The twin-arginine translocation system: Contributions to the pathobiology of Campylobacter jejuni

Future Microbiology

Volumn 6, Issue 11, 2011, Pages 1315-1327

  Kassem, Issmat I ^a   Zhang, Qijing ^b   Rajashekara, Gireesh ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Adaptation; Campylobacter jejuni; Control; Electron transport chain; Pathogenesis; Survival; Tat associated respiratory proteins; Therapeutics; Twin arginine translocation system

Indexed keywords

ALKALINE PHOSPHATASE; BACTERIAL PROTEIN; CARRIER PROTEIN; POLYPHOSPHATE; SIGNAL PEPTIDE;

ADAPTATION; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; CAMPYLOBACTER JEJUNI; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RESPIRATORY CHAIN; REVIEW; TWIN ARGININE TRANSLOCATION SYSTEM;

ANIMALS; CAMPYLOBACTER JEJUNI; HUMANS; MEMBRANE TRANSPORT PROTEINS; PROTEIN TRANSPORT; VIRULENCE FACTORS;

ANIMALIA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

EID: 81255157200     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.11.107     Document Type: Review

References (79)

1. Natale P, Brüser T, Driessen AJ. Sec-and Tat-mediated protein secretion across the bacterial cytoplasmic membrane-distinct translocases and mechanisms. Biochim. Biophys. Acta 1778(9), 1735-1756 (2008).
2. Cline K, Ettinger WF, Theg SM. Proteinspecific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP. J. Biol. Chem. 267(4), 2688-2696 (1992).
3. Creighton AM, Hulford A, Mant A, Robinson D, Robinson C. A monomeric, tightly folded stromal intermediate on the d pH-dependent thylakoidal protein transport pathway. J. Biol. Chem. 270(4), 1663-1669 (1995).
4. Berks BC. A common export pathway for proteins binding complex redox cofactors?. Mol. Microbiol. 22(3), 393-404 (1996). (Pubitemid 26373825)
5. DeLisa MP, Tullman D, Georgiou G. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc. Natl Acad. Sci. USA 100(10), 6115-6120 (2003). (Pubitemid 36576940)
6. Lee PA, Tullman-Ercek D, Georgiou G. The bacterial twin-arginine translocation pathway. Ann. Rev. Microbiol. 60, 373-395 (2006). (Pubitemid 44627954)
7. Ruiz N, Silhavy TJ. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 8(2), 122-126 (2005). (Pubitemid 40417951)
8. Biswas L, Biswas R, Nerz C et al. Role of the twin-arginine translocation pathway in Staphylococcus. J. Bacteriol. 191(19), 5921-5929 (2009).
9. Jongbloed JD, Martin U, Antelmann H et al. TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem. 275(52), 41350-41357 (2000). (Pubitemid 32054969)
10. Pop O, Martin U, Abel C, Muller JP. The twin-arginine signal peptide of PhoD and the TatAd/Cd proteins of Bacillus subtilis form an autonomous Tat translocation system. J. Biol. Chem. 277(5), 3268-3273 (2002). (Pubitemid 34953191)
11. Chan CS, Zlomislic MR, Tieleman DP, Turner RJ. The TatA subunit of Escherichia coli twin-arginine translocase has an N-in topology. Biochemistry 46(25), 7396-7404 (2007). (Pubitemid 46986366)
12. Robinson C, Matos CF, Beck D et al. Transport and proofreading of proteins by the twin-arginine translocation (Tat) system in bacteria. Biochim. Biophys. Acta 1808(3), 876-884 (2011).
13. Palmer T, Sargent F, Berks BC. Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol. 13(4), 175-180 (2005). (Pubitemid 40463319)
14. Musser SM, Theg SM. Characterization of the early steps of OE17 precursor transport by the thylakoid DpH/Tat machinery. Eur. J. Biochem. 267(9), 2588-2598 (2000). (Pubitemid 30304254)
15. Rodrigue A, Chanal A, Beck K, Muller M, Wu LF. Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J. Biol. Chem. 274(19), 13223-13228 (1999).
16. Cristobal S, de Gier JW, Nielsen H, von Heijne G. Competition between Sec-and TATdependent protein translocation in Escherichia coli. EMBO J. 18(11), 2982-2990 (1999). (Pubitemid 29255607)
17. Chaddock AM, Mant A, Karnauchov I et al. A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the d pH-dependent thylakoidal protein translocase, EMBO J. 14(12) 2715-2722 (1995)
18. Sargent F, Bogsch EG, Stanley NR et al. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17(13), 3640-3650 (1998). (Pubitemid 28327382)
19. Hinsley AP, Stanley NR, Palmer T, Berks BC. A naturally occurring bacterial Tat signal peptide lacking one of the invariant' arginine residues of the consensus targeting motif. FEBS Lett. 497(1), 45-49 (2001). (Pubitemid 32480178)
20. Ignatova Z, Hornle C, Nurk A, Kasche V. Unusual signal peptide directs penicillin amidase from Escherichia coli to the Tat translocation machinery. Biochem. Biophys. Res. Comm. 291(1), 146-149 (2002). (Pubitemid 34681150)
21. Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S. Prediction of twin-arginine signal peptides. BMC Bioinformat. 6, 167 (2005).
22. Bagos PG, Nikolaou EP, Liakopoulos TD, Tsirigos KD. Combined prediction of Tat and Sec signal peptides with hidden Markov models. Bioinformatics 26(22), 2811-2817 (2010).
23. Rose RW, Bruser T, Kissinger JC, Pohlschroder M. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol. Microbiol. 45(4), 943-950 (2002). (Pubitemid 35007439)
24. Yen MR, Tseng YH, Nguyen EH, Wu LF, Saier MHJ. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol. 177(6), 441-450 (2002). (Pubitemid 34591645)
25. Dilks K, Rose RW, Hartmann E, Pohlschrder M. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J. Bacteriol. 185(4), 1478-1483 (2003). (Pubitemid 36176885)
26. Stanley NR, Findlay K, Berks BC, Palmer T. Escherichia coli strains blocked in Tatdependent protein export exhibit pleiotropic defects in the cell envelope. J. Bacteriol. 183(1), 139-144 (2001). (Pubitemid 32003117)
27. Ochsner UA, Snyder A, Vasil AI, Vasil ML. Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc. Natl Acad. Sci. USA 99(12), 8312-8317 (2002). (Pubitemid 34651049)
28. Ize B, Porcelli I, Lucchini S, Hinton JC, Berks BC, Palmer T. Novel phenotypes of Escherichia coli tat mutants revealed by global gene expression and phenotypic analysis. J. Biol. Chem. 279(46), 47543-47554 (2004). (Pubitemid 39540899)
29. Pradel N, Ye C, Livrelli V, Xu J, Joly B, Wu LF. Contribution of the twin arginine translocation system to the virulence of enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 71(9), 4908-4916 (2003). (Pubitemid 37070732)
30. Ding Z, Christie PJ. Agrobacterium tumefaciens twin-arginine-dependent translocation is important for virulence, flagellation, and chemotaxis but not type IV secretion. J. Bacteriol. 185(3), 760-771 (2003). (Pubitemid 36139435)
31. De Buck E, Lammertyn E, Ann J. The importance of the twin-arginine translocation pathway for bacterial virulence. Trends Microbiol. 16(9), 442-453 (2008).
32. Voulhoux R, Ball G, Ize B et al. Involvement of the twin-arginine translocation system in protein secretion via the Type II pathway. EMBO J. 20(23), 6735-6741 (2001). (Pubitemid 33134203)
33. Young KT, Davis LM, DiRita VJ. Campylobacter jejuni: molecular biology and pathogenesis. Nat. Rev. Microbiol. 5(9), 665-679 (2007). (Pubitemid 47278861)
34. Gaynor EC, Wells DH, MacKichan JK, Falkow S. The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol. Microbiol. 56(1), 8-27 (2005). (Pubitemid 40461484)
35. Karmali MA, Fleming PC. Campylobacter enteritis in children. J. Pediatr. 94(4), 527-533 (1979). (Pubitemid 9125339)
36. Black RE, Levine MM, Clements ML et al. Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 157(3), 472-479 (1988). (Pubitemid 18071444)
37. Nachamkin I, Allos BM, Ho T. Campylobacter species and Guillain-Barre syndrome. Clin. Microbiol. Rev. 11(3), 555-567 (1998). (Pubitemid 28379100)
38. Salloway S, Mermel LA, Seamans M et al. Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human ganglioside GD3. Infect. Immun. 64(8), 2945-2949 (1996). (Pubitemid 26256130)
39. Marinelli WA, Leatherman JW. Neuromuscular disorders in the intensive care unit. Crit. Care Clin. 18(4), 915-929 (2002). (Pubitemid 35215568)
40. Allos BM. Campylobacter jejuni infections: update on emerging issues and trends. Clin. Infect. Dis. 32(8), 1201-1206 (2001). (Pubitemid 32381123)
41. Genigeorgis C, Hassuneh M, Collins P. Campylobacter jejuni infection on poultry farms and its effect on poultry meat contamination during slaughtering. J. Food Prot. 49(11), 895-903 (1986). (Pubitemid 17225312)
42. Grove-White DH, Leatherbarrow AJ, Cripps PJ, Diggle PJ, French NP. Molecular epidemiology and genetic diversity of Campylobacter jejuni in ruminants. Epidemiol. Infect. 7, 1-11 (2010).
43. Vandeplas S, Marcq C, Dauphin RD, Beckers Y, Thonart P, Thwis A. Contamination of poultry flocks by the human pathogen Campylobacter spp. and strategies to reduce its prevalence at the farm level. Biotechnol. Agron. Soc. Environ. 12(3), 317-334 (2008).
44. Dasti JI, Tareen AM, Lugert R, Zautner AE, Gross U. Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int. J. Med. Microbiol. 300(4), 205-211(2010).
45. Van Mourik A, Bleumink-Pluym NM, Van Dijk L, van Putten JP, Westen MM. Functional analysis of a Campylobacter jejuni alkaline phosphatase secreted via the Tat export machinery. Microbiology 154(Pt 2), 584-592 (2008). (Pubitemid 351292312)
46. Torriani A. From cell membrane to nucleotides: the phosphate regulon in Escherichia coli. Bioessays 12(8), 371-376 (1990). (Pubitemid 120034479)
47. Wosten MM, Parker CT, van Mourik A, Guilhabert MR, van Dijk L, van Putten JP. The Campylobacter jejuni PhosS/PhosR operon represents a non-classical phosphatesensitive two-component system. Mol. Microbiol. 62(1), 278-291 (2006). (Pubitemid 44386566)
48. Pittman MS, Kelly DJ. Electron transport through nitrate and nitrite reductases in Campylobacter jejuni. Biochem. Soc. Trans. 33(Pt 1), 190-192 (2005). (Pubitemid 40313798)
49. Hitchcock A, Hall SJ, Myers JD, Mulholland F, Jones MA, Kelly DJ. Roles of the twin-arginine translocase and associated chaperones in the biogenesis of the electron transport chains of the human pathogen Campylobacter jejuni. Microbiology. 156(Pt 10), 2994-3010 (2010).
50. Rajashekara G, Drozd M, Gangaiah D, Jeon B, Liu Z, Zhang Q. Functional characterization of the twin-arginine translocation system in Campylobacter jejuni. Foodborne Pathog. Dis. 6(8), 935-945 (2009).
51. Bernhardt TG, de Boer PA. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol. 48(5), 1171-1182 (2003). (Pubitemid 36718214)
52. Ize B, Stanley NR, Buchanan G, Palmer T. Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol. Microbiol. 48(5), 1183-1193 (2003). (Pubitemid 36718215)
53. Khattar MM, Kassem II, El-Hajj ZW. Of the morphogenes that make a ring, a rod and a sphere in Escherichia coli. Sci. Prog. 90(Pt 2-3), 59-72 (2007).
54. Weerakoon DR, Borden NJ, Goodson CM, Grimes J, Olson JW. The role of respiratory donor enzymes in Campylobacter jejuni host colonization and physiology. Microb. Pathog. 47(1), 8-15 (2009).
55. Weingarten RA, Grimes JL, Olson JW. Role of Campylobacter jejuni respiratory oxidases and reductases in host colonization. Appl. Environ. Microbiol. 74(5), 1367-1375 (2008). (Pubitemid 351358431)
56. Gennis RB, Stewart V. Respiration. In: Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt FC, Curtiss R 3rd, Ingraham JL, Lin ECC, Low KB (Eds). American Society for Microbiology, WA, USA 217-261 (1996).
57. Guccione E, Hitchcock A, Hall SJ et al. Reduction of fumarate, mesaconate and crotonate by Mfr, a novel oxygen-regulated periplasmic reductase in Campylobacter jejuni. Environ. Microbiol. 12(3), 576-591 (2010).
58. Weingarten RA, Taveirne ME, Olson JW. The dual-functioning fumarate reductase is the sole succinate:quinone reductase in Campylobacter jejuni and is required for full host colonization. J. Bacteriol. 191(16), 5293-5300 (2009).
59. Stintzi A. Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J. Bacteriol. 185(6), 2009-2016 (2003). (Pubitemid 36297902)
60. Palyada K, Sun YQ, Flint A, Butcher J, Naikare H, Stintzi A. Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. BMC Genomics 10, 481 (2009).
61. Berks BC, Palmer T, Sargent F. The Tat protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 47, 187-254 (2003). (Pubitemid 37214151)
62. Jack RL, Buchanan G, Dubini A, Hatzixanthis K, Palmer T, Sargent F. Coordinating assembly and export of complex bacterial proteins. EMBO J. 23, 3962-3972 (2004). (Pubitemid 39472418)
63. Turner RJ, Papish AL, Sargent F. Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can. J. Microbiol. 50, 225-238 (2004). (Pubitemid 38903410)
64. Maillard J, Spronk CA, Buchanan G et al. Structural diversity in twin-arginine signal peptide-binding proteins. Proc. Natl Acad. Sci. USA 104, 15641-15646 (2007). (Pubitemid 350035353)
65. Pommier J, Mejean V, Giordano G, Iobbi-Nivol C. TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine N-oxide reductase enzyme (TorA) in Escherichia coli. J. Biol. Chem. 273, 16615-16620 (1998). (Pubitemid 28311451)
66. Oresnik IJ, Ladner CL, Turner RJ. Identification of a twin-arginine leaderbinding protein. Mol. Microbiol. 40, 323-331 (2001).
67. Graubner W, Schierhorn A, Bruser T. DnaK plays a pivotal role in Tat targeting of CueO and functions beside SlyD as a general Tat signal binding chaperone. J. Biol. Chem. 282, 7116-7124 (2007). (Pubitemid 47093664)
68. Fisher AC, Kim JY, Perez-Rodriguez R et al. Exploration of twin-arginine translocation for expression and purification of correctly folded proteins in Escherichia coli. Microb. Biotechnol. 1(5), 403-415 (2008).
69. Kim JY, Fogarty EA, Lu FJ et al. Twinarginine translocation of active human tissue plasminogen activator in Escherichia coli. Appl. Environ. Microbiol. 71(12), 8451-8459 (2005). (Pubitemid 41803975)
70. Poly F, Read TD, Chen YH et al. Characterization of two Campylobacter jejuni strains for use in volunteer experimentalinfection studies. Infect. Immun. 76(12), 5655-5667 (2008).
71. Moran AP. Structure and conserved characteristics of Campylobacter jejuni lipopolysaccharides. J. Infect. Dis. 176, S115-S121 (1997). (Pubitemid 27505872)
72. Hentzer M, Wu H, Andersen JB et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22(15), 3803-3815 (2003). (Pubitemid 36975709)
73. Nordfelth R, Kauppi AM, Norberg HA, Wolf-Watz H, Elofsson M. Small-molecule inhibitors specifically targeting Type III secretion. Infect. Immun. 73(5), 3104-3114 (2005). (Pubitemid 40570380)
74. Roychoudhury S, Zielinski NA, Ninfa AJ et al. Inhibitors of two-component signal transduction systems: inhibition of alginate gene activation in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 90(3), 965-969 (1993). (Pubitemid 23053931)
75. Shakhnovich EA, Hung DT, Pierson E, Lee K, Mekalanos JJ. Virstatin inhibits dimerization of the transcriptional activator ToxT. Proc. Natl Acad. Sci. USA 104(7), 2372-2377 (2007). (Pubitemid 46391404)
76. Hung DT, Shakhnovich EA, Pierson E, Mekalanos JJ. Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science 310 (5748), 670-674 (2005). (Pubitemid 41528158)
77. Hudson DL, Layton AN, Field TR et al. Inhibition of Type III secretion in Salmonella enterica serovar Typhimurium by smallmolecule inhibitors. Antimicrob. Agents Chemother. 51(7), 2631-2635 (2007). (Pubitemid 47047354)
78. Gangaiah D, Kassem II, Liu Z, Rajashekara G. Importance of polyphosphate kinase 1 for Campylobacter jejuni viable-but-nonculturable cell formation, natural transformation, and antimicrobial resistance. Appl. Environ. Microbiol. 75(24), 7838-7849 (2009).
79. Gangaiah D, Liu Z, Arcos J et al. Polyphosphate kinase 2: a novel determinant of stress responses and pathogenesis in Campylobacter jejuni. PLoS ONE 5(8), e12142 (2010).