The two variants of the Streptococcus pneumoniae pilus 1 RrgA adhesin retain the same function and elicit cross-protection in vivo

Infection and Immunity

Volumn 78, Issue 12, 2010, Pages 5033-5042

  Moschioni, Monica ^a   Emolo, Carla ^a   Biagini, Massimiliano ^a   Maccari, Silvia ^a   Pansegrau, Werner ^a   Donati, Claudio ^a   Hilleringmann, Markus ^a   Ferlenghi, Ilaria ^a   Ruggiero, Paolo ^a   Sinisi, Antonia ^a   Pizza, Mariagrazia ^a   Norais, Nathalie ^a   Barocchi, Michèle A ^a   Masignani, Vega ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; BACTERIUM PILUS 1 PROTEIN; EPITOPE; FIBRONECTIN; GLYCOSAMINOGLYCAN; LAMININ; RECOMBINANT PROTEIN; RECOMBINANT PROTEIN RRGA; STREPTOCOCCUS VACCINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; BACTERIUM ADHERENCE; BACTERIUM PILUS; CELL ADHESION; CONTROLLED STUDY; CROSS PROTECTION; CROSS REACTION; EPITHELIUM CELL; EPITOPE MAPPING; EXTRACELLULAR MATRIX; FEMALE; GENETIC VARIABILITY; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN VARIANT; RABBIT; SITE DIRECTED MUTAGENESIS; STREPTOCOCCUS PNEUMONIAE;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CROSS PROTECTION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FIMBRIAE, BACTERIAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNIZATION, PASSIVE; MICE; MICE, INBRED BALB C; PNEUMOCOCCAL INFECTIONS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STREPTOCOCCUS PNEUMONIAE;

EID: 78649922984     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00601-10     Document Type: Article

References (55)

1. Abbot, E. L., W. D. Smith, G. P. Siou, C. Chiriboga, R. J. Smith, J. A. Wilson, B. H. Hirst, and M. A. Kehoe. 2007. Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiol. 9:1822-1833.
2. Aguiar, S. I., I. Serrano, F. R. Pinto, J. Melo-Cristino, and M. Ramirez. 2008. The presence of the pilus locus is a clonal property among pneumococcal invasive isolates. BMC Microbiol. 8:41.
3. Anderton, J. M., G. Rajam, S. Romero-Steiner, S. Summer, A. P. Kowalczyk, G. M. Carlone, J. S. Sampson, and E. W. Ades. 2007. E-cadherin is a receptor for the common protein pneumococcal surface adhesin A (PsaA) of Streptococcus pneumoniae. Microb. Pathog. 42:225-236.
4. Auranen, K., J. Mehtala, A. Tanskanen, and S. Kaltoft. 2010. Between-strain competition in acquisition and clearance of pneumococcal carriage: epidemiologic evidence from a longitudinal study of day-care children. Am. J. Epidemiol. 171:169-176.
5. Bagnoli, F., M. Moschioni, C. Donati, V. Dimitrovska, I. Ferlenghi, C. Facciotti, A. Muzzi, F. Giusti, C. Emolo, A. Sinisi, M. Hilleringmann, W. Pansegrau, S. Censini, R. Rappuoli, A. Covacci, V. Masignani, and M. A. Barocchi. 2008. A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J. Bacteriol. 190:5480-5492.
6. Barocchi, M. A., J. Ries, X. Zogaj, C. Hemsley, B. Albiger, A. Kanth, S. Dahlberg, J. Fernebro, M. Moschioni, V. Masignani, K. Hultenby, A. R. Taddei, K. Beiter, F. Wartha, A. von Euler, A. Covacci, D. W. Holden, S. Normark, R. Rappuoli, and B. Henriques-Normark. 2006. A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl. Acad. Sci. U. S. A. 103:2857-2862.
7. Basset, A., K. Trzcinski, C. Hermos, K. L. O'Brien, R. Reid, M. Santosham, A. J. McAdam, M. Lipsitch, and R. Malley. 2007. Association of the pneumococcal pilus with certain capsular serotypes but not with increased virulence. J. Clin. Microbiol. 45:1684-1689.
8. Böhm, G., R. Muhr, and R. Jaenicke. 1992. Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng. 5:191-195.
9. Budzik, J. M., C. B. Poor, K. F. Faull, J. P. Whitelegge, C. He, and O. Schneewind. 2009. Intramolecular amide bonds stabilize pili on the surface of bacilli. Proc. Natl. Acad. Sci. U. S. A. 106:19992-19997.
10. Dagan, R. 2004. The potential effect of widespread use of pneumococcal conjugate vaccines on the practice of pediatric otolaryngology: the case of acute otitis media. Curr. Opin. Otolaryngol. Head Neck Surg. 12:488-494.
11. Dagan, R. 2009. Serotype replacement in perspective. Vaccine 27(Suppl. 3):C22-C24.
12. 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 centers. J. Infect. Dis. 185:927-936.
13. Dramsi, S., E. Caliot, I. Bonne, S. Guadagnini, M. C. Prevost, M. Kojadinovic, L. Lalioui, C. Poyart, and P. Trieu-Cuot. 2006. Assembly and role of pili in group B streptococci. Mol. Microbiol. 60:1401-1413.
14. ElMortaji, L., R. Terrasse, A. Dessen, T. Vernet, and A. M. Di Guilmi. 2010. Stability and assembly of pilus subunits of Streptococcus pneumoniae. J. Biol. Chem. 285:12405-12415.
15. Emsley, J., M. Cruz, R. Handin, and R. Liddington. 1998. Crystal structure of the von Willebrand factor A1 domain and implications for the binding of platelet glycoprotein Ib. J. Biol. Chem. 273:10396-10401.
16. Emsley, J., S. L. King, J. M. Bergelson, and R. C. Liddington. 1997. Crystal structure of the I domain from integrin alpha2beta1. J. Biol. Chem. 272: 28512-28517.
17. Fletcher, M. A., and B. Fritzell. 2007. Brief review of the clinical effectiveness of PREVENAR against otitis media. Vaccine 25:2507-2512.
18. Gianfaldoni, C., S. Censini, M. Hilleringmann, M. Moschioni, C. Facciotti, W. Pansegrau, V. Masignani, A. Covacci, R. Rappuoli, M. A. Barocchi, and P. Ruggiero. 2007. Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect. Immun. 75:1059-1062.
19. Givon-Lavi, N., D. Fraser, N. Porat, and R. Dagan. 2002. Spread of Streptococcus pneumoniae and antibiotic-resistant S. pneumoniae from day-care center attendees to their younger siblings. J. Infect. Dis. 186:1608-1614.
20. Hanage, W. P. 2008. Serotype-specific problems associated with pneumococcal conjugate vaccination. Future Microbiol. 3:23-30.
21. Hilleringmann, M., F. Giusti, B. C. Baudner, V. Masignani, A. Covacci, R. Rappuoli, M. A. Barocchi, and I. Ferlenghi. 2008. Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathog. 4:e1000026. (Pubitemid 351631087)
22. Hilleringmann, M., P. Ringler, S. A. Muller, G. De Angelis, R. Rappuoli, I. Ferlenghi, and A. Engel. 2009. Molecular architecture of Streptococcus pneumoniae TIGR4 pili. EMBO J. 28:3921-3930.
23. Huang, S. S., V. L. Hinrichsen, A. E. Stevenson, S. L. Rifas-Shiman, K. Kleinman, S. I. Pelton, M. Lipsitch, W. P. Hanage, G. M. Lee, and J. A. Finkelstein. 2009. Continued impact of pneumococcal conjugate vaccine on carriage in young children. Pediatrics 124:e1-e11.
24. Hynes, R. O., E. E. Marcantonio, M. A. Stepp, L. A. Urry, and G. H. Yee. 1989. Integrin heterodimer and receptor complexity in avian and mammalian cells. J. Cell Biol. 109:409-420.
25. Imai, S., Y. Ito, T. Ishida, T. Hirai, I. Ito, K. Maekawa, S. Takakura, Y. Iinuma, S. Ichiyama, and M. Mishima. 2009. High prevalence of multidrug-resistant pneumococcal molecular epidemiology network clones among Streptococcus pneumoniae isolates from adult patients with community-acquired pneumonia in Japan. Clin. Microbiol. Infect. 15:1039-1045.
26. Izoré, T., C. Contreras-Martel, L. ElMortaji, C. Manzano, R. Terrasse, T. Vernet, A. M. Di Guilmi, and A. Dessen. 2010. Structural basis of host cell recognition by the pilus adhesin from Streptococcus pneumoniae. Structure 18:106-115.
27. Kang, H. J., and E. N. Baker. 2009. Intramolecular isopeptide bonds give thermodynamic and proteolytic stability to the major pilin protein of Streptococcus pyogenes. J. Biol. Chem. 284:20729-20737.
28. Kang, H. J., N. G. Paterson, A. H. Gaspar, H. Ton-That, and E. N. Baker. 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.
29. Käyhty, H., K. Auranen, H. Nohynek, R. Dagan, and H. Makela. 2006. Nasopharyngeal colonization: a target for pneumococcal vaccination. Expert Rev. Vaccines 5:651-667.
30. Kim, K. S. 2010. Acute bacterial meningitis in infants and children. Lancet Infect. Dis. 10:32-42.
31. Klugman, K. P. 2009. The significance of serotype replacement for pneumococcal disease and antibiotic resistance. Adv. Exp. Med. Biol. 634:121-128.
32. Lauer, P., C. D. Rinaudo, M. Soriani, I. Margarit, D. Maione, R. Rosini, A. R. Taddei, M. Mora, R. Rappuoli, G. Grandi, and J. L. Telford. 2005. Genome analysis reveals pili in Group B Streptococcus. Science 309:105.
33. Lipsitch, M., K. O'Neill, D. Cordy, B. Bugalter, K. Trzcinski, C. M. Thompson, R. Goldstein, S. Pelton, H. Huot, V. Bouchet, R. Reid, M. Santosham, and K. L. O'Brien. 2007. Strain characteristics of Streptococcus pneumoniae carriage and invasive disease isolates during a cluster-randomized clinical trial of the 7-valent pneumococcal conjugate vaccine. J. Infect. Dis. 196: 1221-1227.
34. Lucero, M. G., V. E. Dulalia, L. T. Nillos, G. Williams, R. A. Parreno, H. Nohynek, I. D. Riley, and H. Makela. 2009. Pneumococcal conjugate vaccines for preventing vaccine-type invasive pneumococcal disease and X-ray defined pneumonia in children less than two years of age. Cochrane Database Syst. Rev. 7:CD004977.
35. Manetti, A. G., C. Zingaretti, F. Falugi, S. Capo, M. Bombaci, F. Bagnoli, G. Gambellini, G. Bensi, M. Mora, A. M. Edwards, J. M. Musser, E. A. Graviss, J. L. Telford, G. Grandi, and I. Margarit. 2007. Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol. Microbiol. 64:968-983.
36. Manzano, C., T. Izore, V. Job, A. M. Di Guilmi, and A. Dessen. 2009. Sortase activity is controlled by a flexible lid in the pilus biogenesis mechanism of gram-positive pathogens. Biochemistry 48:10549-10557.
37. Melegaro, A., Y. H. Choi, R. George, W. J. Edmunds, E. Miller, and N. J. Gay. 2010. Dynamic models of pneumococcal carriage and the impact of the Heptavalent Pneumococcal Conjugate Vaccine on invasive pneumococcal disease. BMC Infect. Dis. 10:90.
38. Moschioni, M., G. De Angelis, S. Melchiorre, V. Masignani, E. Leibovitz, M. A. Barocchi, and R. Dagan. 2009. Prevalence of pilus encoding islets among acute otitis media Streptococcus pneumoniae isolates from Israel. Clin. Microbiol. Infect. doi:10.1111/j.1469-0691.2009.03105.
39. Moschioni, M., C. Donati, A. Muzzi, V. Masignani, S. Censini, W. P. Hanage, C. J. Bishop, J. N. Reis, S. Normark, B. Henriques-Normark, A. Covacci, R. Rappuoli, and M. A. Barocchi. 2008. Streptococcus pneumoniae contains 3 rlrA pilus variants that are clonally related. J. Infect. Dis. 197:888-896.
40. Muzzi, A., M. Moschioni, A. Covacci, R. Rappuoli, and C. Donati. 2008. Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination. PLoS One 3:e3660.
41. Nelson, A. L., J. Ries, F. Bagnoli, S. Dahlberg, S. Falker, S. Rounioja, J. Tschop, E. Morfeldt, I. Ferlenghi, M. Hilleringmann, D. W. Holden, R. Rappuoli, S. Normark, M. A. Barocchi, and B. Henriques-Normark. 2007. RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol. Microbiol. 66:329-340.
42. Noske, N., U. Kammerer, M. Rohde, and S. Hammerschmidt. 2009. Pneumococcal interaction with human dendritic cells: phagocytosis, survival, and induced adaptive immune response are manipulated by PavA. J. Immunol. 183:1952-1963.
43. O'Brien, K. L., L. J. Wolfson, J. P. Watt, E. Henkle, M. Oria-Knoll, N. McCall, E. Lee, K. Mulholland, O. S. Levine, and T. Cherian. 2009. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374:893-902.
44. Papaconstantinou, M. E., C. J. Carrell, A. O. Pineda, K. M. Bobofchak, F. S. Mathews, C. S. Flordellis, M. E. Maragoudakis, N. E. Tsopanoglou, and E. Di Cera. 2005. Thrombin functions through its RGD sequence in a noncanonical conformation. J. Biol. Chem. 280:29393-29396.
45. Papasergi, S., M. Garibaldi, G. Tuscano, G. Signorino, S. Ricci, S. Peppoloni, I. Pernice, P. C. Lo, G. Teti, F. Felici, and C. Beninati. 2010. Plasminogen- and fibronectin-binding protein B is involved in the adherence of Streptococcus pneumoniae to human epithelial cells. J. Biol. Chem. 285:7517-7524.
46. Pelton, S. I., and E. Leibovitz. 2009. Recent advances in otitis media. Pediatr. Infect. Dis. J. 28:S133-S137.
47. Pezzicoli, A., I. Santi, P. Lauer, R. Rosini, D. Rinaudo, G. Grandi, J. L. Telford, and M. Soriani. 2008. Pilus backbone contributes to group B Streptococcus paracellular translocation through epithelial cells. J. Infect. Dis. 198:890-898.
48. Rinta-Kokko, H., R. Dagan, N. Givon-Lavi, and K. Auranen. 2009. Estimation of vaccine efficacy against acquisition of pneumococcal carriage. Vaccine 27:3831-3837.
49. Rose, L., P. Shivshankar, E. Hinojosa, A. Rodriguez, C. J. Sanchez, and C. J. Orihuela. 2008. Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. J. Infect. Dis. 198:375-383.
50. Ryan, M. W., and P. J. Antonelli. 2000. Pneumococcal antibiotic resistance and rates of meningitis in children. Laryngoscope 110:961-964.
51. Telford, J. L., M. A. Barocchi, I. Margarit, R. Rappuoli, and G. Grandi. 2006. Pili in gram-positive pathogens. Nat. Rev. Microbiol. 4:509-519.
52. Ton-That, H., and O. Schneewind. 2003. Assembly of pili on the surface of Corynebacterium diphtheriae. Mol. Microbiol. 50:1429-1438.
53. Ton-That, H., and O. Schneewind. 2004. Assembly of pili in Gram-positive bacteria. Trends Microbiol. 12:228-234.
54. Uchiyama, S., A. F. Carlin, A. Khosravi, S. Weiman, A. Banerjee, D. Quach, G. Hightower, T. J. Mitchell, K. S. Doran, and V. Nizet. 2009. The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J. Exp. Med. 206:1845-1852.
55. van der Poll, T., and S. M. Opal. 2009. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 374:1543-1556.