Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis

被引:194
作者
Oggioni, Marco R.
Trappetti, Claudia
Kadioglu, Aras
Cassone, Marco
Iannelli, Francesco
Ricci, Susanna
Andrew, Peter W.
Pozzi, Gianni
机构
[1] Univ Siena, Dipartimento Biol Mol, Lab Microbiol Mol & Biotecnol, I-53100 Siena, Italy
[2] Azienda Osped Univ Senese, UOC Batteriol, Siena, Italy
[3] Univ Leicester, Dept Infect Immun & Inflammat, Leicester LE1 7RH, Leics, England
关键词
D O I
10.1111/j.1365-2958.2006.05310.x
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Two main patterns of gene expression of Streptococcus pneumoniae were observed during infection in the host by quantitative real time RT-PCR; one was characteristic of bacteria in blood and one of bacteria in tissue, such as brain and lung. Gene expression in blood was characterized by increased expression of pneumolysin, pspA and hrcA, while pneumococci in tissue infection showed increased expression of neuraminidases, metalloproteinases, oxidative stress and competence genes. In vitro situations with similar expression patterns were detected in liquid culture and in a newly developed pneumococcal model of biofilm respectively. The biofilm model was dependent on addition of synthetic competence stimulating peptide (CSP) and no biofilm was formed by CSP receptor mutants. As one of the differentially expressed gene sets in vivo were the competence genes, we exploited competence-specific tools to intervene on pneumococcal virulence during infection. Induction of the competence system by the quorum-sensing peptide, CSP, not only induced biofilm formation in vitro, but also increased virulence in pneumonia in vivo. In contrast, a mutant for the ComD receptor, which did not form biofilm, also showed reduced virulence in pneumonia. These results were opposite to those found in a bacteraemic sepsis model of infection, where the competence system was downregulated. When pneumococci in the different physiological states were used directly for challenge, sessile cells grown in a biofilm were more effective in inducing meningitis and pneumonia, while planktonic cells from liquid culture were more effective in inducing sepsis. Our data enable us, using in vivo gene expression and in vivo modulation of virulence, to postulate the distinction - from the pneumococcal point of view - between two main types of disease. During bacteraemic sepsis pneumococci resemble planktonic growth, while during tissue infection, such as pneumonia or meningitis, pneumococci are in a biofilm-like state.
引用
收藏
页码:1196 / 1210
页数:15
相关论文
共 63 条
[41]   Streptococcus gordonii biofilm formation:: Identification of genes that code for biofilm phenotypes [J].
Loo, CY ;
Corliss, DA ;
Ganeshkumar, N .
JOURNAL OF BACTERIOLOGY, 2000, 182 (05) :1374-1382
[42]   Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis [J].
Manco, Sonia ;
Hernon, Fidelma ;
Yesilkaya, Hasan ;
Paton, James C. ;
Andrew, Peter W. ;
Kadioglu, Aras .
INFECTION AND IMMUNITY, 2006, 74 (07) :4014-4020
[43]   Differential fluorescence induction analysis of Streptococcus pneumoniae identifies genes involved in pathogenesis [J].
Marra, A ;
Asundi, J ;
Bartilson, M ;
Lawson, S ;
Fang, F ;
Christine, J ;
Wiesner, C ;
Brigham, D ;
Schneider, WP ;
Hromockyj, AE .
INFECTION AND IMMUNITY, 2002, 70 (03) :1422-1433
[44]   The Streptococcus pneumoniae cia regulon:: CiaR target sites and transcription profile analysis [J].
Mascher, T ;
Zähner, D ;
Merai, M ;
Balmelle, N ;
de Saizieu, AB ;
Hakenbeck, R .
JOURNAL OF BACTERIOLOGY, 2003, 185 (01) :60-70
[45]   Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence [J].
Mayville, P ;
Ji, GY ;
Beavis, R ;
Yang, HM ;
Goger, M ;
Novick, RP ;
Muir, TW .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1999, 96 (04) :1218-1223
[46]   Antibacterial activity of a competence-stimulating peptide in experimental sepsis caused by Streptococcus pneumoniae [J].
Oggioni, MR ;
Iannelli, F ;
Ricci, S ;
Chiavolini, D ;
Parigi, R ;
Trappetti, C ;
Claverys, JP ;
Pozzi, G .
ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, 2004, 48 (12) :4725-4732
[47]   Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia [J].
Oggioni, MR ;
Memmi, G ;
Maggi, T ;
Chiavolini, D ;
Lannelli, F ;
Pozzi, G .
MOLECULAR MICROBIOLOGY, 2003, 49 (03) :795-805
[48]   The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo [J].
Ogunniyi, AD ;
Giammarinaro, P ;
Paton, JC .
MICROBIOLOGY-SGM, 2002, 148 :2045-2053
[49]   Tissue-specific contributions of pneumococcal virulence factors to pathogenesis [J].
Orihuela, CJ ;
Gao, GL ;
Francis, KP ;
Yu, J ;
Tuomanen, EI .
JOURNAL OF INFECTIOUS DISEASES, 2004, 190 (09) :1661-1669
[50]   Microarray analysis of pneumococcal gene expression during invasive disease [J].
Orihuela, CJ ;
Radin, JN ;
Sublett, JE ;
Gao, GL ;
Kaushal, D ;
Tuomanen, EI .
INFECTION AND IMMUNITY, 2004, 72 (10) :5582-5596