Bacteriol. 175 1993 1153 1164 (Pubitemid 23060154)
58. D. Qiu, V.M. Eisinger, D.W. Rowen, and H.D. Yu Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U.S.A. 104 2007 8107 8112 (Pubitemid 47185883)
59. F.H. Damron, and H.D. Yu Pseudomonas aeruginosa MucD regulates the alginate pathway through activation of MucA degradation via MucP proteolytic activity J. Bacteriol. 193 2011 286 291
60. L.F. Wood, and D.E. Ohman Use of cell wall stress to characterize sigma 22 (AlgT/U) activation by regulated proteolysis and its regulon in Pseudomonas aeruginosa Mol. Microbiol. 72 2009 183 201
61. L.F. Wood, A.J. Leech, and D.E. Ohman Cell wall-inhibitory antibiotics activate the alginate biosynthesis operon in Pseudomonas aeruginosa: roles of sigma (AlgT) and the AlgW and Prc proteases Mol. Microbiol. 62 2006 412 426 (Pubitemid 44477231)
62. J.C. Boucher, J. Martinez-Salazar, M.J. Schurr, M.H. Mudd, H. Yu, and V. Deretic Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA J. Bacteriol. 178 1996 511 523 (Pubitemid 26030607)
63. R.C. Draper, L.W. Martin, P.A. Beare, and I.L. Lamont Differential proteolysis of sigma regulators controls cell-surface signalling in Pseudomonas aeruginosa Mol. Microbiol. 82 2011 1444 1453
64. N.D. King-Lyons, K.F. Smith, and T.D. Connell 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 (Pubitemid 47378634)
65. T.L. Testerman, A. Vazquez-Torres, Y. Xu, J. Jones-Carson, S.J. Libby, and F.C. Fang The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival Mol. Microbiol. 43 2002 771 782 (Pubitemid 34597269)
66. S. Humphreys, A. Stevenson, A. Bacon, A.B. Weinhardt, and M. Roberts The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium Infect. Immun. 67 1999 1560 1568 (Pubitemid 29144366)
67. C. Muller, I.S. Bang, J. Velayudhan, J. Karlinsey, K. Papenfort, J. Vogel, and F.C. Fang Acid stress activation of the sigma(E) stress response in Salmonella enterica serovar Typhimurium Mol. Microbiol. 71 2009 1228 1238
68. J.S. Matson, and V.J. DiRita 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 (Pubitemid 41688926)
69. J.S. Matson, J.H. Withey, and V.J. DiRita Regulatory networks controlling Vibrio cholerae virulence gene expression Infect. Immun. 75 2007 5542 5549 (Pubitemid 350207790)
70. F.Y. An, and D.B. Clewell Identification of the cAD1 sex pheromone precursor in Enterococcus faecalis J. Bacteriol. 184 2002 1880 1887 (Pubitemid 34275530)
71. F.Y. An, M.C. Sulavik, and D.B. Clewell 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 (Pubitemid 29459900)
72. J.R. Chandler, and G.M. Dunny Characterization of the sequence specificity determinants required for processing and control of sex pheromone by the intramembrane protease Eep and the plasmid-encoded protein PrgY J. Bacteriol. 190 2008 1172 1183 (Pubitemid 351214998)
73. E.L. Denham, P.N. Ward, and J.A. Leigh Lipoprotein signal peptides are processed by Lsp and Eep of Streptococcus uberis J. Bacteriol. 190 2008 4641 4647 (Pubitemid 351898981)
74. A. Saito, Y. Hizukuri, E. Matsuo, S. Chiba, H. Mori, O. Nishimura, K. Ito, and Y. Akiyama Post-liberation cleavage of signal peptides is catalyzed by the site-2 protease (S2P) in bacteria Proc. Natl. Acad. Sci. U.S.A. 108 2011 13740 13745
75. K.L. Frank, A.M. Barnes, S.M. Grindle, D.A. Manias, P.M. Schlievert, and G.M. Dunny Use of recombinase-based in vivo expression technology to characterize Enterococcus faecalis gene expression during infection identifies in vivo-expressed antisense RNAs and implicates the protease Eep in pathogenesis Infect. Immun. 80 2012 539 549
76. X. Zhang, G. Chen, C. Qin, Y. Wang, and D. Wei Slr0643, an S2P homologue, is essential for acid acclimation in the cyanobacterium Synechocystis sp. PCC 6803 Microbiology 158 2012 2765 2780
77. K. Chen, L. Gu, X. Xiang, M. Lynch, and R. Zhou Identification and characterization of five intramembrane metalloproteases in Anabaena variabilis J. Bacteriol. 194 2012 6105 6115
78. G.M. Dunny, and C.M. Johnson Regulatory circuits controlling enterococcal conjugation: lessons for functional genomics Curr. Opin. Microbiol. 14 2011 174 180
79. G.M. Dunny, M.H. Antiporta, and H. Hirt Peptide pheromone-induced transfer of plasmid pCF10 in Enterococcus faecalis: probing the genetic and molecular basis for specificity of the pheromone response Peptides 22 2001 1529 1539 (Pubitemid 32918233)