Chaperone-mediated autophagy prevents apoptosis by degrading BBC3/PUMA

Autophagy

Volumn 11, Issue 9, 2015, Pages 1623-1635

  Xie, Wei ^a   Zhang, Lei ^a   Jiao, Haifeng ^a   Guan, Li ^a   Zha, Junmin ^a   Li, Xiaotong ^a   Wu, Mian ^b   Wang, Zhanxiang ^c   Han, Jiahuai ^a   You, Han ^a  

^a XIAMEN UNIVERSITY   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

Author keywords

Apoptosis; BBC3; Chaperone mediated autophagy; IKBKB; IKK ; PUMA; TNF

Indexed keywords

HEAT SHOCK COGNATE PROTEIN 70; PUMA PROTEIN; TUMOR NECROSIS FACTOR; APOPTOSIS REGULATORY PROTEIN; BBC3 PROTEIN, HUMAN; CHAPERONE; I KAPPA B KINASE; ONCOPROTEIN; PHOSPHOSERINE; SERINE;

APOPTOSIS; ARTICLE; CELL DEATH; CHAPERONE-MEDIATED AUTOPHAGY; CONTROLLED STUDY; CYTOSOL; FEMALE; HUMAN; HUMAN CELL; LYSOSOME; MITOCHONDRION; PHOSPHORYLATION; TUMOR CELL; AUTOPHAGY; BIOLOGICAL MODEL; DRUG EFFECTS; METABOLISM; PROTEIN DEGRADATION; PROTEIN STABILITY; TUMOR CELL LINE;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE, TUMOR; HUMANS; I-KAPPA B KINASE; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN STABILITY; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS; SERINE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84947777062     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1075688     Document Type: Article

References (40)

1. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D. Impaired degradation of mutant a-synuclein by chaperone-mediated autophagy. Science 2004; 305:1292-5; PMID:15333840; http://dx.doi.org/10.1126/science.1101738
2. Kabuta T, Furuta A, Aoki S, Furuta K, Wada K. Aberrant interaction between Parkinson disease-associated mutant UCH-L1 and the lysosomal receptor for chaperone-mediated autophagy. J Biol Chem 2008; 283:23731-8; PMID:18550537; http://dx.doi.org/10.1074/jbc.M801918200
3. Orenstein SJ, Kuo SH, Tasset I, Arias E, Koga H, Fernandez-Carasa I, Cortes E, Honig LS, Dauer W, Consiglio A, et al. Interplay of LRRK2 with chaperonemediated autophagy. Nat Neurosci 2013; 16:394-406; PMID:23455607; http://dx.doi.org/10.1038/nn.3350
4. Wang Y, Martinez-Vicente M, Kruger U, Kaushik S, Wong E, Mandelkow EM, Cuervo AM, Mandelkow E. Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Hum Mol Genet 2009; 18:4153-70; PMID:19654187; http://dx.doi.org/10.1093/hmg/ddp367
5. Yang Q, She H, Gearing M, Colla E, Lee M, Shacka JJ, Mao Z. Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Science 2009; 323:124-7; PMID:19119233; http://dx.doi.org/10.1126/science.1166088
6. Kon M, Kiffin R, Koga H, Chapochnick J, Macian F, Varticovski L, Cuervo AM. Chaperone-mediated autophagy is required for tumor growth. Sci Transl Med 2011; 3:109ra17; PMID:22089453; http://dx.doi.org/10.1126/scitranslmed.3003182
7. Lv L, Li D, Zhao D, Lin R, Chu Y, Zhang H, Zha Z, Liu Y, Li Z, Xu Y, et al. Acetylation targets the M2 isoform of pyruvate kinase for degradation through chaperone-mediated autophagy and promotes tumor growth. Mol Cell 2011; 42:719-30; PMID:21700219; http://dx.doi.org/10.1016/j.molcel.2011.04.025
8. Vakifahmetoglu-Norberg H, Kim M, Xia HG, Iwanicki MP, Ofengeim D, Coloff JL, Pan L, Ince TA, Kroemer G, Brugge JS, et al. Chaperone-mediated autophagy degrades mutant p53. Genes Dev 2013; 27:1718-30; PMID:23913924; http://dx.doi.org/10.1101/gad.220897.113
9. Cuervo AM, Knecht E, Terlecky SR, Dice JF. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am J Physiol 1995; 269:C1200-8; PMID:7491910
10. Kiffin R, Christian C, Knecht E, Cuervo AM. Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell 2004; 15:4829-40; PMID:15331765; http://dx.doi.org/10.1091/mbc.E04-06-0477
11. Dice JF. Chaperone-mediated autophagy. Autophagy 2007; 3:295-9; PMID:17404494; http://dx.doi.org/10.4161/auto.4144
12. Cuervo AM, Dice JF. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 1996; 273:501-3; PMID:8662539; http://dx.doi.org/10.1126/science.273.5274.501
13. Cuervo AM, Dice JF. Regulation of lamp2a levels in the lysosomal membrane. Traffic 2000; 1:570-83; PMID:11208145; http://dx.doi.org/10.1034/j.1600-0854.2000.010707.x
14. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, Ausserlechner MJ, Adams JM, Strasser A. p53- and drug-induced apoptotic responses mediated by BH3-only proteins BBC3 and noxa. Science 2003; 302:1036-8; PMID:14500851; http://dx.doi.org/10.1126/science.1090072
15. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. BBC3 induces the rapid apoptosis of colorectal cancer cells. Mol Cell 2001; 7:673-82; PMID:11463391; http://dx.doi.org/10.1016/S1097-2765(01)00213-1
16. Nakano K, Vousden KH. BBC3, a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 7:683-94; PMID:11463392; http://dx.doi.org/10.1016/S1097-2765(01)00214-3
17. You H, Pellegrini M, Tsuchihara K, Yamamoto K, Hacker G, Erlacher M, Villunger A, Mak TW. FOXO3a-dependent regulation of BBC3 in response to cytokine/growth factor withdrawal. J Exp Med 2006; 203:1657-63; PMID:16801400; http://dx.doi.org/10.1084/jem.20060353
18. Wang P, Qiu W, Dudgeon C, Liu H, Huang C, Zambetti GP, Yu J, Zhang L. BBC3 is directly activated by NF-kappaB and contributes to TNF-a-induced apoptosis. Cell Death Differ 2009; 16:1192-202; PMID:19444283; http://dx.doi.org/10.1038/cdd.2009.51
19. Lee SH, Jung YS, Chung JY, Oh AY, Lee SJ, Choi DH, Jang SM, Jang KS, Paik SS, Ha NC, et al. Novel tumor suppressive function of Smad4 in serum starvationinduced cell death through PAK1-BBC3 pathway. Cell Death Dis 2011; 2:e235; PMID:22130069; http://dx.doi.org/10.1038/cddis.2011.116
20. Fricker M, O’Prey J, Tolkovsky AM, Ryan KM. Phosphorylation of BBC3 modulates its apoptotic function by regulating protein stability. Cell Death Dis 2010; 1: e59; PMID:21364664; http://dx.doi.org/10.1038/cddis.2010.38
21. Sandow JJ, Jabbour AM, Condina MR, Daunt CP, Stomski FC, Green BD, Riffkin CD, Hoffmann P, Guthridge MA, Silke J, et al. Cytokine receptor signaling activates an IKK-dependent phosphorylation of BBC3 to prevent cell death. Cell Death Differ 2012; 19:633-41; PMID:21997190; http://dx.doi.org/10.1038/cdd.2011.131
22. Callus BA, Moujallad DM, Silke J, Gerl R, Jabbour AM, Ekert PG, Vaux DL. Triggering of apoptosis by BBC3 is determined by the threshold set by prosurvival Bcl ¡ 2 family proteins. J Mol Biol 2008; 384:313-23; PMID:18835564; http://dx.doi.org/10.1016/j.jmb.2008.09.041
23. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
24. Cuervo AM. Autophagy: in sickness and in health. Trends Cell Biol 2004; 14:70-7; PMID:15102438; http://dx.doi.org/10.1016/j.tcb.2003.12.002
25. Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004; 306:990-5; PMID:15528435; http://dx.doi.org/10.1126/science.1099993
26. Ming L, Sakaida T, Yue W, Jha A, Zhang L, Yu J. Sp1 and p73 activate BBC3 following serum starvation. Carcinogenesis 2008; 29:1878-84; PMID:18579560; http://dx.doi.org/10.1093/carcin/bgn150
27. Cuervo AM. Chaperone-mediated autophagy: selectivity pays off. Trends Endocrinol Metab 2010; 21:142-50; PMID:19857975; http://dx.doi.org/10.1016/j.tem.2009.10.003
28. Dice JF, Terlecky SR, Chiang HL, Olson TS, Isenman LD, Short-Russell SR, Freundlieb S, Terlecky LJ. A selective pathway for degradation of cytosolic proteins by lysosomes. Sem Cell Biol 1990; 1:449-55;PMID:2103896
29. Essmann F, Pohlmann S, Gillissen B, Daniel PT, Schulze-Osthoff K, Janicke RU. Irradiation-induced translocation of p53 to mitochondria in the absence of apoptosis. J Biol Chem 2005; 280:37169-77; PMID:16148012; http://dx.doi.org/10.1074/jbc.M502052200
30. Yan J, Xiang J, Lin Y, Ma J, Zhang J, Zhang H, Sun J, Danial NN, Liu J, Lin A. Inactivation of BAD by IKK inhibits TNFalpha-induced apoptosis independently of NF-kappaB activation. Cell 2013; 152:304-15; PMID:23332762; http://dx.doi.org/10.1016/j.cell.2012.12.021
31. Kreuz S, Siegmund D, Scheurich P, Wajant H. NFkappaB inducers upregulate cFLIP, a cycloheximidesensitive inhibitor of death receptor signaling. Mol Cell Biol 2001; 21:3964-73; PMID:11359904; http://dx.doi.org/10.1128/MCB.21.12.3964-3973.2001
32. Kaushik S, Cuervo AM. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 2012; 22:407-17; PMID:22748206; http://dx.doi.org/10.1016/j.tcb.2012.05.006
33. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L. BBC3 mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci USA 2003; 100:1931-6; PMID:12574499; http://dx.doi.org/10.1073/pnas.2627984100
34. Li J, Lee B, Lee AS. Endoplasmic reticulum stressinduced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (BBC3) and NOXA by p53. J Biol Chem 2006; 281:7260-70; PMID:16407291; http://dx.doi.org/10.1074/jbc.M509868200
35. Yee KS, Wilkinson S, James J, Ryan KM, Vousden KH. BBC3- and Bax-induced autophagy contributes to apoptosis. Cell Death Differ 2009; 16:1135-45; PMID:19300452; http://dx.doi.org/10.1038/cdd.2009.28
36. Zhang L, Mei Y, Fu NY, Guan L, Xie W, Liu HH, Yu CD, Yin Z, Yu VC, You H. TRIM39 regulates cell cycle progression and DNA damage responses via stabilizing p21. Proc Natl Acad Sci USA 2012; 109:20937-42; PMID:23213251; http://dx.doi.org/10.1073/pnas.1214156110
37. Rago C, Vogelstein B, Bunz F. Genetic knockouts and knockins in human somatic cells. Nature Protocols 2007; 2:2734-46; PMID:18007609; http://dx.doi.org/10.1038/nprot.2007.408
38. Topaloglu O, Hurley PJ, Yildirim O, Civin CI, Bunz F. Improved methods for the generation of human gene knockout and knockin cell lines. Nucleic Acids Res 2005; 33:e158; PMID:16214806; http://dx.doi.org/10.1093/nar/gni160
39. Kohli M, Rago C. An efficient method for generating human somatic cell gene knockouts. Discov Med 2004; 4:37-40; PMID:20705018
40. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, Thompson CB. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003; 162:59-69; PMID:12847083; http://dx.doi.org/10.1083/jcb.200302084