NOTCH1 mediates a switch between two distinct secretomes during senescence

Nature Cell Biology

Volumn 18, Issue 9, 2016, Pages 979-992

  Hoare, Matthew ^a,b   Ito, Yoko ^a   Kang, Tae Won ^c,d   Weekes, Michael P ^b,e   Matheson, Nicholas J ^b,e   Patten, Daniel A ^f   Shetty, Shishir ^f   Parry, Aled J ^a   Menon, Suraj ^a   Salama, Rafik ^a   Antrobus, Robin ^e   Tomimatsu, Kosuke ^a   Howat, William ^a   Lehner, Paul J ^b,e   Zender, Lars ^c,d   Narita, Masashi ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; CYTOKINE; JAGGED1; NOTCH RECEPTOR; NOTCH1 RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; NOTCH1 PROTEIN, HUMAN; NOTCH1 PROTEIN, MOUSE;

ARTICLE; CELL AGING; CONTROLLED STUDY; GENE; GENE FUNCTION; HUMAN; HUMAN CELL; IN VIVO STUDY; LYMPHOCYTE MIGRATION; MOLECULAR DYNAMICS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BLOCKING; SECRETOME GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL CYCLE CHECKPOINT; GENETICS; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; CELL AGING; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; HUMANS; MICE, TRANSGENIC; RECEPTOR, NOTCH1; TRANSFORMING GROWTH FACTOR BETA;

EID: 84982133301     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3397     Document Type: Article

References (66)

1. Campisi, J. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 75, 685-705 (2013
2. Kuilman, T., & Peeper, D. S. Senescence-messaging secretome: SMS-ing cellular stress. Nat. Rev. Cancer 9, 81-94 (2009
3. Childs, B. G., Durik, M., Baker, D. J., & van Deursen, J. M. Cellular senescence in aging and age-related disease: from mechanisms to therapy. Nat. Med. 21, 1424-1435 (2015
4. Acosta, J. C., et al. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat. Cell Biol. 15, 978-990 (2013
5. Hubackova, S., Krejcikova, K., Bartek, J., & Hodny, Z. IL1-And TGFβ-Nox4 signaling, oxidative stress and DNA damage response are shared features of replicative, oncogene-induced, and drug-induced paracrine ?Bystander senescence?. Aging (Albany NY) 4, 932-951 (2012
6. Kuilman, T., et al. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133, 1019-1031 (2008
7. Krizhanovsky, V., et al. Senescence of activated stellate cells limits liver fibrosis. Cell 134, 657-667 (2008
8. Kang, T.-W., et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 479, 547-551 (2011
9. Xue, W., et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445, 656-660 (2007
10. 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
11. Coppé, J.-P., et al. Senescence-Associated secretory phenotypes reveal cellnonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868 (2008
12. Kopan, R., & Ilagan, M. X. G. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233 (2009
13. Ntziachristos, P., Lim, J. S., Sage, J., & Aifantis, I. From fly wings to targeted cancer therapies: a centennial for notch signaling. Cancer Cell 25, 318-334 (2014
14. Weekes, M. P., et al. Latency-Associated degradation of the MRP1 drug transporter during latent human cytomegalovirus infection. Science 340, 199-202 (2013
15. Young, A. R. J., et al. Autophagy mediates the mitotic senescence transition. Genes Dev. 23, 798-803 (2009
16. Cui, H., Kong, Y., Xu, M., & Zhang, H. Notch3 functions as a tumor suppressor by controlling cellular senescence. Cancer Res. 73, 3451-3459 (2013
17. Kagawa, S., et al. Cellular senescence checkpoint function determines differential Notch1-dependent oncogenic and tumor-suppressor activities. Oncogene 34, 2347-2359 (2015
18. Procopio, M.-G., et al. Combined CSL and p53 downregulation promotes cancerassociated fibroblast activation. Nat. Cell Biol. 17, 1193-1204 (2015
19. Kirschner, K., et al. Phenotype specific analyses reveal distinct regulatory mechanism for chronically activated p53. PLoS Genet. 11, e1005053 (2015
20. Acosta, J. C., et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133, 1006-1018 (2008
21. Orjalo, A. V., Bhaumik, D., Gengler, B. K., Scott, G. K., & Campisi, J. Cell surfacebound IL-1alpha is an upstream regulator of the senescence-Associated IL-6/IL-8 cytokine network. Proc. Natl Acad. Sci. USA 106, 17031-17036 (2009
22. Fryer, C. J., Lamar, E., Turbachova, I., Kintner, C., & Jones, K. A. Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev. 16, 1397-1411 (2002
23. Lee, B. Y., et al. Senescence-Associated beta-galactosidase is lysosomal betagalactosidase. Aging Cell 5, 187-195 (2006
24. Hata, A., Lo, R. S., Wotton, D., Lagna, G., & Massague, J. Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 388, 82-87 (1997
25. Lewis, J. Notch signalling and the control of cell fate choices in vertebrates. Semin. Cell Dev. Biol. 9, 583-589 (1998
26. Hartman, B. H., Reh, T. A., & Bermingham-McDonogh, O. Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc. Natl Acad. Sci. USA 107, 15792-15797 (2010
27. D'Souza, B., Miyamoto, A., & Weinmaster, G. The many facets of Notch ligands. Oncogene 27, 5148-5167 (2008
28. Kurpinski, K., et al. Transforming growth factor-beta and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells 28, 734-742 (2010
29. Collado, M., et al. Tumour biology: senescence in premalignant tumours. Nature 436, 642 (2005
30. Hingorani, S. R., et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4, 437-450 (2003
31. Miyamoto, Y., et al. Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 3, 565-576 (2003
32. Avila, J. L., & Kissil, J. L. Notch signaling in pancreatic cancer: oncogene or tumor suppressor? Trends Mol. Med. 19, 320-327 (2013
33. Caldwell, M. E., et al. Cellular features of senescence during the evolution of human and murine ductal pancreatic cancer. Oncogene 31, 1599-1608 (2011
34. Lee, W.-Y., & Kubes, P. Leukocyte adhesion in the liver: distinct adhesion paradigm from other organs. J. Hepatol. 48, 504-512 (2008
35. Shetty, S., Weston, C. J., Adams, D. H., & Lalor, P. F. A flow adhesion assay to study leucocyte recruitment to human hepatic sinusoidal endothelium under conditions of shear stress. J. Vis. Exp. http://dx.doi.org/10.3791/51330 (2014
36. Chien, Y., et al. Control of the senescence-Associated secretory phenotype by NF-kappa;B promotes senescence and enhances chemosensitivity. Genes Dev. 25, 2125-2136 (2011
37. Huggins, C. J., et al. C/EBP suppresses senescence and inflammatory gene expression by heterodimerizing with C/EBP. Mol. Cell. Biol. 33, 3242-3258 (2013
38. Nakazato, Y., et al. Interleukin (IL)-1 and IL-4 synergistically stimulate NF-IL6 activity and IL-6 production in human mesangial cells. Kidney Int. 54, 71-79 (1998
39. ENCODE Project Consortium, An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012
40. Roadmap Epigenomics Consortium, et al. Integrative analysis of 111 reference human epigenomes. Nature 518, 317-330 (2015
41. Jin, F., et al. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503, 290-294 (2013
42. Storer, M., et al. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 155, 1119-1130 (2013
43. Muñoz-Espín, D., et al. Programmed cell senescence during mammalian embryonic development. Cell 155, 1104-1118 (2013
44. Kang, C., et al. The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science 349, aaa5612 (2015
45. Boni, A., et al. Notch1 regulates the fate of cardiac progenitor cells. Proc. Natl Acad. Sci. USA 105, 15529-15534 (2008
46. Pitt, L. A., et al. CXCL12-producing vascular endothelial niches control acute T cell leukemia maintenance. Cancer Cell 27, 755-768 (2015
47. Baker, D. J., et al. Clearance of p16Ink4a-positive senescent cells delays ageingassociated disorders. Nature 479, 232-236 (2011
48. Dörr, J. R., et al. Synthetic lethal metabolic targeting of cellular senescence in cancer therapy. Nature 501, 421-425 (2013
49. Yagüe, E., et al. Ability to acquire drug resistance arises early during the tumorigenesis process. Cancer Res. 67, 1130-1137 (2007
50. Narita, M., et al. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 126, 503-514 (2006
51. Aziz, N., Cherwinski, H., & McMahon, M. Complementation of defective colonystimulating factor 1 receptor signaling and mitogenesis by Raf and v-Src. Mol. Cell. Biol. 19, 1101-1115 (1999
52. Capobianco, A. J., Zagouras, P., Blaumueller, C. M., Artavanis-Tsakonas, S., & Bishop, J. M. Neoplastic transformation by truncated alleles of human NOTCH1/TAN1 and NOTCH2. Mol. Cell. Biol. 17, 6265-6273 (1997
53. Cox, J., et al. A practical guide to the MaxQuant computational platform for SILACbased quantitative proteomics. Nat. Protoc. 4, 698-705 (2009
54. Trapnell, C., Pachter, L., & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009
55. Anders, S., & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010
56. 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
57. Sadaie, M., et al. Redistribution of the Lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev. 27, 1800-1808 (2013
58. Subramanian, A., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005
59. Livak, K. J., & Schmittgen, T. D. Analysis of relative gene expression data using real-Time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408 (2001
60. Shetty, S., et al. Common lymphatic endothelial and vascular endothelial receptor-1 mediates the transmigration of regulatory T cells across human hepatic sinusoidal endothelium. J. Immunol. 186, 4147-4155 (2011
61. Lalor, P. F., et al. Vascular adhesion protein-1 mediates adhesion and transmigration of lymphocytes on human hepatic endothelial cells. J. Immunol. 169, 983-992 (2002
62. Pruitt, K. D., et al. RefSeq: an update on mammalian reference sequences. Nucleic Acids Res. 42, D756-D763 (2014
63. Harrow, J., et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760-1774 (2012
64. Schmidt, D., et al. ChIP-seq: using high-Throughput sequencing to discover protein-DNA interactions. Methods 48, 240-248 (2009
65. Sargent, J. L., et al. A TGFβ-responsive gene signature is associated with a subset of diffuse scleroderma with increased disease severity. J. Invest. Dermatol. 130, 694-705 (2010
66. Brennan, E. P., et al. Next-generation sequencing identifies TGF-β1-Associated gene expression profiles in renal epithelial cells reiterated in human diabetic nephropathy. Biochim. Biophys. Acta 1822, 589-599 (2012