Isolation and characterization of P1 adhesin, a leg protein of the gliding bacterium mycoplasma pneumoniae

Journal of Bacteriology

Volumn 193, Issue 3, 2011, Pages 715-722

  Nakane, Daisuke ^a   Adan Kubo, Jun ^a   Kenri, Tsuyoshi ^b   Miyata, Makoto ^a  

^a Osaka Prefecture University   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; P1 ADHESIN; UNCLASSIFIED DRUG;

ARTICLE; CROSS LINKING; ELECTRON MICROSCOPY; MOLECULAR WEIGHT; MYCOPLASMA PNEUMONIAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN ISOLATION;

ADHESINS, BACTERIAL; CHROMATOGRAPHY, GEL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; MICROSCOPY, ELECTRON; MOLECULAR WEIGHT; MYCOPLASMA PNEUMONIAE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS); MYCOPLASMA; MYCOPLASMA PNEUMONIAE;

EID: 78751536185     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00796-10     Document Type: Article

References (65)

1. Adan-Kubo, J., A. Uenoyama, T. Arata, and M. Miyata. 2006. Morphology of isolated Gli349, a leg protein responsible for glass binding of Mycoplasma mobile gliding revealed by rotary-shadowing electron microscopy. J. Bacteriol. 188:2821-2828.
2. Aluotto, B. B., R. G. Wittler, C. O. Williams, and J. E. Faber. 1970. Standardized bacteriologic techniques for the characterization of mycoplasma species. Int. J. Syst. Bacteriol. 20:35-58.
3. Arata, T. 1998. Electron microscopic observation of monomeric actin attached to a myosin head. J. Struct. Biol. 123:8-16.
4. Burgos, R., et al. 2006. Mycoplasma genitalium P140 and P110 cytadhesins are reciprocally stabilized and required for cell adhesion and terminalorganelle development. J. Bacteriol. 188:8627-8637.
5. Catrein, I., R. Herrmann, A. Bosserhoff, and T. Ruppert. 2005. Experimental proof for a signal peptidase I like activity in Mycoplasma pneumoniae, but absence of a gene encoding a conserved bacterial type I SPase. FEBS J. 272:2892-2900.
6. Dandekar, T., et al. 2000. Re-annotating the Mycoplasma pneumoniae genome sequence: adding value, function and reading frames. Nucleic Acids Res. 28:3278-3288.
7. Fraser, C. M., et al. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397-403.
8. Gerstenecker, B., and E. Jacobs. 1990. Topological mapping of the P1- adhesin of Mycoplasma pneumoniae with adherence-inhibiting monoclonal antibodies. J. Gen. Microbiol. 136:471-476.
9. Glasgow, L. R., and R. L. Hill. 1980. Interaction of Mycoplasma gallisepticum with sialyl glycoproteins. Infect. Immun. 30:353-361.
10. Himmelreich, R., et al. 1996. Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Res. 24:4420-4449.
11. Hiratsuka, Y., M. Miyata, T. Tada, and T. Q. P. Uyeda. 2006. A microrotary motor powered by bacteria. Proc. Natl. Acad. Sci. U. S. A. 103:13618-13623.
12. Hu, P. C., et al. 1982. Mycoplasma pneumoniae infection: role of a surface protein in the attachment organelle. Science 216:313-315.
13. Hu, P. C., A. M. Collier, and J. B. Baseman. 1977. Surface parasitism by Mycoplasma pneumoniae of respiratory epithelium. J. Exp. Med. 145:1328-1343.
14. Iverson-Cabral, S. L., S. G. Astete, C. R. Cohen, E. P. Rocha, and P. A. Totten. 2006. 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. Infect. Immun. 74:3715-3726.
15. Jacobs, E., K. Fuchte, and W. Bredt. 1988. Isolation of the adherence protein of Mycoplasma pneumoniae by fractionated solubilization and size exclusion chromatography. Biol. Chem. Hoppe Seyler 369:1295-1299.
16. Jacobs, E., R. Rock, and L. Dalehite. 1990. A B cell-, T cell-linked epitope located on the adhesin of Mycoplasma pneumoniae. Infect. Immun. 58:2464-2469.
17. Jaffe, J. D., et al. 2004. The complete genome and proteome of Mycoplasma mobile. Genome Res. 14:1447-1461.
18. Kenri, T., et al. 2004. Use of fluorescent-protein tagging to determine the subcellular localization of Mycoplasma pneumoniae proteins encoded by the cytadherence regulatory locus. J. Bacteriol. 186:6944-6955.
19. Kenri, T., et al. 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.
20. Kirchhoff, H. 1992. Motility, p. 289-306. In J. Maniloff, R. N. McElhaney, L. R. Finch, and J. B. Baseman (ed.), Mycoplasmas - molecular biology and pathogenesis. American Society for Microbiology, Washington, DC.
21. Kirchhoff, H., R. Rosengarten, W. Lotz, M. Fischer, and D. Lopatta. 1984. Flask-shaped mycoplasmas: properties and pathogenicity for man and animals. Israel J. Med. Sci. 20:848-853.
22. Krause, D. C., and M. F. Balish. 2004. Cellular engineering in a minimal microbe: structure and assembly of the terminal organelle of Mycoplasma pneumoniae. Mol. Microbiol. 51:917-924.
23. Krivan, H. C., L. D. Olson, M. F. Barile, V. Ginsburg, and D. D. Roberts. 1989. Adhesion of Mycoplasma pneumoniae to sulfated glycolipids and inhibition by dextran sulfate. J. Biol. Chem. 264:9283-9288.
24. Krunkosky, T. M., J. L. Jordan, E. Chambers, and D. C. Krause. 2007. Mycoplasma pneumoniae host-pathogen studies in an air-liquid culture of differentiated human airway epithelial cells. Microb. Pathog. 42:98-103.
25. Layh-Schmitt, G., and R. Herrmann. 1992. Localization and biochemical characterization of the ORF6 gene product of the Mycoplasma pneumoniae P1 operon. Infect. Immun. 60:2906-2913.
26. Layh-Schmitt, G., and R. Herrmann. 1994. Spatial arrangement of gene products of the P1 operon in the membrane of Mycoplasma pneumoniae. Infect. Immun. 62:974-979.
27. Layh-Schmitt, G., A. Podtelejnikov, and M. Mann. 2000. Proteins complexed to the P1 adhesin of Mycoplasma pneumoniae. Microbiology 146:741-747.
28. Lesoil, C., et al. 2010. Molecular shape and binding force of Mycoplasma mobile's leg protein Gli349 revealed by an AFM study. Biochem. Biophys. Res. Commun. 391:1312-1317.
29. Lipman, R. P., W. A. Clyde, Jr., and F. W. Denny. 1969. Characteristics of virulent, attenuated, and avirulent Mycoplasma pneumoniae strains. J. Bacteriol. 100:1037-1043.
30. Loomes, L. M., et al. 1984. Erythrocyte receptors for Mycoplasma pneumoniae are sialylated oligosaccharides of Ii antigen type. Nature 307:560-563.
31. Metsugi, S., et al. 2005. Sequence analysis of the gliding protein Gli349 in Mycoplasma mobile. Biophysics 1:33-43.
32. Miyata, M. 2008. Centipede and inchworm models to explain Mycoplasma gliding. Trends Microbiol. 16:6-12.
33. Miyata, M. 2007. Molecular mechanism of mycoplasma gliding - a novel cell motility system, p. 137-175. In P. Lenz (ed.), Cell motility. Springer, New York, NY.
34. Miyata, M. 2010. Unique centipede mechanism of Mycoplasma gliding. Annu. Rev. Microbiol. 64:519-537.
35. Miyata, M., and H. Ogaki. 2006. Cytoskeleton of Mollicutes. J. Mol. Microbiol. Biotechnol. 11:256-264.
36. Miyata, M., and J. Petersen. 2004. Spike structure at interface between gliding Mycoplasma mobile cell and glass surface visualized by rapid-freeze and fracture electron microscopy. J. Bacteriol. 186:4382-4386.
37. Miyata, M., W. S. Ryu, and H. C. Berg. 2002. Force and velocity of Mycoplasma mobile gliding. J. Bacteriol. 184:1827-1831.
38. Miyata, M., et al. 2000. Gliding mutants of Mycoplasma mobile: relationships between motility and cell morphology, cell adhesion and microcolony formation. Microbiology 146:1311-1320.
39. Nakane, D., and M. Miyata. 2007. Cytoskeletal "jellyfish" structure of Mycoplasma mobile. Proc. Natl. Acad. Sci. U. S. A. 104:19518-19523.
40. Nakane, D., and M. Miyata. 2009. Cytoskeletal asymmetrical-dumbbell structure of a gliding mycoplasma, Mycoplasma gallisepticum, revealed by negative-staining electron microscopy. J. Bacteriol. 191:3256-3264.
41. Nonaka, T., J. Adan-Kubo, and M. Miyata. 2010. Triskelion structure of Gli521 protein involved in gliding mechanism of Mycoplasma mobile. J. Bacteriol. 192:636-642.
42. Ohtani, N., and M. Miyata. 2007. Identification of a novel nucleoside triphosphatase from Mycoplasma mobile: a prime candidate for motor of gliding motility. Biochem. J. 403:71-77.
43. Opitz, O., and E. Jacobs. 1992. Adherence epitopes of Mycoplasma genitalium adhesin. J. Gen. Microbiol. 138:1785-1790.
44. Papazisi, L., et al. 2003. The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain R(low). Microbiology 149:2307-2316.
45. Peterson, S. N., et al. 1995. Characterization of repetitive DNA in the Mycoplasma genitalium genome: possible role in the generation of antigenic variation. Proc. Natl. Acad. Sci. U. S. A. 92:11829-11833.
46. Razin, S., and E. Jacobs. 1992. Mycoplasma adhesion. J. Gen. Microbiol. 138:407-422.
47. Razin, S., D. Yogev, and Y. Naot. 1998. Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 62:1094-1156.
48. Roberts, D. D., L. D. Olson, M. F. Barile, V. Ginsburg, and H. C. Krivan. 1989. Sialic acid-dependent adhesion of Mycoplasma pneumoniae to purified glycoproteins. J. Biol. Chem. 264:9289-9293.
49. 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.
50. Schägger, H., and G. von Jagow. 1991. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199:223-231.
51. Seto, S., T. Kenri, T. Tomiyama, and M. Miyata. 2005. Involvement of P1 adhesin in gliding motility of Mycoplasma pneumoniae as revealed by the inhibitory effects of antibody under optimized gliding conditions. J. Bacteriol. 187:1875-1877.
52. Seto, S., G. Layh-Schmitt, T. Kenri, and M. Miyata. 2001. Visualization of the attachment organelle and cytadherence proteins of Mycoplasma pneumoniae by immunofluorescence microscopy. J. Bacteriol. 183:1621-1630.
53. Seto, S., and M. Miyata. 2003. The attachment organelle formation represented by localization of cytadherence protein and formation of electrondense core in the wild-type and mutant strains of Mycoplasma pneumoniae. J. Bacteriol. 185:1082-1091.
54. Seto, S., A. Uenoyama, and M. Miyata. 2005. Identification of 521-kilodalton protein (Gli521) involved in force generation or force transmission for Mycoplasma mobile gliding. J. Bacteriol. 187:3502-3510.
55. Seybert, A., R. Herrmann, and A. S. Frangakis. 2006. Structural analysis of Mycoplasma pneumoniae by cryo-electron tomography. J. Struct. Biol. 156: 342-354.
56. Shimizu, T., and M. Miyata. 2002. Electron microscopic studies of three gliding mycoplasmas, Mycoplasma mobile, M. pneumoniae, and M. gallisepticum, by using the freeze-substitution technique. Curr. Microbiol. 44:431-434.
57. Spuesens, E. B., et al. 2009. Sequence variations in RepMP2/3 and RepMP4 elements reveal intragenomic homologous DNA recombination events in Mycoplasma pneumoniae. Microbiology 155:2182-2196.
58. 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.
59. 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.
60. Su, C. J., V. V. Tryon, and J. B. Baseman. 1987. Cloning and sequence analysis of cytadhesin P1 gene from Mycoplasma pneumoniae. Infect. Immun. 55:3023-3029.
61. Tham, T. N., et al. 1994. Molecular characterization of the P1-like adhesin gene from Mycoplasma pirum. J. Bacteriol. 176:781-788.
62. Uenoyama, A., and M. Miyata. 2005. Gliding ghosts of Mycoplasma mobile. Proc. Natl. Acad. Sci. U. S. A. 102:12754-12758.
63. Uenoyama, A., and M. Miyata. 2005. Identification of a 123-kilodalton protein (Gli123) involved in machinery for gliding motility of Mycoplasma mobile. J. Bacteriol. 187:5578-5584.
64. Uenoyama, A., S. Seto, D. Nakane, and M. Miyata. 2009. Regions on Gli349 and Gli521 protein molecules directly involved in movements of Mycoplasma mobile gliding machinery suggested by inhibitory antibodies and mutants. J. Bacteriol. 191:1982-1985.
65. Wenzel, R., and R. Herrmann. 1988. Repetitive DNA sequences in Mycoplasma pneumoniae. Nucleic Acids Res. 16:8337-8350.