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Research Paper

CUL3 (cullin 3)-mediated ubiquitination and degradation of BECN1 (beclin 1) inhibit autophagy and promote tumor progression

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Pages 4323-4340 | Received 27 May 2020, Accepted 23 Mar 2021, Published online: 12 May 2021

References

  • Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol. 2010;22(2):124–131.
  • Kliosnky D. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition) (vol 12, pg 1, 2015). Autophagy. 2016;12(2):443.
  • Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132(1):27–42.
  • Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science. 2004;306(5698):990–995.
  • Kang R, Zeh HJ, Lotze MT, et al. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011;18(4):571–580.
  • Funderburk SF, Wang QJ, Yue Z. The Beclin 1-VPS34 complex–at the crossroads of autophagy and beyond. Trends Cell Biol. 2010;20(6):355–362.
  • Matsunaga K, Saitoh T, Tabata K, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol. 2009;11(4):385–396.
  • Zhong Y, Wang QJ, Li X, et al. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol. 2009;11(4):468–476.
  • Wang RC, Wei YJ, An ZY, et al. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science. 2012;338(6109):956–959.
  • Zalckvar E, Berissi H, Mizrachy L, et al. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-X-L and induction of autophagy. EMBO Rep. 2009;10(3):285–292.
  • Wei YJ, Zou ZJ, Becker N, et al. EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance. Cell. 2013;154(6):1269–1284.
  • Yue ZY, Jin SK, Yang CW, et al. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A. 2003;100(25):15077–15082.
  • Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402(6762):672–676.
  • Qu XP, Yu J, Bhagat G, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 2003;112(12):1809–1820.
  • Chau V, Tobias JW, Bachmair A, et al. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science (New York, NY). 1989;243(4898):1576–1583.
  • Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67(1)::425–479.
  • Hoeller D, Dikic I. Targeting the ubiquitin system in cancer therapy. Nature. 2009;458(7237):438–444.
  • Richardson PG, Barlogie B, Berenson J, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med. 2003;348(26):2609–2617.
  • Enchev RI, Schulman BA, Peter M. Protein neddylation: beyond cullin-RING ligases. Nat Rev Mol Cell Biol. 2015;16(1):30–44.
  • Genschik P, Sumara I, Lechner E. The emerging family of CULLIN3-RING ubiquitin ligases (CRL3s): cellular functions and disease implications. Embo J. 2013;32(17):2307–2320.
  • Dhanoa BS, Cogliati T, Satish AG, et al. Update on the Kelch-like (KLHL) gene family. Hum Genomics. 2013;7(1):13.
  • Hosokawa N, Hara T, Kaizuka T, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell. 2009;20(7):1981–1991.
  • Russell RC, Tian Y, Yuan H, et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol. 2013;15(7):741–750.
  • Kim J, Kim YC, Fang C, et al. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell. 2013;152(1–2):290–303.
  • Maejima Y, Kyoi S, Zhai PY, et al. Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2. Nat Med. 2013;19(11):1478-+.
  • Wei Y, Zou Z, Becker N, et al. EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance. Cell. 2013;154(6):1269–1284.
  • Shi CS, Kehrl JH. TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci Signal. 2010;3(123):ra42.
  • Fusco C, Mandriani B, Di Rienzo M, et al. TRIM50 regulates Beclin 1 proautophagic activity. Biochim Biophys Acta Mol Cell Res. 2018;1865(6):908–919.
  • Sun T, Li X, Zhang P, et al. Acetylation of Beclin 1 inhibits autophagosome maturation and promotes tumour growth. Nat Commun. 2015;6(1):7215.
  • Li X, Wu XQ, Deng R, et al. CaMKII-mediated Beclin 1 phosphorylation regulates autophagy that promotes degradation of Id and neuroblastoma cell differentiation. Nat Commun. 2017;8(1):1159.
  • Liu CC, Lin YC, Chen YH, et al. Cul3-KLHL20 ubiquitin ligase governs the turnover of ULK1 and VPS34 complexes to control autophagy termination. Mol Cell. 2016;61(1):84–97.
  • Ji CH, Kwon YT. Crosstalk and interplay between the ubiquitin-proteasome system and autophagy. Mol Cells. 2017;40(7):441–449.
  • Clague MJ, Urbe S. Ubiquitin: same molecule, different degradation pathways. Cell. 2010;143(5):682–685.
  • Collins GA, Goldberg AL. The logic of the 26S proteasome. Cell. 2017;169(5):792–806.
  • Ciechanover A, Stanhill A. The complexity of recognition of ubiquitinated substrates by the 26S proteasome. Biochim Biophys Acta. 2014;1843(1):86–96.
  • Tan JMM, Wong ESP, Kirkpatrick DS, et al. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet. 2008;17(3):431–439.
  • Kirkin V, Lamark T, Sou YS, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell. 2009;33(4):505–516.
  • Pandey UB, Nie ZP, Batlevi Y, et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature. 2007;447(7146):859–863.
  • Cha-Molstad H, Sung KS, Hwang J, et al. Amino-terminal arginylation targets endoplasmic reticulum chaperone BiP for autophagy through p62 binding. Nat Cell Biol. 2015;17(7):917–929.
  • Korolchuk VI, Menzies FM, Rubinsztein DC. A novel link between autophagy and the ubiquitin-proteasome system. Autophagy. 2009;5(6):862–863.
  • Korolchuk VI, Mansilla A, Menzies FM, et al. Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol Cell. 2009;33(4):517–527.
  • Qiao LY, Zhang JH. Inhibition of lysosomal functions reduces proteasomal activity. Neurosci Lett. 2009;456(1):15–19.
  • Bayraktar O, Oral O, Kocaturk NM, et al. IBMPFD disease-causing mutant VCP/p97 proteins are targets of autophagic-lysosomal degradation. PloS One. 2016;11(10): e0164864.
  • Marshall RS, McLoughlin F, Vierstra RD. Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep. 2016;16(6):1717–1732.
  • Marshall RS, Li FQ, Gemperline DC, et al. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/Ubiquitin receptor RPN10 in arabidopsis. Mol Cell. 2015;58(6):1053–1066.
  • Jia R, Bonifacino JS. Regulation of LC3B levels by ubiquitination and proteasomal degradation. Autophagy. 2020;16(2):382–384.
  • Li Y, Zhou X, Zhang Y, et al. CUL4B regulates autophagy via JNK signaling in diffuse large B-cell lymphoma. Cell Cycle. 2019;18(4):379–394.
  • Shin HJ, Kim H, Oh S, et al. AMPK-SKP2-CARM1 signalling cascade in transcriptional regulation of autophagy. Nature. 2016;534(7608):553–557.
  • Antonioli M, Albiero F, Nazio F, et al. AMBRA1 interplay with cullin E3 ubiquitin ligases regulates autophagy dynamics. Dev Cell. 2014;31(6):734–746.
  • Gao D, Inuzuka H, Tan MK, et al. mTOR drives its own activation via SCF(betaTrCP)-dependent degradation of the mTOR inhibitor DEPTOR. Mol Cell. 2011;44(2):290–303.
  • Chen J, Ou Y, Yang Y, et al. KLHL22 activates amino-acid-dependent mTORC1 signalling to promote tumorigenesis and ageing. Nature. 2018;557(7706):585–589.
  • Lee Y, Chou TF, Pittman SK, et al. Keap1/cullin3 modulates p62/SQSTM1 activity via UBA domain ubiquitination. Cell Rep. 2017;20(8):1994.
  • Cao Z, Xue J, Cheng Y, et al. MDM2 promotes genome instability by ubiquitinating the transcription factor HBP1. Oncogene. 2019;38(24):4835–4855.
  • Lee YR, Yuan WC, Ho HC, et al. The cullin 3 substrate adaptor KLHL20 mediates DAPK ubiquitination to control interferon responses. Embo J. 2010;29(10):1748–1761.

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