Cited by 283Telomeres, Telomerase, and SenescenceGenetics, Aging, and Longevity in Model OrganismsReproductive Biology and Fertility

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Effect of Cytotoxic Chemotherapy on Markers of Molecular Age in Patients With Breast Cancer

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Sanoff, Hanna K., Deal, Allison M., Krishnamurthy, Janakiraman, Torrice, Chad, Dillon, Patrick, Sorrentino, Jessica, Ibrahim, Joseph G., Jolly, Trevor A., Williams, Grant, Carey, Lisa A., Drobish, Amy, Gordon, Brittaney-Belle, Alston, Shani, Hurria, Arti, Kleinhans, Karin, Rudolph, K. Lenhard, Sharpless, Norman E., Muss, Hyman B.·2014·JNCI: Journal of the National Cancer Institute

DOI 10.1093/jnci/dju057PMC PMC3982894

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Abstract

BACKGROUND: Senescent cells, which express p16 (INK4a) , accumulate with aging and contribute to age-related pathology. To understand whether cytotoxic agents promote molecular aging, we measured expression of p16 (INK4a) and other senescence markers in breast cancer patients treated with adjuvant chemotherapy. METHODS: Blood and clinical information were prospectively obtained from 33 women with stage I to III breast cancer at four time points: before anthracycline-based chemotherapy, immediately after anthracycline-based chemotherapy, 3 months after anthracycline-based chemotherapy, and 12 months after anthracycline-based chemotherapy. Expression of senescence markers p16 (INK4a) and ARF mRNA was determined using TaqMan quantitative reverse-transcription polymerase chain reaction in CD3(+) T lymphocytes, telomere length was determined by Southern analysis, and senescence-associated cytokines were determined by enzyme-linked immunosorbent assay. Findings were independently assessed in a cross-sectional cohort of 176 breast cancer survivors enrolled a median of 3.4 years after treatment; 39% previously received chemotherapy. All statistical tests were two-sided. RESULTS: In prospectively analyzed patients, expression of p16 (INK4a) and ARF increased immediately after chemotherapy and remained elevated 12 months after treatment. Median increase in log2 p16 (INK4a) was 0.81 (interquartile range = 0.28-1.62; Wilcoxon signed-rank P < .001), or a 75% absolute increase in expression, equivalent to the increase observed over 14.7 years of chronological aging. ARF expression was comparably increased (P < .001). Increased expression of p16 (INK4a) and ARF was associated with dose-dense therapy and hematological toxicity. Expression of two senescence-associated cytokines (VEGFA and MCP1) was durably increased by adjuvant chemotherapy. Telomere length was not affected by chemotherapy. In a cross-sectional cohort, prior chemotherapy exposure was independently associated with a log2-increase in p16 (INK4a) expression of 0.57 (repeated measures model, P < .001), comparable with 10.4 years of chronological aging. CONCLUSIONS: Adjuvant chemotherapy for breast cancer is gerontogenic, inducing cellular senescence in vivo, thereby accelerating molecular aging of hematopoietic tissues.

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Authors: Sanoff, H. K., Deal, A. M., Krishnamurthy, J., Torrice, C., Dillon, P., Sorrentino, J., Ibrahim, J. G., Jolly, T. A., Williams, G., Carey, L. A., Drobish, A., Gordon, B.-B., Alston, S., Hurria, A., Kleinhans, K., Rudolph, K. L., Sharpless, N. E., & Muss, H. B.
Affiliations: University of North Carolina at Chapel Hill (US)
ORCID: Sanoff, Hanna K.
Deal, Allison M.
Dillon, Patrick
Sorrentino, Jessica
Ibrahim, Joseph G.
Jolly, Trevor A.
Williams, Grant
Alston, Shani
Hurria, Arti
Rudolph, K. Lenhard
Sharpless, Norman E.
Muss, Hyman B.
Venue: JNCI: Journal of the National Cancer Institute
Publisher: Oxford University Press (OUP)
Published: 2014-03-28
Volume: 106
Issue: 4
Pages: dju057-dju057
ISSN: 0027-8874 (ISSN-L)
1460-2105
DOI: 10.1093/jnci/dju057
PMC: PMC3982894
OpenAlex: W2126729859
Cited by: 283
References: 54
Citations by year: 2026: 16 · 2025: 20 · 2024: 26 · 2023: 24 · 2022: 35 · 2021: 34 · 2020: 31 · 2019: 15 · 2018: 20 · 2017: 17 · 2016: 19 · 2015: 18 · 2014: 8
FWCI: 13.74
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: JNCI Journal of the National Cancer Institute (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: Breast Cancer Research Foundation
Glenn Foundation for Medical Research
National Institutes of Health (2k12ca120780-16, 5r01ag024379-15, AG024379)
National Institute on Aging (AG024379)
National Cancer Institute (K12-CA120780, K07CA106722, P50CA058223, P30CA016086)
National Institute of Environmental Health Sciences (P30ES010126, T32ES007126)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
Keywords: breast cancer, cytotoxic chemotherapy, molecular aging, cellular senescence, p16INK4a, ARF, anthracycline chemotherapy, adjuvant chemotherapy, dose-dense chemotherapy, hematologic toxicity, VEGF-A, MCP-1, telomere length, T cells, hematopoietic tissue
MeSH terms: Adult, Aged, Animals, Antineoplastic Combined Chemotherapy Protocols, Breast Neoplasms, Cross-Sectional Studies, Female, Humans, Middle Aged, Neoplasm Staging, Prospective Studies, T-Lymphocytes, Biomarkers, Cytokines, Telomere, Cellular Senescence, Anthracyclines, Cyclin-Dependent Kinase Inhibitor p16, Reverse Transcriptase Polymerase Chain Reaction, ADP-Ribosylation Factors, Mice

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Effect of Cytotoxic Chemotherapy on Markers of Molecular Age in Patients With Breast Cancer

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