Regulation of virulence gene expression resulting from streptococcus pneumoniae and nontypeable haemophilus influenzae interactions in chronic disease

Emily K. Cope, Natalia Goldstein-Daruech, Jennifer M. Kofonow, Lanette Christensen, Bridget McDermott, Fernando P Monroy, James N. Palmer, Alexander G. Chiu, Mark E. Shirtliff, Noam A. Cohen, Jeff G. Leid

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

Chronic rhinosinusitis (CRS) is a common inflammatory disease of the sinonasal cavity mediated, in part, by polymicrobial communities of bacteria. Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. These results extend previous studies of population-level virulence and provide novel insight into the importance of S. pneumoniae and NTHi in CRS.

Original languageEnglish (US)
Article numbere28523
JournalPLoS One
Volume6
Issue number12
DOIs
StatePublished - Dec 5 2011

Fingerprint

Haemophilus influenzae
Streptococcus pneumoniae
Gene Expression Regulation
chronic diseases
Gene expression
Virulence
Chronic Disease
virulence
Tissue
gene expression
Biofilms
coculture
Coculture Techniques
Gene Expression
Pyruvate Oxidase
Bacterial RNA
biofilm
RNA-Directed DNA Polymerase
Virulence Factors
Transcription

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Regulation of virulence gene expression resulting from streptococcus pneumoniae and nontypeable haemophilus influenzae interactions in chronic disease. / Cope, Emily K.; Goldstein-Daruech, Natalia; Kofonow, Jennifer M.; Christensen, Lanette; McDermott, Bridget; Monroy, Fernando P; Palmer, James N.; Chiu, Alexander G.; Shirtliff, Mark E.; Cohen, Noam A.; Leid, Jeff G.

In: PLoS One, Vol. 6, No. 12, e28523, 05.12.2011.

Research output: Contribution to journalArticle

Cope, EK, Goldstein-Daruech, N, Kofonow, JM, Christensen, L, McDermott, B, Monroy, FP, Palmer, JN, Chiu, AG, Shirtliff, ME, Cohen, NA & Leid, JG 2011, 'Regulation of virulence gene expression resulting from streptococcus pneumoniae and nontypeable haemophilus influenzae interactions in chronic disease', PLoS One, vol. 6, no. 12, e28523. https://doi.org/10.1371/journal.pone.0028523
Cope, Emily K. ; Goldstein-Daruech, Natalia ; Kofonow, Jennifer M. ; Christensen, Lanette ; McDermott, Bridget ; Monroy, Fernando P ; Palmer, James N. ; Chiu, Alexander G. ; Shirtliff, Mark E. ; Cohen, Noam A. ; Leid, Jeff G. / Regulation of virulence gene expression resulting from streptococcus pneumoniae and nontypeable haemophilus influenzae interactions in chronic disease. In: PLoS One. 2011 ; Vol. 6, No. 12.
@article{5c0f4aab9c1c44af883b5d6128b65c76,
title = "Regulation of virulence gene expression resulting from streptococcus pneumoniae and nontypeable haemophilus influenzae interactions in chronic disease",
abstract = "Chronic rhinosinusitis (CRS) is a common inflammatory disease of the sinonasal cavity mediated, in part, by polymicrobial communities of bacteria. Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. These results extend previous studies of population-level virulence and provide novel insight into the importance of S. pneumoniae and NTHi in CRS.",
author = "Cope, {Emily K.} and Natalia Goldstein-Daruech and Kofonow, {Jennifer M.} and Lanette Christensen and Bridget McDermott and Monroy, {Fernando P} and Palmer, {James N.} and Chiu, {Alexander G.} and Shirtliff, {Mark E.} and Cohen, {Noam A.} and Leid, {Jeff G.}",
year = "2011",
month = "12",
day = "5",
doi = "10.1371/journal.pone.0028523",
language = "English (US)",
volume = "6",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "12",

}

TY - JOUR

T1 - Regulation of virulence gene expression resulting from streptococcus pneumoniae and nontypeable haemophilus influenzae interactions in chronic disease

AU - Cope, Emily K.

AU - Goldstein-Daruech, Natalia

AU - Kofonow, Jennifer M.

AU - Christensen, Lanette

AU - McDermott, Bridget

AU - Monroy, Fernando P

AU - Palmer, James N.

AU - Chiu, Alexander G.

AU - Shirtliff, Mark E.

AU - Cohen, Noam A.

AU - Leid, Jeff G.

PY - 2011/12/5

Y1 - 2011/12/5

N2 - Chronic rhinosinusitis (CRS) is a common inflammatory disease of the sinonasal cavity mediated, in part, by polymicrobial communities of bacteria. Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. These results extend previous studies of population-level virulence and provide novel insight into the importance of S. pneumoniae and NTHi in CRS.

AB - Chronic rhinosinusitis (CRS) is a common inflammatory disease of the sinonasal cavity mediated, in part, by polymicrobial communities of bacteria. Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. These results extend previous studies of population-level virulence and provide novel insight into the importance of S. pneumoniae and NTHi in CRS.

UR - http://www.scopus.com/inward/record.url?scp=82655183579&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=82655183579&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0028523

DO - 10.1371/journal.pone.0028523

M3 - Article

VL - 6

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 12

M1 - e28523

ER -