Plasticity of Repetitive DNA Sequences within a Bacterial (Type IV) Secretion System Component

Journal of Experimental Medicine

Volumn 198, Issue 9, 2003, Pages 1349-1360

  Aras, Rahul A ^a,d   Fischer, Wolfgang ^b   Perez Perez, Guillermo I ^a   Crosatti, MariaLuisa ^a   Ando, Takafumi ^c   Haas, Rainer ^b   Blaser, Martin J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

^c NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d Watson School of Biological Sciences   (United States)

Author keywords

Antigenic variation; Genome plasticity; Helicobacter pylori; Pathogenicity island; Type IV secretion system

Indexed keywords

BACTERIAL PROTEIN; GENE PRODUCT; INTERLEUKIN 8; PROTEIN CAGY; REPETITIVE DNA; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ANTIGEN RECOGNITION; ANTIGENIC VARIATION; ARTICLE; BACTERIAL GENE; BACTERIUM PILUS; CAGY GENE; CELL SECRETION; CONTROLLED STUDY; DNA RECOMBINATION; DNA SEQUENCE; GENE DELETION; GENE DUPLICATION; GENOME; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMORAL IMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENICITY; PERSISTENT INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA PRIMERS; DNA, BACTERIAL; HELICOBACTER PYLORI; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 0242526249     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20030381     Document Type: Article

References (65)

1. Finlay, B.B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
2. Woolhouse, M.E., L.H. Taylor, and D.T. Haydon. 2001. Population biology of multihost pathogens. Science. 292:1109-1112.
3. Krinos, C.M., M.J. Coyne, K.G. Weinacht, A.O. Tzianabos, D.L. Kasper, and L.E. Comstock. 2001. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature. 414:555-558.
4. Dworkin, J., and M.J. Blaser. 1997. Nested DNA inversion as a paradigm of programmed gene rearrangement. Proc. Natl. Acad. Sci. USA. 94:985-990.
5. McCulloch, R., G. Rudenko, and P. Borst. 1997. Gene conversions mediating antigenic variation in Trypanosoma brucei can occur in variant surface glycoprotein expression sites lacking 70-base-pair repeat sequences. Mol. Cell. Biol. 17:833-843.
6. Stevenson, B., S. Casjens, and P. Rosa. 1998. Evidence of past recombination events among the genes encoding the Erp antigens of Borrelia burgdorferi. Microbiol. 144:1869-1879.
7. Biswas, B., R. Vemulapalli, and S.K. Dutta. 1996. Molecular basis for antigenic variation of a protective strain-specific antigen of Ehrlichia risticii. Infect. Immun. 66:3682-3688.
8. Madoff, L.C., J.L. Michel, E.W. Gong, D.E. Kling, and D.L. Kasper. 1996. Group B streptococci escape host immunity by deletion of tandem repeat elements of the alpha C protein. Proc. Natl. Acad. Sci. USA. 93:4136-4141.
9. Peek, R.M., Jr., and M.J. Blaser. 2002. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer. 2:28-37.
10. Blanchard, T.G., S.J. Czinn, and J.G. Nedrud. 1999. Host response and vaccine development to Helicobacter pylori infection. Curr. Top. Microbiol. Immunol. 241:183-214.
11. Perez-Perez, G.I., A. Salomaa, T.U. Kosunen, B. Daverman, H. Rautelin, A. Aromaa, P. Knekt, and M.J. Blaser. 2002. Evidence that cagA(+) Helicobacter pylori strains are disappearing more rapidly than cagA(-) strains. Gut. 50:4295-4298.
12. Censini, S., C. Lange, Z. Xiang, J.E. Crabtree, P. Ghiara, M. Borodovsky, R. Rappuoli, and A. Covacci. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA. 93:14648-14653.
13. Akopyants, N.S., S.W. Clifton, D. Kersulyte, J.E. Crabtree, B.E. Youree, C.A. Reece, N.O. Bukanov, E.S. Drazek, B.A. Roe, and D.E. Berg. 1998. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol. Microbiol. 28:37-53.
14. Tummuru, M.K., S.A. Sharma, and M.J. Blaser. 1995. Helicobacter pylori picB, a homologue of the Bordetella pertussis toxin secretion protein, is required for induction of IL-8 in gastric epithelial cells. Mol. Microbiol. 18:867-876.
15. + Helicobacter pylori strains. Lab Invest. 73:760-770.
16. Crabtree, J.E. 1998. Role of cytokines in pathogenesis of Helicobacter pylori-induced mucosal damage. Dig. Dis. Sci. 43:46-55.
17. Lindholm, C., M. Quiding-Jarbrink, H. Lonroth, A. Hamlet, and A.M. Svennerholm. 1998. Local cytokine response in Helicobacter pylori-infected subjects. Infect. Immun. 66:5964-5971.
18. Blaser, M.J., G.I. Perez-Perez, H. Kleanthous, T.L. Cover, R.M. Peek, P.H. Chyou, G.N. Stemmermann, and A. Nomura. 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.
19. Alm, R.A., L.S. Ling, D.T. Moir, B.L. King, E.D. Brown, P.C. Doig, D.R. Smith, B. Noonan, B.C. Guild, B.L. deJonge, et al. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen. Helicobacter pylori. Nature. 397:176-180.
20. Segal, E.D., J. Cha, J. Lo, S. Falkow, and L.S. Tompkins. 1999. Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc. Natl. Acad. Sci. USA. 96:14559-14564.
21. Odenbreit, S., J. Puls, B. Sedlmaier, E. Gerland, W. Fisher, and R. Haas. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science. 287:1497-1500.
22. Stein, M., R. Rappuoli, and A. Covacci. 2000. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl. Acad. Sci. USA. 97:1263-1268.
23. Higashi, H., R. Tsutsumi, S. Muto, T. Sugiyama, T. Azuma, M. Asaka, and M. Hatakeyama. 2002. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science. 295:683-686.
24. Selbach, M., S. Moese, C.R. Hauck, T.F. Meyer, and S. Backert. 2002. Src is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J. Biol. Chem. 277:6775-6778.
25. Galan, J.E., and A. Collmer. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science. 284:1322-1328.
26. Christie, P.J., and J.P. Vogel. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354-360.
27. Tomb, J.F., O. White, A.R. Kerlavage, R.A. Clayton, G.G. Sutton, R.D. Fleischman, K.A. Ketchum, H.P. Klenk, S. Gill, B.A. Dougherty, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature. 388:539-547.
28. Fischer, W., J. Püls, R. Buhrdorf, B. Gebert, S. Odebreit, and R. Haas. 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.
29. Liu, G., T.K. McDaniel, S. Falkow, and S. Karlin. 1999. Sequence anomalies in the Cag7 gene of the Helicobacter pylori pathogenicity island. Proc. Natl. Acad. Sci. USA. 96:7011-7016.
30. Lovett, S.T., R.L. Hurley, V.A. Sutera, Jr., R.H. Aubuchon, and M.A. Lebedeva. 2002. Crossing over between regions of limited homology in Escherichia coli. RecA-dependent and RecA-independent pathways. Genetics. 160:851-859.
31. van der Ende, A., E.A.J. Rauws, M. Feller, C.J.J. Mulder, G.N.J. Tytgat, and J. Dankert. 1996. Heterogeneous Helicobacter pylori isolates from members of a family with a history of peptic ulcer disease. Gastroenterol. 111:638-647.
32. Kuipers, E.J., D.A. Israel, J.G. Kusters, M.M. Gerrits, J. Weel, A. van der Ende, R.W. van Der Hulst, H.P. Wirth, J. Hook-Nikanne, S.A. Thompson, et al. 2000. Quasispecies development of Helicobacter pylori observed in paired isolates obtained years apart from the same host. J. Infect. Dis. 181:273-282.
33. Dubois, A., D.E. Berg, E.T. Incecik, N. Fiala, L.M. Heman-Ackah, J. Del Valle, M. Yang, H.P. Wirth, G.I. Perez-Perez, and M.J. Blaser. 1999. Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates. Gastroenterology. 16:90-96.
34. Wilson, K. 1987. Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology. F.A. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, and J.G. Seidman, editors. John Wiley & Sons, New York. 2.4.1-2.4.2.
35. Israel, D.A., N. Salama, C.N. Arnold, S.F. Moss, T. Ando, H.P. Wirth, K.T. Tham, M. Camorlinga, M.J. Blaser, S. Falkow, et al. 2001. Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J. Clin. Invest. 107:611-620.
36. Sozzi, M., M. Crosatti, S.K. Kim, J. Romero, and M.J. Blaser. 2001. Heterogeneity of Helicobacter pylori cag genotypes in experimentally infected mice. FEMS Microbiol. Lett. 203:109-114.
37. Kersulyte, D., H. Chalkauskas, and D.E. Berg. 1999. Emergence of recombinant strains of Helicobacter pylori during human infection. Mol. Microbiol. 31:31-43.
38. Rohde, M., J. Püls, R. Buhrdorf, W. Fischer, and R. Haas. 2003. A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system. Mol. Microbiol. 49:219-234.
39. Peek, A.S., V. Souza, L.E. Eguiarte, and B.S. Gaut. 2001. The interaction of protein structure, selection, and recombination on the evolution of the type-1 fimbrial major subunit (fimA) from Escherichia coli. J. Mol. Evol. 52:193-204.
40. Baga, M., S. Normark, J. Hardy, P. O'Hanley, D. Lark, O. Olsson, G. Schoolnik, and S. Falkow. 1984. Nucleotide sequence of the papA gene encoding the Pap pilus subunit of human uropathogenic Escherichia coli. J. Bacteriol. 157:330-333.
41. Schmoll, T., H. Hoschutzky, J. Morschhauser, F. Lottspeich, K. Jann, and J. Hacker. 1989. Analysis of genes coding for the sialic acid-binding adhesin and two other minor fimbrial subunits of the S-fimbrial adhesin determinant of Escherichia coli. Mol. Microbiol. 3:1735-1744.
42. Bessen, D.E., and S.K. Hollingshead. 1994. Allelic polymorphism of emm loci provides evidence for horizontal gene spread in group A streptococci. Proc. Natl. Acad. Sci. USA. 91:3280-3284.
43. Achtman, M., T. Azuma, D.E. Berg, Y. Ito, G. Morelli, Z.J. Pan, S. Suerbaum, S.A. Thompson, A. van der Ende, and L.J. van Doorn. 1999. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol. Microbiol. 32:459-470.
44. Bzymek, M., C.J. Saveson, V.V. Feschenko, and S.T. Lovett. 1999. Slipped misalignment mechanisms of deletion formation: in vivo susceptibility to nucleases. J. Bacteriol. 181:477-482.
45. Aras, R.A., T. Takata, T. Ando, A. van der Ende, and M.J. Blaser. 2001. Regulation of the HpyII restriction-modification system of Helicobacter pylori by gene deletion and horizontal reconstitution. Mol. Microbiol. 42:369-382.
46. Israel, D.A., N. Salama, U. Krishna, U.M. Rieger, J.C. Atherton, S. Falkow, and R.M. Peek, Jr. 2001. Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc. Natl. Acad. Sci. USA. 98:14625-14630.
47. Blaser, M.J., and D. Kirschner. 1999. Dynamics of Helicobacter pylori colonization in relation to the host response. Proc. Natl. Acad. Sci. USA. 96:8359-8364.
48. Hooper, L.V., and J.I. Gordon. 2001. Commensal host-bacterial relationships in the gut. Science. 292:1115-1118.
49. Alm, R.A., and T. Trust. 1999. Analysis of the genetic diversity of Helicobacter pylori: the tale of two genomes. J. Mol. Med. 77:834-847.
50. Achaz, G., E.P. Pocha, P. Netter, and E. Coissac. 2002. Origin and fate of repeats in bacteria. Nucleic Acids Res. 30:2987-2994.
51. Bjorkholm, B., A. Lundin, A. Sillen, K. Guillemin, N. Salama, C. Rubio, J.I. Gordon, P. Falk, and L. Engstrand. 2001. Comparison of genetic divergence and fitness between two subclones of Helicobacter pylori. Infect. Immun. 69:7832-7838.
52. Webb, G.F., and M.J. Blaser. 2002. Dynamics of bacterial phenotype selection in a colonized host. Proc. Natl. Acad. Sci. USA. 99:3135-3140.
53. Nedenskov-Sorensen, P., G. Bukholm, and K. Bovre. 1990. Natural competence for genetic transformation in Campylobacter pylori. J. Infect. Dis. 161:365-366.
54. Tsuda, M., M. Karita, and T. Nakazawa. 1993. Genetic transformation in Helicobacter pylori. Microbiol. Immunol. 37:85-89.
55. Suerbaum, S., J.M. Smith, K. Bapumia, G. Morelli, N.H. Smith, E. Kunstmann, I. Dyrek, and M. Achtman. 1998. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. USA. 95:12619-12624.
56. Kuipers, E.J., D.A. Israel, J.G. Kusters, and M.J. Blaser. 1998. Evidence for a conjugation-like mechanism of DNA transfer in Helicobacter pylori. J. Bacteriol. 180:2901-2905.
57. Seifert, H.S. 1996. Questions about gonococcal pilus phase- and antigenic variation. Mol. Microbiol. 21:433-440.
58. Allred, D.R., J.M.R. Carlton, R.L. Satcher, J.A. Long, W.C. Brown, P.E. Patterson, R.M. O'Connor, and S.E. Stroup. 2000. The ves multigene family of B. bovis encodes components of rapid antigenic variation at the infected erythrocyte surface. Mol. Cell. 5:153-162.
59. Ghose, C., G.I. Perez-Perez, M.G. Dominguez-Bello, D.T. Pride, C.M. Bravi, and M.J. Blaser. 2002. East Asian genotypes of Helicobacter pylori strains in Amerindians provide evidence for its ancient human carriage. Proc. Natl. Acad. Sci. USA. 99:15107-15111.
60. Bjorkholm, B., M. Sjolund, P.G. Falk, O.G. Berg, L. Engstrand, and D.I. Andersson. 2001. Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc. Natl. Acad. Sci. USA. 98:14607-14612.
61. Pride, D.T., R.J. Meinersmann, and M.J. Blaser. 2001. Allelic variation within Helicobacter pylori babA and babB. Infect. Immun. 69:1160-1171.
62. Wirth, H.P., M. Yang, M. Karita, and M.J. Blaser. 1996. Expression of the human cell surface glycoconjugates Lewis x and Lewis y by Helicobacter pylori isolates is related to cagA status. Infect. Immun. 64:4598-4605.
63. Ayala, F.J., and S.M. Rich. 2000. Genetic variation and the recent worldwide expansion of Plasmodium falciparum. Gene. 261:161-170.
64. Aras, R.A., J. Kang, A.I. Tschumi, and M.J. Blaser. Extensive repetitive DNA facilitates prokaryotic genome plasticity. Proc. Natl. Acad. Sci. USA. In press.
65. Rocha, E.P., A. Danchin, and A. Viari. 1999. Functional and evolutionary roles of long repeats in prokaryotes. Res. Microbiol. 150:725-733.