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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Citations
Cites
A biomarker that identifies senescent human cells in culture and in aging skin in vivo.
Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., & Pereira-Smith, O. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9363 · Cited by 7,477
Cancer Immunoediting: Integrating Immunity’s Roles in Cancer Suppression and Promotion
Schreiber, R. D., Old, L. J., & Smyth, M. J. (2011) · Science · doi:10.1126/science.1203486 · Cited by 6,474
The limited in vitro lifetime of human diploid cell strains
Hayflick, L. (1965) · Experimental Cell Research · doi:10.1016/0014-4827(65)90211-9 · Cited by 5,876
Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a
Serrano, M., Lin, A. W., McCurrach, M. E., Beach, D., & Lowe, S. W. (1997) · Cell · doi:10.1016/s0092-8674(00)81902-9 · Cited by 5,218
Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders
Baker, D. J., Wijshake, T., Tchkonia, T., LeBrasseur, N. K., Childs, B. G., van de Sluis, B., Kirkland, J. L., & van Deursen, J. M. (2011) · Nature · doi:10.1038/nature10600 · Cited by 3,670 · cited 1×
“Most strikingly, late-life clearance of senescent cells still attenuated progression of already established age-related disorders (40).”
BackgroundSenescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas
Xue, W., Zender, L., Miething, C., Dickins, R. A., Hernando, E., Krizhanovsky, V., Cordon-Cardo, C., & Lowe, S. W. (2007) · Nature · doi:10.1038/nature05529 · Cited by 2,473
Self-citationSenescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors
Campisi, J. (2005) · Cell · doi:10.1016/j.cell.2005.02.003 · Cited by 2,379
Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion
Rodier, F., Coppé, J.-P., Patil, C. K., Hoeijmakers, W. A. M., Muñoz, D. P., Raza, S. R., Freund, A., Campeau, E., Davalos, A. R., & Campisi, J. (2009) · Nature Cell Biology · doi:10.1038/ncb1909 · Cited by 2,232
BRAFE600-associated senescence-like cell cycle arrest of human naevi
Michaloglou, C., Vredeveld, L. C. W., Soengas, M. S., Denoyelle, C., Kuilman, T., van der Horst, C. M. A. M., Majoor, D. M., Shay, J. W., Mooi, W. J., & Peeper, D. S. (2005) · Nature · doi:10.1038/nature03890 · Cited by 2,160
Oncogene-Induced Senescence Relayed by an Interleukin-Dependent Inflammatory Network
Kuilman, T., Michaloglou, C., Vredeveld, L. C. W., Douma, S., van Doorn, R., Desmet, C. J., Aarden, L. A., Mooi, W. J., & Peeper, D. S. (2008) · Cell · doi:10.1016/j.cell.2008.03.039 · Cited by 2,086
The essence of senescence: Figure 1.
Kuilman, T., Michaloglou, C., Mooi, W. J., & Peeper, D. S. (2010) · Genes & Development · doi:10.1101/gad.1971610 · Cited by 2,038
Senescence of Activated Stellate Cells Limits Liver Fibrosis
Krizhanovsky, V., Yon, M., Dickins, R. A., Hearn, S., Simon, J., Miething, C., Yee, H., Zender, L., & Lowe, S. W. (2008) · Cell · doi:10.1016/j.cell.2008.09.015 · Cited by 2,027
Self-citationCrucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis
Chen, Z., Trotman, L. C., Shaffer, D., Lin, H.-K., Dotan, Z. A., Niki, M., Koutcher, J. A., Scher, H. I., Ludwig, T., Gerald, W., et al. (2005) · Nature · doi:10.1038/nature03918 · Cited by 1,993
Chemokine signaling via the CXCR2 receptor reinforces senescence
Acosta, J. C., O'Loghlen, A., Banito, A., Guijarro, M. V., Augert, A., Raguz, S., Fumagalli, M., Da Costa, M., Brown, C., Popov, N., et al. (2008) · Cell · doi:10.1016/j.cell.2008.03.038 · Cited by 1,801
Krtolica, A., Parrinello, S., Lockett, S., Desprez, P.-Y., & Campisi, J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211053698 · Cited by 1,730
Senescence surveillance of pre-malignant hepatocytes limits liver cancer development
Kang, T.-W., Yevsa, T., Woller, N., Hoenicke, L., Wuestefeld, T., Dauch, D., Hohmeyer, A., Gereke, M., Rudalska, R., Potapova, A., et al. (2011) · Nature · doi:10.1038/nature10599 · Cited by 1,621
Self-citationSenescence in premalignant tumours
Collado, M., Gil, J., Efeyan, A., Guerra, C., Schuhmacher, A. J., Barradas, M., Benguría, A., Zaballos, A., Flores, J. M., Barbacid, M., et al. (2005) · Nature · doi:10.1038/436642a · Cited by 1,482
Reversal of human cellular senescence: roles of the p53 and p16 pathways
Beauséjour, C. M., Krtolica, A., Galimi, F., Narita, M., Lowe, S. W., Yaswen, P., & Campisi, J. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg417 · Cited by 1,457
Lowe, S. W., Cepero, E., & Evan, G. I. (2004) · Nature · doi:10.1038/nature03098 · Cited by 1,374
Inflammatory networks during cellular senescence: causes and consequences.
Freund, A., Orjalo, A. V., Desprez, P.-Y., & Campisi, J. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.03.003 · Cited by 1,354
Oncogene-induced senescence as an initial barrier in lymphoma development
Braig, M., Lee, S., Loddenkemper, C., Rudolph, C., Peters, A. H. F. M., Schlegelberger, B., Stein, H., Dörken, B., Jenuwein, T., & Schmitt, C. A. (2005) · Nature · doi:10.1038/nature03841 · Cited by 1,220
Jun, J.-I., & Lau, L. F. (2010) · Nature Cell Biology · doi:10.1038/ncb2070 · Cited by 998
Senescence-messaging secretome: SMS-ing cellular stress
Kuilman, T., & Peeper, D. S. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2560 · Cited by 909
Wajapeyee, N., Serra, R. W., Zhu, X., Mahalingam, M., & Green, M. R. (2008) · Cell · doi:10.1016/j.cell.2007.12.032 · Cited by 903
Senescence of human fibroblasts induced by oncogenic Raf
Zhu, J., Woods, D., McMahon, M., & Bishop, J. M. (1998) · Genes & Development · doi:10.1101/gad.12.19.2997 · Cited by 826
Microarray analysis of replicative senescence
Shelton, D. N., Chang, E., Whittier, P. S., Choi, D., & Funk, W. D. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80420-5 · Cited by 764
Kortlever, R. M., Higgins, P. J., & Bernards, R. (2006) · Nature Cell Biology · doi:10.1038/ncb1448 · Cited by 637
Parrinello, S., Coppe, J.-P., Krtolica, A., & Campisi, J. (2005) · Journal of Cell Science · doi:10.1242/jcs.01635 · Cited by 631
Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence
Coppé, J.-P., Kauser, K., Campisi, J., & Beauséjour, C. M. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m603307200 · Cited by 604
Bavik, C., Coleman, I., Dean, J. P., Knudsen, B., Plymate, S., & Nelson, P. S. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-1716 · Cited by 453
Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance
Willimsky, G., & Blankenstein, T. J. F. (2005) · Nature · doi:10.1038/nature03954 · Cited by 439
Putting the stress on senescence
Serrano, M., & Blasco, M. A. (2001) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00278-7 · Cited by 413
Coppé, J.-P., Patil, C. K., Rodier, F., Sun, Y., Muñoz, D. P., Goldstein, J., Nelson, P. S., Desprez, P.-Y., & Campisi, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060301 · Cited by 302
Reversal of Senescence in Mouse Fibroblasts through Lentiviral Suppression of p53
Dirac, A. M. G., & Bernards, R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.c300023200 · Cited by 265
Narita, M., & Lowe, S. W. (2005) · Nature Medicine · doi:10.1038/nm0905-920 · Cited by 153
Pitiyage, G. N., Slijepčević, P., Gabrani, A., Chianea, Y. G., Lim, K. P., Prime, S. S., Tilakaratne, W. M., Fortune, F., & Parkinson, E. K. (2010) · The Journal of Pathology · doi:10.1002/path.2839 · Cited by 101
Kato, D., Miyazawa, K., Ruas, M., Starborg, M., Wada, I., Oka, T., Sakai, T., Peters, G. G., & Hara, E. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00426-8 · Cited by 89
Immune reactions in benign and malignant melanocytic lesions: lessons for immunotherapy
Speeckaert, R., van Geel, N., Vermaelen, K., Lambert, J., Gele, M. V., Speeckaert, M. M., & Brochez, L. (2010) · Pigment Cell & Melanoma Research · doi:10.1111/j.1755-148x.2010.00799.x · Cited by 57
Mason, D. X., Keppler, D., Zhang, J., Jackson, T. J., Seger, Y. R., Matsui, S., Abreo, F., Cowell, J. K., Hannon, G. J., Lowe, S. W., et al. (2006) · Carcinogenesis · doi:10.1093/carcin/bgi264 · Cited by 18
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1 of the 40 references couldn’t be matched to a known paper.
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- 1916, J CUTAN DIS, 34, 797
- Krizhanovsky, 2008, Cell, 134, 657, 10.1016/j.cell.2008.06.049 · DOI · Paper page
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Sorted by citations
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013) · Cell · doi:10.1016/j.cell.2013.05.039 · Cited by 14,982
“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 (Hoenicke and Zender, 2012; Kang et al., 2011; Xue et al., 2007).”
BackgroundCellular senescence: from physiology to pathology
Muñoz-Espín, D., & Serrano, M. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3823 · Cited by 2,818
Cellular senescence in aging and age-related disease: from mechanisms to therapy
Childs, B. G., Durik, M., Baker, D. J., & van Deursen, J. M. (2015) · Nature Medicine · doi:10.1038/nm.4000 · Cited by 2,363
Cellular senescence and the senescent secretory phenotype: therapeutic opportunities
Tchkonia, T., Zhu, Y., van Deursen, J., Campisi, J., & Kirkland, J. L. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64098 · Cited by 1,774
Programmed cell senescence during mammalian embryonic development
Muñoz-Espín, D., Cañamero, M., Maraver, A., Gómez-López, G., Contreras, J., Murillo-Cuesta, S., Rodríguez-Baeza, A., Varela-Nieto, I., Ruberte, J., Collado, M., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.019 · Cited by 1,428
“…secretory phenotype (SASP) can also evoke a local inflammatory response with complex effects, including the elimination of senescent cells by phagocytosis, thus leading to tissue remodeling and damage resolution (Freund et al., 2010; Hoenicke and Zender, 2012; Krizhanovsky et al., 2008).”
Influential
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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