Structure and function of MARTX toxins and other large repetitive RTX proteins

Annual Review of Microbiology

Volumn 65, Issue , 2011, Pages 71-90

  Satchell, Karla J F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

FrhA; Legionella pneumophila; Pseudomonas; RtxA; VCBS; Vibrio

Indexed keywords

ADHESIN; AMINO ACID; BACTERIAL PROTEIN; BACTERIAL TOXIN; CYTOLYSIN; HEMOLYSIN; MEMBRANE PROTEIN; MULTIFUNCTIONAL AUTOPROCESSING REPEATS IN TOXINS TOXIN; REPEATS IN TOXINS PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BACTERIAL VIRULENCE; BIOFILM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIA; BACTERIAL PROTEINS; BACTERIAL TOXINS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY;

LEGIONELLA PNEUMOPHILA; PSEUDOMONAS; VIBRIO; YERSINIA;

EID: 80053286819     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-090110-102943     Document Type: Review

References (112)

1. Ahuja N, Kumar P, Bhatnagar R. 2004. The adenylate cyclase toxins. Crit. Rev. Microbiol. 30:187-96 (Pubitemid 39141923)
2. Andersen C, Hughes C, KoronakisV. 2000. Chunnel vision. Export and efflux through bacterial channeltunnels. EMBO Rep. 1:313-18
3. BaumannU,Wu S, FlahertyKM,McKay DB. 1993. Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel 'roll motif. EMBO J. 12:3357-64 (Pubitemid 23256422)
4. Bina JE, Mekalanos JJ. 2001. Vibrio cholerae tolC is required for bile resistance and colonization. Infect. Immun. 69:4681-85 (Pubitemid 32574473)
5. Boardman BK, Meehan BM, Satchell KJ. 2007. Growth phase regulation of Vibrio cholerae RTX toxin export. J. Bacteriol. 189:1827-35 (Pubitemid 46446145)
6. Boardman BK, Satchell KJ. 2004. Vibrio cholerae strains with mutations in an atypical type I secretion system accumulate RTX toxin intracellularly. J. Bacteriol. 186:8137-43 (Pubitemid 39552526)
7. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, et al. 2004. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36:1165-73 (Pubitemid 41288965)
8. Chain PS, Carniel E, Larimer FW, Lamerdin J, Stoutland PO, et al. 2004. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 101:13826-31 (Pubitemid 39298492)
9. Chatterjee R, Nag S, Chaudhuri K. 2008. Identification of a new RTX-like gene cluster in Vibrio cholerae. FEMS Microbiol. Lett. 284:165-71 (Pubitemid 351813420)
10. Chen CY,Wu KM, Chang YC, Chang CH, Tsai HC, et al. 2003. Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res. 13:2577-87
11. Cheong TG, Chan M, Kurunathan S, Ali SA, ZiNing T, et al. 2010. Construction and characterization of rtxA and rtxC mutants of auxotrophic O139 Vibrio cholerae. Microb. Pathog. 48:85-90
12. Chow KH, Ng TK, Yuen KY, Yam WC. 2001. Detection of RTX toxin gene in Vibrio cholerae by PCR. J. Clin. Microbiol. 39:2594-97 (Pubitemid 32606239)
13. Chung KJ, Cho EJ, Kim MK, Kim YR, Kim SH, et al. 2010. RtxA1-induced expression of the small GTPase Rac2 plays a key role in the pathogenicity of Vibrio vulnificus. J. Infect. Dis. 201:97-105
14. Cirillo SL, Bermudez LE, El-Etr SH, Duhamel GE, Cirillo JD. 2001. Legionella pneumophila entry gene rtxA is involved in virulence. Infect. Immun. 69:508-17 (Pubitemid 32038351)
15. Cirillo SL,LumJ, Cirillo JD. 2000. Identification of novel loci involved in entry by Legionella pneumophila. Microbiology 146(Pt. 6):1345-59 (Pubitemid 30364725)
16. Cirillo SL, Yan L, Littman M, Samrakandi MM, Cirillo JD. 2002. Role of the Legionella pneumophila rtxA gene in amoebae. Microbiology 148:1667-77 (Pubitemid 34679021)
17. Cordero CL, Kudryashov DS, Reisler E, Satchell KJ. 2006. The actin cross-linking domain of the Vibrio cholerae RTX toxin directly catalyzes the covalent cross-linking of actin. J. Biol. Chem. 281:32366-74 (Pubitemid 46036791)
18. Cordero CL, Sozhamannan S, Satchell KJ. 2007. RTX toxin actin cross-linking activity in clinical and environmental isolates of Vibrio cholerae. J. Clin. Microbiol. 45:2289-92 (Pubitemid 47203811)
19. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-96 (Pubitemid 32319293)
20. D'Auria G, Jimenez N, Peris-Bondia F, Pelaz C, Latorre A, Moya A. 2008. Virulence factor rtx in Legionella pneumophila, evidence suggesting it is a modular multifunctional protein. BMC Genomics 9:14
21. Daraselia N, Dernovoy D, Tian Y, Borodovsky M, Tatusov R, Tatusova T. 2003. Reannotation of Shewanella oneidensis genome. OMICS 7:171-75 (Pubitemid 36886259)
22. Deng W, Burland V, Plunkett G 3rd, Boutin A, Mayhew GF, et al. 2002. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184:4601-11 (Pubitemid 34832588)
23. Deng W, Liou SR, Plunkett G 3rd, Mayhew GF, Rose DJ, et al. 2003. Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J. Bacteriol. 185:2330-37 (Pubitemid 36363194)
24. Dowling AJ, Daborn PJ, Waterfield NR, Wang P, Streuli CH, ffrench-Constant RH. 2004. The insecticidal toxin Makes caterpillars floppy (Mcf ) promotes apoptosis in mammalian cells. Cell Microbiol. 6:345-53 (Pubitemid 38379817)
25. Dowling AJ, Waterfield NR, HaresMC, Le Goff G, Streuli CH, ffrench-Constant RH. 2007. TheMcf1 toxin induces apoptosis via the mitochondrial pathway and apoptosis is attenuated by mutation of the BH3-like domain. Cell Microbiol. 9:2470-84 (Pubitemid 47365651)
26. Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Givaudan A, et al. 2003. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat. Biotechnol. 21:1307-13 (Pubitemid 37356615)
27. Espinosa-Urgel M, Salido A, Ramos JL. 2000. Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J. Bacteriol. 182:2363-69 (Pubitemid 30212890)
28. Fan JJ, Shao CP, Ho YC, Yu CK, Hor LI. 2001. Isolation and characterization of a Vibrio vulnificus mutant deficient in both extracellular metalloprotease and cytolysin. Infect. Immun. 69:5943-48
29. ffrench-Constant R, Waterfield N, Daborn P, Joyce S, Bennett H, et al. 2003. Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol. Rev. 26:433-56 (Pubitemid 36183527)
30. French CT, Panina EM, Yeh SH, Griffith N, Arambula DG, Miller JF. 2009. The Bordetella type III secretion system effector BteA contains a conserved N-terminal motif that guides bacterial virulence factors to lipid rafts. Cell Microbiol. 11:1735-49
31. Fullner KJ,Mekalanos JJ. 2000. In vivo covalent crosslinking of actin by the RTX toxin of Vibrio cholerae. EMBO J. 19:5315-23
32. Fuqua C. 2010. Passing the baton between laps: adhesion and cohesion in Pseudomonas putida biofilms. Mol. Microbiol. 77:533-36
33. Geissler B, Bonebrake A, Sheahan KL,Walker ME, SatchellKJ. 2009. Genetic determination of essential residues of the Vibrio cholerae actin cross-linking domain reveals functional similarity with glutamine synthetases. Mol. Microbiol. 73:858-68
34. Geissler B, Tungekar R, Satchell KJ. 2010. Identification of a conserved membrane localization domain within numerous large bacterial protein toxins. Proc. Natl. Acad. Sci. USA 107:5581-86
35. Gerlach RG, Claudio N, Rohde M, Jackel D, Wagner C, Hensel M. 2008. Cooperation of Salmonella pathogenicity islands 1 and 4 is required to breach epithelial barriers. Cell Microbiol. 10:2364-76
36. Gerlach RG, Jackel D, Stecher B, Wagner C, Lupas A, et al. 2007. Salmonella pathogenicity island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol. 9:1834-50 (Pubitemid 46958807)
37. Golubov A, Heesemann J, Rakin A. 2006. New RtxA-like protein in Yersinia enterocolitica, its distribution and function. http://www.ncbi.nlm.nih.gov/ protein/CAJ90394. Last accessed 1/2/2011
38. Goodrich-Blair H, Barbazuk B, Bode HB, Darby C, Du Z, et al. 2010. http://www.ncbi.nlm. nih.gov/protein/YP-003467018. Last accessed 1/2/2011
39. Goodrich-Blair H, Barbazuk B, Bode HB, Darby C, Du Z, et al. 2010. http://www.ncbi.nlm. nih.gov/protein/YP-003711644. Last accessed 1/2/2011
40. Gulig PA, Tucker MS, Thiaville PC, Joseph JL, Brown RN. 2009. USER friendly cloning coupled with chitin-based natural transformation enables rapid mutagenesis of Vibrio vulnificus. Appl. Environ. Microbiol. 75:4936-49
41. Harris TJ, Tepass U. 2010. Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11:502-14
42. Hinsa SM, Espinosa-Urgel M, Ramos JL, O'Toole GA. 2003. Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol. Microbiol. 49:905-18 (Pubitemid 36981338)
43. Hoffmann M, Monday SR, Allard MW, Strain EA, Whittaker P, et al. 2010. Vibrio caribbenthicus sp. nov., isolated from marine sponge Scleritoderma cyanea. http://www.ncbi.nlm. nih.gov/protein/ZP-07744927. Last accessed on 1/2/2011
44. Holmquist M. 2000. '/α-hydrolase fold enzymes: structures, functions and mechanisms. Curr. Protein Pept. Sci. 1:209-35
45. Irvine RF, Schell MJ. 2001. Back in the water: the return of the inositol phosphates. Nat. Rev. Mol. Cell Biol. 2:327-38 (Pubitemid 33674045)
46. Kamitani S, Kitadokoro K, Miyazawa M, Toshima H, Fukui A, et al. 2010. Characterization of the membrane-targeting C1 domain in Pasteurella multocida toxin. J. Biol. Chem. 285:25467-75
47. Kim YR, Lee SE, Kook H, Yeom JA, Na HS, et al. 2008. Vibrio vulnificus RTX toxin kills host cells only after contact of the bacteria with host cells. Cell Microbiol. 10:848-62 (Pubitemid 351386941)
48. Kiss T, Morgan E, Nagy G. 2007. Contribution of SPI-4 genes to the virulence of Salmonella enterica. FEMS Microbiol. Lett. 275:153-59 (Pubitemid 47390100)
49. Kitadokoro K, Kamitani S, Miyazawa M, Hanajima-Ozawa M, Fukui A, et al. 2007. Crystal structures reveal a thiol protease-like catalytic triad in the C-terminal region of Pasteurella multocida toxin. Proc. Natl. Acad. Sci. USA 104:5139-44 (Pubitemid 47186189)
50. KrehenbrinkM,Downie JA. 2008. Identification of protein secretion systems and novel secreted proteins in Rhizobium leguminosarum bv. viciae. BMC Genomics 9:55
51. Kudryashov DS, Cordero CL, Reisler E, Satchell KJ. 2008. Characterization of the enzymatic activity of the actin cross-linking domain from the Vibrio cholerae MARTXVc toxin. J. Biol. Chem. 283:445-52
52. Kudryashov DS, Durer ZA, Ytterberg AJ, Sawaya MR, Pashkov I, et al. 2008. Connecting actin monomers by iso-peptide bond is a toxicity mechanism of the Vibrio cholerae MARTX toxin. Proc. Natl. Acad. Sci. USA 105:18537-42
53. Kwak J, Jeong H, Satchell K. 2011. Vibrio vulnificus rtxA1 gene recombination generates novel toxin variants with altered potency during intestinal infection. Proc. Natl. Acad. Sci. USA 108:1645-50
54. Lasa I, Penades JR. 2006. Bap: a family of surface proteins involved in biofilm formation. Res. Microbiol. 157:99-107 (Pubitemid 43243686)
55. Lee BC, Choi SH, Kim TS. 2008. Vibrio vulnificus RTX toxin plays an important role in the apoptotic death of human intestinal epithelial cells exposed to Vibrio vulnificus. Microbes Infect. 10:1504-13
56. Lee BC, Lee JH, KimMW, Kim BS, Oh MH, et al. 2008. Vibrio vulnificus rtxE is important for virulence, and its expression is induced by exposure to host cells. Infect. Immun. 76:1509-17
57. Lee JH, Kim MW, Kim BS, Kim SM, Lee BC, et al. 2007. Identification and characterization of the Vibrio vulnificus rtxA essential for cytotoxicity in vitro and virulence in mice. J. Microbiol. 45:146-52
58. Li L, Rock JL, Nelson DR. 2008. Identification and characterization of a repeat-in-toxin gene cluster in Vibrio anguillarum. Infect. Immun. 76:2620-32
59. Lin W, Fullner KJ, Clayton R, Sexton JA, Rogers MB, et al. 1999. Identification of a Vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc. Natl. Acad. Sci. USA 96:1071-76 (Pubitemid 29072185)
60. Linhartova I, Bumba L, Masin J, Basler M, Osicka R, et al. 2010. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol. Rev. 34:1076-112
61. Liu M, Alice AF, Naka H, Crosa JH. 2007. The HlyU protein is a positive regulator of rtxA1, a gene responsible for cytotoxicity and virulence in the human pathogen Vibrio vulnificus. Infect. Immun. 75:3282-89 (Pubitemid 47040929)
62. Lo HR, Lin JH, Chen YH, Chen CL, Shao CP, et al. 2011. RTX toxin enhances the survival of Vibrio vulnificus during infection by protecting the organism from phagocytosis. J Infect. Dis. doi: 10.1093/infdis/jir070
63. Lucas S, Copeland A, Lapidus A, Glavina del Rio T, Tice H, et al. 2008. Complete genome sequence of chromosome of Shewanella baltica OS223. http://www.ncbi.nlm.nih.gov/protein/217975052. Last accessed on 4/18/2011
64. Ludwig A, Goebel W. 1999. The family of the multigenic encoded RTX toxins. In The Comprehensive Sourcebook of Bacterial Protein Toxins, ed. JE Alouf, JH Freer, pp. 330-48. San Diego, CA: Academic
65. Lupardus PJ, Shen A, Bogyo M, Garcia KC. 2008. Small molecule-induced allosteric activation of the Vibrio cholerae RTX cysteine protease domain. Science 322:265-68
66. Ma AT,McAuley S, Pukatzki S, Mekalanos JJ. 2009. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host. Microbe 5:234-43
67. Main-Hester KL, Colpitts KM, Thomas GA, Fang FC, Libby SJ. 2008. Coordinate regulation of Salmonella pathogenicity island 1 (SPI1) and SPI4 in Salmonella enterica serovar Typhimurium. Infect. Immun. 76:1024-35 (Pubitemid 351428062)
68. Mandel MJ, Stabb EV, Ruby EG. 2008. Comparative genomics-based investigation of resequencing targets in Vibrio fischeri: focus on point miscalls and artefactual expansions. BMC Genomics 9:138
69. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. 2009. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37:D205-10
70. Martinez-Gil M, Yousef-Coronado F, Espinosa-Urgel M. 2010. LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture. Mol. Microbiol. 77:549-61
71. Mathan MM, Chandy G, Mathan VI. 1995. Ultrastructural changes in the upper small intestinal mucosa in patients with cholera. Gastroenterology 109:422-30
72. McClellandM, Sanderson KE, Spieth J,Clifton SW, Latreille P, et al. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-56 (Pubitemid 33026853)
73. McNab R, Jenkinson HF, Loach DM, Tannock GW. 1994. Cell-surface- associated polypeptides CshA and CshB of high molecular mass are colonization determinants in the oral bacterium Streptococcus gordonii. Mol. Microbiol. 14:743-54 (Pubitemid 24364591)
74. Mesmin B, Robbe K, Geny B, Luton F, Brandolin G, et al. 2004. A phosphatidylserine-binding site in the cytosolic fragment of Clostridium sordellii lethal toxin facilitates glucosylation of membrane-bound Rac and is required for cytotoxicity. J. Biol. Chem. 279:49876-82 (Pubitemid 39577794)
75. Morgan E, Bowen AJ, Carnell SC, Wallis TS, StevensMP. 2007. SiiE is secreted by the Salmonella enterica serovar Typhimurium pathogenicity island 4-encoded secretion system and contributes to intestinal colonization in cattle. Infect. Immun. 75:1524-33 (Pubitemid 46385849)
76. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, et al. 2002. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4:799-808 (Pubitemid 36064171)
77. Newton HJ, Ang DK, van Driel IR, Hartland EL. 2010. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin. Microbiol. Rev. 23:274-98
78. Olivier V,Haines GK 3rd, Tan Y, Satchell KJ. 2007. Hemolysin and the multifunctional autoprocessing RTX toxin are virulence factors during intestinal infection of mice with Vibrio cholerae El TorO1 strains. Infect. Immun. 75:5035-42 (Pubitemid 47502177)
79. Olivier V, Queen J, Satchell KJ. 2009. Successful small intestine colonization of adult mice by Vibrio cholerae requires ketamine anesthesia and accessory toxins. PLoS One 4:e7352
80. Olivier V, Salzman NH, Satchell KJ. 2007. Prolonged colonization of mice by Vibrio cholerae El Tor O1 depends on accessory toxins. Infect. Immun. 75:5043-51
81. Orth JH, Preuss I, Fester I, Schlosser A, Wilson BA, Aktories K. 2009. Pasteurella multocida toxin activation of heterotrimeric G proteins by deamidation. Proc. Natl. Acad. Sci. USA 106:7179-84
82. Pearson MM, Sebaihia M, Churcher C, Quail MA, Seshasayee AS, et al. 2008. Complete genome sequence of uropathogenic Proteusmirabilis, a master of both adherence andmotility. J. Bacteriol. 190:4027-37 (Pubitemid 351732882)
83. Pei J, Grishin NV. 2009. The Rho GTPase inactivation domain in Vibrio cholerae MARTX toxin has a circularly permuted papain-like thiol protease fold. Proteins 77:413-19
84. Polz M, Ferriera S, Johnson J, Kravitz S, Halpern A, et al. 2006. http://www.ncbi.nlm.nih.gov/ protein/ZP-00989505. Last accessed 1/2/2011
85. Prochazkova K, Satchell KJ. 2008. Structure-function analysis of inositol hexakisphosphate-induced autoprocessing of the Vibrio cholerae multifunctional autoprocessingRTXtoxin. J. Biol.Chem. 283:23656-64
86. Prochazkova K, Shuvalova LA, Minasov G, Voburka Z, Anderson WF, Satchell KJ. 2009. Structural and molecularmechanism for autoprocessing of MARTXtoxin of Vibrio cholerae at multiple sites. J. Biol. Chem. 284:26557-68
87. Rahman MH, Biswas K, Hossain MA, Sack RB,Mekalanos JJ, Faruque SM. 2008. Distribution of genes for virulence and ecological fitness among diverse Vibrio cholerae population in a cholera endemic area: tracking the evolution of pathogenic strains. DNA Cell Biol. 27:347-55 (Pubitemid 351969856)
88. Read TD, Akmal A, Bishop-Lilly K, Chen PE, Cook C, et al. 2008. Annotation of the Yersinia kristensenii ATCC 33638 genome. http://www.ncbi.nlm. nih.gov/protein/ZP-04623799. Last accessed 1/2/2011
89. Reinert DJ, Jank T, Aktories K, Schulz GE. 2005. Structural basis for the function of Clostridium difficile toxin B. J. Mol. Biol. 351:973-81 (Pubitemid 41133445)
90. Roig FJ, González-Candelas F, Amaro C. 2011. Domain organization and evolution of multifunctional autoprocessing repeats-in-toxin (MARTX) toxin in Vibrio vulnificus. Appl. Environ. Microbiol. 77:657-68
91. Satchell KJ. 2007. MARTX: multifunctional-autoprocessing RTX toxins. Infect. Immun. 75:5079-84
92. Seshadri R, Joseph SW, Chopra AK, Sha J, Shaw J, et al. 2006. Genome sequence of Aeromonas hydrophila ATCC 7966T: jack of all trades. J. Bacteriol. 188:8272-82 (Pubitemid 44845699)
93. Sheahan KL,Cordero CL, SatchellKJ. 2004. Identification of a domain within themultifunctional Vibrio cholerae RTX toxin that covalently cross-links actin. Proc. Natl. Acad. Sci. USA 101:9798-803 (Pubitemid 38869316)
94. Sheahan KL, Cordero CL, Satchell KJ. 2007. Autoprocessing of the Vibrio cholerae RTX toxin by the cysteine protease domain. EMBO J. 26:2552-61 (Pubitemid 46788325)
95. Sheahan KL, Satchell KJ. 2007. Inactivation of small Rho GTPases by the multifunctional RTX toxin from Vibrio cholerae. Cell Microbiol. 9:1324-35 (Pubitemid 46547147)
96. Shen A, Lupardus PJ, AlbrowVE, Guzzetta A, Powers JC, et al. 2009. Mechanistic and structural insights into the proteolytic activation of Vibrio cholerae MARTX toxin. Nat. Chem. Biol. 5:469-78
97. Smith C, Estavillo D, Emsley J, Bankston LA, Liddington RC, Cruz MA. 2000. Mapping the collagenbinding site in the I domain of the glycoprotein Ia/IIa (integrin alpha(2)beta(1)). J. Biol. Chem. 275:4205-9 (Pubitemid 30094656)
98. Stanley P, Koronakis V, Hughes C. 1998. Acylation of Escherichia coli hemolysin: a unique protein lipidation mechanism underlying toxin function. Microbiol. Mol. Biol. Rev. 62:309-33 (Pubitemid 28270277)
99. Starks AM, Bourdage KL, Thiaville PC,Gulig PA. 2006. Use of amarker plasmid to examine differential rates of growth and death between clinical and environmental strains of Vibrio vulnificus in experimentally infected mice. Mol. Microbiol. 61:310-23 (Pubitemid 44356565)
100. Syed KA, Beyhan S, Correa N, Queen J, Liu J, et al. 2009. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J. Bacteriol. 191:6555-70
101. Theunissen S,De Smet L,Dansercoer A,Motte B, Coenye T, et al. 2010. The 285 kDa Bap/RTX hybrid cell surface protein (SO4317) of Shewanella oneidensis MR-1 is a key mediator of biofilm formation. Res. Microbiol. 161:144-52
102. Toma C, Higa N, Koizumi Y, Nakasone N, Ogura Y, et al. 2010. Pathogenic Vibrio activate NLRP3 inflammasome via cytotoxins and TLR/nucleotide-binding oligomerization domain-mediated NF-kappa B signaling. J. Immunol. 184:5287-97
103. Tsuchiya T, Mitsuo E, HayashiN,Hikita Y,Nakao H, et al. 2007. Vibrio vulnificus damagesmacrophages during the early phase of infection. Infect. Immun. 75:4592-96 (Pubitemid 47378120)
104. Vallenet D, Nordmann P, Barbe V, Poirel L, Mangenot S, et al. 2008. Comparative analysis of acinetobacters: three genomes for three lifestyles. PLoS One 3:e1805
105. Vlisidou I, Dowling AJ, Evans IR, Waterfield N, ffrench-Constant RH, Wood W. 2009. Drosophila embryos as model systems for monitoring bacterial infection in real time. PLoS Pathog. 5:e1000518
106. Vonstein V, Bartels D. 2009. http://www.ncbi.nlm.nih.gov/protein/ZP- 04408076. Last accessed 1/2/2011
107. Wilkinson P,Waterfield NR, Crossman L, Corton C, Sanchez-Contreras M, et al. 2009. Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics 10:302
108. Wong KK, McClelland M, Stillwell LC, Sisk EC, Thurston SJ, Saffer JD. 1998. Identification and sequence analysis of a 27-kb chromosomal fragment containing a Salmonella pathogenicity island located at 92 minutes on the chromosome map of Salmonella enterica serovar typhimurium LT2. Infect. Immun. 66:3365-71 (Pubitemid 28303137)
109. Ziegler MO, Jank T, Aktories K, Schulz GE. 2008. Conformational changes and reaction of clostridial glycosylating toxins. J. Mol. Biol. 377:1346-56
110. Egerer M, Satchell KJ. 2010. Inositol hexakisphosphate-induced autoprocessing of large bacterial protein toxins. PLoS Pathog 6: e1000942
111. Ludwig A, Goebel W. 2006. Structure and mode of action of RTX toxins. In The comprehensive sourcebook of bacterial protein toxins (third edition), ed. JE Alouf, MR Popoff. Burlington, MA: Academic press. pp. 547-69
112. Satchell K. 2009. Actin crosslinking toxins of gram-negative bacteria. Toxins 1:123-33