Tissue damage and senescence provide critical signals for cellular reprogramming in vivo

Science

Volumn 354, Issue 6315, 2016, Pages

  Mosteiro, Lluc ^a   Pantoja, Cristina ^a   Alcazar, Noelia ^a   Marión, Rosa M ^a   Chondronasiou, Dafni ^a   Rovira, Miguel ^a   Fernandez Marcos, Pablo J ^a,b   Muñoz Martin, Maribel ^a   Blanco Aparicio, Carmen ^a   Pastor, Joaquin ^a   Gómez López, Gonzalo ^a   De Martino, Alba ^a   Blasco, Maria A ^a   Abad, María ^a,c   Serrano, Manuel ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b IMDEA FOOD INSTITUTE   (Spain)

^c VALL D HEBRON UNIVERSITY HOSPITAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2; ANILINE DERIVATIVE; ANTINEOPLASTIC AGENT; CDKN2A PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; MYC PROTEIN, MOUSE; NAVITOCLAX; POU5F1 PROTEIN, MOUSE; SOX2 PROTEIN, MOUSE; SULFONAMIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX;

APOPTOSIS; CELLS AND CELL COMPONENTS; GENE EXPRESSION; GENETIC ANALYSIS; INJURY; MUSCLE; PROTEIN; SENESCENCE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEDIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GENE LOCUS; GENETIC ANALYSIS; IN VIVO STUDY; INDUCED PLURIPOTENT STEM CELL; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; ONCOGENE C MYC; PRIORITY JOURNAL; SENESCENCE; TERATOMA; TISSUE INJURY; TISSUE REPAIR; ANIMAL; C57BL MOUSE; CELL AGING; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

MUS;

ANILINE COMPOUNDS; ANIMALS; ANTINEOPLASTIC AGENTS; CELL AGING; CELLULAR REPROGRAMMING; CYCLIN-DEPENDENT KINASE INHIBITOR P16; GENE EXPRESSION REGULATION; GENETIC LOCI; INDUCED PLURIPOTENT STEM CELLS; INTERLEUKIN-6; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C57BL; OCTAMER TRANSCRIPTION FACTOR-3; PROTO-ONCOGENE PROTEINS C-MYC; SOXB1 TRANSCRIPTION FACTORS; SULFONAMIDES; TERATOMA; TRANSCRIPTION FACTORS;

EID: 84997501267     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aaf4445     Document Type: Article

References (45)

1. D. A. Robinton, G. Q. Daley, The promise of induced pluripotent stem cells in research and therapy. Nature 481, 295-305 (2012). doi: 10.1038/nature10761; pmid: 22258608
2. K. Takahashi, S. Yamanaka, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006). doi: 10.1016/j.cell.2006.07.024; pmid: 16904174
3. M. Abad et al., Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502, 340-345 (2013). doi: 10.1038/nature12586; pmid: 24025773
4. K. Ohnishi et al., Premature termination of reprogramming in vivo leads to cancer development through altered epigenetic regulation. Cell 156, 663-677 (2014). doi: 10.1016/j.cell.2014.01.005; pmid: 24529372
5. Y. Zhao et al., Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell 3, 475-479 (2008). doi:10.1016/j.stem.2008.10.002; pmid: 18983962
6. A. Banito et al., Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev. 23, 2134-2139 (2009). doi: 10.1101/gad.1811609; pmid: 19696146
7. H. Li et al., The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460, 1136-1139 (2009). doi: 10.1038/nature08290; pmid: 19668188
8. R. M. Marión et al., A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460, 1149-1153 (2009). doi: 10.1038/nature08287; pmid: 19668189
9. T. Kawamura et al., Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460, 1140-1144 (2009). doi: 10.1038/nature08311; pmid: 19668186
10. J. Utikal et al., Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 460, 1145-1148 (2009). doi: 10.1038/nature08285; pmid: 19668190
11. H. Hong et al., Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460, 1132-1135 (2009). doi: 10.1038/nature08235; pmid: 19668191
12. A. Freund, A. V. Orjalo, P.-Y. Desprez, J. Campisi, Inflammatory networks during cellular senescence: Causes and consequences. Trends Mol. Med. 16, 238-246 (2010). doi: 10.1016/j.molmed.2010.03.003; pmid: 20444648
13. R. Salama, M. Sadaie, M. Hoare, M. Narita, Cellular senescence and its effector programs. Genes Dev. 28, 99-114 (2014). doi: 10.1101/gad.235184.113; pmid: 24449267
14. J.-P. Coppé et al., Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLOS Biol. 6, 2853-2868 (2008). pmid: 19053174
15. T. Kuilman et al., Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133, 1019-1031 (2008). doi: 10.1016/j.cell.2008.03.039; pmid: 18555778
16. J. C. Acosta et al., Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133, 1006-1018 (2008). doi: 10.1016/j.cell.2008.03.038; pmid: 18555777
17. C. López-Otín, M. A. Blasco, L. Partridge, M. Serrano, G. Kroemer, The hallmarks of aging. Cell 153, 1194-1217 (2013). doi: 10.1016/j.cell.2013.05.039; pmid: 23746838
18. D. Muñoz-Espin, M. Serrano, Cellular senescence: From physiology to pathology. Nat. Rev. Mol. Cell Biol. 15, 482-496 (2014). doi: 10.1038/nrm3823; pmid: 24954210
19. J. Chang et al., Clearance of senescent cells by ABT263 rejuvenates aged hematopoietic stem cells in mice. Nat. Med. 22, 78-83 (2016). doi: 10.1038/nm.4010; pmid: 26657143
20. Y. Zhu et al., Identification of a novel senolytic agent, navitoclax, targeting the Bcl-2 family of anti-apoptotic factors. Aging Cell 15, 428-435 (2015). doi: 10.1111/acel.12445; pmid: 26711051
21. R. Yosef et al., Directed elimination of senescent cells by inhibition of BCL-W and BCL-XL. Nat. Commun. 7, 11190 (2016). doi: 10.1038/ncomms11190; pmid: 27048913
22. M. A. Dickson, Molecular pathways: CDK4 inhibitors for cancer therapy. Clin. Cancer Res. 20, 3379-3383 (2014). doi: 10.1158/1078-0432.CCR-13-1551; pmid: 24795392
23. Y. Chien et al., Control of the senescence-associated secretory phenotype by NF-κB promotes senescence and enhances chemosensitivity. Genes Dev. 25, 2125-2136 (2011). doi: 10.1101/gad.17276711; pmid: 21979375
24. A. Freund, C. K. Patil, J. Campisi, p38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J. 30, 1536-1548 (2011). doi: 10.1038/emboj.2011.69; pmid: 21399611
25. A. V. Gasparian et al., Targeting transcription factor NFκB: Comparative analysis of proteasome and IKK inhibitors. Cell Cycle 8, 1559-1566 (2009). doi: 10.4161/cc.8.10.8415; pmid: 19372735
26. J. C. Acosta et al., A complex secretory program orchestrated by the inflammasome controlsparacrine senescence. Nat. Cell Biol. 15,978-990 (2013). doi: 10.1038/ncb2784;pmid:23770676
27. J. J. Brady et al., Early role for IL-6 signalling during generation of induced pluripotent stem cells revealed by heterokaryon RNA-Seq. Nat. Cell Biol. 15, 1244-1252 (2013). doi: 10.1038/ncb2835; pmid: 23995732
28. M. Narlik-Grassow, C. Blanco-Aparicio, A. Carnero, The PIM family of serine/threonine kinases in cancer. Med. Res. Rev. 34, 136-159 (2014). doi: 10.1002/med.21284; pmid: 23576269
29. K. Kim, J. H. Kim, B. U. Youn, H. M. Jin, N. Kim, Pim-1 regulates RANKL-induced osteoclastogenesis via NF-κB activation and NFATc1 induction. J. Immunol. 185, 7460-7466 (2010). doi: 10.4049/jimmunol.1000885; pmid: 21068407
30. K. Nihira et al., Pim-1 controls NF-κB signalling by stabilizing RelA/p65. Cell Death Differ. 17, 689-698 (2010). doi: 10.1038/cdd.2009.174; pmid: 19911008
31. K. Aoshiba, T. Tsuji, A. Nagai, Bleomycin induces cellular senescence in alveolar epithelial cells. Eur. Respir. J. 22,436-443 (2003). doi: 10.1183/09031936.03.00011903; pmid: 14516132
32. K. Aoshiba et al., Senescence-associated secretory phenotype in a mouse model of bleomycin-induced lung injury. Exp. Toxicol. Pathol. 65, 1053-1062 (2013). doi: 10.1016/j.etp.2013.04.001; pmid: 23688655
33. M. A. Blasco et al., Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91, 25-34 (1997). doi: 10.1016/s0092-8674(01)80006-4; pmid: 9335332
34. I. García-Cao et al., Increased p53 activity does not accelerate telomere-driven ageing. EMBO Rep. 7, 546-552 (2006). doi: 10.1038/sj.embor.7400667; pmid: 16582880
35. J. Krishnamurthy et al., Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 114, 1299-1307 (2004). doi: 10.1172/JC122475; pmid: 15520862
36. C. Soria-Valles, C. López-Otín, iPSCs: On the road to reprogramming aging. Trends Mol. Med. 22, 713-724 (2016). doi: 10.1016/j.molmed.2016.05.010; pmid: 27286740
37. K. R. Jessen, R. Mirsky, P. Arthur-Farraj, The role of cell plasticity in tissue repair: Adaptive cellular reprogramming. Dev. Cell 34, 613-620 (2015). doi: 10.1016/j.devcel.2015.09.005; pmid: 26418293
38. T. Jacks et al., Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4,1-7 (1994). doi: 10.1016/S0960-9822(00)00002-6; pmid: 7922305
39. M. Serrano et al., Role of the INK4a locus in tumor suppression and cell mortality. Cell 85, 27-37 (1996). doi: 10.1016/S0092-8674(00)81079-X; pmid: 8620534
40. X. Fu, The immunogenicity of cells derived from induced pluripotent stem cells. Cell. Mol. Immunol. 11, 14-16 (2014). doi: 10.1038/cmi.2013.60; pmid: 24336164
41. R. A. Dickins et al., Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat. Genet. 37, 1289-1295 (2005). doi: 10.1038/ng1651; pmid: 16200064
42. C. Trapnell et al., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012). doi: 10.1038/nprot.2012.016; pmid: 22383036
43. B. Langmead, C. Trapnell, M. Pop, S. L. Salzberg, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009). doi: 10.1186/gb-2009-10-3-r25; pmid: 19261174
44. H. Li et al., The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009). doi: 10.1093/bioinformatics/btp352; pmid: 19505943
45. A. Subramanian et al., Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550 (2005). doi: 10.1073/pnas.0506580102; pmid: 16199517