Assessment of Chloroquine Treatment for Modulating Autophagy Flux in Brain of WT and HD Mice

Journal of Huntington's Disease

Volumn 3, Issue 2, 2014, Pages 159-174

  Vodicka, Petr ^a   Lim, Junghyun ^b   Williams, Dana T ^a   Kegel, Kimberly B ^a   Chase, Kathryn ^c   Park, Hyunsun ^d   Marchionini, Deanna ^d   Wilkinson, Stephen ^e   Mead, Tania ^e   Birch, Helen ^e   Yates, Dawn ^e   Lyons, Kathy ^g   Dominguez, Celia ^d   Beconi, Maria ^d,f   Yue, Zhenyu ^b   Aronin, Neil ^c   DiFiglia, Marian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d CHDI MANAGEMENT CHDI FOUNDATION   (United States)

^e BioFocus DPI   (United Kingdom)

^f Retrophin Inc   (United States)

^g NONE

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CHLOROQUINE; DEETHYLCHLOROQUINE; DIDEETHYLCHLOROQUINE; LAMP 2A PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 II; PROTEIN P62; RAB7 PROTEIN; UNCLASSIFIED DRUG; ANTIMALARIAL AGENT; GTF2H1 PROTEIN, MOUSE; HUNTINGTON PROTEIN, MOUSE; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; RAB PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN CORTEX; CONTROLLED STUDY; CORPUS STRIATUM; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG EXPOSURE; DRUG MUSCLE LEVEL; HUNTINGTON CHOREA; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; TISSUE PREPARATION; ANIMAL; BRAIN; C57BL MOUSE; DISEASE MODEL; DRUG EFFECT; GENE TARGETING; GENETICS; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANTIMALARIALS; AUTOPHAGY; BRAIN; CHLOROQUINE; DISEASE MODELS, ANIMAL; GENE KNOCK-IN TECHNIQUES; HUNTINGTON DISEASE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; RAB GTP-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84907217496     PISSN: 18796397     EISSN: 18796400     Source Type: Journal    
DOI: 10.3233/JHD-130081     Document Type: Article

References (54)

1. The Huntington's Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell. 1993;72(6):971-83.
2. Glick D, Barth S, Macleod KF. Autophagy: Cellular and molecular mechanisms. J Pathol. 2010;221(1):3-12.
3. Son JH, Shim JH, Kim K-H, Ha J-Y, Han JY. Neuronal autophagy and neurodegenerative diseases. Exp Mol Med. 2012;44(2):89-98.
4. Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci. 2010;13(7):805-11.
5. Kegel KB, Kim M, Sapp E, McIntyre C, Castaño JG, Aronin N, DiFiglia M. Huntingtin expression stimulates endosomallysosomal activity, endosome tubulation, and autophagy. J Neurosci Off J Soc Neurosci. 2000;20(19):7268-78.
6. Heng MY, Duong DK, Albin RL, Tallaksen-Greene SJ, Hunter JM, Lesort MJ, Osmand A, Paulson HL, Detloff PJ. Early autophagic response in a novel knock-in model of Huntington disease. Hum Mol Genet. 2010;19(19):3702.
7. Wu J, Qi L,WangY,Kegel KB,Yoder J, Difiglia M, Qin Z, Lin F. The regulation of N-terminal Huntingtin (Htt552) accumulation by Beclin1. Acta Pharmacol Sin. 2012;33(6):743-51.
8. Qi L, Zhang X-D, Wu J-C, Lin F, Wang J, DiFiglia M, Qin Z-H. The Role of Chaperone-Mediated Autophagy in Huntingtin Degradation. PLoS ONE. 2012;7(10):e46834.
9. 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, BurschW, Camougrand N, Cebollero E, Cecconi F, Chen Y, Chin L-S, Choi A, Chu CT, Chung J, Clarke PGH,Clark RSB, Clarke SG, ClavéC, 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, Djavaheri-Mergny M, Dorsey FC, Dröge W, Dron M, Dunn WA Jr, Duszenko M, Eissa NT, Elazar Z, Esclatine A, Eskelinen E-L, Fésüs L, Finley KD, Fuentes JM, Fueyo J, Fujisaki K, Galliot B, Gao F-B, Gewirtz DA, Gibson SB, Gohla A, Goldberg AL, Gonzalez R, González-Estévez C, Gorski S, Gottlieb RA, Häussinger D, He Y-W, Heidenreich K, Hill JA, Høyer-Hansen M, Hu X, HuangW-P, Iwasaki A, Jäättelä M, Jackson WT, Jiang X, Jin S, Johansen T, Jung JU, Kadowaki M, Kang C, Kelekar A, Kessel DH, Kiel JAKW, Kim HP, Kimchi A, Kinsella TJ, Kiselyov K, Kitamoto K, Knecht E, Komatsu M, Kominami E, Kondo S, Kovács AL, Kroemer G, Kuan C-Y, Kumar R, Kundu M, Landry J, Laporte M, Le W, Lei H-Y, Lenardo MJ, Levine B, Lieberman A, Lim K-L, Lin F-C, Liou W, Liu LF, Lopez-Berestein G, López-Otín C, Lu B, Macleod KF, Malorni W, MartinetW, Matsuoka K, Mautner J, Meijer AJ, Meléndez A, Michels P, Miotto G, MistiaenWP, Mizushima N, Mograbi B, Monastyrska I, Moore MN, Moreira PI, Moriyasu Y, Motyl T, Münz C, Murphy LO, Naqvi NI, Neufeld TP, Nishino I, Nixon RA, Noda T, Nürnberg B, Ogawa M, Oleinick NL, Olsen LJ, Ozpolat B, Paglin S, Palmer GE, Papassideri I, Parkes M, Perlmutter DH, Perry G, Piacentini M, Pinkas-Kramarski R, Prescott M, Proikas-Cezanne T, Raben N, Rami A, Reggiori F, Rohrer B, Rubinsztein DC, Ryan KM, Sadoshima J, Sakagami H, Sakai Y, Sandri M, Sasakawa C, Sass M, Schneider C, Seglen PO, Seleverstov O, Settleman J, Shacka JJ, Shapiro IM, Sibirny A, Silva-Zacarin ECM, Simon HU, Simone C, Simonsen A, Smith MA, Spanel-Borowski K, Srinivas V, SteevesM, Stenmark H, Stromhaug PE, Subauste CS, Sugimoto S, Sulzer D, Suzuki T, Swanson MS, Tabas I, Takeshita F, Talbot NJ, Tallóczy Z, Tanaka K, Tanaka K, Tanida I, Taylor GS, Taylor JP, Terman A, Tettamanti G, Thompson CB, Thumm M, Tolkovsky AM, Tooze SA, Truant R, Tumanovska LV, Uchiyama Y, Ueno T, Uzcátegui NL, van der Klei I,Vaquero EC,Vellai T,VogelMW,Wang H-G,Webster P, Wiley JW, Xi Z, Xiao G, Yahalom J, Yang J-M, Yap G, Yin X-M, Yoshimori T, Yu L, Yue Z, Yuzaki M, Zabirnyk O, Zheng X, Zhu X, Deter RL. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4(2):151-75.
10. He H, Dang Y, Dai F, Guo Z, Wu J, She X, Pei Y, Chen Y, Ling W, Wu C, Zhao S, Liu JO, Yu L. Post-translational Modifications of Three Members of the Human MAP1LC3 Family and Detection of a Novel Type of Modification for MAP1LC3B. J Biol Chem. 2003;278(31):29278-87.
11. Wang Q, Zhu J, Zhang K, Jiang C, Wang Y, Yuan Y, Bian J, Liu X, Gu J, Liu Z. Induction of cytoprotective autophagy in PC-12 cells by cadmium. Biochem Biophys Res Commun. 2013; 438(1):1861-192.
12. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy. 2007;3(6):542-5.
13. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun J-A, Outzen H, Øvervatn A, Bjørkøy G, Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282(33):24131-45.
14. Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, Johansen T. Chapter 12 Monitoring autophagic degradation of p62/SQSTM1. Autophagy in Mammalian Systems, Part B. Academic Press 2009, pp. 181-97.
15. Rué L, López-Soop G, Gelpi E, Martínez-Vicente M, Alberch J, Pérez-Navarro E. Brain region-and age-dependent dysregulation of p62 and NBR1 in a mouse model of Huntington's disease. Neurobiol Dis. 2013;52(0):219-28.
16. Homewood CA,Warhurst DC, PetersW, Baggaley VC. Lysosomes, pH and the Anti-malarial Action of Chloroquine. Nature. 1972;235(5332):50-2.
17. Iwai-Kanai E,Yuan H, Huang C, Sayen MR, Perry-Garza CN, Kim L, Gottlieb RA, others. A method to measure cardiac autophagic flux in vivo. Autophagy. 2008;4(3):322.
18. Ju J-S, Varadhachary AS, Miller SE, Weihl CC. Quantitation of "autophagic flux" in mature skeletal muscle. Autophagy. 2010;6(7):929-35.
19. Zois CE, Giatromanolaki A, Sivridis E, Papaiakovou M, Kainulainen H, Koukourakis MI. "Autophagic flux" in normal mouse tissues: Focus on endogenous LC3A processing. Autophagy. 2011;7(11):1371-8.
20. Floto RA, Sarkar S, Perlstein EO, Kampmann B, Rubinsztein SLS and DC. Small molecule enhancers of rapamycininduced TOR inhibition promote autophagy, reduce toxicity in Huntington's disease models and enhance killing of mycobacteria by macrophages. Autophagy. 2007;3(6):620-2.
21. Shin BH, Lim Y, Oh HJ, Park SM, Lee S-K, Ahnn J, Kim DH, Song WK, Kwak TH, Park WJ. Pharmacological activation of Sirt1 ameliorates polyglutamine-induced toxicity through the regulation of autophagy. PLoS ONE. 2013;8(6):e64953.
22. Ravikumar B,Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, Rubinsztein DC. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet. 2004;36(6):585-95.
23. Tsunemi T, Ashe TD, Morrison BE, Soriano KR, Au J, Roque RAV, Lazarowski ER, Damian VA, Masliah E, Spada ARL. PGC-1 rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci Transl Med. 2012;4(142):142ra97-142ra97.
24. Settembre C, Di Malta C, PolitoVA, Arencibia MG,Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332:1429-33.
25. Martinez-Vicente M, Talloczy Z, Wong E, Tang G, Koga H, Kaushik S, de Vries R, Arias E, Harris S, Sulzer D, Cuervo AM. Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat Neurosci. 2010;13(5):567-76.
26. Koga H, Martinez-Vicente M, Arias E, Kaushik S, Sulzer D, Cuervo AM. Constitutive upregulation of chaperonemediated autophagy in Huntington's disease. J Neurosci Off J Soc Neurosci. 2011;31(50):18492-505.
27. Bauer PO, Goswami A, Wong HK, Okuno M, Kurosawa M, Yamada M, Miyazaki H, Matsumoto G, Kino Y, Nagai Y, Nukina N. Harnessing chaperone-mediated autophagy for the selective degradation of mutant huntingtin protein. Nat Biotechnol. 2010;28:256-63.
28. Adelusi SA, Salako LA. Tissue and blood concentrations of chloroquine following chronic administration in the rat. J Pharm Pharmacol. 1982;34(11):733-5.
29. Firat E,Weyerbrock A, Gaedicke S, Grosu A-L, Niedermann G. Chloroquine or chloroquine-PI3K/Akt pathway inhibitor combinations strongly promote irradiation-induced cell death in primary stem-like glioma cells. PLoS ONE. 2012;7(10):e47357.
30. Bickar D, Reid PD. A high-affinity protein stain for western blots, tissue prints, and electrophoretic gels. Anal Biochem. 1992;203(1):109-15.
31. Pardo AD, Maglione V, Alpaugh M, Horkey M, Atwal RS, Sassone J, Ciammola A, Steffan JS, Fouad K, Truant R, Sipione S. Ganglioside GM1 induces phosphorylation of mutant huntingtin and restores normal motor behavior in Huntington disease mice. Proc Natl Acad Sci. 2012;109(9): 3528-33.
32. DiFiglia M, Sapp E, Chase K, Schwarz C, Meloni A, Young C, Martin E, Vonsattel JP, Carraway R, Reeves SA, others. Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron. 1995;14(5):1075-81.
33. Li X, Sapp E, Chase K, Comer-Tierney LA, Masso N, Alexander J, Reeves P, Kegel KB, Valencia A, Esteves M, Aronin N, DiFiglia M. Disruption of Rab11 activity in a knockin mouse model of Huntington's disease. Neurobiol Dis. 2009;36(2):374-83.
34. SmithCM,Mayer JA, Duncan ID. Autophagy promotes oligodendrocyte survival and function following dysmyelination in a long-lived myelin mutant. J Neurosci. 2013;33(18):8088-100.
35. Gutierrez MG, Munafó DB, Berón W, Colombo MI. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci. 2004;117(13):2687-97.
36. Jäger S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, Eskelinen E-L. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci. 2004;117(20):4837-48.
37. Hyttinen JMT, Niittykoski M, Salminen A, Kaarniranta K. Maturation of autophagosomes and endosomes: A key role for Rab7. Biochim Biophys Acta BBA-Mol Cell Res. 2013;1833(3):503-10.
38. Jeong H, Then F, Melia TJ, Mazzulli JR, Cui L, Savas JN,Voisine C, Paganetti P, Tanese N, Hart AC, Yamamoto A, Krainc D. Acetylation targets mutant Huntingtin to autophagosomes for degradation. Cell. 2009;137:60-72.
39. Thompson LM, Aiken CT, Kaltenbach LS, Agrawal N, Illes K, Khoshnan A, Martinez-Vincente M, Arrasate M, O'Rourke JG, Khashwji H, Lukacsovich T, Zhu Y-Z, Lau AL, Massey A, Hayden MR, Zeitlin SO, Finkbeiner S, Green KN, LaFerla FM, Bates G, Huang L, Patterson PH, Lo DC, Cuervo AM, Marsh JL, Steffan JS. IKK phosphorylates Huntingtin and targets it for degradation by the proteasome and lysosome. J Cell Biol. 2009;187(7):1083-99.
40. Sprangers R, Li X, Mao X, Rubinstein JL, Schimmer AD, Kay LE. TROSY-based NMR evidence for a novel class of 20S proteasome inhibitors. Biochemistry (Mosc). 2008;47(26):6727-34.
41. Projean D, Baune B, Farinotti R, Flinois J-P, Beaune P, Taburet A-M, Ducharme J. In vitro metabolism of chloroquine: Identification of Cyp2c8, Cyp3a4, and Cyp2d6 as the main isoforms catalyzing N-desethylchloroquine formation. Drug Metab Dispos. 2003;31(6):748-54.
42. Osifo NG. The regional uptake of chloroquine in the rat brain. Toxicol Appl Pharmacol. 1979;50(1):109-14.
43. Moore BR, Page-Sharp M, Stoney JR, Ilett KF, Jago JD, Batty KT. Pharmacokinetics, pharmacodynamics, and allometric scaling of chloroquine in a murine malaria model. Antimicrob Agents Chemother. 2011;55(8):3899-907.
44. Parson WB, Koeniger SL, Johnson RW, Erickson J, Tian Y, Stedman C, Schwartz A, Tarcsa E, Cole R, Van Berkel GJ. Analysis of chloroquine and metabolites directly from whole-body animal tissue sections by liquid extraction surface analysis (LESA) and tandem mass spectrometry. J Mass Spectrom. 2012;47(11):1420-8.
45. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Øvervatn A, Stenmark H, Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005;171(4):603-614.
46. Myeku N, Figueiredo-Pereira ME. Dynamics of the degradation of ubiquitinated proteins by proteasomes and autophagy association with sequestosome 1/p62. J Biol Chem. 2011;286(25):22426-40.
47. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006;441(7095):885-9.
48. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, KoikeM, Uchiyama Y, Kominami E, Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006;441(7095):880-4.
49. Kreutzberg GW. Neuronal dynamics and axonal flow. IV. Blockage of intra-axonal enzyme transport by colchicine. Proc Natl Acad Sci U S A. 1969;62(3):722.
50. Wang C, Liang C-C, Bian ZC, Zhu Y, Guan J-L. FIP200 is required for maintenance and differentiation of postnatal neural stem cells. Nat Neurosci. 2013;16(5):532-42.
51. Wu J, Dang Y, SuW, Liu C, Ma H, Shan Y, Pei Y,Wan B, Guo J, Yu L. Molecular cloning and characterization of rat LC3A and LC3B-Two novel markers of autophagosome. Biochem Biophys Res Commun. 2006;339(1):437-42.
52. Hariharan N, Maejima Y, Nakae J, Paik J, DePinho RA, Sadoshima J. Deacetylation of FoxO by Sirt1 plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ Res. 2010;107(12):1470-82.
53. Roscic A, Baldo B, Crochemore C, Marcellin D, Paganetti P. Induction of autophagy with catalytic mTOR inhibitors reduces huntingtin aggregates in a neuronal cell model. J Neurochem. 2011;119(2):398-407.
54. Tsvetkov AS, Arrasate M, Barmada S, Ando DM, Sharma P, Shaby BA, Finkbeiner S. Proteostasis of polyglutamine varies among neurons and predicts neurodegeneration. Nat Chem Biol. 2013;9(9):586-92.