Characterization of pneumococcal genes involved in bloodstream invasion in a mouse model

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Mahdi, Layla K ^a   Van Der Hoek, Mark B ^a,b   Ebrahimie, Esmaeil ^a   Paton, James C ^a   Ogunniyi, Abiodun D ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; SERINE PROTEINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; SUPEROXIDE DISMUTASE; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BLOOD; CELL WALL; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE ONTOLOGY; MALE; MOUSE; MUTAGENESIS; NASOPHARYNX; NONHUMAN; PRTA GENE; SEROTYPE; SODA GENE; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTOMICS; ULAA GENE; UPREGULATION; VANZ GENE; ANIMAL; BACTEREMIA; BACTERIAL GENE; DISEASE MODEL; GENETICS; MICROBIOLOGY; OTITIS MEDIA; PNEUMOCOCCAL INFECTION; VIRULENCE;

ANIMALS; BACTEREMIA; DISEASE MODELS, ANIMAL; FEMALE; GENES, BACTERIAL; MALE; MICE; NASOPHARYNX; OTITIS MEDIA; PNEUMOCOCCAL INFECTIONS; SEROGROUP; STREPTOCOCCUS PNEUMONIAE; SUPEROXIDE DISMUTASE; UP-REGULATION; VIRULENCE; VIRULENCE FACTORS;

EID: 84951278338     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141816     Document Type: Article

References (60)

1. World Health Organization Media Centre; Pneumonia: Fact sheet No 331. 2013.
2. World Health Organization; Antimicrobial resistance: global report on surveillance. 2014.
3. Brueggemann AB, Pai R, Crook DW, Beall B. Vaccine escape recombinants emerge after pneumococcal vaccination in the United States. PLoS Pathog. 2007 Nov; 3(11):e168. PMID: 18020702
4. Briles DE, Hollingshead SK, Paton JC, Ades EW, Novak L, van Ginkel FW, et al. 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. 2003 Aug 1; 188(3):339-48. PMID: 12870114
5. Ogunniyi AD, Folland RL, Briles DE, Hollingshead SK, Paton JC. Immunization of mice with combinations of pneumococcal virulence proteins elicits enhanced protection against challenge with Streptococcus pneumoniae. Infect Immun. 2000 May; 68(5):3028-33. PMID: 10769009
6. Ogunniyi AD, Grabowicz M, Briles DE, Cook J, Paton JC. Development of a vaccine against invasive pneumococcal disease based on combinations of virulence proteins of Streptococcus pneumoniae. Infect Immun. 2007 Jan; 75(1):350-7. PMID: 17088353
7. Brown JS, Ogunniyi AD, Woodrow MC, Holden DW, Paton JC. Immunization with components of two iron uptake ABC transporters protects mice against systemic Streptococcus pneumoniae infection. Infect Immun. 2001 Nov; 69(11):6702-6. PMID: 11598041
8. Hammerschmidt S, Talay SR, Brandtzaeg P, Chhatwal GS. SpsA, a novel pneumococcal surface protein with specific binding to secretory immunoglobulin A and secretory component. Molecular Microbiology. 1997 Sep; 25(6):1113-24. PMID: 9350867
9. Paton JC, Lock RA, Hansman DJ. Effect of immunization with pneumolysin on survival time of mice challenged with Streptococcus pneumoniae. Infect Immun. 1983 May; 40(2):548-52. PMID: 6840851
10. Rosenow C, Ryan P, Weiser JN, Johnson S, Fontan P, Ortqvist A, et al. Contribution of novel cholinebinding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol Microbiol. 1997 Sep; 25(5):819-29. PMID: 9364908
11. Paton JC. New pneumococcal vaccines: basic science developments, p. 382-402. In: Tuomanen EI, Mitchell TJ, Morrison DA, Spratt BG (ed), The Pneumococcus. 2004; ASM Press, Washington DC.
12. Lock RA, Hansman D, Paton JC. Comparative efficacy of autolysin and pneumolysin as immunogens protecting mice against infection by Streptococcus pneumoniae. Microb Pathog. 1992 Feb; 12(2):137-43. PMID: 1350045
13. Kwon HY, Ogunniyi AD, Choi MH, Pyo SN, Rhee DK, Paton JC. The ClpP protease of Streptococcus pneumoniae modulates virulence gene expression and protects against fatal pneumococcal challenge. Infection and Immunity. 2004 Oct; 72(10):5646-53. PMID: 15385462
14. Lock RA, Paton JC, Hansman D. Comparative efficacy of pneumococcal neuraminidase and pneumolysin as immunogens protective against Streptococcus pneumoniae. Microb Pathog. 1988 Dec; 5 (6):461-7. PMID: 3149709
15. Tong HH, Li D, Chen S, Long JP, DeMaria TF. Immunization with recombinant Streptococcus pneumoniae neuraminidase NanA protects chinchillas against nasopharyngeal colonization. Infect Immun. 2005 Nov; 73(11):7775-8. PMID: 16239584
16. Moschioni M, De Angelis G, Harfouche C, Bizzarri E, Filippini S, Mori E, et al. Immunization with the RrgB321 fusion protein protects mice against both high and low pilus-expressing Streptococcus pneumoniae populations. Vaccine. 2012 Feb 8; 30(7):1349-56. doi: 10.1016/j.vaccine.2011.12.080 PMID: 22210141
17. Adamou JE, Heinrichs JH, Erwin AL, Walsh W, Gayle T, Dormitzer M, et al. Identification and characterization of a novel family of pneumococcal proteins that are protective against sepsis. Infect Immun. 2001 Feb; 69(2):949-58. PMID: 11159990
18. Hamel J, Charland N, Pineau I, Ouellet C, Rioux S, Martin D, et al. Prevention of pneumococcal disease in mice immunized with conserved surface-accessible proteins. Infect Immun. 2004 May; 72(5):2659-70. PMID: 15102774
19. Plumptre CD, Ogunniyi AD, Paton JC. Vaccination against Streptococcus pneumoniae using truncated derivatives of polyhistidine triad protein D. PLoS One. 2013 Oct 31; 8(10):e78916. doi: 10.1371/journal. pone.0078916 PMID: 24205351
20. Shah P, Swiatlo E. Immunization with polyamine transport protein PotD protects mice against systemic infection with Streptococcus pneumoniae. Infect Immun. 2006 Oct; 74(10):5888-92. PMID: 16988268
21. GiefingC,Meinke AL, HannerM, Henics T, BuiMD, Gelbmann D, et al.Discovery of a novel class of highly conserved vaccine antigens using genomic scale antigenic fingerprinting of pneumococcus with human antibodies. J Exp Med. 2008 Jan 21; 205(1):117-31. doi: 10.1084/jem.20071168 PMID: 18166586
22. Mahdi LK, Wang H, Van der Hoek MB, Paton JC, Ogunniyi AD. Identification of a novel pneumococcal vaccine antigen preferentially expressed during meningitis in mice. J Clin Invest. 2012 Jun 1; 122 (6):2208-20. doi: 10.1172/JCI45850 PMID: 22622042
23. Ogunniyi AD, Mahdi LK, Trappetti C, Verhoeven N, Mermans D, Van der Hoek MB, et al. Identification of genes that contribute to the pathogenesis of invasive pneumococcal disease by in vivo transcriptomic analysis. Infect Immun. 2012 Sep; 80(9):3268-78. doi: 10.1128/IAI.00295-12 PMID: 22778095
24. Weiser JN. The pneumococcus: why a commensal misbehaves. J Mol Med (Berl). 2010 Feb; 88(2):97-102.
25. Berry AM, Paton JC. Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect Immun. 2000 Jan; 68(1):133-40. PMID: 10603379
26. Weiser JN, Austrian R, Sreenivasan PK, Masure HR. Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun. 1994 Jun; 62 (6):2582-9. PMID: 8188381
27. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, Peterson S, et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001 Jul 20; 293(5529):498-506. PMID: 11463916
28. Hoskins J, Alborn WE Jr., Arnold J, Blaszczak LC, Burgett S, DeHoff BS, et al. Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol. 2001 Oct; 183(19):5709-17. PMID: 11544234
29. McCluskey J, Hinds J, Husain S, Witney A, Mitchell TJ. A two-component system that controls the expression of pneumococcal surface antigen A (PsaA) and regulates virulence and resistance to oxidative stress in Streptococcus pneumoniae. Mol Microbiol. 2004 Mar; 51(6):1661-75. PMID: 15009893
30. Ogunniyi AD, Mahdi LK, Jennings MP, McEwan AG, McDevitt CA, Van der Hoek MB, et al. Central role of manganese in regulation of stress responses, physiology, and metabolism in Streptococcus pneumoniae. J Bacteriol. 2010 Sep; 192(17):4489-97. doi: 10.1128/JB.00064-10 PMID: 20601473
31. Smyth GK. Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor. New York: Springer; 2005. p. 397-420.
32. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods. 2003 Dec; 31(4):265-73. PMID: 14597310
33. Fox RJ, Dimmic MW. A two-sample Bayesian t-test for microarray data. Bmc Bioinformatics. 2006 Mar 10; 7.
34. Fruzangohar M, Ebrahimie E, Ogunniyi AD, Mahdi LK, Paton JC, Adelson DL. Comparative GO: a web application for comparative gene ontology and gene ontology-based gene selection in bacteria. PLoS One. 2013; 8(3):e58759. doi: 10.1371/journal.pone.0058759 PMID: 23536820
35. Stephens MA. Edf Statistics for Goodness of Fit and Some Comparisons. J Am Stat Assoc. 1974; 69 (347):730-7.
36. Horton RM, Ho SN, Pullen JK, Hunt HD, Cai Z, Pease LR. Gene splicing by overlap extension. Methods Enzymol. 1993; 217:270-9. PMID: 8474334
37. Kim JO, Weiser JN. Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae. J Infect Dis. 1998 Feb; 177(2):368-77. PMID: 9466523
38. Briles DE, Novak L, Hotomi M, van Ginkel FW, King J. Nasal colonization with Streptococcus pneumoniae includes subpopulations of surface and invasive pneumococci. Infect Immun. 2005 Oct; 73 (10):6945-51. PMID: 16177374
39. LeMessurier KS, Ogunniyi AD, Paton JC. Differential expression of key pneumococcal virulence genes in vivo. Microbiology-SGM. 2006 Feb; 152:305-11.
40. Mahdi LK, Ogunniyi AD, LeMessurier KS, Paton JC. Pneumococcal virulence gene expression and host cytokine profiles during pathogenesis of invasive disease. Infect Immun. 2008 Feb; 76(2):646-57. PMID: 18039836
41. Kuppermann N. Occult bacteremia in young febrile children. Pediatr Clin North Am. 1999 Dec; 46 (6):1073-109. PMID: 10629675
42. Hava DL, Camilli A. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol. 2002 Sep; 45(5):1389-406. PMID: 12207705
43. Orihuela CJ, Gao G, Francis KP, Yu J, Tuomanen EI. Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis. 2004 Nov 1; 190(9):1661-9. PMID: 15478073
44. Yesilkaya H, Kadioglu A, Gingles N, Alexander JE, Mitchell TJ, Andrew PW. Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect Immun. 2000 May; 68(5):2819-26. PMID: 10768978
45. Eijkelkamp BA, Morey JR, Ween MP, Ong CL, McEwan AG, Paton JC, et al. Extracellular zinc competitively inhibits manganese uptake and compromises oxidative stress management in Streptococcus pneumoniae. PLoS One. 2014; 9(2):e89427. doi: 10.1371/journal.pone.0089427 PMID: 24558498
46. Brooks-Walter A, Briles DE, Hollingshead SK. 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. 1999 Dec; 67(12):6533-42. PMID: 10569772
47. Ogunniyi AD, LeMessurier KS, Graham RMA, Watt JM, Briles DE, Stroeher UH, et al. Contributions of pneumolysin, pneumococcal surface protein A (PspA), and PspC to pathogenicity of Streptococcus pneumoniae D39 in a mouse model. Infect Immun. 2007 Apr; 75(4):1843-51. PMID: 17261599
48. Orihuela CJ, Mahdavi J, Thornton J, Mann B, Wooldridge KG, Abouseada N, et al. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. J Clin Invest. 2009 Jun; 119(6):1638-46. doi: 10.1172/JCI36759 PMID: 19436113
49. Moffitt KL, Gierahn TM, Lu YJ, Gouveia P, Alderson M, Flechtner JB, et al. T(H)17-based vaccine design for prevention of Streptococcus pneumoniae colonization. Cell Host Microbe. 2011 Feb 17; 9 (2):158-65. doi: 10.1016/j.chom.2011.01.007 PMID: 21320698
50. Bethe G, Nau R, Wellmer A, Hakenbeck R, Reinert RR, Heinz HP, et al. The cell wall-associated serine protease PrtA: a highly conserved virulence factor of Streptococcus pneumoniae. FEMS Microbiol Lett. 2001 Nov 27; 205(1):99-104. PMID: 11728722
51. de Stoppelaar SF, Bootsma HJ, Zomer A, Roelofs JJ, Hermans PW, van 't Veer C, et al. Streptococcus pneumoniae serine protease HtrA, but not SFP or PrtA, is a major virulence factor in pneumonia. PLoS One. 2013; 8(11):e80062. doi: 10.1371/journal.pone.0080062 PMID: 24244609
52. Balachandran P, Brooks-Walter A, Virolainen-Julkunen A, Hollingshead SK, Briles DE. Role of pneumococcal surface protein C in nasopharyngeal carriage and pneumonia and its ability to elicit protection against carriage of Streptococcus pneumoniae. Infect Immun. 2002 May; 70(5):2526-34. PMID: 11953392
53. Iannelli F, Chiavolini D, Ricci S, Oggioni MR, Pozzi G. Pneumococcal surface protein C contributes to sepsis caused by Streptococcus pneumoniae in mice. Infection and Immunity. 2004 May; 72(5):3077-80. PMID: 15102826
54. Hendriksen WT, Bootsma HJ, van Diepen A, Estevao S, Kuipers OP, de Groot R, et al. Strain-specific impact of PsaR of Streptococcus pneumoniae on global gene expression and virulence. Microbiology. 2009 May; 155(Pt 5):1569-79. doi: 10.1099/mic.0.025072-0 PMID: 19372167
55. Arthur M, Depardieu F, Molinas C, Reynolds P, Courvalin P. The vanZ gene of Tn1546 from Enterococcus faecium BM4147 confers resistance to teicoplanin. Gene. 1995 Feb 27; 154(1):87-92. PMID: 7867956
56. Mirza S, Wilson L, Benjamin WH Jr., Novak J, Barnes S, Hollingshead SK, et al. Serine protease PrtA from Streptococcus pneumoniae plays a role in the killing of S. pneumoniae by apolactoferrin. Infect Immun. 2011 Jun; 79(6):2440-50. doi: 10.1128/IAI.00489-10 PMID: 21422179
57. Zysk G, Bethe G, Nau R, Koch D, Grafin Von Bassewitz VC, Heinz HP, et al. Immune response to capsular polysaccharide and surface proteins of Streptococcus pneumoniae in patients with invasive pneumococcal disease. J Infect Dis. 2003 Jan 15; 187(2):330-3. PMID: 12552461
58. Zysk G, Bongaerts RJ, ten Thoren E, Bethe G, Hakenbeck R, Heinz HP. Detection of 23 immunogenic pneumococcal proteins using convalescent-phase serum. Infect Immun. 2000 Jun; 68(6):3740-3. PMID: 10816539
59. Orihuela CJ, Radin JN, Sublett JE, Gao G, Kaushal D, Tuomanen EI. Microarray analysis of pneumococcal gene expression during invasive disease. Infect. Immun. 2004 Oct; 72(10):5582-96. PMID: 15385455
60. Pettigrew MM, Marks LR, Kong Y, Gent JF, Roche-Hakansson H, Hakansson AP. Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection. Infect Immun. 2014 Nov; 82(11):4607-19. doi: 10.1128/IAI. 02225-14 PMID: 25135685