The proton-motive force is required for translocation of CDI toxins across the inner membrane of target bacteria

Molecular Microbiology

Volumn 94, Issue 2, 2014, Pages 466-481

  Ruhe, Zachary C ^a   Nguyen, Josephine Y ^a   Beck, Christina M ^a   Low, David A ^a   Hayes, Christopher S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL TOXIN; COLICIN; CONTACT DEPENDENT GROWTH INHIBITION TOXIN; UNCLASSIFIED DRUG; CDIA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; MEMBRANE PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIAL TRANSLOCATION; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CONTROLLED STUDY; CYTOPLASM; MEMBRANE TRANSPORT; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; PROTON MOTIVE FORCE; TARGET ORGANISM; CELL MEMBRANE; METABOLISM;

BACTERIAL TOXINS; CELL MEMBRANE; COLICINS; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PROTEIN TRANSPORT; PROTON-MOTIVE FORCE;

EID: 84916602414     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12779     Document Type: Article

References (67)

1. Akiyama, Y. (2002) Proton-motive force stimulates the proteolytic activity of FtsH, a membrane-bound ATP-dependent protease in Escherichia coli. Proc Natl Acad Sci USA 99: 8066-8071.
2. Aoki, S.K., Pamma, R., Hernday, A.D., Bickham, J.E., Braaten, B.A., and Low, D.A. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309: 1245-1248.
3. Aoki, S.K., Malinverni, J.C., Jacoby, K., Thomas, B., Pamma, R., Trinh, B.N., etal. (2008) Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 70: 323-340.
4. Aoki, S.K., Webb, J.S., Braaten, B.A., and Low, D.A. (2009) Contact-dependent growth inhibition causes reversible metabolic downregulation in Escherichia coli. J Bacteriol 191: 1777-1786.
5. Aoki, S.K., Diner, E.J., de Roodenbeke, C.T., Burgess, B.R., Poole, S.J., Braaten, B.A., etal. (2010) A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468: 439-442.
6. Arenas, J., Schipper, K., van Ulsen, P., van der Ende, A., and Tommassen, J. (2013) Domain exchange at the 3' end of the gene encoding the fratricide meningococcal two-partner secretion protein A. BMC Genomics 14: 622.
7. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006 0008.
8. Beck, C.M., Morse, R.P., Cunningham, D.A., Iniguez, A., Low, D.A., Goulding, C.W., and Hayes, C.S. (2014) CdiA from enterobacter cloacae delivers a toxic ribosomal RNase into target bacteria. Structure 22: 707-718.
9. Beckwith, J.R., and Signer, E.R. (1966) Transposition of the lac region of Escherichia coli. I. Inversion of the lac operon and transduction of lac by phi80. J Mol Biol 19: 254-265.
10. Bourdineaud, J.P., Boulanger, P., Lazdunski, C., and Letellier, L. (1990) In vivo properties of colicin A: channel activity is voltage dependent but translocation may be voltage independent. Proc Natl Acad Sci USA 87: 1037-1041.
11. Braun, V., Frenz, J., Hantke, K., and Schaller, K. (1980) Penetration of colicin M into cells of Escherichia coli. J Bacteriol 142: 162-168.
12. Buchanan, S.K., Smith, B.S., Venkatramani, L., Xia, D., Esser, L., Palnitkar, M., etal. (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat Struct Biol 6: 56-63.
13. Cascales, E., Buchanan, S.K., Duche, D., Kleanthous, C., Lloubes, R., Postle, K., etal. (2007) Colicin biology. Microbiol Mol Biol Rev 71: 158-229.
14. Chauleau, M., Mora, L., Serba, J., and de Zamaroczy, M. (2011) FtsH-dependent processing of RNase colicins D and E3 means that only the cytotoxic domains are imported into the cytoplasm. J Biol Chem 286: 29397-29407.
15. Cherepanov, P.P., and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14.
16. Darwin, A.J. (2013) Stress relief during host infection: the phage shock protein response supports bacterial virulence in various ways. PLoS Pathog 9: e1003388.
17. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
18. Datta, S., Costantino, N., and Court, D.L. (2006) A set of recombineering plasmids for gram-negative bacteria. Gene 379: 109-115.
19. Devanathan, S., and Postle, K. (2007) Studies on colicin B translocation: FepA is gated by TonB. Mol Microbiol 65: 441-453.
20. Diner, E.J., Beck, C.M., Webb, J.S., Low, D.A., and Hayes, C.S. (2012) Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI). Genes Dev 26: 515-525.
21. Garza-Sánchez, F., Janssen, B.D., and Hayes, C.S. (2006) Prolyl-tRNA(Pro) in the A-site of SecM-arrested ribosomes inhibits the recruitment of transfer-messenger RNA. J Biol Chem 281: 34258-34268.
22. Garza-Sánchez, F., Gin, J.G., and Hayes, C.S. (2008) Amino acid starvation and colicin D treatment induce A-site mRNA cleavage in Escherichia coli. J Mol Biol 378: 505-519.
23. Gentle, I., Gabriel, K., Beech, P., Waller, R., and Lithgow, T. (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164: 19-24.
24. Goemaere, E.L., Cascales, E., and Lloubes, R. (2007) Mutational analyses define helix organization and key residues of a bacterial membrane energy-transducing complex. J Mol Biol 366: 1424-1436.
25. Hayes, C.S., and Sauer, R.T. (2003) Cleavage of the A site mRNA codon during ribosome pausing provides a mechanism for translational quality control. Mol Cell 12: 903-911.
26. Hayes, C.S., Aoki, S.K., and Low, D.A. (2010) Bacterial contact-dependent delivery systems. Annu Rev Genet 44: 71-90.
27. Housden, N.G., Wojdyla, J.A., Korczynska, J., Grishkovskaya, I., Kirkpatrick, N., Brzozowski, A.M., and Kleanthous, C. (2010) Directed epitope delivery across the Escherichia coli outer membrane through the porin OmpF. Proc Natl Acad Sci USA 107: 21412-21417.
28. Housden, N.G., Hopper, J.T., Lukoyanova, N., Rodriguez-Larrea, D., Wojdyla, J.A., Klein, A., etal. (2013) Intrinsically disordered protein threads through the bacterial outer-membrane porin OmpF. Science 340: 1570-1574.
29. Jacob-Dubuisson, F., Guerin, J., Baelen, S., and Clantin, B. (2013) Two-partner secretion: as simple as it sounds? Res Microbiol 164: 583-595.
30. Jakes, K.S., and Cramer, W.A. (2012) Border crossings: colicins and transporters. Annu Rev Genet 46: 209-231.
31. Jakes, K.S., and Finkelstein, A. (2010) The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol Microbiol 75: 567-578.
32. Jetten, A.M., and Jetten, M.E. (1975) Energy requirement for the initiation of colicin action in Escherichia coli. Biochim Biophys Acta 387: 12-22.
33. Jiang, X., Payne, M.A., Cao, Z., Foster, S.B., Feix, J.B., Newton, S.M., and Klebba, P.E. (1997) Ligand-specific opening of a gated-porin channel in the outer membrane of living bacteria. Science 276: 1261-1264.
34. Kajava, A.V., Cheng, N., Cleaver, R., Kessel, M., Simon, M.N., Willery, E., etal. (2001) Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42: 279-292.
35. Kim, S., Malinverni, J.C., Sliz, P., Silhavy, T.J., Harrison, S.C., and Kahne, D. (2007) Structure and function of an essential component of the outer membrane protein assembly machine. Science 317: 961-964.
36. Leonard-Rivera, M., and Misra, R. (2012) Conserved residues of the putative L6 loop of Escherichia coli BamA play a critical role in the assembly of beta-barrel outer membrane proteins, including that of BamA itself. J Bacteriol 194: 4662-4668.
37. Levchenko, I., Seidel, M., Sauer, R.T., and Baker, T.A. (2000) A specificity-enhancing factor for the ClpXP degradation machine. Science 289: 2354-2356.
38. Ma, D., Cook, D.N., Alberti, M., Pon, N.G., Nikaido, H., and Hearst, J.E. (1995) Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol Microbiol 16: 45-55.
39. Maloney, P.C., Kashket, E.R., and Wilson, T.H. (1974) A protonmotive force drives ATP synthesis in bacteria. Proc Natl Acad Sci USA 71: 3896-3900.
40. Manson, M.D., Tedesco, P., Berg, H.C., Harold, F.M., and Van der Drift, C. (1977) A protonmotive force drives bacterial flagella. Proc Natl Acad Sci USA 74: 3060-3064.
41. Matsuzawa, H., Ushiyama, S., Koyama, Y., and Ohta, T. (1984) Escherichia coli K-12 tolZ mutants tolerant to colicins E2, E3, D, Ia, and Ib: defect in generation of the electrochemical proton gradient. J Bacteriol 160: 733-739.
42. Morse, R.P., Nikolakakis, K.C., Willett, J.L., Gerrick, E., Low, D.A., Hayes, C.S., and Goulding, C.W. (2012) Structural basis of toxicity and immunity in contact-dependent growth inhibition (CDI) systems. Proc Natl Acad Sci USA 109: 21480-21485.
43. Mosbahi, K., Lemaitre, C., Keeble, A.H., Mobasheri, H., Morel, B., James, R., etal. (2002) The cytotoxic domain of colicin E9 is a channel-forming endonuclease. Nat Struct Biol 9: 476-484.
44. Mosbahi, K., Walker, D., Lea, E., Moore, G.R., James, R., and Kleanthous, C. (2004) Destabilization of the colicin E9 Endonuclease domain by interaction with negatively charged phospholipids: implications for colicin translocation into bacteria. J Biol Chem 279: 22145-22151.
45. Mosbahi, K., Walker, D., James, R., Moore, G.R., and Kleanthous, C. (2006) Global structural rearrangement of the cell penetrating ribonuclease colicin E3 on interaction with phospholipid membranes. Protein Sci 15: 620-627.
46. Nikaido, H., and Zgurskaya, H.I. (2001) AcrAB and related multidrug efflux pumps of Escherichia coli. J Mol Microbiol Biotechnol 3: 215-218.
47. Nikolakakis, K., Amber, S., Wilbur, J.S., Diner, E.J., Aoki, S.K., Poole, S.J., etal. (2012) The toxin/immunity network of Burkholderia pseudomallei contact-dependent growth inhibition (CDI) systems. Mol Microbiol 84: 516-529.
48. Noinaj, N., Kuszak, A.J., Gumbart, J.C., Lukacik, P., Chang, H., Easley, N.C., etal. (2013) Structural insight into the biogenesis of beta-barrel membrane proteins. Nature 501: 385-390.
49. Ogawa, T., Tomita, K., Ueda, T., Watanabe, K., Uozumi, T., and Masaki, H. (1999) A cytotoxic ribonuclease targeting specific transfer RNA anticodons. Science 283: 2097-2100.
50. Poole, S.J., Diner, E.J., Aoki, S.K., Braaten, B.A., T'Kint de Roodenbeke, C., Low, D.A., and Hayes, C.S. (2011) Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 7: e1002217.
51. Qu, J.N., Makino, S.I., Adachi, H., Koyama, Y., Akiyama, Y., Ito, K., etal. (1996) The tolZ gene of Escherichia coli is identified as the ftsH gene. J Bacteriol 178: 3457-3461.
52. Reynolds, B.L., and Reeves, P.R. (1963) Some observations on the mode of action of colicin F. Biochem Biophys Res Commun 11: 140-145.
53. Reynolds, B.L., and Reeves, P.R. (1969) Kinetics of adsorption of colicin CA42-E2 and reversal of its bactericidal activity. J Bacteriol 100: 301-309.
54. Rigel, N.W., Ricci, D.P., and Silhavy, T.J. (2013) Conformation-specific labeling of BamA and suppressor analysis suggest a cyclic mechanism for beta-barrel assembly in Escherichia coli. Proc Natl Acad Sci USA 110: 5151-5156.
55. Ruhe, Z.C., Low, D.A., and Hayes, C.S. (2013a) Bacterial contact-dependent growth inhibition. Trends Microbiol 21: 230-237.
56. Ruhe, Z.C., Wallace, A.B., Low, D.A., and Hayes, C.S. (2013b) Receptor polymorphism restricts contact-dependent growth inhibition to members of the same species. MBio 4: e00480-13.
57. Smallwood, C.R., Marco, A.G., Xiao, Q., Trinh, V., Newton, S.M., and Klebba, P.E. (2009) Fluoresceination of FepA during colicin B killing: effects of temperature, toxin and TonB. Mol Microbiol 72: 1171-1180.
58. Thanassi, D.G., Cheng, L.W., and Nikaido, H. (1997) Active efflux of bile salts by Escherichia coli. J Bacteriol 179: 2512-2518.
59. Thomason, L., Court, D.L., Bubunenko, M., Costantino, N., Wilson, H., Datta, S., and Oppenheim, A. (2007) Recombineering: genetic engineering in bacteria using homologous recombination. Curr Protoc Mol Biol Chapter 1: Unit 1 16.
60. Tomita, K., Ogawa, T., Uozumi, T., Watanabe, K., and Masaki, H. (2000) A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proc Natl Acad Sci USA 97: 8278-8283.
61. Vankemmelbeke, M., Zhang, Y., Moore, G.R., Kleanthous, C., Penfold, C.N., and James, R. (2009) Energy-dependent immunity protein release during tol-dependent nuclease colicin translocation. J Biol Chem 284: 18932-18941.
62. Voulhoux, R., Bos, M.P., Geurtsen, J., Mols, M., and Tommassen, J. (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299: 262-265.
63. Walker, D., Mosbahi, K., Vankemmelbeke, M., James, R., and Kleanthous, C. (2007) The role of electrostatics in colicin nuclease domain translocation into bacterial cells. J Biol Chem 282: 31389-31397.
64. Webb, J.S., Nikolakakis, K.C., Willett, J.L., Aoki, S.K., Hayes, C.S., and Low, D.A. (2013) Delivery of CdiA nuclease toxins into target cells during contact-dependent growth inhibition. PLoS ONE 8: e57609.
65. Werner, J., and Misra, R. (2005) YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol Microbiol 57: 1450-1459.
66. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T.J., and Kahne, D. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121: 235-245.
67. Yamashita, E., Zhalnina, M.V., Zakharov, S.D., Sharma, O., and Cramer, W.A. (2008) Crystal structures of the OmpF porin: function in a colicin translocon. EMBO J 27: 2171-2180.