Analysis of surface-exposed outer membrane proteins in Helicobacter pylori

Journal of Bacteriology

Volumn 196, Issue 13, 2014, Pages 2455-2471

  Voss, Bradley J ^a   Gaddy, Jennifer A ^a,b   McDonald, W Hayes ^a   Cover, Timothy L ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; LIPOPROTEIN; OUTER MEMBRANE PROTEIN; PROTEINASE K; SIGNAL PEPTIDE;

ARTICLE; BETA SHEET; BIOTINYLATION; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; HELICOBACTER PYLORI; HOST PATHOGEN INTERACTION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; TYPE IV SECRETION SYSTEM;

BACTERIAL OUTER MEMBRANE PROTEINS; ENDOPEPTIDASE K; GENE EXPRESSION REGULATION, BACTERIAL; HELICOBACTER PYLORI; IMMUNOHISTOCHEMISTRY; PROTEIN TRANSPORT;

EID: 84902007682     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01768-14     Document Type: Article

References (56)

1. Atherton JC, Blaser MJ. 2009. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J. Clin. Invest. 119:2475-2487. http://dx.doi.org/10.1172/JCI38605.
2. Cover TL, Blaser MJ. 2009. Helicobacter pylori in health and disease. Gastroenterology 136:1863-1873. http://dx.doi.org/10.1053/j.gastro .2009.01.073.
3. Amieva MR, El-Omar EM. 2008. Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134:306-323. http://dx.doi.org /10.1053/j.gastro.2007.11.009.
4. Polk DB, Peek RM, Jr. 2010. Helicobacter pylori: gastric cancer and beyond. Nat. Rev. Cancer 10:403-414. http://dx.doi.org/10.1038/nrc2857.
5. Cover TL, Blanke SR. 2005. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat. Rev. Microbiol. 3:320-332. http://dx.doi .org/10.1038/nrmicro1095.
6. Hatakeyama M. 2011. Anthropological and clinical implications for the structural diversity of the Helicobacter pylori CagA oncoprotein. Cancer Sci. 102:36-43. http://dx.doi.org/10.1111/j.1349-7006.2010.01743.x.
7. Liechti G, Goldberg JB. 2012. Outer membrane biogenesis in Escherichia coli, Neisseria meningitidis, and Helicobacter pylori: paradigm deviations in H. pylori. Front. Cell. Infect. Microbiol. 2:29. http://dx.doi.org/10.3389 /fcimb.2012.00029.
8. Ilver D, Arnqvist A, Ogren J, Frick IM, Kersulyte D, Incecik ET, Berg DE, Covacci A, Engstrand L, Boren T. 1998. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279:373-377. http://dx.doi.org/10.1126/science.279.5349.373.
9. Mahdavi J, Sonden B, Hurtig M, Olfat FO, Forsberg L, Roche N, Angstrom J, Larsson T, Teneberg S, Karlsson KA, Altraja S, Wadstrom T, Kersulyte D, Berg DE, Dubois A, Petersson C, Magnusson KE, Norberg T, Lindh F, Lundskog BB, Arnqvist A, Hammarstrom L, Boren T. 2002. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297:573-578. http://dx.doi.org/10.1126 /science.1069076.
10. Odenbreit S, Till M, Hofreuter D, Faller G, Haas R. 1999. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 31: 1537-1548. http://dx.doi.org/10.1046/j.1365-2958.1999.01300.x.
11. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, Konig W, Backert S. 2007. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449:862-866. http://dx.doi.org/10.1038/nature06187.
12. Jimenez-Soto LF, Kutter S, Sewald X, Ertl C, Weiss E, Kapp U, Rohde M, Pirch T, Jung K, Retta SF, Terradot L, Fischer W, Haas R. 2009. Helicobacter pylori type IV secretion apparatus exploits beta1 integrin in a novel RGD-independent manner. PLoS Pathog. 5:e1000684. http://dx .doi.org/10.1371/journal.ppat.1000684.
13. Sause WE, Castillo AR, Ottemann KM. 2012. The Helicobacter pylori autotransporter ImaA (HP0289) modulates the immune response and contributes to host colonization. Infect. Immun. 80:2286-2296. http://dx .doi.org/10.1128/IAI.00312-12.
14. Belogolova E, Bauer B, Pompaiah M, Asakura H, Brinkman V, Ertl C, Bartfeld S, Nechitaylo TY, Haas R, Machuy N, Salama N, Churin Y, Meyer TF. 2013. Helicobacter pylori outer membrane protein HopQ identified as a novel T4SS-associated virulence factor. Cell. Microbiol. 15:1896-1912. http://dx.doi.org/10.1111/cmi.12158.
15. Jimenez-Soto LF, Clausen S, Sprenger A, Ertl C, Haas R. 2013. Dynamics of the Cag-type IV secretion system of Helicobacter pylori as studied by bacterial co-infections. Cell. Microbiol. 15:1924-1937. http://dx.doi.org /10.1111/cmi.12166.
16. Ishijima N, Suzuki M, Ashida H, Ichikawa Y, Kanegae Y, Saito I, Boren T, Haas R, Sasakawa C, Mimuro H. 2011. BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J. Biol. Chem. 286:25256-25264. http://dx.doi.org/10 .1074/jbc.M111.233601.
17. Sabarth N, Hurvitz R, Schmidt M, Zimny-Arndt U, Jungblut PR, Meyer TF, Bumann D. 2005. Identification of Helicobacter pylori surface proteins by selective proteinase K digestion and antibody phage display. J. Microbiol. Methods 62:345-349. http://dx.doi.org/10.1016/j.mimet.2005 .04.030.
18. Radin JN, Gaddy JA, Gonzalez-Rivera C, Loh JT, Algood HM, Cover TL. 2013. Flagellar localization of a Helicobacter pylori autotransporter protein. mBio 4(2):e00613-12.
19. Sabarth N, Lamer S, Zimny-Arndt U, Jungblut PR, Meyer TF, Bumann D. 2002. Identification of surface proteins of Helicobacter pylori by selective biotinylation, affinity purification, and two-dimensional gel electrophoresis. J. Biol. Chem. 277:27896-27902. http://dx.doi.org/10.1074/jbc .M204473200.
20. Baik SC, Kim KM, Song SM, Kim DS, Jun JS, Lee SG, Song JY, Park JU, Kang HL, Lee WK, Cho MJ, Youn HS, Ko GH, Rhee KH. 2004. Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Helicobacter pylori strain 26695. J. Bacteriol. 186:949-955. http://dx.doi .org/10.1128/JB.186.4.949-955.2004.
21. Doig P, Trust TJ. 1994. Identification of surface-exposed outer membrane antigens of Helicobacter pylori. Infect. Immun. 62:4526-4533.
22. Exner MM, Doig P, Trust TJ, Hancock RE. 1995. Isolation and characterization of a family of porin proteins from Helicobacter pylori. Infect. Immun. 63:1567-1572.
23. Phadnis SH, Parlow MH, Levy M, Ilver D, Caulkins CM, Connors JB, Dunn BE. 1996. Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect. Immun. 64:905-912.
24. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547. http://dx.doi .org/10.1038/41483.
25. Alm RA, Bina J, Andrews BM, Doig P, Hancock RE, Trust TJ. 2000. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect. Immun. 68:4155-4168. http://dx.doi.org/10 .1128/IAI.68.7.4155-4168.2000.
26. Peck B, Ortkamp M, Diehl KD, Hundt E, Knapp B. 1999. Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucleic Acids Res. 27:3325-3333. http://dx.doi.org /10.1093/nar/27.16.3325.
27. Doig P, Exner MM, Hancock RE, Trust TJ. 1995. Isolation and characterization of a conserved porin protein from Helicobacter pylori. J. Bacteriol. 177:5447-5452.
28. Shaffer CL, Gaddy JA, Loh JT, Johnson EM, Hill S, Hennig EE, McClain MS, McDonald WH, Cover TL. 2011. Helicobacter pylori exploits a unique repertoire of type IV secretion system components for pilus assembly at the bacteria-host cell interface. PLoS Pathog. 7:e1002237. http://dx .doi.org/10.1371/journal.ppat.1002237.
29. Busler VJ, Torres VJ, McClain MS, Tirado O, Friedman DB, Cover TL. 2006. Protein-protein interactions among Helicobacter pylori cag proteins. J. Bacteriol. 188:4787-4800. http://dx.doi.org/10.1128/JB.00066-06.
30. Kutter S, Buhrdorf R, Haas J, Schneider-Brachert W, Haas R, Fischer W. 2008. Protein subassemblies of the Helicobacter pylori Cag type IV secretion system revealed by localization and interaction studies. J. Bacteriol. 190:2161-2171. http://dx.doi.org/10.1128/JB.01341-07.
31. Pham KT, Weiss E, Jimenez Soto LF, Breithaupt U, Haas R, Fischer W. 2012. CagI is an essential component of the Helicobacter pylori Cag type IV secretion system and forms a complex with CagL. PLoS One 7:e35341. http://dx.doi.org/10.1371/journal.pone.0035341.
32. MacCoss MJ, McDonald WH, Saraf A, Sadygov R, Clark JM, Tasto JJ, Gould KL, Wolters D, Washburn M, Weiss A, Clark JI, Yates JR, III. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl. Acad. Sci. U. S. A. 99:7900-7905. http: //dx.doi.org/10.1073/pnas.122231399.
33. Old WM, Meyer-Arendt K, Aveline-Wolf L, Pierce KG, Mendoza A, Sevinsky JR, Resing KA, Ahn NG. 2005. Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics 4:1487-1502. http://dx.doi.org/10.1074/mcp .M500084-MCP200.
34. Li M, Gray W, Zhang H, Chung CH, Billheimer D, Yarbrough WG, Liebler DC, Shyr Y, Slebos RJ. 2010. Comparative shotgun proteomics using spectral count data and quasi-likelihood modeling. J. Proteome Res. 9:4295-4305. http://dx.doi.org/10.1021/pr100527g.
35. Fischer W, Puls J, Buhrdorf R, Gebert B, Odenbreit S, Haas R. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42:1337-1348.
36. Keenan J, Oliaro J, Domigan N, Potter H, Aitken G, Allardyce R, Roake J. 2000. Immune response to an 18-kilodalton outer membrane antigen identifies lipoprotein 20 as a Helicobacter pylori vaccine candidate. Infect. Immun. 68:3337-3343. http://dx.doi.org/10.1128/IAI .68.6.3337-3343.2000.
37. Duncan SS, Valk PL, McClain MS, Shaffer CL, Metcalf JA, Bordenstein SR, Cover TL. 2013. Comparative genomic analysis of East Asian and non-Asian Helicobacter pylori strains identifies rapidly evolving genes. PLoS One 8:e55120. http://dx.doi.org/10.1371/journal.pone.0055120.
38. Hoy B, Lower M, Weydig C, Carra G, Tegtmeyer N, Geppert T, Schroder P, Sewald N, Backert S, Schneider G, Wessler S. 2010. Helicobacter pylori HtrA is a new secreted virulence factor that cleaves Ecadherin to disrupt intercellular adhesion. EMBO Rep. 11:798-804. http: //dx.doi.org/10.1038/embor.2010.114.
39. Bumann D, Aksu S, Wendland M, Janek K, Zimny-Arndt U, Sabarth N, Meyer TF, Jungblut PR. 2002. Proteome analysis of secreted proteins of the gastric pathogen Helicobacter pylori. Infect. Immun. 70:3396-3403. http://dx.doi.org/10.1128/IAI.70.7.3396-3403.2002.
40. Jonsson K, Guo BP, Monstein HJ, Mekalanos JJ, Kronvall G. 2004. Molecular cloning and characterization of two Helicobacter pylori genes coding for plasminogen-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 101:1852-1857. http://dx.doi.org/10.1073/pnas.0307329101.
41. Jones AC, Logan RP, Foynes S, Cockayne A, Wren BW, Penn CW. 1997.Aflagellar sheath protein of Helicobacter pylori is identical to HpaA, a putative N-acetylneuraminyllactose-binding hemagglutinin, but is not an adhesin for AGS cells. J. Bacteriol. 179:5643-5647.
42. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
43. Bos MP, Robert V, Tommassen J. 2007. Biogenesis of the gram-negative bacterial outer membrane. Annu. Rev. Microbiol. 61:191-214. http://dx .doi.org/10.1146/annurev.micro.61.080706.093245.
44. Hagan CL, Silhavy TJ, Kahne D. 2011. β-Barrel membrane protein assembly by the Bam complex. Annu. Rev. Biochem. 80:189-210. http: //dx.doi.org/10.1146/annurev-biochem-061408-144611.
45. Struyvé M, Moons M, Tommassen J. 1991. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol. 218:141-148. http://dx.doi.org/10 .1016/0022-2836(91)90880-F.
46. Fischer W. 2011. Assembly and molecular mode of action of the Helicobacter pylori Cag type IV secretion apparatus. FEBS J. 278:1203-1212. http://dx.doi.org/10.1111/j.1742-4658.2011.08036.x.
47. Babu MM, Priya ML, Selvan AT, Madera M, Gough J, Aravind L, Sankaran K. 2006. A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J. Bacteriol. 188:2761-2773. http://dx.doi.org/10.1128/JB.188.8.2761-2773.2006.
48. Masuda K, Matsuyama S, Tokuda H. 2002. Elucidation of the function of lipoprotein-sorting signals that determine membrane localization. Proc. Natl. Acad. Sci. U. S. A. 99:7390-7395. http://dx.doi.org/10.1073/pnas .112085599.
49. Lewis LA, Rohde K, Gipson M, Behrens B, Gray E, Toth SI, Roe BA, Dyer DW. 1998. Identification and molecular analysis of lbpBA, which encodes the two-component meningococcal lactoferrin receptor. Infect. Immun. 66:3017-3023.
50. Nothaft H, Szymanski CM. 2010. Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8:765-778. http://dx.doi.org/10 .1038/nrmicro2383.
51. Thompson LJ, Merrell DS, Neilan BA, Mitchell H, Lee A, Falkow S. 2003. Gene expression profiling of Helicobacter pylori reveals a growthphase-dependent switch in virulence gene expression. Infect. Immun. 71: 2643-2655. http://dx.doi.org/10.1128/IAI.71.5.2643-2655.2003.
52. Fischer W, Buhrdorf R, Gerland E, Haas R. 2001. Outer membrane targeting of passenger proteins by the vacuolating cytotoxin autotransporter of Helicobacter pylori. Infect. Immun. 69:6769-6775. http://dx .doi.org/10.1128/IAI.69.11.6769-6775.2001.
53. Ilver D, Barone S, Mercati D, Lupetti P, Telford JL. 2004. Helicobacter pylori toxin VacA is transferred to host cells via a novel contact-dependent mechanism. Cell. Microbiol. 6:167-174. http://dx.doi.org/10.1046/j.1462-5822.2003.00349.x.
54. Junker M, Schuster CC, McDonnell AV, Sorg KA, Finn MC, Berger B, Clark PL. 2006. Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. U. S. A. 103:4918-4923. http://dx.doi.org/10.1073 /pnas.0507923103.
55. Gangwer KA, Mushrush DJ, Stauff DL, Spiller B, McClain MS, Cover TL, Lacy DB. 2007. Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain. Proc. Natl. Acad. Sci. U. S. A. 104:16293-16298. http://dx.doi.org/10.1073/pnas.0707447104.
56. Pang SS, Nguyen ST, Perry AJ, Day CJ, Panjikar S, Tiralongo J, Whisstock JC, Kwok T. 27 December 2013. The three-dimensional structure of the extracellular adhesion domain of the sialic acid-binding adhesin SabA from Helicobacter pylori. J. Biol. Chem. http://dx.doi.org/10 .1074/jbc.M113.513135.