Transcriptional and proteomic characterization of telomere-induced senescence in a human alveolar epithelial cell line
Open accessAbstract
Cellular senescence due to telomere dysfunction has been hypothesized to play a role in age-associated diseases including idiopathic pulmonary fibrosis (IPF). It has been postulated that paracrine mediators originating from senescent alveolar epithelia signal to surrounding mesenchymal cells and contribute to disease pathogenesis. However, murine models of telomere-induced alveolar epithelial senescence fail to display the canonical senescence-associated secretory phenotype (SASP) that is observed in senescent human cells. In an effort to understand human-specific responses to telomere dysfunction, we modeled telomere dysfunction-induced senescence in a human alveolar epithelial cell line. We hypothesized that this system would enable us to probe for differences in transcriptional and proteomic senescence pathways in vitro and to identify novel secreted protein (secretome) changes that potentially contribute to the pathogenesis of IPF. Following induction of telomere dysfunction, a robust senescence phenotype was observed. RNA-seq analysis of the senescent cells revealed the SASP and comparisons to previous murine data highlighted differences in response to telomere dysfunction. We conducted a proteomic analysis of the senescent cells using a novel biotin ligase capable of labeling secreted proteins. Candidate biomarkers selected from our transcriptional and secretome data were then evaluated in IPF and control patient plasma. Four novel proteins were found to be differentially expressed between the patient groups: stanniocalcin-1, contactin-1, tenascin C, and total inhibin. Our data show that human telomere-induced, alveolar epithelial senescence results in a transcriptional SASP that is distinct from that seen in analogous murine cells. Our findings suggest that studies in animal models should be carefully validated given the possibility of species-specific responses to telomere dysfunction. We also describe a pragmatic approach for the study of the consequences of telomere-induced alveolar epithelial cell senescence in humans.
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Multiplexed antibody-based imaging technologies such as imaging mass cytometry and CODEX can detect 20-50 selected genes simultaneously in each cell at the protein level, complementing transcript-based detection especially given the potential for poor correlation of transcriptomic and proteomic data sets in senescent cells.
“For example, multiplexed antibody-based imaging (mABI) technologies such as imaging mass cytometry (IMC) [31] and codetection by indexing (CODEX) [32] can detect 20–50 selected genes simultaneously in each cell at the protein level, which is a useful complement to transcript-based detection – especially given the potential for poor correlation of transcriptomic and proteomic data sets implicated”
From The heterogeneity of cellular senescence: insights at the single-cell level (2023) · cites this paper as [33]
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- Authors
- Sullivan, D. I., Jiang, M., Hinchie, A. M., Roth, M. G., Bahudhanapati, H., Nouraie, M., Liu, J., McDyer, J. F., Mallampalli, R. K., Zhang, Y., Kass, D. J., Finkel, T., & Alder, J. K.
- Affiliations
- University of Pittsburgh (US)
- Central South University (CN)
- The Ohio State University (US)
- Corresponding author
- Alder, Jonathan K.
- ORCID
- Venue
- Frontiers in Medicine
- Publisher
- Frontiers Media SA
- Published
- 2021-02-09
- Volume
- 8
- Pages
- 600626-600626
- ISSN
- 2296-858X (ISSN-L)
- PMC
- PMC7902064
- OpenAlex
- W3128360456
- Cited by
- 16
- References
- 59
- Citations by year
- 2026: 5 · 2025: 3 · 2022: 7 · 2021: 1
- FWCI
- 1.26
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- journal article
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- en
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- PubMed Central (publishedVersion, cc-by)
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- Funders
- National Heart, Lung, and Blood Institute
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Interstitial Lung Diseases and Idiopathic Pulmonary Fibrosis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- telomere dysfunction, cellular senescence, alveolar epithelial cells, idiopathic pulmonary fibrosis, senescence-associated secretory phenotype, secretome, senescence biomarkers, stanniocalcin-1, contactin-1, tenascin-C, inhibin, paracrine signaling
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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