Relevance of pili in pathogenic streptococci pathogenesis and vaccine development

Future Microbiology

Volumn 5, Issue 5, 2010, Pages 735-747

  Soriani, Marco ^a   Telford, John L ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

Author keywords

Colonization; GAS; GBS; Gram positive bacteria; Infectious disease; Pathogenic streptococci; Pili; Sortase; Streptococcus pneumoniae; Vaccine development

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; ESCHERICHIA COLI VACCINE; FIMBRIAL ANTIGEN; GROUP B STREPTOCOCCUS VACCINE; PILIN; SORTASE; SORTASE A; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBODY PRODUCTION; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM PILUS; BIOFILM; CELL ACTIVITY; CELL ADHESION; CELL INVASION; CELL STRUCTURE; ESCHERICHIA COLI INFECTION; GRAM POSITIVE BACTERIUM; GROUP B STREPTOCOCCAL INFECTION; HOST PATHOGEN INTERACTION; HUMAN; NONHUMAN; PATHOGENESIS; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS GROUP A; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION REGULATION; URINARY TRACT INFECTION; VACCINE PRODUCTION;

ANIMALS; BACTERIAL ADHESION; FIMBRIAE, BACTERIAL; HUMANS; MICE; STREPTOCOCCAL INFECTIONS; STREPTOCOCCAL VACCINES; STREPTOCOCCUS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA; STREPTOCOCCUS PNEUMONIAE;

EID: 77952384217     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.10.37     Document Type: Review

References (87)

1. Houwink AL, Van Iterson W: Electron microscopical observations on bacterial cytology; a study on flagellation. Biochim. Biophys. Acta 5 (1), 10-44 (1950).
2. Duguid JP, Smith IW, Dempster G, Edmunds PN: Non-flagellar filamentous appendages (fimbriae) and haemagglutinating activity in bacterium coli. J. Pathol. Bacteriol. 70 (2), 335-348 (1955).
3. Brinton CC Jr: Non-flagellar appendages of bacteria. Nature 183 (4664), 782-786 (1959).
4. Brinton CC 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. NY Acad. Sci. 27 (8), 1003-1054 (1965).
5. Proft T, Baker EN: Pili in Gram-negative and Gram-positive bacteria - structure, assembly and their role in disease. Cell Mol. Life Sci. 66 (4), 613-635 (2009).
6. Duguid JP, Campbell I: Antigens of the type-1 fimbriae of salmonellae and other enterobacteria. J. Med. Microbiol. 2 (4), 535-553 (1969).
7. Koga T, Ishimoto K, Lory S: Genetic and functional characterization of the gene cluster specifying expression of Pseudomonas aeruginosa pili. Infect. Immun. 61 (4), 1371-1377 (1993). (Pubitemid 23099209)
8. Freitag NE, Seifert HS, Koomey M: Characterization of the pilf-pild pilusassembly locus of Neisseria gonorrhoeae. Mol. Microbiol. 16 (3), 575-586 (1995).
9. Olsen A, Jonsson A, Normark S: Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338 (6217), 652-655 (1989). (Pubitemid 19104644)
10. Kikuchi T, Mizunoe Y, Takade A, Naito S, Yoshida S: Curli fibers are required for development of biofilm architecture in Escherichia coli k-12 and enhance bacterial adherence to human uroepithelial cells. Microbiol. Immunol. 49 (9), 875-884 (2005). (Pubitemid 41373940)
11. Hahn E, Wild P, Hermanns U et al.: Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J. Mol. Biol. 323 (5), 845-857 (2002). (Pubitemid 35341059)
12. Connell I, Agace W, Klemm P, Schembri M, Marild S, Svanborg C: Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl Acad. Sci. USA 93 (18), 9827-9832 (1996). (Pubitemid 26296694)
13. Craig L, Pique ME, Tainer JA: Type IV pilus structure and bacterial pathogenicity Nat. Rev. Microbiol. 2 (5), 363-378 (2004). (Pubitemid 39490116)
14. Mattick JS: Type IV pili and twitching motility Annu. Rev. Microbiol. 56, 289-314 (2002).
15. Cisar JO, Vatter AE, Clark WB, Curl SH, Hurst-Calderone S, Sandberg AL: Mutants of actinomyces viscosus t14v lacking type 1, type 2, or both types of fimbriae. Infect. Immun. 56 (11), 2984-2989 (1988). (Pubitemid 18259959)
16. Yeung MK, Ragsdale PA: Synthesis and function of Actinomyces naeslundii t14v type 1 fimbriae require the expression of additional fimbria-associated genes. Infect. Immun. 65 (7), 2629-2639 (1997).
17. Yeung MK, Donkersloot JA, Cisar JO, Ragsdale PA: Identification of a gene involved in assembly of Actinomyces naeslundii t14v type 2 fimbriae. Infect. Immun. 66 (4), 1482-1491 (1998).
18. Ton-That H, Schneewind O: Assembly of pili on the surface of Corynebacterium diphtheriae. Mol. Microbiol. 50 (4), 1429-1438 (2003). (Pubitemid 37475871)
19. Gaspar AH, Ton-That H: Assembly of distinct pilus structures on the surface of Corynebacterium diphtheriae. J. Bacteriol 188 (4), 1526-1533 (2006). (Pubitemid 43228686)
20. Fives-Taylor PM, Thompson DW: Surface properties of Streptococcus sanguis fw213 mutants nonadherent to saliva-coated hydroxyapatite. Infect. Immun. 47 (3), 752-759 (1985).
21. Levesque C, Vadeboncoeur C, Chandad F, Frenette M: Streptococcus salivarius fimbriae are composed of a glycoprotein containing a repeated motif assembled into a filamentous nondissociable structure. J. Bacteriol. 183 (9), 2724-2732 (2001). (Pubitemid 32319274)
22. Weerkamp AH, Handley PS, Baars A, Slot JW: Negative staining and immunoelectron microscopy of adhesiondeficient mutants of Streptococcus salivarius reveal that the adhesive protein antigens are separate classes of cell surface fibril. J. Bacteriol. 165 (3), 746-755 (1986). (Pubitemid 16071401)
23. Lauer P, Rinaudo CD, Soriani M et al.: Genome ana lysis reveals pili in group B Streptococcus. Science 309 (5731), 105 (2005). (Pubitemid 40934983)
24. Rosini R, Rinaudo CD, Soriani M et al.: Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol. Microbiol. 61 (1), 126-141 (2006). (Pubitemid 43911503)
25. Mora M, Bensi G, Capo S et al.: Group A Streptococcus produce pilus-like structures containing protective antigens and lancefield T antigens. Proc. Natl Acad. Sci. USA 102 (43), 15641-15646 (2005). (Pubitemid 41528109)
26. Barocchi MA, Ries J, Zogaj X et al.: A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl Acad. Sci. USA 103 (8), 2857-2862 (2006). (Pubitemid 43306639)
27. Maione D, Margarit I, Rinaudo CD et al.: Identification of a universal group B Streptococcus vaccine by multiple genome screen. Science 309 (5731), 148-150 (2005). (Pubitemid 40934997)
28. Gianfaldoni C, Censini S, Hilleringmann M et al.: Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect. Immun. 75 (2), 1059-1062 (2007). (Pubitemid 46203474)
29. Mcnab R, Forbes H, Handley PS, Loach DM, Tannock GW, Jenkinson HF: Cell wallanchored csha polypeptide (259 kilodaltons) in Streptococcus gordonii forms surface fibrils that confer hydrophobic and adhesive properties. J. Bacteriol. 181 (10), 3087-3095 (1999). (Pubitemid 29236913)
30. Willcox MD, Drucker DB: Surface structures, co-aggregation and adherence phenomena of Streptococcus oralis and related species. Microbios 59 (238), 19-29 (1989).
31. Yanagawa R, Otsuki K, Tokui T: Electron microscopy of fine structure of Corynebacterium renale with special reference to pili. Jpn J. Vet. Res. 16 (1), 31-37 (1968).
32. Yanagawa R, Otsuki K: Some properties of the pili of Corynebacterium renale. J. Bacteriol. 101 (3), 1063-1069 (1970).
33. Jameson MW, Jenkinson HF, Parnell K, Handley PS: Polypeptides associated with tufts of cell-surface fibrils in an oral Streptococcus. Microbiology 141 (Pt 10), 2729-2738 (1995).
34. Yamaguchi T, Matsunoshita N: Isolation and some properties of fimbriae of oral Streptococcus intermedius. Curr. Microbiol. 49 (1), 59-65 (2004). (Pubitemid 38924623)
35. Manetti AG, Zingaretti C, Falugi F et al.: Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol. Microbiol. 64 (4), 968-983 (2007). (Pubitemid 46743959)
36. Pezzicoli A, Santi I, Lauer P et al.: Pilus backbone contributes to group B Streptococcus paracellular translocation through epithelial cells. J. Infect. Dis. 198 (6), 890-898 (2008).
37. Konto-Ghiorghi Y, Mairey E, Mallet A et al.: Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae. PLoS Pathog. 5 (5), E1000422 (2009).
38. Baker CJ: Group B streptococcal infections. Clin. Perinatol. 24 (1), 59-70 (1997).
39. Margarit I, Rinaudo CD, Galeotti CL et al.: Preventing bacterial infections with pilus-based vaccines: the group B Streptococcus paradigm. J. Infect. Dis. 199 (1), 108-115 (2009).
40. Marraffini LA, Dedent AC, Schneewind O: Sortases and the art of anchoring proteins to the envelopes of Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 70 (1), 192-221 (2006).
41. Cunningham MW: Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13 (3), 470-511 (2000).
42. Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN: Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science 318 (5856), 1625-1628 (2007). (Pubitemid 350233661)
43. Falugi F, Zingaretti C, Pinto V et al.: Sequence variation in group a Streptococcus pili and association of pilus backbone types with lancefield T serotypes. J. Infect. Dis. 198 (12), 1834-1841 (2008).
44. Kadioglu A, Weiser JN, Paton JC, Andrew PW: The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6 (4), 288-301 (2008). (Pubitemid 351404773)
45. Lemieux J, Hava DL, Basset A, Camilli A: RRGA and RRGB are components of a multisubunit pilus encoded by the Streptococcus pneumoniae RLRA pathogenicity islet. Infect. Immun. 74 (4), 2453-2456 (2006).
46. Hemsley C, Joyce E, Hava DL, Kawale A, Camilli A: MGRA, an orthologue of MGA, acts as a transcriptional repressor of the genes within the RLRA pathogenicity islet in Streptococcus pneumoniae. J. Bacteriol. 185 (22), 6640-6647 (2003). (Pubitemid 37385884)
47. Moschioni M, Donati C, Muzzi A et al.: Streptococcus pneumoniae contains 3 RLRA pilus variants that are clonally related. J. Infect. Dis. 197 (6), 888-896 (2008). (Pubitemid 351417013)
48. Nelson AL, Ries J, Bagnoli F et al.: RRGA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol. Microbiol. 66 (2), 329-340 (2007). (Pubitemid 47482375)
49. Falker S, Nelson AL, Morfeldt E et al.: Sortase-mediated assembly and surface topology of adhesive pneumococcal pili. Mol. Microbiol. 70 (3), 595-607 (2008).
50. Hilleringmann M, Giusti F, Baudner BC et al.: Pneumococcal pili are composed of protofilaments exposing adhesive clusters of RRG A. PLoS Pathog. 4 (3), E1000026 (2008). (Pubitemid 351631087)
51. Castelain M, Koutris E, Andersson M et al.: Characterization of the biomechanical properties of t4 pili expressed by Streptococcus pneumoniae - a comparison between helix-like and open coil-like pili. Chemphyschem. 10 (9-10), 1533-1540 (2009).
52. Hilleringmann M, Ringler P, Muller SA et al.: Molecular architecture of Streptococcus pneumoniae tigr4 pili. EMBO J. 28 (24), 3921-3930 (2009).
53. Bagnoli F, Moschioni M, Donati C et al.: A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J. Bacteriol. 190 (15), 5480-5492 (2008).
54. Basset A, Trzcinski K, Hermos C et al.: Association of the pneumococcal pilus with certain capsular serotypes but not with increased virulence. J. Clin. Microbiol. 45 (6), 1684-1689 (2007). (Pubitemid 46933892)
55. Podbielski A, Woischnik M, Leonard BA, Schmidt KH: Characterization of NRA, a global negative regulator gene in group a streptococci. Mol. Microbiol. 31 (4), 1051-1064 (1999). (Pubitemid 29082236)
56. Kreikemeyer B, Beckert S, Braun-Kiewnick A, Podbielski A: Group A streptococcal rofa-type global regulators exhibit a strain-specific genomic presence and regulation pattern. Microbiology 148 (Pt 5), 1501-1511 (2002). (Pubitemid 34567228)
57. Nakata M, Podbielski A, Kreikemeyer B: MSMR, a specific positive regulator of the Streptococcus pyogenes FCT pathogenicity region and cytolysin-mediated translocation system genes. Mol. Microbiol. 57 (3), 786-803 (2005). (Pubitemid 41025960)
58. Gutekunst H, Eikmanns BJ, Reinscheid DJ: Analysis of ROGB-controlled virulence mechanisms and gene repression in Streptococcus agalactiae. Infect. Immun. 71 (9), 5056-5064 (2003). (Pubitemid 37070748)
59. Dramsi S, Caliot E, Bonne I et al.: Assembly and role of pili in group B streptococci. Mol. Microbiol. 60 (6), 1401-1413 (2006). (Pubitemid 43801433)
60. Johri Ak, Margarit I, Broenstrup M et al.: Transcriptional and proteomic profiles of group B Streptococcus type V reveal potential adherence proteins associated with high-level invasion. Infect. Immun. 75 (3), 1473-1483 (2007). (Pubitemid 46385841)
61. Santi I, Grifantini R, Jiang SM et al.: Csrrs regulates group B Streptococcus virulence gene expression in response to environmental pH: a new perspective on vaccine development. J. Bacteriol. 191 (17), 5387-5397 (2009).
62. Hava DL, Hemsley CJ, Camilli A: Transcriptional regulation in the Streptococcus pneumoniae RLRA pathogenicity islet by RLRA. J. Bacteriol. 185 (2), 413-421 (2003). (Pubitemid 36070466)
63. Swaminathan A, Mandlik A, Swierczynski A, Gaspar A, Das A, Ton-That H: Housekeeping sortase facilitates the cell wall anchoring of pilus polymers in Corynebacterium diphtheriae. Mol. Microbiol. 66 (4), 961-974 (2007). (Pubitemid 350050422)
64. Ton-That H, Marraffini LA, Schneewind O: Sortases and pilin elements involved in pilus assembly of Corynebacterium diphtheriae. Mol. Microbiol. 53 (1), 251-261 (2004). (Pubitemid 38901395)
65. Ton-That H, Schneewind O: Assembly of pili in Gram-positive bacteria. Trends Microbiol. 12 (5), 228-234 (2004). (Pubitemid 38534627)
66. Kang HJ, Middleditch M, Proft T, Baker EN: Isopeptide bonds in bacterial pili and their characterisation by x-ray crystallography and mass spectrometry. Biopolymers 91 (12), 1126-1134 (2009).
67. Nobbs AH, Rosini R, Rinaudo CD, Maione D, Grandi G, Telford JL: Sortase a utilizes an ancillary protein anchor for efficient cell wall anchoring of pili in Streptococcus agalactiae. Infect. Immun. 76 (8), 3550-3560 (2008).
68. Patti JM, Allen BL, Mcgavin MJ, Hook M: MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48, 585-617 (1994). (Pubitemid 2157780)
69. Kreikemeyer B, Nakata M, Oehmcke S, Gschwendtner C, Normann J, Podbielski A: Streptococcus pyogenes collagen type I-binding Cpa surface protein: expression profile, binding characteristics, biological functions, and potential clinical impact. J. Biol. Chem. 280 (39), 33228-33239 (2005). (Pubitemid 41397119)
70. Maisey HC, Hensler M, Nizet V, Doran KS: Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J. Bacteriol. 189 (4), 1464-1467 (2007). (Pubitemid 46239769)
71. Abbot EL, Smith WD, Siou GP et al.: Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiol. 9 (7), 1822-1833 (2007).
72. Maisey HC, Quach D, Hensler ME et al.: A group B streptococcal pilus protein promotes phagocyte resistance and systemic virulence. FASEB J. 22 (6), 1715-1724 (2008). (Pubitemid 351811449)
73. Soriani M, Santi I, Taddei A, Rappuoli R, Grandi G, Telford JL: Group B Streptococcus crosses human epithelial cells by a paracellular route. J. Infect. Dis. 193 (2), 241-250 (2006). (Pubitemid 43113486)
74. Ochiai K, Kurita-Ochiai T, Kamino Y, Ikeda T: Effect of co-aggregation on the pathogenicity of oral bacteria. J. Med. Microbiol. 39 (3), 183-190 (1993). (Pubitemid 23279693)
75. Paranjpye RN, Strom MS: A Vibrio vulnificus type IV pilin contributes to biofilm formation, adherence to epithelial cells, and virulence. Infect. Immun. 73 (3), 1411-1422 (2005).
76. Edwards AM, Manetti AG, Falugi F et al.: Scavenger receptor gp340 aggregates group a streptococci by binding pili. Mol. Microbiol. 68 (6), 1378-1394 (2008). (Pubitemid 351725250)
77. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G: Pili in Gram-positive pathogens. Nat. Rev. Microbiol. 4 (7), 509-519 (2006). (Pubitemid 43905610)
78. Brinton CC: Immunobiology of Neisseria gonnorhoeae. American Society for Microbiology, Washington, DC, USA (1978).
79. Johnson SC, Chung RC, Deal CD et al.: Human immunization with PGH 3-2 gonococcal pilus results in cross-reactive antibody to the cyanogen bromide fragment-2 of pilin. J. Infect. Dis. 163 (1), 128-134 (1991).
80. Morgan RL, Isaacson RE, Moon HW, Brinton CC, To CC: Immunization of suckling pigs against enterotoxigenic Escherichia coli-induced diarrheal disease by vaccinating dams with purified 987 or k99 pili: protection correlates with pilus homology of vaccine and challenge. Infect. Immun. 22 (3), 771-777 (1978).
81. Li B, Jiang L, Song Q et al.: Protein microarray for profiling antibody responses to Yersinia pestis live vaccine. Infect. Immun. 73 (6), 3734-3739 (2005). (Pubitemid 40745918)
82. Goluszko P, Goluszko E, Nowicki B, Nowicki S, Popov V, Wang HQ: Vaccination with purified dr fimbriae reduces mortality associated with chronic urinary tract infection due to Escherichia coli bearing dr adhesin. Infect. Immun. 73 (1), 627-631 (2005). (Pubitemid 40041160)
83. Kao DJ, Churchill ME, Irvin RT, Hodges RS: Animal protection and structural studies of a consensus sequence vaccine targeting the receptor binding domain of the type IV pilus of Pseudomonas aeruginosa. J. Mol. Biol. 374 (2), 426-442 (2007).
84. Creti R, Imperi M, Baldassarri L et al.: Emm types, virulence factors, and antibiotic resistance of invasive Streptococcus pyogenes isolates from Italy: what has changed in 11 years? J. Clin. Microbiol. 45 (7), 2249-2256 (2007). (Pubitemid 47203800)
85. Shulman ST, Tanz RR, Kabat W et al.: Group A streptococcal pharyngitis serotype surveillance in North America, 2000-2002. Clin. Infect. Dis. 39 (3), 325-332 (2004). (Pubitemid 39050479)
86. Gianfaldoni C, Maccari S, Pancotto L et al.: Sortase a confers protection against Streptococcus pneumoniae in mice. Infect. Immun. 77 (7), 2957-2961 (2009).
87. Manzano C, Izore T, Job V, Di Guilmi AM, Dessen A: Sortase activity is controlled by a flexible lid in the pilus biogenesis mechanism of Gram-positive pathogens. Biochemistry 48 (44), 10549-10557 (2009).