Helicobacter pylori exploits a unique repertoire of type iv secretion system components for pilus assembly at the bacteria-host cell interface

PLoS Pathogens

Volumn 7, Issue 9, 2011, Pages

  Shaffer, Carrie L ^a   Gaddy, Jennifer A ^a   Loh, John T ^a   Johnson, Elizabeth M ^a   Hill, Salisha ^a   Hennig, Ewa E ^b   McClain, Mark S ^a   McDonald, W Hayes ^a   Cover, Timothy L ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF ONCOLOGY   (Poland)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HEXAPEPTIDE; INTERLEUKIN 8; PROTEIN CAGH; PROTEIN CAGI; PROTEIN CAGL; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; CAGA PROTEIN, HELICOBACTER PYLORI; CAGL PROTEIN, HELICOBACTER PYLORI;

ARTICLE; BACTERIUM PILUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; HELICOBACTER PYLORI; HOST CELL; HUMAN; HUMAN CELL; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN STABILITY; SCANNING ELECTRON MICROSCOPY; STOMACH EPITHELIUM; TYPE IV SECRETION SYSTEM; AMINO ACID SEQUENCE; FIMBRIA; GENOMIC ISLAND; HELICOBACTER INFECTION; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; STOMACH;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; FIMBRIAE, BACTERIAL; GENOMIC ISLANDS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; STOMACH;

EID: 80053460306     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002237     Document Type: Article

References (84)

1. Suerbaum S, Michetti P, (2002) Helicobacter pylori infection. N Engl J Med 347: 1175-1186.
2. Amieva MR, El-Omar EM, (2008) Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134: 306-323.
3. Blaser MJ, Atherton JC, (2004) Helicobacter pylori persistence: biology and disease. J Clin Invest 113: 321-333.
4. Cover TL, Blaser MJ, (2009) Helicobacter pylori in health and disease. Gastroenterology 136: 1863-1873.
5. Parsonnet J, Friedman GD, Orentreich N, Vogelman H, (1997) Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 40: 297-301.
6. Kuipers EJ, Perez-Perez GI, Meuwissen SG, Blaser MJ, (1995) Helicobacter pylori and atrophic gastritis: importance of the cagA status. J Natl Cancer Inst 87: 1777-1780.
7. Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, et al. (1995) Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55: 2111-2115.
8. Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, et al. (1996) cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A 93: 14648-14653.
9. Akopyants NS, Clifton SW, Kersulyte D, Crabtree JE, Youree BE, et al. (1998) Analyses of the cag pathogenicity island of Helicobacter pylori. Mol Microbiol 28: 37-53.
10. Hatakeyama M, (2004) Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer 4: 688-694.
11. Backert S, Selbach M, (2008) Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol 10: 1573-1581.
12. Bourzac KM, Guillemin K, (2005) Helicobacter pylori-host cell interactions mediated by type IV secretion. Cell Microbiol 7: 911-919.
13. Jones KR, Whitmire JM, Merrell DS, (2010) A tale of two toxins: H. pylori CagA and VacA modulate host pathways that impact disease. Frontiers Microbiol 1: 115.
14. Odenbreit S, Puls J, Sedlmaier B, Gerland E, Fischer W, et al. (2000) Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287: 1497-1500.
15. Tegtmeyer N, Wessler S, Backert S, (2011) Role of the cag-pathogenicity island encoded type IV secretion system in Helicobacter pylori pathogenesis. FEBS J 278: 1190-1202.
16. Fischer W, (2011) Assembly and molecular mode of action of the Helicobacter pylori Cag type IV secretion apparatus. FEBS J 278: 1203-1212.
17. Terradot L, Waksman G, (2011) Architecture of the Helicobacter pylori Cag-type IV secretion system. FEBS J 278: 1213-22.
18. Segal ED, Cha J, Lo J, Falkow S, Tompkins LS, (1999) Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci U S A 96: 14559-14564.
19. Amieva MR, Vogelmann R, Covacci A, Tompkins LS, Nelson WJ, et al. (2003) Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300: 1430-1434.
20. Guillemin K, Salama NR, Tompkins LS, Falkow S, (2002) Cag pathogenicity island-specific responses of gastric epithelial cells to Helicobacter pylori infection. Proc Natl Acad Sci U S A 99: 15136-15141.
21. Fischer W, Puls J, Buhrdorf R, Gebert B, Odenbreit S, et al. (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.
22. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, et al. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5: 1166-1174.
23. Brandt S, Kwok T, Hartig R, Konig W, Backert S, (2005) NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci U S A 102: 9300-9305.
24. Kim SY, Lee YC, Kim HK, Blaser MJ, (2006) Helicobacter pylori CagA transfection of gastric epithelial cells induces interleukin-8. Cell Microbiol 8: 97-106.
25. Argent RH, Hale JL, El-Omar EM, Atherton JC, (2008) Differences in Helicobacter pylori CagA tyrosine phosphorylation motif patterns between western and East Asian strains, and influences on interleukin-8 secretion. J Med Microbiol 57: 1062-1067.
26. Selbach M, Moese S, Meyer TF, Backert S, (2002) Functional analysis of the Helicobacter pylori cag pathogenicity island reveals both VirD4-CagA-dependent and VirD4-CagA-independent mechanisms. Infect Immun 70: 665-671.
27. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, et al. (2009) Structure of a type IV secretion system core complex. Science 323: 266-268.
28. Cascales E, Christie PJ, (2003) The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1: 137-149.
29. Alvarez-Martinez CE, Christie PJ, (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
30. Yeo HJ, Waksman G, (2004) Unveiling molecular scaffolds of the type IV secretion system. J Bacteriol 186: 1919-1926.
31. Fronzes R, Christie PJ, Waksman G, (2009) The structural biology of type IV secretion systems. Nat Rev Micro 7: 703-714.
32. Li SD, Kersulyte D, Lindley IJD, Neelam B, Berg DE, et al. (1999) Multiple genes in the left half of the cag pathogenicity island of Helicobacter pylori are required for tyrosine kinase-dependent transcription of interleukin-8 in gastric epithelial cells. Infect Immun 67: 3893-3899.
33. Pinto-Santini DM, Salama NR, (2009) Cag3 is a novel essential component of the Helicobacter pylori cag type IV secretion system outer membrane subcomplex. J Bacteriol 191: 7343-7352.
34. Kutter S, Buhrdorf R, Haas J, Schneider-Brachert W, Haas R, et al. (2008) Protein subassemblies of the Helicobacter pylori Cag type IV secretion system revealed by localization and interaction studies. J Bacteriol 190: 2161-2171.
35. Busler VJ, Torres VJ, McClain MS, Tirado O, Friedman DB, et al. (2006) Protein-protein interactions among Helicobacter pylori Cag proteins. J Bacteriol 188: 4787-4800.
36. Jurik A, Hausser E, Kutter S, Pattis I, Prassl S, et al. (2010) The coupling protein Cagβ and its interaction partner CagZ are required for type IV secretion of the Helicobacter pylori CagA protein. Infect Immun 78: 5244-5251.
37. Yuan Q, Carle A, Gao C, Sivanesan D, Aly KA, et al. (2005) Identification of the VirB4-VirB8-VirB5-VirB2 pilus assembly sequence of type IV secretion systems. J Biol Chem 280: 26349-26359.
38. Rohde M, Puls J, Buhrdorf R, Fischer W, Haas R, (2003) A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system. Mol Microbiol 49: 219-234.
39. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, et al. (2007) Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449: 862-866.
40. Andrzejewska J, Lee SK, Olbermann P, Lotzing N, Katzowitsch E, et al. (2006) Characterization of the pilin ortholog of the Helicobacter pylori type IV cag pathogenicity apparatus, a surface-associated protein expressed during infection. J Bacteriol 188: 5865-5877.
41. Tanaka J, Suzuki T, Mimuro H, Sasakawa C, (2003) Structural definition on the surface of Helicobacter pylori type IV secretion apparatus. Cell Microbiol 5: 395-404.
42. Tegtmeyer N, Hartig R, Delahay RM, Rohde M, Brandt S, et al. (2010) A small fibronectin-mimicking protein from bacteria induces cell spreading and focal adhesion formation. J Biol Chem 285: 23515-23526.
43. Kutter S, Buhrdorf R, Haas J, Schneider-Brachert W, Haas R, et al. (2008) Protein subassemblies of the Helicobacter pylori Cag type IV secretion system revealed by localization and interaction studies. J Bacteriol 190: 2161-2171.
44. Jiménez-Soto LF, Kutter S, Sewald X, Ertl C, Weiss E, et al. (2009) Helicobacter pylori type IV secretion apparatus exploits β1 integrin in a novel RGD-independent manner. PLoS Pathog 5: e1000684.
45. Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ, (2010) Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H, K-ATPase α subunit. Gastroenterology 139: 239-248.
46. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeisz S, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
47. Pattis I, Weiss E, Laugks R, Haas R, Fischer W, (2007) The Helicobacter pylori CagF protein is a type IV secretion chaperone-like molecule that binds close to the C-terminal secretion signal of the CagA effector protein. Microbiology 153: 2896-2909.
48. Fernandez D, Spudich G, Zhou X, Christie P, (1996) The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J Bacteriol 178: 3168-3176.
49. Hapfelmeier S, Domke N, Zambryski PC, Baron C, (2000) VirB6 is required for stabilization of VirB5 and VirB3 and formation of VirB7 homodimers in Agrobacterium tumefaciens. J Bacteriol 182: 4505-4511.
50. 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.
51. 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.
52. Marcus EA, Moshfegh AP, Sachs G, Scott DR, (2005) The periplasmic α-carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J Bacteriol 187: 729-738.
53. Zerovnik E, Zavasnik-Bergant V, Kopitar-Jerala N, Pompe-Novak M, Skarabot M, et al. (2002) Amyloid fibril formation by human stefin B in vitro: immunogold labelling and comparison to stefin A. Biol Chem 383: 859-863.
54. Hatakeyama M, (2011) Anthropological and clinical implications for the structural diversity of the Helicobacter pylori CagA oncoprotein. Cancer Sci 102: 36-43.
55. Backert S, Kwok T, Schmid M, Selbach M, Moese S, et al. (2005) Subproteomes of soluble and structure-bound Helicobacter pylori proteins analyzed by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 5: 1331-1345.
56. Olbermann P, Josenhans C, Moodley Y, Uhr M, Stamer C, et al. (2010) A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island. PLoS Genet 6: e1001069.
57. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37: D205-D210.
58. Muramoto K, Makishima S, Aizawa S-I, Macnab RM, (1999) Effect of hook subunit concentration on assembly and control of length of the flagellar hook of Salmonella. J Bacteriol 181: 5808-5813.
59. Erhardt M, Hirano T, Su Y, Paul K, Wee DH, et al. (2010) The role of the FliK molecular ruler in hook-length control in Salmonella enterica. Mol Microbiol 75: 1272-1284.
60. Kawagishi I, Homma M, Williams A, Macnab R, (1996) Characterization of the flagellar hook length control protein FliK of Salmonella typhimurium and Escherichia coli. J Bacteriol 178: 2954-2959.
61. Williams A, Yamaguchi S, Togashi F, Aizawa S, Kawagishi I, et al. (1996) Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J Bacteriol 178: 2960-2970.
62. Kutsukake K, Minamino T, Yokoseki T, (1994) Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J Bacteriol 176: 7625-7629.
63. Makishima S, Komoriya K, Yamaguchi S, Aizawa S-I, (2001) Length of the flagellar hook and the capacity of the type III export apparatus. Science 291: 2411-2413.
64. Journet L, Agrain Cl, Broz P, Cornelis GR, (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302: 1757-1760.
65. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, et al. (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci U S A 102: 826-831.
66. Vergunst AC, van Lier MCM, den Dulk-Ras A, Grosse Stüve TA, Ouwehand A, et al. (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci U S A 102: 832-837.
67. Schulein R, Guye P, Rhomberg TA, Schmid MC, Schröder G, et al. (2005) A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci U S A 102: 856-861.
68. Ivie S, McClain M, Algood H, Lacy DB, Cover T, (2010) Analysis of a beta-helical region in the p55 domain of Helicobacter pylori vacuolating toxin. BMC Microbiol 10: 60.
69. Loh JT, Torres VJ, Cover TL, (2007) Regulation of Helicobacter pylori cagA expression in response to salt. Cancer Res 67: 4709-4715.
70. Dailidiene D, Dailide G, Kersulyte D, Berg DE, (2006) Contraselectable streptomycin susceptibility determinant for genetic manipulation and analysis of Helicobacter pylori. Appl Environ Microbiol 72: 5908-5914.
71. Copass M, Grandi G, Rappuoli R, (1997) Introduction of unmarked mutations in the Helicobacter pylori vacA gene with a sucrose sensitivity marker. Infect Immun 65: 1949-1952.
72. Loh JT, Forsyth MH, Cover TL, (2004) Growth phase regulation of flaA expression in Helicobacter pylori is luxS dependent. Infect Immun 72: 5506-5510.
73. Hopp TP, Woods KR, (1981) Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci U S A 78: 3824-3828.
74. MacCoss MJ, McDonald WH, Saraf A, Sadygov R, Clark JM, et al. (2002) Shotgun identification of protein modifications from protein complexes and lens tissue. Proc Natl Acad Sci U S A 99: 7900-7905.
75. Yates JR, Eng JK, McCormack AL, Schieltz D, (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67: 1426-1436.
76. Ma ZQ, Dasari S, Chambers MC, Litton MD, Sobecki SM, et al. (2009) IDPicker 2.0: Improved protein assembly with high discrimination peptide identification filtering. J Proteome Res 8: 3872-3881.
77. Wessel D, Flügge UI, (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138: 141-143.
78. Schraw W, Li Y, McClain M, van der Goot FG, Cover TL, (2002) Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J Biol Chem 277: 34642-34650.
79. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics Internat 11: 36-42.
80. Zhang B, VerBerkmoes NC, Langston MA, Uberbacher E, Hettich RL, et al. (2006) Detecting differential and correlated protein expression in label-free shotgun proteomics. J Proteome Res 5: 2909-2918.
81. Zar JH, (1999) Biostatistical Analysis. New Jersey Prentice Hall.
82. Nakai K, Kanehisa M, (1991) Expert system for predicting protein localization sites in gram-negative bacteria. Proteins: Structure, Function, and Bioinformatics 11: 95-110.
83. Nielsen H, Engelbrecht J, Brunak S, von Heijne G, (1997) A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int J Neural Syst 8: 581-599.
84. Crooks GE, Hon G, Chandonia J-M, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.