用户名: 密码: 验证码:
Phenotypic, genomic, and transcriptional characterization of Streptococcus pneumoniae interacting with human pharyngeal cells
详细信息    查看全文
  • 作者:Sheila Z Kimaro Mlacha (1) (2) (7)
    Sandra Romero-Steiner (3)
    Julie C Dunning Hotopp (2)
    Nikhil Kumar (2)
    Nadeeza Ishmael (2)
    David R Riley (2)
    Umar Farooq (2)
    Todd H Creasy (2)
    Luke J Tallon (2)
    Xinyue Liu (2)
    Cynthia S Goldsmith (4)
    Jacquelyn Sampson (3)
    George M Carlone (3)
    Susan K Hollingshead (5)
    J Anthony G Scott (1) (6)
    Hervé Tettelin (2)
  • 关键词:Streptococcus pneumoniae ; Gene expression ; Microarray ; Adherence ; Invasion ; Genome ; Mutagenesis ; SP_1922 ; Ply operon
  • 刊名:BMC Genomics
  • 出版年:2013
  • 出版时间:December 2013
  • 年:2013
  • 卷:14
  • 期:1
  • 全文大小:1321KB
  • 参考文献:1. O’Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, Lee E, Mulholland K, Levine OS, Cherian T: Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. / Lancet 2009, 374:893-02. CrossRef
    2. Roush SW, Murphy TV: Historical comparisons of morbidity and mortality for vaccine-preventable diseases in the United States. / JAMA 2007, 298:2155-163. CrossRef
    3. LeMessurier KS, Ogunniyi AD, Paton JC: Differential expression of key pneumococcal virulence genes in vivo. / Microbiology 2006, 152:305-11. CrossRef
    4. Orihuela CJ, Radin JN, Sublett JE, Gao G, Kaushal D, Tuomanen EI: Microarray analysis of pneumococcal gene expression during invasive disease. / Infect Immun 2004, 72:5582-596. CrossRef
    5. Song XM, Connor W, Hokamp K, Babiuk LA, Potter AA: Streptococcus pneumoniae early response genes to human lung epithelial cells. / BMC Res Notes 2008, 1:64. CrossRef
    6. Song XM, Connor W, Hokamp K, Babiuk LA, Potter AA: Transcriptome studies on Streptococcus pneumoniae , illustration of early response genes to THP-1 human macrophages. / Genomics 2009, 93:72-2. CrossRef
    7. Williamson YM, Gowrisankar R, Longo DL, Facklam R, Gipson IK, Ades EP, Carlone GM, Sampson JS: Adherence of nontypeable Streptococcus pneumoniae to human conjunctival epithelial cells. / Microb Pathog 2008, 44:175-85. CrossRef
    8. Romero-Steiner S, Pilishvili T, Sampson JS, Johnson SE, Stinson A, Carlone GM, Ades EW: Inhibition of pneumococcal adherence to human nasopharyngeal epithelial cells by anti-PsaA antibodies. / Clin Diagn Lab Immunol 2003, 10:246-51.
    9. Orihuela CJ: Role played by psrP-secY2A2 (accessory region 34) in the invasive disease potential of Streptococcus pneumoniae . / J Infect Dis 2009, 200:1180-181. author reply 1181-182 CrossRef
    10. Orihuela CJ, Mahdavi J, Thornton J, Mann B, Wooldridge KG, Abouseada N, Oldfield NJ, Self T, Ala’Aldeen DA, Tuomanen EI: Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. / J Clin Invest 2009, 119:1638-646. CrossRef
    11. Nelson AL, Ries J, Bagnoli F, Dahlberg S, Falker S, Rounioja S, Tschop J, Morfeldt E, Ferlenghi I, Hilleringmann M, / et al.: RrgA is a pilus-associated adhesin in Streptococcus pneumoniae . / Mol Microbiol 2007, 66:329-40. CrossRef
    12. Pracht D, Elm C, Gerber J, Bergmann S, Rohde M, Seiler M, Kim KS, Jenkinson HF, Nau R, Hammerschmidt S: PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. / Infect Immun 2005, 73:2680-689. CrossRef
    13. Hilleringmann M, Giusti F, Baudner BC, Masignani V, Covacci A, Rappuoli R, Barocchi MA, Ferlenghi I: Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. / PLoS Pathog 2008, 4:e1000026. CrossRef
    14. Papasergi S, Garibaldi M, Tuscano G, Signorino G, Ricci S, Peppoloni S, Pernice I, Lo Passo C, Teti G, Felici F, / et al.: Plasminogen- and fibronectin-binding protein B is involved in the adherence of Streptococcus pneumoniae to human epithelial cells. / J Biol Chem 2010, 285:7517-524. CrossRef
    15. Yamaguchi M, Terao Y, Mori Y, Hamada S, Kawabata S: PfbA, a novel plasmin- and fibronectin-binding protein of Streptococcus pneumoniae, contributes to fibronectin-dependent adhesion and antiphagocytosis. / J Biol Chem 2008, 283:36272-6279. CrossRef
    16. Weiser JN, Austrian R, Sreenivasan PK, Masure HR: Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. / Infect Immun 1994, 62:2582-589.
    17. Rajam G, Phillips DJ, White E, Anderton J, Hooper CW, Sampson JS, Carlone GM, Ades EW, Romero-Steiner S: A functional epitope of the pneumococcal surface adhesin A activates nasopharyngeal cells and increases bacterial internalization. / Microb Pathog 2008, 44:186-96. CrossRef
    18. Mollenhauer HH: Plastic Embedding Mixtures for Use in Electron Microscopy. / Stain Technol 1964, 39:111-14.
    19. Jiang SM, Ishmael N, Dunning Hotopp J, Puliti M, Tissi L, Kumar N, Cieslewicz MJ, Tettelin H, Wessels MR: Variation in the group B Streptococcus CsrRS regulon and effects on pathogenicity. / J Bacteriol 2008, 190:1956-965. CrossRef
    20. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, / et al.: TM4: a free, open-source system for microarray data management and analysis. / Biotechniques 2003, 34:374-78.
    21. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(?Delta Delta C(T)) Method. / Methods 2001, 25:402-08. CrossRef
    22. Lau PC, Sung CK, Lee JH, Morrison DA, Cvitkovitch DG: PCR ligation mutagenesis in transformable streptococci: application and efficiency. / J Microbiol Methods 2002, 49:193-05. CrossRef
    23. Sung CK, Li H, Claverys JP, Morrison DA: An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae . / Appl Environ Microbiol 2001, 67:5190-196. CrossRef
    24. Riley DR, Angiuoli SV, Crabtree J, Dunning Hotopp JC, Tettelin H: Using Sybil for interactive comparative genomics of microbes on the web. / Bioinformatics 2012, 28:160-66. CrossRef
    25. Ogunniyi AD, LeMessurier KS, Graham RM, Watt JM, Briles DE, Stroeher UH, Paton JC: Contributions of pneumolysin, pneumococcal surface protein A (PspA), and PspC to pathogenicity of Streptococcus pneumoniae D39 in a mouse model. / Infect Immun 2007, 75:1843-851. CrossRef
    26. Rubins JB, Paddock AH, Charboneau D, Berry AM, Paton JC, Janoff EN: Pneumolysin in pneumococcal adherence and colonization. / Microb Pathog 1998, 25:337-42. CrossRef
    27. Mahdi LK, Ogunniyi AD, LeMessurier KS, Paton JC: Pneumococcal virulence gene expression and host cytokine profiles during pathogenesis of invasive disease. / Infect Immun 2008, 76:646-57. CrossRef
    28. Rubins JB, Janoff EN: Pneumolysin: a multifunctional pneumococcal virulence factor. / J Lab Clin Med 1998, 131:21-7. CrossRef
    29. Larsen JE, Lund O, Nielsen M: Improved method for predicting linear B-cell epitopes. / Immunome Res 2006, 2:2. CrossRef
    30. Croucher NJ, Thomson NR: Studying bacterial transcriptomes using RNA-seq. / Curr Opin Microbiol 2010, 13:619-24. CrossRef
    31. Peppoloni S, Ricci S, Orsi CF, Colombari B, De Santi MM, Messino M, Fabio G, Zanardi A, Righi E, Braione V, / et al.: The encapsulated strain TIGR4 of Streptococcus pneumoniae is phagocytosed but is resistant to intracellular killing by mouse microglia. / Microbes Infect 2010, 12:990-001. CrossRef
    32. 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, 73:6945-951. CrossRef
    33. Cundell DR, Gerard NP, Gerard C, Idanpaan-Heikkila I, Tuomanen EI: Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. / Nature 1995, 377:435-38. CrossRef
    34. Brock SC, McGraw PA, Wright PF, Crowe JE Jr: The human polymeric immunoglobulin receptor facilitates invasion of epithelial cells by Streptococcus pneumoniae in a strain-specific and cell type-specific manner. / Infect Immun 2002, 70:5091-095. CrossRef
    35. Barocchi MA, Ries J, Zogaj X, Hemsley C, Albiger B, Kanth A, Dahlberg S, Fernebro J, Moschioni M, Masignani V, / et al.: A pneumococcal pilus influences virulence and host inflammatory responses. / Proc Natl Acad Sci USA 2006, 103:2857-862. CrossRef
    36. Rosch JW, Mann B, Thornton J, Sublett J, Tuomanen E: Convergence of regulatory networks on the pilus locus of Streptococcus pneumoniae . / Infect Immun 2008, 76:3187-196. CrossRef
    37. Obert C, Sublett J, Kaushal D, Hinojosa E, Barton T, Tuomanen EI, Orihuela CJ: Identification of a Candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. / Infect Immun 2006, 74:4766-777. CrossRef
    38. Munoz-Almagro C, Selva L, Sanchez CJ, Esteva C, De Sevilla MF, Pallares R, Orihuela CJ: PsrP, a protective pneumococcal antigen, is highly prevalent in children with pneumonia and is strongly associated with clonal type. / Clin Vaccine Immunol 2010, 17:1672-678. CrossRef
    39. Cron LE, Bootsma HJ, Noske N, Burghout P, Hammerschmidt S, Hermans PW: Surface-associated lipoprotein PpmA of Streptococcus pneumoniae is involved in colonization in a strain-specific manner. / Microbiology 2009, 155:2401-410. CrossRef
    40. Kerr AR, Paterson GK, McCluskey J, Iannelli F, Oggioni MR, Pozzi G, Mitchell TJ: The contribution of PspC to pneumococcal virulence varies between strains and is accomplished by both complement evasion and complement-independent mechanisms. / Infect Immun 2006, 74:5319-324. CrossRef
    41. Yuste J, Khandavilli S, Ansari N, Muttardi K, Ismail L, Hyams C, Weiser J, Mitchell T, Brown JS: The effects of PspC on complement-mediated immunity to Streptococcus pneumoniae vary with strain background and capsular serotype. / Infect Immun 2010, 78:283-92. CrossRef
    42. Harvey RM, Stroeher UH, Ogunniyi AD, Smith-Vaughan HC, Leach AJ, Paton JC: A variable region within the genome of Streptococcus pneumoniae contributes to strain-strain variation in virulence. / PLoS One 2011, 6:e19650. CrossRef
    43. McAllister LJ, Ogunniyi AD, Stroeher UH, Leach AJ, Paton JC: Contribution of Serotype and Genetic Background to Virulence of Serotype 3 and Serogroup 11 Pneumococcal Isolates. / Infect Immun 2011, 70:4839-849. CrossRef
    44. Claverys JP, Dintilhac A, Mortier-Barriere I, Martin B, Alloing G: Regulation of competence for genetic transformation in Streptococcus pneumoniae . / Soc Appl Bacteriol Symp Ser 1997, 26:32S-41S. CrossRef
    45. Peterson SN, Sung CK, Cline R, Desai BV, Snesrud EC, Luo P, Walling J, Li H, Mintz M, Tsegaye G, / et al.: Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. / Mol Microbiol 2004, 51:1051-070. CrossRef
    46. Fontaine L, Boutry C, Guedon E, Guillot A, Ibrahim M, Grossiord B, Hols P: Quorum-sensing regulation of the production of Blp bacteriocins in Streptococcus thermophilus . / J Bacteriol 2007, 189:7195-205. CrossRef
    47. Claverys JP, Havarstein LS: Extracellular-peptide control of competence for genetic transformation in Streptococcus pneumoniae . / Front Biosci 2002, 7:d1798-d1814. CrossRef
    48. Thornton J, McDaniel LS: THP-1 monocytes up-regulate intercellular adhesion molecule 1 in response to pneumolysin from Streptococcus pneumoniae . / Infect Immun 2005, 73:6493-498. CrossRef
    49. Price KE, Camilli A: Pneumolysin localizes to the cell wall of Streptococcus pneumoniae . / J Bacteriol 2009, 191:2163-168. CrossRef
    50. Yadav P, Thompson C, Lu J, Malley R: / Genetic requirements for pneumolysin localization. Abstractcts 7th International Symposium on Pneumococci and Pneumococcal Diseases (ISPPD-7).. Israel: Tel Aviv; 2010:35.
    51. Shivshankar P, Sanchez C, Rose LF, Orihuela CJ: The Streptococcus pneumoniae adhesin PsrP binds to Keratin 10 on lung cells. / Mol Microbiol 2009, 73:663-79. CrossRef
    52. Berry AM, Paton JC: Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae . / Infect Immun 1996, 64:5255-262.
    53. Sampson JS, O’Connor SP, Stinson AR, Tharpe JA, Russell H: Cloning and nucleotide sequence analysis of psaA, the Streptococcus pneumoniae gene encoding a 37-kilodalton protein homologous to previously reported Streptococcus sp. adhesins. / Infect Immun 1994, 62:319-24.
    54. Metcalf WW, Wanner BL: Mutational analysis of an Escherichia coli fourteen-gene operon for phosphonate degradation, using TnphoA-elements. / J Bacteriol 1993, 175:3430-442.
    55. Hava DL, Camilli A: Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. / Mol Microbiol 2002, 45:1389-406.
    56. Stroeher UH, Kidd SP, Stafford SL, Jennings MP, Paton JC, McEwan AG: A pneumococcal MerR-like regulator and S-nitrosoglutathione reductase are required for systemic virulence. / J Infect Dis 2007, 196:1820-826. CrossRef
    57. Kloosterman TG, van der Kooi-Pol MM, Bijlsma JJ, Kuipers OP: The novel transcriptional regulator SczA mediates protection against Zn2+ stress by activation of the Zn2-??resistance gene czcD in Streptococcus pneumoniae . / Mol Microbiol 2007, 65:1049-063. CrossRef
    58. Kidd SP, Jiang D, Jennings MP, McEwan AG: Glutathione-dependent alcohol dehydrogenase AdhC is required for defense against nitrosative stress in Haemophilus influenzae . / Infect Immun 2007, 75:4506-513. CrossRef
    59. Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS: A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. / Nature 2001, 410:490-94. CrossRef
    60. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, Peterson S, Heidelberg J, DeBoy RT, Haft DH, Dodson RJ, / et al.: Complete genome sequence of a virulent isolate of Streptococcus pneumoniae . / Science 2001, 293:498-06. CrossRef
    61. Tettelin H, Hollingshead S: / Comparative genomics of Streptococcus pneumoniae: intrastrain diversity and genome plasticity. The pneumococcus.. Washington, DC: ASM Press; 2004:15-9.
    62. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B: Artemis: sequence visualization and annotation. / Bioinformatics 2000, 16:944-45. CrossRef
  • 作者单位:Sheila Z Kimaro Mlacha (1) (2) (7)
    Sandra Romero-Steiner (3)
    Julie C Dunning Hotopp (2)
    Nikhil Kumar (2)
    Nadeeza Ishmael (2)
    David R Riley (2)
    Umar Farooq (2)
    Todd H Creasy (2)
    Luke J Tallon (2)
    Xinyue Liu (2)
    Cynthia S Goldsmith (4)
    Jacquelyn Sampson (3)
    George M Carlone (3)
    Susan K Hollingshead (5)
    J Anthony G Scott (1) (6)
    Hervé Tettelin (2)

    1. Kenya Medical Research Institute, Wellcome Trust Research Programme, Kilifi, Kenya
    2. Department of Microbiology and Immunology, Institute for Genome Sciences, University of Maryland School of Medicine, 801 W. Baltimore Street, Baltimore, MD, 21201, USA
    7. Respiratory & Meningeal Pathogens Research Unit, University of the Witwatersrand/Medical Research Council, Johannesburg, South Africa
    3. Division of Bacterial Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA
    4. Division of High-Consequence Pathogens and Pathology, Centers for Disease Control and Prevention, Atlanta, GA, USA
    5. Department of Microbiology, University of Alabama at Birmingham, Birmingham, AL, USA
    6. Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK
文摘
Background Streptococcus pneumoniae is a leading cause of childhood morbidity and mortality worldwide, despite the availability of effective pneumococcal vaccines. Understanding the molecular interactions between the bacterium and the host will contribute to the control and prevention of pneumococcal disease. Results We used a combination of adherence assays, mutagenesis and functional genomics to identify novel factors involved in adherence. By contrasting these processes in two pneumococcal strains, TIGR4 and G54, we showed that adherence and invasion capacities vary markedly by strain. Electron microscopy showed more adherent bacteria in association with membranous pseudopodia in the TIGR4 strain. Operons for cell wall phosphorylcholine incorporation (lic), manganese transport (psa) and phosphate utilization (phn) were up-regulated in both strains on exposure to epithelial cells. Pneumolysin, pili, stress protection genes (adhC-czcD) and genes of the type II fatty acid synthesis pathway were highly expressed in the naturally more invasive strain, TIGR4. Deletion mutagenesis of five gene regions identified as regulated in this study revealed attenuation in adherence. Most strikingly, ?SP_1922 which was predicted to contain a B-cell epitope and revealed significant attenuation in adherence, appeared to be expressed as a part of an operon that includes the gene encoding the cytoplasmic pore-forming toxin and vaccine candidate, pneumolysin. Conclusion This work identifies a list of novel potential pneumococcal adherence determinants.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700