The Vibrio cholerae cytolysin promotes chloride secretion from intact human intestinal mucosa

PLoS ONE

Volumn 4, Issue 3, 2009, Pages

  Debellis, Lucantonio ^a   Diana, Anna ^a   Arcidiacono, Diletta ^b   Fiorotto, Romina ^c   Portincasa, Piero ^d   Altomare, Donato Francesco ^a   Spirlì, Carlo ^c   de Bernard, Marina ^b,e  

^a UNIVERSITY OF BARI   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

^e UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE; CYTOLYSIN; HEMOLYSIN; PERFORIN;

ARTICLE; BACTERIAL STRAIN; CELL LEVEL; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE RESISTANCE; CHLORIDE TRANSPORT; COLON RESECTION; CONTROLLED STUDY; DIARRHEA; DIGESTIVE SYSTEM ELECTROPHYSIOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE CELL; INTESTINE MUCOSA; PATHOGENESIS; SHORT CIRCUIT CURRENT; SIGMOID; SODIUM TRANSPORT; TRANSEPITHELIAL RESISTANCE; VIBRIO CHOLERAE; VOLTAGE CLAMP; WATER TRANSPORT; COLON; ELECTROPHYSIOLOGY; METABOLISM; METHODOLOGY; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

VIBRIO CHOLERAE;

CHLORIDES; COLON; DIARRHEA; ELECTROPHYSIOLOGY; HEMOLYSIN PROTEINS; HUMANS; INTESTINAL MUCOSA; PERFORIN; VIBRIO CHOLERAE; VIRULENCE;

EID: 63749099761     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005074     Document Type: Article

References (46)

1. World Health Organization (2001) Cholera vaccines. Wkly Epidemiol Rec 76: 117-124.
2. Faruque SM, Albert MJ, Mekalanos JJ (1998) Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62: 1301-1314.
3. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, et al. (1998) A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci U S A 95: 3134-3139.
4. Sanyal SC, Huq MI, Neogy PK, Alam K, Kabir MI, et al. (1984) Experimental studies on the pathogenicity of Vibrio mimicus strains isolated in Bangladesh. Aust J Exp Biol Med Sci 62: 515-521.
5. Saha DR, Pal A, Rajendran K, Dutta P (2006) Histopathological changes in experimental cholera with a non toxigenic non- O1 non-O139 Vibrio cholerae strain isolated from Kolkata, India. Indian J Exp Biol 44: 221-227.
6. Saka HA, Bidinost C, Sola C, Carranza P, Collino C, et al. (2008) Vibrio cholerae cytolysin is essential for high enterotoxicity and apoptosis induction produced by a cholera toxin gene-negative V. cholerae non-O1, non-O139 strain. Microb Pathog 44: 118-128.
7. Coelho A, Andrade JR, Vicente AC, Salles CA (1995) New variant of Vibrio cholerae O1 from clinical isolates in Amazonia. J Clin Microbiol 33: 114-118.
8. Saha PK, Koley H, Mukhopadhyay AK, Bhattacharya SK, Nair GB, et al. (1996) Nontoxigenic Vibrio cholerae O1 serotype Inaba biotype E1 Tor associated with a cluster of cases of cholera in southern India. J Clin Microbiol 34: 1114-1147.
9. Ninin E, Caroff N, El Kouri D, Espaze E, Richet H, et al. (2000) Nontoxigenic Vibrio cholerae O1 bacteremia: case report and review. Eur J Clin Microbiol Infect Dis 19: 489-491.
10. Alm RA, Stroeher UH, Manning PA (1988) Extracellular proteins of Vibrio cholerae: nucleotide sequence of the structural gene (hlyA) for the haemolysin of the haemolytic El Tor strain 017 and characterization of the hlyA mutation in the non-haemolytic classical strain 569B. Mol Microbiol 2: 481-488.
11. Yamamoto K, Ichinose Y, Shinagawa H, Makino K, Nakata A, et al. (1990) Two-step processing for activation of the cytolysin/hemolysin of Vibrio cholerae O1 biotype El Tor: nucleotide sequence of the structural gene (hlyA) and characterization of the processed products. Infect Immun 58: 4106-4116.
12. Nagamune K, Yamamoto K, Honda T (1997) Intramolecular chaperone activity of the pro-region of Vibrio cholerae El Tor cytolysin. J Biol Chem 10: 1338-1343.
13. Zitzer A, Zitzer O, Bhakdi S, Palmer M (1999) Oligomerization of Vibrio cholerae cytolysin yields a pentameric pore and has a dual specificity for cholesterol and sphingolipids in the target membrane. J Biol Chem 274: 1375-1380.
14. Krasilnikov OV, Merzlyak PG, Lima VL, Zitzer AO, Valeva A, et al. (2007) Pore formation by Vibrio cholerae cytolysin requires cholesterol in both monolayers of the target membrane. Biochimie 89: 271-277.
15. Pantano S, Montecucco C (2006) A molecular model of the Vibrio cholerae cytolysin transmembrane pore. Toxicon 47: 35-40.
16. Coelho A, Andrade JR, Vicentem AC, Dirita VJ (2000) Cytotoxic cell vacuolating activity from Vibrio cholerae hemolysin. Infect Immun 68: 1700-1705.
17. Figueroa-Arredondo P, Heuser JE, Akopyants NS, Morisaki JH, Giono-Cerezo S, et al. (2001) Cell vacuolation caused by Vibrio cholerae hemolysin. Infect Immun 69: 1613-1624.
18. Moschioni M, Tombola F, de Bernard M, Coelho A, Zitzer A, et al. (2002) The Vibrio cholerae haemolysin anion channel is required for cell vacuolation and death. Cell Microbiol 4: 397-409.
19. Saka HA, Gutiérrez MG, Bocco JL, Colombo MI (2007) The autophagic pathway: a cell survival strategy against the bacterial pore-forming toxin Vibrio cholerae cytolysin. Autophagy 3: 363-365.
20. Hichinose Y, Yamamoto K, Nakasone N, Tanabe MJ, Takeda T, et al. (1987) Enterotoxicity of El Tor-like hemolysin of non-O1 Vibrio cholerae. Infect Immun 55: 1090-1093.
21. Singh DV, Matte MH, Matte GR, Jiang S, Sabeena F, et al. (2001) Molecular analysis of Vibrio cholerae O1, O139, non-O1, and non-O139 strains: clonal relationships between clinical and environmental isolates. Appl Environ Microbiol 67: 910-921.
22. Laohachai KN, Bahadi R, Hardo MB, Hardo PG, Kourie JI (2003) The role of bacterial toxins in the induction of changes in membrane transport: implications for diarrhoea. Toxicon 42: 687-707.
23. Hall RH, Drasar BS (1990) Vibrio cholerae HlyA hemolysin is processed by proteolysis. Infect Immun 58: 3375-3379.
24. Zitzer A, Palmer M, Weller U, Wassenaar T, Biermann C, et al. (1997) Mode of primary binding to target membranes and pore formation induced by Vibrio cholerae cytolysin (hemolysin). Eur J Biochem 247: 209-216.
25. Spirlì C, Nathanson MH, Fiorotto R, Duner E, Denson LA, et al. (2001) Proinflammatory cytokines inhibit secretion in rat bile duct epithelium. Gastroenterology 121: 156-169.
26. Biwersi J, Verkman AS (1991) Cell-permeable fluorescent indicator for cytosolic chloride. Biochemistry 30: 7879-7883.
27. Flemström G, Hällgren A, Nylander O, Engstrand L, Wilander E, et al. (1999) Adherent surface mucus gel restricts diffusion of macromolecules in rat duodenum in vivo. Am J Physiol 277: G375-G382.
28. Debellis L, Papini E, Caroppo R, Montecucco C, Curci S (2001) Helicobacter pylori cytotoxin VacA increases alkaline secretion in gastric epithelial cells. Am J Physiol Gastrointest Liver Physiol 281: G1440-G1448.
29. Mayol JM, Adame-Navarrete Y, Alarma-Estrany P, Molina-Roldan E, Huete-Toral F, et al. (2006) Luminal oxidants selectively modulate electrogenic ion transport in rat colon. World J Gastroenterol 12: 5523-5527.
30. Kunzelmann K, Mall M (2002) Electrolyte transport in the mammalian colon: mechanisms and implications for disease. Physiol Rev 82: 245-289.
31. Atuma C, Strugala V, Allen A, Holm L (2001) The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol Gastrointest Liver Physiol 280: G922-G929.
32. Strugala V, Allen A, Dettmar PW, Pearson JP (2003) Colonic mucin: methods of measuring mucus thickness. Proc Nutr Soc 62: 237-243.
33. Bhakdi S, Bayley H, Valeva A, Walev I, Walker B, Kehoe M, Palmer M (1996) Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch Microbiol 165: 73-79.
34. Eichstaedt S, Gäbler K, Below S, Müller C, Kohler C, Engelmann S, Hildebrandt P, Völker U, Hecker M, Hildebrandt JP (2009) Effects of Staphylococcus aureus-hemolysin A on calcium signalling in immortalized human airway epithelial cells. Cell Calcium 45: 165-176.
35. Prasad M, Ito S, Silen W (1997) Functional studies of in vitro rat distal colon before and after restitution. Surgery 121: 430-439.
36. Gitter AH, Bendfeldt K, Schulzke JD, Fromm M (2000) Trans/paracellular, surface/crypt, and epithelial/subepithelial resistances of mammalian colonic epithelia. Pflugers Arch 439: 477-482.
37. Peixoto EB, Collares-Buzato CB (2005) Protamine-induced epithelial barrier disruption involves rearrangement of cytoskeleton and decreased tight junction-associated protein expression in cultured MDCK strains. Cell Struct Funct 29: 165-178.
38. Sandle GI, Wills NK, Alles W, Binder HJ (1986) Electrophysiology of the human colon: evidence of segmental heterogeneity. Gut 27: 999-1005.
39. Mall M, Bleich M, Leich M, Kuehr J, Brandis M, et al. (1999) CFTR-mediated inhibition of amiloride sensitive sodium conductance by CFTR in human colon is defective in cystic fibrosis. Am J Physiol Gastrointest Liver Physiol 277: G709-G716.
40. Alrefai WA, Ramaswamy K, Dudeja PK (2001) Mechanism(s) of chloride transport in human distal colonic apical membrane vesicles. Dig Dis Sci 46: 2209-2218.
41. - secretion induced by taurodeoxycholate from colon mucosa. Biol Cell 95: 115-122.
42. Greger R, Bleich M, Leipziger J, Ecke D, Mall M, et al. (1997) Regulation of ion transport in colonic crypts. News Physiol Sci 12: 62-66.
43. Blake PA, Weaver RE, Hollis DG (1980) Diseases of humans (other than cholera) caused by vibrios. Annu Rev Microbiol 34: 341-367.
44. Finch MJ, Valdespinom JL, Wellsm JG, Perez-Perez G, Arjona F, et al. (1987) Non-01 Vibrio cholerae infections in Cancun, Mexico. Am J Trop Med Hyg 36: 393-397.
45. Faruque SM, Chowdhury N, Kamruzzaman M, Dziejman M, Rahman MH, et al. (2004) Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. Proc Natl Acad Sci U S A 101: 2123-2128.
46. Zitzer AO, Nakisbekov NO, Li AV, Semiotrokev VL, Kiseliov Y, et al. (1993) Entero-cytolysin (EC) from Vibrio cholerae non-O1 (some properties and poreforming activity). Zentralbl Bakteriol 279: 494-504.