دورية أكاديمية

Urban Particles Elevated Streptococcus pneumoniae Biofilms, Colonization of the Human Middle Ear Epithelial Cells, Mouse Nasopharynx and Transit to the Middle Ear and Lungs.

التفاصيل البيبلوغرافية
العنوان: Urban Particles Elevated Streptococcus pneumoniae Biofilms, Colonization of the Human Middle Ear Epithelial Cells, Mouse Nasopharynx and Transit to the Middle Ear and Lungs.
المؤلفون: Yadav MK; Department of Biotechnology, Pachhunga University College, Mizoram Central University, Aizawl, Mizoram 796001, India.; Institute for Medical Device Clinical Trials, Korea University College of Medicine, Seoul, South Korea., Go YY; Department of Otorhinolaryngology-Head and Neck Surgery, Korea University College of Medicine, Seoul, South Korea., Jun I; Department of Otorhinolaryngology-Head and Neck Surgery, Korea University College of Medicine, Seoul, South Korea., Chae SW; Department of Otorhinolaryngology-Head and Neck Surgery, Korea University College of Medicine, Seoul, South Korea., Song JJ; Department of Otorhinolaryngology-Head and Neck Surgery, Korea University College of Medicine, Seoul, South Korea. jjsong23@gmail.com.
المصدر: Scientific reports [Sci Rep] 2020 Apr 06; Vol. 10 (1), pp. 5969. Date of Electronic Publication: 2020 Apr 06.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE
أسماء مطبوعة: Original Publication: London : Nature Publishing Group, copyright 2011-
مواضيع طبية MeSH: Air Pollutants*, Biofilms/*drug effects , Ear, Middle/*microbiology , Lung/*microbiology , Nasopharynx/*microbiology , Particulate Matter/*administration & dosage , Streptococcus pneumoniae/*drug effects, Animals ; Gene Expression Regulation, Bacterial/drug effects ; Humans ; Mice ; Quorum Sensing
مستخلص: Air-pollutants containing toxic particulate matters (PM) deposit in the respiratory tract and increases microbial infections. However, the mechanism by which this occurs is not well understood. This study evaluated the effect of urban particles (UP) on Streptococcus pneumoniae (pneumococcus) in vitro biofilm formation, colonization of human middle ear epithelium cells (HMEECs) as well as mouse nasal cavity and its transition to the middle ear and lungs. The in vitro biofilms and planktonic growth of S. pneumoniae were evaluated in metal ion free medium in the presence of UP. Biofilms were quantified by crystal violet (CV) microplate assay, colony forming unit (cfu) counts and resazurin staining. Biofilm structures were analyzed using a scanning electron microscope (SEM) and confocal microscopy (CM). Gene expressions of biofilms were evaluated using real time RT-PCR. Effects of UP exposure on S. pneumoniae colonization to HMEECs were evaluated using fluorescent in-situ hybridization (FISH), cell viability was detected using the Ezcyto kit, apoptosis in HMEECs were evaluated using Annexin-V/PI based cytometry analysis and reactive oxygen species (ROS) production were evaluated using the Oxiselect kit. Alteration of HMEECs gene expressions on UP exposure or pneumococci colonization was evaluated using microarray. In vivo colonization of pneumococci in the presence of UP and transition to middle ear and lungs were evaluated using an intranasal mice colonization model. The UP exposure significantly increased (*p < 0.05) pneumococcal in vitro biofilms and planktonic growth. In the presence of UP, pneumococci formed organized biofilms with a matrix, while in absence of UP bacteria were unable to form biofilms. The luxS, ply, lytA, comA, comB and ciaR genes involved in bacterial pathogenesis, biofilm formation and quorum sensing were up-regulated in pneumococci biofilms grown in the presence of UP. The HMEECs viability was significantly decreased (p < 0.05) and bacteria colonization was significantly elevated (p < 0.05) in co-treatment (UP + S. pneumoniae) when compared to single treatment. Similarly, increased apoptosis and ROS production were detected in HMEECs treated with UP + pneumococci. The microarray analysis of HMEECs revealed that the genes involve in apoptosis and cell death, inflammation, and immune response, were up-regulated in co-treatment and were unchanged or expressed in less fold in single treatments of UP or S. pneumoniae. The in vivo study showed an increased pneumococcal colonization of the nasopharynx in the presence of UP and a higher transition of bacteria to the middle ear and lungs in the presence of UP. The UP exposure elevated S. pneumoniae in vitro biofilm and colonization of HMEECs, and in vivo mouse nasopharyngeal colonization, and increased dissemination to mouse middle ear and lungs.
References: Kelly, F. J. & Fussell, C. Size, source and chemical composition as determinants of toxicity attributable to ambient particulate matter. Atmos. Environ. 60, 504–526 (2012). (PMID: 10.1016/j.atmosenv.2012.06.039)
Thurston, G. & Lippmann, M. Ambient particulate matter air pollution and cardiopulmonary diseases. Semin. Respir. Crit. Care Med. 36, 422–432 (2015). (PMID: 10.1055/s-0035-1549455)
Xu, Q. et al. Fine Particulate Air Pollution and Hospital Emergency Room Visits for Respiratory Disease in Urban Areas in Beijing, China, in 2013. PLoS One 11, e0153099–e0153099, https://doi.org/10.1371/journal.pone.0153099 (2016). (PMID: 10.1371/journal.pone.0153099270545824824441)
Vijayan, V. K., Paramesh, H., Salvi, S. S. & Dalal, A. A. K. Enhancing indoor air quality -The air filter advantage. Lung India 32, 473–479 (2015). (PMID: 10.4103/0970-2113.164174)
Nel, A. Air Pollution-Related Illness: Effects of Particles. Science. 308, 804–806 (2005). (PMID: 10.1126/science.1108752)
Valavanidis, A., Fiotakis, K. & Vlachogianni, T. Airborne Particulate Matter and Human Health: Toxicological Assessment and Importance of Size and Composition of Particles for Oxidative Damage and Carcinogenic Mechanisms. J. Env. Sci. Health, Part. C. 26, 339–362 (2008). (PMID: 10.1080/10590500802494538)
Baskaran, V., Murray, R. L., Hunter, A., Lim, W. S. & McKeever, T. M. Effect of tobacco smoking on the risk of developing community acquired pneumonia: A systematic review and meta-analysis. PLoS One. 14, e0220204, https://doi.org/10.1371/journal.pone.0220204 (2019). (PMID: 10.1371/journal.pone.0220204313189676638981)
Cheng, M.-H., Chiu, H.-F. & Yang, C.-Y. Coarse Particulate Air Pollution Associated with Increased Risk of Hospital Admissions for Respiratory Diseases in a Tropical City, Kaohsiung, Taiwan. Int. J. Env. Res. Public. Health. 12, 13053–13068 (2015). (PMID: 10.3390/ijerph121013053)
Medina-Ramón, M., Zanobetti, A. & Schwartz, J. The Effect of Ozone and PM10 on Hospital Admissions for Pneumonia and Chronic Obstructive Pulmonary Disease: A National Multicity Study. Am. J. Epidemiol. 163, 579–588 (2006). (PMID: 10.1093/aje/kwj078)
Nuorti, J. P. et al. Cigarette Smoking and Invasive Pneumococcal Disease. N. Engl. J. Med. 342, 681–689 (2000). (PMID: 10.1056/NEJM200003093421002)
Ghio, A. J. Particle exposures and infections. Infect. Immun. 42, 459–467 (2014). (PMID: 10.1007/s15010-014-0592-6)
Greenberg, D. et al. The Contribution of Smoking and Exposure to Tobacco Smoke to Streptococcus pneumoniae and Haemophilus influenzae Carriage in Children and Their Mothers. Clin. Infect. Dis. 42, 897–903 (2006). (PMID: 10.1086/500935)
Wahl, B. et al. Burden of Streptococcus pneumoniae and Haemophilus influenzae type b disease in children in the era of conjugate vaccines: global, regional, and national estimates for 2000-15. Lancet. Glob. Health. 6, e744–e757, https://doi.org/10.1016/S2214-109X(18)30247-X (2018). (PMID: 10.1016/S2214-109X(18)30247-X)
Yu, Y. Y. et al. Epidemiological characteristics of nasopharyngeal Streptococcus pneumoniae strains among children with pneumonia in Chongqing, China. Sci. Rep. 9, 3324, https://doi.org/10.1038/s41598-019-40088-6 (2019). (PMID: 10.1038/s41598-019-40088-6308248116397308)
Chao, Y., Marks, L. R., Pettigrew, M. M. & Hakansson, A. P. Streptococcus pneumoniae biofilm formation and dispersion during colonization and disease. Front. Cell Infect. Microbiol. 4, 194–194, https://doi.org/10.3389/fcimb.2014.00194 (2015). (PMID: 10.3389/fcimb.2014.00194256290114292784)
Kadioglu, A., Weiser, J. N., Paton, J. C. & Andrew, P. W. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6, 288, https://doi.org/10.1038/nrmicro1871 (2008). (PMID: 10.1038/nrmicro187118340341)
Becker, S. S. J. Exposure to urban air particulates alters the macrophage-mediated inflammatory response to respiratory viral infection. J. Toxicol. Env. Health A. 57, 445–457 (1999). (PMID: 10.1080/009841099157539)
Zelikoff, J. T., Schermerhorn, K. R., Fang, K., Cohen, M. D. & Schlesinger, R. B. A role for associated transition metals in the immunotoxicity of inhaled ambient particulate matter. Env. Health Perspect. 110(5), 871–875 (2002). (PMID: 10.1289/ehp.02110s5871)
Im, G. J., Park, M. K. & Song, J.-J. Effect of urban particles on human middle ear epithelial cells. Int. J. Pediatr. Otorhinolaryngol. 78, 777–781 (2014). (PMID: 10.1016/j.ijporl.2014.02.008)
Park, M. et al. Air pollution influences the incidence of otitis media in children: A national population-based study. PLOS One. 13, e0199296, https://doi.org/10.1371/journal.pone.0199296 (2018). (PMID: 10.1371/journal.pone.0199296299534846023207)
Park, M. K., Chae, S. W., Kim, H.-B., Cho, J. G. & Song, J.-J. Middle ear inflammation of rat induced by urban particles. Int. J. Pediatr. Otorhinolaryngol. 78, 2193–2197 (2014). (PMID: 10.1016/j.ijporl.2014.10.011)
Avery, O. T., Macleod, C. M. & McCarty, M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79, 137–158 (1944). (PMID: 10.1084/jem.79.2.137)
LeMessurier, K. S., Ogunniyi, A. D. & Paton, J. C. Differential expression of key pneumococcal virulence genes in vivo. Microbiology. 152, 305–311 (2006). (PMID: 10.1099/mic.0.28438-0)
Yadav, M. K. et al. The LuxS/AI-2 Quorum-Sensing System of Streptococcus pneumoniae Is Required to Cause Disease, and to Regulate Virulence- and Metabolism-Related Genes in a Rat Model of Middle Ear Infection. Front. Cell Infect. Microbiol. 8, 138–138, https://doi.org/10.3389/fcimb.2018.00138 (2018). (PMID: 10.3389/fcimb.2018.00138297807505945837)
Brown, L. R. et al. Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae. Front. Cell Infect. Microbiol. 7, 233–233 (2017). (PMID: 10.3389/fcimb.2017.00233)
Christensen, G. D. et al. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J. Clin. Microbiol. 22, 996–1006 (1985). (PMID: 10.1128/JCM.22.6.996-1006.1985)
Yadav, M. K., Go, Y. Y., Kim, S. H., Chae, S.-W. & Song J.-J. Antimicrobial and Antibiofilm Effects of Human Amniotic/Chorionic Membrane Extract on Streptococcus pneumoniae. Front Microbiol. 8, https://doi.org/10.3389/fmicb.2017.01948 (2017).
Malic, S. et al. Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA FISH). Microbiol. 155, 2603–2611 (2009). (PMID: 10.1099/mic.0.028712-0)
Rocha, R., Almeida, C. & Azevedo, N. F. Influence of the fixation/permeabilization step on peptide nucleic acid fluorescence in situ hybridization (PNA-FISH) for the detection of bacteria. PLoS One. 13, e0196522, https://doi.org/10.1371/journal.pone.0196522 (2018). (PMID: 10.1371/journal.pone.0196522298519615979007)
Affymetrix GeneChip. Expression analysis technical manual. Santa Clara, CA: Affymetrix, (2001).
Hussey, S. J. K. et al. Air pollution alters Staphylococcus aureus and Streptococcus pneumoniae biofilms, antibiotic tolerance and colonisation. Env. Microbiol. 19, 1868–1880 (2017). (PMID: 10.1111/1462-2920.13686)
McCool, T. L. & Weiser, J. N. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect. Immun. 72, 5807–5813, https://doi.org/10.1128/IAI.72.10.5807-5813.2004 (2004). (PMID: 10.1128/IAI.72.10.5807-5813.200415385481517579)
Puchta, A., Verschoor, C. P., Thurn, T. & Bowdish, D. M. E. Characterization of inflammatory responses during intranasal colonization with Streptococcus pneumoniae. J Vis Exp. e50490–e50490,; https://doi.org/10.3791/50490 (2014).
Trappetti, C., Potter, A. J., Paton, A. W., Oggioni, M. R. & Paton, J. C. LuxS Mediates Iron-Dependent Biofilm Formation, Competence, and Fratricide in Streptococcus pneumoniae. Infect. Immun. 79, 4550–4558, https://doi.org/10.1128/iai.05644-11 (2011). (PMID: 10.1128/iai.05644-11218759623257940)
Marks, L. R., Parameswaran, G. I. & Hakansson, A. P. Pneumococcal interactions with epithelial cells are crucial for optimal biofilm formation and colonization in vitro and in vivo. Infect. Immun. 80, 2744–2760, https://doi.org/10.1128/IAI.00488-12 (2012). (PMID: 10.1128/IAI.00488-12226452833434590)
Shen, P., Lees, J. A., Bee, G. C. W., Brown, S. P. & Weiser, J. N. Pneumococcal quorum sensing drives an asymmetric owner–intruder competitive strategy during carriage via the competence regulon. Nat. Microbiol. 4, 198–208 (2019). (PMID: 10.1038/s41564-018-0314-4)
Honsa, E., Johnson, M. & Rosch, J. The roles of transition metals in the physiology and pathogenesis of Streptococcus pneumoniae. Front Cell Infect Microbiol. 3, https://doi.org/10.3389/fcimb.2013.00092 (2013).
Rai, P., He, F., Kwang, J., Engelward, B. P. & Chow, V. T. K. Pneumococcal Pneumolysin Induces DNA Damage and Cell Cycle Arrest. Sci. Rep. 6, 22972, https://doi.org/10.1038/srep22972 (2016). (PMID: 10.1038/srep22972270265014812240)
Zahlten, J. et al. Streptococcus pneumoniae–Induced Oxidative Stress in Lung Epithelial Cells Depends on Pneumococcal Autolysis and Is Reversible by Resveratrol. J. Infect. Dis. 211, 1822–1830 (2015). (PMID: 10.1093/infdis/jiu806)
Vuong, N. Q. et al. In vitro toxicoproteomic analysis of A549 human lung epithelial cells exposed to urban air particulate matter and its water-soluble and insoluble fractions. Part. Fibre Toxicol. 14, 39, https://doi.org/10.1186/s12989-017-0220-6 (2017). (PMID: 10.1186/s12989-017-0220-6289696635625787)
Go, Y. Y. et al. Microarray Analysis of Gene Expression Alteration in Human Middle Ear Epithelial Cells Induced by Asian Sand Dust. Clin. Exp. Otorhinolaryngol. 8, 345–353 (2015). (PMID: 10.3342/ceo.2015.8.4.345)
Li, P. et al. Streptococcus pneumoniae Induces Autophagy through the Inhibition of the PI3K-I/Akt/mTOR Pathway and ROS Hypergeneration in A549 Cells. PLoS One. 10, e0122753, https://doi.org/10.1371/journal.pone.0122753 (2015). (PMID: 10.1371/journal.pone.0122753258030504372526)
Rai, P. et al. Streptococcus pneumoniae secretes hydrogen peroxide leading to DNA damage and apoptosis in lung cells. Proc. Natl. Acad. Sci. USA 112, E3421–E3430 (2015). (PMID: 10.1073/pnas.1424144112)
Ross, B. X. et al. IL-24 Promotes Pseudomonas aeruginosa Keratitis in C57BL/6 Mouse Corneas. J. Immunol. 198, 3536–3547 (2017). (PMID: 10.4049/jimmunol.1602087)
Sebastián, V. P. et al. Heme Oxygenase-1 as a Modulator of Intestinal Inflammation Development and Progression. Front. Immunol. 9, 1956, https://doi.org/10.3389/fimmu.2018.01956 (2018). (PMID: 10.3389/fimmu.2018.01956302584366143658)
Agard M., Asakrah S. & Morici L. PGE2 suppression of innate immunity during mucosal bacterial infection. Front Cell Infect Microbiol. 3, https://doi.org/10.3389/fcimb.2013.00045 (2013).
Lim, H. W., Pak, K., Kurabi, A. & Ryan, A. F. Lack of the hyaluronan receptor CD44 affects the course of bacterial otitis media and reduces leukocyte recruitment to the middle ear. BMC Immunol. 20, 20, https://doi.org/10.1186/s12865-019-0302-3 (2019). (PMID: 10.1186/s12865-019-0302-3312269446588864)
Candé, C., Cecconi, F., Dessen, P. & Kroemer, G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J. Cell Sci. 115, 4727–4734 (2002). (PMID: 10.1242/jcs.00210)
Krause, K. et al. CASP4/caspase-11 promotes autophagosome formation in response to bacterial infection. Autophagy. 14, 1928–1942 (2018). (PMID: 10.1080/15548627.2018.1491494)
Hagenbuchner, J. et al. FOXO3-induced reactive oxygen species are regulated by BCL2L11 (Bim) and SESN3. J. Cell Sci. 125, 1191–1203 (2012). (PMID: 10.1242/jcs.092098)
Liu, X. et al. The Role of the Notch Signal Pathway in Mucosal Cell Metaplasia in Mouse Acute Otitis Media. Sci. Rep. 7, 4588, https://doi.org/10.1038/s41598-017-04639-z (2017). (PMID: 10.1038/s41598-017-04639-z286767225496876)
Meyer, K. et al. Interferon-α inducible protein 6 impairs EGFR activation by CD81 and inhibits hepatitis C virus infection. Sci. Rep. 5, 9012, https://doi.org/10.1038/srep09012 (2015). (PMID: 10.1038/srep09012257575714355636)
Liu, X. et al. Flagellin-induced expression of CXCL10 mediates direct fungal killing and recruitment of NK cells to the cornea in response to Candida albicans infection. Eur. J. Immunol. 44, 2667–2679 (2014). (PMID: 10.1002/eji.201444490)
Yoon, G. S. et al. Interferon regulatory factor-1 in flagellin-induced reprogramming: potential protective role of CXCL10 in cornea innate defense against Pseudomonas aeruginosa infection. Invest. Ophthalmol. Vis. Sci. 54, 7510–7521 (2013). (PMID: 10.1167/iovs.13-12453)
Andrews, G. K. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem. Pharmacol. 59, 95–104 (2000). (PMID: 10.1016/S0006-2952(99)00301-9)
Xu, Q. L. et al. Fine Particulate Air Pollution and Hospital Emergency Room Visits for Respiratory Disease in Urban Areas in Beijing, China, in 2013. PLoS one 11, e0153099–e0153099, https://doi.org/10.1371/journal.pone.0153099 (2016). (PMID: 10.1371/journal.pone.0153099270545824824441)
Chen, X. et al. Urban particulate matter (PM) suppresses airway antibacterial defence. Respir. Res. 19, 5, https://doi.org/10.1186/s12931-017-0700-0 (2018). (PMID: 10.1186/s12931-017-0700-0293106425759166)
Hoa, M., Syamal, M., Sachdeva, L., Berk, R. & Coticchia, J. Demonstration of Nasopharyngeal and Middle Ear Mucosal Biofilms in an Animal Model of Acute Otitis Media. Ann. Otol, Rhinol. Laryngol. 118, 292–298, https://doi.org/10.1177/000348940911800410 (2009). (PMID: 10.1177/000348940911800410)
Reid, S. D. et al. Streptococcus pneumoniae Forms Surface-Attached Communities in the Middle Ear of Experimentally Infected Chinchillas. J. Infect. Dis. 199, 786–794 (2009). (PMID: 10.1086/597042)
Hall-Stoodley, L. et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA. 296, 202–211 (2006). (PMID: 10.1001/jama.296.2.202)
Sanchez, C. J. et al. The pneumococcal serine-rich repeat protein is an intra-species bacterial adhesin that promotes bacterial aggregation in vivo and in biofilms. PLoS Pathog. 6, e1001044–e1001044, https://doi.org/10.1371/journal.ppat.1001044 (2010). (PMID: 10.1371/journal.ppat.1001044207143502920850)
Shak, J. R., Vidal, J. E. & Klugman, K. P. Influence of bacterial interactions on pneumococcal colonization of the nasopharynx. Trends Microbiol. 21, 129–135 (2013). (PMID: 10.1016/j.tim.2012.11.005)
Weimer, K. E. et al. Coinfection with Haemophilus influenzae Promotes Pneumococcal Biofilm Formation during Experimental Otitis Media and Impedes the Progression of Pneumococcal Disease. J. Infect. Dis. 202, 1068–1075 (2010). (PMID: 10.1086/656046)
Brugha, R. & Grigg, J. Urban Air Pollution and Respiratory Infections. Paediatr. Respir. Rev. 15, 194–199 (2014). (PMID: 24704510)
المشرفين على المادة: 0 (Air Pollutants)
0 (Particulate Matter)
تواريخ الأحداث: Date Created: 20200407 Date Completed: 20201130 Latest Revision: 20210406
رمز التحديث: 20231215
مُعرف محوري في PubMed: PMC7136263
DOI: 10.1038/s41598-020-62846-7
PMID: 32249803
قاعدة البيانات: MEDLINE
الوصف
تدمد:2045-2322
DOI:10.1038/s41598-020-62846-7