Molecular and structural analysis of the Helicobacter pylori cag type IV secretion system core complex

mBio

Volumn 7, Issue 1, 2016, Pages

  Frick Cheng, Arwen E ^a   Pyburn, Tasia M ^a   Voss, Bradley J ^a   McDonald, W Hayes ^a   Ohi, Melanie D ^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

CAG PROTEIN; CAG3 PROTEIN; CAGM PROTEIN; CAGT PROTEIN; CAGX PROTEIN; CAGY PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; MACROMOLECULE; TYPE IV SECRETION SYSTEM;

ARTICLE; BACTERIUM ISOLATION; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GASTRIC MUCOSA; HELICOBACTER PYLORI; IMMUNOGOLD LABELING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STOMACH CANCER; STOMACH EPITHELIUM; STRUCTURE ANALYSIS; TYPE IV SECRETION SYSTEM; CHEMISTRY; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; MACROMOLECULE; ULTRASTRUCTURE;

HELICOBACTER PYLORI; HUMANS; IMMUNOHISTOCHEMISTRY; MACROMOLECULAR SUBSTANCES; MICROSCOPY, ELECTRON; TYPE IV SECRETION SYSTEMS;

EID: 84960172313     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02001-15     Document Type: Article

References (47)

1. Robin Warren J, Marshall B. 1983. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 321:1273–1275. http://dx.doi.org/10.1016/S0140-6736(83)92719-8.
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. Peek RM, Jr, Blaser MJ. 2002. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2:28–37. http://dx.doi.org/10.1038/nrc703.
4. Atherton JC. 2006. The pathogenesis of Helicobacter pylori-induced gastroduodenal diseases. Annu Rev Pathol 1:63–96. http://dx.doi.org/10.1146/annurev.pathol.1.110304.100125.
5. Suerbaum S, Michetti P. 2002. Helicobacter pylori infection. N Engl J Med 347:1175–1186. http://dx.doi.org/10.1056/NEJMra020542.
6. Covacci A, Censini S, Bugnoli M, Petracca R, Burroni D, Macchia G, Massone A, Papini E, Xiang Z, Figura N. 1993. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci U S A 90:5791–5795. http://dx.doi.org/10.1073/pnas.90.12.5791.
7. Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, Stemmermann GN, Nomura A. 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. Odenbreit S, Püls J, Sedlmaier B, Gerland E, Fischer W, Haas R. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287:1497–1500. http://dx.doi.org/10.1126/science.287.5457.1497.
9. Fischer W, Püls 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. http://dx.doi.org/10.1046/j.1365-2958.2001.02714.x.
10. Olbermann P, Josenhans C, Moodley Y, Uhr M, Stamer C, Vauterin M, Suerbaum S, Achtman M, Linz B. 2010. A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island. PLoS Genet 6: e1001069. http://dx.doi.org/10.1371/journal.pgen.1001069.
11. 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. http://dx.doi.org/10.1111/j.1742-4658.2011.08035.x.
12. Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, Borodovsky M, Rappuoli R, Covacci A. 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. http://dx.doi.org/10.1073/pnas.93.25.14648.
13. 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.
14. Akopyants NS, Clifton SW, Kersulyte D, Crabtree JE, Youree BE, Reece CA, Bukanov NO, Drazek ES, Roe BA, Berg DE. 1998. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol Microbiol 28:37–53. http://dx.doi.org/10.1046/j.1365-2958.1998.00770.x.
15. Nešic´ D, Buti L, Lu X, Stebbins CE. 2014. Structure of the Helicobacter pylori CagA oncoprotein bound to the human tumor suppressor ASPP2. Proc Natl Acad Sci U S A 111:1562–1567. http://dx.doi.org/10.1073/pnas.1320631111.
16. Hatakeyama M. 2014. Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe 15:306–316. http://dx.doi.org/10.1016/j.chom.2014.02.008.
17. Hayashi T, Senda M, Morohashi H, Higashi H, Horio M, Kashiba Y, Nagase L, Sasaya D, Shimizu T, Venugopalan N, Kumeta H, Noda N, Inagaki F, Senda T, Hatakeyama M. 2012. Tertiary structure-function analysis reveals the pathogenic signaling potentiation mechanism of Helicobacter pylori oncogenic effector CagA. Cell Host Microbe 12:20–33. http://dx.doi.org/10.1016/j.chom.2012.05.010.
18. Kaplan-Türköz B, Jiménez-Soto LF, Dian C, Ertl C, Remaut H, Louche A, Tosi T, Haas R, Terradot L. 2012. Structural insights into Helicobacter pylori oncoprotein CagA interaction with β1 integrin. Proc Natl Acad Sci U S A 109:14640–14645. http://dx.doi.org/10.1073/pnas.1206098109.
19. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Mémet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL. 2004. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5:1166–1174. http://dx.doi.org/10.1038/ni1131.
20. Alvarez-Martinez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73:775–808. http://dx.doi.org/10.1128/MMBR.00023-09.
21. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat Rev Microbiol 7:703–714. http://dx.doi.org/10.1038/nrmicro2218.
22. Wallden K, Rivera-Calzada A, Waksman G. 2010. Type IV secretion systems: versatility and diversity in function. Cell Microbiol 12: 1203–1212. http://dx.doi.org/10.1111/j.1462-5822.2010.01499.x.
23. Christie PJ, Cascales E. 2005. Structural and dynamic properties of bacterial type IV secretion systems. Mol Membr Biol 22:51–61. http://dx.doi.org/10.1080/09687860500063316.
24. Fronzes R, Schäfer E, Wang L, Saibil HR, Orlova EV, Waksman G. 2009. Structure of a type IV secretion system core complex. Science 323: 266–268. http://dx.doi.org/10.1126/science.1166101.
25. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. 2009. Structure of the outer membrane complex of a type IV secretion system. Nature 462:1011–1015. http://dx.doi.org/10.1038/nature08588.
26. Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S, Dujeancourt A, Lu F, Redzej A, Fronzes R, Orlova EV, Waksman G. 2014. Structure of a type IV secretion system. Nature 508:550–553. http://dx.doi.org/10.1038/nature13081.
27. Cendron L, Zanotti G. 2011. Structural and functional aspects of unique type IV secretory components in the Helicobacter pylori cag-pathogenicity island. FEBS J 278:1223–1231. http://dx.doi.org/10.1111/j.1742-4658.2011.08038.x.
28. Terradot L, Waksman G. 2011. Architecture of the Helicobacter pylori cag-type IV secretion system. FEBS J 278:1213–1222. http://dx.doi.org/10.1111/j.1742-4658.2011.08037.x.
29. Bourzac KM, Guillemin K. 2005. Helicobacter pylori-host cell interactions mediated by type IV secretion. Cell Microbiol 7:911–919. http://dx.doi.org/10.1111/j.1462-5822.2005.00541.x.
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. 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. http://dx.doi.org/10.1099/mic.0.2007/007385-0.
32. Bonsor DA, Weiss E, Iosub-Amir A, Reingewertz TH, Chen TW, Haas R, Friedler A, Fischer W, Sundberg EJ. 2013. Characterization of the translocation-competent complex between the Helicobacter pylori oncogenic protein CagA and the accessory protein CagF. J Biol Chem 288: 32897–32909. http://dx.doi.org/10.1074/jbc.M113.507657.
33. Couturier MR, Tasca E, Montecucco C, Stein M. 2006. Interaction with CagF is required for translocation of CagA into the host via the Helicobacter pylori type IV secretion system. Infect Immun 74:273–281. http://dx.doi.org/10.1128/IAI.74.1.273-281.2006.
34. Voss BJ, Gaddy JA, McDonald WH, Cover TL. 2014. Analysis of surfaceexposed outer membrane proteins in Helicobacter pylori. J Bacteriol 196: 2455–2471. http://dx.doi.org/10.1128/JB.01768-14.
35. Stein M, Rappuoli R, Covacci A. 2000. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc Natl Acad Sci U S A 97:1263–1268. http://dx.doi.org/10.1073/pnas.97.3.1263.
36. Johnson EM, Gaddy JA, Voss BJ, Hennig EE, Cover TL. 2014. Genes required for assembly of pili associated with the Helicobacter pylori cag type IV secretion system. Infect Immun 82:3457–3470. http://dx.doi.org/10.1128/IAI.01640-14.
37. 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.
38. 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. http://dx.doi.org/10.1128/JB.00946-09.
39. Jurik A, Hausser E, Kutter S, Pattis I, Prassl S, Weiss E, Fischer W. 2010. The coupling protein Cagbeta and its interaction partner CagZ are required for type IV secretion of the Helicobacter pylori CagA protein. Infect Immun 78:5244–5251. http://dx.doi.org/10.1128/IAI.00796-10.
40. Sarkar MK, Husnain SI, Jakubowski SJ, Christie PJ. 2013. Isolation of bacterial type IV machine subassemblies. Methods Mol Biol 966:187–204. http://dx.doi.org/10.1007/978-1-62703-245-2_12.
41. Kubori T, Koike M, Bui XT, Higaki S, Aizawa S-, Nagai H. 2014. Native structure of a type IV secretion system core complex essential for Legionella pathogenesis. Proc Natl Acad Sci U S A 111:11804–11809. http://dx.doi.org/10.1073/pnas.1404506111.
42. Rohde M, Püls 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. http://dx.doi.org/10.1046/j.1365-2958.2003.03549.x.
43. 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.
44. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, König 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.
45. Murata-Kamiya N, Kikuchi K, Hayashi T, Higashi H, Hatakeyama M. 2010. Helicobacter pylori exploits host membrane phosphatidylserine for delivery, localization, and pathophysiological action of the CagA oncoprotein. Cell Host Microbe 7:399–411. http://dx.doi.org/10.1016/j.chom.2010.04.005.
46. Ohi M, Li Y, Cheng Y, Walz T. 2004. Negative staining and image classification—powerful tools in modern electron microscopy. Biol Proced Online 6:23–34. http://dx.doi.org/10.1251/bpo70.
47. Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, Leith A, Frank J. 2008. Spider image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3:1941–1974. http://dx.doi.org/10.1038/nprot.2008.156.