Choline dehydrogenase interacts with SQSTM1/p62 to recruit LC3 and stimulate mitophagy

Autophagy

Volumn 10, Issue 11, 2014, Pages 1906-1920

  Park, Sungwoo ^a   Choi, Seon Guk ^a   Yoo, Seung Min ^a   Son, Jin H ^b   Jung, Yong Keun ^a  

^a Seoul National University   (South Korea)

^b Ewha Womans University   (South Korea)

Author keywords

Choline dehydrogenase; LC3; Mitophagy; PARK2 parkin; SQSTM1 p62

Indexed keywords

CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CHOLINE DEHYDROGENASE; PARKIN; PARKIN RBR E3 UBIQUITIN PROTEIN LIGASE; PROTEIN; PROTEIN LC3; PROTEIN P62; SEQUESTOSOME 1; UNCLASSIFIED DRUG; DOPAMINE; GREEN FLUORESCENT PROTEIN; LIGHT CHAIN 3, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL DNA; PROTEIN BINDING; PROTEINASE K; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; SQSTM1 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; CYTOSOL; DELETION MUTANT; DOPAMINERGIC NERVE CELL; HELA CELL LINE; HUMAN; HUMAN CELL; INNER MEMBRANE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOPHAGY; MOLECULAR BIOLOGY; OUTER MEMBRANE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; ANIMAL; CHEMISTRY; FLOW CYTOMETRY; GENE DELETION; HEK293 CELL LINE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MITOCHONDRION; NERVE CELL; TUMOR CELL LINE;

MAMMALIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE, TUMOR; CHOLINE DEHYDROGENASE; CHROMATOGRAPHY, LIQUID; CYTOSOL; DNA, MITOCHONDRIAL; DOPAMINE; ENDOPEPTIDASE K; FLOW CYTOMETRY; GENE DELETION; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; MASS SPECTROMETRY; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; NEURONS; PROTEIN BINDING; RNA, SMALL INTERFERING; UBIQUITIN-PROTEIN LIGASES;

EID: 84919777530     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.32177     Document Type: Article

References (52)

1. De Ridder JJ, van Dam K. The efflux of betaine from rat-liver mitochondria, a possible regulating step in choline oxidation. Biochim Biophys Acta 1973; 291: 557-63; PMID: 4690868; http://dx.doi.org/10.1016/0005-2736(73)90507-5
2. Garrow TA Purification, kinetic properties, and cDNA cloning of mammalian betaine-homocysteine methyltransferase. J Biol Chem 1996; 271: 22831-8; PMID: 8798461
3. Olthof MR, Verhoef P. Effects of betaine intake on plasma homocysteine concentrations and consequences for health. Curr Drug Metab 2005; 6: 15-22; PMID: 15720203; http://dx.doi.org/10.2174/1389200052997366
4. Ma XJ, Wang Z, Ryan PD, Isakoff SJ, Barmettler A, Fuller A, Muir B, Mohapatra G, Salunga R, Tuggle JT, et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 2004; 5: 607-16; PMID: 15193263; http://dx.doi.org/10.1016/j.ccr.2004.05.015
5. Wang Z, Dahiya S, Provencher H, Muir B, Carney E, Coser K, Shioda T, Ma XJ, Sgroi DC. The prognostic biomarkers HOXB13, IL17BR, and CHDH are regulated by estrogen in breast cancer. Clin Cancer Res 2007; 13: 6327-34; PMID: 17975144; http://dx.doi.org/10.1158/1078-0432.CCR-07-0310
6. Johnson AR, Craciunescu CN, Guo Z, Teng YW, Thresher RJ, Blusztajn JK, Zeisel SH. Deletion of murine choline dehydrogenase results in diminished sperm motility. FASEB J 2010; 24: 2752-61; PMID: 20371614; http://dx.doi.org/10.1096/fj.09-153718
7. da Costa KA, Kozyreva OG, Song J, Galanko JA, Fischer LM, Zeisel SH. Common genetic polymorphisms affect the human requirement for the nutrient choline. FASEB J 2006; 20: 1336-44; PMID: 16816108; http://dx.doi.org/10.1096/fj.06-5734com
8. Xu X, Gammon MD, Zeisel SH, Lee YL, Wetmur JG, Teitelbaum SL, Bradshaw PT, Neugut AI, Santella RM, Chen J. Choline metabolism and risk of breast cancer in a population-based study. FASEB J 2008; 22: 2045-52; PMID: 18230680; http://dx.doi.org/10.1096/fj.07-101279
9. Johnson AR, Lao S, Wang T, Galanko JA, Zeisel SH. Choline dehydrogenase polymorphism rs12676 is a functional variation and is associated with changes in human sperm cell function. PLoS One 2012; 7: e36047; PMID: 22558321; http://dx.doi.org/10.1371/journal.pone.0036047
10. Tatsuta T, Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 2008; 27: 306-14; PMID: 18216873; http://dx.doi.org/10.1038/sj.emboj.7601972
11. Ding WX, Ni HM, Li M, Liao Y, Chen X, Stolz DB, Dorn GW 2nd, Yin XM. 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 2010; 285: 27879-90; PMID: 20573959; http://dx.doi.org/10.1074/jbc.M110.119537
12. Itakura E, Kishi-Itakura C, Koyama-Honda I, Mizushima N. Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J Cell Sci 2012; 125: 1488-99; PMID: 22275429; http://dx.doi.org/10.1242/jcs.094110
13. Joo JH, Dorsey FC, Joshi A, Hennessy-Walters KM, Rose KL, McCastlain K, Zhang J, Iyengar R, Jung CH, Suen DF, et al. Hsp90-Cdc37 chaperone complex regulates Ulk1- and Atg13-mediated mitophagy. Mol Cell 2011; 43: 572-85; PMID: 21855797; http://dx.doi.org/10.1016/j.molcel.2011.06.018
14. Ashrafi G, Schwarz TL. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ 2013; 20: 31-42; PMID: 22743996; http://dx.doi.org/10.1038/cdd.2012.81
15. Chu CT, Zhu J, Dagda R. Beclin 1-independent pathway of damage-induced mitophagy and autophagic stress: implications for neurodegeneration and cell death. Autophagy 2007; 3: 663-6; PMID: 17622797; http://dx.doi.org/10.4161/auto.4625
16. Gilkerson RW, De Vries RL, Lebot P, Wikstrom JD, Torgyekes E, Shirihai OS, Przedborski S, Schon EA. Mitochondrial autophagy in cells with mtDNA mutations results from synergistic loss of transmembrane potential and mTORC1 inhibition. Hum Mol Genet 2012; 21: 978-90; PMID: 22080835; http://dx.doi.org/10.1093/hmg/ddr529
17. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998; 392: 605-8; PMID: 9560156; http://dx.doi.org/10.1038/33416
18. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004; 304: 1158-60; PMID: 15087508; http://dx.doi.org/10.1126/science.1096284
19. Greene AW, Grenier K, Aguileta MA, Muise S, Farazifard R, Haque ME, McBride HM, Park DS, Fon EA. Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep 2012; 13: 378-85; PMID: 22354088; http://dx.doi.org/10.1038/embor.2012.14
20. Jin SM, Lazarou M, Wang C, Kane LA, Narendra DP, Youle RJ. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol 2010; 191: 933-42; PMID: 21115803; http://dx.doi.org/10.1083/jcb.201008084
21. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, Sou YS, Saiki S, Kawajiri S, Sato F, et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol 2010; 189: 211-21; PMID: 20404107; http://dx.doi.org/10.1083/jcb.200910140
22. Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 2009; 17: 98-109; PMID: 19619495; http://dx.doi.org/10.1016/j.devcel.2009.06.014
23. Okamoto K, Kondo-Okamoto N, Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 2009; 17: 87-97; PMID: 19619494; http://dx.doi.org/10.1016/j.devcel.2009.06.013
24. Orvedahl A, Sumpter R Jr., Xiao G, Ng A, Zou Z, Tang Y, Narimatsu M, Gilpin C, Sun Q, Roth M, et al. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 2011; 480: 113-7; PMID: 22020285; http://dx.doi.org/10.1038/nature10546
25. Cai Q, Zakaria HM, Simone A, Sheng ZH. Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr Biol 2012; 22: 545-52; PMID: 22342752; http://dx.doi.org/10.1016/j.cub.2012.02.005
26. Geisler S, Holmström KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12: 119-31; PMID: 20098416; http://dx.doi.org/10.1038/ncb2012
27. Kim NC, Tresse E, Kolaitis RM, Molliex A, Thomas RE, Alami NH, Wang B, Joshi A, Smith RB, Ritson GP, et al. VCP is essential for mitochondrial quality control by PINK1/Parkin and this function is impaired by VCP mutations. Neuron 2013; 78: 65-80; PMID: 23498974; http://dx.doi.org/10.1016/j.neuron.2013.02.029
28. Son JH, Chun HS, Joh TH, Cho S, Conti B, Lee JW. Neuroprotection and neuronal differentiation studies using substantia nigra dopaminergic cells derived from transgenic mouse embryos. J Neurosci 1999; 19: 10-20; PMID: 9870933
29. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8: e1000298; PMID: 20126261; http://dx.doi.org/10.1371/journal.pbio.1000298
30. Lazarou M, Jin SM, Kane LA, Youle RJ. Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev Cell 2012; 22: 320-33; PMID: 22280891; http://dx.doi.org/10.1016/j.devcel.2011.12.014
31. Lever M, Slow S. The clinical significance of betaine, an osmolyte with a key role in methyl group metabolism. Clin Biochem 2010; 43: 732-44; PMID: 20346934; http://dx.doi.org/10.1016/j.clinbiochem.2010.03.009
32. Lin CS, Wu RD. Choline Oxidation and Choline Dehydrogenase. J Protein Chem 1986; 5: 193-200; http://dx.doi.org/10.1007/BF01025488
33. Huang S, Lin Q. Functional expression and processing of rat choline dehydrogenase precursor. Biochem Biophys Res Commun 2003; 309: 344-50; PMID: 12951056; http://dx.doi.org/10.1016/j.bbrc.2003.08.010
34. Reichert AS, Neupert W. Contact sites between the outer and inner membrane of mitochondria-role in protein transport. Biochim Biophys Acta 2002; 1592: 41-9; PMID: 12191767; http://dx.doi.org/10.1016/S0167-4889(02)00263-X
35. Chu CT, Ji J, Dagda RK, Jiang JF, Tyurina YY, Kapralov AA, Tyurin VA, Yanamala N, Shrivastava IH, Mohammadyani D, et al. Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat Cell Biol 2013; 15: 1197-205; PMID: 24036476; http://dx.doi.org/10.1038/ncb2837
36. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, 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: 24131-45; PMID: 17580304; http://dx.doi.org/10.1074/jbc.M702824200
37. Jin SM, Youle RJ. PINK1- and Parkin-mediated mitophagy at a glance. J Cell Sci 2012; 125: 795-9; PMID: 22448035; http://dx.doi.org/10.1242/jcs.093849
38. Watanabe Y, Tanaka M. p62/SQSTM1 in autophagic clearance of a non-ubiquitylated substrate. J Cell Sci 2011; 124: 2692-701; PMID: 21771882; http://dx.doi.org/10.1242/jcs.081232
39. Gal J, Ström AL, Kwinter DM, Kilty R, Zhang J, Shi P, Fu W, Wooten MW, Zhu H. Sequestosome 1/p62 links familial ALS mutant SOD1 to LC3 via an ubiquitin-independent mechanism. J Neurochem 2009; 111: 1062-73; PMID: 19765191; http://dx.doi.org/10.1111/j.1471-4159.2009.06388.x
40. Exner N, Lutz AK, Haass C, Winklhofer KF. Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J 2012; 31: 3038-62; PMID: 22735187; http://dx.doi.org/10.1038/emboj.2012.170
41. Mandemakers W, Morais VA, De Strooper B. A cell biological perspective on mitochondrial dysfunction in Parkinson disease and other neurodegenerative diseases. J Cell Sci 2007; 120: 1707-16; PMID: 17502481; http://dx.doi.org/10.1242/jcs.03443
42. Deas E, Plun-Favreau H, Gandhi S, Desmond H, Kjaer S, Loh SH, Renton AE, Harvey RJ, Whitworth AJ, Martins LM, et al. PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum Mol Genet 2011; 20: 867-79; PMID: 21138942; http://dx.doi.org/10.1093/hmg/ddq526
43. Lee JY, Nagano Y, Taylor JP, Lim KL, Yao TP. Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J Cell Biol 2010; 189: 671-9; PMID: 20457763; http://dx.doi.org/10.1083/jcb.201001039
44. Narendra D, Kane LA, Hauser DN, Fearnley IM, Youle RJ. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010; 6: 1090-106; PMID: 20890124; http://dx.doi.org/10.4161/auto.6.8.13426
45. Wilson MI, Gill DJ, Perisic O, Quinn MT, Williams RL. PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol Cell 2003; 12: 39-50; PMID: 12887891; http://dx.doi.org/10.1016/S1097-2765(03)00246-6
46. Lamark T, Perander M, Outzen H, Kristiansen K, Øvervatn A, Michaelsen E, Bjørkøy G, Johansen T. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem 2003; 278: 34568-81; PMID: 12813044; http://dx.doi.org/10.1074/jbc.M303221200
47. Okatsu K, Saisho K, Shimanuki M, Nakada K, Shitara H, Sou YS, Kimura M, Sato S, Hattori N, Komatsu M, et al. p62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria. Genes Cells 2010; 15: 887-900; PMID: 20604804
48. Lee JY, Koga H, Kawaguchi Y, Tang W, Wong E, Gao YS, Pandey UB, Kaushik S, Tresse E, Lu J, et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 2010; 29: 969-80; PMID: 20075865; http://dx.doi.org/10.1038/emboj.2009.405
49. Liu L, Feng D, Chen G, Chen M, Zheng Q, Song P, Ma Q, Zhu C, Wang R, Qi W, et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxiainduced mitophagy in mammalian cells. Nat Cell Biol 2012; 14: 177-85; PMID: 22267086; http://dx.doi.org/10.1038/ncb2422
50. Novak I, Dikic I. Autophagy receptors in developmental clearance of mitochondria. Autophagy 2011; 7: 301-3; PMID: 21206218; http://dx.doi.org/10.4161/auto.7.3.14509
51. Pyo JO, Yoo SM, Ahn HH, Nah J, Hong SH, Kam TI, Jung S, Jung YK. Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nat Commun 2013; 4: 2300; PMID: 23939249; http://dx.doi.org/10.1038/ncomms3300
52. Park S, Lee KM, Ju JH, Kim J, Noh DY, Lee T, Shin I. Protein expression profiling of primary mammary epithelial cells derived from MMTV-neu mice revealed that HER2/NEU-driven changes in protein expression are functionally clustered. IUBMB Life 2010; 62: 41-50; PMID: 19960538