Direct Evaluation of Pseudomonas aeruginosa Biofilm Mediators in a Chronic Infection Model

被引:64
作者
Byrd, Matthew S. [1 ]
Pang, Bing [1 ]
Hong, Wenzhou [1 ]
Waligora, Elizabeth A. [1 ]
Juneau, Richard A. [1 ]
Armbruster, Chelsie E. [1 ]
Weimer, Kristen E. D. [1 ]
Murrah, Kyle
Mann, Ethan E. [5 ]
Lu, Haiping [1 ]
Sprinkle, April [1 ]
Parsek, Matthew R. [4 ]
Kock, Nancy D. [2 ,3 ]
Wozniak, Daniel J. [5 ]
Swords, W. Edward [1 ]
机构
[1] Wake Forest Univ Hlth Sci, Dept Microbiol & Immunol, Winston Salem, NC 27157 USA
[2] Wake Forest Univ Hlth Sci, Dept Pathol, Winston Salem, NC 27157 USA
[3] Wake Forest Univ Hlth Sci, Dept Pathol Comparat Med, Winston Salem, NC 27157 USA
[4] Univ Washington, Dept Microbiol, Seattle, WA 98195 USA
[5] Ohio State Univ, Ctr Microbial Interface Biol, Columbus, OH 43210 USA
关键词
NONTYPABLE HAEMOPHILUS-INFLUENZAE; MIDDLE-EAR MUCOSA; QUORUM-SENSING SYSTEMS; BACTERIAL BIOFILMS; CHINCHILLA MODEL; OTITIS-MEDIA; IN-VIVO; MOTILITY; EXOPOLYSACCHARIDE; PERSISTENCE;
D O I
10.1128/IAI.00057-11
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
Biofilms contribute to Pseudomonas aeruginosa persistence in a variety of diseases, including cystic fibrosis, burn wounds, and chronic suppurative otitis media. However, few studies have directly addressed P. aeruginosa biofilms in vivo. We used a chinchilla model of otitis media, which has previously been used to study persistent Streptococcus pneumoniae and Haemophilus influenzae infections, to show that structures formed in vivo are biofilms of bacterial and host origin within a matrix that includes Psl, a P. aeruginosa biofilm polysaccharide. We evaluated three biofilm and/or virulence mediators of P. aeruginosa known to affect biofilm formation in vitro and pathogenesis in vivo-bis-(3',5')-cyclic dimeric GMP (c-di-GMP), flagella, and quorum sensing-in a chinchilla model. We show that c-di-GMP overproduction has a positive impact on bacterial persistence, while quorum sensing increases virulence. We found no difference in persistence attributed to flagella. We conclude from these studies that a chinchilla otitis media model provides a means to evaluate pathogenic mediators of P. aeruginosa and that in vitro phenotypes should be examined in multiple infection systems to fully understand their role in disease.
引用
收藏
页码:3087 / 3095
页数:9
相关论文
共 53 条
[1]   A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms [J].
Allesen-Holm, M ;
Barken, KB ;
Yang, L ;
Klausen, M ;
Webb, JS ;
Kjelleberg, S ;
Molin, S ;
Givskov, M ;
Tolker-Nielsen, T .
MOLECULAR MICROBIOLOGY, 2006, 59 (04) :1114-1128
[2]   Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures [J].
An, DD ;
Danhorn, T ;
Fuqua, C ;
Parsek, MR .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (10) :3828-3833
[3]   LuxS Promotes Biofilm Maturation and Persistence of Nontypeable Haemophilus influenzae In Vivo via Modulation of Lipooligosaccharides on the Bacterial Surface [J].
Armbruster, Chelsie E. ;
Hong, Wenzhou ;
Pang, Bing ;
Dew, Kristin E. ;
Juneau, Richard A. ;
Byrd, Matthew S. ;
Love, Cheraton F. ;
Kock, Nancy D. ;
Swords, W. Edward .
INFECTION AND IMMUNITY, 2009, 77 (09) :4081-4091
[4]   The role of flagellin versus motility in acute lung disease caused by Pseudomonas aeruginosa [J].
Balloy, Viviane ;
Verma, Amrisha ;
Kuravi, Sudha ;
Si-Tahar, Mustapha ;
Chignard, Michel ;
Ramphal, Reuben .
JOURNAL OF INFECTIOUS DISEASES, 2007, 196 (02) :289-296
[5]   Pseudomonas aeruginosa Biofilms in the Respiratory Tract of Cystic Fibrosis Patients [J].
Bjarnsholt, Thomas ;
Jensen, Peter Ostrup ;
Fiandaca, Mark J. ;
Pedersen, Jette ;
Hansen, Christine Ronne ;
Andersen, Claus Bogelund ;
Pressler, Tacjana ;
Givskov, Michael ;
Hoiby, Niels .
PEDIATRIC PULMONOLOGY, 2009, 44 (06) :547-558
[6]   Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix [J].
Borlee, Bradley R. ;
Goldman, Aaron D. ;
Murakami, Keiji ;
Samudrala, Ram ;
Wozniak, Daniel J. ;
Parsek, Matthew R. .
MOLECULAR MICROBIOLOGY, 2010, 75 (04) :827-842
[7]   SYNTHESIS OF MULTIPLE EXOPRODUCTS IN PSEUDOMONAS-AERUGINOSA IS UNDER THE CONTROL OF RHLR-RHLI, ANOTHER SET OF REGULATORS IN STRAIN PAO1 WITH HOMOLOGY TO THE AUTOINDUCER-RESPONSIVE LUXR-LUXI FAMILY [J].
BRINT, JM ;
OHMAN, DE .
JOURNAL OF BACTERIOLOGY, 1995, 177 (24) :7155-7163
[8]   The Pseudomonas aeruginosa Exopolysaccharide Psl Facilitates Surface Adherence and NF-κB Activation in A549 Cells [J].
Byrd, Matthew S. ;
Pang, Bing ;
Mishra, Meenu ;
Swords, W. Edward ;
Wozniak, Daniel J. .
MBIO, 2010, 1 (03)
[9]   Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production [J].
Byrd, Matthew S. ;
Sadovskaya, Irina ;
Vinogradov, Evgueny ;
Lu, Haiping ;
Sprinkle, April B. ;
Richardson, Stephen H. ;
Ma, Luyan ;
Ralston, Brad ;
Parsek, Matthew R. ;
Anderson, Erin M. ;
Lam, Joseph S. ;
Wozniak, Daniel J. .
MOLECULAR MICROBIOLOGY, 2009, 73 (04) :622-638
[10]   Impact of Pseudomonas aeruginosa quorum sensing on biofilm persistence in an in vivo intraperitoneal foreign-body infection model [J].
Christensen, Louise D. ;
Moser, Claus ;
Jensen, Peter O. ;
Rasmussen, Thomas B. ;
Christophersen, Lars ;
Kielleberg, Staffan ;
Kumar, Naresh ;
Hoiby, Niels ;
Givskov, Michael ;
Bjarnsholt, Thomas .
MICROBIOLOGY-SGM, 2007, 153 :2312-2320