Cellular senescence mediated by p16INK4A-coupled miRNA pathways

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 1606-1618

  Overhoff, Marita G ^a   Garbe, James C ^b   Koh, James ^c   Stampfer, Martha R ^b   Beach, David H ^a   Bishop, Cleo L ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; EMBRYONIC ECTODERM DEVELOPMENT PROTEIN; MICRORNA; MICRORNA 181A; MICRORNA 210; MICRORNA 26B; MICRORNA 424; POLYCOMB GROUP PROTEIN; PROTEIN CBX7; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BREAST EPITHELIUM; CELL AGING; CELL CYCLE ARREST; CELLULAR SENESCENCE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPIGENETICS; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROARRAY ANALYSIS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; YOUNG ADULT;

CELL AGING; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; EPIGENESIS, GENETIC; FEEDBACK, PHYSIOLOGICAL; FIBROBLASTS; GENE SILENCING; HUMANS; MICRORNAS; POLYCOMB-GROUP PROTEINS; YOUNG ADULT;

EID: 84896732413     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1096     Document Type: Article

References (50)

1. Hayflick, L. (1965) The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res., 37, 614-636.
2. Michaloglou, C., Vredeveld, L.C., Soengas, M.S., Denoyelle, C., Kuilman, T., van der Horst, C.M., Majoor, D.M., Shay, J.W., Mooi, W.J. and Peeper, D.S. (2005) BRAFE600-Associated senescence-like cell cycle arrest of human naevi. Nature, 436, 720-724.
3. Krishnamurthy, J., Torrice, C., Ramsey, M.R., Kovalev, G.I., Al- Regaiey, K., Su, L. and Sharpless, N.E. (2004) Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest., 114, 1299-1307.
4. Campisi, J. and dAdda di Fagagna, F. (2007) Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol., 8, 729-740.
5. Scott, L.J., Mohlke, K.L., Bonnycastle, L.L., Willer, C.J., Li, Y., Duren, W.L., Erdos, M.R., Stringham, H.M., Chines, P.S., Jackson, A.U. et al. (2007) A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science, 316, 1341-1345.
6. Saxena, R., Voight, B.F., Lyssenko, V., Burtt, N.P., de Bakker, P.I., Chen, H., Roix, J.J., Kathiresan, S., Hirschhorn, J.N., Daly, M.J. et al. (2007) Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science, 316, 1331-1336.
7. Zeggini, E., Weedon, M.N., Lindgren, C.M., Frayling, T.M., Elliott, K.S., Lango, H., Timpson, N.J., Perry, J.R., Rayner, N.W., Freathy, R.M. et al. (2007) Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science, 316, 1336-1341.
8. McPherson, R., Pertsemlidis, A., Kavaslar, N., Stewart, A., Roberts, R., Cox, D.R., Hinds, D.A., Pennacchio, L.A., Tybjaerg- Hansen, A., Folsom, A.R. et al. (2007) A common allele on chromosome 9 associated with coronary heart disease. Science, 316, 1488-1491.
9. Trust, T.W. (2007) Genome-wide association study of 14 000 cases of seven common diseases and 3000 shared controls. Nature, 447, 661-678.
10. Zindy, F., Quelle, D.E., Roussel, M.F. and Sherr, C.J. (1997) Expression of the p16INK4a tumor suppressor versus other INK4 family members during mouse development and aging. Oncogene, 15, 203-211.
11. Garbe, J.C., Bhattacharya, S., Merchant, B., Bassett, E., Swisshelm, K., Feiler, H.S., Wyrobek, A.J. and Stampfer, M.R. (2009) Molecular distinctions between stasis and telomere attrition senescence barriers shown by long-term culture of normal human mammary epithelial cells. Cancer Res., 69, 7557-7568.
12. Itahana, K., Zou, Y., Itahana, Y., Martinez, J.L., Beausejour, C., Jacobs, J.J., Van Lohuizen, M., Band, V., Campisi, J. and Dimri, G.P. (2003) Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol. Cell Biol., 23, 389-401.
13. Gil, J., Bernard, D., Martinez, D. and Beach, D. (2004) Polycomb CBX7 has a unifying role in cellular lifespan. Nat. Cell Biol., 6, 67-72.
14. Dietrich, N., Bracken, A.P., Trinh, E., Schjerling, C.K., Koseki, H., Rappsilber, J., Helin, K. and Hansen, K.H. (2007) Bypass of senescence by the polycomb group protein CBX8 through direct binding to the INK4A-ARF locus. EMBO J., 26, 1637-1648.
15. Bracken, A.P., Kleine-Kohlbrecher, D., Dietrich, N., Pasini, D., Gargiulo, G., Beekman, C., Theilgaard-Monch, K., Minucci, S., Porse, B.T., Marine, J.C. et al. (2007) The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev., 21, 525-530.
16. Mills, A.A. (2010) Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat. Rev. Cancer, 10, 669-682.
17. Hock, H. (2012) A complex Polycomb issue: the two faces of EZH2 in cancer. Genes Dev., 26, 751-755.
18. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
19. Ambros, V. (2004) The functions of animal microRNAs. Nature, 431, 350-355.
20. Boehm, M. and Slack, F. (2005) A developmental timing microRNA and its target regulate life span in C. elegans. Science, 310, 1954-1957.
21. Maes, O.C., Sarojini, H. and Wang, E. (2009) Stepwise upregulation of microRNA expression levels from replicating to reversible and irreversible growth arrest states in WI-38 human fibroblasts. J. Cell Physiol., 221, 109-119.
22. Ito, T., Yagi, S. and Yamakuchi, M. (2010) MicroRNA-34a regulation of endothelial senescence. Biochem. Biophys. Res. Commun., 398, 735-740.
23. Zhao, T., Li, J. and Chen, A.F. (2010) MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am. J. Physiol. Endocrinol. Metab., 299, E110-E116.
24. Li, X., Khanna, A., Li, N. and Wang, E. (2011) Circulatory miR34a as an RNAbased, noninvasive biomarker for brain aging. Aging (Albany NY), 3, 985-1002.
25. Yang, J., Chen, D., He, Y., Melendez, A., Feng, Z., Hong, Q., Bai, X., Li, Q., Cai, G., Wang, J. et al. (2011) MiR-34 modulates Caenorhabditis elegans lifespan via repressing the autophagy gene atg9. Age (Dordr), 35, 11-22.
26. Li, N., Muthusamy, S., Liang, R., Sarojini, H. and Wang, E. (2011) Increased expression of miR-34a and miR-93 in rat liver during aging, and their impact on the expression of Mgst1 and Sirt1. Mech. Ageing Dev., 132, 75-85.
27. Romanov, S.R., Kozakiewicz, B.K., Holst, C.R., Stampfer, M.R., Haupt, L.M. and Tlsty, T.D. (2001) Normal human mammary epithelial cells spontaneously escape senescence and acquire genomic changes. Nature, 409, 633-637.
28. Bishop, C.L., Bergin, A.M., Fessart, D., Borgdorff, V., Hatzimasoura, E., Garbe, J.C., Stampfer, M.R., Koh, J. and Beach, D.H. (2010) Primary cilium-dependent and -independent Hedgehog signaling inhibits p16(INK4A). Mol. Cell, 40, 533-547.
29. Ritchie, M.E., Silver, J., Oshlack, A., Holmes, M., Diyagama, D., Holloway, A. and Smyth, G.K. (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics, 23, 2700-2707.
30. Borgdorff, V., Lleonart, M.E., Bishop, C.L., Fessart, D., Bergin, A.H., Overhoff, M.G. and Beach, D.H. (2010) Multiple microRNAs rescue from Ras-induced senescence by inhibiting p21(Waf1/Cip1). Oncogene, 29, 2262-2271.
31. Garbe, J.C., Pepin, F., Pelissier, F.A., Sputova, K., Fridriksdottir, A.J., Guo, D.E., Villadsen, R., Park, M., Petersen, O.W., Borowsky, A.D. et al. (2012) Accumulation of multipotent progenitors with a basal differentiation bias during aging of human mammary epithelia. Cancer Res., 72, 3687-3701.
32. Betel, D., Koppal, A., Agius, P., Sander, C. and Leslie, C. (2010) Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol., 11, R90.
33. Dweep, H., Sticht, C., Pandey, P. and Gretz, N. (2011) miRWalk- database: prediction of possible miRNA binding sites by walking the genes of three genomes. J. Biomed. Inform., 44, 839-847.
34. Cao, Q., Mani, R.S., Ateeq, B., Dhanasekaran, S.M., Asangani, I.A., Prensner, J.R., Kim, J.H., Brenner, J.C., Jing, X., Cao, X. et al. (2011) Coordinated regulation of polycomb group complexes through microRNAs in cancer. Cancer Cell, 20, 187-199.
35. Kumamoto, K., Spillare, E.A., Fujita, K., Horikawa, I., Yamashita, T., Appella, E., Nagashima, M., Takenoshita, S., Yokota, J. and Harris, C.C. (2008) Nutlin-3a activates p53 to both down-regulate inhibitor of growth 2 and up-regulate mir-34a, mir-34b, and mir-34c expression, and induce senescence. Cancer Res., 68, 3193-3203.
36. Liu, N., Landreh, M., Cao, K., Abe, M., Hendriks, G.J., Kennerdell, J.R., Zhu, Y., Wang, L.S. and Bonini, N.M. (2012) The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature, 482, 519-523.
37. Tazawa, H., Tsuchiya, N., Izumiya, M. and Nakagama, H. (2007) Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc. Natl Acad. Sci. USA, 104, 15472-15477.
38. Tzatsos, A., Paskaleva, P., Lymperi, S., Contino, G., Stoykova, S., Chen, Z., Wong, K.K. and Bardeesy, N. (2011) Lysine-specific demethylase 2B (KDM2B)-let-7-enhancer of zester homolog 2 (EZH2) pathway regulates cell cycle progression and senescence in primary cells. J. Biol. Chem., 286, 33061-33069.
39. Nishino, J., Kim, I., Chada, K. and Morrison, S.J. (2008) Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell, 135, 227-239.
40. ElSharawy, A., Keller, A., Flachsbart, F., Wendschlag, A., Jacobs, G., Kefer, N., Brefort, T., Leidinger, P., Backes, C., Meese, E. et al. (2012) Genome-wide miRNA signatures of human longevity. Aging Cell, 11, 607-616.
41. Shin, K.H., Bae, S.D., Hong, H.S., Kim, R.H., Kang, M.K. and Park, N.H. (2011) miR-181a shows tumor suppressive effect against oral squamous cell carcinoma cells by downregulating K-ras. Biochem. Biophys. Res. Commun., 404, 896-902.
42. Rivetti di Val Cervo, P., Lena, A.M., Nicoloso, M., Rossi, S., Mancini, M., Zhou, H., Saintigny, G., Dellambra, E., Odorisio, T., Mahe, C. et al. (2012) p63-microRNA feedback in keratinocyte senescence. Proc. Natl Acad. Sci. USA, 109, 1133-1138.
43. Khanna, A., Muthusamy, S., Liang, R., Sarojini, H. and Wang, E. (2011) Gain of survival signaling by down-regulation of three key miRNAs in brain of calorie-restricted mice. Aging (Albany NY), 3, 223-236.
44. Faraonio, R., Salerno, P., Passaro, F., Sedia, C., Iaccio, A., Bellelli, R., Nappi, T.C., Comegna, M., Romano, S., Salvatore, G. et al. (2012) A set of miRNAs participates in the cellular senescence program in human diploid fibroblasts. Cell Death Differ., 19, 713-721.
45. Bonifacio, L.N. and Jarstfer, M.B. (2010) MiRNA profile associated with replicative senescence, extended cell culture, and ectopic telomerase expression in human foreskin fibroblasts. PLoS One, 5, e12519.
46. Forrest, A.R., Kanamori-Katayama, M., Tomaru, Y., Lassmann, T., Ninomiya, N., Takahashi, Y., de Hoon, M.J., Kubosaki, A., Kaiho, A., Suzuki, M. et al. (2010) Induction of microRNAs, mir- 155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia, 24, 460-466.
47. Lu, J., He, M.L., Wang, L., Chen, Y., Liu, X., Dong, Q., Chen, Y.C., Peng, Y., Yao, K.T., Kung, H.F. et al. (2011) MiR-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of EZH2. Cancer Res., 71, 225-233.
48. Wong, C.F. and Tellam, R.L. (2008) MicroRNA-26a targets the histone methyltransferase Enhancer of Zeste homolog 2 during myogenesis. J. Biol. Chem., 283, 9836-9843.
49. OLoghlen, A., Munoz-Cabello, A.M., Gaspar-Maia, A., Wu, H.A., Banito, A., Kunowska, N., Racek, T., Pemberton, H.N., Beolchi, P., Lavial, F. et al. (2012) MicroRNA regulation of Cbx7 mediates a switch of Polycomb orthologs during ESC differentiation. Cell Stem Cell, 10, 33-46.
50. Baker, D.J., Wijshake, T., Tchkonia, T., LeBrasseur, N.K., Childs, B.G., van de Sluis, B., Kirkland, J.L. and van Deursen, J.M. (2011) Clearance of p16Ink4a-positive senescent cells delays ageing-Associated disorders. Nature, 479, 232-236.