PspA protects Streptococcus pneumoniae from killing by apolactoferrin, and antibody to PspA enhances killing of pneumococci by apolactoferrin

Infection and Immunity

Volumn 72, Issue 9, 2004, Pages 5031-5040

  Shaper, Mirza ^a   Hollingshead, Susan K ^a   Benjamin Jr , William H ^b   Briles, David E ^a,c  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTIBODY; APOLACTOFERRIN; BINDING PROTEIN; CHOLINE; IRON; LACTOFERRICIN; LACTOFERRIN; MEMBRANE PROTEIN; MUTANT PROTEIN; PNEUMOCOCCAL SURFACE PROTEIN A; PROTEIN PCPA; PROTEIN PSPC; PSPA ANTIBODY; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; GENE MUTATION; IMMUNITY; IMMUNOMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; STREPTOCOCCUS PNEUMONIAE;

AMINO ACID SEQUENCE; ANTIBODIES, BACTERIAL; APOPROTEINS; BACTERIAL PROTEINS; CULTURE MEDIA; HUMANS; LACTOFERRIN; MOLECULAR SEQUENCE DATA; STREPTOCOCCUS PNEUMONIAE;

EID: 4544281498     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.9.5031-5040.2004     Document Type: Article

References (67)

1. Achen, M. G., B. E. Davidson, and A. J. Hillier. 1986. Construction of plasmid vectors for the detection of streptococcal promoters. Gene 45:45-49.
2. Akin, D. T., M. Q. Lu, S. J. Lu, S. Kendall, J. Rundegren, and R. R. Arnold. 1994. Bactericidal activity of different forms of lactoferrin. Adv. Exp. Med. Biol. 357:61-70.
3. Aniansson, G., B. Alm, B. Andersson, P. Larsson, O. Nylen, H. Peterson, P. Rigner, M. Svanborg, and C. Svanborg. 1992. Nasopharyngeal colonization during the first year of life. J. Infect. Dis. 165(Suppl. 1):S38-S42.
4. Arnold, R. R., M. Brewer, and J. J. Gauthier. 1980. Bactericidal activity of human lactoferrin: sensitivity of a variety of microorganisms. Infect. Immun. 28:893-898.
5. Arnold, R. R., J. E. Russell, W. J. Champion, M. Brewer, and J. J. Gauthier. 1982. Bactericidal activity of human lactoferrin: differentiation from the stasis of iron deprivation. Infect. Immun. 35:792-799.
6. Arnold, R. R., J. E. Russell, W. J. Champion, and J. J. Gauthier. 1981. Bactericidal activity of human lactoferrin: influence of physical conditions and metabolic state of the target microorganism. Infect. Immun. 32:655-660.
7. Balachandran, P., A. Brooks-Walter, A. Virolainen-Julkunen, S. K. Hollingshead, and D. E. Briles. 2002. The role of pneumococcal surface protein C (PspC) in nasopharyngeal carriage and pneumonia and its ability to elicit protection against carriage of Streptococcus pneumoniae. Infect. Immun. 70: 2526-2534.
8. Berry, A. M., and J. C. Paton. 2000. Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect. Immun. 68: 133-140.
9. Black, S. B., H. R. Shinefield, S. Ling, J. Hansen, B. Fireman, D. Spring, J. Noyes, E. Lewis, P. Ray, J. Lee, and J. Hackell. 2002. Effectiveness of heptavalent pneumococcal conjugate vaccine in children younger than five years of age for prevention of pneumonia. Pediatr. Infect. Dis. J. 21:810-815.
10. Briles, D. E., E. Ades, J. C. Paton, J. S. Sampson, G. M. Carlone, R. C. Huebner, A. Virolainen, E. Swiatlo, and S. K. Hollingshead. 2000. Intranasal immunization of mice with a mixture of the pneumococcal proteins PsaA and PspA is highly protective against nasopharyngeal carriage of Streptococcus pneumoniae. Infect. Immun. 68:796-800.
11. Briles, D. E., M. J. Crain, B. M. Gray, C. Forman, and J. Yother. 1992. A strong association between capsular type and mouse virulence among human isolates of Streptococcus pneumoniae. Infect. Immun. 60:111-116.
12. Briles, D. E., S. K. Hollingshead, J. King, A. Swift, P. A. Braun, M. K. Park, L. M. Ferguson, M. H. Nahm, and G. S. Nabors. 2000. Immunization of humans with rPspA elicits antibodies, which passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J. Infect. Dis. 182:1694-1701.
13. Briles, D. E., S. K. Hollingshead, J. C. Paton, E. W. Ades, L. Novak, F. W. van Ginkel, and W. H. J. Benjamin. 2003. Immunizations with pneumococcal surface protein A and pneumolysin are protective against pneumonia in a murine model of pulmonary infection with Streptococcus pneumoniae. J. Infect. Dis. 188:339-348.
14. Briles, D. E., S. K. Hollingshead, E. Swiatlo, A. Brooks-Walter, A. Szalai, A. Virolainen, L. S. McDaniel, K. A. Benton, P. White, K. Prellner, A. Hermansson, P. C. Aerts, H. Van Dijk, and M. J. Crain. 1997. PspA and PspC: their potential for use as pneumococcal vaccines. Microb. Drug Resist. 3: 401-408.
15. Briles, D. E., J. C. Paton, and S. K. Hollingshead. 2004. Pneumococcal common proteins and other vaccine strategies, p. 459-469. In M. M. Levine, J. B. Kaper, R. Rappuoli, M. Liu, and M. Good (ed.), New generation vaccines, 3rd ed. Marcel Dekker, Inc., New York, N.Y.
16. Briles, D. E., J. Yother, and L. S. McDaniel. 1988. Role of pneumococcal surface protein A in the virulence of Streptococcus pneumoniae. Rev. Infect. Dis. 10:8372-8374.
17. Brock, J. H. 2002. The physiology of lactoferrin. Biochem. Cell. Biol. 80:1-6.
18. Brooks-Walter, A., D. E. Briles, and S. K. Hollingshead. 1999. The pspC gene of Streptococcus pneumoniae encodes a polymorphic protein PspC, which elicits cross-reactive antibodies to PspA and provides immunity to pneumococcal bacteremia. Infect. Immun. 67:6533-6542.
19. Brown, E. J., S. W. Hosea, and M. M. Frank. 1983. The role of antibody and complement in the reticuloendothelial clearance of pneumococci from the bloodstream. Rev. Infect. Dis. 5(Suppl. 4):S797-S805.
20. Butler, J. C., J. Hofmann, M. S. Cetron, J. A. Elliott, R. R. Facklam, and R. F. Breiman. 1996. The continued emergence of drug-resistant Streptococcus pneumoniae in the United States: an update from the Centers for Disease Control and Prevention's Pneumococcal Sentinel Surveillance System. J. Infect. Dis. 174:986-993.
21. Butler, J. C., E. D. Shapiro, and G. M. Carlone. 1999. Pneumococcal vaccines: history, current status, and future directions. Am. J. Med. 107(1A): 69S-76S.
22. Centers for Disease Control and Prevention. 1996. Defining the public health impact of drug-resistant Streptococcus pneumoniae: report of a working group. Morb. Mortal. Wkly. Rep. 45:1-20.
23. Chapple, D. S., C. L. Joannou, D. J. Mason, J. K. Shergill, E. W. Odell, V. Gant, and R. W. Evans. 1998. A helical region on human lactoferrin. Its role in antibacterial pathogenesis. Adv. Exp. Med. Biol. 443:215-220.
24. Chapple, D. S., D. J. Mason, C. L. Joannou, E. W. Odell, V. Gant, and R. W. Evans. 1998. Structure-function relationship of antibacterial synthetic peptides homologous to a helical surface region on human lactoferrin against Escherichia coli serotype O111. Infect. Immun. 66:2434-2440.
25. Coral, M. C. V., N. Fonseca, E. Castaneda, J. L. Di Fabio, S. K. Hollingshead, and D. E. Briles. 2001. Families of pneumococcal surface protein A (PspA) of Streptococcus pneumoniae invasive isolates recovered from Colombian children. Emerg. Infect. Dis. 7:832-336.
26. Crain, M. J., W. D. Waltman, J. S. Turner, J. Yother, D. E. Talkington, L. M. McDaniel, B. M. Gray, and D. E. Briles. 1990. Pneumococcal surface protein A (PspA) is serologically highly variable and is expressed by all clinically important capsular serotypes of Streptococcus pneumoniae. Infect. Immun. 58:3293-3299.
27. Dagan, R., N. Givon-Lavi, O. Zamir, M. Sikuler-Cohen, L. Guy, J. Janco, P. Yagupsky, and D. Fraser. 2002. Reduction of nasopharyngeal carriage of Streptococcus pneumoniae after administration of a 9-valent pneumococcal conjugate vaccine to toddlers attending day care enters. J. Infect. Dis. 185: 927-936.
28. Dagan, R., R. Melamed, M. Muallem, L. Piglansky, D. Greenburg, O. Abramson, P. M. Mendalman, N. Bohidar, and P. Yagupsky. 1996. Reduction of nasopharyngeal carriage of pneumococci during the second year of life by a heptavalent conjugate pneumococcal vaccine. J. Infect. Dis. 174:1271-1278.
29. de Lillo, A., L. M. Quiros, and J. F. Fierro. 1997. Relationship between antibacterial activity and cell surface binding of lactoferrin in species of genus Micrococcus. FEMS Microbiol. Lett. 150:89-94.
30. Desai, P. J., E. Garges, and C. A. Genco. 2000. Pathogenic neisseriae can use hemoglobin, transferrin, and lactoferrin independently of the tonB locus. J. Bacteriol. 182:5586-5591.
31. Farnaud, S., and R. W. Evans. 2003. Lactoferrin - a multifunctional protein with antimicrobial properties. Mol. Immunol. 40:395-405.
32. Gray, B. M., G. M. Converse III, and H. C. Dillon. 1980. Epidemiologic studies of Streptococcus pneumoniae in infants: acquisition, carriage, and infection during the first 24 months of life. J. Infect. Dis. 142:923-933.
33. Hakansson, A., H. Roche, S. Mirza, L. S. McDaniel, A. Brooks-Walter, and D. E. Briles. 2001. Characterization of the binding of human lactoferrin to pneumococcal surface protein A (PspA). Infect. Immun. 69:3372-3381.
34. Hammerschmidt, S., G. Bethe, P. Remanen, and G. S. Chhatwal. 1999. Identification of pneumococcal surface protein A as a lactoferrin-binding protein of Streptococcus pneumoniae. Infect. Immun. 67:1683-1687.
35. Haug, B. E., M. L. Skar, and J. S. Svendsen. 2001. Bulky aromatic amino acids increase the antibacterial activity of 15-residue-bovine lactoferricin derivatives. J. Peptide Sci. 7:425-432.
36. Haug, B. E., and J. S. Svendsen. 2001. The role of tryptophan in the antibacterial activity of a 15-residue bovine lactoferricin peptide. J. Peptide Sci. 7:190-196.
37. Haverstein, L. S., G. Coomaraswamy, and D. A. Morrison. 1995. An unmodified heptadecapetide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 92:11140-11144.
38. Hollingshead, S. K., R. S. Becker, and D. E. Briles. 2000. Diversity of PspA: mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect. Immun. 68:5889-5900.
39. Jedrzejas, M. J., S. K. Hollingshead, J. Lebowitz, L. Chantalat, D. E. Briles, and E. Lamani. 2000. Production and characterization of the functional fragment of pneumococcal surface protein A. Arch. Biochem. Biophys. 373: 116-125.
40. Leiten, E. C., and M. D. Willcox. 1998. Synergic antistaphylococcal properties of lactoferrin and lysozyme. J. Med. Microbiol. 47:837-542.
41. Marston, B. J., J. F. Ploutfe, T. M. File, Jr., B. A. Hackman, S. J. Salstrom, H. B. Lipman, M. S. Kolczak, R. F. Breiman, et al. 1997. Incidence of community-acquired pneumonia requiring hospitalization. Results of a population-based active surveillance study in Ohio. Arch. Intern. Med. 157: 1709-1718.
42. McCool, T. L., T. R. Gate, G. Moy, and J. N. Weiser. 2002. The immune response to pneumococcal proteins during experimental human carriage. J. Exp. Med. 195:359-365.
43. McDaniel, L. S., J. S. Sheffield, P. Delucchi, and D. E. Briles. 1991. PspA, a surface protein of Streptococcus pneumoniae, is capable of eliciting protection against pneumococci of more than one capsular type. Infect. Immun. 59: 222-228.
44. McDaniel, L. S., J. Yother, M. Vijayakumar, L. McGarry, W. R. Guild, and D. E. Briles. 1987. Use of insertional inactivation to facilitate studies of biological properties of pneumococcal surface protein A (PspA). J. Exp. Med. 165:381-394.
45. Nabors, G. S., P. A. Braun, D. J. Hermann, M. L. Heise, D. J. Pyle, S. Gravenstein, M. Schilling, L. M. Ferguson, S. K. Hollingshead, D. E. Briles, and R. S. Becker. 2000. Immunization of healthy adults with a single recombinant pneumococcal surface protein A (PspA) variant stimulates broadly cross-reactive antibodies. Vaccine 18:1743-1754.
46. Neeleman, C., P. M. Sibyl, S. P. Geelen, P. C. Aerts, M. R. Daha, T. E. Mollnes, J. J. Roord, G. Posthuma, H. van Dyk, and A. Fleer. 1999. Resistance to both complement activation and phagocytosis in type 3 pneumococci is mediated by binding of complement regulatory protein factor H. Infect. Immun. 67:4517-4524.
47. O'Brien, K. L., and H. Nohynek. 2003. Report from a W.H.O. working group: standard method for detecting upper respiratory carriage of Streptococcus pneumoniae. Pediatr. Infect. Dis. J. 22:E1-E11.
48. Otto, B. R., A. M. Verweij-van Vught, and D. M. MacLaren. 1992. Transferrins and heme compounds as iron sources for pathogenic bacteria. Crit. Rev. Microbiol. 18:217-233.
49. Rello, J., R. Rodriguez, P. Jubert, and B. Alverez. 1996. Severe community-acquired pneumonia in the elderly: epidemiology and prognosis. Clin. Infect. Dis. 23:723-728.
50. Ren, B., A. J. Szalai, S. K. Hollingshead, and D. E. Briles. 2004. Effects of PspA and antibodies to PspA on activation and deposition of complement on the pneumococcal surface. Infect Immun. 72:114-122.
51. Ren, B., A. J. Szalai, O. Thomas, S. K. Hollingshead, and D. E. Briles. 2003. Both family 1 and family 2 PspAs can inhibit complement deposition and confer virulence to a capsular 3 serotype Streptococcus pneumoniae. Infect. Immun. 71:75-55.
52. Sanchez-Beato, A. R., R. Lopez, and J. L. Garcia. 1998. Molecular characterization of PcpA: a novel choline-binding protein of Streptococcus pneumoniae. FEMS Microbiol. Lett. 164:207-214.
53. Shinefield, H. R. 2000. Safety and efficacy of the heptavalent pneumococcal conjugate vaccine. Infect. Dis. Children June:12-15.
54. Tai, S. S., C. J. Lee, and R. E. Winter. 1993. Hemin utilization is related to virulence of Streptococcus pneumoniae. Infect. Immun. 61:5401-5405.
55. Tomita, M., W. Bellamy, M. Takase, K. Yamauchi, H. Wakabayashi, and K. Kawase. 1991. Potent antibacterial peptides generated by pepsin digestion of bovine lactoferrin. J. Dairy Sci. 74:4137-4142.
56. Tu, A.-H. T., R. L. Fulgham, M. A. McCory, D. E. Briles, and A. J. Szalai. 1999. Pneumococcal surface protein A (PspA) inhibits complement activation by Streptococcus pneumoniae. Infect. Immun. 67:4720-4724.
57. Vogel, H. J., D. J. Schibli, W. Jing, E. M. Lohmeier-Vogel, R. F. Epand, and R. M. Epand. 2002. Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem. Cell. Biol. 80:49-63.
58. Wang, X., S. Hirmo, R. Willen, and T. Wadstrom. 2001. Inhibition of Helicobacter pylori infection by bovine milk glycoconjugates in a BALB/cA mouse model. J. Med. Microbiol. 50:430-435.
59. Ward, P. P., S. Uribe-Luna, and O. M. Conneely. 2002. Lactoferrin and host defense. Biochem. Cell. Biol. 80:95-102.
60. World Health Organization. 1999. Pneumococcal vaccines. W.H.O. position paper. Wkly. Epidemiol. Rec. 74:177-183.
61. Wu, H.-Y., M. Nahm, Y. Guo, M. Russell, and D. E. Briles. 1997. Intranasal immunization of mice with PspA (pneumococcal surface protein A) can prevent intranasal carriage and infection with Streptococcus pneumoniae. J. Infect. Dis. 175:839-846.
62. Yamamoto, M., L. S. McDaniel, K. Kawabata, D. E. Briles, R. J. Jackson, J. R. McGhee, and H. Kiyono. 1997. Oral immunization with PspA elicits protective humoral immunity against Streptococcus pneumoniae infection. Infect. Immun. 65:640-644.
63. Yamauchi, K., M. Tomita, T. J. Giehl, and R. T. Ellison III. 1993. Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect. Immun 61:719-728.
64. Yother, J., and D. E. Briles. 1992. Structural properties and evolutionary relationships of PspA, a surface protein of Streptococcus pneumoniae, as revealed by sequence analysis. J. Bacteriol. 174:601-609.
65. Yother, J., G. L. Handsome, and D. E. Briles. 1992. Truncated forms of PspA that are secreted from Streptococcus pneumoniae and their use in functional studies and cloning of the pspA gene. J. Bacteriol. 174:610-618.
66. Yother, J., L. S. McDaniel, M. J. Grain, D. F. Talkington, and D. E. Briles. 1991. Pneumococcal surface protein A: structural analysis and biological significance, p. 88-91. In G. M. Dunny, P. P. Cleary, and L. L. McKay (ed.), Genetics and molecular biology of streptococci, lactococci, and enterococci. American Society for Microbiology, Washington, D.C.
67. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 414:389-395.