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Cellular senescence increases expression of bacterial ligands in the lungs and is positively correlated with increased susceptibility to pneumococcal pneumonia
Open accessAbstract
Summary: Cellular senescence is an age‐associated phenomenon that promotes tumor invasiveness owing to the secretion of proinflammatory cytokines, proteases, and growth factors. Herein we demonstrate that cellular senescence also potentially increases susceptibility to bacterial pneumonia caused by Streptococcus pneumoniae (the pneumococcus), the leading cause of infectious death in the elderly. Aged mice had increased lung inflammation as determined by cytokine analysis and histopathology of lung sections. Immunoblotting for p16, pRb, and mH2A showed that elderly humans and aged mice had increased levels of these senescence markers in their lungs vs. young controls. Keratin 10 (K10), laminin receptor (LR), and platelet‐activating factor receptor (PAFr), host proteins known to be co‐opted for bacterial adhesion, were also increased. Aged mice were found to be highly susceptible to pneumococcal challenge in a PsrP, the pneumococcal adhesin that binds K10, dependent manner. In vitro senescent A549 lung epithelial cells had elevated K10 and LR protein levels and were up to 5‐fold more permissive for bacterial adhesion. Additionally, exposure of normal cells to conditioned media from senescent cells doubled PAFr levels and pneumococcal adherence. Genotoxic stress induced by bleomycin and oxidative stress enhanced susceptibility of young mice to pneumonia and was positively correlated with enhanced p16, inflammation, and LR levels. These findings suggest that cellular senescence facilitates bacterial adhesion to cells in the lungs and provides an additional molecular mechanism for the increased incidence of community‐acquired pneumonia in the elderly. This study is the first to suggest a second negative consequence for the senescence‐associated secretory phenotype.
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“Further, age-associated changes in genomic instability, telomere shortening, epigenetic alterations, cellular senescence, impaired autophagy, and mitochondrial dysfunction may promote IPF development and progression (3, 12, 62, 84, 88, 89, 116, 145).”
From Aging and Lung Disease (2020) · cites this paper as [62]
Experimental — accuracy not yet measuredIn the citing paper
“Bacteria, especially Streptococcus pneumoniae, are the most common pathogens that commonly cause CAP in the elderly (62).”
From Aging and Lung Disease (2020) · cites this paper as [62]
In the citing paper
“Age-associated alterations in immune surveillance, specifically decreased innate and adaptive immune responses, and dysfunctional immune response regulation can be responsible for increased lung pathology in response to infectious stimuli (3, 62, 106, 110, 114, 135).”
From Aging and Lung Disease (2020) · cites this paper as [62]
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“Upregulation of epithelial cell surface receptors in response to chronic inflammation increases bacterial adhesion and accumulation in the aged lung and correlates with susceptibility to pneumonia (62, 97).”
From Aging and Lung Disease (2020) · cites this paper as [62]
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Metadata
- Authors
- Shivshankar, P., Boyd, A. R., Le Saux, C. J., Yeh, I., & Orihuela, C. J.
- Affiliations
- The University of Texas at San Antonio Health Science Center (US)
- Corresponding author
- Orihuela, Carlos J.
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2011-06-14
- Volume
- 10
- Issue
- 5
- Pages
- 798-806
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC3173515
- OpenAlex
- W1569854985
- Cited by
- 117
- References
- 37
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 10 · 2023: 9 · 2022: 4 · 2021: 14 · 2020: 6 · 2019: 6 · 2018: 8 · 2017: 6 · 2016: 5 · 2015: 8 · 2014: 9 · 2013: 15 · 2012: 7
- FWCI
- 7.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Aging Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (AG092313, R21AG029313, AG033274, R21AG033274)
- National Institute of Allergy and Infectious Diseases (R01AI078972, AI078972)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- cellular senescence, pneumococcal pneumonia, Streptococcus pneumoniae, bacterial adhesion, keratin 10, laminin receptor, platelet-activating factor receptor, senescence-associated secretory phenotype, lung inflammation, p16, oxidative stress, genotoxic stress, aged mice, bacterial ligands
- MeSH terms
- Adult, Age Factors, Aged, Aged, 80 and over, Aging, Animals, Bacterial Adhesion, Bleomycin, Disease Susceptibility, Female, Humans, Immunohistochemistry, Inflammation, Lung, Mice, Inbred BALB C, Middle Aged, Pneumonia, Pneumococcal, Streptococcus pneumoniae, Immunoblotting, Biomarkers, Cytokines, Cellular Senescence, Receptors, Laminin, Oxidative Stress, Cell Line, Tumor, Mice, Kaplan-Meier Estimate, Keratin-10
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