Enterotoxigenic escherichia coli secretes a highly conserved mucin-degrading metalloprotease to effectively engage intestinal epithelial cells

Infection and Immunity

Volumn 82, Issue 2, 2014, Pages 509-521

  Luo, Qingwei ^a   Kumar, Pardeep ^a   Vickers, Tim J ^a   Sheikh, Alaullah ^a   Lewis, Warren G ^a   Rasko, David A ^c   Sistrunk, Jeticia ^c   Fleckenstein, James M ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL TOXIN; CELL SURFACE RECEPTOR; METALLOPROTEINASE; MUCIN; MUCIN 2; MUCIN 3; PROTEIN YGHJ; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENTEROTOXIGENIC ESCHERICHIA COLI; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SMALL INTESTINE; TYPE II SECRETION SYSTEM;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; ENTEROTOXIGENIC ESCHERICHIA COLI; EPITHELIAL CELLS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; HUMANS; HYDROLYSIS; METALLOPROTEASES; MICE; MUCIN-2; MUCIN-3; VIRULENCE FACTORS;

EID: 84892966750     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01106-13     Document Type: Article

References (60)

1. 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.
2. 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.
3. Qadri F, Svennerholm AM, Faruque AS, Sack RB. 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin. Microbiol. Rev. 18:465- 483. http://dx.doi.org/10.1128/CMR.18.3.465-483.2005.
4. 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.
5. 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.
6. Isidean SD, Riddle MS, Savarino SJ, Porter CK. 2011. A systematic review of ETEC epidemiology focusing on colonization factor and toxin expression. Vaccine 29:6167-6178. http://dx.doi.org/10.1016/j.vaccine .2011.06.084.
7. 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.
8. 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.
9. 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.
10. Kansal R, Rasko DA, Sahl JW, Munson GP, Roy K, Luo Q, Sheikh A, Kuhne KJ, Fleckenstein JM. 2013. Transcriptional modulation of enterotoxigenic Escherichia coli virulence genes in response to epithelial cell interactions. Infect. Immun. 81:259-270. http://dx.doi.org/10.1128/IAI .00919-12.
11. 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.
12. 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.
13. 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.
14. Strozen TG, Li G, Howard SP. 2012. YghG (GspSbeta) is a novel pilot protein required for localization of the GspSbeta type II secretion system secretin of enterotoxigenic Escherichia coli. Infect. Immun. 80:2608-2622. http://dx.doi.org/10.1128/IAI.06394-11.
15. Sahl JW, Steinsland H, Redman JC, Angiuoli SV, Nataro JP, Sommerfelt H, Rasko DA. 2011.Acomparative 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.
16. Boratyn GM, Schaffer AA, Agarwala R, Altschul SF, Lipman DJ, Madden TL. 2012. Domain enhanced lookup time accelerated BLAST. Biol. Direct 7:12. http://dx.doi.org/10.1186/1745-6150-7-12.
17. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371. http://dx.doi .org/10.1038/nprot.2009.2.
18. Harlow E, Lane D, Harlow E. 1999. Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. 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.
20. 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.
21. 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.
22. Davies JR, Carlstedt I. 2000. Isolation of large gel-forming mucins. Methods Mol. Biol. 125:3-13.
23. 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.
24. 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.
25. 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.
26. Harris JA, Roy K, Woo-Rasberry V, Hamilton DJ, Kansal R, Qadri F, Fleckenstein JM. 2011. Directed evaluation of enterotoxigenic Escherichia coli autotransporter proteins as putative vaccine candidates. PLoS Negl. Trop. Dis. 5:e1428. http://dx.doi.org/10.1371/journal.pntd.0001428.
27. Tauschek M, Gorrell RJ, Strugnell RA, Robins-Browne RM. 2002. Identification of a protein secretory pathway for the secretion of heatlabile enterotoxin by an enterotoxigenic strain of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99:7066-7071. http://dx.doi.org/10.1073/pnas .092152899.
28. Moriel DG, Bertoldi I, Spagnuolo A, Marchi S, Rosini R, Nesta B, Pastorello I, Corea VA, Torricelli G, Cartocci E, Savino S, Scarselli M, Dobrindt U, Hacker J, Tettelin H, Tallon LJ, Sullivan S, Wieler LH, Ewers C, Pickard D, Dougan G, Fontana MR, Rappuoli R, Pizza M, Serino L. 2010. Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 107:9072-9077. http://dx.doi.org/10.1073 /pnas.0915077107.
29. Oshima K, Toh H, Ogura Y, Sasamoto H, Morita H, Park SH, Ooka T, Iyoda S, Taylor TD, Hayashi T, Itoh K, Hattori M. 2008. Complete genome sequence and comparative analysis of the wild-type commensal Escherichia coli strain SE11 isolated from a healthy adult. DNA Res. 15: 375-386. http://dx.doi.org/10.1093/dnares/dsn026.
30. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, Henderson IR, Sperandio V, Ravel J. 2008. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 190:6881-6893. http://dx.doi.org/10.1128/JB.00619-08.
31. Levine MM, Bergquist EJ, Nalin DR, Waterman DH, Hornick RB, Young CR, Sotman S. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are noninvasive. Lancet i:1119-1122.
32. Vejborg RM, Friis C, Hancock V, Schembri MA, Klemm P. 2010. A virulent parent with probiotic progeny: comparative genomics of Escherichia coli strains CFT073, Nissle 1917 and ABU 83972. Mol. Genet. Genomics 283:469-484. http://dx.doi.org/10.1007/s00438-010-0532-9.
33. Parsot C, Taxman E, Mekalanos JJ. 1991. ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 88:1641-1645. http://dx.doi.org/10.1073 /pnas.88.5.1641.
34. Peterson KM, Mekalanos JJ. 1988. Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization. Infect. Immun. 56:2822-2829.
35. Wang P, Granados RR. 1997. An intestinal mucin is the target substrate for a baculovirus enhancin. Proc. Natl. Acad. Sci. U. S. A. 94:6977-6982. http://dx.doi.org/10.1073/pnas.94.13.6977.
36. 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.
37. Crossman LC, Chaudhuri RR, Beatson SA, Wells TJ, Desvaux M, Cunningham AF, Petty NK, Mahon V, Brinkley C, Hobman JL, Savarino SJ, Turner SM, Pallen MJ, Penn CW, Parkhill J, Turner AK, Johnson TJ, Thomson NR, Smith SG, Henderson IR. 2010. A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J. Bacteriol. 192:5822-5831. http://dx .doi.org/10.1128/JB.00710-10.
38. Rawlings ND, Barrett AJ. 1995. Evolutionary families of metallopeptidases. Methods Enzymol. 248:183-228.
39. Lepore LS, Roelvink PR, Granados RR. 1996. Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J. Invertebr. Pathol. 68:131-140. http://dx.doi.org/10 .1006/jipa.1996.0070.
40. Nakjang S, Ndeh DA, Wipat A, Bolam DN, Hirt RP. 2012. A novel extracellular metallopeptidase domain shared by animal host-associated mutualistic and pathogenic microbes. PLoS One 7:e30287. http://dx.doi .org/10.1371/journal.pone.0030287.
41. Karaolis DK, Lan R, Kaper JB, Reeves PR. 2001. Comparison of Vibrio cholerae pathogenicity islands in sixth and seventh pandemic strains. Infect. Immun. 69:1947-1952. http://dx.doi.org/10.1128/IAI.69.3.1947 -1952.2001.
42. Overbye LJ, Sandkvist M, Bagdasarian M. 1993. Genes required for extracellular secretion of enterotoxin are clustered in Vibrio cholerae. Gene 132:101-106. http://dx.doi.org/10.1016/0378-1119(93)90520-D.
43. 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.
44. 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.
45. 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.
46. Lathem WW, Grys TE, Witowski SE, Torres AG, Kaper JB, Tarr PI, Welch RA. 2002. StcE, a metalloprotease secreted by Escherichia coli O157: H7, specifically cleaves C1 esterase inhibitor. Mol. Microbiol. 45:277-288. http://dx.doi.org/10.1046/j.1365-2958.2002.02997.x.
47. Gutierrez-Jimenez J, Arciniega I, Navarro-Garcia F. 2008. The serine protease motif of Pic mediates a dose-dependent mucolytic activity after binding to sugar constituents of the mucin substrate. Microb. Pathog. 45:115-123. http://dx.doi.org/10.1016/j.micpath.2008.04.006.
48. Harrington SM, Sheikh J, Henderson IR, Ruiz-Perez F, Cohen PS, Nataro JP. 2009. The Pic protease of enteroaggregative Escherichia coli promotes intestinal colonization and growth in the presence of mucin. Infect. Immun. 77:2465-2473. http://dx.doi.org/10.1128/IAI.01494-08.
49. Bradbury NA. 2000. Protein kinase-A-mediated secretion of mucin from human colonic epithelial cells. J. Cell. Physiol. 185:408-415. http://dx.doi .org/10.1002/1097-4652(200012)185:3408::AID-JCP11 3.0.CO;2-2.
50. Vandooren J, Geurts N, Martens E, Van den Steen PE, Opdenakker G. 2013. Zymography methods for visualizing hydrolytic enzymes. Nat. Methods 10:211-220. http://dx.doi.org/10.1038/nmeth.2371.
51. Cohen PS, Arruda JC, Williams TJ, Laux DC. 1985. Adhesion of a human fecal Escherichia coli strain to mouse colonic mucus. Infect. Immun. 48:139-145.
52. Mantle M, Husar SD. 1994. Binding of Yersinia enterocolitica to purified, native small intestinal mucins from rabbits and humans involves interactions with the mucin carbohydrate moiety. Infect. Immun. 62:1219-1227.
53. Cohen PS, Rossoll R, Cabelli VJ, Yang SL, Laux DC. 1983. Relationship between the mouse colonizing ability of a human fecal Escherichia coli strain and its ability to bind a specific mouse colonic mucous gel protein. Infect. Immun. 40:62-69.
54. 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. http://dx.doi.org/10.1128/CVI.00364-12.
55. 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.
56. 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.
57. Evans DJ, Jr, Evans DG. 1973. Three characteristics associated with enterotoxigenic Escherichia coli isolated from man. Infect. Immun. 8:322- 328.
58. Levine MM, Ristaino P, Marley G, Smyth C, Knutton S, Boedeker E, Black R, Young C, Clements ML, Cheney C, Patnaik R. 1984. Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans. Infect. Immun. 44:409-420.
59. DuPont HL, Formal SB, Hornick RB, Snyder MJ, Libonati JP, Sheahan DG, LaBrec EH, Kalas JP. 1971. Pathogenesis of Escherichia coli diarrhea. N. Engl. J. Med. 285:1-9. http://dx.doi.org/10.1056/NEJM197107012850101.
60. Kumar P, Luo Q, Vickers TJ, Sheikh A, Lewis WG, Fleckenstein JM. 2014. EatA, an immununogenic protective antigen of enterotoxigenic Escherichia coli, degrades intestinal mucin. Infect. Immun. 82:500-508.