Targeting SQSTM1/p62 induces cargo loading failure and converts autophagy to apoptosis via NBK/Bik

Molecular and Cellular Biology

Volumn 34, Issue 18, 2014, Pages 3435-3449

  Chen, Shuang ^a   Zhou, Liang ^a   Zhang, Yu ^a,b   Leng, Yun ^a,c   Pei, Xin Yan ^a   Lin, Hui ^a   Jones, Richard ^d   Orlowski, Robert Z ^d   Dai, Yun ^a   Grant, Steven ^a,e  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b NORTHEAST NORMAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; ADAPTOR PROTEIN; ADAPTOR PROTEIN SQSTM1; AUTOPHAGY PROTEIN 5; BECLIN 1; BH3 PROTEIN; BH3 PROTEIN NBK; CHLOROQUINE; CYCLIN DEPENDENT KINASE 9; CYCLIN T1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; PROTEIN; PROTEIN P62; SHORT HAIRPIN RNA; ULK1 PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; U266 CELL LINE; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BORONIC ACIDS; CELL LINE, TUMOR; CELLS, CULTURED; CYCLIN T; CYCLIN-DEPENDENT KINASE 9; CYCLOHEXIMIDE; FLAVONOIDS; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HUMANS; LEUPEPTINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; PIPERIDINES; PROTEIN TRANSPORT; PYRAZINES; PYRROLES; RNA, SMALL INTERFERING;

EID: 84906043176     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01383-13     Document Type: Article

References (62)

1. Elgendy M, Sheridan C, Brumatti G, Martin SJ. 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.
2. Janku F, McConkey DJ, Hong DS, Kurzrock R. 2011. Autophagy as a target for anticancer therapy. Nat. Rev. Clin. Oncol. 8:528-539. http://dx.doi.org/10.1038/nrclinonc.2011.71.
3. Levine B, Sinha S, Kroemer G. 2008. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4:600-606.
4. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939. http://dx.doi.org/10.1016/j.cell.2005.07.002.
5. Chen S, Dai Y, Pei XY, Myers J, Wang L, Kramer LB, Garnett M, Schwartz DM, Su F, Simmons GL, Richey JD, Larsen DG, Dent P, Orlowski RZ, Grant S. 2012. CDK inhibitors up-regulate BH3-only proteins to sensitize human myeloma cells to BH3 mimetic therapies. Cancer Res. 72:4225-4237. http://dx.doi.org/10.1158/0008-5472.CAN-12-1118.
6. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676. http://dx.doi.org/10.1038/45257.
7. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, Hickman JA, Geneste O, Kroemer G. 2007. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 26:2527-2539. http://dx.doi.org/10.1038/sj.emboj.7601689.
8. Bonapace L, Bornhauser BC, Schmitz M, Cario G, Ziegler U, Niggli FK, Schafer BW, Schrappe M, Stanulla M, Bourquin JP. 2010. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J. Clin. Invest. 120:1310-1323. http://dx.doi.org/10.1172/JCI39987.
9. White E. 2012. Deconvoluting the context-dependent role for autophagy in cancer. Nat. Rev. Cancer 12:401- 410. http://dx.doi.org/10.1038/nrc3262.
10. White E, Dipaola RS. 2009. The double-edged sword of autophagy modulation in cancer. Clin. Cancer Res. 15:5308-5316. http://dx.doi.org/10.1158/1078-0432.CCR-07-5023.
11. Amaravadi RK, Lippincott-Schwartz J, Yin XM, Weiss WA, Takebe N, Timmer W, Dipaola RS, Lotze MT, White E. 2011. Principles and current strategies for targeting autophagy for cancer treatment. Clin. Cancer Res. 17:654-666. http://dx.doi.org/10.1158/1078-0432.CCR-10-2634.
12. Lee JY, Koga H, Kawaguchi Y, Tang W, Wong E, Gao YS, Pandey UB, Kaushik S, Tresse E, Lu J, Taylor JP, Cuervo AM, Yao TP. 2010. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 29:969-980. http://dx.doi.org/10.1038/emboj.2009.405.
13. He C, Klionsky DJ. 2009. Regulation mechanisms and signaling pathwaysof autophagy. Annu. Rev. Genet. 43:67-93. http://dx.doi.org/10.1146/annurev-genet-102808-114910.
14. Deretic V. 2010. A master conductor for aggregate clearance by autophagy. Dev. Cell 18:694-696. http://dx.doi.org/10.1016/j.devcel.2010.04.009.
15. Dikic I, Johansen T, Kirkin V. 2010. Selective autophagy in cancer development and therapy. Cancer Res. 70:3431-3434. http://dx.doi.org/10.1158/0008-5472.CAN-09-4027.
16. Kraft C, Peter M, Hofmann K. 2010. Selective autophagy: ubiquitinmediated recognition and beyond. Nat. Cell Biol. 12:836-841. http://dx.doi.org/10.1038/ncb0910-836.
17. Itakura E, Mizushima N. 2011. p62 targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J. Cell Biol. 192:17-27. http://dx.doi.org/10.1083/jcb.201009067.
18. Weidberg H, Shvets E, Elazar Z. 2011. Biogenesis and cargo selectivity of autophagosomes. Annu. Rev. Biochem. 80:125-156. http://dx.doi.org/10.1146/annurev-biochem-052709-094552.
19. Kirkin V, Lamark T, Sou YS, Bjorkoy G, Nunn JL, Bruun JA, Shvets E, McEwan DG, Clausen TH, Wild P, Bilusic I, Theurillat JP, Overvatn A, Ishii T, Elazar Z, Komatsu M, Dikic I, Johansen T. 2009. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33: 505-516. http://dx.doi.org/10.1016/j.molcel.2009.01.020.
20. Johansen T, Lamark T. 2011. Selective autophagy mediated by autophagic adapter proteins. Autophagy 7:279-296. http://dx.doi.org/10.4161/auto.7.3.14487.
21. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T. 2007. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282:24131-24145. http://dx.doi.org/10.1074/jbc.M702824200.
22. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. 2005. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtininduced cell death. J. Cell Biol. 171:603- 614. http://dx.doi.org/10.1083/jcb.200507002.
23. Ichimura Y, Kominami E, Tanaka K, Komatsu M. 2008. Selective turnover of p62/A170/SQSTM1 by autophagy. Autophagy 4:1063-1066.
24. Ding WX, Ni HM, Li M, Liao Y, Chen X, Stolz DB, Dorn GW, Yin XM. 2010. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62- mediated mitochondrial priming. J. Biol. Chem. 285:27879-27890. http://dx.doi.org/10.1074/jbc.M110.119537.
25. Kirkin V, McEwan DG, Novak I, Dikic I. 2009. A role for ubiquitin in selective autophagy. Mol. Cell 34:259-269. http://dx.doi.org/10.1016/j.molcel.2009.04.026.
26. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, Bray K, Reddy A, Bhanot G, Gelinas C, Dipaola RS, Karantza-Wadsworth V, White E. 2009. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137:1062-1075. http://dx.doi.org/10.1016/j.cell.2009.03.048.
27. Iwata J, Ezaki J, Komatsu M, Yokota S, Ueno T, Tanida I, Chiba T, Tanaka K, Kominami E. 2006. Excess peroxisomes are degraded by autophagic machinery in mammals. J. Biol. Chem. 281:4035-4041. http://dx.doi.org/10.1074/jbc.M512283200.
28. Martinez-Vicente M, Talloczy Z, Wong E, Tang G, Koga H, Kaushik S, de Vries R, Arias E, Harris S, Sulzer D, Cuervo AM. 2010. Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat. Neurosci. 13:567-576. http://dx.doi.org/10.1038/nn.2528.
29. Wong E, Bejarano E, Rakshit M, Lee K, Hanson HH, Zaarur N, Phillips GR, Sherman MY, Cuervo AM. 2012. Molecular determinants of selective clearance of protein inclusions by autophagy. Nat. Commun. 3:1240. http://dx.doi.org/10.1038/ncomms2244.
30. Linares JF, Duran A, Yajima T, Pasparakis M, Moscat J, Diaz-Meco MT. 2013. K63 polyubiquitination and activation of mTOR by the p62- TRAF6 complex in nutrient-activated cells. Mol. Cell 51:283-296. http://dx.doi.org/10.1016/j.molcel.2013.06.020.
31. Calvo-Garrido J, Escalante R. 2010. Autophagy dysfunction and ubiquitin- positive protein aggregates in Dictyostelium cells lacking Vmp1. Autophagy 6:100-109. http://dx.doi.org/10.4161/auto.6.1.10697.
32. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT, Bursch W, Camougrand N, Ce-bollero E, Cecconi F, Chen Y, Chin LS, Choi A, Chu CT, Chung J, Clarke PG, Clark RS, Clarke SG, Clave C, Cleveland JL, Codogno P, Colombo MI, Coto-Montes A, Cregg JM, Cuervo AM, Debnath J, Demarchi F, Dennis PB, Dennis PA, Deretic V, Devenish RJ, Di Sano F, Dice JF, Difiglia M, Dinesh-Kumar S, Distelhorst CW, et al. 2008. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4:151-175.
33. Mizushima N, Yoshimori T, Levine B. 2010. Methods in mammalian autophagy research. Cell 140:313-326. http://dx.doi.org/10.1016/j.cell.2010.01.028.
34. Jackson WT, Giddings TH, Jr, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3:e156. http://dx.doi.org/10.1371/journal.pbio.0030156.
35. N'Diaye EN, Kajihara KK, Hsieh I, Morisaki H, Debnath J, Brown EJ. 2009. PLIC proteins or ubiquilins regulate autophagy-dependent cell survival during nutrient starvation. EMBO Rep. 10:173-179. http://dx.doi.org/10.1038/embor.2008.238.
36. Gamerdinger M, Kaya AM, Wolfrum U, Clement AM, Behl C. 2011.BAG3 mediates chaperone-based aggresome-targeting and selective autophagy of misfolded proteins. EMBO Rep. 12:149-156. http://dx.doi.org/10.1038/embor.2010.203.
37. Hoang B, Benavides A, Shi Y, Frost P, Lichtenstein A. 2009. Effect of autophagy on multiple myeloma cell viability. Mol. Cancer Ther. 8:1974-1984. http://dx.doi.org/10.1158/1535-7163.MCT-08-1177.
38. Schwartz-Roberts JL, Shajahan AN, Cook KL, Warri A, Abu-Asab M, Clarke R. 2013. GX15-070 (obatoclax) induces apoptosis and inhibits cathepsin D- and L-mediated autophagosomal lysis in antiestrogenresistant breast cancer cells. Mol. Cancer Ther. 12:448-459. http://dx.doi.org/10.1158/1535-7163.MCT-12-0617.
39. Bauer PO, Goswami A, Wong HK, Okuno M, Kurosawa M, Yamada M, Miyazaki H, Matsumoto G, Kino Y, Nagai Y, Nukina N. 2010. Harnessing chaperone-mediated autophagy for the selective degradation of mutant huntingtin protein. Nat. Biotechnol. 28:256-263. http://dx.doi.org/10.1038/nbt.1608.
40. Johnson AJ, Yeh YY, Smith LL, Wagner AJ, Hessler J, Gupta S, Flynn J, Jones J, Zhang X, Bannerji R, Grever MR, Byrd JC. 2012. The novel cyclin-dependent kinase inhibitor dinaciclib (SCH727965) promotes apoptosis and abrogates microenvironmental cytokine protection in chronic lymphocytic leukemia cells. Leukemia 26:2554-2557. http://dx.doi.org/10.1038/leu.2012.144.
41. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A. 2011. TFEB links autophagy to lysosomal biogenesis. Science 332:1429-1433. http://dx.doi.org/10.1126/science .1204592.
42. Su H, Li F, Ranek MJ, Wei N, Wang X. 2011. COP9 signalosome regulates autophagosome maturation. Circulation 124:2117-2128. http://dx.doi.org/10.1161/CIRCULATIONAHA.111.048934.
43. Kimmelman AC. 2011. The dynamic nature of autophagy in cancer. Genes Dev. 25:1999-2010. http://dx.doi.org/10.1101/gad.17558811.
44. Myeku N, Figueiredo-Pereira ME. 2011. Dynamics of the degradation of ubiquitinated proteins by proteasomes and autophagy: association with sequestosome 1/p62. J. Biol. Chem. 286:22426-22440. http://dx.doi.org/10.1074/jbc.M110.149252.
45. Dai Y, Grant S. 2004. Small molecule inhibitors targeting cyclindependent kinases as anticancer agents. Curr. Oncol. Rep. 6:123-130. http://dx.doi.org/10.1007/s11912-004-0024-3.
46. Liu J, Xia H, Kim M, Xu L, Li Y, Zhang L, Cai Y, Norberg HV, Zhang T, Furuya T, Jin M, Zhu Z, Wang H, Yu J, Li Y, Hao Y, Choi A, Ke H, Ma D, Yuan J. 2011. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell 147:223-234. http://dx.doi.org/10.1016/j.cell.2011.08.037.
47. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G. 2005. Inhibition of macroautophagy triggersapoptosis. Mol. Cell. Biol. 25:1025-1040. http://dx.doi.org/10.1128/MCB.25.3.1025-1040.2005.
48. Germain M, Mathai JP, Shore GC. 2002. BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J. Biol. Chem. 277:18053-18060. http://dx.doi.org/10.1074/jbc.M201235200.
49. Chang NC, Nguyen M, Germain M, Shore GC. 2010. Antagonism of Beclin 1-dependent autophagy by BCL-2 at the endoplasmic reticulum requires NAF-1. EMBO J. 29:606-618. http://dx.doi.org/10.1038/emboj.2009.369.
50. Zhu H, Zhang L, Dong F, Guo W, Wu S, Teraishi F, Davis JJ, Chiao PJ, Fang B. 2005. Bik/NBK accumulation correlates with apoptosisinduction by bortezomib (PS-341, Velcade) and other proteasome inhibitors. Oncogene 24:4993- 4999. http://dx.doi.org/10.1038/sj.onc.1208683.
51. Lopez J, Hesling C, Prudent J, Popgeorgiev N, Gadet R, Mikaelian I, Rimokh R, Gillet G, Gonzalo P. 2012. Src tyrosine kinase inhibits apoptosis through the Erk1/2-dependent degradation of the death accelerator Bik. Cell Death Differ. 19:1459 -1469. http://dx.doi.org/10.1038/cdd.2012.21.
52. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB. 2007. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J. Clin. Invest. 117:326-336. http://dx.doi.org/10.1172/JCI28833.
53. Cho DH, Jo YK, Hwang JJ, Lee YM, Roh SA, Kim JC. 2009. Caspasemediated cleavage of ATG6/Beclin-1 links apoptosis to autophagy in HeLa cells. Cancer Lett. 274:95-100. http://dx.doi.org/10.1016/j.canlet.2008.09.004.
54. Luo S, Rubinsztein DC. 2010. Apoptosis blocks Beclin 1-dependent autophagosome synthesis-an effect rescued by Bcl-xL. Cell Death Differ. 17:268 -277. http://dx.doi.org/10.1038/cdd.2009.121.
55. Wirawan E, Vande Walle L, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I, Roelandt R, De Rycke R, Verspurten J, Declercq W, Agostinis P, Vanden Berghe T, Lippens S, Vandenabeele P. 2010. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis. 1:e18. http://dx.doi.org/10.1038/cddis.2009.16.
56. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU. 2006. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat. Cell Biol. 8:1124-1132. http://dx.doi.org/10.1038/ncb1482.
57. Betin VM, Lane JD. 2009. Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis. J. Cell Sci. 122:2554-2566. http://dx.doi.org/10.1242/jcs.046250.
58. Tsvetkov AS, Miller J, Arrasate M, Wong JS, Pleiss MA, Finkbeiner S. 2010. A small-molecule scaffold induces autophagy in primary neurons and protects against toxicity in a Huntington disease model. Proc. Natl. Acad. Sci. U. S. A. 107:16982-16987. http://dx.doi.org/10.1073/pnas.1004498107.
59. Ling J, Kang Y, Zhao R, Xia Q, Lee DF, Chang Z, Li J, Peng B, Fleming JB, Wang H, Liu J, Lemischka IR, Hung MC, Chiao PJ. 2012. KrasG12D-induced IKK2/beta/NF-kappaB activation by IL-1alpha and p62 feedforward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell 21:105-120. http://dx.doi.org/10.1016/j.ccr.2011.12.006.
60. Maiuri MC, Criollo A, Kroemer G. 2010. Crosstalk between apoptosis and autophagy within the Beclin 1 interactome. EMBO J. 29:515-516. http://dx.doi.org/10.1038/emboj.2009.377.
61. Wong E, Cuervo AM. 2010. Integration of clearance mechanisms: the proteasome and autophagy. Cold Spring Harb. Perspect. Biol. 2:a006734. http://dx.doi.org/10.1101/cshperspect.a006734.
62. Ma X, Godar RJ, Liu H, Diwan A. 2012. Enhancing lysosome biogenesis attenuates BNIP3-induced cardiomyocyte death. Autophagy 8:297-309. http://dx.doi.org/10.4161/auto.18658.