p53 inhibits autophagy by interacting with the human ortholog of yeast Atg17, RB1CC1/FIP200

Cell Cycle

Volumn 10, Issue 16, 2011, Pages 2763-2769

  Morselli, Eugenia ^a,b,c   Shen, Shensi ^a,b,c   Ruckenstuhl, Christoph ^d,e   Bauer, Maria Anna ^d   Mariño, Guillermo ^a,b,c   Galluzzi, Lorenzo ^a,b,c   Criollo, Alfredo ^a,b,c   Michaud, Mickael ^a,b,c   Maiuri, Maria Chiara ^a,b,c   Chano, Tokuhiro ^f   Madeo, Frank ^d   Kroemer, Guido ^a,b,g,h  

^a Institut Gustave Roussy   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF GRAZ   (Austria)

^e MEDICAL UNIVERSITY OF GRAZ   (Austria)

^f SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^g HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^h UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Aging; Longevity; mTOR; Rapamycin; Saccharomyces cerevisiae

Indexed keywords

ARGININE; AUTOPHAGY PROTEIN 17; FIP200 PROTEIN; FOCAL ADHESION KINASE; FUNGAL PROTEIN; LYSINE; PROTEIN P53; RB1 INDUCIBLE COILED COIL 1 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; AUTOPHAGY; BIOINFORMATICS; CANCER CELL; CHROMATIN IMMUNOPRECIPITATION; COLON CANCER; CONTROLLED STUDY; CYTOPLASM; GENETIC TRANSFECTION; GROWTH INHIBITION; HUMAN; HUMAN CELL; MAMMAL; MUTATIONAL ANALYSIS; NONHUMAN; POINT MUTATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WILD TYPE; YEAST; YEAST CELL;

MAMMALIA; NEMATODA; SACCHAROMYCES CEREVISIAE;

EID: 80051707399     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.16.16868     Document Type: Article

References (61)

1. Lane DP. Cancer p53, guardian of the genome. Nature 1992; 358:15-6; PMID: 1614522; DOI: 10.1038/358015a0.
2. Vousden K.H., Ryan KM. p53 and metabolism. Nat Rev Cancer 2009; 9:691-700; PMID: 19759539; DOI: 10.1038/nrc2715.
3. Vousden K.H., Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007; 8:275-83; PMID: 17380161; DOI: 10.1038/nrm2147.
4. Bensaad K., Vousden KH. p53: new roles in metabolism. Trends Cell Biol 2007; 17:286-91; PMID: 17481900; DOI: 10.1016/j.tcb.2007.04.004.
5. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88:323-31; PMID: 9039259; DOI: 10.1016/S0092-8674(00)81871-1.
6. Green D.R., Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009; 458:1127-30; PMID: 19407794; DOI: 10.1038/nature07986.
7. Galluzzi L., Kepp O., Kroemer G. A new role for cytoplasmic p53: binding and destroying double-stranded. RNA Cell Cycle 2010; 9:2491-2; PMID: 20647755; DOI: 10.4161/cc.9.13.12191.
8. Galluzzi L., Morselli E., Kepp O., Tajeddine N., Kroemer G. Targeting p53 to mitochondria for cancer therapy. Cell Cycle 2008; 7:1949-55; PMID: 18642442; DOI: 10.4161/cc.7.13.6222.
9. Shinmura K., Bennett R.A., Tarapore P., Fukasawa K. Direct evidence for the role of centrosomally localized p53 in the regulation of centrosome duplication. Oncogene 2007; 26:2939-44; PMID: 17072342; DOI: 10.1038/sj.onc.1210085.
10. Galluzzi L., Morselli E., Kepp O., Vitale I., Pinti M., Kroemer G. Mitochondrial liaisons of p53. Antioxid Redox Signal 2011; In press; PMID: 20712408.
11. Boya P., Gonzalez-Polo R.A., Casares N., Perfettini J.L., Dessen P., Larochette N., et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25:1025-40; PMID: 15657430; DOI: 10.1128/MCB.25.3.1025-40.2005.
12. Chipuk J.E., Kuwana T., Bouchier-Hayes L., Droin N.M., Newmeyer D.D., Schuler M., et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004; 303:1010-4; PMID: 14963330; DOI: 10.1126/science.1092734.
13. Maiuri M.C., Galluzzi L., Morselli E., Kepp O., Malik S.A., Kroemer G. Autophagy regulation by p53. Curr Opin Cell Biol 2010; 22:181-5; PMID: 20044243; DOI: 10.1016/j.ceb.2009.12.001.
14. Tasdemir E., Maiuri M.C., Galluzzi L., Vitale I., Djavaheri-Mergny M., D'Amelio M., et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 2008; 10:676-87; PMID: 18454141; DOI: 10.1038/ncb1730.
15. Kroemer G., Marino G., Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40:280-93; PMID: 20965422; DOI: 10.1016/j.molcel.2010. 09.023.
16. Feng Z., Zhang H., Levine A.J., Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 2005; 102:8204-9; PMID: 15928081; DOI: 10.1073/pnas.0502857102.
17. Crighton D., Wilkinson S., O'Prey J., Syed N., Smith P., Harrison P.R., et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006; 126:121-34; PMID: 16839881; DOI: 10.1016/j.cell.2006.05.034.
18. Crighton D., Wilkinson S., Ryan K.M. DRAM links autophagy to p53 and programmed cell death. Autophagy 2007; 3:72-74; PMID: 17102582.
19. Tasdemir E., Chiara Maiuri M., Morselli E., Criollo A., D'Amelio M., Djavaheri-Mergny M., et al. A dual role of p53 in the control of autophagy. Autophagy 2008; 4:810-814; PMID: 18604159.
20. Tavernarakis N., Pasparaki A., Tasdemir E., Maiuri M.C., Kroemer G. The effects of p53 on whole organism longevity are mediated by autophagy. Autophagy 2008; 4:870-873; PMID: 18728385.
21. Morselli E., Tasdemir E., Maiuri M.C., Galluzzi L., Kepp O., Criollo A., et al. Mutant p53 protein localized in the cytoplasm inhibits autophagy. Cell Cycle 2008; 7:3056-61; PMID: 18818522; DOI: 10.4161/cc.7.19.6751.
22. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-39; PMID: 16179260; DOI: 10.1016/j.cell.2005.07.002.
23. Maiuri M.C., Le Toumelin G., Criollo A., Rain J.C., Gautier F., Juin P., et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 2007; 26:2527-39; PMID: 17446862; DOI: 10.1038/sj.emboj.7601689.
24. Tang Y., Zhao W., Chen Y., Zhao Y., Gu W Acetylation is indispensable for p53 activation Cell 2008; 133:612-26; PMID: 18485870; DOI: 10.1016/j.cell.2008. 03.025.
25. Vaziri H., Dessain S.K., Ng Eaton E., Imai S.I., Frye R.A., Pandita T.K., et al. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 2001; 107:149-59; PMID: 11672523; DOI: 10.1016/S0092- 8674(01)00527-X.
26. Morselli E., Galluzzi L., Kepp O., Criollo A., Maiuri M.C., Tavernarakis N., et al. Autophagy mediates pharmacological lifespan extension by spermidine and resveratrol. Aging (Albany NY) 2009; 1:961-970; PMID: 20157579.
27. Morselli E., Maiuri M.C., Markaki M., Megalou E., Pasparaki A., Palikaras K., et al. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis 2010; 1:10; PMID: 21364612; DOI: 10.1038/cddis.2009.8.
28. Morselli E., Maiuri M.C., Markaki M., Megalou E., Pasparaki A., Palikaras K., et al. The life span-prolonging effect of sirtuin-1 is mediated by autophagy. Autophagy 2010; 6:186-8; PMID: 20023410; DOI: 10.4161/auto.6.1.10817.
29. Morselli E., Marino G., Bennetzen M.V., Eisenberg T., Megalou E., Schroeder S., et al. Spermidine and resveratrol induce autophagy by distinct pathways converging on the acetylproteome. J Cell Biol 2011; 192:615-29; PMID: 21339330; DOI: 10.1083/jcb.201008167.
30. Behrends C., Sowa M.E., Gygi S.P., Harper JW Network organization of the human autophagy system Nature 2010; 466:68-76; PMID: 20562859; DOI: 10.1038/nature09204.
31. Martin N., Schwamborn K., Urlaub H., Gan B., Guan J.L., Dejean A Spatial interplay between PIASy and FIP200 in the regulation of signal transduction and transcriptional activity Mol Cell Biol 2008; 28:2771-81; PMID: 18285457; DOI: 10.1128/MCB.01210-07.
32. Chano T., Ikegawa S., Kontani K., Okabe H., Baldini N., Saeki Y Identification of RB1CC1, a novel human gene that can induce RB1 in various human cells Oncogene 2002; 21:1295-8; PMID: 11850849; DOI: 10.1038/sj.onc. 1205178.
33. Ueda H., Abbi S., Zheng C., Guan JL Suppression of Pyk2 kinase and cellular activities by FIP200 J Cell Biol 2000; 149:423-30; PMID: 10769033; DOI: 10.1083/jcb.149.2.423.
34. Abbi S., Ueda H., Zheng C., Cooper L.A., Zhao J., Christopher R., et al. Regulation of focal adhesion kinase by a novel protein inhibitor FIP200. Mol Biol Cell 2002; 13:3178-91; PMID: 12221124; DOI: 10.1091/mbc.E02-05-0295.
35. Gan B., Melkoumian Z.K., Wu X., Guan K.L., Guan JL Identification of FIP200 interaction with the TSC1-TSC2 complex and its role in regulation of cell size control J Cell Biol 2005; 170:379-89; PMID: 16043512; DOI: 10.1083/jcb.200411106.
36. Chano T., Saeki Y., Serra M., Matsumoto K., Okabe H Preferential expression of RB1-inducible coiled-coil 1 in terminal differentiated musculoskeletal cells Am J Pathol 2002; 161:359-64; PMID: 12163359; DOI: 10.1016/S0002-9440(10)64190-9.
37. Gan B., Peng X., Nagy T., Alcaraz A., Gu H., Guan JL Role of FIP200 in cardiac and liver development and its regulation of TNFalpha and TSC-mTOR signaling pathways J Cell Biol 2006; 175:121-33; PMID: 17015619; DOI: 10.1083/jcb.200604129.
38. Chano T., Kontani K., Teramoto K., Okabe H., Ikegawa S Truncating mutations of RB1CC1 in human breast cancer Nat Genet 2002; 31:285-8; PMID: 12068296; DOI: 10.1038/ng911.
39. Hara T., Takamura A., Kishi C., Iemura S., Natsume T., Guan J.L., et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 2008; 181:497-510; PMID: 18443221; DOI: 10.1083/jcb.200712064.
40. Liang C.C., Wang C., Peng X., Gan B., Guan JL Neural-specific deletion of FIP200 leads to cerebellar degeneration caused by increased neuronal death and axon degeneration J Biol Chem 2010; 285:3499-509; PMID: 19940130; DOI: 10.1074/jbc.M109.072389.
41. Melkoumian Z.K., Peng X., Gan B., Wu X., Guan JL Mechanism of cell cycle regulation by FIP200 in human breast cancer cells Cancer Res 2005; 65:6676-84; PMID: 16061648; DOI: 10.1158/0008-5472.CAN-04-4142.
42. Chano T., Ikebuchi K., Ochi Y., Tameno H., Tomita Y., Jin Y., et al. RB1CC1 activates RB1 pathway and inhibits proliferation and cologenic survival in human cancer. PLoS ONE 2010; 5:11404; PMID: 20614030; DOI: 10.1371/journal.pone.0011404.
43. Itakura E., Mizushima N Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins Autophagy 2010; 6:764-76; PMID: 20639694; DOI: 10.4161/auto.6.6.12709.
44. Ganley IG, Lam du H, Wang J, Ding X, Chen S, Jiang X ULK1ATG13FIP200 complex mediates mTOR signaling and is essential for autophagy J Biol Chem 2009; 284:12297-305; PMID: 19258318; DOI: 10.1074/jbc.M900573200.
45. Jung C.H., Jun C.B., Ro S.H., Kim Y.M., Otto N.M., Cao J., et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992-2003; PMID: 19225151; DOI: 10.1091/mbc.E08-12-1249.
46. Hosokawa N., Hara T., Kaizuka T., Kishi C., Takamura A., Miura Y., et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20:1981-91; PMID: 19211835; DOI: 10.1091/mbc.E08-12-1248.
47. Galluzzi L., Kepp O., Kroemer G. Tp53 and MTOR crosstalk to regulate cellular senescence. Aging (Albany NY) 2010; 2:535-537; PMID: 20876940.
48. Vigneron A., Vousden K.H. p53, ROS and senescence in the control of aging. Aging (Albany NY) 2010; 2:471-474; PMID: 20729567.
49. Bauer J.H., Morris S.N., Chang C., Flatt T., Wood J.G., Helfand S.L. dSir2 and Dmp53 interact to mediate aspects of CR-dependent lifespan extension in D. melanogaster. Aging (Albany NY) 2009; 1:38-48; PMID: 19851477.
50. Waskar M., Landis G.N., Shen J., Curtis C., Tozer K., Abdueva D., et al. Drosophila melanogaster p53 has developmental stage-specific and sex-specific effects on adult life span indicative of sexual antagonistic pleiotropy. Aging (Albany NY) 2009; 1:903-936; PMID: 20157574.
51. de Keizer P.L., Laberge R.M., Campisi J. p53: Pro-aging or pro-longevity? Aging (Albany NY) 2010; 2:377-379; PMID: 20657035.
52. Donehower L.A. Longevity regulation in flies: a role for p53. Aging (Albany NY) 2009; 1:6-8; PMID: 20157591.
53. Poyurovsky M.V., Prives C. p53 and aging: A fresh look at an old paradigm. Aging (Albany NY) 2010; 2:380-382; PMID: 20657036.
54. Madeo F., Tavernarakis N., Kroemer G Can autophagy promote longevity? Nat Cell Biol 2010; 12:842-6; PMID: 20811357; DOI: 10.1038/ncb0910-842.
55. Feng Z., Levine AJ The regulation of energy metabolism and the IGF-1/mTOR pathways by the p53 protein Trends Cell Biol 2010; 20:427-34; PMID: 20399660; DOI: 10.1016/j.tcb.2010.03.004.
56. Bunz F., Hwang P.M., Torrance C., Waldman T., Zhang Y., Dillehay L., et al. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest 1999; 104:263-9; PMID: 10430607; DOI: 10.1172/JCI6863.
57. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720-8; PMID: 11060023; DOI: 10.1093/emboj/19.21.5720.
58. Castedo M., Coquelle A., Vitale I., Vivet S., Mouhamad S., Viaud S., et al. Selective resistance of tetraploid cancer cells against DNA damage-induced apoptosis. Ann NY Acad Sci 2006; 1090:35-49; PMID: 17384245; DOI: 10.1196/annals.1378.004.
59. Criollo A., Maiuri M.C., Tasdemir E., Vitale I., Fiebig A.A., Andrews D., et al. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ 2007; 14:1029-1039; PMID: 17256008.
60. Criollo A., Senovilla L., Authier H., Maiuri M.C., Morselli E., Vitale I., et al. The IKK complex contributes to the induction of autophagy. EMBO J 2010; 29:619-31; PMID: 19959994; DOI: 10.1038/emboj.2009.364.
61. Noda T., Matsuura A., Wada Y., Ohsumi Y Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae Biochem Biophys Res Commun 1995; 210:126-32; PMID: 7741731; DOI: 10.1006/bbrc.1995.1636.