Diverse evolutionary patterns of pneumococcal antigens identified by pangenome-wide immunological screening

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 3, 2017, Pages E357-E366

  Croucher, Nicholas J ^a   Campo, Joseph J ^b   Le, Timothy Q ^b   Liang, Xiaowu ^b   Bentley, Stephen D ^c   Hanage, William P ^d   Lipsitch, March ^d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b Antigen Discovery Inc   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Epidemiology; Evolution; Genomics; Immunology; Pathogens

Indexed keywords

ABC TRANSPORTER; BACTERIAL ANTIGEN; BACTERIAL DNA; EPITOPE; HISTIDINE; METALLOPROTEINASE; NEURAMINIDASE NANB; NEURAMINIDASE NANC; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN; SIALIDASE; UNCLASSIFIED DRUG; ZINC METALLOPROTEASE ZMPC; ZINC METALLOPROTEASE ZMPD; ADHESIN; BACTERIAL PROTEIN; BACTERIUM ANTIBODY; CARRIER PROTEIN; IMMUNOGLOBULIN G; MEMBRANE PROTEIN; PNEUMOCOCCUS VACCINE;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; ANTIGEN BINDING; ANTIGEN DETECTION; BACTERIAL CHROMOSOME; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL TRANSMISSION; BACTERIOPHAGE; CELL DIVISION; CELL SURFACE; CLADISTICS; CONFERENCE PAPER; DNA TRANSFER; FRAMESHIFT MUTATION; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENOTYPE; HOST PATHOGEN INTERACTION; HUMAN; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; POPULATION STRUCTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SEROTYPE; STREPTOCOCCUS PNEUMONIAE; STRUCTURAL GENE; WHOLE GENOME SEQUENCING; ADULT; ANTIBODY PRODUCTION; IMMUNOLOGY; PNEUMOCOCCAL INFECTION;

ADHESINS, BACTERIAL; ADULT; ANTIBODIES, BACTERIAL; ANTIBODY FORMATION; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; EPITOPES; HUMANS; IMMUNOGLOBULIN G; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; PNEUMOCOCCAL INFECTIONS; PNEUMOCOCCAL VACCINES; STREPTOCOCCUS PNEUMONIAE;

EID: 85009751223     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1613937114     Document Type: Article

References (75)

1. Gratten M, et al. (1986) Colonisation of Haemophilus influenzae and Streptococcus pneumoniae in the upper respiratory tract of neonates in Papua New Guinea: Primary acquisition, duration of carriage, and relationship to carriage in mothers. Biol Neonate 50(2):114-120.
2. Gray BM, Turner ME, Dillon HC, Jr (1982) Epidemiologic studies of Streptococcus pneumoniae in infants. The effects of season and age on pneumococcal acquisition and carriage in the first 24 months of life. Am J Epidemiol 116(4):692-703.
3. Zhang Q, et al. (2006) Serum and mucosal antibody responses to pneumococcal protein antigens in children: Relationships with carriage status. Eur J Immunol 36(1):46-57.
4. Holmgren J, Czerkinsky C (2005) Mucosal immunity and vaccines. Nat Med 11(4, Suppl):S45-S53.
5. Anttila M, Voutilainen M, Jäntti V, Eskola J, Käyhty H (1999) Contribution of serotypespecific IgG concentration, IgG subclasses and relative antibody avidity to opsonophagocytic activity against Streptococcus pneumoniae. Clin Exp Immunol 118(3):402-407.
6. Janoff EN, et al. (1999) Killing of Streptococcus pneumoniae by capsular polysaccharidespecific polymeric IgA, complement, and phagocytes. J Clin Invest 104(8):1139-1147.
7. Zhang Z, Clarke TB, Weiser JN (2009) Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 119(7):1899-1909.
8. Malley R, et al. (2005) CD4+ T cells mediate antibody-independent acquired immunity to pneumococcal colonization. Proc Natl Acad Sci USA 102(13):4848-4853.
9. Li Y, et al. (2012) Distinct effects on diversifying selection by two mechanisms of immunity against Streptococcus pneumoniae. PLoS Pathog 8(11):e1002989.
10. Cobey S, Lipsitch M (2012) Niche and neutral effects of acquired immunity permit coexistence of pneumococcal serotypes. Science 335(6074):1376-1380.
11. Rennels MB, et al. (1998) Safety and immunogenicity of heptavalent pneumococcal vaccine conjugated to CRM197 in United States infants. Pediatrics 101(4 Pt 1):604-611.
12. Ghaffar F, et al. (2004) Effect of the 7-valent pneumococcal conjugate vaccine on nasopharyngeal colonization by Streptococcus pneumoniae in the first 2 years of life. Clin Infect Dis 39(7):930-938.
13. Shinefield HR, et al. (1999) Safety and immunogenicity of heptavalent pneumococcal CRM197 conjugate vaccine in infants and toddlers. Pediatr Infect Dis J 18(9):757-763.
14. Moffitt KL, Malley R (2011) Next generation pneumococcal vaccines. Curr Opin Immunol 23(3):407-413.
15. Goldblatt D, et al. (2005) Antibody responses to nasopharyngeal carriage of Streptococcus pneumoniae in adults: A longitudinal household study. J Infect Dis 192(3):387-393.
16. Beghetto E, et al. (2006) Discovery of novel Streptococcus pneumoniae antigens by screening a whole-genome λ-display library. FEMS Microbiol Lett 262(1):14-21.
17. Giefing C, et al. (2008) Discovery of a novel class of highly conserved vaccine antigens using genomic scale antigenic fingerprinting of pneumococcus with human antibodies. J Exp Med 205(1):117-131.
18. Barocchi MA, et al. (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci USA 103(8):2857-2862.
19. Bagnoli F, et al. (2008) A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J Bacteriol 190(15):5480-5492.
20. Hollingshead SK, Becker R, Briles DE (2000) Diversity of PspA:Mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect Immun 68(10):5889-5900.
21. Brooks-Walter A, Briles DE, Hollingshead SK (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(12):6533-6542.
22. Croucher NJ, et al. (2015) Selective and genetic constraints on pneumococcal serotype switching. PLoS Genet 11(3):e1005095.
23. Huang SS, et al. (2009) Continued impact of pneumococcal conjugate vaccine on carriage in young children. Pediatrics 124(1):e1-e11.
24. Croucher NJ, et al. (2013) Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 45(6):656-663.
25. Croucher NJ, et al. (2015) Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 43(3):e15.
26. Croucher NJ, et al. (2015) Population genomic datasets describing the post-vaccine evolutionary epidemiology of Streptococcus pneumoniae. Sci Data 2:150058.
27. Croucher NJ, et al. (2014) Diversification of bacterial genome content through distinct mechanisms over different timescales. Nat Commun 5:5471.
28. Moschioni M, et al. (2008) Streptococcus pneumoniae contains 3 rlrA pilus variants that are clonally related. J Infect Dis 197(6):888-896.
29. Tettelin H, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293(5529):498-506.
30. Loisel E, et al. (2011) Biochemical characterization of the histidine triad protein PhtD as a cell surface zinc-binding protein of pneumococcus. Biochemistry 50(17):3551-3558.
31. Anderton JM, et al. (2007) E-cadherin is a receptor for the common protein pneumococcal surface adhesin A (PsaA) of Streptococcus pneumoniae. Microb Pathog 42(5-6):225-236.
32. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585-595.
33. Yang Z (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586-1591.
34. Anisimova M, Bielawski JP, Yang Z (2001) Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18(8):1585-1592.
35. Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164(3):1229-1236.
36. Boni MF, Posada D, Feldman MW (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176(2):1035-1047.
37. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34(2):126-129.
38. Piganeau G, Gardner M, Eyre-Walker A (2004) A broad survey of recombination in animal mitochondria. Mol Biol Evol 21(12):2319-2325.
39. Croucher NJ, et al. (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331(6016):430-434.
40. Croucher NJ, et al. (2014) Evidence for soft selective sweeps in the evolution of pneumococcal multidrug resistance and vaccine escape. Genome Biol Evol 6(7): 1589-1602.
41. Croucher NJ, et al. (2014) Variable recombination dynamics during the emergence, transmission and 'disarming' of a multidrug-resistant pneumococcal clone. BMC Biol 12(1):49.
42. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303(5655):223-226.
43. Smith JM, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90(10):4384-4388.
44. Paterson GK, Nieminen L, Jefferies JM, Mitchell TJ (2008) PclA, a pneumococcal collagen- like protein with selected strain distribution, contributes to adherence and invasion of host cells. FEMS Microbiol Lett 285(2):170-176.
45. Rose L, et al. (2008) Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. J Infect Dis 198(3):375-383.
46. Bensing BA, Sullam PM (2002) An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol 44(4):1081-1094.
47. Bensing BA, Gibson BW, Sullam PM (2004) The Streptococcus gordonii platelet binding protein GspB undergoes glycosylation independently of export. J Bacteriol 186(3):638-645.
48. Feltcher ME, Braunstein M (2012) Emerging themes in SecA2-mediated protein export. Nat Rev Microbiol 10(11):779-789.
49. Yen YT, et al. (2013) Differential localization of the streptococcal accessory sec components and implications for substrate export. J Bacteriol 195(4):682-695.
50. Gupta S, et al. (1996) The maintenance of strain structure in populations of recombining infectious agents. Nat Med 2(4):437-442.
51. Gupta S, Ferguson N, Anderson R (1998) Chaos, persistence, and evolution of strain structure in antigenically diverse infectious agents. Science 280(5365):912-915.
52. Buckee CO, Gupta S, Kriz P, Maiden MCJ, Jolley KA (2010) Long-term evolution of antigen repertoires among carried meningococci. Proc Biol Sci 277(1688):1635-1641.
53. Callaghan MJ, et al. (2008) The effect of immune selection on the structure of the meningococcal Opa protein repertoire. PLoS Pathog 4(3):e1000020.
54. Regev-Yochay G, et al. (2010) Re-emergence of the type 1 pilus among Streptococcus pneumoniae isolates in Massachusetts, USA. Vaccine 28(30):4842-4846.
55. Hausdorff WP, Feikin DR, Klugman KP (2005) Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis 5(2):83-93.
56. Waite RD, Struthers JK, Dowson CG (2001) Spontaneous sequence duplication within an open reading frame of the pneumococcal type 3 capsule locus causes high-frequency phase variation. Mol Microbiol 42(5):1223-1232.
57. Waite RD, Penfold DW, Struthers JK, Dowson CG (2003) Spontaneous sequence duplications within capsule genes cap8E and tts control phase variation in Streptococcus pneumoniae serotypes 8 and 37. Microbiology 149(Pt 2):497-504.
58. Hyams C, Camberlein E, Cohen JM, Bax K, Brown JS (2010) The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect Immun 78(2):704-715.
59. Tu AH, Fulgham RL, McCrory MA, Briles DE, Szalai AJ (1999) Pneumococcal surface protein A inhibits complement activation by Streptococcus pneumoniae. Infect Immun 67(9):4720-4724.
60. Janulczyk R, Iannelli F, Sjoholm AG, Pozzi G, Bjorck L (2000) Hic, a novel surface protein of Streptococcus pneumoniae that interferes with complement function. J Biol Chem 275(47):37257-37263.
61. Wani JH, Gilbert JV, Plaut AG, Weiser JN (1996) Identification, cloning, and sequencing of the immunoglobulin A1 protease gene of Streptococcus pneumoniae. Infect Immun 64(10):3967-3974.
62. Gor DO, Ding X, Briles DE, Jacobs MR, Greenspan NS (2005) Relationship between surface accessibility for PpmA, PsaA, and PspA and antibody-mediated immunity to systemic infection by Streptococcus pneumoniae. Infect Immun 73(3):1304-1312.
63. Jomaa M, et al. (2005) Antibodies to the iron uptake ABC transporter lipoproteins PiaA and PiuA promote opsonophagocytosis of Streptococcus pneumoniae. Infect Immun 73(10):6852-6859.
64. Brown JS, Ogunniyi AD, Woodrow MC, Holden DW, Paton JC (2001) Immunization with components of two iron uptake ABC transporters protects mice against systemic Streptococcus pneumoniae infection. Infect Immun 69(11):6702-6706.
65. Saxena S, Khan N, Dehinwal R, Kumar A, Sehgal D (2015) Conserved surface accessible nucleoside ABC transporter component SP0845 is essential for pneumococcal virulence and confers protection in vivo. PLoS One 10(2):e0118154.
66. Jomaa M, et al. (2006) Immunization with the iron uptake ABC transporter proteins PiaA and PiuA prevents respiratory infection with Streptococcus pneumoniae. Vaccine 24(24):5133-5139.
67. Briles DE, et al. (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(2):796-800.
68. Iannelli F, Oggioni MR, Pozzi G (2002) Allelic variation in the highly polymorphic locus pspC of Streptococcus pneumoniae. Gene 284(1-2):63-71.
69. Trzciński K, et al. (2015) Effect of serotype on pneumococcal competition in a mouse colonization model. MBio 6(5):e00902-e00915.
70. R Core Development Team (2011) R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna).
71. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
72. Stajich JE, et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12(10):1611-1618.
73. Lawrence TJ, et al. (2015) FAST: FAST Analysis of Sequences Toolbox. Front Genet 6:172.
74. Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21(4):456-463.
75. Kamvar ZN, Brooks JC, Grünwald NJ (2015) Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front Genet 6(JUN):208.