1932

Abstract

Protein degradation is essential for all living things. Bacteria use energy-dependent proteases to control protein destruction in a highly specific manner. Recognition of substrates is determined by the inherent specificity of the proteases and through adaptor proteins that alter the spectrum of substrates. In the α-proteobacterium , regulated protein degradation is required for stress responses, developmental transitions, and cell cycle progression. In this review, we describe recent progress in our understanding of the regulated and stress-responsive protein degradation pathways in . We discuss how organization of highly specific adaptors into functional hierarchies drives destruction of proteins during the bacterial cell cycle. Because all cells must balance the need for degradation of many true substrates with the toxic consequences of nonspecific protein destruction, principles found in one system likely generalize to others.

Keyword(s): AAA+ proteaseadaptorcell cycleClpAPClpXPLon
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2016-11-23
2024-06-20
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Literature Cited

  1. Aakre CD, Phung TN, Huang D, Laub MT. 1.  2013. A bacterial toxin inhibits DNA replication elongation through a direct interaction with the beta sliding clamp. Mol. Cell 52:617–28 [Google Scholar]
  2. Abel S, Bucher T, Nicollier M, Hug I, Kaever V. 2.  et al. 2013. Bi-modal distribution of the second messenger c-di-GMP controls cell fate and asymmetry during the Caulobacter cell cycle. PLOS Genet 9:e1003744 [Google Scholar]
  3. Abel S, Chien P, Wassmann P, Schirmer T, Kaever V. 3.  et al. 2011. Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol. Cell 43:550–60 [Google Scholar]
  4. Alvarez-Martinez CE, Baldini RL, Gomes SL. 4.  2006. A Caulobacter crescentus extracytoplasmic function sigma factor mediating the response to oxidative stress in stationary phase. J. Bacteriol. 188:1835–46 [Google Scholar]
  5. Angelastro PS, Sliusarenko O, Jacobs-Wagner C. 5.  2010. Polar localization of the CckA histidine kinase and cell cycle periodicity of the essential master regulator CtrA in Caulobacter crescentus. J. Bacteriol. 192:539–52 [Google Scholar]
  6. Battesti A, Gottesman S. 6.  2013. Roles of adaptor proteins in regulation of bacterial proteolysis. Curr. Opin. Microbiol. 16:140–47 [Google Scholar]
  7. Battesti A, Hoskins JR, Tong S, Milanesio P, Mann JM. 7.  et al. 2013. Anti-adaptors provide multiple modes for regulation of the RssB adaptor protein. Genes Dev 27:2722–35 [Google Scholar]
  8. Beaufay F, Coppine J, Mayard A, Laloux G, De Bolle X, Hallez R. 8.  2015. A NAD-dependent glutamate dehydrogenase coordinates metabolism with cell division in Caulobacter crescentus. EMBO J 34:1786–800 [Google Scholar]
  9. Becker G, Klauck E, Hengge-Aronis R. 9.  1999. Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. PNAS 96:6439–44 [Google Scholar]
  10. Bezawork-Geleta A, Brodie EJ, Dougan DA, Truscott KN. 10.  2015. LON is the master protease that protects against protein aggregation in human mitochondria through direct degradation of misfolded proteins. Sci. Rep. 5:17397 [Google Scholar]
  11. Bhat NH, Vass RH, Stoddard PR, Shin DK, Chien P. 11.  2013. Identification of ClpP substrates in Caulobacter crescentus reveals a role for regulated proteolysis in bacterial development. Mol. Microbiol. 88:1083–92 [Google Scholar]
  12. Biondi EG, Reisinger SJ, Skerker JM, Arif M, Perchuk BS. 12.  et al. 2006. Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444:899–904 [Google Scholar]
  13. Bolon DN, Wah DA, Hersch GL, Baker TA, Sauer RT. 13.  2004. Bivalent tethering of SspB to ClpXP is required for efficient substrate delivery: a protein-design study. Mol. Cell 13:443–49 [Google Scholar]
  14. Bougdour A, Wickner S, Gottesman S. 14.  2006. Modulating RssB activity: IraP, a novel regulator of σS stability in Escherichia coli. Genes Dev 20:884–97 [Google Scholar]
  15. Brilli M, Fondi M, Fani R, Mengoni A, Ferri L. 15.  et al. 2010. The diversity and evolution of cell cycle regulation in α-proteobacteria: a comparative genomic analysis. BMC Syst. Biol. 4:52 [Google Scholar]
  16. Butler SM, Festa RA, Pearce MJ, Darwin KH. 16.  2006. Self-compartmentalized bacterial proteases and pathogenesis. Mol. Microbiol. 60:553–62 [Google Scholar]
  17. Chan CM, Garg S, Lin AA, Zuber P. 17.  2012. Geobacillus thermodenitrificans YjbH recognizes the C-terminal end of Bacillus subtilis Spx to accelerate Spx proteolysis by ClpXP. Microbiology 158:1268–78 [Google Scholar]
  18. Chan CM, Hahn E, Zuber P. 18.  2014. Adaptor bypass mutations of Bacillus subtilis Spx suggest a mechanism for YjbH-enhanced proteolysis of the regulator Spx by ClpXP. Mol. Microbiol. 93:426–38 [Google Scholar]
  19. Chen YE, Tsokos CG, Biondi EG, Perchuk BS, Laub MT. 19.  2009. Dynamics of two phosphorelays controlling cell cycle progression in Caulobacter crescentus. J. Bacteriol. 191:7417–29 [Google Scholar]
  20. Chien P, Grant RA, Sauer RT, Baker TA. 20.  2007. Structure and substrate specificity of an SspB ortholog: design implications for AAA+ adaptors. Structure 15:1296–305 [Google Scholar]
  21. Chien P, Perchuk BS, Laub MT, Sauer RT, Baker TA. 21.  2007. Direct and adaptor-mediated substrate recognition by an essential AAA+ protease. PNAS 104:6590–95 [Google Scholar]
  22. Chowdhury T, Chien P, Ebrahim S, Sauer RT, Baker TA. 22.  2010. Versatile modes of peptide recognition by the ClpX N domain mediate alternative adaptor-binding specificities in different bacterial species. Protein Sci 19:242–54 [Google Scholar]
  23. Collier J. 23.  2016. Cell cycle control in Alphaproteobacteria. Curr. Opin. Microbiol. 30:107–13 [Google Scholar]
  24. Collier J, Murray SR, Shapiro L. 24.  2006. DnaA couples DNA replication and the expression of two cell cycle master regulators. EMBO J 25:346–56 [Google Scholar]
  25. Collier JL, Grossman AR. 25.  1994. A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039–47 [Google Scholar]
  26. Cordova JC, Olivares AO, Shin Y, Stinson BM, Calmat S. 26.  et al. 2014. Stochastic but highly coordinated protein unfolding and translocation by the ClpXP proteolytic machine. Cell 158:647–58 [Google Scholar]
  27. Curtis PD, Brun YV. 27.  2014. Identification of essential alphaproteobacterial genes reveals operational variability in conserved developmental and cell cycle systems. Mol. Microbiol. 93:713–35 [Google Scholar]
  28. Davis NJ, Cohen Y, Sanselicio S, Fumeaux C, Ozaki S. 28.  et al. 2013. De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle. Genes Dev 27:2049–62 [Google Scholar]
  29. Domian IJ, Quon KC, Shapiro L. 29.  1997. Cell type–specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90:415–24 [Google Scholar]
  30. Dougan DA, Reid BG, Horwich AL, Bukau B. 30.  2002. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell 9:673–83 [Google Scholar]
  31. Dougan DA, Weber-Ban E, Bukau B. 31.  2003. Targeted delivery of an ssrA-tagged substrate by the adaptor protein SspB to its cognate AAA+ protein ClpX. Mol. Cell 12:373–80 [Google Scholar]
  32. Dubnau D. 32.  1991. Genetic competence in Bacillus subtilis. Microbiol. Rev. 55:395–424 [Google Scholar]
  33. Duerig A, Abel S, Folcher M, Nicollier M, Schwede T. 33.  et al. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23:93–104 [Google Scholar]
  34. Ebersbach G, Briegel A, Jensen GJ, Jacobs-Wagner C. 34.  2008. A self-associating protein critical for chromosome attachment, division, and polar organization in Caulobacter. Cell 134:956–68 [Google Scholar]
  35. Farrell CM, Baker TA, Sauer RT. 35.  2007. Altered specificity of a AAA+ protease. Mol. Cell 25:161–66 [Google Scholar]
  36. Feaga HA, Viollier PH, Keiler KC. 36.  2014. Release of nonstop ribosomes is essential. mBio 5:e01916 [Google Scholar]
  37. Fischer B, Rummel G, Aldridge P, Jenal U. 37.  2002. The FtsH protease is involved in development, stress response and heat shock control in Caulobacter crescentus. Mol. Microbiol. 44:461–78 [Google Scholar]
  38. Flynn JM, Levchenko I, Sauer RT, Baker TA. 38.  2004. Modulating substrate choice: The SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev 18:2292–301 [Google Scholar]
  39. Flynn JM, Levchenko I, Seidel M, Wickner SH, Sauer RT, Baker TA. 39.  2001. Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. PNAS 98:10584–89 [Google Scholar]
  40. Garg SK, Kommineni S, Henslee L, Zhang Y, Zuber P. 40.  2009. The YjbH protein of Bacillus subtilis enhances ClpXP-catalyzed proteolysis of Spx. J. Bacteriol. 191:1268–77 [Google Scholar]
  41. Gerth U, Kruger E, Derre I, Msadek T, Hecker M. 41.  1998. Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol. Microbiol. 28:787–802 [Google Scholar]
  42. Ghelardi E, Salvetti S, Ceragioli M, Gueye SA, Celandroni F, Senesi S. 42.  2012. Contribution of surfactin and SwrA to flagellin expression, swimming, and surface motility in Bacillus subtilis. Appl. Environ. Microbiol. 78:6540–44 [Google Scholar]
  43. Goldberg AL. 43.  1972. Degradation of abnormal proteins in Escherichia coli (protein breakdown-protein structure-mistranslation-amino acid analogs-puromycin). PNAS 69:422–26 [Google Scholar]
  44. Gora KG, Cantin A, Wohlever M, Joshi KK, Perchuk BS. 44.  et al. 2013. Regulated proteolysis of a transcription factor complex is critical to cell cycle progression in Caulobacter crescentus. Mol. Microbiol. 87:1277–89 [Google Scholar]
  45. Gora KG, Tsokos CG, Chen YE, Srinivasan BS, Perchuk BS, Laub MT. 45.  2010. A cell-type–specific protein-protein interaction modulates transcriptional activity of a master regulator in Caulobacter crescentus. Mol. Cell 39:455–67 [Google Scholar]
  46. Gorbatyuk B, Marczynski GT. 46.  2005. Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus. Mol. Microbiol. 55:1233–45 [Google Scholar]
  47. Gottesman S, Roche E, Zhou Y, Sauer RT. 47.  1998. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the ssrA-tagging system. Genes Dev 12:1338–47 [Google Scholar]
  48. Grunenfelder B, Rummel G, Vohradsky J, Roder D, Langen H, Jenal U. 48.  2001. Proteomic analysis of the bacterial cell cycle. PNAS 98:4681–86 [Google Scholar]
  49. Grunenfelder B, Tawfilis S, Gehrig S, ØSterås M, Eglin D, Jenal U. 49.  2004. Identification of the protease and the turnover signal responsible for cell cycle–dependent degradation of the Caulobacter FliF motor protein. J. Bacteriol. 186:4960–71 [Google Scholar]
  50. Gur E. 50.  2013. The Lon AAA+ protease. Subcell. Biochem. 66:35–51 [Google Scholar]
  51. Gur E, Sauer RT. 51.  2008. Recognition of misfolded proteins by Lon, a AAA+ protease. Genes Dev 22:2267–77 [Google Scholar]
  52. Gur E, Sauer RT. 52.  2009. Degrons in protein substrates program the speed and operating efficiency of the AAA+ Lon proteolytic machine. PNAS 106:18503–8 [Google Scholar]
  53. Haakonsen DL, Yuan AH, Laub MT. 53.  2015. The bacterial cell cycle regulator GcrA is a σ70 cofactor that drives gene expression from a subset of methylated promoters. Genes Dev 29:2272–86 [Google Scholar]
  54. Hengge R. 54.  2009. Proteolysis of σS (RpoS) and the general stress response in Escherichia coli. Res. Microbiol. 160:667–76 [Google Scholar]
  55. Higgins D, Dworkin J. 55.  2012. Recent progress in Bacillus subtilis sporulation. FEMS Microbiol. Rev. 36:131–48 [Google Scholar]
  56. Ingmer H, Brondsted L. 56.  2009. Proteases in bacterial pathogenesis. Res. Microbiol. 160:704–10 [Google Scholar]
  57. Iniesta AA, Hillson NJ, Shapiro L. 57.  2010. Polar remodeling and histidine kinase activation, which is essential for Caulobacter cell cycle progression, are dependent on DNA replication initiation. J. Bacteriol. 192:3893–902 [Google Scholar]
  58. Iniesta AA, McGrath PT, Reisenauer A, McAdams HH, Shapiro L. 58.  2006. A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. PNAS 103:10935–40 [Google Scholar]
  59. Iniesta AA, Shapiro L. 59.  2008. A bacterial control circuit integrates polar localization and proteolysis of key regulatory proteins with a phospho-signaling cascade. PNAS 105:16602–7 [Google Scholar]
  60. Jacobs C, Ausmees N, Cordwell SJ, Shapiro L, Laub MT. 60.  2003. Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol. Microbiol. 47:1279–90 [Google Scholar]
  61. Jacobs C, Domian IJ, Maddock JR, Shapiro L. 61.  1999. Cell cycle–dependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division. Cell 97:111–20 [Google Scholar]
  62. Jenal U, Fuchs T. 62.  1998. An essential protease involved in bacterial cell-cycle control. EMBO J 17:5658–69 [Google Scholar]
  63. Jonas K, Liu J, Chien P, Laub MT. 63.  2013. Proteotoxic stress induces a cell-cycle arrest by stimulating Lon to degrade the replication initiator DnaA. Cell 154:623–36 [Google Scholar]
  64. Joshi KK, Berge M, Radhakrishnan SK, Viollier PH, Chien P. 64.  2015. An adaptor hierarchy regulates proteolysis during a bacterial cell cycle. Cell 163:419–31 [Google Scholar]
  65. Kearns DB. 65.  2010. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 8:634–44 [Google Scholar]
  66. Keiler KC. 66.  2015. Mechanisms of ribosome rescue in bacteria. Nat. Rev. Microbiol. 13:285–97 [Google Scholar]
  67. Keiler KC, Shapiro L. 67.  2003. tmRNA in Caulobacter crescentus is cell cycle regulated by temporally controlled transcription and RNA degradation. J. Bacteriol. 185:1825–30 [Google Scholar]
  68. Keiler KC, Shapiro L. 68.  2003. tmRNA is required for correct timing of DNA replication in Caulobacter crescentus. J. Bacteriol. 185:573–80 [Google Scholar]
  69. Keiler KC, Shapiro L, Williams KP. 69.  2000. tmRNAs that encode proteolysis-inducing tags are found in all known bacterial genomes: a two-piece tmRNA functions in Caulobacter. PNAS 97:7778–83 [Google Scholar]
  70. Keiler KC, Waller PR, Sauer RT. 70.  1996. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271:990–93 [Google Scholar]
  71. Kelly AJ, Sackett MJ, Din N, Quardokus E, Brun YV. 71.  1998. Cell cycle–dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev 12:880–93 [Google Scholar]
  72. Kirstein J, Moliere N, Dougan DA, Turgay K. 72.  2009. Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat. Rev. Microbiol. 7:589–99 [Google Scholar]
  73. Kobayashi H, De Nisco NJ, Chien P, Simmons LA, Walker GC. 73.  2009. Sinorhizobium meliloti CpdR1 is critical for co-ordinating cell cycle progression and the symbiotic chronic infection. Mol. Microbiol. 73:586–600 [Google Scholar]
  74. Lau J, Hernandez-Alicea L, Vass RH, Chien P. 74.  2015. A phosphosignaling adaptor primes the AAA+ protease ClpXP to drive cell cycle–regulated proteolysis. Mol. Cell 59:104–16 [Google Scholar]
  75. Lesley JA, Shapiro L. 75.  2008. SpoT regulates DnaA stability and initiation of DNA replication in carbon-starved Caulobacter crescentus. J. Bacteriol. 190:6867–80 [Google Scholar]
  76. Leslie DJ, Heinen C, Schramm FD, Thuring M, Aakre CD. 76.  et al. 2015. Nutritional control of DNA replication initiation through the proteolysis and regulated translation of DnaA. PLOS Genet 11:e1005342 [Google Scholar]
  77. Lessner FH, Venters BJ, Keiler KC. 77.  2007. Proteolytic adaptor for transfer-messenger RNA-tagged proteins from α-proteobacteria. J. Bacteriol. 189:272–75 [Google Scholar]
  78. Levchenko I, Seidel M, Sauer RT, Baker TA. 78.  2000. A specificity-enhancing factor for the ClpXP degradation machine. Science 289:2354–56 [Google Scholar]
  79. Liu J, Francis LI, Jonas K, Laub MT, Chien P. 78a.  2016. ClpAP is an auxiliary protease for DnaA degradation in Caulobacter crecentus. Mol. Microbiol. In press. doi: 10.1111/mmi13537 [Google Scholar]
  80. Lori C, Ozaki S, Steiner S, Bohm R, Abel S. 79.  et al. 2015. Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication. Nature 523:236–39 [Google Scholar]
  81. Lu B, Lee J, Nie X, Li M, Morozov YI. 80.  et al. 2013. Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA+ Lon protease. Mol. Cell 49:121–32 [Google Scholar]
  82. Martin ME, Trimble MJ, Brun YV. 81.  2004. Cell cycle–dependent abundance, stability and localization of FtsA and FtsQ in Caulobacter crescentus. Mol. Microbiol. 54:60–74 [Google Scholar]
  83. Maurizi MR, Clark WP, Katayama Y, Rudikoff S, Pumphrey J. 82.  et al. 1990. Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J. Biol. Chem. 265:12536–45 [Google Scholar]
  84. Maurizi MR, Trisler P, Gottesman S. 83.  1985. Insertional mutagenesis of the lon gene in Escherichia coli: lon is dispensable. J. Bacteriol. 164:1124–35 [Google Scholar]
  85. McGrath PT, Iniesta AA, Ryan KR, Shapiro L, McAdams HH. 84.  2006. A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124:535–47 [Google Scholar]
  86. Mettert EL, Kiley PJ. 85.  2005. ClpXP-dependent proteolysis of FNR upon loss of its O2-sensing [4Fe-4S] cluster. J. Mol. Biol. 354:220–32 [Google Scholar]
  87. Modell JW, Hopkins AC, Laub MT. 86.  2011. A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW. Genes Dev 25:1328–43 [Google Scholar]
  88. Moliere N, Hossmann J, Schafer H, Turgay K. 87.  2016. Role of Hsp100/Clp protease complexes in controlling the regulation of motility in Bacillus subtilis. Front. Microbiol. 7:315 [Google Scholar]
  89. Msadek T, Dartois V, Kunst F, Herbaud ML, Denizot F, Rapoport G. 88.  1998. ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol. Microbiol. 27:899–914 [Google Scholar]
  90. Mukherjee S, Bree AC, Liu J, Patrick JE, Chien P, Kearns DB. 89.  2015. Adaptor-mediated Lon proteolysis restricts Bacillus subtilis hyperflagellation. PNAS 112:250–55 [Google Scholar]
  91. Narayanan S, Janakiraman B, Kumar L, Radhakrishnan SK. 90.  2015. A cell cycle–controlled redox switch regulates the topoisomerase IV activity. Genes Dev 29:1175–87 [Google Scholar]
  92. Nishimura K, Apitz J, Friso G, Kim J, Ponnala L. 91.  et al. 2015. Discovery of a unique Clp component, ClpF, in chloroplasts: A proposed binary ClpF-ClpS1 adaptor complex functions in substrate recognition and delivery. Plant Cell 27:2677–91 [Google Scholar]
  93. Ogura M, Liu L, Lacelle M, Nakano MM, Zuber P. 92.  1999. Mutational analysis of ComS: evidence for the interaction of ComS and MecA in the regulation of competence development in Bacillus subtilis. Mol. Microbiol. 32:799–812 [Google Scholar]
  94. Olivares AO, Baker TA, Sauer RT. 93.  2016. Mechanistic insights into bacterial AAA+ proteases and protein-remodelling machines. Nat. Rev. Microbiol. 14:33–44 [Google Scholar]
  95. Olivares AO, Nager AR, Iosefson O, Sauer RT, Baker TA. 94.  2014. Mechanochemical basis of protein degradation by a double-ring AAA+ machine. Nat. Struct. Mol. Biol. 21:871–75 [Google Scholar]
  96. Ozaki S, Schalch-Moser A, Zumthor L, Manfredi P, Ebbensgaard A. 95.  et al. 2014. Activation and polar sequestration of PopA, a c-di-GMP effector protein involved in Caulobacter crescentus cell cycle control. Mol. Microbiol. 94:580–94 [Google Scholar]
  97. Persuh M, Turgay K, Mandic-Mulec I, Dubnau D. 96.  1999. The N- and C-terminal domains of MecA recognize different partners in the competence molecular switch. Mol. Microbiol. 33:886–94 [Google Scholar]
  98. Pierechod M, Nowak A, Saari A, Purta E, Bujnicki JM, Konieczny I. 97.  2009. Conformation of a plasmid replication initiator protein affects its proteolysis by ClpXP system. Protein Sci 18:637–49 [Google Scholar]
  99. Pini F, De Nisco NJ, Ferri L, Penterman J, Fioravanti A. 98.  et al. 2015. Cell cycle control by the master regulator CtrA in Sinorhizobium meliloti. PLOS Genet 11:e1005232 [Google Scholar]
  100. Potocka I, Thein M, ØSterås M, Jenal U, Alley MR. 99.  2002. Degradation of a Caulobacter soluble cytoplasmic chemoreceptor is ClpX dependent. J. Bacteriol. 184:6635–41 [Google Scholar]
  101. Pratt LA, Silhavy TJ. 100.  1996. The response regulator SprE controls the stability of RpoS. PNAS 93:2488–92 [Google Scholar]
  102. Pruteanu M, Neher SB, Baker TA. 101.  2007. Ligand-controlled proteolysis of the Escherichia coli transcriptional regulator ZntR. J. Bacteriol. 189:3017–25 [Google Scholar]
  103. Quon KC, Marczynski GT, Shapiro L. 102.  1996. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84:83–93 [Google Scholar]
  104. Radhakrishnan SK, Pritchard S, Viollier PH. 103.  2010. Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog. Dev. Cell 18:90–101 [Google Scholar]
  105. Raju RM, Jedrychowski MP, Wei JR, Pinkham JT, Park AS. 104.  et al. 2014. Post-translational regulation via Clp protease is critical for survival of Mycobacterium tuberculosis. PLOS Pathog 10:e1003994 [Google Scholar]
  106. Reisinger SJ, Huntwork S, Viollier PH, Ryan KR. 105.  2007. DivL performs critical cell cycle functions in Caulobacter crescentus independent of kinase activity. J. Bacteriol. 189:8308–20 [Google Scholar]
  107. Rood KL, Clark NE, Stoddard PR, Garman SC, Chien P. 106.  2012. Adaptor-dependent degradation of a cell-cycle regulator uses a unique substrate architecture. Structure 20:1223–32 [Google Scholar]
  108. Rudyak SG, Shrader TE. 107.  2000. Polypeptide stimulators of the Ms-Lon protease. Protein Sci 9:1810–17 [Google Scholar]
  109. Ruvolo MV, Mach KE, Burkholder WF. 108.  2006. Proteolysis of the replication checkpoint protein Sda is necessary for the efficient initiation of sporulation after transient replication stress in Bacillus subtilis. Mol. Microbiol. 60:1490–508 [Google Scholar]
  110. Sanselicio S, Berge M, Theraulaz L, Radhakrishnan SK, Viollier PH. 109.  2015. Topological control of the Caulobacter cell cycle circuitry by a polarized single-domain PAS protein. Nat. Commun. 6:7005 [Google Scholar]
  111. Schallies KB, Sadowski C, Meng J, Chien P, Gibson KE. 110.  2015. Sinorhizobium meliloti CtrA stability is regulated in a CbrA-dependent manner that is influenced by CpdR1. J. Bacteriol. 197:2139–49 [Google Scholar]
  112. Schmidt R, Decatur AL, Rather PN, Moran CP Jr., Losick R. 111.  1994. Bacillus subtilis lon protease prevents inappropriate transcription of genes under the control of the sporulation transcription factor sigma G. J. Bacteriol. 176:6528–37 [Google Scholar]
  113. Sen M, Maillard RA, Nyquist K, Rodriguez-Aliaga P, Presse S. 112.  et al. 2013. The ClpXP protease unfolds substrates using a constant rate of pulling but different gears. Cell 155:636–46 [Google Scholar]
  114. Sendersky E, Kozer N, Levi M, Garini Y, Shav-Tal Y, Schwarz R. 113.  2014. The proteolysis adaptor, NblA, initiates protein pigment degradation by interacting with the cyanobacterial light-harvesting complexes. Plant J 79:118–26 [Google Scholar]
  115. Shah IM, Wolf RE Jr. 114.  2006. Inhibition of Lon-dependent degradation of the Escherichia coli transcription activator SoxS by interaction with “soxbox” DNA or RNA polymerase. Mol. Microbiol. 60:199–208 [Google Scholar]
  116. Smith SC, Joshi KK, Zik JJ, Trinh K, Kamajaya A. 115.  et al. 2014. Cell cycle–dependent adaptor complex for ClpXP-mediated proteolysis directly integrates phosphorylation and second messenger signals. PNAS 111:14229–34 [Google Scholar]
  117. Studemann A, Noirclerc-Savoye M, Klauck E, Becker G, Schneider D, Hengge R. 116.  2003. Sequential recognition of two distinct sites in σS by the proteolytic targeting factor RssB and ClpX. EMBO J 22:4111–20 [Google Scholar]
  118. Tan IS, Weiss CA, Popham DL, Ramamurthi KS. 117.  2015. A quality-control mechanism removes unfit cells from a population of sporulating bacteria. Dev. Cell 34:682–93 [Google Scholar]
  119. Tan MH, Kozdon JB, Shen X, Shapiro L, McAdams HH. 118.  2010. An essential transcription factor, SciP, enhances robustness of Caulobacter cell cycle regulation. PNAS 107:18985–90 [Google Scholar]
  120. Taylor JA, Wilbur JD, Smith SC, Ryan KR. 119.  2009. Mutations that alter RcdA surface residues decouple protein localization and CtrA proteolysis in Caulobacter crescentus. J. Mol. Biol. 394:46–60 [Google Scholar]
  121. Tsai JW, Alley MR. 120.  2001. Proteolysis of the Caulobacter McpA chemoreceptor is cell cycle regulated by a ClpX-dependent pathway. J. Bacteriol. 183:5001–7 [Google Scholar]
  122. Tsokos CG, Laub MT. 121.  2012. Polarity and cell fate asymmetry in Caulobacter crescentus. Curr. Opin. Microbiol. 15:744–50 [Google Scholar]
  123. Tsokos CG, Perchuk BS, Laub MT. 122.  2011. A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev. Cell 20:329–41 [Google Scholar]
  124. Turgay K, Hahn J, Burghoorn J, Dubnau D. 123.  1998. Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. EMBO J 17:6730–38 [Google Scholar]
  125. Vass RH, Chien P. 124.  2013. Critical clamp loader processing by an essential AAA+ protease in Caulobacter crescentus. PNAS 110:18138–43 [Google Scholar]
  126. Wah DA, Levchenko I, Rieckhof GE, Bolon DN, Baker TA, Sauer RT. 125.  2003. Flexible linkers leash the substrate binding domain of SspB to a peptide module that stabilizes delivery complexes with the AAA+ ClpXP protease. Mol. Cell 12:355–63 [Google Scholar]
  127. Watabe S, Hara M, Yamamoto M, Yoshida M, Yamamoto Y, Takahashi SY. 126.  2001. Activation of mitochondrial ATP-dependent protease by peptides and proteins. Tohoku J. Exp. Med. 195:153–61 [Google Scholar]
  128. Waxman L, Goldberg AL. 127.  1982. Protease La from Escherichia coli hydrolyzes ATP and proteins in a linked fashion. PNAS 79:4883–87 [Google Scholar]
  129. Waxman L, Goldberg AL. 128.  1986. Selectivity of intracellular proteolysis: Protein substrates activate the ATP-dependent protease (La). Science 232:500–3 [Google Scholar]
  130. Willett JW, Herrou J, Briegel A, Rotskoff G, Crosson S. 129.  2015. Structural asymmetry in a conserved signaling system that regulates division, replication, and virulence of an intracellular pathogen. PNAS 112:E3709–18 [Google Scholar]
  131. Williams B, Bhat N, Chien P, Shapiro L. 130.  2014. ClpXP and ClpAP proteolytic activity on divisome substrates is differentially regulated following the Caulobacter asymmetric cell division. Mol. Microbiol. 93:853–66 [Google Scholar]
  132. Wright R, Stephens C, Zweiger G, Shapiro L, Alley MR. 131.  1996. Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation. Genes Dev 10:1532–42 [Google Scholar]
  133. Zhou Y, Gottesman S, Hoskins JR, Maurizi MR, Wickner S. 132.  2001. The RssB response regulator directly targets σS for degradation by ClpXP. Genes Dev 15:627–37 [Google Scholar]
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