Cytotoxic and inflammatory responses induced by outer membrane vesicle-associated biologically active proteases from Vibrio cholerae

Infection and Immunity

Volumn 84, Issue 5, 2016, Pages 1478-1490

  Mondal, Ayan ^a   Tapader, Rima ^a   Chatterjee, Nabendu Sekhar ^a   Ghosh, Amit ^a,c   Sinha, Ritam ^a   Koley, Hemanta ^a   Saha, Dhira Rani ^a   Chakrabarti, Manoj K ^a   Wai, Sun Nyunt ^b   Pal, Amit ^a  

^a NATIONAL INSTITUTE OF CHOLERA AND ENTERIC DISEASES   (India)

^b UMEÅ UNIVERSITY   (Sweden)

^c ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 8; PROTEINASE; SERINE PROTEINASE; PEPTIDE HYDROLASE; VIRULENCE FACTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL OUTER MEMBRANE; CYTOTOXICITY; ENZYME RELEASE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; INTESTINE EPITHELIUM CELL; MEMBRANE VESICLE; MOUSE; NECROSIS; NONHUMAN; PRIORITY JOURNAL; VIBRIO CHOLERAE; ANIMAL; BAGG ALBINO MOUSE; CELL DEATH; CELL LINE; ENZYMOLOGY; EPITHELIUM CELL; EXOSOME; ILEUM; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY;

ANIMALS; CELL DEATH; CELL LINE; EPITHELIAL CELLS; EXOSOMES; HUMANS; ILEUM; INFLAMMATION; MICE, INBRED BALB C; PEPTIDE HYDROLASES; VIBRIO CHOLERAE; VIRULENCE FACTORS;

EID: 84965095965     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01365-15     Document Type: Article

References (59)

1. Farmer P, Almazor CP, Bahnsen ET, Barry D, Bazile J, Bloom BR, Bose N, Brewer T, Calderwood SB, Clemens JD, Cravioto A, Eustache E, Jérôme G, Gupta N, Harris JB, Hiatt HH, Holstein C, Hotez PJ, Ivers LC, Kerry VB, Koenig SP, Larocque RC, Léandre F, Lambert W, Lyon E, Mekalanos JJ, Mukherjee JS, Oswald C, Pape JW, Gretchko Prosper A, Rabinovich R, Raymonville M, Réjouit JR, Ronan LJ, Rosenberg ML, Ryan ET, Sachs JD, Sack DA, Surena C, Suri AA, Ternier R, Waldor MK, Walton D, Weigel JL. 2011. Meeting cholera's challenge to Haiti and the world: a joint statement on cholera prevention and care. PLoS Negl Trop Dis 5:e1145. http://dx.doi.org/10.1371/journal.pntd.0001145.
2. Faruque SM, Albert MJ, Mekalanos JJ. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62:1301-1314.
3. Miyoshi S. 2013. Extracellular proteolytic enzymes produced by human pathogenic Vibrio species. Front Microbiol 4:339. http://dx.doi.org/10.3389/fmicb.2013.00339.
4. Häse CC, Finkelstein RA. 1991. Cloning and nucleotide sequence of the Vibrio cholerae hemagglutinin/protease (HA/protease) gene and construction of an HA/protease-negative strain. J Bacteriol 173:3311-3317.
5. Finkelstein RA, Boesman-Finkelstein M, Chang Y, Häse CC. 1992. Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infect Immun 60:472-478.
6. Booth BA, Boesman-Finkelstein M, Finkelstein RA. 1984. Vibrio cholerae hemagglutinin/protease nicks cholera enterotoxin. Infect Immun 45: 558-560.
7. Nagamune K, Yamamoto K, Honda T. 1997. Intramolecular chaperone activity of the pro-region of Vibrio cholerae El Tor cytolysin. J Biol Chem 272:1338-1343. http://dx.doi.org/10.1074/jbc.272.2.1338.
8. Ghosh A, Saha DR, Hoque KM, Asakuna M, Yamasaki S, Koley H, Das SS, Chakrabarti MK, Pal A. 2006. Enterotoxigenicity of mature 45-kilodalton and processed 35-kilodalton forms of hemagglutinin protease purified from a cholera toxin gene-negative Vibrio cholerae non-O1, non-O139 strain. Infect Immun 74:2937-2946. http://dx.doi.org/10.1128/IAI.74.5.2937-2946.2006.
9. Vaitkevicius K, Lindmark B, Ou G, Song T, Toma C, Iwanaga M, Zhu J, Andersson A, Hammarström ML, Tuck S, Wai SN. 2006. A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. Proc Natl Acad Sci U S A 103: 9280-9285. http://dx.doi.org/10.1073/pnas.0601754103.
10. Syngkon A, Elluri S, Koley H, Rompikunata PK, Saha DR, Chakrabarti MK, Bhadra RK, Wai SN, Pal A. 2010. Studies on a novel serine protease of a ΔhapAΔprtV Vibrio cholerae O1 strain and its role in haemorrhagic response in the rabbit ileal loop model. PLoS One 5:e13122. http://dx.doi.org/10.1371/journal.pone.0013122.
11. Pugsley AP. 1993. The complete general secretory pathway in gramnegative bacteria. Microbiol Rev 57:50-108.
12. Kuehn MJ, Kesty NC. 2005. Bacterial outer membrane vesicles and host pathogen interaction. Genes Dev 19:2645-2655. http://dx.doi.org/10.1101/gad.1299905.
13. Wai SN, Lindmark B, Soderblom T, Takade A, Westermark M, Oscarsson J, Jass J, Richter-Dhalfors A, Mizunoe Y, Uhlin BE. 2003. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:25-35. http://dx.doi.org/10.1016/S0092-8674(03)00754-2.
14. Balsalobre C, Silvan JM, Berglund S, Mizunoe Y, Uhlin BE, Wai SN. 2006. Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol Microbiol 59:99-112. http://dx.doi.org/10.1111/j.1365-2958.2005.04938.x.
15. Davis JM, Carvalho HM, Rasmussen SB, O'Brien AD. 2006. Cytotoxic necrotizing factor type 1 delivered by outer membrane vesicles of uropathogenic E. coli attenuates polymorphonuclear leukocyte antimicrobial activity and chemotaxis. Infect Immun 74:4401-4408. http://dx.doi.org/10.1128/IAI.00637-06.
16. Lindmark B, Rompikuntal PK, Vaitkevicius K, Song T, Mizunoe Y, Uhlin BE, Guerry P, Wai SN. 2009. Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol 9:220. http://dx.doi.org/10.1186/1471-2180-9-220.
17. Parker H, Chitcholtan K, Hampton MB, Keenan JI. 2010. Uptake of Helicobacter pylori outer membrane vesicles by gastric epithelial cells. Infect Immun 78:5054-5061. http://dx.doi.org/10.1128/IAI.00299-10.
18. Bomberger JM, MacEachran DP, Coutermarsh BA, Ye S, O'Toole GA, Stanton BA. 2009. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5:e1000382. http://dx.doi.org/10.1371/journal.ppat.1000382.
19. Chatterjee D, Chaudhuri K. 2011. Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett 585:1357-1362. http://dx.doi.org/10.1016/j.febslet.2011.04.017.
20. Elluri S, Enow C, Vdovikova S, Rompikunal P, Dongre M, Carlsson S, Pal A, Uhlin BE, Wai SN. 2014. Outer membrane vesicles mediate transport of biologically active Vibrio cholerae cytolysin (VCC) from V. cholerae strains. PLoS One 9:e106731. http://dx.doi.org/10.1371/journal.pone.0106731.
21. Rompikuntal PK, Vdovikova S, Duperthuy M, Jhonson TL, Ahlund M, Lundmark R, Oscarson J, Sandkvist M, Uhlin BE, Wai SN. 2015. Outer membrane vesicle mediated export of processed PrtV protease from Vibrio cholerae. PLoS One 10:e0134098. http://dx.doi.org/10.1371/journal.pone.0134098.
22. Altindis E, Fu Y, Mekalanos JJ. 2014. Proteomic analysis of Vibrio cholerae outer membrane vesicles. Proc Natl Acad Sci U S A 111:E1548-E1556. http://dx.doi.org/10.1073/pnas.1403683111.
23. Gosink KK, Kobayashi R, Kawagishi I, Hase CC. 2002. Analyses of the roles of three cheA homologs in chemotaxis of Vibrio cholerae. J Bacteriol 184:1767-1771. http://dx.doi.org/10.1128/JB.184.6.1767-1771.2002.
24. Chen DJ, Osterrieder N, Metzger SM, Buckles E, Doody AM, DeLisa MP, Putnam D. 2010. Delivery of foreign antigens by engineered outer membrane vesicle vaccines. Proc Natl Acad Sci U S A 107:3099-3104. http://dx.doi.org/10.1073/pnas.0805532107.
25. Schild S, Nelson EJ, Camilli A. 2008. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect Immun 76:4554-4563. http://dx.doi.org/10.1128/IAI.00532-08.
26. Cheng LW, Schneewind O. 2000. Yersinia enterocolitica TyeA, an intracellular regulator of the type III machinery, is required for specific targeting of YopE, YopH, YopM, and YopN into the cytosol of eukaryotic cells. J Bacteriol 182:3183-3190. http://dx.doi.org/10.1128/JB.182.11.3183-3190.2000.
27. Parker H, Chitcholtan K, Hampton MB, Keenan JI. 2010. Uptake of Helicobacter pylori outer membrane vesicles by gastric epithelial cells. Infect Immun 72:5054-5061. http://dx.doi.org/10.1128/IAI.00299-10.
28. Sawasvirojwong S, Srimanote P, Chatsudthipong V, Muanprasat C. 2013. An adult mouse model of Vibrio cholerae induced diarrhea for studying pathogenesis and potential therapy of cholera. PLoS Negl Trop Dis 7:e2293. http://dx.doi.org/10.1371/journal.pntd.0002293.
29. Thay B, Wai SN, Oscarsson J. 2013. Staphylococcus aureus α-toxin dependent induction of host cell death by membrane derived vesicles. PLoS One 8:e54661. http://dx.doi.org/10.1371/journal.pone.0054661.
30. Oku Y, Uesaka Y, Hirayama T, Takeda Y. 1988. Development of highly sensitive bead-ELISA to detect bacterial protein toxins. Microbiol Immunol 32:807-816. http://dx.doi.org/10.1111/j.1348-0421.1988.tb01442.x.
31. Olivier V, Queen J, Satchell KJF. 2009. Successful small intestine colonization of adult mice by Vibrio cholerae requires ketamine anesthesia and accessory toxins. PLoS One 4:e7352. http://dx.doi.org/10.1371/journal.pone.0007352.
32. Chatterjee SN, Das J. 1967. Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J Gen Microbiol 49:1-11. http://dx.doi.org/10.1099/00221287-49-1-1.
33. Rodal SK, Skretting G, Garred F, Vilhardt B, Van Duers B, Sandvig. 1999. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 10:961-974. http://dx.doi.org/10.1091/mbc.10.4.961.
34. Bonnington KE, Kuehn MJ. 2014. Protein secretion and export via outer membrane vesicles. Biochim Biophys Acta 1843:1612-1619. http://dx.doi.org/10.1016/j.bbamcr.2013.12.011.
35. - secretion via modulation of apical KCNN4c channels in diarrhea. J Biol Chem 288:20404-20415. http://dx.doi.org/10.1074/jbc.M113.467860.
36. Scott ME, Dossani ZY, Sandkvist M. 2001. Directed polar secretion of protease from single cells of Vibrio cholerae via the type II secretion pathway. Proc Natl Acad SciUS A 98:13978-13983. http://dx.doi.org/10.1073/pnas.241411198.
37. Young DB, Broadbent DA. 1982. Biochemical characterization of extracellular proteases from Vibrio cholerae. Infect Immun 37:875-883.
38. Sikora AE, Zielke RA, Lawrence DA, Andrews PC, Sandkvist M. 2011. Proteomic analysis of the Vibrio cholerae type II secretome reveals new proteins, including three related serine proteases. J Biol Chem 286:16555-16566. http://dx.doi.org/10.1074/jbc.M110.211078.
39. Silva AJ, Pham K, Benitez JA. 2003. Hemaglutinnin/protease expression and mucin gel penetration in El Tor biotype Vibrio cholerae. Microbiology 149:1883-1891. http://dx.doi.org/10.1099/mic.0.26086-0.
40. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163-184. http://dx.doi.org/10.1146/annurev.micro.091208.073413.
41. Boardman BK, Meehan BM, Fullner-Satchell KJ. 2007. Growth phase regulation of Vibrio cholerae RTX toxin export. J Bacteriol 189:1827-1835. http://dx.doi.org/10.1128/JB.01766-06.
42. Ikigai H, Ono T, Nakae T, Otsuru H, Shimamura T. 1999. Two form of Vibrio cholerae O1 El Tor hemolysin derived from identical precursor protein. Biochim Biophys Acta 1415:297-305. http://dx.doi.org/10.1016/S0005-2736(98)00183-7.
43. Benitez JA, Silva AJ, Finkelstein RA. 2001. Environmental signals controlling production of hemagglutinin/protease in Vibrio cholerae. Infect Immun 69:6549-6553. http://dx.doi.org/10.1128/IAI.69.10.6549-6553.2001.
44. Bénitez JA, Spelbrink RG, Silva A, Phillips TE, Stanley CM, Boesman-Finkelstein M, Finkelstein RA. 1997. Adherence of Vibrio cholerae to cultured differentiated human intestinal cells: an in vitro colonization model. Infect Immun 65:3474-3477.
45. Zhou X, Gao DQ, Michalski J, Benitez JA, Kaper JB. 2004. Induction of interleukin-8 in T84 cells by Vibrio cholerae. Infect Immun 72:389-397. http://dx.doi.org/10.1128/IAI.72.1.389-397.2004.
46. Ou G, Rompikuntal PK, Bitar A, Lindmark B, Vaitkevicius K, Wai SN, Hammarström ML. 2009. Vibrio cholerae cytolysin causes an inflammatory response in human intestinal epithelial cells that is modulated by the PrtV protease. PLoS One 4:e7806. http://dx.doi.org/10.1371/journal.pone.0007806.
47. Whitmire WM, Garon CF. 1993. Specific and nonspecific responses of murine B cells to membrane blebs of Borrelia burgdoferi. Infect Immun 61:1460-1467.
48. Opal SM. 2007. The host response to endotoxin, antilipopolysaccaride strategies, and the management of severe sepsis. Int J Med Microbiol 297: 365-377. http://dx.doi.org/10.1016/j.ijmm.2007.03.006.
49. Ellis TN, Kuehn MJ. 2010. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 74:81-94. http://dx.doi.org/10.1128/MMBR.00031-09.
50. Alaniz RC, Deatherage BL, Lara JC, Cookson BT. 2007. Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J Immunol 179:7692-7701. http://dx.doi.org/10.4049/jimmunol.179.11.7692.
51. Bauman SJ, Kuehn MJ. 2006. Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect 8:2400-2408. http://dx.doi.org/10.1016/j.micinf.2006.05.001.
52. Ismail S, Hampton MB, Keenan JI. 2003. Helicobacter pylori outer membrane vesicles modulate proliferation and interleukin-8 production by gastric epithelial cells. Infect Immun 71:5670-5675. http://dx.doi.org/10.1128/IAI.71.10.5670-5675.2003.
53. McCormick BA, Siber AM, Maurelli AT. 1998. Requirement of the Shigella flexneri virulence plasmid in the ability to induce trafficking of neutrophils across polarized monolayers of the intestinal epithelium. Infect Immun 66:4237-4243.
54. Chatterjee D, Chaudhuri K. 2013. Vibrio cholera O395 outer membrane vesicles modulate intestinal epithelial cells in a NOD1 dependent manner and induces dendritic cell-mediated Th2/Th17 responses. J Biol Chem 288:4299-4309. http://dx.doi.org/10.1074/jbc.M112.408302.
55. Holst J, Martin D, Arnold R, Huergo CC, Oster P, O'Hallahhan J, Rosenqvist E. 2009. Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitides. Vaccine 27: B3-B12. http://dx.doi.org/10.1016/j.vaccine.2009.04.071.
56. Haralalka S, Nandi S, Bhadra RK. 2003. Mutation in the relA gene of Vibrio cholerae affects in vitro and in vivo expression of virulence factors. J Bacteriol 185:4672-4682. http://dx.doi.org/10.1128/JB.185.16.4672-4682.2003.
57. Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, Morzycka-Wroblewska E, Kagnoff MF. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 95:55-65. http://dx.doi.org/10.1172/JCI117676.
58. Sarkar M, Chaudhuri K. 2004. Association of adherence and motility in interleukin 8 induction in human intestinal epithelial cells by Vibrio cholerae. Microbes Infect 6:676-685. http://dx.doi.org/10.1016/j.micinf.2004.02.018.
59. Silva AJ, Leitch GJ, Camilli A, Benitez JA. 2006. Contribution of hemagglutinin/protease and motility to the pathogenesis of El Tor biotype cholera. Infect Immun 74:2072-2079. http://dx.doi.org/10.1128/IAI.74.4.2072-2079.2006.