An intramolecular interaction involving the N terminus of a streptococcal adhesin affects its conformation and adhesive function

Journal of Biological Chemistry

Volumn 288, Issue 19, 2013, Pages 13762-13774

  Heim, Kyle P ^a   Crowley, Paula J ^a   Brady, L Jeannine ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CELL SURFACES; HIGH AFFINITY; INTRAMOLECULAR INTERACTIONS; MECHANISM OF ACTION; N TERMINUS; S. MUTANS; STREPTOCOCCUS MUTANS;

BIOCHEMISTRY; BIOLOGY;

CELL MEMBRANES;

ADHESIN; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ADHERENCE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMPLEX FORMATION; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR INTERACTION; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; STREPTOCOCCUS MUTANS; SURFACE PLASMON RESONANCE;

BACTERIAL ADHESION; CELL SURFACE PROTEIN; CIRCULAR DICHROISM (CD); ISOTHERMAL TITRATION CALORIMETRY; PROTEIN CONFORMATION; PROTEIN FOLDING; STREPTOCOCCUS; SURFACE PLASMON RESONANCE (SPR);

ADHESINS, BACTERIAL; AGGLUTININS; BACTERIAL ADHESION; CIRCULAR DICHROISM; IMMOBILIZED PROTEINS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE DELETION; STREPTOCOCCUS MUTANS; THERMODYNAMICS;

EID: 84877702684     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.459974     Document Type: Article

References (74)

1. Guzmán-Armstrong, S. (2005) Rampant caries. J. Sch. Nurs. 21, 272-278
2. Balakrishnan, M., Simmonds, R. S., and Tagg, J. R. (2000) Dental caries is a preventable infectious disease. Aust. Dent. J. 45, 235-245
3. Hamada, S., and Slade, H. D. (1980) Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol. Rev. 44, 331-384
4. Mosci, F., Perito, S., Bassa, S., Capuano, A., and Marconi, P. F. (1990) The role of Streptococcus mutans in human caries. Minerva Stomatol. 39, 413-429
5. Zucca, M., Cenna, S., Berzioli, S., Gariglio, M., and Fagnoni, V. (1990) Streptococcus mutans and dental caries. Microbiological aspects. G. Batteriol. Virol. Immunol. 83, 108-117
6. Nobbs, A. H., Lamont, R. J., and Jenkinson, H. F. (2009) Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 73, 407-450
7. Koga, T., Asakawa, H., Okahashi, N., and Hamada, S. (1986) Sucrose-dependent cell adherence and cariogenicity of serotype c Streptococcus mutans. J. Gen. Microbiol. 132, 2873-2883
8. Hajishengallis, G., Koga, T., and Russell, M. W. (1994) Affinity and specificity of the interactions between Streptococcus mutans antigen I/II and salivary components. J. Dent. Res. 73, 1493-1502
9. Russell, M. W., and Mansson-Rahemtulla, B. (1989) Interaction between surface protein antigens of Streptococcus mutans and human salivary components. Oral Microbiol. Immunol. 4, 106-111
10. Russell, M. W., Bergmeier, L. A., Zanders, E. D., and Lehner, T. (1980) Protein antigens of Streptococcus mutans. Purification and properties of a double antigen and its protease-resistant component. Infect. Immun. 28, 486-493
11. Russell, R. R. (1979) Wall-associated protein antigens of Streptococcus mutans. J. Gen. Microbiol. 114, 109-115
12. Hajishengallis, G., Nikolova, E., and Russell, M. W. (1992) Inhibition of Streptococcus mutans adherence to saliva-coated hydroxyapatite by human secretory immunoglobulin A (S-IgA) antibodies to cell surface protein antigen I/II. Reversal by IgA1 protease cleavage. Infect. Immun. 60, 5057-5064
13. Brady, L. J., Piacentini, D. A., Crowley, P. J., Oyston, P. C., and Bleiweis, A. S. (1992) Differentiation of salivary agglutinin-mediated adherence and aggregation of mutans streptococci by use of monoclonal antibodies against the major surface adhesin P1. Infect. Immun. 60, 1008-1017
14. Bleiweis, A. S., Oyston, P. C., and Brady, L. J. (1992) Molecular, immunological, and functional characterization of the major surface adhesin of Streptococcus mutans. Adv. Exp. Med. Biol. 327, 229-241
15. Crowley, P. J., Brady, L. J., Michalek, S. M., and Bleiweis, A. S. (1999) Virulence of a spaP mutant of Streptococcus mutans in a gnotobiotic rat model. Infect. Immun. 67, 1201-1206
16. Crowley, P. J., Brady, L. J., Piacentini, D. A., and Bleiweis, A. S. (1993) Identification of a salivary agglutinin binding domain within cell surface adhesin P1 of Streptococcus mutans. Infect. Immun. 61, 1547-1552
17. Oho, T., Yu, H., Yamashita, Y., and Koga, T. (1998) Binding of salivary glycoprotein-secretory immunoglobulin A complex to the surface protein antigen of Streptococcus mutans. Infect. Immun. 66, 115-121
18. Kishimoto, E., Hay, D. I., and Gibbons, R. J. (1989) A human salivary protein which promotes adhesion of Streptococcus mutans serotype c strains to hydroxyapatite. Infect. Immun. 57, 3702-3707
19. Ericson, T., and Rundegren, J. (1983) Characterization of a salivary agglutinin reacting with a serotype c strain of Streptococcus mutans. Eur. J. Biochem. 133, 255-261
20. Munro, G. H., Evans, P., Todryk, S., Buckett, P., Kelly, C. G., and Lehner, T. (1993) A protein fragment of streptococcal cell surface antigen I/II which prevents adhesion of Streptococcus mutans. Infect. Immun. 61, 4590-4598
21. van Dolleweerd, C. J., Kelly, C. G., Chargelegue, D., and Ma, J. K. (2004) Peptide mapping of a novel discontinuous epitope of the major surface adhesin from Streptococcus mutans. J. Biol. Chem. 279, 22198-22203
22. Bikker, F. J., Ligtenberg, A. J., Nazmi, K., Veerman, E. C., van't Hof, W., Bolscher, J. G., Poustka, A., Nieuw Amerongen, A. V., and Mollenhauer, J. (2002) Identification of the bacteria binding peptide domain on salivary agglutinin (gp-340/DMBT1), a member of the scavenger receptor cys-teine-rich superfamily. J. Biol. Chem. 277, 32109-32115
23. Bikker, F. J., Ligtenberg, A. J., End, C., Renner, M., Blaich, S., Lyer, S., Wittig, R., van't Hof, W., Veerman, E. C., Nazmi, K., de Blieck-Hogervorst, J. M., Kioschis, P., Nieuw Amerongen, A. V., Poustka, A., and Mollenhauer, J. (2004) Bacteria binding by DMBT1/SAG/gp-340 is confined to the VEVLXXXXWmotif in its scavenger receptor cysteine-rich domains. J. Biol. Chem. 279, 47699-47703
24. Madsen, J., Mollenhauer, J., and Holmskov, U. (2010) Review. Gp-340/DMBT1 in mucosal innate immunity. Innate Immun. 16, 160-167
25. Jakubovics, N. S., Strömberg, N., van Dolleweerd, C. J., Kelly, C. G., and Jenkinson, H. F. (2005) Differential binding specificities of oral streptococcal antigen I/II family adhesins for human or bacterial ligands. Mol. Microbiol. 55, 1591-1605
26. Koga, T., Okahashi, N., Takahashi, I., Kanamoto, T., Asakawa, H., and Iwaki, M. (1990) Surface hydrophobicity, adherence, and aggregation of cell surface protein antigen mutants of Streptococcus mutans serotype c. Infect. Immun. 58, 289-296
27. Bleiweis, A. S., Lee, S. F., Brady, L. J., Progulske-Fox, A., and Crowley, P. J. (1990) Cloning and inactivation of the gene responsible for a major surface antigen on Streptococcus mutans. Arch. Oral Biol. 35, 15S-23S
28. Lee, S. F., Progulske-Fox, A., Erdos, G. W., Piacentini, D. A., Ayakawa, G. Y., Crowley, P. J., and Bleiweis, A. S. (1989) Construction and characterization of isogenic mutants of Streptococcus mutans deficient in major surface protein antigen P1 (I/II). Infect. Immun. 57, 3306-3313
29. Bowen, W. H., Schilling, K., Giertsen, E., Pearson, S., Lee, S. F., Bleiweis, A., and Beeman, D. (1991) Role of a cell surface-associated protein in adherence and dental caries. Infect. Immun. 59, 4606-4609
30. Loimaranta, V., Jakubovics, N. S., Hytönen, J., Finne, J., Jenkinson, H. F., and Strömberg, N. (2005) Fluid-or surface-phase human salivary scavenger protein gp340 exposes different bacterial recognition properties. Infect. Immun. 73, 2245-2252
31. Brady, L. J., Piacentini, D. A., Crowley, P. J., and Bleiweis, A. S. (1991) Identification of monoclonal antibody-binding domains within antigen P1 of Streptococcus mutans and cross-reactivity with related surface antigens of oral streptococci. Infect. Immun. 59, 4425-4435
32. McArthur, W. P., Rhodin, N. R., Seifert, T. B., Oli, M. W., Robinette, R. A., Demuth, D. R., and Brady, L. J. (2007) Characterization of epitopes recognized by anti-Streptococcus mutans P1 monoclonal antibodies. FEMS Immunol. Med. Microbiol. 50, 342-353
33. Oli, M. W., McArthur, W. P., and Brady, L. J. (2006) A whole cell BIAcore assay to evaluate P1-mediated adherence of Streptococcus mutans to human salivary agglutinin and inhibition by specific antibodies. J. Microbiol. Methods 65, 503-511
34. Brady, L. J., Crowley, P. J., Ma, J. K., Kelly, C., Lee, S. F., Lehner, T., and Bleiweis, A. S. (1991) Restriction fragment length polymorphisms and sequence variation within the spaP gene of Streptococcus mutans serotype c isolates. Infect. Immun. 59, 1803-1810
35. Kelly, C., Evans, P., Ma, J. K., Bergmeier, L. A., Taylor, W., Brady, L. J., Lee, S. F., Bleiweis, A. S., and Lehner, T. (1990) Sequencing and characterization of the 185 kDa cell surface antigen of Streptococcus mutans. Arch. Oral Biol. 35, 33S-38S
36. Larson, M. R., Rajashankar, K. R., Crowley, P. J., Kelly, C., Mitchell, T. J., Brady, L. J., and Deivanayagam, C. (2011) Crystal structure of the C-terminus of Streptococcus mutans antigen I/II and characterization of salivary agglutinin adherence domains. J. Biol. Chem. 286, 21657-21666
37. Lee, S. F., and Boran, T. L. (2003) Roles of sortase in surface expression of the major protein adhesin P1, saliva-induced aggregation and adherence, and cariogenicity of Streptococcus mutans. Infect. Immun. 71, 676-681
38. Larson, M. R., Rajashankar, K. R., Patel, M. H., Robinette, R. A., Crowley, P. J., Michalek, S., Brady, L. J., and Deivanayagam, C. (2010) Elongated fibrillar structure of a streptococcal adhesin assembled by the high-affinity association of α-and PPII-helices. Proc. Natl. Acad. Sci. U.S.A. 107, 5983-5988
39. Nylander, A., Forsgren, N., and Persson, K. (2011) Structure of the C-terminal domain of the surface antigen SpaP from the caries pathogen Streptococcus mutans. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 23-26
40. Kang, H. J., Paterson, N. G., Gaspar, A. H., Ton-That, H., and Baker, E. N. (2009) The Corynebacterium diphtheriae shaft pilin SpaA is built of tandem Ig-like modules with stabilizing isopeptide and disulfide bonds. Proc. Natl. Acad. Sci. U.S.A. 106, 16967-16971
41. Kang, H. J., and Baker, E. N. (2009) Intramolecular isopeptide bonds give thermodynamic and proteolytic stability to the major pilin protein of Streptococcus pyogenes. J. Biol. Chem. 284, 20729-20737
42. Pointon, J. A., Smith, W. D., Saalbach, G., Crow, A., Kehoe, M. A., and Banfield, M. J. (2010) A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. J. Biol. Chem. 285, 33858-33866
43. Hu, X., Hu, H., Melvin, J. A., Clancy, K. W., McCafferty, D. G., and Yang, W. (2010) Autocatalytic intramolecular isopeptide bond formation in gram-positive bacterial pili. A QM/MM simulation. J. Am. Chem. Soc. 133, 478-485
44. Forsgren, N., Lamont, R. J., and Persson, K. (2010) Two intramolecular isopeptide bonds are identified in the crystal structure of the Streptococcus gordonii SspB C-terminal domain. J. Mol. Biol. 397, 740-751
45. Crowley, P. J., Seifert, T. B., Isoda, R., van Tilburg, M., Oli, M. W., Robinette, R. A., McArthur, W. P., Bleiweis, A. S., and Brady, L. J. (2008) Requirements for surface expression and function of adhesin P1 from Streptococcus mutans. Infect. Immun. 76, 2456-2468
46. Ayakawa, G. Y., Boushell, L. W., Crowley, P. J., Erdos, G. W., McArthur, W. P., and Bleiweis, A. S. (1987) Isolation and characterization of monoclonal antibodies specific for antigen P1, a major surface protein of mutans streptococci. Infect. Immun. 55, 2759-2767
47. Buckley, N. D., Lee, L. N., and LeBlanc, D. J. (1995) Use of a novel mobilizable vector to inactivate the scrA gene of Streptococcus sobrinus by allelic replacement. J. Bacteriol. 177, 5028-5034
48. Perry, D., and Kuramitsu, H. K. (1989) Genetic linkage among cloned genes of Streptococcus mutans. Infect. Immun. 57, 805-809
49. Oli, M. W., Otoo, H. N., Crowley, P. J., Heim, K. P., Nascimento, M. M., Ramsook, C. B., Lipke, P. N., and Brady, L. J. (2012) Functional amyloid formation by Streptococcus mutans. Microbiology 158, 2903-2916
50. Brady, L. J., Cvitkovitch, D. G., Geric, C. M., Addison, M. N., Joyce, J. C., Crowley, P. J., and Bleiweis, A. S. (1998) Deletion of the central prolinerich repeat domain results in altered antigenicity and lack of surface expression of the Streptococcus mutans P1 adhesin molecule. Infect. Immun. 66, 4274-4282
51. Yang, J. T., Wu, C. S., and Martinez, H. M. (1986) Calculation of protein conformation from circular dichroism. Methods Enzymol. 130, 208-269
52. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra. Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
53. Sreerama, N., and Woody, R. W. (2004) Computation and analysis of protein circular dichroism spectra. Methods Enzymol. 383, 318-351
54. Sreerama, N., Venyaminov, S. Y., and Woody, R. W. (1999) Estimation of the number of α-helical and β-strand segments in proteins using circular dichroism spectroscopy. Protein Sci. 8, 370-380
55. Compton, L. A., and Johnson, W. C., Jr. (1986) Analysis of protein circular dichroism spectra for secondary structure using a simple matrix multiplication. Anal. Biochem. 155, 155-167
56. Hennessey, J. P., Jr., and Johnson, W. C., Jr. (1981) Information content in the circular dichroism of proteins. Biochemistry 20, 1085-1094
57. Robinette, R. A., Oli, M. W., McArthur, W. P., and Brady, L. J. (2009) Beneficial immunomodulation by Streptococcus mutans anti-P1 monoclonal antibodies is Fc-independent and correlates with increased exposure of a relevant target epitope. J. Immunol. 183, 4628-4638
58. Rhodin, N. R., Cutalo, J. M., Tomer, K. B., McArthur, W. P., and Brady, L. J. (2004) Characterization of the Streptococcus mutans P1 epitope recognized by immunomodulatory monoclonal antibody 6-11A. Infect. Immun. 72, 4680-4688
59. Rhodin, N. R., Van Tilburg, M. L., Oli, M. W., McArthur, W. P., and Brady, L. J. (2004) Further characterization of immunomodulation by a monoclonal antibody against Streptococcus mutans antigen P1. Infect. Immun. 72, 13-21
60. Lopez, M. M., and Makhatadze, G. I. (2002) Isothermal titration calorimetry. Methods Mol. Biol. 173, 121-126
61. Velazquez-Campoy, A., Ohtaka, H., Nezami, A., Muzammil, S., and Freire, E. (2004) Isothermal titration calorimetry. Curr. Protoc. Cell Biol. Chapter 17, Unit 17.8
62. Lewis, E. A., and Murphy, K. P. (2005) Isothermal titration calorimetry. Methods Mol. Biol. 305, 1-16
63. Holdgate, G. (2009) Isothermal titration calorimetry and differential scanning calorimetry. Methods Mol. Biol. 572, 101-133
64. Seifert, T. B., Bleiweis, A. S., and Brady, L. J. (2004) Contribution of the alanine-rich region of Streptococcus mutans P1 to antigenicity, surface expression, and interaction with the proline-rich repeat domain. Infect. Immun. 72, 4699-4706
65. Livingstone, J. R., Spolar, R. S., and Record, M. T., Jr. (1991) Contribution to the thermodynamics of protein folding from the reduction in wateraccessible nonpolar surface area. Biochemistry 30, 4237-4244
66. Spolar, R. S., Livingstone, J. R., and Record, M. T., Jr. (1992) Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water. Biochemistry 31, 3947-3955
67. Spolar, R. S., and Record, M. T., Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science 263, 777-784
68. Murphy, K. P., Bhakuni, V., Xie, D., and Freire, E. (1992) Molecular basis of cooperativity in protein folding. III. Structural identification of cooperative folding units and folding intermediates. J. Mol. Biol. 227, 293-306
69. Murphy, K. P., and Freire, E. (1992) Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv. Protein Chem. 43, 313-361
70. Gómez, J., and Freire, E. (1995) Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin. J. Mol. Biol. 252, 337-350
71. Gómez, J., Hilser, V. J., Xie, D., and Freire, E. (1995) The heat capacity of proteins. Proteins 22, 404-412
72. Ma, B., Tsai, C. J., and Nussinov, R. (2000) Binding and folding. In search of intramolecular chaperone-like building block fragments. Protein Eng. 13, 617-627
73. Tsai, C. D., Ma, B., Kumar, S., Wolfson, H., and Nussinov, R. (2001) Protein folding. Binding of conformationally fluctuating building blocks via population selection. Crit. Rev. Biochem. Mol. Biol. 36, 399-433
74. Leito, J. T., Ligtenberg, A. J., Nazmi, K., de Blieck-Hogervorst, J. M., Veerman, E. C., and Nieuw Amerongen, A. V. (2008) A common binding motif for various bacteria of the bacteria-binding peptide SRCRP2 of DMBT1/gp-340/salivary agglutinin. Biol. Chem. 389, 1193-1200