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. 1984 May 1;159(5):1351–1370. doi: 10.1084/jem.159.5.1351

Gonococcal pili. Primary structure and receptor binding domain

PMCID: PMC2187295  PMID: 6143785

Abstract

The complete amino acid sequence of pilin from gonococcal strain MS11 and the sequence of constant and variable regions from strain R10 pilin have been determined in order to elucidate the structural basis for adherence function, antigenic diversity, and polymeric structure. The MS11 pilin sequence consists of 159 amino acids in a single polypeptide chain with two cysteines in disulfide linkage and serine-bonded phosphate residues. TC-2 (31-111), a soluble monomeric pilus peptide prepared by arginine-specific digestion, bound human endocervical, but not buccal or HeLa cells and therefore is postulated to encompass the receptor binding domain. Variable regions of CNBr-3 appear to confer antigenic diversity and comprise segments in which changes in the position of charged residues occur in hydrophilic, beta-turns. Residues 2-21 and 202-221 of gonococcal pilins and lower eucaryotic actins, respectively, exhibit 50% homology. When these residues are arranged at intervals of 100 degrees of arc on "helical wheels," the identical amino acids comprise a hydrophobic face on one side of the helix. This observation, the hydrophobic character of this region and the tendency for TC-1 (residues 1-30) to aggregate in water, suggest that this stretch interacts with other subunits to stabilize polymeric structure.

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Selected References

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  1. Adelstein R. S., Kuehl W. M. Structural studies on rabbit skeletal actin. I. Isolation and characterization of the peptides produced by cyanogen bromide cleavage. Biochemistry. 1970 Mar 17;9(6):1355–1364. doi: 10.1021/bi00808a009. [DOI] [PubMed] [Google Scholar]
  2. Brinton C. C., Jr The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. Trans N Y Acad Sci. 1965 Jun;27(8):1003–1054. doi: 10.1111/j.2164-0947.1965.tb02342.x. [DOI] [PubMed] [Google Scholar]
  3. Buchanan T. M. Antigenic heterogeneity of gonococcal pili. J Exp Med. 1975 Jun 1;141(6):1470–1475. doi: 10.1084/jem.141.6.1470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chipman D. M., Sharon N. Mechanism of lysozyme action. Science. 1969 Aug 1;165(3892):454–465. doi: 10.1126/science.165.3892.454. [DOI] [PubMed] [Google Scholar]
  5. Chou P. Y., Fasman G. D. Conformational parameters for amino acids in helical, beta-sheet, and random coil regions calculated from proteins. Biochemistry. 1974 Jan 15;13(2):211–222. doi: 10.1021/bi00699a001. [DOI] [PubMed] [Google Scholar]
  6. Dayhoff M. O., Barker W. C., Hunt L. T. Establishing homologies in protein sequences. Methods Enzymol. 1983;91:524–545. doi: 10.1016/s0076-6879(83)91049-2. [DOI] [PubMed] [Google Scholar]
  7. Dilworth J. A., Hendley J. O., Mandell G. L. Attachment and ingestion of gonococci human neutrophils. Infect Immun. 1975 Mar;11(3):512–516. doi: 10.1128/iai.11.3.512-516.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. ELLMAN G. L. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959 May;82(1):70–77. doi: 10.1016/0003-9861(59)90090-6. [DOI] [PubMed] [Google Scholar]
  9. GREAVES R. I. Preservation of living cells by freeze-drying. Ann N Y Acad Sci. 1960 Apr 13;85:723–728. doi: 10.1111/j.1749-6632.1960.tb49992.x. [DOI] [PubMed] [Google Scholar]
  10. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GROSS E., WITKOP B. Nonenzymatic cleavage of peptide bonds: the methionine residues in bovine pancreatic ribonuclease. J Biol Chem. 1962 Jun;237:1856–1860. [PubMed] [Google Scholar]
  12. Grimes W. J., Greegor S. Carbohydrate compositions of normal, spontaneously transformed, and virally transformed cells derived from BALB/c mice. Cancer Res. 1976 Nov;36(11 Pt 1):3905–3910. [PubMed] [Google Scholar]
  13. Gubish E. R., Jr, Chen K. C., Buchanan T. M. Attachment of gonococcal pili to lectin-resistant clones of Chinese hamster ovary cells. Infect Immun. 1982 Jul;37(1):189–194. doi: 10.1128/iai.37.1.189-194.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hayashi R., Moore S., Stein W. H. Carboxypeptidase from yeast. Large scale preparation and the application to COOH-terminal analysis of peptides and proteins. J Biol Chem. 1973 Apr 10;248(7):2296–2302. [PubMed] [Google Scholar]
  15. Hermodson M. A., Chen K. C., Buchanan T. M. Neisseria pili proteins: amino-terminal amino acid sequences and identification of an unusual amino acid. Biochemistry. 1978 Feb 7;17(3):442–445. doi: 10.1021/bi00596a010. [DOI] [PubMed] [Google Scholar]
  16. Hopp T. P., Woods K. R. Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3824–3828. doi: 10.1073/pnas.78.6.3824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. James J. F., Swanson J. Studies on gonococcus infection. XIII. Occurrence of color/opacity colonial variants in clinical cultures. Infect Immun. 1978 Jan;19(1):332–340. doi: 10.1128/iai.19.1.332-340.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Lambden P. R., Robertson J. N., Watt P. J. The preparation and properties of alpha and beta pili from variants of Neisseria gonorrhoeae P9. J Gen Microbiol. 1981 May;124(1):109–117. doi: 10.1099/00221287-124-1-109. [DOI] [PubMed] [Google Scholar]
  20. Levitt M. A simplified representation of protein conformations for rapid simulation of protein folding. J Mol Biol. 1976 Jun 14;104(1):59–107. doi: 10.1016/0022-2836(76)90004-8. [DOI] [PubMed] [Google Scholar]
  21. Mahoney W. C., Hermodson M. A. High-yield cleavage of tryptophanyl peptide bonds by o-iodosobenzoic acid. Biochemistry. 1979 Aug 21;18(17):3810–3814. doi: 10.1021/bi00584a026. [DOI] [PubMed] [Google Scholar]
  22. Meek J. L. Prediction of peptide retention times in high-pressure liquid chromatography on the basis of amino acid composition. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1632–1636. doi: 10.1073/pnas.77.3.1632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Newcomer M. E., Miller D. M., 3rd, Quiocho F. A. Location of the sugar-binding site of L-arabinose-binding protein. Sugar derivative syntheses, sugar binding specificity, and difference Fourier analyses. J Biol Chem. 1979 Aug 25;254(16):7529–7533. [PubMed] [Google Scholar]
  24. Novotny P., Turner W. H. Immunological heterogeneity of pili of Neisseria gonorrhoeae. J Gen Microbiol. 1975 Jul;89(1):87–92. doi: 10.1099/00221287-89-1-87. [DOI] [PubMed] [Google Scholar]
  25. Oliveira E. B., Gotschlich C., Liu T. Y. Primary structure of human C-reactive protein. J Biol Chem. 1979 Jan 25;254(2):489–502. [PubMed] [Google Scholar]
  26. Pearce W. A., Buchanan T. M. Attachment role of gonococcal pili. Optimum conditions and quantitation of adherence of isolated pili to human cells in vitro. J Clin Invest. 1978 Apr;61(4):931–943. doi: 10.1172/JCI109018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Phillips G. N., Jr, Lattman E. E., Cummins P., Lee K. Y., Cohen C. Crystal structure and molecular interactions of tropomyosin. Nature. 1979 Mar 29;278(5703):413–417. doi: 10.1038/278413a0. [DOI] [PubMed] [Google Scholar]
  28. Salit I. E., Blake M., Gotschlich E. C. Intra-strain heterogeneity of gonococcal pili is related to opacity colony variance. J Exp Med. 1980 Mar 1;151(3):716–725. doi: 10.1084/jem.151.3.716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sastry P. A., Pearlstone J. R., Smillie L. B., Paranchych W. Amino acid sequence of pilin isolated from pseudomonas aeruginosa PAK. FEBS Lett. 1983 Jan 24;151(2):253–256. doi: 10.1016/0014-5793(83)80080-5. [DOI] [PubMed] [Google Scholar]
  30. Schiffer M., Edmundson A. B. Use of helical wheels to represent the structures of proteins and to identify segments with helical potential. Biophys J. 1967 Mar;7(2):121–135. doi: 10.1016/S0006-3495(67)86579-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schoolnik G. K., Tai J. Y., Gotschlich E. C. A pilus peptide vaccine for the prevention of gonorrhea. Prog Allergy. 1983;33:314–331. [PubMed] [Google Scholar]
  32. Simpson R. J., Neuberger M. R., Liu T. Y. Complete amino acid analysis of proteins from a single hydrolysate. J Biol Chem. 1976 Apr 10;251(7):1936–1940. [PubMed] [Google Scholar]
  33. Swanson J., Kraus S. J., Gotschlich E. C. Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J Exp Med. 1971 Oct 1;134(4):886–906. doi: 10.1084/jem.134.4.886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Swanson J. Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J Exp Med. 1973 Mar 1;137(3):571–589. doi: 10.1084/jem.137.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Swanson J. Studies on gonococcus infection. XII. Colony color and opacity varienats of gonococci. Infect Immun. 1978 Jan;19(1):320–331. doi: 10.1128/iai.19.1.320-331.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vandekerckhove J., Weber K. Vegetative Dictyostelium cells containing 17 actin genes express a single major actin. Nature. 1980 Apr 3;284(5755):475–477. doi: 10.1038/284475a0. [DOI] [PubMed] [Google Scholar]
  37. Virji M., Heckels J. E., Watt P. J. Monoclonal antibodies to gonococcal pili: studies on antigenic determinants on pili from variants of strain P9. J Gen Microbiol. 1983 Jun;129(6):1965–1973. doi: 10.1099/00221287-129-6-1965. [DOI] [PubMed] [Google Scholar]
  38. Ward M. E., Watt P. J., Robertson J. N. The human fallopian tube: a laboratory model for gonococcal infection. J Infect Dis. 1974 Jun;129(6):650–659. doi: 10.1093/infdis/129.6.650. [DOI] [PubMed] [Google Scholar]
  39. Watts T. H., Kay C. M., Paranchych W. Dissociation and characterization of pilin isolated from Pseudomonas aeruginosa strains PAK and PAO. Can J Biochem. 1982 Sep;60(9):867–872. doi: 10.1139/o82-110. [DOI] [PubMed] [Google Scholar]
  40. Watts T. H., Worobec E. A., Paranchych W. Identification of pilin pools in the membranes of Pseudomonas aeruginosa. J Bacteriol. 1982 Nov;152(2):687–691. doi: 10.1128/jb.152.2.687-691.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]

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