Colicin

From Proteopedia

spinqualitylabelsall models Crystal structure of Colicin Ia, the first colicin to be identified, 1cii. Show:Asymmetric Unit Biological Assembly Drag the structure with the mouse to rotate   Export Animated Image Contents 1 Function 2 Synthesis, Production and Release 3 Targeting and Receptors 4 Colicin Uptake 5 Killing Activities 6 3D structure of Colicin Function Colicins are a type of bacteriocin - peptide and protein antibiotics released by bacteria to kill other bacteria of the same species, in order to provide a competitive advantage for nutrient acquisition [1]. Bacteriocins are named after their species of origin; colicins are so-called because they are produced by E. Coli[2]. Because of their narrow killing spectrum which focuses primarily on the species which has made the peptide (or occasionally closely related species[3]), bacteriocins are important in microbial biodiversity and the stable co-existence of the bacterial populations[4][5]. Colicin peptides are plasmid-encoded. The peptide is released by the cell into the area surrounding it, and then parasitises proteins present in the host cell membrane to translocate across into the host cell. Many protein-protein interactions are involved in the cell entry, and the main system is involved in the grouping of colicins into two families: Group A colicins use the Tol system to enter the host cell, and Group B use the Ton system. Once inside the host cell, the cell killing follows 1st order kinetics - ie one molecule is theoretically sufficient to kill the cell[6]. Colicin-A see Colicin-A Colicin-B forms small, ion-permeable channels. It inhibits the transport of Pro and enhances the transport of methylglucoside[7]. Colicin-D cleaves the anticodon loop of tRNAArg[8] Colicin-E1 binds to TolC and plug channels of Gram-negative bacteria[9] Colicin-E2 and Colicin-E9 bind to BtuB and cleaves the target DNA[10], [11] Colicin-E3 cleaves the ribosome A site[12] Colicin-E5 cleaves tRNA which contain the nucleotide queuosine[13] Colicin-E7 binds to immunity protein 7[14] Colicin-Ia see Colicin-Ia Colicin-M cleaves peptidoglycans by hydrolysing their phosphoester bonds[15] The structure of all colicins, of which over 20 have been identified, follows a 3 domain design: At the N terminus is the Translocation domain (T-): Residues in ColIa. The Receptor binding domain is at the centre of the peptide (R-): Residues in ColIa. The C terminus contains the Cytotoxic domain (C-): Residues in ColIa[16]. The 3 domain structure of all colicins Some colicins exhibit DNase Activity and others TRNase activity. For more details see also Pore Formation Translocation domain H-N-H motif 16s rRNase activity Cloacin DF13. Colicin Immunity Protein Synthesis, Production and Release Synthesis of many colicins is repressed by the LexA protein, which is part of the SOS regulon[17]. The structure of a typical colicin operon, highlighting the 3 proteins encoded together. Targeting and Receptors Colicins vary significantly in the receptors that they target to initiate their uptake. The majority of the group A colicins use the BtuB receptor, which is present on E. coli as a vitamin B12 uptake receptor. Once bound to the receptor, the coiled-coil receptor binding domain unfolds, in an essential step that removes the immunity protein and triggers translocation[18]. Other colicins use other receptors - generally involved in the uptake of small metabolite growth factors. Colicin Uptake Colicins are divided into two groups depending on the method of uptake which they target. Group A colicins use the Tol system to bind to and enter the target cell, and group B use the Ton system. The Tol system consists of 5 proteins - TolA, TolB, TolR, TolQ and Pal[19], and group A proteins using this often recruit a second co-receptor involved in translocation, usually OmpF or TolC, but could be OmpC and PhoE[20]. The Ton system consists of TonB, ExbB and ExbD[21], and no known co-receptor is utilised in translocation[22].It could be possible that Ton-dependent colicins are indiscriminate in use of coreceptors, or that the colicins move down the outside wall of a β barrel protein[23]. It is known that colicins do unfold during translocation, but the peptides resulting from this exceed the diameter of pores formed by any of the molecules mentioned above[24][25]. However, while unfolding does occur, this is not induced by receptor binding in either Tol or Ton dependent colicins[26]. Understanding how the colicins can cross the membrane is highly important, as if this could be targeted and exploited it could be useful for novel therapeutic agents[27]. It is also estimated that a single colicin molecule is sufficient to kill the bacterial cell, following first order kinetics[28]. Killing Activities Colicins kill their target cell through a variety of different methods. The main killing activities are carried out through Pore Formation, DNase Activity and 16s rRNase activity, and some colicins also exhibit tRNase activity. The killing activities carried out by colicins could be used medicinally as an alternative to antibiotics in the case where the specific strain of E. coli can be identified[29], and as potential natural replacements for food preservatives[30]. List of colicins, with their translocation proteins and cytotoxic activity Colicin Group OM Receptor Translocation Proteins Cytotoxic activity Immunity protein Colicin A A BtuB OmpF/TolQRAB Pore-forming Colicin_Immunity_Protein[31] Colicin E1 A BtuB TolC/TolAQ Pore-forming ImmE1[32] Colicin E2 A BtuB OmpF/TolQRAB DNase Im2[33] Colicin E3 A BtuB OmpF/TolQRAB 16s rRNase Im3[34] Colicin E4 A BtuB OmpF/TolQRAB 16s rRNase Im4[35] Colicin E5 A BtuB OmpF/TolQRAB tRNase ImmE5[36] Colicin E6 A BtuB OmpF/TolQRAB 16s rRNase ImmE6[37] Colicin E7 A BtuB OmpF/TolQRAB DNase Im7[38] Colicin E8 A BtuB OmpF/TolQRAB DNase Im8[39] Colicin E9 A BtuB OmpF/TolQRAB DNase Im9[40] Colicin N A OmpF OmpF/TolQRA Pore-forming Cni[41] Colicin S4 A OmpW OmpF/TolQRAB Pore-forming Csi[42] Colicin K A Tsx OmpF/TolQRAB Pore-forming  ? Cloacin DF13 A lutA [43] TolQRA [44] 16s rRNase [45] Colicin U A  ? OmpAF, TolQRAB Pore-forming Cui[46] Colicin 5 B Tsx TolC/TonB, ExbBD Pore-forming Cfi[47] Colicin 6 B Tsx TolC/TonB, ExbBD Pore-forming  ? Colicin 7 B Tsx TolC/TonB, ExbBD Pore-forming  ? Colicin 8 B Tsx TolC/TonB, ExbBD Pore-forming  ? Colicin 9 B Tsx TolC/TonB, ExbBD Pore-forming  ? Colicin 10 B Tsx TolC/TonB, ExbBD Pore-forming Cti[48] Colicin Ia B Cir Cir/TonB, ExbBD Pore-forming Iia[49] Colicin Ib B Cir Cir/TonB, ExbBD Pore-forming Imm Colicin B B FepA  ?/TonB, ExbBD Pore-forming Cbi[50] Colicin D B FepA  ?/TonB, ExbBD tRNase ImmD[51] Colicin M B FhuA  ?/TonB, ExbBD Inhibition of PG synthesis Cmi[52] Colicin V B Cir? [53] TonB, ExbB Disruption of membrane potential Cvi[54] Colicin Js B CjrBC [55] ExbBD, VirB [56]  ? Cji [57] Colicin Y  ?  ?  ? Pore-forming [58] Cyi[59] Table taken from [60] except where indicated. 3D structure of Colicin Colicin 3D structures

References

1. ↑ Hands SL, Holland LE, Vankemmelbeke M, Fraser L, Macdonald CJ, Moore GR, James R, Penfold CN. Interactions of TolB with the translocation domain of colicin E9 require an extended TolB box. J Bacteriol. 2005 Oct;187(19):6733-41. PMID:16166536 doi:10.1128/JB.187.19.6733-6741.2005
2. ↑ Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D. Colicin biology. Microbiol Mol Biol Rev. 2007 Mar;71(1):158-229. PMID:17347522 doi:10.1128/MMBR.00036-06
3. ↑ Riley MA, Wertz JE. Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie. 2002 May-Jun;84(5-6):357-64. PMID:12423779
4. ↑ Czaran TL, Hoekstra RF, Pagie L. Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):786-90. Epub 2002 Jan 15. PMID:11792831 doi:10.1073/pnas.012399899
5. ↑ Kerr B, Riley MA, Feldman MW, Bohannan BJ. Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature. 2002 Jul 11;418(6894):171-4. PMID:12110887 doi:10.1038/nature00823
6. ↑ Wallis R, Moore GR, James R, Kleanthous C. Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex. Biochemistry. 1995 Oct 24;34(42):13743-50. PMID:7577966
7. ↑ Pressler U, Braun V, Wittmann-Liebold B, Benz R. Structural and functional properties of colicin B. J Biol Chem. 1986 Feb 25;261(6):2654-9 PMID:2419320
8. ↑ Graille M, Mora L, Buckingham RH, van Tilbeurgh H, de Zamaroczy M. Structural inhibition of the colicin D tRNase by the tRNA-mimicking immunity protein. EMBO J. 2004 Apr 7;23(7):1474-82. Epub 2004 Mar 11. PMID:15014439 doi:10.1038/sj.emboj.7600162
9. ↑ Budiardjo SJ, Stevens JJ, Calkins AL, Ikujuni AP, Wimalasena VK, Firlar E, Case DA, Biteen JS, Kaelber JT, Slusky JSG. Colicin E1 opens its hinge to plug TolC. Elife. 2022 Feb 24;11. pii: 73297. doi: 10.7554/eLife.73297. PMID:35199644 doi:http://dx.doi.org/10.7554/eLife.73297
10. ↑ Duché D. Colicin E2 is still in contact with its receptor and import machinery when its nuclease domain enters the cytoplasm. J Bacteriol. 2007 Jun;189(11):4217-22. PMID:17416663 doi:10.1128/JB.00092-07
11. ↑ Vankemmelbeke M, Healy B, Moore GR, Kleanthous C, Penfold CN, James R. Rapid detection of colicin E9-induced DNA damage using Escherichia coli cells carrying SOS promoter-lux fusions. J Bacteriol. 2005 Jul;187(14):4900-7. PMID:15995205 doi:10.1128/JB.187.14.4900-4907.2005
12. ↑ Soelaiman S, Jakes K, Wu N, Li C, Shoham M. Crystal structure of colicin E3: implications for cell entry and ribosome inactivation. Mol Cell. 2001 Nov;8(5):1053-62. PMID:11741540
13. ↑ Lin YL, Elias Y, Huang RH. Structural and mutational studies of the catalytic domain of colicin E5: a tRNA-specific ribonuclease. Biochemistry. 2005 Aug 9;44(31):10494-500. PMID:16060658 doi:10.1021/bi050749s
14. ↑ Ko TP, Liao CC, Ku WY, Chak KF, Yuan HS. The crystal structure of the DNase domain of colicin E7 in complex with its inhibitor Im7 protein. Structure. 1999 Jan 15;7(1):91-102. PMID:10368275
15. ↑ Touzé T, Barreteau H, El Ghachi M, Bouhss A, Barnéoud-Arnoulet A, Patin D, Sacco E, Blanot D, Arthur M, Duché D, Lloubès R, Mengin-Lecreulx D. Colicin M, a peptidoglycan lipid-II-degrading enzyme: potential use for antibacterial means? Biochem Soc Trans. 2012 Dec 1;40(6):1522-7. PMID:23176510 doi:10.1042/BST20120189
16. ↑ Ghosh P, Mel SF, Stroud RM. The domain structure of the ion channel-forming protein colicin Ia. Nat Struct Biol. 1994 Sep;1(9):597-604. PMID:7543362
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19. ↑ Braun V, Patzer SI, Hantke K. Ton-dependent colicins and microcins: modular design and evolution. Biochimie. 2002 May-Jun;84(5-6):365-80. PMID:12423780
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21. ↑ Braun V, Patzer SI, Hantke K. Ton-dependent colicins and microcins: modular design and evolution. Biochimie. 2002 May-Jun;84(5-6):365-80. PMID:12423780
22. ↑ Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D. Colicin biology. Microbiol Mol Biol Rev. 2007 Mar;71(1):158-229. PMID:17347522 doi:10.1128/MMBR.00036-06
23. ↑ Bainbridge G, Armstrong GA, Dover LG, Whelan KF, Lakey JH. Displacement of OmpF loop 3 is not required for the membrane translocation of colicins N and A in vivo. FEBS Lett. 1998 Aug 7;432(3):117-22. PMID:9720908
24. ↑ Benedetti H, Lloubes R, Lazdunski C, Letellier L. Colicin A unfolds during its translocation in Escherichia coli cells and spans the whole cell envelope when its pore has formed. EMBO J. 1992 Feb;11(2):441-7. PMID:1537329
25. ↑ Cowan SW, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit RA, Jansonius JN, Rosenbusch JP. Crystal structures explain functional properties of two E. coli porins. Nature. 1992 Aug 27;358(6389):727-33. PMID:1380671 doi:http://dx.doi.org/10.1038/358727a0
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27. ↑ Mosbahi K, Walker D, Lea E, Moore GR, James R, Kleanthous C. Destabilization of the colicin E9 Endonuclease domain by interaction with negatively charged phospholipids: implications for colicin translocation into bacteria. J Biol Chem. 2004 May 21;279(21):22145-51. Epub 2004 Mar 23. PMID:15044477 doi:10.1074/jbc.M400402200
28. ↑ Nomura M. Colicins and related bacteriocins. Annu Rev Microbiol. 1967;21:257-84. PMID:4860260 doi:http://dx.doi.org/10.1146/annurev.mi.21.100167.001353
29. ↑ Cutler SA, Lonergan SM, Cornick N, Johnson AK, Stahl CH. Dietary inclusion of colicin e1 is effective in preventing postweaning diarrhea caused by F18-positive Escherichia coli in pigs. Antimicrob Agents Chemother. 2007 Nov;51(11):3830-5. Epub 2007 Aug 27. PMID:17724148 doi:10.1128/AAC.00360-07
30. ↑ Gillor O, Kirkup BC, Riley MA. Colicins and microcins: the next generation antimicrobials. Adv Appl Microbiol. 2004;54:129-46. PMID:15251279 doi:10.1016/S0065-2164(04)54005-4
31. ↑ Nardi A, Corda Y, Baty D, Duche D. Colicin A immunity protein interacts with the hydrophobic helical hairpin of the colicin A channel domain in the Escherichia coli inner membrane. J Bacteriol. 2001 Nov;183(22):6721-5. PMID:11673448 doi:10.1128/JB.183.22.6721-6725.2001
32. ↑ Song HY, Cramer WA. Membrane topography of ColE1 gene products: the immunity protein. J Bacteriol. 1991 May;173(9):2935-43. PMID:1708384
33. ↑ Duche D, Issouf M, Lloubes R. Immunity protein protects colicin E2 from OmpT protease. J Biochem. 2009 Jan;145(1):95-101. Epub 2008 Nov 5. PMID:18990718 doi:10.1093/jb/mvn149
34. ↑ Jakes K, Zinder ND, Boon T. Purification and properties of colicin E3 immunity protein. J Biol Chem. 1974 Jan 25;249(2):438-44. PMID:4588566
35. ↑ Carr S, Walker D, James R, Kleanthous C, Hemmings AM. Crystallization of the cytotoxic domain of a ribosome-inactivating colicin in complex with its immunity protein. Acta Crystallogr D Biol Crystallogr. 2000 Dec;56(Pt 12):1630-3. PMID:11092930
36. ↑ Lau PC, Condie JA. Nucleotide sequences from the colicin E5, E6 and E9 operons: presence of a degenerate transposon-like structure in the ColE9-J plasmid. Mol Gen Genet. 1989 Jun;217(2-3):269-77. PMID:2549375
37. ↑ Akutsu A, Masaki H, Ohta T. Molecular structure and immunity specificity of colicin E6, an evolutionary intermediate between E-group colicins and cloacin DF13. J Bacteriol. 1989 Dec;171(12):6430-6. PMID:2687234
38. ↑ Dennis CA, Videler H, Pauptit RA, Wallis R, James R, Moore GR, Kleanthous C. A structural comparison of the colicin immunity proteins Im7 and Im9 gives new insights into the molecular determinants of immunity-protein specificity. Biochem J. 1998 Jul 1;333 ( Pt 1):183-91. PMID:9639578
39. ↑ Keeble AH, Kleanthous C. The kinetic basis for dual recognition in colicin endonuclease-immunity protein complexes. J Mol Biol. 2005 Sep 23;352(3):656-71. PMID:16109424 doi:10.1016/j.jmb.2005.07.035
40. ↑ Osborne MJ, Breeze AL, Lian LY, Reilly A, James R, Kleanthous C, Moore GR. Three-dimensional solution structure and 13C nuclear magnetic resonance assignments of the colicin E9 immunity protein Im9. Biochemistry. 1996 Jul 23;35(29):9505-12. PMID:8755730 doi:10.1021/bi960401k
41. ↑ Geli V, Baty D, Pattus F, Lazdunski C. Topology and function of the integral membrane protein conferring immunity to colicin A. Mol Microbiol. 1989 May;3(5):679-87. PMID:2668695
42. ↑ Pilsl H, Smajs D, Braun V. Characterization of colicin S4 and its receptor, OmpW, a minor protein of the Escherichia coli outer membrane. J Bacteriol. 1999 Jun;181(11):3578-81. PMID:10348872
43. ↑ Wooldridge KG, Williams PH. Sensitivity of Escherichia coli to cloacin DF13 involves the major outer membrane protein OmpF. J Bacteriol. 1991 Apr;173(8):2420-4. PMID:2013565
44. ↑ Thomas JA, Valvano MA. Role of tol genes in cloacin DF13 susceptibility of Escherichia coli K-12 strains expressing the cloacin DF13-aerobactin receptor IutA. J Bacteriol. 1993 Jan;175(2):548-52. PMID:8419302
45. ↑ Baan RA, Duijfjes JJ, van Leerdam E, van Knippenberg PH, Bosch L. Specific in situ cleavage of 16S ribosomal RNA of Escherichia coli interferes with the function of initiation factor IF-1. Proc Natl Acad Sci U S A. 1976 Mar;73(3):702-6. PMID:768982
46. ↑ Smajs D, Pilsl H, Braun V. Colicin U, a novel colicin produced by Shigella boydii. J Bacteriol. 1997 Aug;179(15):4919-28. PMID:9244283
47. ↑ Pilsl H, Braun V. Evidence that the immunity protein inactivates colicin 5 immediately prior to the formation of the transmembrane channel. J Bacteriol. 1995 Dec;177(23):6966-72. PMID:7592492
48. ↑ Pilsl H, Braun V. Novel colicin 10: assignment of four domains to TonB- and TolC-dependent uptake via the Tsx receptor and to pore formation. Mol Microbiol. 1995 Apr;16(1):57-67. PMID:7651137
49. ↑ Weaver CA, Redborg AH, Konisky J. Plasmid-determined immunity of Escherichia coli K-12 to colicin Ia Is mediated by a plasmid-encoded membrane protein. J Bacteriol. 1981 Dec;148(3):817-28. PMID:6273383
50. ↑ Schramm E, Olschlager T, Troger W, Braun V. Sequence, expression and localization of the immunity protein for colicin B. Mol Gen Genet. 1988 Jan;211(1):176-82. PMID:2830463
51. ↑ Graille M, Mora L, Buckingham RH, van Tilbeurgh H, de Zamaroczy M. Structural inhibition of the colicin D tRNase by the tRNA-mimicking immunity protein. EMBO J. 2004 Apr 7;23(7):1474-82. Epub 2004 Mar 11. PMID:15014439 doi:10.1038/sj.emboj.7600162
52. ↑ Olschlager T, Schramm E, Braun V. Cloning and expression of the activity and immunity genes of colicins B and M on ColBM plasmids. Mol Gen Genet. 1984;196(3):482-7. PMID:6094976
53. ↑ Waters VL, Crosa JH. Colicin V virulence plasmids. Microbiol Rev. 1991 Sep;55(3):437-50. PMID:1943995
54. ↑ Frick KK, Quackenbush RL, Konisky J. Cloning of immunity and structural genes for colicin V. J Bacteriol. 1981 Nov;148(2):498-507. PMID:6271732
55. ↑ Braun V, Patzer SI, Hantke K. Ton-dependent colicins and microcins: modular design and evolution. Biochimie. 2002 May-Jun;84(5-6):365-80. PMID:12423780
56. ↑ Smajs D, Weinstock GM. The iron- and temperature-regulated cjrBC genes of Shigella and enteroinvasive Escherichia coli strains code for colicin Js uptake. J Bacteriol. 2001 Jul;183(13):3958-66. PMID:11395459 doi:10.1128/JB.183.13.3958-3966.2001
57. ↑ Smajs D, Weinstock GM. Genetic organization of plasmid ColJs, encoding colicin Js activity, immunity, and release genes. J Bacteriol. 2001 Jul;183(13):3949-57. PMID:11395458 doi:10.1128/JB.183.13.3949-3957.2001
58. ↑ Riley MA, Cadavid L, Collett MS, Neely MN, Adams MD, Phillips CM, Neel JV, Friedman D. The newly characterized colicin Y provides evidence of positive selection in pore-former colicin diversification. Microbiology. 2000 Jul;146 ( Pt 7):1671-7. PMID:10878131
59. ↑ Smajs D, Matejkova P, Weinstock GM. Recognition of pore-forming colicin Y by its cognate immunity protein. FEMS Microbiol Lett. 2006 May;258(1):108-13. PMID:16630264 doi:10.1111/j.1574-6968.2006.00201.x
60. ↑ Kleanthous C. Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nat Rev Microbiol. 2010 Dec;8(12):843-8. Epub 2010 Nov 9. PMID:21060316 doi:10.1038/nrmicro2454