A novel curcumin analog binds to and activates TFEB in vitro and in vivo independent of MTOR inhibition

Autophagy

Volumn 12, Issue 8, 2016, Pages 1372-1389

  Song, Ju Xian ^a   Sun, Yue Ru ^b   Peluso, Ivana ^c   Zeng, Yu ^a   Yu, Xing ^a   Lu, Jia Hong ^d   Xu, Zheng ^b   Wang, Ming Zhong ^a   Liu, Liang Feng ^a   Huang, Ying Yu ^a   Chen, Lei Lei ^a   Durairajan, Siva Sundara Kumar ^a   Zhang, Hong Jie ^a   Zhou, Bo ^e   Zhang, Hong Qi ^a   Lu, Aiping ^a   Ballabio, Andrea ^c   Medina, Diego L ^c   Guo, Zhihong ^b   Li, Min ^a  

^a HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^c TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^d University of Macau   (Macao)

^e LANZHOU UNIVERSITY   (China)

Author keywords

autophagy; curcumin analogs; lysosomal biogenesis; mechanistic target of rapamycin; transcription factor EB

Indexed keywords

CURCUMIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN; TFEB PROTEIN; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; MTOR PROTEIN, RAT; PROTEIN BINDING; TARGET OF RAPAMYCIN KINASE; TCFEB PROTEIN, MOUSE; TFEB PROTEIN, HUMAN; TFEB PROTEIN, RAT;

ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISSOCIATION CONSTANT; DRUG PROTEIN BINDING; ENHANCER REGION; FEMALE; HELA CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; ISOTHERMAL TITRATION CALORIMETRY; LYSOSOME; MALE; MOLECULAR WEIGHT; MOUSE; NEUROBLASTOMA CELL LINE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; BRAIN; CELL NUCLEUS; CHEMISTRY; DEGENERATIVE DISEASE; METABOLISM; PHOSPHORYLATION; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; AUTOPHAGY; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BRAIN; CELL NUCLEUS; CURCUMIN; HELA CELLS; HUMANS; LYSOSOMES; MALE; MICE; NEURODEGENERATIVE DISEASES; PHOSPHORYLATION; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; TOR SERINE-THREONINE KINASES;

EID: 84976541097     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1179404     Document Type: Article

References (55)

1. E.L.Eskelinen, P.Saftig. Autophagy:a lysosomal degradation pathway with a central role in health and disease. Biochim Biophys Acta 2009; 1793:664-73; PMID:18706940; http://dx.doi.org/10.1016/j.bbamcr.2008.07.014
2. A.P.Lieberman, R.Puertollano, N.Raben, S.Slaugenhaupt, S.U.Walkley, A.Ballabio. Autophagy in lysosomal storage disorders. Autophagy 2012; 8:719-30; PMID:22647656; http://dx.doi.org/10.4161/auto.19469
3. T.Pan, S.Kondo, W.Le, J.Jankovic. The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson disease. Brain 2008; 131:1969-78; PMID:18187492; http://dx.doi.org/10.1093/brain/awm318
4. R.A.Nixon. The role of autophagy in neurodegenerative disease. Nat Med 2013; 19:983-97; PMID:23921753; http://dx.doi.org/10.1038/nm.3232
5. C.Settembre, C.Di Malta, V.A.Polito, M.Garcia Arencibia, F.Vetrini, S.Erdin, S.U.Erdin, T.Huynh, D.Medina, P.Colella, et al. TFEB links autophagy to lysosomal biogenesis. Science 2011; 332:1429-33; PMID:21617040; http://dx.doi.org/10.1126/science.1204592
6. M.Sardiello, M.Palmieri, A.di Ronza, D.L.Medina, M.Valenza, V.A.Gennarino, C.Di Malta, F.Donaudy, V.Embrione, R.S.Polishchuk, et al. A gene network regulating lysosomal biogenesis and function. Science 2009; 325:473-7; PMID:19556463; http://dx.doi.org/10.1126/science.1174447
7. C.Settembre, R.De Cegli, G.Mansueto, P.K.Saha, F.Vetrini, O.Visvikis, T.Huynh, A.Carissimo, D.Palmer, T.J.Klisch, et al. TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat Cell Biol 2013; 15:647-58; PMID:23604321; http://dx.doi.org/10.1038/ncb2718
8. J.A.Martina, Y.Chen, M.Gucek, R.Puertollano. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy 2012; 8:903-14; PMID:22576015; http://dx.doi.org/10.4161/auto.19653
9. C.Settembre, R.Zoncu, D.L.Medina, F.Vetrini, S.Erdin, S.Erdin, T.Huynh, M.Ferron, G.Karsenty, M.C.Vellard, et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 2012; 31:1095-108; PMID:22343943; http://dx.doi.org/10.1038/emboj.2012.32
10. A.Roczniak-Ferguson, C.S.Petit, F.Froehlich, S.Qian, J.Ky, B.Angarola, T.C.Walther, S.M.Ferguson. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 2012; 5:ra42; PMID:22692423; http://dx.doi.org/10.1126/scisignal.2002790
11. M.Moskot, S.Montefusco, J.Jakobkiewicz-Banecka, P.Mozolewski, A.Wegrzyn, D.Di Bernardo, G.Węgrzyn, D.L.Medina, A.Ballabio, M.Gabig-Cimińska. The phytoestrogen genistein modulates lysosomal metabolism and transcription factor EB (TFEB) activation. J Biol Chem 2014; 289:17054-69; PMID:24770416; http://dx.doi.org/10.1074/jbc.M114.555300
12. C.Spampanato, E.Feeney, L.Li, M.Cardone, J.A.Lim, F.Annunziata, H.Zare, R.Polishchuk, R.Puertollano, G.Parenti, et al. Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol Med 2013; 5:691-706; PMID:23606558; http://dx.doi.org/10.1002/emmm.201202176
13. D.L.Medina, A.Fraldi, V.Bouche, F.Annunziata, G.Mansueto, C.Spampanato, C.Puri, A.Pignata, J.A.Martina, M.Sardiello, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell 2011; 21:421-30; PMID:21889421; http://dx.doi.org/10.1016/j.devcel.2011.07.016
14. M.Decressac, B.Mattsson, P.Weikop, M.Lundblad, J.Jakobsson, A.Bjorklund. TFEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity. Proc Natl Acad Sci U S A 2013; 110:E1817-26; PMID:23610405; http://dx.doi.org/10.1073/pnas.1305623110
15. C.Parr, R.Carzaniga, S.M.Gentleman, F.Van Leuven, J.Walter, M.Sastre. Glycogen synthase kinase 3 inhibition promotes lysosomal biogenesis and autophagic degradation of the amyloid-β precursor protein. Mol Cell Biol 2012; 32:4410-8; PMID:22927642; http://dx.doi.org/10.1128/MCB.00930-12
16. V.A.Polito, H.Li, H.Martini-Stoica, B.Wang, L.Yang, Y.Xu, D.B.Swartzlander, M.Palmieri, A.di Ronza, V.M.Lee, et al. Selective clearance of aberrant tau proteins and rescue of neurotoxicity by transcription factor EB. EMBO Mol Med 2014; 6(9):1142-60; PMID:25069841; http://dx.doi.org/10.15252/emmm.201303671
17. Q.Xiao, P.Yan, X.Ma, H.Liu, R.Perez, A.Zhu, E.Gonzales, J.M.Burchett, D.R.Schuler, J.R.Cirrito, et al. Enhancing astrocytic lysosome biogenesis facilitates Abeta clearance and attenuates amyloid plaque pathogenesis. J Neurosci 2014; 34:9607-20; PMID:25031402; http://dx.doi.org/10.1523/JNEUROSCI.3788-13.2014
18. T.Tsunemi, T.D.Ashe, B.E.Morrison, K.R.Soriano, J.Au, R.A.Roque, E.R.Lazarowski, V.A.Damian, E.Masliah, A.R.La Spada. PGC-1alpha rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci Transl Med 2012; 4:142ra97; PMID:22786682; http://dx.doi.org/10.1126/scitranslmed.3003799
19. P.Anand, A.B.Kunnumakkara, R.A.Newman, B.B.Aggarwal. Bioavailability of curcumin:problems and promises. Mol Pharm 2007; 4:807-18; PMID:17999464; http://dx.doi.org/10.1021/mp700113r
20. J.Han, X.Y.Pan, Y.Xu, Y.Xiao, Y.An, L.Tie, Y.Pan, X.J.Li. Curcumin induces autophagy to protect vascular endothelial cell survival from oxidative stress damage. Autophagy 2012; 8:812-25; PMID:22622204; http://dx.doi.org/10.4161/auto.19471
21. H.Aoki, Y.Takada, S.Kondo, R.Sawaya, B.B.Aggarwal, Y.Kondo. Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy:role of Akt and extracellular signal-regulated kinase signaling pathways. Mol Pharmacol 2007; 72:29-39; PMID:17395690; http://dx.doi.org/10.1124/mol.106.033167
22. A.Shehzad, S.Khan, O.Shehzad, Y.S.Lee. Curcumin therapeutic promises and bioavailability in colorectal cancer. Drugs Today (Barc) 2010; 46:523-32; PMID:20683505; http://dx.doi.org/10.1358/dot.2010.46.7.1509560
23. D.Subramaniam, R.May, S.M.Sureban, K.B.Lee, R.George, P.Kuppusamy, R.P.Ramanujam, K.Hideg, B.K.Dieckgraefe, C.W.Houchen, et al. Diphenyl difluoroketone:a curcumin derivative with potent in vivo anticancer activity. Cancer Res 2008; 68:1962-9; PMID:18339878; http://dx.doi.org/10.1158/0008-5472.CAN-07-6011
24. H.Ohori, H.Yamakoshi, M.Tomizawa, M.Shibuya, Y.Kakudo, A.Takahashi, S.Takahashi, S.Kato, T.Suzuki, C.Ishioka, et al. Synthesis and biological analysis of new curcumin analogues bearing an enhanced potential for the medicinal treatment of cancer. Mol Cancer Ther 2006; 5:2563-71; PMID:17041101; http://dx.doi.org/10.1158/1535-7163.MCT-06-0174
25. G.Liang, H.Zhou, Y.Wang, E.C.Gurley, B.Feng, L.Chen, J.Xiao, S.Yang, X.Li. Inhibition of LPS-induced production of inflammatory factors in the macrophages by mono-carbonyl analogues of curcumin. J Cell Mol Med 2009; 13:3370-9; PMID:19243473; http://dx.doi.org/10.1111/j.1582-4934.2009.00711.x
26. C.A.Mosley, D.C.Liotta, J.P.Snyder. Highly active anticancer curcumin analogues. Adv Exp Med Biol 2007; 595:77-103; PMID:17569206; http://dx.doi.org/10.1007/978-0-387-46401-5_2
27. A.Zheng, H.Li, X.Wang, Z.Feng, J.Xu, K.Cao, B.Zhou, J.Wu, J.Liu. Anticancer Effect of a Curcumin Derivative B63:ROS Production and Mitochondrial Dysfunction. Curr Cancer Drug Targets 2014; 14:156-66; PMID:24274397.
28. X.Zhang, H.Q.Zhang, G.H.Zhu, Y.H.Wang, X.C.Yu, X.B.Zhu, G.Liang, J.Xiao, X.K.Li. A novel mono-carbonyl analogue of curcumin induces apoptosis in ovarian carcinoma cells via endoplasmic reticulum stress and reactive oxygen species production. Mol Med Rep 2012; 5:739-44; PMID:22159410; http://dx.doi.org/10.3892/mmr.2011.700
29. C.S.Beevers, L.Chen, L.Liu, Y.Luo, N.J.Webster, S.Huang. Curcumin disrupts the Mammalian target of rapamycin-raptor complex. Cancer Res 2009; 69:1000-8; PMID:19176385; http://dx.doi.org/10.1158/0008-5472.CAN-08-2367
30. C.C.Thoreen, S.A.Kang, J.W.Chang, Q.Liu, J.Zhang, Y.Gao, L.J.Reichling, T.Sim, D.M.Sabatini, N.S.Gray. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 2009; 284:8023-32; PMID:19150980; http://dx.doi.org/10.1074/jbc.M900301200
31. J.Kim, M.Kundu, B.Viollet, K.L.Guan. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13:132-41; PMID:21258367; http://dx.doi.org/10.1038/ncb2152
32. J.Chen, J.Xie, Z.Jiang, B.Wang, Y.Wang, X.Hu. Shikonin and its analogs inhibit cancer cell glycolysis by targeting tumor pyruvate kinase-M2. Oncogene 2011; 30:4297-306; PMID:21516121; http://dx.doi.org/10.1038/onc.2011.137
33. D.J.Klionsky, F.C.Abdalla, H.Abeliovich, R.T.Abraham, A.Acevedo-Arozena, K.Adeli, L.Agholme, M.Agnello, P.Agostinis, J.A.Aguirre-Ghiso, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490
34. S.Kimura, T.Noda, T.Yoshimori. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3:452-60; PMID:17534139;
35. E.Wong, A.M.Cuervo. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 2010; 13:805-11; PMID:20581817; http://dx.doi.org/10.1038/nn.2575
36. C.Settembre, A.Fraldi, D.L.Medina, A.Ballabio. Signals from the lysosome:a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 2013; 14:283-96; PMID:23609508; http://dx.doi.org/10.1038/nrm3565
37. C.J.Cortes, H.C.Miranda, H.Frankowski, Y.Batlevi, J.E.Young, A.Le, N.Ivanov, B.L.Sopher, C.Carromeu, A.R.Muotri, et al. Polyglutamine-expanded androgen receptor interferes with TFEB to elicit autophagy defects in SBMA. Nat Neurosci 2014; 17:1180-9; PMID:25108912; http://dx.doi.org/10.1038/nn.3787
38. Q.Xiao, P.Yan, X.Ma, H.Liu, R.Perez, A.Zhu, E.Gonzales, D.L.Tripoli, L.Czerniewski, A.Ballabio, et al. Neuronal-Targeted TFEB Accelerates Lysosomal Degradation of APP, Reducing Abeta Generation and Amyloid Plaque Pathogenesis. J Neurosci 2015; 35:12137-51; PMID:26338325; http://dx.doi.org/10.1523/JNEUROSCI.0705-15.2015
39. J.Zhou, S.H.Tan, V.Nicolas, C.Bauvy, N.D.Yang, J.Zhang, Y.Xue, P.Codogno, H.M.Shen. Activation of lysosomal function in the course of autophagy via mTORC1 suppression and autophagosome-lysosome fusion. Cell Res 2013; 23:508-23; PMID:23337583; http://dx.doi.org/10.1038/cr.2013.11
40. N.Pallet, C.Legendre. Adverse events associated with mTOR inhibitors. Expert Opin Drug Saf 2013; 12:177-86; PMID:23252795; http://dx.doi.org/10.1517/14740338.2013.752814
41. H.Jia, J.R.Liggins, W.S.Chow. Entropy and biological systems:experimentally-investigated entropy-driven stacking of plant photosynthetic membranes. Sci Rep 2014; 4:4142; PMID:24561561; http://dx.doi.org/10.1038/srep04142
42. R.Perozzo, G.Folkers, L.Scapozza. Thermodynamics of protein-ligand interactions:history, presence, and future aspects. J Recept Signal Transduct Res 2004; 24:1-52; PMID:15344878
43. J.A.Martina, R.Puertollano. Rag GTPases mediate amino acid-dependent recruitment of TFEB and MITF to lysosomes. J Cell Biol 2013; 200:475-91; PMID:23401004; http://dx.doi.org/10.1083/jcb.201209135
44. M.Ferron, C.Settembre, J.Shimazu, J.Lacombe, S.Kato, D.J.Rawlings, A.Ballabio, G.Karsenty. A RANKL-PKCbeta-TFEB signaling cascade is necessary for lysosomal biogenesis in osteoclasts. Genes Dev 2013; 27:955-69; PMID:23599343; http://dx.doi.org/10.1101/gad.213827.113
45. M.Palmieri, S.Impey, H.Kang, A.di Ronza, C.Pelz, M.Sardiello, A.Ballabio. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 2011; 20:3852-66; PMID:21752829; http://dx.doi.org/10.1093/hmg/ddr306
46. N.Mizushima, A.Yamamoto, M.Matsui, T.Yoshimori, Y.Ohsumi. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15:1101-11; PMID:14699058; http://dx.doi.org/10.1091/mbc.E03-09-0704
47. C.He, R.Sumpter, Jr., B.Levine. Exercise induces autophagy in peripheral tissues and in the brain. Autophagy 2012; 8:1548-51; PMID:22892563; http://dx.doi.org/10.4161/auto.21327
48. J.Xiao, Y.Wang, J.Peng, L.Guo, J.Hu, M.Cao, X.Zhang, H.Zhang, Z.Wang, X.Li, et al. A synthetic compound, 1,5-bis(2-methoxyphenyl)penta-1,4-dien- 3-one (B63), induces apoptosis and activates endoplasmic reticulum stress in non-small cell lung cancer cells. Int J Cancer 2012; 131:1455-65; PMID:22189907; http://dx.doi.org/10.1002/ijc.27406
49. F.Dai, G.Y.Liu, Y.Li, W.J.Yan, Q.Wang, J.Yang, D.L.Lu, D.J.Ding, D.Lin, B.Zhou. Insights into the importance for designing curcumin-inspired anticancer agents by a prooxidant strategy:The case of diarylpentanoids. Free Radic Biol Med 2015; 85:127-37; PMID:25912482; http://dx.doi.org/10.1016/j.freeradbiomed.2015.04.017
50. H.Liu, J.Naismith. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnology 2008; 8:91; http://dx.doi.org/10.1186/1472-6750-8-91;
51. F.W.Studier. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 2005; 41:207-34; PMID:15915565
52. J.A.Martina, H.I.Diab, L.Lishu, A.L.Jeong, S.Patange, N.Raben, R.Puertollano. The nutrient-responsive transcription factor TFE3 promotes autophagy, lysosomal biogenesis, and clearance of cellular debris. Sci Signal 2014; 7:ra9; PMID:24448649; http://dx.doi.org/10.1126/scisignal.2004754
53. K.Chiu, W.M.Lau, H.T.Lau, K.F.So, R.C.Chang. Micro-dissection of rat brain for RNA or protein extraction from specific brain region. J Vis Exp 2007; 7:e269; PMID:18989440; http://dx.doi.org/10.3791/269.
54. J.Lu, L.He, C.Behrends, M.Araki, K.Araki, Q.Jun Wang, J.M.Catanzaro, S.L.Friedman, W.X.Zong, M.I.Fiel, et al. NRBF2 regulates autophagy and prevents liver injury by modulating Atg14L-linked phosphatidylinositol-3 kinase III activity. Nat Commun 2014; 5:3920; PMID:24849286; http://dx.doi.org/10.1038/ncomms4920
55. A.P.French, S.Mills, R.Swarup, M.J.Bennett, T.P.Pridmore. Colocalization of fluorescent markers in confocal microscope images of plant cells. Nat Protoc 2008; 3:619-28; PMID:18388944; http://dx.doi.org/10.1038/nprot.2008.31