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      The hallmarks of aging as a conceptual framework for health and longevity research

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          Abstract

          The inexorability of the aging process has sparked the curiosity of human beings since ancient times. However, despite this interest and the extraordinary scientific advances in the field, the complexity of the process has hampered its comprehension. In this context, The Hallmarks of Aging were defined in 2013 with the aim of establishing an organized, systematic and integrative view of this topic, which would serve as a conceptual framework for aging research. Ten years later and promoted by the progress in the area, an updated version included three new hallmarks while maintaining the original scope. The aim of this review is to determine to what extent The Hallmarks of Aging achieved the purpose that gave rise to them. For this aim, we have reviewed the literature citing any of the two versions of The Hallmarks of Aging and conclude that they have served as a conceptual framework not only for aging research but also for related areas of knowledge. Finally, this review discusses the new candidates to become part of the Hallmarks list, analyzing the evidence that supports whether they should or should not be incorporated.

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          The Hallmarks of Aging

          Carlos López-Otín, Maria Blasco, Linda Partridge … (2014)
          Aging is characterized by a progressive loss of physiological integrity, leading to impaired function and increased vulnerability to death. This deterioration is the primary risk factor for major human pathologies, including cancer, diabetes, cardiovascular disorders, and neurodegenerative diseases. Aging research has experienced an unprecedented advance over recent years, particularly with the discovery that the rate of aging is controlled, at least to some extent, by genetic pathways and biochemical processes conserved in evolution. This Review enumerates nine tentative hallmarks that represent common denominators of aging in different organisms, with special emphasis on mammalian aging. These hallmarks are: genomic instability, telomere attrition, epigenetic alterations, loss of proteostasis, deregulated nutrient sensing, mitochondrial dysfunction, cellular senescence, stem cell exhaustion, and altered intercellular communication. A major challenge is to dissect the interconnectedness between the candidate hallmarks and their relative contributions to aging, with the final goal of identifying pharmaceutical targets to improve human health during aging, with minimal side effects. Copyright © 2013 Elsevier Inc. All rights reserved.
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            The Hallmarks of Cancer

            Douglas Hanahan, Robert Weinberg (2000)
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              Ageing as a risk factor for neurodegenerative disease

              Yujun Hou, Xiuli Dan, Mansi Babbar … (2019)
              Ageing is the primary risk factor for most neurodegenerative diseases, including Alzheimer disease (AD) and Parkinson disease (PD). One in ten individuals aged ≥65 years has AD and its prevalence continues to increase with increasing age. Few or no effective treatments are available for ageing-related neurodegenerative diseases, which tend to progress in an irreversible manner and are associated with large socioeconomic and personal costs. This Review discusses the pathogenesis of AD, PD and other neurodegenerative diseases, and describes their associations with the nine biological hallmarks of ageing: genomic instability, telomere attrition, epigenetic alterations, loss of proteostasis, mitochondrial dysfunction, cellular senescence, deregulated nutrient sensing, stem cell exhaustion and altered intercellular communication. The central biological mechanisms of ageing and their potential as targets of novel therapies for neurodegenerative diseases are also discussed, with potential therapies including NAD+ precursors, mitophagy inducers and inhibitors of cellular senescence.
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                Author and article information

                Contributors
                Antonio G. Tartiere: URI : https://loop.frontiersin.org/people/2572128/overviewRole: Role:
                José M. P. Freije: URI : https://loop.frontiersin.org/people/36043/overviewRole:
                Carlos López-Otín: URI : https://loop.frontiersin.org/people/24710/overviewRole:
                Journal
                Journal ID (nlm-ta): Front Aging
                Journal ID (iso-abbrev): Front Aging
                Journal ID (publisher-id): Front. Aging
                Title: Frontiers in Aging
                Publisher: Frontiers Media S.A.
                ISSN (Print): 2673-6217
                ISSN (Electronic): 2673-6217
                Publication date (Electronic): 15 January 2024
                Publication date Collection: 2024
                Volume: 5
                Electronic Location Identifier: 1334261
                Affiliations
                [1] 1 Departamento de Bioquímica y Biología Molecular , Instituto Universitario de Oncología (IUOPA) , Universidad de Oviedo , Oviedo, Spain
                [2] 2 Instituto de Investigación Sanitaria del Principado de Asturias (ISPA) , Oviedo, Spain
                [3] 3 Facultad de Ciencias de la Vida y la Naturaleza , Universidad Nebrija , Madrid, Spain
                [4] 4 Centre de Recherche des Cordeliers , Universite de Paris Cite , Sorbonne Universite , INSERM , Paris, France
                Author notes

                Edited by: Hugo Alberto Barrera-Saldaña, Vitagénesis, S.A., Mexico

                Reviewed by: Michael Robert MacArthur, ETH Zürich, Switzerland

                Stella Victorelli, Mayo Clinic, United States

                *Correspondence: José M. P. Freije, jmpf@ 123456uniovi.es
                Article
                Publisher ID: 1334261
                DOI: 10.3389/fragi.2024.1334261
                PMC ID: 10824251
                PubMed ID: 38292053
                SO-VID: 661ae158-1f6a-4efb-8943-738b5e3b8ff8
                Copyright © Copyright © 2024 Tartiere, Freije and López-Otín.
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                Date received : 06 November 2023
                Date accepted : 03 January 2024
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Our work is supported by the Ministerio de Ciencia e Innovación (Spain) (PDI 2020-118394RB-100), Consejería de Ciencia, Innovación y Universidad del Gobierno del Principado de Asturias (FICYT), co-financed by the European Regional Development Fund (FEDER) (AYUD/2021/51062) and the European Research Council (742067, DeAge). The IUOPA is funded by the Gobierno del Principado de Asturias and Fundación Cajastur Liberbank.
                Categories
                Subject: Aging
                Subject: Review
                Custom metadata
                section-at-acceptance Molecular Mechanisms of Aging

                Keywords: healthspan,lifespan,senescence,progeria,biomarkers,rejuvenation
                Data availability:
                Keywords: healthspan, lifespan, senescence, progeria, biomarkers, rejuvenation

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