Skip to main content

Advertisement

SpringerLink
Log in

Cytokine-induced senescence for cancer surveillance

  • NON-THEMATIC REVIEW
  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Abstract

The immune response is a first-line systemic defense to curb tumorigenesis and metastasis. Much effort has been invested to design antitumor interventions that would boost the immune system in its fight to defeat or contain cancerous growth. Tumor vaccination protocols, transfer of tumor-associated-antigen-specific T cells, T cell activity-regulating antibodies, and recombinant cytokines are counted among a toolbox filled with immunotherapeutic options. Although the mechanistic underpinnings of tumor immune control remain to be deciphered, these are studied with the goal of cancer cell destruction. In contrast, tumor dormancy is considered as a dangerous equilibrium between cell proliferation and cell death. There is, however, emerging evidence that tumor immune control can be achieved in the absence of overt cancer cell death. Here, we propose cytokine-induced senescence (CIS) by transfer of T helper-1 cells (TH1) or by recombinant cytokines as a novel therapeutic intervention for cancer treatment. Immunity-induced senescence triggers a stable cell cycle arrest of cancer cells. It engages the immune system to construct defensive, isolating barriers around tumors, and prevents tumor growth through the delivery or induction of TH1-cytokines in the tumor microenvironment. Keeping cancer cells in a non-proliferating state is a strategy, which directly copes with the lost homeostasis of aggressive tumors. As most studies show that even after efficient cancer therapies minimal residual disease persists, we suggest that therapies should include immune-mediated senescence for cancer surveillance. CIS has the goal to control the residual tumor and to transform a deadly disease into a state of silent tumor persistence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Perez-Mancera, P. A., Young, A. R., & Narita, M. (2014). Inside and out: the activities of senescence in cancer. Nature Reviews: Cancer, 14(8), 547–558.

    CAS  PubMed  Google Scholar 

  2. Lopez-Otin, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013). The hallmarks of aging. Cell, 153(6), 1194–1217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Fumagalli, M., Rossiello, F., Clerici, M., Barozzi, S., Cittaro, D., Kaplunov, J. M., et al. (2012). Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nature Cell Biology, 14(4), 355–365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Burd, C. E., Sorrentino, J. A., Clark, K. S., Darr, D. B., Krishnamurthy, J., Deal, A. M., et al. (2013). Monitoring tumorigenesis and senescence in vivo with a p16(INK4a)-luciferase model. Cell, 152(1–2), 340–351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Baker, D. J., Wijshake, T., Tchkonia, T., LeBrasseur, N. K., Childs, B. G., van de Sluis, B., et al. (2011). Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature, 479(7372), 232–236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Campisi, J., Andersen, J. K., Kapahi, P., & Melov, S. (2011). Cellular senescence: a link between cancer and age-related degenerative disease? Seminars in Cancer Biology, 21(6), 354–359.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Munoz-Espin, D., Canamero, M., Maraver, A., Gomez-Lopez, G., Contreras, J., Murillo-Cuesta, S., et al. (2013). Programmed cell senescence during mammalian embryonic development. Cell, 155(5), 1104–1118.

    Article  CAS  PubMed  Google Scholar 

  8. Storer, M., Mas, A., Robert-Moreno, A., Pecoraro, M., Ortells, M. C., Di Giacomo, V., et al. (2013). Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell, 155(5), 1119–1130.

    Article  CAS  PubMed  Google Scholar 

  9. Michaloglou, C., Vredeveld, L. C., Soengas, M. S., Denoyelle, C., Kuilman, T., van der Horst, C. M., et al. (2005). BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature, 436(7051), 720–724.

    Article  CAS  PubMed  Google Scholar 

  10. Lee, S., Schmitt, C. A., & Reimann, M. (2011). The Myc/macrophage tango: oncogene-induced senescence, Myc style. Seminars in Cancer Biology, 21(6), 377–384.

    Article  CAS  PubMed  Google Scholar 

  11. Chang, B. D., Broude, E. V., Dokmanovic, M., Zhu, H., Ruth, A., Xuan, Y., et al. (1999). A senescence-like phenotype distinguishes tumor cells that undergo terminal proliferation arrest after exposure to anticancer agents. Cancer Research, 59(15), 3761–3767.

    CAS  PubMed  Google Scholar 

  12. Schmitt, C. A., Fridman, J. S., Yang, M., Lee, S., Baranov, E., Hoffman, R. M., et al. (2002). A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell, 109(3), 335–346.

    Article  CAS  PubMed  Google Scholar 

  13. Reimann, M., Lee, S., Loddenkemper, C., Dorr, J. R., Tabor, V., Aichele, P., et al. (2010). Tumor stroma-derived TGF-beta limits myc-driven lymphomagenesis via Suv39h1-dependent senescence. Cancer Cell, 17(3), 262–272.

    Article  CAS  PubMed  Google Scholar 

  14. Braumüller, H., Wieder, T., Brenner, E., Assmann, S., Hahn, M., Alkhaled, M., et al. (2013). T-helper-1-cell cytokines drive cancer into senescence. Nature, 494(7437), 361–365.

  15. Schilbach, K., Alkhaled, M., Welker, C., Eckert, F., Blank, G., Ziegler, H., et al. (2015). Cancer-targeted IL-12 controls human rhabdomyosarcoma by senescence induction and myogenic differentiation. OncoImmunology, 4(7), e1014760.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kang, T.-W., Yevsa, T., Woller, N., Hoenicke, L., Wuestefeld, T., Dauch, D., et al. (2011). Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature, 479(7374), 547–551. doi:10.1038/nature10599.

    Article  CAS  PubMed  Google Scholar 

  17. Campisi, J. (2013). Aging, cellular senescence, and cancer. Annual Review of Physiology, 75, 685–705.

    Article  CAS  PubMed  Google Scholar 

  18. Durante, M., & Loeffler, J. S. (2010). Charged particles in radiation oncology. Nature Reviews: Clinical Oncology, 7(1), 37–43.

    PubMed  Google Scholar 

  19. Friesen, C., Herr, I., Krammer, P. H., & Debatin, K. M. (1996). Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nature Medicine, 2(5), 574–577.

    Article  CAS  PubMed  Google Scholar 

  20. Mocikat, R., Braumüller, H., Gumy, A., Egeter, O., Ziegler, H., Reusch, U., et al. (2003). Natural killer cells activated by MHC class I (low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity, 19(4), 561–569.

  21. Baum, V., Buhler, P., Gierschner, D., Herchenbach, D., Fiala, G. J., Schamel, W. W., et al. (2013). Antitumor activities of PSMAxCD3 diabodies by redirected T-cell lysis of prostate cancer cells. Immunotherapy, 5(1), 27–38.

    Article  CAS  PubMed  Google Scholar 

  22. Wieder, T., Essmann, F., Prokop, A., Schmelz, K., Schulze-Osthoff, K., Beyaert, R., et al. (2001). Activation of caspase-8 in drug-induced apoptosis of B-lymphoid cells is independent of CD95/Fas receptor-ligand interaction and occurs downstream of caspase-3. Blood, 97(5), 1378–1387.

    Article  CAS  PubMed  Google Scholar 

  23. Scholz, C., Wieder, T., Starck, L., Essmann, F., Schulze-Osthoff, K., Dörken, B., et al. (2005). Arsenic trioxide triggers a regulated form of caspase-independent necrotic cell death via the mitochondrial death pathway. Oncogene, 24(11), 1904–1913.

  24. Boujrad, H., Gubkina, O., Robert, N., Krantic, S., & Susin, S. A. (2007). AIF-mediated programmed necrosis: a highly regulated way to die. Cell Cycle, 6(21), 2612–2619.

    Article  CAS  PubMed  Google Scholar 

  25. Feoktistova, M., Geserick, P., Panayotova-Dimitrova, D., & Leverkus, M. (2012). Pick your poison: the Ripoptosome, a cell death platform regulating apoptosis and necroptosis. Cell Cycle, 11(3), 460–467.

    Article  CAS  PubMed  Google Scholar 

  26. Wang, Y., Zhan, Y., Xu, R., Shao, R., Jiang, J., & Wang, Z. (2015). Src mediates extracellular signal-regulated kinase 1/2 activation and autophagic cell death induced by cardiac glycosides in human non-small cell lung cancer cell lines. Molecular Carcinogenesis, 54(Suppl 1), E26–E34.

    Article  CAS  PubMed  Google Scholar 

  27. van Spriel, A. B., Leusen, J. H., van Egmond, M., Dijkman, H. B., Assmann, K. J., Mayadas, T. N., et al. (2001). Mac-1 (CD11b/CD18) is essential for Fc receptor-mediated neutrophil cytotoxicity and immunologic synapse formation. Blood, 97(8), 2478–2486.

    Article  PubMed  Google Scholar 

  28. Sporn, M. B. (1996). The war on cancer. Lancet, 347(9012), 1377–1381.

    Article  CAS  PubMed  Google Scholar 

  29. Ewald, J. A., Desotelle, J. A., Wilding, G., & Jarrard, D. F. (2010). Therapy-induced senescence in cancer. Journal of the National Cancer Institute, 102(20), 1536–1546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nardella, C., Clohessy, J. G., Alimonti, A., & Pandolfi, P. P. (2011). Pro-senescence therapy for cancer treatment. Nature Reviews: Cancer, 11(7), 503–511.

    CAS  PubMed  Google Scholar 

  31. Acosta, J. C., & Gil, J. (2012). Senescence: a new weapon for cancer therapy. Trends in Cell Biology, 22(4), 211–219.

    Article  CAS  PubMed  Google Scholar 

  32. Xue, W., Zender, L., Miething, C., Dickins, R. A., Hernando, E., Krizhanovsky, V., et al. (2007). Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature, 445(7128), 656–660. doi:10.1038/nature05529.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rakhra, K., Bachireddy, P., Zabuawala, T., Zeiser, R., Xu, L., Kopelman, A., et al. (2010). CD4(+) T cells contribute to the remodeling of the microenvironment required for sustained tumor regression upon oncogene inactivation. Cancer Cell, 18(5), 485–498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Alimonti, A., Nardella, C., Chen, Z., Clohessy, J. G., Carracedo, A., Trotman, L. C., et al. (2010). A novel type of cellular senescence that can be enhanced in mouse models and human tumor xenografts to suppress prostate tumorigenesis. Journal of Clinical Investigation, 120(3), 681–693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Boelens, M. C., Nethe, M., Klarenbeek, S., de Ruiter, J. R., Schut, E., Bonzanni, N., et al. (2016). PTEN loss in E-cadherin-deficient mouse mammary epithelial cells rescues apoptosis and results in development of classical invasive lobular carcinoma. Cell Reports, 16(8), 2087–2101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Jolly, L. A., Massoll, N., & Franco, A. T. (2016). Immune suppression mediated by myeloid and lymphoid derived immune cells in the tumor microenvironment facilitates progression of thyroid cancers driven by HrasG12V and Pten loss. Journal of Clinical & Cellular Immunology, 7(5), 451.

    Article  Google Scholar 

  37. Benhamed, M., Herbig, U., Ye, T., Dejean, A., & Bischof, O. (2012). Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells. Nature Cell Biology, 14(3), 266–275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Haferkamp, S., Borst, A., Adam, C., Becker, T. M., Motschenbacher, S., Windhovel, S., et al. (2013). Vemurafenib induces senescence features in melanoma cells. Journal of Investigative Dermatology, 133(6), 1601–1609.

    Article  CAS  PubMed  Google Scholar 

  39. Hunder, N. N., Wallen, H., Cao, J., Hendricks, D. W., Reilly, J. Z., Rodmyre, R., et al. (2008). Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. New England Journal of Medicine, 358(25), 2698–2703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Müller-Hermelink, N., Braumüller, H., Pichler, B., Wieder, T., Mailhammer, R., Schaak, K., et al. (2008). TNFR1 signaling and IFN-gamma signaling determine whether T cells induce tumor dormancy or promote multistage carcinogenesis. Cancer Cell, 13(6), 507–518.

  41. Wolchok, J. D., Kluger, H., Callahan, M. K., Postow, M. A., Rizvi, N. A., Lesokhin, A. M., et al. (2013). Nivolumab plus ipilimumab in advanced melanoma. New England Journal of Medicine, 369(2), 122–133.

    Article  CAS  PubMed  Google Scholar 

  42. Robert, C., Long, G. V., Brady, B., Dutriaux, C., Maio, M., Mortier, L., et al. (2015). Nivolumab in previously untreated melanoma without BRAF mutation. New England Journal of Medicine, 372(4), 320–330.

    Article  CAS  PubMed  Google Scholar 

  43. Borghaei, H., Paz-Ares, L., Horn, L., Spigel, D. R., Steins, M., Ready, N. E., et al. (2015). Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. New England Journal of Medicine, 373(17), 1627–1639.

    Article  CAS  PubMed  Google Scholar 

  44. Herbst, R. S., Soria, J. C., Kowanetz, M., Fine, G. D., Hamid, O., Gordon, M. S., et al. (2014). Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature, 515(7528), 563–567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Tumeh, P. C., Harview, C. L., Yearley, J. H., Shintaku, I. P., Taylor, E. J., Robert, L., et al. (2014). PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature, 515(7528), 568–571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J. J., Cowey, C. L., & Lao, C. D., et al. (2015). Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. New England Journal of Medicine.

  47. Le, D. T., Uram, J. N., Wang, H., Bartlett, B. R., Kemberling, H., Eyring, A. D., et al. (2015). PD-1 blockade in tumors with mismatch-repair deficiency. New England Journal of Medicine, 372(26), 2509–2520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Rosenberg, J. E., Hoffman-Censits, J., Powles, T., van der Heijden, M. S., Balar, A. V., Necchi, A., et al. (2016). Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial. Lancet, 387(10031), 1909–1920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mlecnik, B., Bindea, G., Angell, H. K., Maby, P., Angelova, M., Tougeron, D., et al. (2016). Integrative analyses of colorectal cancer show immunoscore is a stronger predictor of patient survival than microsatellite instability. Immunity, 44(3), 698–711.

    Article  CAS  PubMed  Google Scholar 

  50. Topalian, S. L., Hodi, F. S., Brahmer, J. R., Gettinger, S. N., Smith, D. C., McDermott, D. F., et al. (2012). Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. New England Journal of Medicine, 366(26), 2443–2454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Brahmer, J. R., Tykodi, S. S., Chow, L. Q., Hwu, W. J., Topalian, S. L., Hwu, P., et al. (2012). Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. New England Journal of Medicine, 366(26), 2455–2465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Gatenby, R. A. (2009). A change of strategy in the war on cancer. Nature, 459(7246), 508–509.

    Article  CAS  PubMed  Google Scholar 

  53. Wieder, T., Braumüller, H., Kneilling, M., Pichler, B., & Röcken, M. (2008). T cell-mediated help against tumors. Cell Cycle, 7(19), 2974–2977.

  54. Wieder, T., Braumüller, H., Brenner, E., Zender, L., & Röcken, M. (2013). Changing T-cell enigma: cancer killing or cancer control? Cell Cycle, 12(19), 3146–3153.

  55. Finn, O. J. (2008). Cancer immunology. New England Journal of Medicine, 358(25), 2704–2715.

    Article  CAS  PubMed  Google Scholar 

  56. Schreiber, R. D., Old, L. J., & Smyth, M. J. (2011). Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science, 331(6024), 1565–1570.

    Article  CAS  PubMed  Google Scholar 

  57. Bruyere, C., & Meijer, L. (2013). Targeting cyclin-dependent kinases in anti-neoplastic therapy. Current Opinion in Cell Biology, 25(6), 772–779.

    Article  CAS  PubMed  Google Scholar 

  58. Collado, M., Gil, J., Efeyan, A., Guerra, C., Schuhmacher, A. J., Barradas, M., et al. (2005). Tumour biology: senescence in premalignant tumours. Nature, 436(7051), 642.

    Article  CAS  PubMed  Google Scholar 

  59. Lasorella, A., Benezra, R., & Iavarone, A. (2014). The ID proteins: master regulators of cancer stem cells and tumour aggressiveness. Nature Reviews: Cancer, 14(2), 77–91.

    CAS  PubMed  Google Scholar 

  60. Folkman, J., & Ingber, D. (1992). Inhibition of angiogenesis. Seminars in Cancer Biology, 3(2), 89–96.

    CAS  PubMed  Google Scholar 

  61. Hanahan, D., & Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell, 144(5), 646–674.

    Article  CAS  PubMed  Google Scholar 

  62. Daniel, P. T., Wieder, T., Sturm, I., & Schulze-Osthoff, K. (2001). The kiss of death: promises and failures of death receptors and ligands in cancer therapy. Leukemia, 15(7), 1022–1032.

    Article  CAS  PubMed  Google Scholar 

  63. Trapani, J. A., & Smyth, M. J. (2002). Functional significance of the perforin/granzyme cell death pathway. Nature Reviews: Immunology, 2(10), 735–747.

    CAS  PubMed  Google Scholar 

  64. Thiery, J., & Lieberman, J. (2014). Perforin: a key pore-forming protein for immune control of viruses and cancer. Sub-Cellular Biochemistry, 80, 197–220.

    Article  CAS  PubMed  Google Scholar 

  65. Gao, J., Shi, L. Z., Zhao, H., Chen, J., Xiong, L., He, Q., et al. (2016). Loss of IFN-gamma pathway genes in tumor cells as a mechanism of resistance to anti-CTLA-4 therapy. Cell, 167(2), 397–404.e399.

    Article  CAS  PubMed  Google Scholar 

  66. Dorand, R. D., Nthale, J., Myers, J. T., Barkauskas, D. S., Avril, S., Chirieleison, S. M., et al. (2016). Cdk5 disruption attenuates tumor PD-L1 expression and promotes antitumor immunity. Science, 353(6297), 399–403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Pencik, J., Schlederer, M., Gruber, W., Unger, C., Walker, S. M., Chalaris, A., et al. (2015). STAT3 regulated ARF expression suppresses prostate cancer metastasis. Nature Communications, 6, 7736.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Hortobagyi, G. N., Stemmer, S. M., Burris, H. A., Yap, Y. S., Sonke, G. S., Paluch-Shimon, S., et al. (2016). Ribociclib as first-line therapy for HR-positive, advanced breast cancer. New England Journal of Medicine, 375(18), 1738–1748.

    Article  CAS  PubMed  Google Scholar 

  69. Parrinello, S., Coppe, J. P., Krtolica, A., & Campisi, J. (2005). Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation. Journal of Cell Science, 118(Pt 3), 485–496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Wieder, T., Orfanos, C. E., & Geilen, C. C. (1998). Induction of ceramide-mediated apoptosis by the anticancer phospholipid analog, hexadecylphosphocholine. Journal of Biological Chemistry, 273(18), 11025–11031.

    Article  CAS  PubMed  Google Scholar 

  71. Gillies, R. J., Verduzco, D., & Gatenby, R. A. (2012). Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nature Reviews: Cancer, 12(7), 487–493.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Kayser, S., Bobeta, C., Feucht, J., Witte, K. E., Scheu, A., Bulow, H. J., et al. (2015). Rapid generation of NY-ESO-1-specific CD4 T1 cells for adoptive T-cell therapy. Oncoimmunology, 4(5), e1002723.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Prokop, A., Wrasidlo, W., Lode, H., Herold, R., Lang, F., Henze, G., et al. (2003). Induction of apoptosis by enediyne antibiotic calicheamicin thetaII proceeds through a caspase-mediated mitochondrial amplification loop in an entirely Bax-dependent manner. Oncogene, 22(57), 9107–9120.

    Article  CAS  PubMed  Google Scholar 

  74. Kaplon, J., Zheng, L., Meissl, K., Chaneton, B., Selivanov, V. A., Mackay, G., et al. (2013). A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature, 498(7452), 109–112.

    Article  CAS  PubMed  Google Scholar 

  75. Blagosklonny, M. V. (2012). Cell cycle arrest is not yet senescence, which is not just cell cycle arrest: terminology for TOR-driven aging. Aging (Albany NY), 4(3), 159–165.

    Article  CAS  Google Scholar 

  76. Finley, L. W., Carracedo, A., Lee, J., Souza, A., Egia, A., Zhang, J., et al. (2011). SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell, 19(3), 416–428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Tannahill, G. M., Curtis, A. M., Adamik, J., Palsson-McDermott, E. M., McGettrick, A. F., Goel, G., et al. (2013). Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature, 496(7444), 238–242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The work of the authors is supported by the Sander Stiftung (2012.056.1, 2012.056.2 and 2012.056.3), the Deutsche Krebshilfe (No. 109037 and 110664), the Deutsche Forschungsgemeinschaft (DFG WI 1279/4-1 and Sonderforschungsbereich SFB 685) and Fondation ARC pour la recherche sur le Cancer, Agence Nationale Recherche ANR, Fondation Pasteur-Weizmann, and Association LNCC La Ligue National Contre le Cancer. O. Bischof is CNRS-DR2.

Author information

Author notes

  1. Thomas Wieder and Ellen Brenner contributed equally.

Authors and Affiliations

  1. Department of Dermatology, Eberhard Karls University, Liebermeisterstr. 25, 72076, Tübingen, Germany

    Thomas Wieder, Ellen Brenner, Heidi Braumüller & Martin Röcken

  2. Nuclear Organization and Oncogenesis Unit, Department of Cell Biology and Infection, Institut Pasteur, 28, Rue du Dr. Roux, 75724, Paris, France

    Oliver Bischof

  3. Inserm, U993, Paris, France

    Oliver Bischof

Authors
  1. Thomas Wieder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ellen Brenner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heidi Braumüller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Oliver Bischof
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martin Röcken
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Wieder.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wieder, T., Brenner, E., Braumüller, H. et al. Cytokine-induced senescence for cancer surveillance. Cancer Metastasis Rev 36, 357–365 (2017). https://doi.org/10.1007/s10555-017-9667-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10555-017-9667-z

Keywords

Search

Navigation