The DOI matches its Crossref record; 39 of the 40 references it cites were found in a registry or an index.
Immune surveillance of senescent cells--biological significance in cancer- and non-cancer pathologies
Open accessAbstract
Cellular senescence, a state of stable growth arrest, can occur in response to various stress stimuli such as telomere shortening, treatment with chemotherapeutic drugs or the aberrant activation of oncogenes. Senescent cells communicate with their environment by secreting various cytokines and growth factors, and it has become clear that this 'secretory phenotype' can have pro- as well as anti-tumorigenic effects. Recent work from our laboratory showed that premalignant, senescent hepatocytes are recognized and cleared through an antigen-specific immune response and that this immune response, designated as 'senescence surveillance' is crucial for tumor suppression in the liver [(Kang,T.W. et al. (2011) Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature, 479, 547-551]. It is an emerging concept that immune responses against senescent cells have a broader biological significance in cancer- as well as non-cancer pathologies and current data suggest that distinct immune responses are engaged to clear senescent cells in different disease settings. In this review article, we will discuss different examples how immune responses against senescent cells are involved to restrict disease progression in cancer- and non-cancer pathologies.
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In the citing paper
“In the case of senescent tumor cells, there is good evidence that they are subjected to strict immune surveillance and are efficiently removed by phagocytosis”
From The Hallmarks of Aging (2013) · cites this paper as Hoenicke and Zender, 2012
Experimental — accuracy not yet measuredIn the citing paper
“Although senescent cells can be recognized by T helper cells and cleared by macrophages and natural killer lymphocytes [27,34,35], their number has been shown to increase with normal ageing in tissues of humans, primates and rodents [36,37].”
From Ageing, Cellular Senescence and Neurodegenerative Disease (2018) · cites this paper as [35]
In the citing paper
“Senescent cells can be eliminated through a SASP-induced immune response, which can involve both innate and adaptive immunity.”
From Inside and out: the activities of senescence in cancer (2014) · cites this paper as [111]
In the citing paper
“activating an immune response”
From Inside and out: the activities of senescence in cancer (2014) · cites this paper as [111]
In the citing paper
“Indeed, senescent cells formed following tissue damage can promote their own clearance by secreting chemo-attractants that recruit and activate immune cells [265].”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [265]
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Cites
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“Senescent cells secrete an array of cytokines, chemokines, growth factors, and proteases collectively referred to as the senescence-associated secretory phenotype (SASP) (Baker et al., 2011; Hoenicke & Zender, 2012).”
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Pompili, S., Vetuschi, A., Latella, G., Smakaj, A., Sferra, R., & Cappariello, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24108952 · Cited by 25
“This complex secretum alerts neighboring cells to the occurrence of an injury and recruits the immune cells to delete the senescent cells [24].”
BackgroundSMARCA4 regulates the NK-mediated killing of senescent cells
Reen, V., D’Ambrosio, M., Søgaard, P. P., Tyson, K., Leeke, B. J., Clément, I., Dye, I. C., Pombo, J., Kuba, A., Lan, Y., et al. (2025) · Science Advances · doi:10.1126/sciadv.adn2811 · Cited by 26
“Different immune cell types, including CD4 + T cells ( 6 ), CD8 + T cells ( 7 , 8 ), macrophages, neutrophils, or natural killer (NK) cells ( 5 , 9 ), are involved in the immune surveillance and elimination of senescent cells ( 10 ).”
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“Although senescent PC cancer cells should attract immune cells and get eliminated through the immune surveillance (17, 18), most PC cancer cells upregulate senescence markers and accumulate within the tumor.”
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The Unusual Immune System of the Naked Mole-Rat
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“SC interact with the immune system in a mutual way – besides being a target of the immune system (senescence immunosurveillance; [18]), SC can modulate the immune system function by either immunoactivation [18] or immunosuppression [19, 20].”
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“Secretion of these and similar proteins by senescent cells induces inflammation and, at least in some cases, may be necessary for phagocytotic senescent cell clearance [62,63].”
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Self-citationCell-in-Cell Events in Oral Squamous Cell Carcinoma
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“These cells expressed typical inflammatory mediators related to a senescence-associated secretory phenotype (14), which in turn may be responsible for stimulating clearance of these cells through non-professional phagocytosis (73, 74).”
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“In vivo data have shown the accumulation of senescent cells in aged tissues (33, 34).”
Backgroundp16ink4a Positivity of Melanocytes in Non-Segmental Vitiligo
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Senescence as a main mechanism of Ritonavir and Ritonavir‐NO action against melanoma
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“In our opinion, a model that could explain these findings is that a population of treated tumor cells, indeed, enter a state of cellular senescence, from which some get cleared (immune surveillance) and some escape or bypass senescence [68,69]; however, in any case, at the time of surgery, when a significant period of…”
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“It is unclear why other cells escape this decline but “selectivity” is relevant because CD4 T lymphocytes mediate in cancer progression (7).”
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“During senescence, cells communicate with their surrounding microenvironment by secreting various cytokines and growth factors [37].”
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“The invasive growth andmetastasis of tumor tissues can be achieved by the escape from the immunologic surveillance [4, 5].”
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“Let us have a quick look, to close the brief yet challenging list of controversies discussed, alternating from good to evil beliefs in medicine (Hoenicke & Zender, 2012).”
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Senescence and Senescence-Related Disorders
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“75,76 And this immune response plays an important role in the treatment of delayed aging.”
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Novedades en inmunología del melanoma
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Senescence: An Overlooked VSMC Phenotype and Therapeutic Opportunity?
Herman, A. B., Grešová, K., Maragkakis, M., & Autieri, M. V. (2025) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.125.323131 · Cited by 7
A Multiparametric Assay to Evaluate Senescent Cells
Gal, H., Porat, Z., & Krizhanovsky, V. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8931-7_11 · Cited by 7
Kim, K., Admasu, T. D., Stolzing, A., & Sharma, A. (2022) · Aging · doi:10.18632/aging.203931 · Cited by 8
Nutritional Modulators of Cellular Senescence In Vitro
Provinciali, M., Pierpaoli, E., Piacenza, F., Giacconi, R., Costarelli, L., Basso, A., Recchioni, R., Marcheselli, F., Bray, D. H., Benlhassan, K., et al. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801816-3.00022-4 · Cited by 6
Wu, W., Yu, A., Chen, K., Lu, P., Yang, J., Liu, K., Mao, Z., & Yao, Z. (2019) · Medical Science Monitor · doi:10.12659/msm.917867 · Cited by 6
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“…extracellular proteases, and extracellular matrix proteins that compose the SASP mediate senescent cells functions in tissue repair (Coppe et al., 2008; Freund et al., 2010; Freund et al., 2011; Hoenicke and Zender, 2012; Krizhanovsky et al., 2008; Malaquin et al., 2016; Rodier et al., 2009).”
BackgroundA Multidimensional Systems Biology Analysis of Cellular Senescence in Ageing and DiseasePreprint
Avelar, R. A., Ortega, J. G., Tăcutu, R., Tyler, E. J., Bennett, D. F., Binetti, P., Budovsky, A., Chatsirisupachai, K., Johnson, E., Murray, A., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/743781 · Cited by 6
“A visual inspection showed a number of bottleneck genes between Module 1 and Module 16, consistent with the role of the immune system in clearance and surveillance of senescence cells and the secretion of immunomodulators by senescent cells (Hoenicke and Zender, 2012) (SI Table 34).”
BackgroundIn vitro senescence and senolytic functional assays
Ryan, P., & Lee, J. (2025) · Biomaterials Science · doi:10.1039/d4bm01684j · Cited by 7
Functional screening to identify senescence regulators in cancer
Lujambio, A., & Banito, A. (2019) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2019.02.001 · Cited by 6
Koziej, P., Kluszczyńska, K., Hartman, M. L., & Czyż, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24097891 · Cited by 5
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Stem Cell Senescence as the Memory of Past Injuries
Gianfranceschi, G., Gri, G., Cesselli, D., & Beltrami, A. P. (2015) · Current Pathobiology Reports · doi:10.1007/s40139-015-0071-5 · Cited by 4
“CD4 acquired immune cells too are attracted, together with macrophages, by premalignant senescent cells expressing oncogenic N-Ras [71] and are involved in their clearance, representing an efficient immune surveillance system of the liver [72].”
BackgroundInsight on sarcopenic obesity and epicatechin as a promising treatment option
Sabarathinam, S., Dhanasekaran, D., & Ganamurali, N. (2023) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2023.102856 · Cited by 6
Immunosenescence, Oxidative Stress, and Cancers
Fülöp, T., Pawelec, G., Dupuis, G., Kotb, R. R., Friguet, B., Witkowski, J. M., & Larbi, A. (2020) · Springer eBooks · doi:10.1007/978-3-030-30845-2_23 · Cited by 4
Sotoudeh, N., Noormohammadi, Z., Habibi‐Anbouhi, M., Kazemi‐Lomedasht, F., & Behdani, M. (2019) · Monoclonal Antibodies in Immunodiagnosis and Immunotherapy · doi:10.1089/mab.2019.0031 · Cited by 4
“(8,9) 18) Hence, molecular detecting of CTLA-4 protein is an important goal in many fundamental types of research.”
Rožman, P. J., Jazbec, K., & Jež, M. (2018) · InTech eBooks · doi:10.5772/intechopen.71764 · Cited by 4
“For instance, there is good evidence that the senescent tumor cells are subjected to strict immune surveillance and are efficiently removed by phagocytosis [248].”
BackgroundIonizing Radiation Effects In Vitro Study; Using The Rat Whole Embryo Culture Model
Balcıoğlu, E., Baran, M., Nisari, M., Göktepe, Ö., Bilgici, P., Bolat, D., Suna, P. A., Al, Ö., Yıldız, O. G., & Arzu Hanım, Y. A. Y. (2021) · Gevher Nesibe Journal IESDR · doi:10.46648/gnj.162 · Cited by 3
Zedoary Turmeric Oil Induces Senescence and Apoptosis in Human Colon Cancer HCT116 Cells
Su, M.-Q., Zhou, Y., Li, C., Wang, Z., Wang, Y.-L., Shen, B., & Dou, J. (2018) · Natural Product Communications · doi:10.1177/1934578x1801300731 · Cited by 3
Coates, P. J. (2013) · The Journal of Pathology · doi:10.1002/path.4182 · Cited by 3
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“The CD4+ T helper cells increase the rate of the transition of the tumor cells in the 'MYC off state to 'Senescence' and macrophages mediate clearance of senescent tumor cells [9].”
BackgroundThe Molecular Basis of the Immune Response to Stressed Cells and Tissues
Gonzalez, S. R., López‐Larrea, C., & López‐Soto, A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801968-9.00003-9 · Cited by 3
Cellular Senescence and Tumor Promotion
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Doxorubicin Induces Senescence in Intestinal Epithelial CellsPreprint
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Novel Immunologic Approaches to Melanoma Treatment
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“The interaction between the immune system and melanoma is dynamic, however, and tumor cells use various mechanisms to avoid recognition and destruction by the immune system, favoring disease progression.(5) Treatment strategies aimed at boosting the immune response through vaccines and biochemotherapy were attempted f…”
BackgroundObesity, inflammation, and aging
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Xu, Y., Yang, W., Yao, F., Wang, Z.-H., Liu, J., Huang, B., Li, X., Zhong, F., & Wang, X. (2024) · Journal of Inflammation Research · doi:10.2147/jir.s483705 · Cited by 1
Oncogene-Induced Senescence Transcriptomes Signify Premalignant Colorectal Adenomas
Shboul, S. A., Awad, H., Abu-Humaidan, A. H. A., Ababneh, N. A., Khasawneh, A. I., & Saleh, T. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47040221 · Cited by 1
“…signatures is indicative of a state of escaping the senescent phenotype, one alternative explanation behind it is that the accumulating senescent, premalignant cells might be a target for removal by the immune system [57,58], especially in the context of colorectal tumorigenesis [15,59].”
View Micronuclei in the Extent of Evolution: New Insight Into an Old Issue
Yang, S., Yao, H., Zhang, Y., Zhang, W., Jin, S., Huang, K., Song, J., Feng, Y., Li, X., & Wang, X. (2025) · Journal of Cellular Physiology · doi:10.1002/jcp.70079 · Cited by 1
“SASP can inhibit tumorigenesis by promoting cell senescence transformation and subsequent senescent cell clearance (Hoenicke and Zender 2012; Serrano 2011).”
Ekumi, K. M., Johnston, M. J., Murphy, M. P., Rakoczy, S. G., Painter, T., & Brown‐Borg, H. M. (2026) · NAR Molecular Medicine · doi:10.1093/narmme/ugag018 · Cited by 1
Metadata
- Authors
- Hoenicke, L., & Zender, L.
- Affiliations
- Helmholtz Centre for Infection Research (DE)
- Medizinische Hochschule Hannover (DE)
- Corresponding author
- Zender, L.
- Venue
- Carcinogenesis
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-04-02
- Volume
- 33
- Issue
- 6
- Pages
- 1123-1126
- ISSN
- 0143-3334 (ISSN-L)
- 1460-2180
- OpenAlex
- W2121022075
- Cited by
- 248
- References
- 40
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 11 · 2023: 15 · 2022: 26 · 2021: 21 · 2020: 31 · 2019: 24 · 2018: 24 · 2017: 14 · 2016: 22 · 2015: 14 · 2014: 12 · 2013: 17 · 2012: 1
- FWCI
- 1.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Carcinogenesis (publishedVersion)
- PubMed (publishedVersion)
- HZI (Helmholtz Centre for Infection Research) (submittedVersion)
- 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 › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- cellular senescence, senescence-associated secretory phenotype, tumor suppression, liver cancer, antigen-specific immune response, tumor immunology, telomere shortening, chemotherapy-induced senescence, oncogene activation
- MeSH terms
- Humans, Immunologic Surveillance, Liver, Neoplasms, Precancerous Conditions, Cytokines, Cellular Senescence, Disease Progression, Chemokines, Hepatocytes
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