Intrastrain heterogeneity of the mgpB gene in Mycoplasma genitalium is extensive in vitro and in vivo and suggests that variation is generated via recombination with repetitive chromosomal sequences

Infection and Immunity

Volumn 74, Issue 7, 2006, Pages 3715-3726

  Iverson Cabral, Stefanie L ^a   Astete, Sabina G ^a   Cohen, Craig R ^b   Rocha, Eduardo P C ^c   Totten, Patricia A ^a,d  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CASE REPORT; FEMALE; GENETIC HETEROGENEITY; GENETIC RECOMBINATION; HUMAN; MGPB GENE; MYCOPLASMA GENITALIUM; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PERSISTENT INFECTION; PRIORITY JOURNAL; STRAIN DIFFERENCE;

ADHESINS, BACTERIAL; ADULT; BACTERIAL ADHESION; BASE SEQUENCE; CHROMOSOMES, BACTERIAL; EVOLUTION, MOLECULAR; FEMALE; HUMANS; MOLECULAR SEQUENCE DATA; MYCOPLASMA GENITALIUM; MYCOPLASMA INFECTIONS; RECOMBINATION, GENETIC; REPETITIVE SEQUENCES, NUCLEIC ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY; VARIATION (GENETICS);

EID: 33745606207     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00239-06     Document Type: Article

References (60)

1. Amundsen, S. K., and G. R. Smith. 2003. Interchangeable parts of the Escherichia coli recombination machinery. Cell 112:741-744.
2. Aravind, L., and E. V. Koonin. 1998. A novel family of predicted phosphoesterases includes Drosophila prune protein and bacterial RecJ exonuclease. Trends Biochem. Sci. 23:17-19.
3. Bjornelius, E., P. Lidbrink, and J. S. Jensen. 2000. Mycoplasma genitalium in non-gonococcal urethritis - a study in Swedish male STD patients. Int. J. STD AIDS 11:292-296.
4. Carvalho, F. M., M. M. Fonseca, S. Batistuzzo De Medeiros, K. C. Scortecci, C. A. Blaha, and L. F. Agnez-Lima. 2005. DNA repair in reduced genome: the mycoplasma model. Gene 360:111-119.
5. Centurion-Lara, A., R. E. LaFond, K. Hevner, C. Godornes, B. J. Molini, W. C. Van Voorhis, and S. A. Lukehart. 2004. Gene conversion: a mechanism for generation of heterogeneity in the tprK gene of Treponema pallidum during infection. Mol. Microbiol. 52:1579-1596.
6. Clausen, H. F., J. Fedder, M. Drasbek, P. K. Nielsen, B. Toft, H. J. Ingerslev, S. Birkelund, and G. Christiansen. 2001. Serological investigation of Mycoplasma genitalium in infertile women. Hum. Reprod. 16:1866-1874.
7. Cohen, C. R., L. E. Manhart, E. A. Bukusi, S. Astete, R. C. Brunham, K. K. Holmes, S. K. Sinei, J. J. Bwayo, and P. A. Totten. 2002. Association between Mycoplasma genitalium and acute endometritis. Lancet 359:765-766.
8. Collier, A. M., J. L. Carson, P. C. Hu, S. S. Hu, C. H. Huang, and M. F. Barile. 1990. Attachment of Mycoplasma genitalium to the ciliated epithelium of human fallopian tubes, p. 730-732. In G. H. C. G. Stanek, J. G. Tully, and R. F. Whitcomb (ed.), Recent advances in mycoplasmology. Gustav Fischer Verlag, Stuttgart, Germany.
9. Colman, S. D., P. C. Hu, W. Litaker, and K. F. Bott. 1990. A physical map of the Mycoplasma genitalium genome. Mol. Microbiol. 4:683-687.
10. Dallo, S. F., and J. B. Baseman. 1991. Adhesin gene of Mycoplasma genitalium exists as multiple copies. Microb. Pathog. 10:475-480.
11. Dallo, S. F., J. R. Horton, C. J. Su, and J. B. Baseman. 1989. Homologous regions shared by adhesin genes of Mycoplasma pneumoniae and Mycoplasma genitalium. Microb. Pathog. 6:69-73.
12. Dehio, C., S. D. Gray-Owen, and T. F. Meyer. 1998. The role of neisserial Opa proteins in interactions with host cells. Trends Microbiol. 6:489-495.
13. Dorigo-Zetsma, J. W., J. Dankert, and S. A. Zaat. 2000. Genotyping of Mycoplasma pneumoniae clinical isolates reveals eight P1 subtypes within two genomic groups. J. Clin. Microbiol. 38:965-970.
14. Dorigo-Zetsma, J. W., B. Wilbrink, J. Dankert, and S. A. Zaat. 2001. Mycoplasma pneumoniae P1 type 1- and type 2-specific sequences within the P1 cytadhesin gene of individual strains. Infect. Immun. 69:5612-5618.
15. Dumke, R., I. Catrein, E. Pirkil, R. Herrmann, and E. Jacobs. 2003. Subtyping of Mycoplasma pneumoniae isolates based on extended genome sequencing and on expression profiles. Int. J. Med. Microbiol. 292:513-525.
16. Dutro, S. M., J. K. Hebb, C. A. Garin, J. P. Hughes, G. E. Kenny, and P. A. Totten. 2003. Development and performance of a microwell-plate-based polymerase chain reaction assay for Mycoplasma genitalium. Sex. Transm. Dis. 30:756-763.
17. Fraser, C. M., J. D. Gocayne, O. White, M. D. Adams, R. A. Clayton, R. D. Fleischmann, C. J. Bull, A. R. Kerlavage, G. Sutton, J. M. Kelley, R. D. Fritchman, J. F. Weidman, K. V. Small, M. Sandusky, J. Fuhrmann, D. Nguyen, T. R. Utterback, D. M. Saudek, C. A. Phillips, J. M. Merrick, J. F. Tomb, B. A. Dougherty, K. F. Bott, P. C. Hu, T. S. Lucier, S. N. Peterson, H. O. Smith, C. A. Hutchison III, and J. C. Venter. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397-403.
18. Gambini, D., I. Decleva, L. Lupica, M. Ghislanzoni, M. Cusini, and E. Alessi. 2000. Mycoplasma genitalium in males with nongonococcal urethritis: prevalence and clinical efficacy of eradication. Sex. Transm. Dis. 27:226-229.
19. Hamrick, T. S., J. A. Dempsey, M. S. Cohen, and J. G. Cannon. 2001. Antigenic variation of gonococcal pilin expression in vivo: analysis of the strain FA1090 pilin repertoire and identification of the pilS gene copies recombining with pilE during experimental human infection. Microbiology 147:839-849.
20. Hauck, C. R., and T. F. Meyer. 2003. 'Small' talk: Opa proteins as mediators of Neisseria-host-cell communication. Curr. Opin. Microbiol. 6:43-49.
21. Hjorth, S. V., E. Björnelius, P. Lidbrink, L. Falk, B. Dohn, L. Berthelsen, L. Ma, D. H. Martin, and J. S. Jensen. Sequence based typing of Mycoplasma genitalium reveals sexual transmission. J. Clin. Micriobiol., in press.
22. Horner, P., B. Thomas, C. Gilroy, M. Egger, M. McClure, and D. Taylor-Robinson. 2003. Antibodies to Chlamydia trachomatis heat-shock protein 60 kDa and detection of Mycoplasma genitalium and Ureaplasma urealyticum are associated independently with chronic nongonococcal urethritis. Sex. Transm. Dis. 30:129-133.
23. Horner, P. J., C. B. Gilroy, B. J. Thomas, R. O. Naidoo, and D. Taylor-Robinson. 1993. Association of Mycoplasma genitalium with acute non-gonococcal urethritis. Lancet 342:582-585.
24. Bowell-Adams, B., and B. S. Seifert. 2000. Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol. Microbiol. 37:1146-1158.
25. Bu, P. C., U. Schaper, A. M. Collier, W. A. Clyde, Jr., M. Borikawa, Y. S. Buang, and M. F. Barile. 1987. A Mycoplasma genitalium protein resembling the Mycoplasma pneumoniae attachment protein. Infect. Immun. 55:1126-1131.
26. Inamine, J. M., K. C. Bo, S. Loechel, and P. C. Bu. 1990. Evidence that UGA is read as a tryptophan codon rather than as a stop codon by Mycoplasma pneumoniae, Mycoplasma genitalium, and Mycoplasma gallisepticum. J. Bacteriol. 172:504-506.
27. Inamine, J. M., S. Loechel, A. M. Collier, M. F. Barile, and P. C. Bu. 1989. Nucleotide sequence of the MgPa (mgp) operon of Mycoplasma genitalium and comparison to the P1 (mpp) operon of Mycoplasma pneumoniae. Gene 82:259-267.
28. Jensen, J. S. 2004. Mycoplasma genitalium: the aetiological agent of urethritis and other sexually transmitted diseases. J. Eur. Acad. Dermatol. Venereol. 18:1-11.
29. Jensen, J. S., E. Bjornelius, B. Dohn, and P. Lidbrink. 2004. Use of TaqMan 5′ nuclease real-time PCR for quantitative detection of Mycoplasma genitalium DNA in males with and without urethritis who were attendees at a sexually transmitted disease clinic. J. Clin. Microbiol. 42:683-692.
30. Jensen, J. S., R. Orsum, B. Dohn, S. Uldum, A. M. Worm, and K. Lind. 1993. Mycoplasma genitalium: a cause of male urethritis? Genitourin. Med. 69:265-269.
31. Jonsson, A. B., D. Ilver, P. Falk, J. Pepose, and S. Normark. 1994. Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol. Microbiol. 13:403-416.
32. Kenny, G. E. 1985. Mycoplasmas, p. 407-411. In H. W. Balows and H. J. Shadomy (ed.), Manual of clinical microbiology, 4th ed. American Society for Microbiology, Washington, D.C.
33. Kenri, T., R. Taniguchi, Y. Sasaki, N. Okazaki, M. Narita, K. Izumikawa, M. Umetsu, and T. Sasaki. 1999. Identification of a new variable sequence in the P1 cytadhesin gene of Mycoplasma pneumoniae: evidence for the generation of antigenic variation by DNA recombination between repetitive sequences. Infect. Immun. 67:4557-4562.
34. Maeda, S., M. Tamaki, M. Nakano, M. Uno, T. Deguchi, and Y. Kawada. 1998. Detection of Mycoplasma genitalium in patients with urethritis. J. Urol. 159:405-407.
35. Manhart, L. E., C. W. Critchlow, K. K. Bolmes, S. M. Dutro, D. A. Eschenbach, C. E. Stevens, and P. A. Totten. 2003. Mucopurulent cervicitis and Mycoplasma genitalium. J. Infect. Dis. 187:650-657.
36. Miller, J. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
37. Morrison-Plummer, J., A. Lazzell, and J. B. Baseman. 1987. Shared epitopes between Mycoplasma pneumoniae major adhesin protein P1 and a 140-kilodalton protein of Mycoplasma genitalium. Infect. Immun. 55:49-56.
38. Nassif, X., C. Pujol, P. Morand, and E. Eugene. 1999. Interactions of pathogenic Neisseria with host cells. Is it possible to assemble the puzzle? Mol. Microbiol. 32:1124-1132.
39. Nassif, X., and M. So. 1995. Interaction of pathogenic neisseriae with non-phagocytic cells. Clin. Microbiol. Rev. 8:376-388.
40. Opitz, O., and E. Jacobs. 1992. Adherence epitopes of Mycoplasma genitalium adhesin. J. Gen. Microbiol. 138:1785-1790.
41. Pepin, J., A. C. Labbe, N. Khonde, S. Deslandes, M. Alary, A. Dzokoto, C. Asamoah-Adu, B. Meda, and E. Frost. 2005. Mycoplasma genitalium: an organism commonly associated with cervicitis among west African sex workers. Sex. Transm. Infect. 81:67-72.
42. Peterson, S. N., C. C. Bailey, J. S. Jensen, M. B. Borre, E. S. King, K. F. Bott, and C. A. Hutchison III. 1995. Characterization of repetitive DNA in the Mycoplasma genitalium genome: possible role in the generation of antigenic variation. Proc. Natl. Acad. Sci. USA 92:11829-11833.
43. Peterson, S. N., P. C. Hu, K. F. Bott, and C. A. Hutchison III. 1993. A survey of the Mycoplasma genitalium genome by using random sequencing. J. Bacteriol. 175:7918-7930.
44. Rocha, E. P., and A. Blanchard. 2002. Genomic repeats, genome plasticity and the dynamics of Mycoplasma evolution. Nucleic Acids Res. 30:2031-2042.
45. Rocha, E. P., E. Cornet, and B. Michel. 2005. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet. 1:e15.
46. Ruland, K., R. Wenzel, and R. Herrmann. 1990. Analysis of three different repeated DNA elements present in the P1 operon of Mycoplasma pneumoniae: size, number and distribution on the genome. Nucleic Acids Res. 18:6311-6317.
47. Shen, P., and H. V. Huang. 1986. Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112:441-457.
48. Simms, I., K. Eastick, H. Mallinson, K. Thomas, R. Gokhale, P. Hay, A. Herring, and P. A. Rogers. 2003. Associations between Mycoplasma genitalium, Chlamydia trachomatis and pelvic inflammatory disease. J. Clin. Pathol. 56:616-618.
49. Su, C. J., and J. B. Baseman. 1990 Genome size of Mycoplasma genitalium. J. Bacteriol. 172:4705-4707.
50. Su, C. J., A. Chavoya, S. F. Dallo, and J. B. Baseman. 1990. Sequence divergency of the cytadhesin gene of Mycoplasma pneumoniae. Infect. Immun. 58:2669-2674.
51. Su, C. J., S. F. Dallo, A. Chavoya, and J. B. Baseman. 1993. Possible origin of sequence divergence in the P1 cytadhesin gene of Mycoplasma pneumoniae. Infect. Immun. 61:816-822.
52. Taylor-Robinson, D. 2002. Mycoplasma genitalium - an up-date. Int. J. STD AIDS 13:145-151.
53. Taylor-Robinson, D., C. B. Gilroy, B. J. Thomas, and P. E. Hay. 2004. Mycoplasma genitalium in chronic non-gonococcal urethritis. Int. I. STD AIDS 15:21-25.
54. Tomb, J. F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, E. K. Hickey, D. E. Berg, J. D. Gocayne, T. R. Utterback, J. D. Peterson, J. M. Kelley, M. D. Cotton, J. M. Weidman, C. Fujii, C. Bowman, L. Watthey, E. Wallin, W. S. Hayes, M. Borodovsky, P. D. Karp, H. O. Smith, C. M. Fraser, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
55. Totten, P. A., L. E. Manhart, and A. Centurion-Lara. 2004. PCR detection of Haemophilus ducreyi, Treponema pallidum, and Mycoplasma genitalium, p. 349-360. In D. H. Persing, F. C. Tenover, I. Versalovic, Y.-W. Tang, E. R. Unger, D. A. Relman, and T. I. White (ed.), Molecular microbiology: diagnostic principles and practice. ASM Press, Washington, D.C.
56. Totten, P. A., M. A. Schwartz, K. E. Sjostrom, G. E. Kenny, H. H. Handsfield, J. B. Weiss, and W. L. Whittington. 2001. Association of Mycoplasma genitalium with nongonococcal urethritis in heterosexual men. I. Infect. Dis. 183:269-276.
57. Tully, J. G., D. Taylor-Robinson, R. M. Cole, and D. L. Rose. 1981. A newly discovered mycoplasma in the human urogenital tract. Lancet i:1288-1291.
58. Tully, J. G., D. Taylor-Robinson, D. L. Rose, R. M. Cole, and J. M. Bove. 1983. Mycoplasma genitalium, a new species from the human urogenital tract. Int. I. Syst. Bacteriol. 33:387-396.
59. Watt, V. M., C. J. Ingles, M. S. Urdea, and W. J. Rutter. 1985. Homology requirements for recombination in Escherichia coli. Proc. Natl. Acad. Sci. USA 82:4768-4772.
60. Wenzel, R., E. Pirkl, K. Ruland, and R. Herrmann. 1990. Multiple copies of Mycoplasma pneumoniae gene P1 sequences, p. 193-198. In G. H. C. G. Stanek, J. G. Tully, and R. F. Whitcomb (ed.), Recent advances in mycoplasmology. Gustav Fischer Verlag, Stuttgart, Germany.