Cited by 376Telomeres, Telomerase, and SenescenceGenetics, Aging, and Longevity in Model OrganismsSingle-cell and spatial transcriptomics

The DOI matches its Crossref record; 168 of the 170 references it cites were found in a registry or an index; 182 of the 236 sources its claims cite were checked for support.

Guidelines for minimal information on cellular senescence experimentation in vivo

Open access

Abstract

Cellular senescence is a cell fate triggered in response to stress and is characterized by stable cell-cycle arrest and a hypersecretory state. It has diverse biological roles, ranging from tissue repair to chronic disease. The development of new tools to study senescence in vivo has paved the way for uncovering its physiological and pathological roles and testing senescent cells as a therapeutic target. However, the lack of specific and broadly applicable markers makes it difficult to identify and characterize senescent cells in tissues and living organisms. To address this, we provide practical guidelines called "minimum information for cellular senescence experimentation in vivo" (MICSE). It presents an overview of senescence markers in rodent tissues, transgenic models, non-mammalian systems, human tissues, and tumors and their use in the identification and specification of senescent cells. These guidelines provide a uniform, state-of-the-art, and accessible toolset to improve our understanding of cellular senescence in vivo.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.cell.2024.05.059

Cites

168 of 168 references verified0 citation errors · 0 not checkable

Statistics

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Verification

Claims the paper makes

68 Own interpretation · 49 Couldn’t confirm · 43 Partly supported · 7 No full text of the sources · 5 Sources not found · 2 Supported so far · 2 No basis given · 1 Supported · 1 Not supported · 1 Own method · accuracy not yet measured

Show all 93 claims

  • It may state two separate claims as one. 67
  • Probably not a substantial claim. 25
  • Not yet classified. 1
86 of 86
  • The paper relies on this without support.

    The lack of specific and broadly applicable markers makes it difficult to identify and characterize senescent cells in tissues and living organisms.

    “However, the lack of specific and broadly applicable markers makes it difficult to identify and characterize senescent cells in tissues and living organisms.”
  • The paper relies on this without support.

    Classical senescence markers discovered and established in cell culture have limited utility for experimentation in the natural tissue microenvironment or in situ.

    “An important limitation is that classical markers of senescence, originally discovered and established using cell culture models, have limited utility for experimentation in the natural tissue microenvironment, or “in situ”.”
  • The paper relies on this without support.

    The absence of a specific cellular senescence biomarker requires measuring multiple endpoints, including nucleic acids, proteins, and enzymatic activity in the same or adjacent tissue sections.

    “In addition, the lack of a specific biomarker for cellular senescence demands that multiple endpoints be measured, requiring multiplexing and measuring nucleic acids, proteins, and enzymatic activity in the same or adjacent tissue sections.”
  • The paper relies on this without support.

    No single biomarker is sufficient to detect cellular senescence in vivo, and multiplexing remains a necessary requirement.

    “No single biomarker is sufficient to detect cellular senescence in vivo, and multiplexing remains a necessary requirement.”
  • The paper relies on this without support.

    p21Cip1/Waf and p16Ink4a are the cyclin-dependent kinase inhibitors most commonly expressed by senescent cells in vivo.

    “While there are multiple cyclin-dependent kinase inhibitors (CDKIs), p21Cip1/Waf (CDKN1A locus; encoding p21Cip1/Waf) and p16Ink4a (CDKN2A locus; encoding p16Ink4a) are the inhibitors most commonly expressed by senescent cells in vivo (Fig. 1 A).”
  • The paper relies on this without support.

    In situ skin fibroblasts are much smaller than in vitro, limiting histological visualization.

    “In contrast to in vitro conditions, skin fibroblasts in situ are much smaller and only a fraction of their volume can be visualized by histology.”
  • The paper relies on this without support.

    Keratinocytes and fibroblasts differ dramatically in replication dynamics, capacity, and lifespan in vivo.

    “since keratinocytes and fibroblasts differ dramatically in replication dynamics, capacity, and lifespan in vivo”
  • The paper relies on this without support.

    Bone is a hard tissue that requires special processing and presents methodological challenges for detecting senescence markers, particularly histology-based ones.

    “Bone is an especially hard tissue that requires special processing and presents several methodological challenges for the detection of senescence markers, particularly those that rely on histology.”
  • The paper relies on this without support.

    Bone has a specific resorption-deposition cycle and extensive endocrine regulation.

    “In addition, bone has a very specific resorption-deposition cycle and extensive endocrine regulation.”
  • The paper relies on this without support.

    Mature adipose tissue is composed of >50–90% terminally differentiated post-mitotic adipocytes, ~10% preadipocytes, and ~10% immune cells.

    “Mature adipose tissue is composed of >50–90% terminally differentiated post-mitotic adipocytes, ~10% preadipocytes, and ~10% immune cells, including macrophages and lymphocytes.”
  • The paper relies on this without support.

    SA-β-gal staining is a common method for detecting senescent cells in adipose tissue.

    “Although SA-β-gal staining is a common method for detecting senescent cells in adipose tissue”
  • The paper relies on this without support.

    Adipose tissue cellular composition varies by anatomical location, sex, and obesity, contributing to senescence heterogeneity.

    “Moreover, adipose tissue differs greatly in cellular composition based on anatomical location, sex, and degree of obesity, which undoubtedly contributes to the heterogeneity of cellular senescence.”
  • The paper relies on this without support.

    Muscle is a complex tissue composed of post-mitotic multinucleated myofibers and a heterogeneous population of mononuclear cells including satellite cells, FAPs, endothelial cells, and macrophages.

    “Muscle is a complex tissue composed of post-mitotic multinucleated cells, referred to as myofibers, and a heterogeneous population of mononuclear cells, encompassing satellite cells, fibroadipogenic progenitors (FAPs), endothelial cells, and macrophages (Fig. 2 G).”
  • The paper relies on this without support.

    Fluorescent SPiDER-ß-Gal identifies senescent-like immune cell subsets by flow cytometry with high sensitivity.

    “In addition, fluorescent SPiDER-ß-Gal has been used to identify senescent-like subsets of immune cells by flow cytometry with high sensitivity.”
  • The paper relies on this without support.

    Measurements of cellular senescence in animals and assessment of the impact of senescent cells on physiology and pathology can be aided by a wide range of transgenic mouse models.

    “Measurements of cellular senescence in animals and assessment of the impact of senescent cells on physiology and pathology can be aided by a wide range of transgenic mouse models.”
  • The paper relies on this without support.

    It is possible to drive senescence in vivo by using a variety of drugs that promote cellular, organelle, or macromolecular stress.

    “It is also possible to drive senescence in vivo by using a variety of drugs that promote cellular, organelle, or macromolecular stress.”
  • The paper relies on this without support.

    The majority of currently available models are constitutive, while inducible KO or overexpression models are in development.

    “While the majority of currently available models are constitutive (active from conception), models of inducible KO or overexpression of senescence modulators are in development.”
  • The paper relies on this without support.

    p21, p16, TP53 (p53), and other senescence-associated proteins are involved in physiology distinct from cellular senescence.

    “Moreover, p21, p16, TP53 (p53), and other senescence-associated proteins are involved in physiology that is distinct from cellular senescence.”
  • The paper relies on this without support.

    Senescence can be induced efficiently by accelerated telomere shortening, disruption of the cell division machinery, and increased DNA damage levels in vivo.

    “In accordance with research on fibroblasts in vitro, senescence can be induced efficiently by accelerated telomere shortening, disruption of the cell division machinery, and increased DNA damage levels in vivo.”
  • The paper relies on this without support.

    Genes that induce accelerated senescence upon genetic depletion play pleiotropic roles in normal physiology.

    “Genes that induce accelerated senescence upon genetic depletion play pleiotropic roles in normal physiology.”
  • The paper relies on this without support.

    Luminescence signals are strongly influenced by tissue density and light penetration, which may bias measurement of senescent cell burden.

    “Luminescence signals are strongly influenced by tissue density and light penetration, which may bias the measurement of the senescent cell burden.”
  • The paper relies on this without support.

    Reporter construct design influences the reporter signal.

    “In addition to the caveats of various reporter genes, reporter construct design also influences the reporter signal.”
  • The paper relies on this without support.

    In pharmacogenetic elimination models, an inactive apoptosis-inducing gene is expressed from a senescence regulator promoter, and drug administration eliminates p21+ or p16+ cells.

    “In these mice, an inactive form of an apoptosis-inducing gene is expressed from the promoter of a key senescence regulator, such as p21 or p16, and administration of a drug to the mice drives the elimination of p21+ or p16+ cells.”
  • The paper relies on this without support.

    These models are typically designed to enable drug-inducible elimination and to report senescence levels in situ and/or in vivo.

    “These models are typically designed to not only enable drug-inducible elimination of senescent cells, but also to report the level of cellular senescence in situ and/or in vivo.”
  • The paper relies on this without support.

    The transgene is expressed throughout the body in these models.

    “it should be acknowledged that the transgene is expressed throughout the body.”
  • The paper relies on this without support.

    Our understanding of senescence in non-mammals is limited by the shortage of reagents for molecular analysis in many of these organisms.

    “However, our understanding of senescence in non-mammals is limited by the shortage of reagents for molecular analysis in many of these organisms.”
  • The paper relies on this without support.

    Cells from non-mammals are capable of undergoing cell cycle arrest resembling cellular senescence, but it might be driven by alternative mechanisms.

    “Although cells from non-mammals are capable of undergoing cell cycle arrest that resembles cellular senescence, it might be driven by alternative mechanisms.”
  • The paper relies on this without support.

    Other markers of cellular senescence, such as SA-β-gal, appear to function similarly across different animals, and their use has been instrumental in determining the presence of senescence in vivo across organisms.

    “Other markers of cellular senescence, such as SA-β-gal, appear to function similarly across different animals, and their use has been instrumental in determining the presence of senescence in vivo across organisms.”
  • The paper relies on this without support.

    The impact of senescent cells on non-mammalian biology has been mainly investigated in development, tissue remodeling, and regeneration, while disease and aging need further exploration.

    “The impact of senescent cells on the biology of non-mammalian species has been mainly investigated in the context of development, tissue remodeling, and regeneration, while conditions such as disease and aging still need to be further explored.”
  • The paper relies on this without support.

    The omics revolution enables in-depth characterization of the macromolecular composition of biological samples.

    “The omics revolution enables in-depth characterization of the macromolecular composition of biological samples.”
  • The paper relies on this without support.

    Senescent fibroblasts produced in vitro have been thoroughly characterized using epigenomic, transcriptomic, proteomic, lipidomic, metabolomic, and phenomic approaches.

    “Senescent fibroblasts produced in vitro have been thoroughly characterized using epigenomic, transcriptomic, proteomic, lipidomic, metabolomic, and phenomic approaches.”
  • The paper relies on this without support.

    Spatial omics platforms allow correlation of an omic dataset with spatial location within a tissue and have the potential to revolutionize in vivo senescence research.

    “Furthermore, spatial omics platforms allow for the correlation of an omic dataset (currently either whole genome transcriptomics or targeted transcriptomics or proteomics) with spatial location within a tissue and have the potential to revolutionize in vivo senescence research.”
  • The paper relies on this without support.

    Both bulk and single-cell omics have been applied to in vivo senescence research; however, analysis and interpretation pose challenges.

    “Both bulk and single-cell omics have been applied to in vivo senescence research; however, the analysis and interpretation of results pose challenges.”
  • The paper relies on this without support.

    Spatial transcriptomics is less sensitive than scRNA-seq and can introduce bias due to detection methods that do not always distinguish splice variants of CDKI genes such as CDKN2A.

    “Spatial transcriptomics is less sensitive than scRNA-seq and can introduce bias based on methods of either detection of the 3’ end of (polyA tail) or nucleic acid ISH probes, which do not always distinguish between splice variants of CDKI genes such as CDKN2A.”
  • The paper relies on this without support.

    Single-cell transcriptomics requires a large number of intact cells.

    “Single-cell transcriptomics requires a large number of intact cells.”
  • The paper relies on this without support.

    Multiple sources of bias can be introduced through tissue dissociation, microfluidics, data analysis, and statistics.

    “Furthermore, multiple sources of bias can be introduced through tissue dissociation (loss of fragile cells), microfluidics (loss of large cells), data analysis, and statistics.”
  • The paper relies on this without support.

    There is no evidence that cellular senescence is regulated at a transcriptional level.

    “Finally, there is no evidence that cellular senescence is regulated at a transcriptional level.”
  • The paper relies on this without support.

    Changes in nuclear and cellular morphology are largely conserved across senescent cells in vitro and in vivo.

    “Changes in nuclear and cellular morphology are largely conserved across senescent cells, both in vitro and in vivo.”
  • The paper relies on this without support.

    Methods for detecting anti-apoptotic proteins in situ or in vivo are not yet well established.

    “Methods for detecting anti-apoptotic proteins in situ or in vivo are not yet well established but would provide targetable senescence biomarkers in the context of cancer.”
  • The paper relies on this without support.

    p16 is easier to detect in humans than in murine samples due to a reliable antibody against human p16Ink4a.

    “Some markers of senescence, such as p16, are easier to detect in humans than in murine samples (because of the availability of a reliable antibody against human p16Ink4a developed as a clinical prognostic tool for cancer).”
  • The paper relies on this without support.

    Metabolically active and lipid-rich tissues are more vulnerable to rapid ex vivo degradation.

    “Similarly, metabolically active and lipid-rich tissues are more vulnerable to rapid ex vivo degradation.”
  • The paper relies on this without support.

    Aging drives heterogeneity among individuals, which has not been observed in young individuals.

    “Aging also drives incredible heterogeneity among individuals, which has not been observed in young individuals.”
  • The paper relies on this without support.

    There is little control over variables in humans that affect senescent cell burden.

    “Furthermore, unlike laboratory models, there is little control over variables in humans that affect senescent cell burden, such as occult disease, body mass index, environmental factors, genetic factors impacting genome instability and telomere length, and levels of psychosocial stress.”
  • The paper relies on this without support.

    There is currently limited knowledge about SASP factors in liquid biopsies.

    “While surrogate biomarkers of senescence burden from liquid biopsies, preferably from minimally invasive sampling such as blood, saliva, wound pus, urine, synovial, or cerebrospinal fluid, would provide a necessary and more accessible alternative, there is currently limited knowledge about SASP factors in these liquid biopsies.”
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Authors
Ogrodnik, M., Carlos Acosta, J., Adams, P. D., d’Adda di Fagagna, F., Baker, D. J., Bishop, C. L., Chandra, T., Collado, M., Gil, J., Gorgoulis, V., Gruber, F., Hara, E., Jansen-Dürr, P., Jurk, D., Khosla, S., Kirkland, J. L., Krizhanovsky, V., Minamino, T., Niedernhofer, L. J., Passos, J. F., Ring, N. A. R., Redl, H., Robbins, P. D., Rodier, F., Scharffetter-Kochanek, K., Sedivy, J. M., Sikora, E., Witwer, K., von Zglinicki, T., Yun, M. H., Grillari, J., & Demaria, M.
Affiliations
  • Ludwig Boltzmann Gesellschaft (AT)
  • Sanford Burnham Prebys Medical Discovery Institute (US)
  • Mayo Clinic (US)
  • Queen Mary University of London (GB)
  • University of Edinburgh (GB)
  • Consejo Superior de Investigaciones Científicas (ES)
  • University of Dundee (GB)
  • Immunology Frontier Research Center, The University of Osaka (JP)
  • Weizmann Institute of Science (IL)
  • Japan Agency for Medical Research and Development (JP)
  • University of Minnesota (US)
  • Brown University (US)
  • Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
  • Johns Hopkins University (US)
  • Max Planck Institute of Molecular Cell Biology and Genetics (DE)
  • Institute of Molecular Biotechnology (AT)
  • University Medical Center Groningen (NL)
Corresponding author
  • Ogrodnik, Mikolaj
  • Grillari, Johannes
  • Demaria, Marco
Venue
Cell
Publisher
Elsevier BV
Published
2024-08
Volume
187
Issue
16
Pages
4150-4175
ISSN
0092-8674 (ISSN-L)
OpenAlex
W4401420229
Cited by
376
References
170
Citations by year
2026: 206 · 2025: 142 · 2024: 27
FWCI
21.30
Type
journal article
Language
en
Open access
Locations
  • Cell (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by)
  • UCrea (University of Cantabria) (submittedVersion, cc-by)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
  • Digital Library of the University of Innsbruck (University of Innsbruck) (submittedVersion, cc-by)
  • Newcastle University ePrints (Newcastle Univesity) (cc-by)
Funders
  • Glenn Foundation for Medical Research
  • Pfizer
  • Brown University
  • Cancer Research Society (20087)
  • Merck KGaA
  • Buck Institute for Research on Aging
  • Noaber Foundation
  • Ovarian Cancer Canada
  • Cancer Research UK (C15075/A28647)
  • Imperial College London (H2020)
  • European Commission (2014‐2020, HORIZON2020, H2020, 857524, POR FESR 2014-2020, 825575, 70/3/8916, 856487)
  • Deutsche Forschungsgemeinschaft (450807335, 825575, GRK-1789, 450627322, CRC 1506, 497658823, 22137416)
  • ZonMw
  • Austrian Science Fund (P36483, P 35268, P 37321, P35382)
  • Fondation pour la Recherche Médicale
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (09150172010029)
  • General Secretariat for Research and Technology (2020SE01300001, H2020)
  • Herzfelder'sche Familienstiftung
  • Associazione Italiana per la Ricerca sul Cancro (21762, 21091)
  • Universität für Bodenkultur Wien
  • Allgemeine Unfallversicherungsanstalt
  • Zentrum für Regenerative Therapien Dresden
  • Regione Lombardia (POR FESR 20142020, 2014–2020, FESR 2014-2020)
  • Ludwig Boltzmann Gesellschaft
  • Fondazione Regionale per la Ricerca Biomedica (825575)
  • National Institutes of Health (ASAP-000592, H2020, AG031862)
  • Horizon 2020 Framework Programme (825575, 857524)
  • Natural Sciences and Engineering Research Council of Canada
  • Fonds de Recherche du Québec - Santé (281706, 33070, 22624)
  • Medical Research Council (MC-U120085810)
  • Biotechnology and Biological Sciences Research Council (BB/S006710/1)
  • European Regional Development Fund (FESR 2014-2020, 2014-2020’, H2020, POR FESR 2014-2020)
  • Agencia Estatal de Investigación (H2020)
  • National Institute on Aging (P01AG031862, P01AG043376, R01AG068182, R01AG053229, R01AG068076, R01AG068048, R33AG061456, R37AG013925, R01AG082708, U19AG056278, U54AG079779, U54AG079754, U54AG076041, P01AG062413, U54AG079758, R01AG071861, P01AG051449, R01AG063543)
  • National Cancer Institute (UH3CA268103, UG3CA268103)
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
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
Keywords
cellular senescence, senescence markers, senolytics, cell cycle arrest, senescence-associated secretory phenotype, tumors, reporting guidelines
MeSH terms
Animals, Humans, Neoplasms, Biomarkers, Cellular Senescence, Guidelines as Topic

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