Deacetylation of p53 induces autophagy by suppressing bmf expression

Journal of Cell Biology

Volumn 201, Issue 3, 2013, Pages 427-437

  Contreras, Amelia U ^a   Mebratu, Yohannes ^a   Delgado, Monica ^a   Montano, Gilbert ^a   Hu, Chien an A ^b   Ryter, Stefan W ^c   Choi, Augustine M K ^c   Lin, Yuting ^d   Xiang, Jialing ^d   Chand, Hitendra ^a   Tesfaigzi, Yohannes ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; BH3 PROTEIN; BMF PROTEIN; GAMMA INTERFERON; HISTONE DEACETYLASE INHIBITOR; PROLINE; PROTEIN BCL 2; PROTEIN P53; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL DEATH; CONTROLLED STUDY; DEACETYLATION; DOWN REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RESPIRATORY EPITHELIUM; ULTRAVIOLET RADIATION;

ACETYLATION; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; BUTYRIC ACID; CELL NUCLEUS; CELLS, CULTURED; EPITHELIAL CELLS; GENE EXPRESSION; GENE SILENCING; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; INTERFERON-GAMMA; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; RESPIRATORY MUCOSA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84878643354     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201205064     Document Type: Article

References (59)

1. Banerjee, T., S. Nath, and S. Roychoudhury. 2009. DNA damage induced p53 downregulates Cdc20 by direct binding to its promoter causing chromatin remodeling. Nucleic Acids Res. 37:2688-2698. http://dx.doi.org/10.1093/nar/gkp110
2. Borden, E.C., G.C. Sen, G. Uze, R.H. Silverman, R.M. Ransohoff, G.R. Foster, and G.R. Stark. 2007. Interferons at age 50: past, current and future impact on biomedicine. Nat. Rev. Drug Discov. 6:975-990. http://dx.doi.org/10.1038/nrd2422
3. Boyd, S.D., K.Y. Tsai, and T. Jacks. 2000. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nat. Cell Biol. 2:563-568. http://dx.doi.org/10.1038/35023500
4. Chun, A.C., and D.Y. Jin. 2003. Transcriptional regulation of mitotic checkpoint gene MAD1 by p53. J. Biol. Chem. 278:37439-37450. http://dx.doi.org/10.1074/jbc.M307185200
5. Coultas, L., P. Bouillet, E.G. Stanley, T.C. Brodnicki, J.M. Adams, and A. Strasser. 2004. Proapoptotic BH3-only Bcl-2 family member Bik/Blk/ Nbk is expressed in hemopoietic and endothelial cells but is redundant for their programmed death. Mol. Cell. Biol. 24:1570-1581. http://dx.doi.org/10.1128/MCB.24.4.1570-1581.2004
6. Deiss, L.P., E. Feinstein, H. Berissi, O. Cohen, and A. Kimchi. 1995. Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. Genes Dev. 9:15-30. http://dx.doi.org/10.1101/gad.9.1.15
7. Dornan, D., H. Shimizu, L. Burch, A.J. Smith, and T.R. Hupp. 2003. The proline repeat domain of p53 binds directly to the transcriptional coactivator p300 and allosterically controls DNA-dependent acetylation of p53. Mol. Cell. Biol. 23:8846-8861. http://dx.doi.org/10.1128/MCB.23.23.8846-8861.2003
8. Elgendy, M., C. Sheridan, G. Brumatti, and S.J. Martin. 2011. Oncogenic Rasinduced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol. Cell. 42:23-35. http://dx.doi.org/10.1016/j.molcel.2011.02.009
9. Gao, J., M. Senthil, B. Ren, J. Yan, Q. Xing, J. Yu, L. Zhang, and J.H. Yim. 2010. IRF-1 transcriptionally upregulates PUMA, which mediates the mitochondrial apoptotic pathway in IRF-1-induced apoptosis in cancer cells. Cell Death Differ. 17:699-709. http://dx.doi.org/10.1038/cdd.2009.156
10. Greenberg, J.R. 1972. High stability of messenger RNA in growing cultured cells. Nature. 240:102-104. http://dx.doi.org/10.1038/240102a0
11. Grespi, F., C. Soratroi, G. Krumschnabel, B. Sohm, C. Ploner, S. Geley, L. Hengst, G. Häcker, and A. Villunger. 2010. BH3-only protein Bmf mediates apoptosis upon inhibition of CAP-dependent protein synthesis. Cell Death Differ. 17:1672-1683. http://dx.doi.org/10.1038/cdd.2010.97
12. Gu, W., and R.G. Roeder. 1997. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell. 90:595-606. http://dx.doi.org/10.1016/S0092-8674(00)80521-8
13. Hausmann, M., K. Leucht, C. Ploner, S. Kiessling, A. Villunger, H. Becker, C. Hofmann, W. Falk, M. Krebs, S. Kellermeier, et al. 2011. BCL-2 modifying factor (BMF) is a central regulator of anoikis in human intestinal epithelial cells. J. Biol. Chem. 286:26533-26540. http://dx.doi.org/10.1074/jbc.M111.265322
14. Hu, X., and L.B. Ivashkiv. 2009. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity. 31:539-550. http://dx.doi.org/10.1016/j.immuni.2009.09.002
15. Inbal, B., S. Bialik, I. Sabanay, G. Shani, and A. Kimchi. 2002. DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J. Cell Biol. 157:455-468. http://dx.doi.org/10.1083/jcb.200109094
16. Itahana, Y., H. Ke, and Y. Zhang. 2009. p53 oligomerization is essential for its C-terminal lysine acetylation. J. Biol. Chem. 284:5158-5164. http://dx.doi.org/10.1074/jbc.M805696200
17. Kidokoro, T., C. Tanikawa, Y. Furukawa, T. Katagiri, Y. Nakamura, and K. Matsuda. 2008. CDC20, a potential cancer therapeutic target, is negatively regulated by p53. Oncogene. 27:1562-1571. http://dx.doi.org/10.1038/sj.onc.1210799
18. Labi, V., M. Erlacher, S. Kiessling, C. Manzl, A. Frenzel, L. O'Reilly, A. Strasser, and A. Villunger. 2008. Loss of the BH3-only protein Bmf impairs B cell homeostasis and accelerates irradiation-induced thymic lymphoma development. J. Exp. Med. 205:641-655. http://dx.doi.org/10.1084/jem.20071658
19. Lee, J.T., and W. Gu. 2010. The multiple levels of regulation by p53 ubiquitination. Cell Death Differ. 17:86-92. http://dx.doi.org/10.1038/cdd.2009.77
20. Liu, X., D. Wang, Y. Zhao, B. Tu, Z. Zheng, L. Wang, H. Wang, W. Gu, R.G. Roeder, and W.G. Zhu. 2011. Methyltransferase Set7/9 regulates p53 activity by interacting with Sirtuin 1 (SIRT1). Proc. Natl. Acad. Sci. USA. 108:1925-1930. http://dx.doi.org/10.1073/pnas.1019619108
21. Luo, J., F. Su, D. Chen, A. Shiloh, and W. Gu. 2000. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature. 408:377-381. http://dx.doi.org/10.1038/35042612
22. Luo, J., M. Li, Y. Tang, M. Laszkowska, R.G. Roeder, and W. Gu. 2004. Acetylation of p53 augments its site-specific DNA binding both in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 101:2259-2264. http://dx.doi.org/10.1073/pnas.0308762101
23. Luo, S., M. Garcia-Arencibia, R. Zhao, C. Puri, P.P. Toh, O. Sadiq, and D.C. Rubinsztein. 2012. Bim inhibits autophagy by recruiting Beclin 1 to microtubules. Mol. Cell. 47:359-370. http://dx.doi.org/10.1016/j.molcel.2012.05.040
24. Lüth, S., J. Schrader, S. Zander, A. Carambia, J. Buchkremer, S. Huber, K. Reifenberg, K. Yamamura, P. Schirmacher, A.W. Lohse, and J. Herkel. 2011. Chronic inflammatory IFN-signaling suppresses hepatocarcinogenesis in mice by sensitizing hepatocytes for apoptosis. Cancer Res. 71:3763-3771. http://dx.doi.org/10.1158/0008-5472.CAN-10-3232
25. Maiuri, M.C., L. Galluzzi, E. Morselli, O. Kepp, S.A. Malik, and G. Kroemer. 2010. Autophagy regulation by p53. Curr. Opin. Cell Biol. 22:181-185. http://dx.doi.org/10.1016/j.ceb.2009.12.001
26. Marchenko, N.D., W. Hanel, D. Li, K. Becker, N. Reich, and U.M. Moll. 2010. Stress-mediated nuclear stabilization of p53 is regulated by ubiquitination and importin-alpha3 binding. Cell Death Differ. 17:255-267. http://dx.doi.org/10.1038/cdd.2009.173
27. Mebratu, Y.A., B.F. Dickey, C. Evans, and Y. Tesfaigzi. 2008. The BH3-only protein Bik/Blk/Nbk inhibits nuclear translocation of activated ERK1/2 to mediate IFN-induced cell death. J. Cell Biol. 183:429-439. http://dx.doi.org/10.1083/jcb.200801186
28. Murphy, M., J. Ahn, K.K. Walker, W.H. Hoffman, R.M. Evans, A.J. Levine, and D.L. George. 1999. Transcriptional repression by wild-type p53 utilizes histone deacetylases, mediated by interaction with mSin3a. Genes Dev. 13:2490-2501. http://dx.doi.org/10.1101/gad.13.19.2490
29. Ossina, N.K., A. Cannas, V.C. Powers, P.A. Fitzpatrick, J.D. Knight, J.R. Gilbert, E.M. Shekhtman, L.D. Tomei, S.R. Umansky, and M.C. Kiefer. 1997. Interferon-gamma modulates a p53-independent apoptotic pathway and apoptosis-related gene expression. J. Biol. Chem. 272:16351-16357. http://dx.doi.org/10.1074/jbc.272.26.16351
30. Porta, C., R. Hadj-Slimane, M. Nejmeddine, M. Pampin, M.G. Tovey, L. Espert, S. Alvarez, and M.K. Chelbi-Alix. 2005. Interferons alpha and gamma induce p53-dependent and p53-independent apoptosis, respectively. Oncogene. 24:605-615. http://dx.doi.org/10.1038/sj.onc.1208204
31. Puthalakath, H., A. Villunger, L.A. O'Reilly, J.G. Beaumont, L. Coultas, R.E. Cheney, D.C. Huang, and A. Strasser. 2001. Bmf: a proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science. 293:1829-1832. http://dx.doi.org/10.1126/science.1062257
32. Roperch, J.P., V. Alvaro, S. Prieur, M. Tuynder, M. Nemani, F. Lethrosne, L. Piouffre, M.C. Gendron, D. Israeli, J. Dausset, et al. 1998. Inhibition of presenilin 1 expression is promoted by p53 and p21WAF-1 and results in apoptosis and tumor suppression. Nat. Med. 4:835-838. http://dx.doi.org/10.1038/nm0798-835
33. Ruiz-Ruiz, C., C. Muñoz-Pinedo, and A. López-Rivas. 2000. Interferon-gamma treatment elevates caspase-8 expression and sensitizes human breast tumor cells to a death receptor-induced mitochondria-operated apoptotic program. Cancer Res. 60:5673-5680.
34. Schmelzle, T., A.A. Mailleux, M. Overholtzer, J.S. Carroll, N.L. Solimini, E.S. Lightcap, O.P. Veiby, and J.S. Brugge. 2007. Functional role and oncogene-regulated expression of the BH3-only factor Bmf in mammary epithelial anoikis and morphogenesis. Proc. Natl. Acad. Sci. USA. 104:3787-3792. http://dx.doi.org/10.1073/pnas.0700115104
35. Schwalm, K., J.F. Stevens, Z. Jiang, M.R. Schuyler, R. Schrader, S.H. Randell, F.H. Green, and Y. Tesfaigzi. 2008. Expression of the proapoptotic protein Bax is reduced in bronchial mucous cells of asthmatic subjects. Am. J. Physiol. Lung Cell. Mol. Physiol. 294:L1102-L1109. http://dx.doi.org/10.1152/ajplung.00424.2007
36. Shi, Z.O., M.J. Fischer, G.T. De Sanctis, M.R. Schuyler, and Y. Tesfaigzi. 2002. IFN-gamma, but not Fas, mediates reduction of allergen-induced mucous cell metaplasia by inducing apoptosis. J. Immunol. 168:4764-4771.
37. St Clair, S., L. Giono, S. Varmeh-Ziaie, L. Resnick-Silverman, W.J. Liu, A. Padi, J. Dastidar, A. DaCosta, M. Mattia, and J.J. Manfredi. 2004. DNA damage-induced downregulation of Cdc25C is mediated by p53 via two independent mechanisms: one involves direct binding to the cdc25C promoter. Mol. Cell. 16:725-736. http://dx.doi.org/10.1016/j.molcel.2004.11.002
38. Stoecklin, G., and P. Anderson. 2007. In a tight spot: ARE-mRNAs at processing bodies. Genes Dev. 21:627-631. http://dx.doi.org/10.1101/gad.1538807
39. Stout, B.A., K. Melendez, J. Seagrave, M.J. Holtzman, B. Wilson, J. Xiang, and Y. Tesfaigzi. 2007. STAT1 activation causes translocation of Bax to the endoplasmic reticulum during the resolution of airway mucous cell hyperplasia by IFN-. J. Immunol. 178:8107-8116.
40. Strasser, A. 2005. The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5:189-200. http://dx.doi.org/10.1038/nri1568
41. Sun, Y., J.M. Cheung, J. Martel-Pelletier, J.P. Pelletier, L. Wenger, R.D. Altman, D.S. Howell, and H.S. Cheung. 2000. Wild type and mutant p53 differentially regulate the gene expression of human collagenase-3 (hMMP-13). J. Biol. Chem. 275:11327-11332. http://dx.doi.org/10.1074/jbc.275.15.11327
42. Tang, Y., J. Luo, W. Zhang, and W. Gu. 2006. Tip60-dependent acetylation of p53 modulates the decision between cell-cycle arrest and apoptosis. Mol. Cell. 24:827-839. http://dx.doi.org/10.1016/j.molcel.2006.11.021
43. Tang, Y., W. Zhao, Y. Chen, Y. Zhao, and W. Gu. 2008. Acetylation is indispensable for p53 activation. Cell. 133:612-626. http://dx.doi.org/10.1016/j.cell.2008.03.025
44. Tasdemir, E., M.C. Maiuri, L. Galluzzi, I. Vitale, M. Djavaheri-Mergny, M. D'Amelio, A. Criollo, E. Morselli, C. Zhu, F. Harper, et al. 2008. Regulation of autophagy by cytoplasmic p53. Nat. Cell Biol. 10:676-687. http://dx.doi.org/10.1038/ncb1730
45. Tesfaigzi, Y. 2006. Roles of apoptosis in airway epithelia. Am. J. Respir. Cell Mol. Biol. 34:537-547. http://dx.doi.org/10.1165/rcmb.2006-0014OC
46. Tesfaigzi, Y., M.J. Fischer, M. Daheshia, F.H. Green, G.T. De Sanctis, and J.A. Wilder. 2002a. Bax is crucial for IFN-gamma-induced resolution of allergen-induced mucus cell metaplasia. J. Immunol. 169:5919-5925.
47. Tesfaigzi, Y., M.J. Fischer, M. Daheshia, F.H. Green, G.T. De Sanctis, and J.A. Wilder. 2002b. Bax is crucial for IFN--induced resolution of allergeninduced mucus cell metaplasia. J. Immunol. 169:5919-5925.
48. Toledo, F., K.A. Krummel, C.J. Lee, C.W. Liu, L.W. Rodewald, M. Tang, and G.M. Wahl. 2006. A mouse p53 mutant lacking the proline-rich domain rescues Mdm4 deficiency and provides insight into the Mdm2-Mdm4-p53 regulatory network. Cancer Cell. 9:273-285. http://dx.doi.org/10.1016/j.ccr.2006.03.014
49. Toledo, F., C.J. Lee, K.A. Krummel, L.W. Rodewald, C.W. Liu, and G.M. Wahl. 2007. Mouse mutants reveal that putative protein interaction sites in the p53 proline-rich domain are dispensable for tumor suppression. Mol. Cell. Biol. 27:1425-1432. http://dx.doi.org/10.1128/MCB.00999-06
50. Trautmann, A., M. Akdis, D. Kleemann, F. Altznauer, H.U. Simon, T. Graeve, M. Noll, E.B. Bröcker, K. Blaser, and C.A. Akdis. 2000. T cell-mediated Fas-induced keratinocyte apoptosis plays a key pathogenetic role in eczematous dermatitis. J. Clin. Invest. 106:25-35. http://dx.doi.org/10.1172/JCI9199
51. Tu, S.P., M. Quante, G. Bhagat, S. Takaishi, G. Cui, X.D. Yang, S. Muthuplani, W. Shibata, J.G. Fox, D.M. Pritchard, and T.C. Wang. 2011. IFN-inhibits gastric carcinogenesis by inducing epithelial cell autophagy and T-cell apoptosis. Cancer Res. 71:4247-4259. http://dx.doi.org/10.1158/0008-5472.CAN-10-4009
52. Wei, C.L., Q. Wu, V.B. Vega, K.P. Chiu, P. Ng, T. Zhang, A. Shahab, H.C. Yong, Y. Fu, Z. Weng, et al. 2006. A global map of p53 transcriptionfactor binding sites in the human genome. Cell. 124:207-219. http://dx.doi.org/10.1016/j.cell.2005.10.043
53. Xiang, J., D.T. Chao, and S.J. Korsmeyer. 1996. BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA. 93:14559-14563. http://dx.doi.org/10.1073/pnas.93.25.14559
54. Yan, J., Z.Y. Wang, H.Z. Yang, H.Z. Liu, S. Mi, X.X. Lv, X.M. Fu, H.M. Yan, X.W. Zhang, Q.M. Zhan, and Z.W. Hu. 2011. Timing is critical for an effective anti-metastatic immunotherapy: the decisive role of IFN/STAT1-mediated activation of autophagy. PLoS ONE. 6:e24705. http://dx.doi.org/10.1371/journal.pone.0024705
55. You, Y., E.J. Richer, T. Huang, and S.L. Brody. 2002. Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am. J. Physiol. Lung Cell. Mol. Physiol. 283:L1315-L1321.
56. Yun, J., H.D. Chae, H.E. Choy, J. Chung, H.S. Yoo, M.H. Han, and D.Y. Shin. 1999. p53 negatively regulates cdc2 transcription via the CCAAT-binding NF-Y transcription factor. J. Biol. Chem. 274:29677-29682. http://dx.doi.org/10.1074/jbc.274.42.29677
57. Zhang, Y., and Y. Xiong. 2001. A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science. 292: 1910-1915. http://dx.doi.org/10.1126/science.1058637
58. Zhang, Y., M. Adachi, R. Kawamura, and K. Imai. 2006a. Bmf is a possible mediator in histone deacetylase inhibitors FK228 and CBHAinduced apoptosis. Cell Death Differ. 13:129-140. http://dx.doi.org/10.1038/sj.cdd.4401686
59. Zhang, Y., M. Adachi, R. Kawamura, H.C. Zou, K. Imai, M. Hareyama, and Y. Shinomura. 2006b. Bmf contributes to histone deacetylase inhibitormediated enhancing effects on apoptosis after ionizing radiation. Apoptosis. 11:1349-1357. http://dx.doi.org/10.1007/s10495-006-8266-1