DNA damage response (DDR) and senescence: shuttled inflamma-miRNAs on the stage of inflamm-aging

Olivieri, Fabiola; Albertini, Maria Cristina; Orciani, Monia; Ceka, Artan; Cricca, Monica; Procopio, Antonio Domenico; Bonafè, Massimiliano

doi:10.18632/oncotarget.5899

Cited by 163Telomeres, Telomerase, and SenescenceGenetics, Aging, and Longevity in Model OrganismsMicroRNA in disease regulation

DNA damage response (DDR) and senescence: shuttled inflamma-miRNAs on the stage of inflamm-aging

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Olivieri, Fabiola, Albertini, Maria Cristina, Orciani, Monia, Ceka, Artan, Cricca, Monica, Procopio, Antonio Domenico, Bonafè, Massimiliano·2015·Oncotarget

DOI 10.18632/oncotarget.5899PMC PMC4742121

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Abstract

// Fabiola Olivieri 1,2 , Maria Cristina Albertini 3 , Monia Orciani 1 , Artan Ceka 1 , Monica Cricca 4 , Antonio Domenico Procopio 1,2 and Massimiliano Bonafè 4 1 Department of Clinical and Molecular Sciences (DISCLIMO), Università Politecnica delle Marche, Ancona, Italy 2 Center of Clinical Pathology and Innovative Therapy, Italian National Research Center on Aging, INRCA-IRCCS, Ancona, Italy 3 Department of Biomolecular Sciences, Biochemistry and Molecular Biology, Università degli Studi di Urbino “Carlo Bo”, Urbino, Italy 4 Department of Experimental, Diagnostic and Specialty Medicine, DIMES, University of Bologna, Bologna, Italy Correspondence to: Fabiola Olivieri, email: // Keywords : microRNA, senescence-associated secretory phenotype, senescence, inflamm-aging, Gerotarget Received : June 18, 2015 Accepted : September 17, 2015 Published : September 29, 2015 Abstract A major issue in aging research is how cellular phenomena affect aging at the systemic level. Emerging evidence suggests that DNA damage response (DDR) signaling is a key mechanism linking DNA damage accumulation, cell senescence, and organism aging. DDR activation in senescent cells promotes acquisition of a proinflammatory secretory phenotype (SASP), which in turn elicits DDR and SASP activation in neighboring cells, thereby creating a proinflammatory environment extending at the local and eventually the systemic level. DDR activation is triggered by genomic lesions as well as emerging bacterial and viral metagenomes. Therefore, the buildup of cells with an activated DDR probably fuels inflamm-aging and predisposes to the development of the major age-related diseases (ARDs). Micro (mi)-RNAs - non-coding RNAs involved in gene expression modulation - are released locally and systemically by a variety of shuttles (exosomes, lipoproteins, proteins) that likely affect the efficiency of their biological effects. Here we suggest that some miRNAs, previously found to be associated with inflammation and senescence - miR-146, miR-155, and miR-21 - play a central role in the interplay among DDR, cell senescence and inflamm-aging. The identification of the functions of shuttled senescence-associated miRNAs is expected to shed light on the aging process and on how to delay ARD development.

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The SASP is a universal, dynamic, and complex phenomenon arising with cellular senescence and is the phenomenon of senescent cells secreting pro-inflammatory cytokines.
“The SASP, considered to be molecular inflammation, is a universal, dynamic, and complex phenomenon arising with cellular senescence. It is the phenomenon of senescent cells secreting pro-inflammatory cytokines.189”
From Inflammation and aging: signaling pathways and intervention therapies (2023) · cites this paper as [189]
The Introduction describes SASP as a secretory phenotype associated with senescence and lists pro-inflammatory mediators, including cytokines, among its components. It also describes SASP as an evolutionarily conserved program, but does not establish that it arises universally with cellular senescence or explicitly characterize it as dynamic. Its secretome includes more than cytokines. (LLM, conf=0.85)
Experimental — accuracy not yet measured
The DDR is lost in ageing in association with the accumulation of senescent cells and 'inflammaging'.
“Concomitantly, the DDR is lost in ageing in association with the accumulation of senescent cells and “inflammaging” [111, 150].”
From Early onset senescence and cognitive impairment in a murine model of repeated mTBI (2021) · cites this paper as [111]

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[30]Nelson G Wordsworth J Wang C Jurk D Lawless C Martin-Ruiz C von Zglinicki T A senescent cell bystander effect: senescence-induced senescence Aging Cell 2012 11 345 9 22321662 PMC3488292
[70]Bhaumik D Scott GK Schokrpur S Patil CK Orjalo AV Rodier F Lithgow GJ Campisi J MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8 Aging (Albany NY) 2009 1 402 411 20148189 PMC2818025
[104]Dellago H Preschitz-Kammerhofer B Terlecki-Zaniewicz L Schreiner C Fortschegger K Chang MW Hackl M Monteforte R Kühnel H Schosserer M Gruber F Tschachler E Scheideler M Freund A Orjalo AV Desprez PY Campisi J Inflammatory networks during cellular senescence: causes and consequences Trends Mol Med 2010 16 238 246 20444648 PMC2879478
[122]Vickers KC Remaley AT Lipid-based carriers of microRNAs and intercellular communication Curr Opin Lipidol 2012 23 91 7 22418571 PMC5570485

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Skin Senescence: Mechanisms and Impact on Whole-Body Aging
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Immunobiography and the heterogeneity of immune responses in the elderly: A focus on inflammaging and trained immunity
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Inflammation, Frailty and Cardiovascular Disease
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Human Inflammaging
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miR-21 and miR-146a: The microRNAs of inflammaging and age-related diseases
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Oxidative stress-induced premature senescence dysregulates VEGF and CFH expression in retinal pigment epithelial cells: Implications for Age-related Macular Degeneration
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SASP: Tumor Suppressor or Promoter? Yes!
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Anti-senescence compounds: A potential nutraceutical approach to healthy aging
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Emerging role of extracellular vesicles as a senescence-associated secretory phenotype: Insights into the pathophysiology of lung diseases
Kadota, T., Fujita, Y., Yoshioka, Y., Araya, J., Kuwano, K., & Ochiya, T. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.11.005 · Cited by 177 · see citing works
Exosome Determinants of Physiological Aging and Age-Related Neurodegenerative Diseases
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Immunosenescence and inflammaging: Mechanisms and role in diseases
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The Link between Chronic Stress and Accelerated Aging
Yegorov, Y. E., Poznyak, A. V., Nikiforov, N. G., Sobenin, I. A., & Orekhov, A. N. (2020) · Biomedicines · doi:10.3390/biomedicines8070198 · Cited by 147 · see citing works
POLD1: Central mediator of DNA replication and repair, and implication in cancer and other pathologies
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Extracellular Vesicles as New Players in Cellular Senescence
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Amnion-Epithelial-Cell-Derived Exosomes Demonstrate Physiologic State of Cell under Oxidative Stress
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Circulating miRNAs and miRNA shuttles as biomarkers: Perspective trajectories of healthy and unhealthy aging
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The Link Between Inflammaging and Degenerative Joint Diseases
Rezuş, E., Cardoneanu, A., Burlui, A., Luca, A., Codreanu, C., Tamba, B.-I., Stanciu, G. D., Dima, N., Badescu, C. M., & Rezuș, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030614 · Cited by 120 · see citing works
Long Noncoding RNAs and RNA‐Binding Proteins in Oxidative Stress, Cellular Senescence, and Age‐Related Diseases
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Regulation of lung epithelial cell senescence in smoking-induced COPD/emphysema by microR-125a-5p via Sp1 mediation of SIRT1/HIF-1a
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Microvesicles as Potential Biomarkers for the Identification of Senescence in Human Mesenchymal Stem Cells
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DNA Damage and Pulmonary Hypertension
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The role of myeloid-derived suppressor cells (MDSC) in the inflammaging process
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The Challenge by Multiple Environmental and Biological Factors Induce Inflammation in Aging: Their Role in the Promotion of Chronic Disease
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Extracellular vesicles and aging
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Radiation-Induced Bystander Effect is Mediated by Mitochondrial DNA in Exosome-Like Vesicles
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Cancer secretome and inflammation: The bright and the dark sides of NF-κB
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The aged extracellular matrix and the profibrotic role of senescence-associated secretory phenotype
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Exosome-based immunomodulation during aging: A nano-perspective on inflamm-aging
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Age-related bone diseases: Role of inflammaging
Bi, J., Zhang, C., Lu, C., Mo, C., Zeng, J., Yao, M., Jia, B., Liu, Z., Yuan, P., & Xu, S. (2024) · Journal of Autoimmunity · doi:10.1016/j.jaut.2024.103169 · Cited by 83 · see citing works
Inflammation-Accelerated Senescence and the Cardiovascular System: Mechanisms and Perspectives
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The impact of age-related syndromes on ICU process and outcomes in very old patients
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Bioactive Nutrients and Nutrigenomics in Age-Related Diseases
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Leukocyte telomere length and mortality risk in patients with type 2 diabetes
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Extracellular microRNAs and endothelial hyperglycaemic memory: a therapeutic opportunity?
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MicroRNAs and the metabolic hallmarks of aging
Victoria, B., López, Y. O. N., & Masternak, M. M. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.12.021 · Cited by 63 · see citing works
Sirt1 and Parp1 as epigenome safeguards and microRNAs as SASP-associated signals, in cellular senescence and aging
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MicroRNAs are critical regulators of senescence and aging in mesenchymal stem cells
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Senescence-associated extracellular vesicle release plays a role in senescence-associated secretory phenotype (SASP) in age-associated diseases
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Circulating markers of ageing and allostatic load: A slow train coming
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miR-29b overexpression induces cochlear hair cell apoptosis through the regulation of SIRT1/PGC-1α signaling: Implications for age-related hearing loss
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A prototypical non-malignant epithelial model to study genome dynamics and concurrently monitor micro-RNAs and proteins in situ during oncogene-induced senescence
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Immunosenescence: participation of T lymphocytes and myeloid-derived suppressor cells in aging-related immune response changes
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The RNA world of human ageing
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Applications of Exosomal miRNAs from Mesenchymal Stem Cells as Skin Boosters
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miR-592/WSB1/HIF-1α axis inhibits glycolytic metabolism to decrease hepatocellular carcinoma growth
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Secretome of Stem Cells: Roles of Extracellular Vesicles in Diseases, Stemness, Differentiation, and Reprogramming
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Exosomes and Micro-RNAs in Aging Process
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A genetic view of laryngeal cancer heterogeneity
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Extracellular Vesicles, Ageing, and Therapeutic Interventions
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Early onset senescence and cognitive impairment in a murine model of repeated mTBI
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Physical Activity Modulates the Overexpression of the Inflammatory miR‐146a‐5p in Obese Patients
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Targeting Premature Renal Aging: from Molecular Mechanisms of Cellular Senescence to Senolytic Trials
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The role of oxidative stress in intervertebral disc cellular senescence
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T cell senescence: a new perspective on immunotherapy in lung cancer
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Microglia in Neurodegenerative Events—An Initiator or a Significant Other?
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Prognostic Role of MicroRNAs in Human Non-Small-Cell Lung Cancer: A Systematic Review and Meta-Analysis
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Recent update on discovery and development of Hsp90 inhibitors as senolytic agents
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Role of Complement in Regulating Inflammation Processes in Renal and Prostate Cancers
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Resistance Training Diminishes the Expression of Exosome CD63 Protein without Modification of Plasma miR-146a-5p and cfDNA in the Elderly
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Inflammaging and Cannabinoids
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Effect of alcohol use disorder on cellular aging
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Targeting the p53-p21 axis in liver cancer: Linking cellular senescence to tumor suppression and progression
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Inflamm-aging microRNAs may integrate signals from food and gut microbiota by modulating common signalling pathways
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MicroRNA Profile of Exosomes and Parental Cells is Differently Affected by Ionizing Radiation
Abramowicz, A., Łabaj, W., Mika, J., Szołtysek, K., Ślęzak-Prochazka, I., Mielańczyk, Ł., Story, M. D., Pietrowska, M., Polański, A., & Widłak, P. (2020) · Radiation Research · doi:10.1667/rade-20-00007 · Cited by 29 · see citing works
Update of Immunosenescence in Cerebral Small Vessel Disease
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Ochratoxin A induced premature senescence in human renal proximal tubular cells
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Role of Inflammasomes in HIV-1 and Drug Abuse Mediated Neuroinflammaging
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Anti-Aging Potential of Platelet Rich Plasma (PRP): Evidence from Osteoarthritis (OA) and Applications in Senescence and Inflammaging
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Etoposide-induced DNA damage affects multiple cellular pathways in addition to DNA damage response
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Seminal Plasma and Seminal Plasma Exosomes of Aged Male Mice Affect Early Embryo Implantation via Immunomodulation
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How Diet Intervention via Modulation of DNA Damage Response through MicroRNAs May Have an Effect on Cancer Prevention and Aging, an in Silico Study
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The Interplay of Aging and PANoptosis in Osteoarthritis Pathogenesis: Implications for Novel Therapeutic Strategies
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Molecular Insights Into Withaferin-A-Induced Senescence: Bioinformatics and Experimental Evidence to the Role of NFκB and CARF
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l-Carnitine inhibits the senescence-associated secretory phenotype of aging adipose tissue by JNK/p53 pathway
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Identification and functional analysis of senescence-associated secretory phenotype of premature senescent hepatocytes induced by hexavalent chromium
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Senescence Phenomena and Metabolic Alteration in Mesenchymal Stromal Cells from a Mouse Model of Rett Syndrome
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Potential Nutrients from Natural and Synthetic Sources Targeting Inflammaging—A Review of Literature, Clinical Data and Patents
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Planar Proton Minibeam Irradiation Elicits Spatially Confined DNA Damage in a Human Epidermis Model
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The In Vitro Activity of Angelica archangelica L. Essential Oil on Inflammation
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Feprazone Mitigates IL-1β-Induced Cellular Senescence in Chondrocytes
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The Acute Effect of Multi-Ingredient Antioxidant Supplementation following Ionizing Radiation
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Decoding the secrets of longevity: unraveling nutraceutical and miRNA-Mediated aging pathways and therapeutic strategies
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Role of microRNAs in inflammaging and age related diseases
Giuliani, A. (2018) · Università Politecnica delle Marche (Università Politecnica delle Marche)

Authors: Olivieri, F., Albertini, M. C., Orciani, M., Ceka, A., Cricca, M., Procopio, A. D., & Bonafè, M.
Affiliations: Marche Polytechnic University (IT)
University of Urbino (IT)
Department of Clinical and Molecular Sciences (DISCLIMO), Università Politecnica delle Marche, Ancona, Italy
University of Bologna (IT)
Corresponding author: Olivieri, Fabiola
ORCID: Olivieri, Fabiola
Albertini, Maria Cristina
Orciani, Monia
Cricca, Monica
Procopio, Antonio Domenico
Bonafè, Massimiliano
Venue: Oncotarget
Publisher: Impact Journals, LLC
Published: 2015-09-29
Volume: 6
Issue: 34
Pages: 35509-35521
ISSN: 1949-2553 (ISSN-L)
DOI: 10.18632/oncotarget.5899
PMC: PMC4742121
OpenAlex: W2153079244
Cited by: 163
References: 146
Citations by year: 2026: 7 · 2025: 14 · 2024: 15 · 2023: 13 · 2022: 9 · 2021: 24 · 2020: 15 · 2019: 13 · 2018: 21 · 2017: 16 · 2016: 15 · 2015: 1
FWCI: 2.17
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: cc-by
Locations: Oncotarget (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, cc-by)
Università Politecnica delle Marche (Università Politecnica delle Marche) (submittedVersion)
CINECA IRIS Institutional Research information system (University of Urbino) (submittedVersion, cc-by-nc-nd)
Funders: Università Politecnica delle Marche
Topics: Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Keywords: DNA damage response, cellular senescence, inflammaging, senescence-associated secretory phenotype, microRNA, miR-146, miR-155, miR-21, exosomes, lipoproteins, age-related diseases, inflammation, systemic inflammation, non-coding RNA
MeSH terms: Aging, Animals, DNA Damage, Humans, Inflammation, Signal Transduction, Cellular Senescence, MicroRNAs

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DNA damage response (DDR) and senescence: shuttled inflamma-miRNAs on the stage of inflamm-aging

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