Eata, an immunogenic protective antigen of enterotoxigenic escherichia coli, degrades intestinal mucin

Infection and Immunity

Volumn 82, Issue 2, 2014, Pages 500-508

  Kumar, Pardeep ^a   Luo, Qingwei ^a   Vickers, Tim J ^a   Sheikh, Alaullah ^a   Lewis, Warren G ^a   Fleckenstein, James M ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL TOXIN; MUCIN 2; PROTEIN EATA; RECOMBINANT PROTEIN; RECOMBINANT PROTEIN EATA PASSENGER DOMAIN; UNCLASSIFIED DRUG;

ANTIBODY TITER; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL SURFACE; CONTROLLED STUDY; CYTOTOXICITY; ENTEROTOXIGENIC ESCHERICHIA COLI; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOGENICITY; IN VITRO STUDY; INTESTINE CELL; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; INTESTINE MUCOSA; LEUKEMIA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SMALL INTESTINE; VACCINATION;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; ESCHERICHIA COLI VACCINES; HUMANS; HYDROLYSIS; MICE; MUCIN-2; VACCINES, SUBUNIT; VIRULENCE FACTORS;

EID: 84892956435     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01078-13     Document Type: Article

References (53)

1. Levine MM, Kotloff KL, Nataro JP, Muhsen K. 2012. The Global Enteric Multicenter Study (GEMS): impetus, rationale, and genesis. Clin. Infect. Dis. 55(Suppl 4):S215-S224. http://dx.doi.org/10.1093/cid/cis761.
2. Black RE, Morris SS, Bryce J. 2003. Where and why are 10 million children dying every year? Lancet 361:2226-2234. http://dx.doi.org/10.1016/S0140-6736(03)13779-8.
3. Sack RB, Gorbach SL, Banwell JG, Jacobs B, Chatterjee BD, Mitra RC. 1971. Enterotoxigenic Escherichia coli isolated from patients with severe cholera-like disease. J. Infect. Dis. 123:378-385. http://dx.doi.org/10.1093/infdis/123.4.378.
4. Sack DA, McLaughlin JC, Sack RB, Orskov F, Orskov I. 1977. Enterotoxigenic Escherichia coli isolated from patients at a hospital in Dacca. J. Infect. Dis. 135:275-280. http://dx.doi.org/10.1093/infdis/135.2.275.
5. Gupta SK, Keck J, Ram PK, Crump JA, Miller MA, Mintz ED. 2008. Part III. Analysis of data gaps pertaining to enterotoxigenic Escherichia coli infections in low and medium human development index countries, 1984-2005. Epidemiol. Infect. 136:721-738.
6. Qadri F, Saha A, Ahmed T, Al Tarique A, Begum YA, Svennerholm AM. 2007. Disease burden due to enterotoxigenic Escherichia coli in the first 2 years of life in an urban community in Bangladesh. Infect. Immun. 75:3961-3968. http://dx.doi.org/10.1128/IAI.00459-07.
7. Qadri F, Das SK, Faruque ASG, Fuchs GJ, Albert MJ, Sack RB, Svennerholm A-M. 2000. Prevalence of toxin types and colonization factors in enterotoxigenic Escherichia coli isolated during a 2-year period from diarrheal patients in Bangladesh. J. Clin. Microbiol. 38:27-31.
8. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE. 2012. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 379:2151-2161. http: //dx.doi.org/10.1016/S0140-6736(12)60560-1.
9. Fischer Walker CL, Sack D, Black RE. 2010. Etiology of diarrhea in older children, adolescents and adults: a systematic review. PLoS Negl. Trop. Dis. 4:e768. http://dx.doi.org/10.1371/journal.pntd.0000768.
10. Chowdhury F, Rahman MA, Begum YA, Khan AI, Faruque AS, Saha NC, Baby NI, Malek MA, Kumar AR, Svennerholm AM, Pietroni M, Cravioto A, Qadri F. 2011. Impact of rapid urbanization on the rates of infection by Vibrio cholerae O1 and enterotoxigenic Escherichia coli in Dhaka, Bangladesh. PLoS Negl. Trop. Dis. 5:e999. http://dx.doi.org/10.1371/journal.pntd.0000999.
11. Reference deleted.
12. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acacio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209-222. http://dx.doi.org/10.1016/S0140-6736(13)60844-2.
13. Mondal D, Haque R, Sack RB, Kirkpatrick BD, Petri WA, Jr. 2009. Attribution of malnutrition to cause-specific diarrheal illness: evidence from a prospective study of preschool children in Mirpur, Dhaka, Bangladesh. Am. J. Trop. Med. Hyg. 80:824-826.
14. Mondal D, Minak J, Alam M, Liu Y, Dai J, Korpe P, Liu L, Haque R, Petri WA, Jr. 2012. Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh. Clin. Infect. Dis. 54:185-192. http://dx.doi.org/10.1093/cid/cir807.
15. Fleckenstein JM, Hardwidge PR, Munson GP, Rasko DA, Sommerfelt H, Steinsland H. 2010. Molecular mechanisms of enterotoxigenic Escherichia coli infection. Microbes Infect. 12:89-98. http://dx.doi.org/10.1016/j.micinf.2009.10.002.
16. Svennerholm AM, Lundgren A. 2012. Recent progress toward an enterotoxigenic Escherichia coli vaccine. Expert Rev. Vaccines 11:495-507. http: //dx.doi.org/10.1586/erv.12.12.
17. Zhang W, Sack DA. 2012. Progress and hurdles in the development of vaccines against enterotoxigenic Escherichia coli in humans. Expert Rev. Vaccines 11:677-694. http://dx.doi.org/10.1586/erv.12.37.
18. Steinsland H, Valentiner-Branth P, Gjessing HK, Aaby P, Molbak K, Sommerfelt H. 2003. Protection from natural infections with enterotoxigenic Escherichia coli: longitudinal study. Lancet 362:286-291. http://dx .doi.org/10.1016/S0140-6736(03)13971-2.
19. Cravioto A, Reyes RE, Trujillo F, Uribe F, Navarro A, De La Roca JM, Hernandez JM, Perez G, Vazquez V. 1990. Risk of diarrhea during the first year of life associated with initial and subsequent colonization by specific enteropathogens. Am. J. Epidemiol. 131:886-904.
20. Darsley MJ, Chakraborty S, DeNearing B, Sack DA, Feller A, Buchwaldt C, Bourgeois AL, Walker R, Harro CD. 3 October 2012. The oral, live attenuated enterotoxigenic Escherichia coli vaccine ACE527 reduces the incidence and severity of diarrhea in a human challenge model of diarrheal disease. Clin. Vaccine Immunol. 19:1921-1931 http://dx.doi.org/10.1128/CVI.00364-12.
21. Roy K, Bartels S, Qadri F, Fleckenstein JM. 2010. Enterotoxigenic Escherichia coli elicits immune responses to multiple surface proteins. Infect. Immun. 78:3027-3035. http://dx.doi.org/10.1128/IAI.00264-10.
22. Sahl JW, Steinsland H, Redman JC, Angiuoli SV, Nataro JP, Sommerfelt H, Rasko DA. 2011. A comparative genomic analysis of diverse clonal types of enterotoxigenic Escherichia coli reveals pathovar-specific conservation. Infect. Immun. 79:950-960. http://dx.doi.org/10.1128/IAI.00932-10.
23. Del Canto F, Valenzuela P, Cantero L, Bronstein J, Blanco JE, Blanco J, Prado V, Levine M, Nataro J, Sommerfelt H, Vidal R. 2011. Distribution of classical and nonclassical virulence genes in enterotoxigenic Escherichia coli isolates from Chilean children and tRNA gene screening for putative insertion sites for genomic islands. J. Clin. Microbiol. 49: 3198-3203. http://dx.doi.org/10.1128/JCM.02473-10.
24. Patel SK, Dotson J, Allen KP, Fleckenstein JM. 2004. Identification and molecular characterization of EatA, an autotransporter protein of enterotoxigenic Escherichia coli. Infect. Immun. 72:1786-1794. http://dx.doi.org /10.1128/IAI.72.3.1786-1794.2004.
25. Roy K, Kansal R, Bartels SR, Hamilton DJ, Shaaban S, Fleckenstein JM. 2011. Adhesin degradation accelerates delivery of heat-labile toxin by enterotoxigenic Escherichia coli. J. Biol. Chem. 286:29771-29779. http://dx .doi.org/10.1074/jbc.M111.251546.
26. Fleckenstein JM, Roy K, Fischer JF, Burkitt M. 2006. Identification of a two-partner secretion locus of enterotoxigenic Escherichia coli. Infect. Immun. 74:2245-2258. http://dx.doi.org/10.1128/IAI.74.4.2245-2258.2006.
27. Benjelloun-Touimi Z, Sansonetti PJ, Parsot C. 1995. SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol. Microbiol. 17:123-135. http://dx.doi.org/10.1111/j.1365-2958.1995.mmi_17010123.x.
28. Boisen N, Scheutz F, Rasko DA, Redman JC, Persson S, Simon J, Kotloff KL, Levine MM, Sow S, Tamboura B, Toure A, Malle D, Panchalingam S, Krogfelt KA, Nataro JP. 2012. Genomic characterization of enteroaggregative Escherichia coli from children in Mali. J. Infect. Dis. 205:431-444. http://dx.doi.org/10.1093/infdis/jir757.
29. Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin CS, Iliopoulos D, Klammer A, Peluso P, Lee L, Kislyuk AO, Bullard J, Kasarskis A, Wang S, Eid J, Rank D, Redman JC, Steyert SR, Frimodt-Moller J, Struve C, Petersen AM, Krogfelt KA, Nataro JP, Schadt EE, Waldor MK. 2011. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N. Engl. J. Med. 365:709-717. http://dx.doi.org/10.1056/NEJMoa1106920.
30. Evans DJ, Jr, Evans DG. 1973. Three characteristics associated with enterotoxigenic Escherichia coli isolated from man. Infect. Immun. 8:322- 328.
31. Tom BH, Rutzky LP, Jakstys MM, Oyasu R, Kaye CI, Kahan BD. 1976. Human colonic adenocarcinoma cells. I. Establishment and description of a new line. In Vitro 12:180-191.
32. Harlow E, Lane D, Harlow E. 1999. Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. van Klinken BJ, Oussoren E, Weenink JJ, Strous GJ, Buller HA, Dekker J, Einerhand AW. 1996. The human intestinal cell lines Caco-2 and LS174T as models to study cell-type specific mucin expression. Glycoconj. J. 13:757-768. http://dx.doi.org/10.1007/BF00702340.
34. Bu XD, Li N, Tian XQ, Huang PL. 2011. Caco-2 and LS174T cell lines provide different models for studying mucin expression in colon cancer. Tissue Cell 43:201-206. http://dx.doi.org/10.1016/j.tice.2011.03.002.
35. Davies J, Carlstedt I. 2000. Isolation of large gel-forming mucins. Methods Mol. Biol. 125:3-13.
36. Lewis WG, Robinson LS, Perry J, Bick JL, Peipert JF, Allsworth JE, Lewis AL. 2012. Hydrolysis of secreted sialoglycoprotein immunoglobulin A (IgA) in ex vivo and biochemical models of bacterial vaginosis. J. Biol. Chem. 287:2079-2089. http://dx.doi.org/10.1074/jbc.M111.278135.
37. Ruiz-Perez F, Wahid R, Faherty CS, Kolappaswamy K, Rodriguez L, Santiago A, Murphy E, Cross A, Sztein MB, Nataro JP. 2011. Serine protease autotransporters from Shigella flexneri and pathogenic Escherichia coli target a broad range of leukocyte glycoproteins. Proc. Natl. Acad. Sci. U. S. A. 108:12881-12886. http://dx.doi.org/10.1073/pnas.1101006108.
38. Szabady RL, Yanta JH, Halladin DK, Schofield MJ, Welch RA. 2011. TagA is a secreted protease of Vibrio cholerae that specifically cleaves mucin glycoproteins. Microbiology 157:516-525. http://dx.doi.org/10.1099/mic.0.044529-0.
39. Dorsey FC, Fischer JF, Fleckenstein JM. 2006. Directed delivery of heat-labile enterotoxin by enterotoxigenic Escherichia coli. Cell. Microbiol. 8:1516-1527. http://dx.doi.org/10.1111/j.1462-5822.2006.00736.x.
40. Allen KP, Randolph MM, Fleckenstein JM. 2006. Importance of heatlabile enterotoxin in colonization of the adult mouse small intestine by human enterotoxigenic Escherichia coli strains. Infect. Immun. 74:869-875. http://dx.doi.org/10.1128/IAI.74.2.869-875.2006.
41. Tsang VC, Wilson BC, Maddison SE. 1980. Kinetic studies of a quantitative single-tube enzyme-linked immunosorbent assay. Clin. Chem. 26: 1255-1260.
42. Roy K, Hamilton DJ, Fleckenstein JM. 2012. Cooperative role of antibodies against heat-labile toxin and the EtpA adhesin in preventing toxin delivery and intestinal colonization by enterotoxigenic Escherichia coli. Clin. Vaccine Immunol. 19:1603-1608. http://dx.doi.org/10.1128/CVI.00351-12.
43. Fallingborg J. 1999. Intraluminal pH of the human gastrointestinal tract. Dan. Med. Bull. 46:183-196.
44. Dutta PR, Cappello R, Navarro-Garcia F, Nataro JP. 2002. Functional comparison of serine protease autotransporters of Enterobacteriaceae. Infect. Immun. 70:7105-7113. http://dx.doi.org/10.1128/IAI.70.12.7105-7113.2002.
45. Bergstrom KS, Kissoon-Singh V, Gibson DL, Ma C, Montero M, Sham HP, Ryz N, Huang T, Velcich A, Finlay BB, Chadee K, Vallance BA. 2010. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog. 6:e1000902. http://dx.doi.org/10.1371/journal.ppat.1000902.
46. McGuckin MA, Linden SK, Sutton P, Florin TH. 2011. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9:265-278. http://dx.doi.org/10.1038/nrmicro2538.
47. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. U. S. A. 105:15064-15069. http://dx.doi.org/10.1073/pnas.0803124105.
48. Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM, Dekker J. 2010. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 1:254-268. http://dx.doi.org/10.4161/gmic.1.4.12778.
49. Johansson ME, Sjovall H, Hansson GC. 2013. The gastrointestinal mucus system in health and disease. Nat. Rev. Gastroenterol. Hepatol. 10: 352-361. http://dx.doi.org/10.1038/nrgastro.2013.35.
50. Henderson IR, Czeczulin J, Eslava C, Noriega F, Nataro JP. 1999. Characterization of Pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect. Immun. 67:5587-5596.
51. Sack RB. 2011. The discovery of cholera-like enterotoxins produced by Escherichia coli causing secretory diarrhoea in humans. Indian J. Med. Res. 133:171-180.
52. Evans DG, Silver RP, Evans DJ, Jr, Chase DG, Gorbach SL. 1975. Plasmid-controlled colonization factor associated with virulence in Escherichia coli enterotoxigenic for humans. Infect. Immun. 12:656-667.
53. Luo Q, Kumar P, Vickers T, Sheikh A, Lewis WG, Rasko DA, Sistrunk J, Fleckenstein JM. 2014. Enterotoxigenic Escherichia coli secretes a highly conserved mucin-degrading metalloprotease to effectively engage intestinal epithelial cells. Infect. Immun. 82:509-521.