Chaperone-mediated autophagy degrades mutant p53

Genes and Development

Volumn 27, Issue 15, 2013, Pages 1718-1730

  Vakifahmetoglu Norberg, Helin ^a   Kim, Minsu ^a   Xia, Hong guang ^a   Iwanicki, Marcin P ^a   Ofengeim, Dimitry ^a   Coloff, Jonathan L ^a   Pan, Lifeng ^b   Ince, Tan A ^c,d   Kroemer, Guido ^e,f,g,h,i   Brugge, Joan S ^a   Yuan, Junying ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MIAMI   (United States)

^e INSERM   (France)

^f INSTITUT GUSTAVE ROUSSY   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

^h CENTRE DE RECHERCHE DES CORDELIERS   (France)

ⁱ HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

Autophagy; Cancer; CMA; P53; Spautin 1

Indexed keywords

AMMONIUM CHLORIDE; ANTINEOPLASTIC AGENT; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; CATHEPSIN INHIBITOR E64D; CHAPERONE; CHLOROQUINE; DOXORUBICIN; FLUOROURACIL; MUTANT PROTEIN; PEPTIDE HYDROLASE INHIBITOR; PROTEASOME; PROTEIN P53; SPAUTIN 1; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL DEATH; CELL KILLING; CHAPERONE-MEDIATED AUTOPHAGY; CONTROLLED STUDY; CYTOTOXICITY; DRUG SENSITIVITY; HUMAN; HUMAN CELL; LYSOSOME; MACROAUTOPHAGY; MISSENSE MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; SELECTIVE AUTOPHAGY; SENSITIZATION; UBIQUITINATION; WESTERN BLOTTING; WILD TYPE;

AUTOPHAGY; CANCER; CMA; P53; SPAUTIN-1;

ANTINEOPLASTIC AGENTS; AUTOPHAGY; BORONIC ACIDS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEUPEPTINS; LYSOSOMES; MOLECULAR CHAPERONES; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; PYRAZINES; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINATION;

EID: 84881061593     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.220897.113     Document Type: Article

References (34)

1. Aniento F., Roche E, Cuervo AM, Knecht E. 1993. Uptake and degradation of glyceraldehyde-3-phosphate dehydrogenase by rat liver lysosomes. J Biol Chem 268: 10463-10470.
2. Ano Bom AP, Rangel LP, Costa DC, de Oliveira GA, Sanches D, Braga C. A, Gava LM, Ramos CH, Cepeda AO, Stumbo AC, et al. 2012. Mutant p53 aggregates into prion-like amyloid oligomers and fibrils: Implications for cancer. J Biol Chem 287: 28152-28162.
3. Bartek J., Bartkova J, Vojtesek B, Staskova Z, Lukas J, Rejthar A, Kovarik J., Midgley CA, Gannon JV, Lane DP. 1991. Aberrant expression of the p53 oncoprotein is a common feature of a wide spectrum of human malignancies. Oncogene 6: 1699-1703.
4. Bauer P. O, Goswami A, Wong HK, Okuno M, Kurosawa M, Yamada M., Miyazaki H, Matsumoto G, Kino Y, Nagai Y, et al. 2010. Harnessing chaperone-mediated autophagy for the selective degradation of mutant huntingtin protein. Nat Biotechnol 28: 256-263.
5. Chu A., Matusiewicz N, Stochaj U. 2001. Heat-induced nuclear accumulation of hsc70s is regulated by phosphorylation and inhibited in confluent cells. FASEB J 15: 1478-1480.
6. Cuervo A.M. 2011. Chaperone-mediated autophagy: Dice's 'wild' idea about lysosomal selectivity. Nat Rev Mol Cell Biol 12: 535-541.
7. Cuervo A. M, Knecht E, Terlecky SR, Dice JF. 1995. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am J Physiol 269: C1200-C1208.
8. Cuervo A. M, Hu W, Lim B, Dice JF. 1998. IkB is a substrate for a selective pathway of lysosomal proteolysis. Mol Biol Cell 9: 1995-2010.
9. Dice J.F. 2007. Chaperone-mediated autophagy. Autophagy 3: 295-299.
10. Fuertes G., Martin De Llano JJ, Villarroya A, Rivett AJ, Knecht E. 2003. Changes in the proteolytic activities of proteasomes and lysosomes in human fibroblasts produced by serum withdrawal, amino-acid deprivation and confluent conditions. Biochem J 375: 75-86.
11. Haupt Y., Maya R, Kazaz A, Oren M. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299.
12. Hinds P. W, Finlay CA, Quartin RS, Baker SJ, Fearon ER, Vogelstein B., Levine AJ. 1990. Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: A comparison of the 'hot spot' mutant phenotypes. Cell Growth Differ 1: 571-580.
13. Jacks T., Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson R. T, Weinberg RA. 1994. Tumor spectrum analysis in p53-mutant mice. Curr Biol 4: 1-7.
14. Kaushik S., Cuervo AM. 2009. Methods to monitor chaperonemediated autophagy. Methods Enzymol 452: 297-324.
15. Kaushik S., Massey AC, Mizushima N, Cuervo AM. 2008. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol Biol Cell 19: 2179-2192.
16. Kubbutat M. H, Jones SN, Vousden KH. 1997. Regulation of p53 stability by Mdm2. Nature 387: 299-303.
17. Kupryjanczyk J., Thor AD, Beauchamp R, Merritt V, Edgerton SM, Bell DA, Yandell DW. 1993. p53 gene mutations and protein accumulation in human ovarian cancer. Proc Natl Acad Sci 90: 4961-4965.
18. Li D., Marchenko ND, Moll UM. 2011a. SAHA shows preferential cytotoxicity in mutant p53 cancer cells by destabilizing mutant p53 through inhibition of the HDAC6-Hsp90 chaperone axis. Cell Death Differ 18: 1904-1913.
19. Li D., Marchenko ND, Schulz R, Fischer V, Velasco-Hernandez T, Talos F, Moll UM. 2011b. Functional inactivation of endogenous MDM2 and CHIP by HSP90 causes aberrant stabilization of mutant p53 in human cancer cells. Mol Cancer Res 9: 577-588.
20. Liu H., Wang P, Song W, Sun X. 2009. Degradation of regulator of calcineurin 1 (RCAN1) is mediated by both chaperonemediated autophagy and ubiquitin proteasome pathways. FASEB J 23: 3383-3392.
21. Liu J., Xia HG, Kim M, Xu L, Li Y, Zhang L, Yu C, Norberg-Vakifahmetoglu H., Zhang T, Furuya T, et al. 2011. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell 147: 223-234.
22. Massey A. C, Kaushik S, Sovak G, Kiffin R, Cuervo AM. 2006. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci 103: 5805-5810.
23. Muller P. A, Vousden KH. 2013. p53 mutations in cancer. Nat Cell Biol 15: 2-8.
24. Muller P. A, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S, Lukashchuk N., Gillespie DA, Ludwig RL, Gosselin P, et al. 2009. Mutant p53 drives invasion by promoting integrin recycling. Cell 139: 1327-1341.
25. Olive K. P, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT, Crowley D., Jacks T. 2004. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 119: 847-860.
26. Petitjean A., Mathe E, Kato S, Ishioka C, Tavtigian SV, Hainaut P, Olivier M. 2007. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: Lessons from recent developments in the IARC TP53 database. Hum Mutat 28: 622-629.
27. Rodriguez O. C, Choudhury S, Kolukula V, Vietsch EE, Catania J, Preet A., Reynoso K, Bargonetti J, Wellstein A, Albanese C, et al. 2012. Dietary downregulation of mutant p53 levels via glucose restriction: Mechanisms and implications for tumor therapy. Cell Cycle 11: 4436-4446.
28. Sigal A., Rotter V. 2000. Oncogenic mutations of the p53 tumor suppressor: The demons of the guardian of the genome. Cancer Res 60: 6788-6793.
29. Suh Y. A, Post SM, Elizondo-Fraire AC, Maccio DR, Jackson JG, El-Naggar AK, Van Pelt C, Terzian T, Lozano G. 2011. Multiple stress signals activate mutant p53 in vivo. Cancer Res 71: 7168-7175.
30. Terzian T., Suh YA, Iwakuma T, Post SM, Neumann M, Lang GA, Van Pelt CS, Lozano G. 2008. The inherent instability of mutant p53 is alleviated by Mdm2 or p16INK4a loss. Genes Dev 22: 1337-1344.
31. Wang Y., Martinez-Vicente M, Kruger U, Kaushik S, Wong E, Mandelkow E. M, Cuervo AM, Mandelkow E. 2009. Tau fragmentation, aggregation and clearance: The dual role of lysosomal processing. Hum Mol Genet 18: 4153-4170.
32. Whitesell L., Sutphin PD, Pulcini EJ, Martinez JD, Cook PH. 1998. The physical association of multiple molecular chaperone proteins with mutant p53 is altered by geldanamycin, an hsp90-binding agent. Mol Cell Biol 18: 1517-1524.
33. Wiech M., Olszewski MB, Tracz-Gaszewska Z, Wawrzynow B, Zylicz M., Zylicz A. 2012. Molecular mechanism of mutant p53 stabilization: The role of HSP70 and MDM2. PLoS ONE 7: e51426.
34. Yuan J., Luo K, Zhang L, Cheville JC, Lou Z. 2010. USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 140: 384-396.