The regulator HlyU, the repeat-in-toxin gene rtxA1, and their roles in the pathogenesis of Vibrio vulnificus infections

MicrobiologyOpen

Volumn 1, Issue 4, 2012, Pages 502-513

  Liu, Moqing ^a   Crosa, Jorge H ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Gene regulation; HlyU, pathogenesis, repeat in toxin, Vibrio

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; CYTOLYSIN; CYTOTOXIC FACTOR; HEMOLYSIN; MARTX TOXIN; PROTEIN HLYU; PROTEIN RTXA1; REGULATOR PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BINDING SITE; CYTOTOXICITY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE REGULATORY NETWORK; HUMAN; NONHUMAN; OPERON; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RTXA1 GENE; SEQUENCE ALIGNMENT; SPECIES COMPARISON; TOXIN SYNTHESIS; VIBRIO CHOLERAE; VIBRIO VULNIFICUS; VIBRIO VULNIFICUS INFECTION;

EID: 84923059957     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.48     Document Type: Article

References (85)

1. Arunkumar, A. I., M. A. Pennella, X. Kong, and D. P. Giedroc. 2007. Resonance assignments of the metal sensor CzrA in the apo-, Zn2- and DNA-bound (42 kDa) states. Biomol. NMR Assign. 1:99-101.
2. Arunkumar, A. I., G. C. Campanello, and D. P. Giedroc. 2009. Solution structure of a paradigm ArsR family zinc sensor in the DNA-bound state. Proc. Natl. Acad. Sci. USA 106:18177-18182.
3. Boardman, B. K., and K. J. Satchell. 2004. Vibrio cholerae strains with mutations in an atypical type I secretion system accumulate RTX toxin intracellularly. J. Bacteriol. 186:8137-8143.
4. Boardman, B. K., B. M. Meehan, and K. J. Fullner Satchell. 2007. Growth phase regulation of Vibrio cholerae RTX toxin export. J. Bacteriol. 189:1827-1835.
5. Bullen, J. J., P. B. Spalding, C. G. Ward, and J. M. Gutteridge. 1991. Hemochromatosis, iron and septicemia caused by Vibrio vulnificus. Arch. Intern. Med. 151:1606-1609.
6. Busenlehner, L. S., T. C. Weng, J. E. Penner-Hahn, and D. P. Giedroc. 2002. Elucidation of primary (alpha(3)N) and vestigial (alpha(5)) heavy metal-binding sites in Staphylococcus aureus pI258 CadC: evolutionary implications for metal ion selectivity of ArsR/SmtB metal sensor proteins. J. Mol. Biol. 319:685-701.
7. Busenlehner, L. S., M. A. Pennella, and D. P. Giedroc. 2003. The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol. Rev. 27:131-143.
8. Chen, C. Y., K. M. Wu, Y. C. Chang, C. H. Chang, H. C. Tsai, T. L. Liao, et al. 2003. Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res. 13:2577-2587.
9. Chung, K. J., E. J. Cho, M. K. Kim, Y. R. Kim, S. H. Kim, H. Y. Yang, 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.
10. Cordero, C. L., D. S. Kudryashov, E. Reisler, and K. J. Satchell. 2006. The actin cross-linking domain of the Vibrio cholerae RTX toxin directly catalyzes the covalent cross-linking of actin. J. Biol. Chem. 281:32366-32374.
11. Dame, R. T., M. S. Luijsterburg, E. Krin, P. N. Bertin, R. Wagner, and G. J. Wuite. 2005. DNA bridging: a property shared among H-NS-like proteins. J. Bacteriol. 187:1845-1848.
12. Dorman, C. J. 2004. H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2:391-400.
13. Dorman, C. J. 2007. Probing bacterial nucleoid structure with optical tweezers. BioEssays 29:212-216.
14. Dorman, C. J., and K. A. Kane. 2009. DNA bridging and antibridging: a role for bacterial nucleoid-associated proteins in regulating the expression of laterally acquired genes. FEMS Microbiol. Rev. 33:587-592.
15. Endo, G., and S. Silver. 1995. CadC, the transcriptional regulatory protein of the cadmium resistance system of Staphylococcus aureus plasmid pI258. J. Bacteriol. 177:4437-4441.
16. Fan, J. J., C. P. Shao, Y. C. Ho, C. K. Yu, and L. I. Hor. 2001. Isolation and characterization of a Vibrio vulnificus mutant deficient in both extracellular metalloprotease and cytolysin. Infect. Immun. 69:5943-5948.
17. Fujioka, M., G. Nishimura, O. Miyazato, T. Yamamoto, F. Okamoto, and K. Tsunenori. 2003. Necrotising fasciitis and myositis that originated from gastrointestinal bacterial infection: two fatal cases. Scand. J. Plast. Reconstr. Surg. Hand Surg. 37:239-242.
18. Fullner, K. J., and J. J. Mekalanos. 2000. In vivo covalent cross-linking of cellular actin by the Vibrio cholerae RTX toxin. EMBO J. 19:5315-5323.
19. Gray, L. D., and A. S. Kreger. 1987. Mouse skin damage caused by cytolysin from Vibrio vulnificus and by V. vulnificus infection. J. Infect. Dis. 155:236-241.
20. Haq, S. M., and H. H. Dayal. 2005. Chronic liver disease and consumption of raw oysters: a potentially lethal combination - a review of Vibrio vulnificus septicemia. Am. J. Gastroenterol. 100:1195-1199.
21. Helms, S. D., J. D. Oliver, and J. C. Travis. 1984. Role of heme compounds and haptoglobin in Vibrio vulnificus pathogenicity. Infect. Immun. 45:345-349.
22. Hor, L. I., T. T. Chang, and S. T. Wang. 1999. Survival of Vibrio vulnificus in whole blood from patients with chronic liver diseases: association with phagocytosis by neutrophils and serum ferritin levels. J. Infect. Dis. 179:275-278.
23. Huckle, J. W., A. P. Morby, J. S. Turner, and N. J. Robinson. 1993. Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol. Microbiol. 7:177-187.
24. Jeong, H. G., and K. J. Satchell. 2012. Additive function of Vibrio vulnificus MARTX(Vv) and VvhA cytolysins promotes rapid growth and epithelial tissue necrosis during intestinal infection. PLoS Pathog. 8:e1002581.
25. Jeong, K. C., H. S. Jeong, J. H. Rhee, S. E. Lee, S. S. Chung, A. M. Starks, et al. 2000. Construction and phenotypic evaluation of a Vibrio vulnificus vvpE mutant for elastolytic protease. Infect. Immun. 68:5096-5106.
26. Jones, M. K., and J. D. Oliver. 2009. Vibrio vulnificus: disease and pathogenesis. Infect. Immun. 77:1723-1733.
27. Kashimoto, T., S. Ueno, M. Hanajima, H. Hayashi, Y. Akeda, S. Miyoshi, et al. 2003. Vibrio vulnificus induces macrophage apoptosis in vitro and in vivo. Infect. Immun. 71:533-535.
28. Kim, Y. R., and J. H. Rhee. 2003. Flagellar basal body flg operon as a virulence determinant of Vibrio vulnificus. Biochem. Biophys. Res. Commun. 304:405-410.
29. Kim, H. R., H. W. Rho, M. H. Jeong, J. W. Park, J. S. Kim, B. H. Park, et al. 1993. Hemolytic mechanism of cytolysin produced from V. vulnificus. Life Sci. 53:571-577.
30. Kim, S. Y., S. E. Lee, Y. R. Kim, C. M. Kim, P. Y. Ryu, H. E. Choy, et al. 2003a. Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol. Microbiol. 48:1647-1664.
31. Kim, Y. R., S. E. Lee, C. M. Kim, S. Y. Kim, E. K. Shin, D. H. Shin, et al. 2003b. Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect. Immun. 71:5461-5471.
32. Kim, Y. R., S. E. Lee, H. Kook, J. A. Yeom, H. S. Na, S. Y. Kim, et al. 2008. Vibrio vulnificus RTX toxin kills host cells only after contact of the bacteria with host cells. Cell. Microbiol. 10:848-862.
33. Kim, C. M., Y. Y. Chung, and S. H. Shin. 2009. Iron differentially regulates gene expression and extracellular secretion of Vibrio vulnificus cytolysin-hemolysin. J. Infect. Dis. 200:582-589.
34. Koo, B. S., J. H. Lee, S. C. Kim, H. Y. Yoon, K. A. Kim, K. B. Kwon, et al. 2007. Phospholipase A as a potent virulence factor of Vibrio vulnificus. Int. J. Mol. Med. 20:913-918.
35. Kwak, J. S., H. G. Jeong, and K. J. Satchell. 2011. Vibrio vulnificus rtxA1 gene recombination generates toxin variants with altered potency during intestinal infection. Proc. Natl. Acad. Sci. USA 108:1645-1650.
36. Lee, J. H., J. B. Rho, K. J. Park, C. B. Kim, Y. S. Han, S. H. Choi, et al. 2004a. Role of flagellum and motility in pathogenesis of Vibrio vulnificus. Infect. Immun. 72:4905-4910.
37. Lee, S. E., P. Y. Ryu, S. Y. Kim, Y. R. Kim, J. T. Koh, O. J. Kim, et al. 2004b. Production of Vibrio vulnificus hemolysin in vivo and its pathogenic significance. Biochem. Biophys. Res. Commun. 324:86-91.
38. Lee, S., A. I. Arunkumar, X. Chen, and D. P. Giedroc. 2006. Structural insights into homo- and heterotropic allosteric coupling in the zinc sensor S. aureus CzrA from covalently fused dimers. J. Am. Chem. Soc. 128:1937-1947.
39. Lee, J. H., M. W. Kim, B. S. Kim, S. M. Kim, B. C. Lee, T. S. Kim, et al. 2007a. Identification and characterization of the Vibrio vulnificus rtxA essential for cytotoxicity in vitro and virulence in mice. J. Microbiol. 45:146-152.
40. Lee, J. H., J. E. Rhee, U. Park, H. M. Ju, B. C. Lee, T. S. Kim, et al. 2007b. Identification and functional analysis of Vibrio vulnificus SmcR, a novel global regulator. J. Microbiol. Biotechnol. 17:325-334.
41. Lee, B. C., S. H. Choi, and T. S. Kim. 2008a. Vibrio vulnificus RTX toxin plays an important role in the apoptotic death of human intestinal epithelial cells exposed to Vibrio vulnificus. Microbes Infect. 10:1504-1513.
42. Lee, B. C., J. H. Lee, M. W. Kim, B. S. Kim, M. H. Oh, K. S. Kim, et al. 2008b. Vibrio vulnificus rtxE is important for virulence, and its expression is induced by exposure to host cells. Infect. Immun. 76:1509-1517.
43. Li, L., J. L. Rock, and D. R. Nelson. 2008. Identification and characterization of a repeat-in-toxin gene cluster in Vibrio anguillarum. Infect. Immun. 76:2620-2632.
44. Lin, W., K. J. Fullner, R. Clayton, J. A. Sexton, M. B. Rogers, K. E. Calia, 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 96:1071-1076.
45. Linhartova, I., L. Bumba, J. Masin, M. Basler, R. Osicka, J. Kamanova, et al. 2010. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol. Rev. 34:1076-1112.
46. Lithgow, J. K., F. Haider, I. S. Roberts, and J. Green. 2007. Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12. Mol. Microbiol. 66:685-698.
47. Litwin, C. M., T. W. Rayback, and J. Skinner. 1996. Role of catechol siderophore synthesis in Vibrio vulnificus virulence. Infect. Immun. 64:2834-2838.
48. Liu, M., A. F. Alice, H. Naka, and J. H. Crosa. 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. 75:3282-3289.
49. Liu, M., H. Naka, and J. H. Crosa. 2009. HlyU acts as an H-NS antirepressor in the regulation of the RTX toxin gene essential for the virulence of the human pathogen Vibrio vulnificus CMCP6. Mol. Microbiol. 72:491-505.
50. Liu, M., M. Rose, and J. H. 2011. Homodimerization and binding of specific domains to the target DNA are essential requirements for HlyU to regulate expression of the virulence gene rtxA1 encoding the repeat-in-toxin protein in the human pathogen Vibrio vulnificus. J. Bacteriol. 193: 6895-6901.
51. Lo, H. R., J. H. Lin, Y. H. Chen, C. L. Chen, C. P. Shao, Y. C. Lai, et al. 2011. RTX toxin enhances the survival of Vibrio vulnificus during infection by protecting the organism from phagocytosis. J. Infect. Dis. 203:1866-1874.
52. Morby, A. P., J. S. Turner, J. W. Huckle, and N. J. Robinson. 1993. SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA: identification of a Zn inhibited DNA-protein complex. Nucleic Acids Res. 21:921-925.
53. Mouzopoulos, G., M. Stamatakos, M. Tzurbakis, G. Batanis, E. Michou, D. Mouzopoulos, et al. 2008. Lower extremity infections by Vibrio vulnificus. Chirurgia (Bucur) 103:201-203.
54. Muldrew, K. L., R. R. Miller, M. Kressin, Y. W. Tang, and C. Stratton. 2007. Necrotizing fasciitis from Vibrio vulnificus in a patient with undiagnosed hepatitis and cirrhosis. J. Clin. Microbiol. 45:1058-1062.
55. Nishi, K., H. J. Lee, S. Y. Park, S. J. Bae, S. E. Lee, P. D. Adams, et al. 2010. Crystal structure of the transcriptional activator HlyU from Vibrio vulnificus CMCP6. FEBS Lett. 584:1097-1102.
56. Oliver, J. D. 2005. Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiol. Infect. 133:383-391.
57. Olivier, V., G. K. Haines III, Y. Tan, and K. J. Satchell. 2007. Hemolysin and the multifunctional autoprocessing RTX toxin are virulence factors during intestinal infection of mice with Vibrio cholerae El Tor O1 strains. Infect. Immun. 75:5035-5042.
58. Paranjpye, R. N., and M. S. Strom. 2005. A Vibrio vulnificus type IV pilin contributes to biofilm formation, adherence to epithelial cells, and virulence. Infect. Immun. 73:1411-1422.
59. Pukatzki, S., A. T. Ma, D. Sturtevant, B. Krastins, D. Sarracino, W. C. Nelson, et al. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 103:1528-1533.
60. Rock, J. L., and D. R. Nelson. 2006. Identification and characterization of a hemolysin gene cluster in Vibrio anguillarum. Infect. Immun. 74:2777-2786.
61. Roh, J. B., M. A. Lee, H. J. Lee, S. M. Kim, Y. Cho, Y. J. Kim, et al. 2006. Transcriptional regulatory cascade for elastase production in Vibrio vulnificus: LuxO activates luxT expression and LuxT represses smcR expression. J. Biol. Chem. 281:34775-34784.
62. Roig, F. J., F. Gonzalez-Candelas, and C. Amaro. 2011. Domain organization and evolution of multifunctional autoprocessing repeats-in-toxin (MARTX) toxin in Vibrio vulnificus. Appl. Environ. Microbiol. 77:657-668.
63. Saha, R. P., G. Basu, and P. Chakrabarti. 2006. Cloning, expression, purification, and characterization of Vibrio cholerae transcriptional activator, HlyU. Protein Expr. Purif. 48:118-125.
64. Satchell, K. J. 2007. MARTX, multifunctional autoprocessing repeats-in-toxin toxins. Infect. Immun. 75:5079-5084.
65. Shao, C. P., and L. I. Hor. 2000. Metalloprotease is not essential for Vibrio vulnificus virulence in mice. Infect. Immun. 68:3569-3573.
66. Shao, C. P., H. R. Lo, J. H. Lin, and L. I. Hor. 2011. Regulation of cytotoxicity by quorum-sensing signaling in Vibrio vulnificus is mediated by SmcR, a repressor of hlyU. J. Bacteriol. 193:2557-2565.
67. Sheahan, K. L., and K. J. Satchell. 2007. Inactivation of small Rho GTPases by the multifunctional RTX toxin from Vibrio cholerae. Cell. Microbiol. 9:1324-1335.
68. Sheahan, K. L., C. L. Cordero, and K. J. Satchell. 2004. Identification of a domain within the multifunctional Vibrio cholerae RTX toxin that covalently cross-links actin. Proc. Natl. Acad. Sci. USA 101:9798-9803.
69. Shi, W., J. Wu, and B. P. Rosen. 1994. Identification of a putative metal binding site in a new family of metalloregulatory proteins. J. Biol. Chem. 269:19826-19829.
70. Shinoda, S., and S. Miyoshi. 2011. Proteases produced by Vibrios. Biocontrol Sci. 16:1-11.
71. Smith, A. B., and R. J. Siebeling. 2003. Identification of genetic loci required for capsular expression in Vibrio vulnificus. Infect. Immun. 71:1091-1097.
72. Stoebner, J. A., and S. M. Payne. 1988. Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect. Immun. 56:2891-2895.
73. Sun, Y., M. D. Wong, and B. P. Rosen. 2001. Role of cysteinyl residues in sensing Pb(II), Cd(II), and Zn(II) by the plasmid pI258 CadC repressor. J. Biol. Chem. 276:14955-14960.
74. Tendeng, C., and P. N. Bertin. 2003. H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol. 11:511-518.
75. Tsuchiya, T., E. Mitsuo, N. Hayashi, Y. Hikita, H. Nakao, S. Yamamoto, et al. 2007. Vibrio vulnificus damages macrophages during the early phase of infection. Infect. Immun. 75:4592-4596.
76. Vinh, D. C., S. Mubareka, B. Fatoye, P. Plourde, and P. Orr. 2006. Vibrio vulnificus septicemia after handling Tilapia species fish: a Canadian case report and review. Can. J. Infect. Dis. Med. Microbiol. 17:129-132.
77. Vollberg, C. M., and J. L. Herrera. 1997. Vibrio vulnificus infection: an important cause of septicemia in patients with cirrhosis. South. Med. J. 90:1040-1042.
78. Wang, J., T. Sasaki, Y. Maehara, H. Nakao, T. Tsuchiya, and S. Miyoshi. 2008. Variation of extracellular proteases produced by Vibrio vulnificus clinical isolates: genetic diversity of the metalloprotease gene (vvp), and serine protease secretion by vvp-negative strains. Microb. Pathog. 44:494-500.
79. Williams, S. G., and P. A. Manning. 1991. Transcription of the Vibrio cholerae haemolysin gene, hlyA, and cloning of a positive regulatory locus, hlyU. Mol. Microbiol. 5:2031-2038.
80. Williams, S. G., S. R. Attridge, and P. A. Manning. 1993. The transcriptional activator HlyU of Vibrio cholerae: nucleotide sequence and role in virulence gene expression. Mol. Microbiol. 9:751-760.
81. Williams, S. G., L. T. Varcoe, S. R. Attridge, and P. A. Manning. 1996. Vibrio cholerae Hcp, a secreted protein coregulated with HlyA. Infect. Immun. 64:283-289.
82. Wright, A. C., and J. G. J. Morris. 1991. The extracellular cytolysin of Vibrio vulnificus: inactivation and relationship to virulence in mice. Infect. Immun. 59:192-197.
83. Wright, A. C., L. M. Simpson, J. D. Oliver, and J. G. J. Morris. 1990. Phenotypic evaluation of acapsular transposon mutants of Vibrio vulnificus. Infect. Immun. 58:1769-1773.
84. Wu, J., and B. P. Rosen. 1993. Metalloregulated expression of the ars operon. J. Biol. Chem. 268:52-58.
85. Zhang, Y. B., S. Monchy, B. Greenberg, M. Mergeay, O. Gang, S. Taghavi, et al. 2009. ArsR arsenic-resistance regulatory protein from Cupriavidus metallidurans CH34. Antonie Van Leeuwenhoek 96:161-170.