Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1995 Jun;63(6):2093–2099. doi: 10.1128/iai.63.6.2093-2099.1995

Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium.

M Nishibuchi 1, J B Kaper 1
PMCID: PMC173271  PMID: 7768586

Full Text

The Full Text of this article is available as a PDF (290.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albert M. J. Vibrio cholerae O139 Bengal. J Clin Microbiol. 1994 Oct;32(10):2345–2349. doi: 10.1128/jcm.32.10.2345-2349.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baba K., Shirai H., Terai A., Kumagai K., Takeda Y., Nishibuchi M. Similarity of the tdh gene-bearing plasmids of Vibrio cholerae non-O1 and Vibrio parahaemolyticus. Microb Pathog. 1991 Jan;10(1):61–70. doi: 10.1016/0882-4010(91)90066-j. [DOI] [PubMed] [Google Scholar]
  3. Baba K., Shirai H., Terai A., Takeda Y., Nishibuchi M. Analysis of the tdh gene cloned from a tdh gene- and trh gene-positive strain of Vibrio parahaemolyticus. Microbiol Immunol. 1991;35(3):253–258. doi: 10.1111/j.1348-0421.1991.tb01554.x. [DOI] [PubMed] [Google Scholar]
  4. Blake P. A., Weaver R. E., Hollis D. G. Diseases of humans (other than cholera) caused by vibrios. Annu Rev Microbiol. 1980;34:341–367. doi: 10.1146/annurev.mi.34.100180.002013. [DOI] [PubMed] [Google Scholar]
  5. Brown D. F., Spaulding P. L., Twedt R. M. Enteropathogenicity of Vibrio parahaemolyticus in the ligated rabbit ileum. Appl Environ Microbiol. 1977 Jan;33(1):10–14. doi: 10.1128/aem.33.1.10-14.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Goldberg I., Mekalanos J. J. Effect of a recA mutation on cholera toxin gene amplification and deletion events. J Bacteriol. 1986 Mar;165(3):723–731. doi: 10.1128/jb.165.3.723-731.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Grindley N. D., Joyce C. M. Genetic and DNA sequence analysis of the kanamycin resistance transposon Tn903. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7176–7180. doi: 10.1073/pnas.77.12.7176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hall R. H., Khambaty F. M., Kothary M., Keasler S. P. Non-O1 Vibrio cholerae. Lancet. 1993 Aug 14;342(8868):430–430. doi: 10.1016/0140-6736(93)92839-l. [DOI] [PubMed] [Google Scholar]
  9. Honda T., Abad-Lapuebla M. A., Ni Y. X., Yamamoto K., Miwatani T. Characterization of a new thermostable direct haemolysin produced by a Kanagawa-phenomenon-negative clinical isolate of Vibrio parahaemolyticus. J Gen Microbiol. 1991 Feb;137(2):253–259. doi: 10.1099/00221287-137-2-253. [DOI] [PubMed] [Google Scholar]
  10. Honda T., Chearskul S., Takeda Y., Miwatani T. Immunological methods for detection of Kanagawa phenomenon of Vibrio parahaemolyticus. J Clin Microbiol. 1980 Jun;11(6):600–603. doi: 10.1128/jcm.11.6.600-603.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Honda T., Ni Y. X., Miwatani T. Purification and characterization of a hemolysin produced by a clinical isolate of Kanagawa phenomenon-negative Vibrio parahaemolyticus and related to the thermostable direct hemolysin. Infect Immun. 1988 Apr;56(4):961–965. doi: 10.1128/iai.56.4.961-965.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Honda T., Ni Y., Miwatani T., Adachi T., Kim J. The thermostable direct hemolysin of Vibrio parahaemolyticus is a pore-forming toxin. Can J Microbiol. 1992 Nov;38(11):1175–1180. doi: 10.1139/m92-192. [DOI] [PubMed] [Google Scholar]
  13. Honda T., Nishibuchi M., Miwatani T., Kaper J. B. Demonstration of a plasmid-borne gene encoding a thermostable direct hemolysin in Vibrio cholerae non-O1 strains. Appl Environ Microbiol. 1986 Nov;52(5):1218–1220. doi: 10.1128/aem.52.5.1218-1220.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hondo S., Goto I., Minematsu I., Ikeda N., Asano N., Ishibashi M., Kinoshita Y., Nishibuchi N., Honda T., Miwatani T. Gastroenteritis due to Kanagawa negative Vibrio parahaemolyticus. Lancet. 1987 Feb 7;1(8528):331–332. doi: 10.1016/s0140-6736(87)92062-9. [DOI] [PubMed] [Google Scholar]
  15. Huntley J. S., Hall A. C., Sathyamoorthy V., Hall R. H. Cation flux studies of the lesion induced in human erythrocyte membranes by the thermostable direct hemolysin of Vibrio parahaemolyticus. Infect Immun. 1993 Oct;61(10):4326–4332. doi: 10.1128/iai.61.10.4326-4332.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Iida T., Yamamoto K. Cloning and expression of two genes encoding highly homologous hemolysins from a Kanagawa phenomenon-positive Vibrio parahaemolyticus T4750 strain. Gene. 1990 Sep 1;93(1):9–15. doi: 10.1016/0378-1119(90)90129-f. [DOI] [PubMed] [Google Scholar]
  17. Janda J. M., Powers C., Bryant R. G., Abbott S. L. Current perspectives on the epidemiology and pathogenesis of clinically significant Vibrio spp. Clin Microbiol Rev. 1988 Jul;1(3):245–267. doi: 10.1128/cmr.1.3.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johnson D. E., Calia F. M. False-positive rabbit ileal loop reactions attributed to Vibrio parahaemolyticus broth filtrates. J Infect Dis. 1976 Apr;133(4):436–440. doi: 10.1093/infdis/133.4.436. [DOI] [PubMed] [Google Scholar]
  19. Kaper J. B., Campen R. K., Seidler R. J., Baldini M. M., Falkow S. Cloning of the thermostable direct or Kanagawa phenomenon-associated hemolysin of Vibrio parahaemolyticus. Infect Immun. 1984 Jul;45(1):290–292. doi: 10.1128/iai.45.1.290-292.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kaper J. B., Morris J. G., Jr, Levine M. M. Cholera. Clin Microbiol Rev. 1995 Jan;8(1):48–86. doi: 10.1128/cmr.8.1.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kishishita M., Matsuoka N., Kumagai K., Yamasaki S., Takeda Y., Nishibuchi M. Sequence variation in the thermostable direct hemolysin-related hemolysin (trh) gene of Vibrio parahaemolyticus. Appl Environ Microbiol. 1992 Aug;58(8):2449–2457. doi: 10.1128/aem.58.8.2449-2457.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kita-Tsukamoto K., Oyaizu H., Nanba K., Simidu U. Phylogenetic relationships of marine bacteria, mainly members of the family Vibrionaceae, determined on the basis of 16S rRNA sequences. Int J Syst Bacteriol. 1993 Jan;43(1):8–19. doi: 10.1099/00207713-43-1-8. [DOI] [PubMed] [Google Scholar]
  23. Knapp S., Then I., Wels W., Michel G., Tschäpe H., Hacker J., Goebel W. Analysis of the flanking regions from different haemolysin determinants of Escherichia coli. Mol Gen Genet. 1985;200(3):385–392. doi: 10.1007/BF00425721. [DOI] [PubMed] [Google Scholar]
  24. Koronakis V., Cross M., Senior B., Koronakis E., Hughes C. The secreted hemolysins of Proteus mirabilis, Proteus vulgaris, and Morganella morganii are genetically related to each other and to the alpha-hemolysin of Escherichia coli. J Bacteriol. 1987 Apr;169(4):1509–1515. doi: 10.1128/jb.169.4.1509-1515.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lin Z., Kumagai K., Baba K., Mekalanos J. J., Nishibuchi M. Vibrio parahaemolyticus has a homolog of the Vibrio cholerae toxRS operon that mediates environmentally induced regulation of the thermostable direct hemolysin gene. J Bacteriol. 1993 Jun;175(12):3844–3855. doi: 10.1128/jb.175.12.3844-3855.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mekalanos J. J. Duplication and amplification of toxin genes in Vibrio cholerae. Cell. 1983 Nov;35(1):253–263. doi: 10.1016/0092-8674(83)90228-3. [DOI] [PubMed] [Google Scholar]
  27. Miller V. L., DiRita V. J., Mekalanos J. J. Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter. J Bacteriol. 1989 Mar;171(3):1288–1293. doi: 10.1128/jb.171.3.1288-1293.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Miller V. L., Mekalanos J. J. Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3471–3475. doi: 10.1073/pnas.81.11.3471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Miyamoto Y., Kato T., Obara Y., Akiyama S., Takizawa K., Yamai S. In vitro hemolytic characteristic of Vibrio parahaemolyticus: its close correlation with human pathogenicity. J Bacteriol. 1969 Nov;100(2):1147–1149. doi: 10.1128/jb.100.2.1147-1149.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Miyamoto Y., Obara Y., Nikkawa T., Yamai S., Kato T., Yamada Y., Ohashi M. Simplified purification and biophysicochemical characteristics of Kanagawa phenomenon-associated hemolysin of Vibrio parahaemolyticus. Infect Immun. 1980 May;28(2):567–576. doi: 10.1128/iai.28.2.567-576.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nishibuchi M., Doke S., Toizumi S., Umeda T., Yoh M., Miwatani T. Isolation from a coastal fish of Vibrio hollisae capable of producing a hemolysin similar to the thermostable direct hemolysin of Vibrio parahaemolyticus. Appl Environ Microbiol. 1988 Aug;54(8):2144–2146. doi: 10.1128/aem.54.8.2144-2146.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nishibuchi M., Fasano A., Russell R. G., Kaper J. B. Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect Immun. 1992 Sep;60(9):3539–3545. doi: 10.1128/iai.60.9.3539-3545.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nishibuchi M., Ishibashi M., Takeda Y., Kaper J. B. Detection of the thermostable direct hemolysin gene and related DNA sequences in Vibrio parahaemolyticus and other vibrio species by the DNA colony hybridization test. Infect Immun. 1985 Sep;49(3):481–486. doi: 10.1128/iai.49.3.481-486.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nishibuchi M., Kaper J. B. Duplication and variation of the thermostable direct haemolysin (tdh) gene in Vibrio parahaemolyticus. Mol Microbiol. 1990 Jan;4(1):87–99. doi: 10.1111/j.1365-2958.1990.tb02017.x. [DOI] [PubMed] [Google Scholar]
  35. Nishibuchi M., Kaper J. B. Nucleotide sequence of the thermostable direct hemolysin gene of Vibrio parahaemolyticus. J Bacteriol. 1985 May;162(2):558–564. doi: 10.1128/jb.162.2.558-564.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Nishibuchi M., Khaeomanee-iam V., Honda T., Kaper J. B., Miwatani T. Comparative analysis of the hemolysin genes of Vibrio cholerae non-01, V. mimicus, and V. hollisae that are similar to the tdh gene of V. parahaemolyticus. FEMS Microbiol Lett. 1990 Feb;55(3):251–256. doi: 10.1016/0378-1097(90)90004-a. [DOI] [PubMed] [Google Scholar]
  37. Nishibuchi M., Kumagai K., Kaper J. B. Contribution of the tdh1 gene of Kanagawa phenomenon-positive Vibrio parahaemolyticus to production of extracellular thermostable direct hemolysin. Microb Pathog. 1991 Dec;11(6):453–460. doi: 10.1016/0882-4010(91)90042-9. [DOI] [PubMed] [Google Scholar]
  38. Nishibuchi M., Taniguchi T., Misawa T., Khaeomanee-Iam V., Honda T., Miwatani T. Cloning and nucleotide sequence of the gene (trh) encoding the hemolysin related to the thermostable direct hemolysin of Vibrio parahaemolyticus. Infect Immun. 1989 Sep;57(9):2691–2697. doi: 10.1128/iai.57.9.2691-2697.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Pearson G. D., Woods A., Chiang S. L., Mekalanos J. J. CTX genetic element encodes a site-specific recombination system and an intestinal colonization factor. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3750–3754. doi: 10.1073/pnas.90.8.3750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  41. Sakazaki R., Tamura K., Kato T., Obara Y., Yamai S. Studies on the enteropathogenic, facultatively halophilic bacterium, Vibrio parahaemolyticus. 3. Enteropathogenicity. Jpn J Med Sci Biol. 1968 Oct;21(5):325–331. doi: 10.7883/yoken1952.21.325. [DOI] [PubMed] [Google Scholar]
  42. Sakazaki R., Tamura K., Nakamura A., Kurata T., Goda A. Studies on enteropathogenic activity of Vibrio parahaemolyticus using ligated gut loop model in rabbits. Jpn J Med Sci Biol. 1974 Feb;27(1):35–43. doi: 10.7883/yoken1952.27.35. [DOI] [PubMed] [Google Scholar]
  43. Sakurai J., Matsuzaki A., Miwatani T. Purification and characterization of thermostable direct hemolysin of Vibrio parahaemolyticus. Infect Immun. 1973 Nov;8(5):775–780. doi: 10.1128/iai.8.5.775-780.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Seyama I., Irisawa H., Honda T., Takeda Y., Miwatani T. Effect of hemolysin produced by Vibrio parahaemolyticus on membrane conductance and mechanical tension of rabbit myocardium. Jpn J Physiol. 1977;27(1):43–56. doi: 10.2170/jjphysiol.27.43. [DOI] [PubMed] [Google Scholar]
  45. Shirai H., Ito H., Hirayama T., Nakamoto Y., Nakabayashi N., Kumagai K., Takeda Y., Nishibuchi M. Molecular epidemiologic evidence for association of thermostable direct hemolysin (TDH) and TDH-related hemolysin of Vibrio parahaemolyticus with gastroenteritis. Infect Immun. 1990 Nov;58(11):3568–3573. doi: 10.1128/iai.58.11.3568-3573.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Takashi K., Nishiyama M., Kuga T. Hemolysis and hyperpotassemia in rat induced by the thermostable direct hemolysin of Vibrio parahaemolyticus. Jpn J Pharmacol. 1982 Apr;32(2):377–380. doi: 10.1254/jjp.32.377. [DOI] [PubMed] [Google Scholar]
  47. Takeda Y. Thermostable direct hemolysin of Vibrio parahaemolyticus. Pharmacol Ther. 1982;19(1):123–146. doi: 10.1016/0163-7258(82)90044-4. [DOI] [PubMed] [Google Scholar]
  48. Taniguchi H., Hirano H., Kubomura S., Higashi K., Mizuguchi Y. Comparison of the nucleotide sequences of the genes for the thermostable direct hemolysin and the thermolabile hemolysin from Vibrio parahaemolyticus. Microb Pathog. 1986 Oct;1(5):425–432. doi: 10.1016/0882-4010(86)90004-5. [DOI] [PubMed] [Google Scholar]
  49. Terai A., Baba K., Shirai H., Yoshida O., Takeda Y., Nishibuchi M. Evidence for insertion sequence-mediated spread of the thermostable direct hemolysin gene among Vibrio species. J Bacteriol. 1991 Aug;173(16):5036–5046. doi: 10.1128/jb.173.16.5036-5046.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Terai A., Shirai H., Yoshida O., Takeda Y., Nishibuchi M. Nucleotide sequence of the thermostable direct hemolysin gene (tdh gene) of Vibrio mimicus and its evolutionary relationship with the tdh genes of Vibrio parahaemolyticus. FEMS Microbiol Lett. 1990 Sep 15;59(3):319–323. doi: 10.1016/0378-1097(90)90241-h. [DOI] [PubMed] [Google Scholar]
  51. Tsunasawa S., Sugihara A., Masaki T., Sakiyama F., Takeda Y., Miwatani T., Narita K. Amino acid sequence of thermostable direct hemolysin produced by Vibrio parahaemolyticus. J Biochem. 1987 Jan;101(1):111–121. doi: 10.1093/oxfordjournals.jbchem.a121882. [DOI] [PubMed] [Google Scholar]
  52. Twedt R. M., Peeler J. T., Spaulding P. L. Effective ileal loop dose of Kanagawa-positive Vibrio parahaemolyticus. Appl Environ Microbiol. 1980 Dec;40(6):1012–1016. doi: 10.1128/aem.40.6.1012-1016.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Xu M., Iida T., Yamamoto K., Takarada Y., Miwatani T., Honda T. Demonstration and characterization of simultaneous production of a thermostable direct hemolysin (TDH/I) and a TDH-related hemolysin (TRHx) by a clinically isolated Vibrio parahaemolyticus strain, TH3766. Infect Immun. 1994 Jan;62(1):166–171. doi: 10.1128/iai.62.1.166-171.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Yamasaki S., Shirai H., Takeda Y., Nishibuchi M. Analysis of the gene of Vibrio hollisae encoding the hemolysin similar to the thermostable direct hemolysin of Vibrio parahaemolyticus. FEMS Microbiol Lett. 1991 May 15;64(2-3):259–263. doi: 10.1016/0378-1097(91)90606-b. [DOI] [PubMed] [Google Scholar]
  55. Yoh M., Honda T., Miwatani T., Nishibuchi M. Characterization of thermostable direct hemolysins encoded by four representative tdh genes of Vibrio parahaemolyticus. Microb Pathog. 1991 Feb;10(2):165–172. doi: 10.1016/0882-4010(91)90077-n. [DOI] [PubMed] [Google Scholar]
  56. Zabala J. C., García-Lobo J. M., Diaz-Aroca E., de la Cruz F., Ortiz J. M. Escherichia coli alpha-haemolysin synthesis and export genes are flanked by a direct repetition of IS91-like elements. Mol Gen Genet. 1984;197(1):90–97. doi: 10.1007/BF00327927. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES