Autophagy is induced through the ROS-TP53-DRAM1 pathway in response to mitochondrial protein synthesis inhibition

Autophagy

Volumn 8, Issue 7, 2012, Pages 1071-1084

  Xie, Xiaolei ^a   Le, Li ^a   Fan, Yanxin ^a   Lv, Lin ^a   Zhang, Junjie ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

Author keywords

Autophagy; Chloramphenicol; DRAM1; ERAL1; Mitoribosome; ROS; TP53

Indexed keywords

CHLORAMPHENICOL; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DRAM1 PROTEIN; ERAL1 PROTEIN; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P21; PROTEIN P53; RAS PROTEIN; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CELL VACUOLE; CONTROLLED STUDY; GENE TARGETING; HELA CELL; HUMAN; HUMAN CELL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; RNA INTERFERENCE; TRANSCRIPTION REGULATION; UBIQUITINATION; UPREGULATION;

MAMMALIA;

EID: 84866112397     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.20250     Document Type: Article

References (47)

1. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858
2. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538
3. Cherra SJ, 3rd, Dagda RK, Chu CT. Review: autophagy and neurodegeneration: survival at a cost? Neuropathol Appl Neurobiol 2010; 36:125-32; PMID:20202120
4. Rodriguez-Enriquez S, He L, Lemasters JJ. Role of mitochondrial permeability transition pores in mitochondrial autophagy. Int J Biochem Cell Biol 2004; 36:2463-72; PMID:15325585
5. Scherz-Shouval R, Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol 2007; 17:422-7; PMID:17804237
6. Kenmochi N, Suzuki T, Uechi T, Magoori M, Kuniba M, Higa S, et al. The human mitochondrial ribosomal protein genes: mapping of 54 genes to the chromosomes and implications for human disorders. Genomics 2001; 77:65-70; PMID:11543634
7. Pel HJ, Grivell LA. Protein synthesis in mitochondria. Mol Biol Rep 1994; 19:183-94; PMID:7969106
8. O'Brien TW. Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease. Gene 2002; 286:73-9; PMID:11943462
9. Chen SM, Takiff HE, Barber AM, Dubois GC, Bardwell JC, Court DL. Expression and characterization of RNase III and Era proteins. Products of the rnc operon of Escherichia coli. J Biol Chem 1990; 265:2888-95; PMID:2105934
10. Tu C, Zhou X, Tarasov SG, Tropea JE, Austin BP, Waugh DS, et al. The Era GTPase recognizes the GAUCACCUCC sequence and binds helix 45 near the 3′ end of 16S rRNA. Proc Natl Acad Sci U S A 2011; 108:10156-61; PMID:21646538
11. Sharma MR, Barat C, Wilson DN, Booth TM, Kawazoe M, Hori-Takemoto C, et al. Interaction of Era with the 30S ribosomal subunit implications for 30S subunit assembly. Mol Cell 2005; 18:319-29; PMID:15866174
12. Britton RA, Chen SM, Wallis D, Koeuth T, Powell BS, Shaffer LG, et al. Isolation and preliminary characterization of the human and mouse homologues of the bacterial cell cycle gene era. Genomics 2000; 67:78-82; PMID:10945472
13. Ingram GC, Simon R, Carpenter R, Coen ES. The Antirrhinum ERG gene encodes a protein related to bacterial small GTPases and is required for embryonic viability. Curr Biol 1998; 8:1079-82; PMID:9768362
14. Akiyama T, Gohda J, Shibata S, Nomura Y, Azuma S, Ohmori Y, et al. Mammalian homologue of E. coli Ras-like GTPase (ERA) is a possible apoptosis regulator with RNA binding activity. Genes Cells 2001; 6:987-1001; PMID:11733036
15. Gohda J, Nomura Y, Suzuki H, Arai H, Akiyama T, Inoue J. Elimination of the vertebrate Escherichia coli Ras-like protein homologue leads to cell cycle arrest at G1 phase and apoptosis. Oncogene 2003; 22:1340-8; PMID:12618759
16. Dennerlein S, Rozanska A, Wydro M, Chrzanowska-Lightowlers ZM, Lightowlers RN. Human ERAL1 is a mitochondrial RNA chaperone involved in the assembly of the 28S small mitochondrial ribosomal subunit. Biochem J 2010; 430:551-8; PMID:20604745
17. Uchiumi T, Ohgaki K, Yagi M, Aoki Y, Sakai A, Matsumoto S, et al. ERAL1 is associated with mitochondrial ribosome and elimination of ERAL1 leads to mitochondrial dysfunction and growth retardation. Nucleic Acids Res 2010; 38:5554-68; PMID:20430825
18. Brady NR, Hamacher-Brady A, Westerhoff HV, Gottlieb RA. A wave of reactive oxygen species (ROS)-induced ROS release in a sea of excitable mitochondria. Antioxid Redox Signal 2006; 8:1651-65; PMID:16987019
19. Azad MB, Chen Y, Gibson SB. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 2009; 11:777-90; PMID:18828708
20. Komatsu M, Ichimura Y. Physiological significance of selective degradation of p62 by autophagy. FEBS Lett 2010; 584:1374-8; PMID:20153326
21. Ichimura Y, Komatsu M. Selective degradation of p62 by autophagy. Semin Immunopathol 2010; 32:431-6; PMID:20814791
22. Balaburski GM, Hontz RD, Murphy ME. p53 and ARF: unexpected players in autophagy. Trends Cell Biol 2010; 20:363-9; PMID:20303758
23. Jin S. p53, Autophagy and tumor suppression. Autophagy 2005; 1:171-3; PMID:16874039
24. Liu B, Chen Y, St Clair DK. ROS and p53: a versatile partnership. Free Radic Biol Med 2008; 44:1529-35; PMID:18275858
25. Maiuri MC, Galluzzi L, Morselli E, Kepp O, Malik SA, Kroemer G. Autophagy regulation by p53. Curr Opin Cell Biol 2010; 22:181-5; PMID:20044243
26. 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; 4:810-4; PMID:18604159
27. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006; 126:121-34; PMID:16839881
28. Criollo A, Dessen P, Kroemer G. DRAM: a phylogenetically ancient regulator of autophagy. Cell Cycle 2009; 8:2319-20; PMID:19633415
29. Kerley-Hamilton JS, Pike AM, Hutchinson JA, Freemantle SJ, Spinella MJ. The direct p53 target gene, FLJ11259/DRAM, is a member of a novel family of transmembrane proteins. Biochim Biophys Acta 2007; 1769:209-19.
30. Karbowski M, Kurono C, Wozniak M, Ostrowski M, Teranishi M, Soji T, et al. Cycloheximide and 4-OH-TEMPO suppress chloramphenicol-induced apoptosis in RL-34 cells via the suppression of the formation of megamitochondria. Biochim Biophys Acta 1999; 1449:25-40; PMID:10076048
31. Leiter LM, Thatte HS, Okafor C, Marks PW, Golan DE, Bridges KR. Chloramphenicol-induced mitochondrial dysfunction is associated with decreased transferrin receptor expression and ferritin synthesis in K562 cells and is unrelated to IRE-IRP interactions. J Cell Physiol 1999; 180:334-44; PMID:10430173
32. Li CH, Tzeng SL, Cheng YW, Kang JJ. Chloramphenicol-induced mitochondrial stress increases p21 expression and prevents cell apoptosis through a p21-dependent pathway. J Biol Chem 2005; 280:26193-9; PMID:15905168
33. Kruse JP, Gu W. Modes of p53 regulation. Cell 2009; 137:609-22; PMID:19450511
34. Bode AM, Dong Z. Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer 2004; 4:793-805; PMID:15510160
35. Brooks CL, Gu W. New insights into p53 activation. Cell Res 2010; 20:614-21; PMID:20404858
36. Kim SJ, Hwang SG, Shin DY, Kang SS, Chun JS. p38 kinase regulates nitric oxide-induced apoptosis of articular chondrocytes by accumulating p53 via NFkappa B-dependent transcription and stabilization by serine 15 phosphorylation. J Biol Chem 2002; 277:33501-8; PMID:12091386
37. Pérez-Martínez X, Funes S, Camacho-Villasana Y, Marjavaara S, Tavares-Carreón F, Shingú-Vázquez M. Protein synthesis and assembly in mitochondrial disorders. Curr Top Med Chem 2008; 8:1335-50; PMID:18991722
38. Jacobs HT. Disorders of mitochondrial protein synthesis. Hum Mol Genet 2003; 12(Spec No 2):R293-301; PMID:12928485
39. Scherz-Shouval R, Shvets E, Elazar Z. Oxidation as a post-translational modification that regulates autophagy. Autophagy 2007; 3:371-3; PMID:17438362
40. Zhang H, Kong X, Kang J, Su J, Li Y, Zhong J, et al. Oxidative stress induces parallel autophagy and mitochondria dysfunction in human glioma U251 cells. Toxicol Sci 2009; 110:376-88; PMID:19451193
41. Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 1997; 91:325-34; PMID:9363941
42. Lambert PF, Kashanchi F, Radonovich MF, Shiekhattar R, Brady JN. Phosphorylation of p53 serine 15 increases interaction with CBP. J Biol Chem 1998; 273:33048-53; PMID:9830059
43. Prigione A, Cortopassi G. Mitochondrial DNA deletions and chloramphenicol treatment stimulate the autophagic transcript ATG12. Autophagy 2007; 3:377-80; PMID:17457038
44. Tanaka A. Parkin-mediated selective mitochondrial autophagy, mitophagy: Parkin purges damaged organelles from the vital mitochondrial network. FEBS Lett 2010; 584:1386-92; PMID:20188730
45. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183:795-803; PMID:19029340
46. Miller C, Saada A, Shaul N, Shabtai N, Ben-Shalom E, Shaag A, et al. Defective mitochondrial translation caused by a ribosomal protein (MRPS16) mutation. Ann Neurol 2004; 56:734-8; PMID:15505824
47. Suomalainen A, Isohanni P. Mitochondrial DNA depletion syndromes - many genes, common mechanisms. Neuromuscul Disord 2010; 20:429-37; PMID:20444604