Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection

Pettigrew, Melinda M.; Marks, Laura R.; Kong, Yong; Gent, Janneane F.; Roche-Hakansson, Hazeline; Hakansson, Anders P.

doi:10.1128/iai.02225-14

Cited by 110Bacterial biofilms and quorum sensingPneumonia and Respiratory InfectionsMicrobial infections and disease research

Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection

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Pettigrew, Melinda M., Marks, Laura R., Kong, Yong, Gent, Janneane F., Roche-Hakansson, Hazeline, Hakansson, Anders P.·2014·Infection and Immunity

DOI 10.1128/iai.02225-14PMC PMC4249342

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Abstract

Streptococcus pneumoniae is a leading cause of infectious disease globally. Nasopharyngeal colonization occurs in biofilms and precedes infection. Prior studies have indicated that biofilm-derived pneumococci are avirulent. However, influenza A virus (IAV) infection releases virulent pneumococci from biofilms in vitro and in vivo. Triggers of dispersal include IAV-induced changes in the nasopharynx, such as increased temperature (fever) and extracellular ATP (tissue damage). We used whole-transcriptome shotgun sequencing (RNA-seq) to compare the S. pneumoniae transcriptome in biofilms, bacteria dispersed from biofilms after exposure to IAV, febrile-range temperature, or ATP, and planktonic cells grown at 37°C. Compared with biofilm bacteria, actively dispersed S. pneumoniae, which were more virulent in invasive disease, upregulated genes involved in carbohydrate metabolism. Enzymatic assays for ATP and lactate production confirmed that dispersed pneumococci exhibited increased metabolism compared to those in biofilms. Dispersed pneumococci also upregulated genes associated with production of bacteriocins and downregulated colonization-associated genes related to competence, fratricide, and the transparent colony phenotype. IAV had the largest impact on the pneumococcal transcriptome. Similar transcriptional differences were also observed when actively dispersed bacteria were compared with avirulent planktonic bacteria. Our data demonstrate complex changes in the pneumococcal transcriptome in response to IAV-induced changes in the environment. Our data suggest that disease is caused by pneumococci that are primed to move to tissue sites with altered nutrient availability and to protect themselves from the nasopharyngeal microflora and host immune response. These data help explain pneumococcal virulence after IAV infection and have important implications for studies of S. pneumoniae pathogenesis.

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Influenza affects the S. pneumoniae transcriptome in terms of downregulating expression of genes associated with the colonizer state and upregulations of bacteriocins.
“Influenza has been shown to affect the S. pneumoniae transcriptome in terms of downregulating expression of genes associated with the colonizer state and upregulations of bacteriocins (142).”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [142]
Viruses impair bacterial biofilm formation and disrupt existing biofilm.
“Viruses have also been found to impair bacterial biofilm formation and disrupt existing biofilm (141–144).”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [142]

The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
Differential expression analysis for sequence count data
Anders, S., & Huber, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-10-r106 · Cited by 15,581 · see citing works
Integrative genomics viewer
Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., & Mesirov, J. P. (2011) · Nature Biotechnology · doi:10.1038/nbt.1754 · Cited by 15,390 · see citing works
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration
Thorvaldsdottir, H., Robinson, J. T., & Mesirov, J. P. (2013) · Briefings in Bioinformatics · doi:10.1093/bib/bbs017 · Cited by 9,049 · see citing works
Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates
O'Brien, K. L., Wolfson, L. J., Watt, J. P., Henkle, E., Deloria-Knoll, M., McCall, N., Lee, E., Mulholland, K., Levine, O. S., & Cherian, T. (2009) · The Lancet · doi:10.1016/s0140-6736(09)61204-6 · Cited by 2,398 · see citing works
Global burden of childhood pneumonia and diarrhoea
Walker, C. L. F., Rudan, I., Liu, L., Nair, H., Theodoratou, E., Bhutta, Z. A., O'Brien, K. L., Campbell, H., & Black, R. E. (2013) · The Lancet · doi:10.1016/s0140-6736(13)60222-6 · Cited by 2,356 · see citing works
Bacteriocins—A viable alternative to antibiotics?
Cotter, P. D., Ross, R. P., & Hill, C. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2937 · Cited by 1,793 · see citing works
Predominant Role of Bacterial Pneumonia as a Cause of Death in Pandemic Influenza: Implications for Pandemic Influenza Preparedness
Morens, D. M., Taubenberger, J. K., & Fauci, A. S. (2008) · The Journal of Infectious Diseases · doi:10.1086/591708 · Cited by 1,625 · see citing works
Direct Detection of Bacterial Biofilms on the Middle-Ear Mucosa of Children With Chronic Otitis Media
Hall‐Stoodley, L., Hu, F. Z., Gieseke, A., Nistico, L., Nguyen, D., Hayes, J. D., Forbes, M. L., Greenberg, D. P., Dice, B., Burrows, A. C., et al. (2006) · JAMA · doi:10.1001/jama.296.2.202 · Cited by 874 · see citing works
Insights into the Interaction between Influenza Virus and Pneumococcus
McCullers, J. A. (2006) · Clinical Microbiology Reviews · doi:10.1128/cmr.00058-05 · Cited by 846 · see citing works
Epidemiologic Studies of Streptococcus pneumoniae in Infants: Acquisition, Carriage, and Infection during the First 24 Months of Life
Gray, B. M., Converse, G. M., & Dillon, H. C. (1980) · The Journal of Infectious Diseases · doi:10.1093/infdis/142.6.923 · Cited by 797 · see citing works
The co-pathogenesis of influenza viruses with bacteria in the lung.
McCullers, J. A. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3231 · Cited by 722 · see citing works
Inhibition of pulmonary antibacterial defense by interferon-γ during recovery from influenza infection
Sun, K., & Metzger, D. W. (2008) · Nature Medicine · doi:10.1038/nm1765 · Cited by 587 · see citing works
B-1 and B-2 Cell–Derived Immunoglobulin M Antibodies Are Nonredundant Components of the Protective Response to Influenza Virus Infection
Baumgarth, N., Herman, O. C., Jager, G. C., Brown, L. E., Herzenberg, L. A., & Chen, J. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.2.271 · Cited by 583 · see citing works
Btrim: A fast, lightweight adapter and quality trimming program for next-generation sequencing technologies
Kong, Y. (2011) · Genomics · doi:10.1016/j.ygeno.2011.05.009 · Cited by 580 · see citing works
Self-citation
Liaisons dangereuses: P2X7 and the inflammasome
Di Virgilio, F. (2007) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2007.07.002 · Cited by 493 · see citing works
High-Throughput Illumina Strand-Specific RNA Sequencing Library PreparationPreprint
Zhong, S., Joung, J., Zheng, Y., Chen, Y.-R., Liu, B., Shao, Y., Xiang, J., Fei, Z., & Giovannoni, J. J. (2011) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5652 · Cited by 471 · see citing works
The Bacterial Phosphoenolpyruvate:Carbohydrate Phosphotransferase System: Regulation by Protein Phosphorylation and Phosphorylation-Dependent Protein-Protein Interactions
Deutscher, J., Aké, F. M., Derkaoui, M., Zébré, A. C., Cao, T. N., Bouraoui, H., Kentache, T., Mokhtari, A., Milohanic, E., & Joyet, P. (2014) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00001-14 · Cited by 432 · see citing works
Role of Neuraminidase in Lethal Synergism between Influenza Virus and Streptococcus pneumoniae
McCullers, J. A., & Bartmess, K. C. (2003) · The Journal of Infectious Diseases · doi:10.1086/368163 · Cited by 384 · see citing works
Association of Intrastrain Phase Variation in Quantity of Capsular Polysaccharide and Teichoic Acid with the Virulence ofStreptococcus pneumoniae
Kim, J. O., & Weiser, J. N. (1998) · The Journal of Infectious Diseases · doi:10.1086/514205 · Cited by 358 · see citing works
New Patterns in the Otopathogens Causing Acute Otitis Media Six to Eight Years After Introduction of Pneumococcal Conjugate Vaccine
Casey, J. R., Adlowitz, D. G., & Pichichero, M. E. (2010) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0b013e3181c1bc48 · Cited by 344 · see citing works
Tissue‐Specific Contributions of Pneumococcal Virulence Factors to Pathogenesis
Orihuela, C. J., Gao, G., Francis, K. P., Yu, J., & TUOMANEN, E. I. (2004) · The Journal of Infectious Diseases · doi:10.1086/424596 · Cited by 327 · see citing works
Intracerebral Microdialysis in Clinical Practice: Baseline Values for Chemical Markers during Wakefulness, Anesthesia, and Neurosurgery
Reinstrup, P., Ståhl, N., Mellergård, P., et al. (2000) · Neurosurgery · doi:10.1227/00006123-200009000-00035 · Cited by 315 · see citing works
Respiratory viruses predisposing to bacterial infections: role of neuraminidase.
PELTOLA, V. T., & MCCULLERS, J. A. (2004) · Pediatric Infectious Disease Journal · doi:10.1097/01.inf.0000108197.81270.35 · Cited by 290 · see citing works
Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis
Oggioni, M. R., Trappetti, C., Kadioglu, A., Cassone, M., Iannelli, F., Ricci, S., Andrew, P. W., & Pozzi, G. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05310.x · Cited by 273 · see citing works
Continued Impact of Pneumococcal Conjugate Vaccine on Carriage in Young Children
Huang, S. S., Hinrichsen, V. L., Stevenson, A. E., Rifas‐Shiman, S. L., KLEINMAN, K. P., Pelton, S. I., Lipsitch, M., Hanage, W. P., Lee, G. M., & Finkelstein, J. A. (2009) · PEDIATRICS · doi:10.1542/peds.2008-3099 · Cited by 269 · see citing works
Role of Novel Choline Binding Proteins in Virulence of Streptococcus pneumoniae
Gosink, K. K., Mann, E. R., Guglielmo, C., TUOMANEN, E. I., & Masure, H. R. (2000) · Infection and Immunity · doi:10.1128/iai.68.10.5690-5695.2000 · Cited by 267 · see citing works
Microarray Analysis of Pneumococcal Gene Expression during Invasive Disease
Orihuela, C. J., Radin, J. N., Sublett, J. E., Gao, G., Kaushal, D., & TUOMANEN, E. I. (2004) · Infection and Immunity · doi:10.1128/iai.72.10.5582-5596.2004 · Cited by 243 · see citing works
Identification of an active disaccharide unit of a glycoconjugate receptor for pneumococci attaching to human pharyngeal epithelial cells.
Andersson, B. A., Dahmén, J., FREJD, T., Leffler, H., Magnusson, G., Noori, G. F. M., & Edén, C. S. (1983) · The Journal of Experimental Medicine · doi:10.1084/jem.158.2.559 · Cited by 242 · see citing works
Interkingdom signaling induces Streptococcus pneumoniae biofilm dispersion and transition from asymptomatic colonization to disease
Marks, L. R., Davidson, B. A., Knight, P. R., & Hakansson, A. P. (2013) · mBio · doi:10.1128/mbio.00438-13 · Cited by 240 · see citing works
Immunizations with Pneumococcal Surface Protein A and Pneumolysin Are Protective against Pneumonia in a Murine Model of Pulmonary Infection withStreptococcus pneumoniae
Briles, D. E., Hollingshead, S. K., Paton, J. C., et al. (2003) · The Journal of Infectious Diseases · doi:10.1086/376571 · Cited by 234 · see citing works
Nasopharyngeal Colonization during the First Year of Life
Aniansson, G., Aim, B., Andersson, B. A., Larsson, P., Nylén, O., Peterson, H., Rignér, P., Svanborg, M., & Svanborg, C. (1992) · The Journal of Infectious Diseases · doi:10.1093/infdis/165-supplement_1-s38 · Cited by 232 · see citing works
Lactic Acid Assay with L(+)lactic Acid Dehydrogenase from Rabbit Muscle
Lundholm, L., Mohme‐Lundholm, E., & Vamos, N. (1963) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1963.tb02645.x · Cited by 203 · see citing works
Pneumococcal Neuraminidases A and B Both Have Essential Roles during Infection of the Respiratory Tract and Sepsis
Manco, S., Hernon, F., Yeşilkaya, H., Paton, J. C., Andrew, P. W., & Kadioglu, A. (2006) · Infection and Immunity · doi:10.1128/iai.01237-05 · Cited by 196 · see citing works
The role of fever in the infected host
Hasday, J. D., Fairchild, K. D., & Shanholtz, C. B. (2000) · Microbes and Infection · doi:10.1016/s1286-4579(00)01337-x · Cited by 192 · see citing works
Recognition of Streptococcus pneumoniae by the innate immune system
Koppe, U., Suttorp, N., & Opitz, B. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01746.x · Cited by 191 · see citing works
The blp Bacteriocins of Streptococcus pneumoniae Mediate Intraspecies Competition both In Vitro and In Vivo
Dawid, S. R., Roche, A. M., & Weiser, J. N. (2006) · Infection and Immunity · doi:10.1128/iai.01775-05 · Cited by 188 · see citing works
Catabolite Control Protein A (CcpA) Contributes to Virulence and Regulation of Sugar Metabolism in Streptococcus pneumoniae
Iyer, R., Baliga, N. S., & Camilli, A. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.24.8340-8349.2005 · Cited by 186 · see citing works
A Functional Genomics Approach to Establish the Complement of Carbohydrate Transporters in Streptococcus pneumoniae
Bidossi, A., Mulas, L., Decorosi, F., Colomba, L., Ricci, S., Pozzi, G., Deutscher, J., Viti, C., & Oggioni, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033320 · Cited by 179 · see citing works
Intracerebral Microdialysis in Clinical Practice: Baseline Values for Chemical Markers during Wakefulness, Anesthesia, and Neurosurgery
Reinstrup, P., Ståhl, N., Mellergård, P., et al. (2000) · Neurosurgery · doi:10.1097/00006123-200009000-00035 · Cited by 177 · see citing works
Identification of a Candidate Streptococcus pneumoniae Core Genome and Regions of Diversity Correlated with Invasive Pneumococcal Disease
Obert, C. A., Sublett, J. E., Kaushal, D., Hinojosa, E., Barton, T., TUOMANEN, E. I., & Orihuela, C. J. (2006) · Infection and Immunity · doi:10.1128/iai.00316-06 · Cited by 176 · see citing works
Deep RNA sequencing of L. monocytogenes reveals overlapping and extensive stationary phase and sigma B-dependent transcriptomes, including multiple highly transcribed noncoding RNAs
Oliver, H. F., Orsi, R. H., Ponnala, L., Keich, U., Wang, W., Sun, Q., Cartinhour, S. W., Filiatrault, M. J., Wiedmann, M., & Boor, K. J. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-641 · Cited by 173 · see citing works
Nasopharyngeal Carriage of Streptococcus pneumoniae in Gambian Villagers
Hill, P. C., Akisanya, A., Sankareh, K., Cheung, Y. B., Saaka, M., Lahai, G., Greenwood, B. M., & Adegbola, R. A. (2006) · Clinical Infectious Diseases · doi:10.1086/506941 · Cited by 170 · see citing works
Role of Pneumococcal Surface Protein C in Nasopharyngeal Carriage and Pneumonia and Its Ability To Elicit Protection against Carriage of Streptococcus pneumoniae
Balachandran, P., Brooks-Walter, A., Virolainen-Julkunen, A., Hollingshead, S. K., & Briles, D. E. (2002) · Infection and Immunity · doi:10.1128/iai.70.5.2526-2534.2002 · Cited by 168 · see citing works
Cold Spring Harbor
Hughes, R. C. (2014) · Arcadia Pub. eBooks · Cited by 164 · see citing works
Isolation of Streptococcus pneumoniae Biofilm Mutants and Their Characterization during Nasopharyngeal Colonization
Muñoz‐Elías, E. J., Marcano, J., & Camilli, A. (2008) · Infection and Immunity · doi:10.1128/iai.00425-08 · Cited by 153 · see citing works
Sialic Acid: A Preventable Signal for Pneumococcal Biofilm Formation, Colonization, and Invasion of the Host
Trappetti, C., Kadioglu, A., Carter, M., Hayre, J. K., Iannelli, F., Pozzi, G., Andrew, P. W., & Oggioni, M. R. (2009) · The Journal of Infectious Diseases · doi:10.1086/598483 · Cited by 152 · see citing works
Global Transcriptional Analysis of clpP Mutations of Type 2 Streptococcus pneumoniae and Their Effects on Physiology and Virulence
Robertson, G. T., Ng, W., Foley, J., Gilmour, R., & Winkler, M. E. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.13.3508-3520.2002 · Cited by 150 · see citing works
Identifying the interaction between influenza and pneumococcal pneumonia using incidence data.
Shrestha, S., Foxman, B., Weinberger, D. M., Steiner, C., Viboud, C., & Rohani, P. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005982 · Cited by 148 · see citing works
Pneumococcal Interactions with Epithelial Cells Are Crucial for Optimal Biofilm Formation and Colonization In Vitro and In Vivo
Marks, L. R., Parameswaran, G. I., & Håkansson, A. (2012) · Infection and Immunity · doi:10.1128/iai.00488-12 · Cited by 145 · see citing works
Self-citation
Phenotypic Characterization ofStreptococcus pneumoniaeBiofilm Development
Allegrucci, M., Hu, F. Z., Shen, K., Hayes, J., Ehrlich, G. D., Post, J. C., & Sauer, K. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.7.2325-2335.2006 · Cited by 141 · see citing works
The LuxS-Dependent Quorum-Sensing System Regulates Early Biofilm Formation by Streptococcus pneumoniae Strain D39
Vidal, J. E., Ludewick, H. P., Kunkel, R., Zähner, D., & Klugman, K. P. (2011) · Infection and Immunity · doi:10.1128/iai.05186-11 · Cited by 140 · see citing works
Quantitative Subcellular Proteome and Secretome Profiling of Influenza A Virus-Infected Human Primary Macrophages
Lietzén, N., Öhman, T., Rintahaka, J., Julkunen, I., Aittokallio, T., Matikainen, S., & Nyman, T. A. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1001340 · Cited by 137 · see citing works
Impact of the 2009 influenza pandemic on pneumococcal pneumonia hospitalizations in the United States.
Weinberger, D. M., Simonsen, L., Jordan, R., Steiner, C., Miller, M., & Viboud, C. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir749 · Cited by 132 · see citing works
Cutting Edge: Sympathetic Nervous System Increases Proinflammatory Cytokines and Exacerbates Influenza A Virus Pathogenesis
Grebe, K. M., Takeda, K., Hickman, H. D., Bailey, A. M., Embry, A. C., Bennink, J. R., & Yewdell, J. W. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903395 · Cited by 130 · see citing works
The Prevalence and Risk Factors for Pneumococcal Colonization of the Nasopharynx among Children in Kilifi District, Kenya
Abdullahi, O. A., Karani, A., Tigoi, C., Mugo, D., Kungu, S., Wanjiru, E., Jomo, J., Musyimi, R., Lipsitch, M., & Scott, J. A. G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030787 · Cited by 118 · see citing works
LuxS Mediates Iron-Dependent Biofilm Formation, Competence, and Fratricide in Streptococcus pneumoniae
Trappetti, C., Potter, A. J., Paton, A. W., Oggioni, M. R., & Paton, J. C. (2011) · Infection and Immunity · doi:10.1128/iai.05644-11 · Cited by 117 · see citing works
Identification of adenoid biofilms with middle ear pathogens in otitis-prone children utilizing SEM and FISH
Hoa, M., Tomovic, S., Nistico, L., et al. (2009) · International Journal of Pediatric Otorhinolaryngology · doi:10.1016/j.ijporl.2009.05.016 · Cited by 111 · see citing works
Streptococcus pneumoniae in Biofilms Are Unable to Cause Invasive Disease Due to Altered Virulence Determinant Production
Sánchez, C. J., Kumar, N., Lizcano, A., Shivshankar, P., Hotopp, J. C. D., Jorgensen, J. H., Tettelin, H., & Orihuela, C. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028738 · Cited by 110 · see citing works
Association of Nasopharyngeal Bacterial Colonization during Upper Respiratory Tract Infection and the Development of Acute Otitis Media
Revai, K., Mamidi, D. K., & Chonmaitree, T. (2008) · Clinical Infectious Diseases · doi:10.1086/525856 · Cited by 107 · see citing works
Streptococcus pneumoniae Biofilm Formation Is Strain Dependent, Multifactorial, and Associated with Reduced Invasiveness and Immunoreactivity during Colonization
Blanchette, K. A., Hinojosa, C. A., Babu, R. A. S., Lizcano, A., González-Juarbe, N., Muñoz‐Almagro, C., Sánchez, C. J., Bergman, M. A., & Orihuela, C. J. (2013) · mBio · doi:10.1128/mbio.00745-13 · Cited by 104 · see citing works
Sucrose metabolism contributes to in vivo fitness of Streptococcus pneumoniae
Iyer, R., & Camilli, A. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05878.x · Cited by 102 · see citing works
A simple method for directional transcriptome sequencing using Illumina technology
Croucher, N. J., Fookes, M. C., Perkins, T. T., Turner, D., Marguerat, S., Keane, T., Quail, M. A., He, M., Assefa, S., Bähler, J., et al. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp811 · Cited by 102 · see citing works
Activation of P2X7 Receptor by ATP Plays an Important Role in Regulating Inflammatory Responses during Acute Viral Infection
Lee, B. H., Hwang, D. M., Palaniyar, N., Grinstein, S., Philpott, D. J., & Hu, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035812 · Cited by 102 · see citing works
Coinfection withHaemophilus influenzaePromotes Pneumococcal Biofilm Formation during Experimental Otitis Media and Impedes the Progression of Pneumococcal Disease
Weimer, K. E. D., Armbruster, C. E., Juneau, R. A., Hong, W., Pang, B., & Swords, W. E. (2010) · The Journal of Infectious Diseases · doi:10.1086/656046 · Cited by 102 · see citing works
Early acquisition and high nasopharyngeal co-colonisation by Streptococcus pneumoniae and three respiratory pathogens amongst Gambian new-borns and infants
Kwambana-Adams, B., Barer, M. R., Bottomley, C., Adegbola, R. A., & Antonio, M. (2011) · BMC Infectious Diseases · doi:10.1186/1471-2334-11-175 · Cited by 95 · see citing works
Paracytosis of Haemophilus influenzae through cell layers of NCI-H292 lung epithelial cells
van Schilfgaarde, M., van Alphen, L., Eijk, P. P., Everts, V. E., & Dankert, J. (1995) · Infection and Immunity · doi:10.1128/iai.63.12.4729-4737.1995 · Cited by 91 · see citing works
Activation of P2X7-mediated apoptosis Inhibits DMBA/TPA-induced formation of skin papillomas and cancer in mice
Fu, W., McCormick, T., Qi, X., Luo, L., Zhou, L., Li, X., Wang, B.-C., Gibbons, H. E., Abdul‐Karim, F. W., & Gorodeski, G. I. (2009) · BMC Cancer · doi:10.1186/1471-2407-9-114 · Cited by 85 · see citing works
Pneumococcal carbohydrate transport: food for thought
Buckwalter, C. M., & King, S. J. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.08.008 · Cited by 76 · see citing works
Identification of Genes That Contribute to the Pathogenesis of Invasive Pneumococcal Disease by In Vivo Transcriptomic Analysis
Ogunniyi, A. D., Mahdi, L. K., Trappetti, C., Verhoeven, N., Mermans, D., der Hoek, M. B. V., Plumptre, C. D., & Paton, J. C. (2012) · Infection and Immunity · doi:10.1128/iai.00295-12 · Cited by 69 · see citing works
Sialic Acid Transport Contributes to Pneumococcal Colonization
Marion, C., Burnaugh, A. M., Woodiga, S. A., & King, S. J. (2010) · Infection and Immunity · doi:10.1128/iai.00832-10 · Cited by 69 · see citing works
Coupled Nucleotide and Mucin Hypersecretion from Goblet-Cell Metaplastic Human Airway Epithelium
Okada, S. F., Zhang, L., Kreda, S. M., Abdullah, L. H., Davis, C. W., Pickles, R. J., Lazarowski, E. R., & Boucher, R. C. (2010) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2010-0253oc · Cited by 65 · see citing works
Extracellular Matrix Formation Enhances the Ability of Streptococcus pneumoniae to Cause Invasive Disease
Trappetti, C., Ogunniyi, A. D., Oggioni, M. R., & Paton, J. C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019844 · Cited by 64 · see citing works
Invasive Bacterial Infections in Relation to Influenza Outbreaks, 2006–2010
Tasher, D., Stein, M., Simões, E. A. F., Shohat, T., Bromberg, M., & Somekh, E. (2011) · Clinical Infectious Diseases · doi:10.1093/cid/cir726 · Cited by 62 · see citing works
Identification of a novel pneumococcal vaccine antigen preferentially expressed during meningitis in mice
Mahdi, L. K., Wang, H., der Hoek, M. B. V., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci45850 · Cited by 55 · see citing works
Role of Dihydrolipoamide Dehydrogenase in Regulation of Raffinose Transport in Streptococcus pneumoniae
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Li, G., Hu, F. Z., Yang, X., et al. (2012) · Journal of Bacteriology · doi:10.1128/jb.00363-12 · Cited by 22 · see citing works
HPLC simultaneous determination of glycerol and mannitol in human tissues for forensic analysis
Kiyoshima, A., Kudo, K., Nishida, N., et al. (2002) · Forensic Science International · doi:10.1016/s0379-0738(01)00624-7 · Cited by 21 · see citing works
Proteomic analysis of protein expression in Streptococcus pneumoniae in response to temperature shift.
Lee, M., Bae, S., Kim, T., et al. (2006) · PubMed · Cited by 18 · see citing works
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Coles, C. L., Labrique, A. B., Saha, S. K., Ali, H., Al‐Emran, H. M., Rashid, M., Christian, P. S., & West, K. P. (2011) · Journal of Nutrition · doi:10.3945/jn.111.141622 · Cited by 16 · see citing works

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Authors: Pettigrew, M. M., Marks, L. R., Kong, Y., Gent, J. F., Roche-Hakansson, H., & Hakansson, A. P.
Affiliations: Yale University (US)
University at Buffalo, State University of New York (US)
W. M. Keck Foundation (US)
Department of Microbiology and Immunology, University at Buffalo, State University of New York, Buffalo, New York, USA
ORCID: Pettigrew, Melinda M.
Marks, Laura R.
Kong, Yong
Venue: Infection and Immunity
Publisher: American Society for Microbiology
Published: 2014-11
Volume: 82
Issue: 11
Pages: 4607-4619
ISSN: 0019-9567 (ISSN-L)
1098-5522
DOI: 10.1128/iai.02225-14
PMC: PMC4249342
OpenAlex: W2317658790
Cited by: 110
References: 85
Citations by year: 2026: 3 · 2025: 9 · 2024: 6 · 2023: 8 · 2022: 12 · 2021: 14 · 2020: 11 · 2019: 9 · 2018: 11 · 2017: 8 · 2016: 10 · 2015: 7 · 2014: 2
FWCI: 3.69
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Infection and Immunity (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Lund University Publications (Lund University) (submittedVersion)
Funders: National Institutes of Health (UL1TR000142)
National Institute on Deafness and Other Communication Disorders (R21DC011667, R01DC013554)
National Institute of General Medical Sciences (T32GM099607)
National Center for Advancing Translational Sciences
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
Keywords: Streptococcus pneumoniae, biofilm dispersal, influenza A virus, pneumococcal virulence, transcriptome, invasive pneumococcal disease, nasopharyngeal carriage, extracellular ATP, fever, carbohydrate metabolism, bacteriocins, competence, fratricide, bacterioplankton, host-pathogen interaction
MeSH terms: Animals, Epithelial Cells, Humans, Mice, Inbred BALB C, Orthomyxoviridae Infections, Influenza A virus, Pneumococcal Infections, Streptococcus pneumoniae, Biofilms, Sepsis, Reverse Transcriptase Polymerase Chain Reaction, Cell Line, Tumor, Mice

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Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection

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