A complex secretory program orchestrated by the inflammasome controls paracrine senescence

Nature Cell Biology

Volumn 15, Issue 8, 2013, Pages 978-990

  Acosta, Juan Carlos ^a,h   Banito, Ana ^a   Wuestefeld, Torsten ^b   Georgilis, Athena ^a   Janich, Peggy ^c   Morton, Jennifer P ^d   Athineos, Dimitris ^d   Kang, Tae Won ^b   Lasitschka, Felix ^e   Andrulis, Mindaugas ^e   Pascual, Gloria ^c   Morris, Kelly J ^a   Khan, Sadaf ^a   Jin, Hong ^f   Dharmalingam, Gopuraja ^a   Snijders, Ambrosius P ^a   Carroll, Thomas ^a   Capper, David ^e   Pritchard, Catrin ^f   Inman, Gareth J ^g   Longerich, Thomas ^e   Sansom, Owen J ^d   Benitah, Salvador Aznar ^c   Zender, Lars ^b   Gil, Jesús ^a   more..

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f UNIVERSITY OF LEICESTER   (United Kingdom)

^g UNIVERSITY OF DUNDEE   (United Kingdom)

^h UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; B RAF KINASE; CXCL1 CHEMOKINE; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2B; CYTOKERATIN 5; INFLAMMASOME; INTERLEUKIN 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VASCULOTROPIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL AGING; CELL CULTURE; CELL CYCLE ARREST; CELL ONCOGENE; COCULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; IN VIVO STUDY; MOUSE; NONHUMAN; ONCOGENE INDUCED SENESCENCE; PARACRINE SIGNALING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; QUANTITATIVE ANALYSIS; SENESCENCE ASSOCIATED SECRETORY PHENOTYPE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ANIMALS; CELL AGING; CELL LINE, TUMOR; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMASOMES; INTERLEUKIN-1; MICE; MODELS, ANIMAL; PARACRINE COMMUNICATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84881399206     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2784     Document Type: Article

References (53)

1. Kuilman, T., Michaloglou, C., Mooi, W. J. & Peeper, D. S. The essence of senescence. Genes Dev. 24, 2463-2479 (2010).
2. Campisi, J. & d'Adda di Fagagna, F. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8, 729-740 (2007). (Pubitemid 47312822)
3. Kuilman, T. & Peeper, D.S. Senescence-messaging secretome: SMS-ing cellular stress. Nat. Rev. Cancer 9, 81-94 (2009).
4. Coppe, J. P. et al. A human-like senescence-associated secretory phenotype is conserved in mouse cells dependent on physiological oxygen. PLoS One 5, e9188 (2010).
5. Krtolica, A., Parrinello, S., Lockett, S., Desprez, P. Y. & Campisi, J. Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc. Natl Acad. Sci. USA 98, 12072-12077 (2001). (Pubitemid 32959828)
6. Coppe, J. P., Kauser, K., Campisi, J. & Beausejour, C. M. Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J. Biol. Chem. 281, 29568-29574 (2006). (Pubitemid 44536964)
7. Coppe, J. P. et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868 (2008).
8. Acosta, J. C. et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133, 1006-1018 (2008). (Pubitemid 351795610)
9. Kuilman, T. et al. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133, 1019-1031 (2008). (Pubitemid 351787746)
10. Kortlever, R. M., Higgins, P. J. & Bernards, R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat. Cell Biol. 8, 877-884 (2006).
11. Wajapeyee, N., Serra, R. W., Zhu, X., Mahalingam, M. & Green, M. R. Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132, 363-374 (2008). (Pubitemid 351191995)
12. Kang, T. W. et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 479, 547-551 (2011).
13. Xue, W. et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445, 656-660 (2007). (Pubitemid 46232886)
14. Krizhanovsky, V. et al. Senescence of activated stellate cells limits liver fibrosis. Cell 134, 657-667 (2008).
15. Hayflick, L. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636 (1965).
16. Hayflick, L. & Moorhead, P. S. The serial cultivation of human diploid cell strains. Exp. Cell Res. 25, 585-621 (1961).
17. Nelson, G. et al. A senescent cell bystander effect: senescence-induced senescence. Aging Cell 11, 345-349 (2012).
18. Fridman, A. L. & Tainsky, M. A. Critical pathways in cellular senescence and immortalization revealed by gene expression profiling. Oncogene 27, 5975-5987 (2008).
19. Collado, M. et al. Tumour biology: senescence in premalignant tumours. Nature 436, 642 (2005). (Pubitemid 41117258)
20. Massague, J. TGFbeta in Cancer. Cell 134, 215-230 (2008).
21. Kaneda, A. et al. Activation of Bmp2-Smad1 signal and its regulation by coordinated alteration of H3K27 trimethylation in Ras-induced senescence. PLoS Genet. 7, e1002359 (2011).
22. Reynisdottir, I., Polyak, K., Iavarone, A. & Massague, J. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β. Genes Dev. 9, 1831-1845 (1995).
23. Hingorani, S. R. et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4, 437-450 (2003). (Pubitemid 38050041)
24. Morton, J. P. et al. Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc. Natl Acad. Sci. USA 107, 246-251 (2010).
25. Larsson, J. et al. Abnormal angiogenesis but intact hematopoietic potential in TGF-β type I receptor-deficient mice. EMBO J. 20, 1663-1673 (2001). (Pubitemid 32299403)
26. Morton, J. P. et al. LKB1 haploinsufficiency cooperates with Kras to promote pancreatic cancer through suppression of p21-dependent growth arrest. Gastroenterology 139, 586-597 (2010).
27. Morton, J. P. et al. Dasatinib inhibits the development of metastases in a mouse model of pancreatic ductal adenocarcinoma. Gastroenterology 139, 292-303 (2010).
28. Orjalo, A. V., Bhaumik, D., Gengler, B. K., Scott, G. K. & Campisi, J. Cell surface-bound IL-1α is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc. Natl Acad. Sci. USA 106, 17031-17036 (2009).
29. Schroder, K. & Tschopp, J. The inflammasomes. Cell 140, 821-832 (2010).
30. Strowig, T., Henao-Mejia, J., Elinav, E. & Flavell, R. Inflammasomes in health and disease. Nature 481, 278-286 (2012).
31. Carragher, L. A. et al. V600EBraf induces gastrointestinal crypt senescence and promotes tumour progression through enhanced CpG methylation of p16INK4a. EMBO Mol. Med. 2, 458-471 (2010).
32. Keller, M., Ruegg, A., Werner, S. & Beer, H. D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 132, 818-831 (2008). (Pubitemid 351312798)
33. Sibilia, M. et al. The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell 102, 211-220 (2000).
34. Kriegl, L. et al. Up and downregulation of p16(Ink4a) expression in BRAF-mutated polyps/adenomas indicates a senescence barrier in the serrated route to colon cancer. Mod. Pathol. 24, 1015-1022 (2011).
35. Bennecke, M. et al. Ink4a/Arf and oncogene-induced senescence prevent tumor progression during alternative colorectal tumorigenesis. Cancer Cell 18, 135-146 (2010).
36. Caruso, M. et al. Over-expression of cathepsin E and trefoil factor 1 in sessile serrated adenomas of the colorectum identified by gene expression analysis. Virchows Archiv. 454, 291-302 (2009).
37. Schmitt, C. A. Cellular senescence and cancer treatment. Biochim. Biophys. Acta 1775, 5-20 (2007). (Pubitemid 44881196)
38. Prise, K. M. & O'Sullivan, J. M. Radiation-induced bystander signalling in cancer therapy. Nature Rev. Cancer 9, 351-360 (2009).
39. Baker, D.J. et al. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479, 232-236 (2011).
40. Burd, C. E. et al. Monitoring tumorigenesis and senescence in vivo with a p16(INK4a)-luciferase model. Cell 152, 340-351 (2013).
41. Chien, Y. et al. Control of the senescence-associated secretory phenotype by NF-{K}B promotes senescence and enhances chemosensitivity. Genes Dev. 25, 2125-2136 (2011).
42. Jing, H. et al. Opposing roles of NF-{K}B in anti-cancer treatment outcome unveiled by cross-species investigations. Genes Dev. 25, 2137-2146 (2011).
43. Zitvogel, L, Kepp, O., Galluzzi, L. & Kroemer, G. Inflammasomes in carcinogenesis and anticancer immune responses. Nat. Immun. 13, 343-351 (2012).
44. Ling, J. et al. KrasG12D-induced IKK2/ß/NF-KB activation by IL-1a and p62 feedforward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell 21, 105-120(2012).
45. Barradas, M. et al. Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev. 23, 1177-1182 (2009).
46. Banito, A. & Gil, J. Induced pluripotent stem cells and senescence: learning the biology to improve the technology. EMBO Rep. 11, 353-359 (2010).
47. Banito, A. et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 23, 2134-2139 (2009).
48. Bishop, C.L. et al. Primary cilium-dependent and-independent Hedgehog signaling inhibits p16(INK4A). Mol. Cell 40, 533-547 (2010).
49. Acosta, J. C., Snijders, A. P. & Gil, J. Unbiased characterization of the senescence-associated secretome using SILAC-based quantitative proteomics. Methods Mol. Biol. 965, 175-184 (2013).
50. Chen, Y. et al. SPD-a web-based secreted protein database. Nucleic Acids Res. 33, D169-D73 (2005).
51. Gonzalez, R. et al. Screening the mammalian extracellular proteome for regulators of embryonic human stem cell pluripotency. Proc. Natl Acad. Sci. USA 107, 3552-3557 (2010).
52. Jackson, E. L. et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15, 3243-3248 (2001). (Pubitemid 34008190)
53. Capper, D. et al. Assessment of BRAF V600E mutation status by immunohisto-chemistry with a mutation-specific monoclonal antibody. Acta Neuropathol. 122, 11-19 (2011).