High-resolution visualization and assessment of basal and OXPHOS-induced mitophagy in H9c2 cardiomyoblasts

References

• Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev. 2014 Jul;94(3):909–950. Pubmed PMID: 24987008. doi: 10.1152/physrev.00026.2013
   PubMed Web of Science ®Google Scholar
• Pathak T, Trebak M. Mitochondrial Ca2+ signaling. Pharmacol Ther. 2018 Dec;192:112–123. Pubmed PMID: 30036491. doi: 10.1016/j.pharmthera.2018.07.001
   PubMed Web of Science ®Google Scholar
• Dietz JV, Fox JL, Khalimonchuk O. Down the Iron path: mitochondrial Iron Homeostasis and Beyond. Cells. 2021 Aug 25;10(9):2198. Pubmed PMID: 34571846. doi: 10.3390/cells10092198
   PubMed Web of Science ®Google Scholar
• Sandhir R, Halder A, Sunkaria A. Mitochondria as a centrally positioned hub in the innate immune response. Biochim Biophys Acta Mol Basis Dis. 2017 May;1863(5):1090–1097. Pubmed PMID: 27794419. doi: 10.1016/j.bbadis.2016.10.020
   PubMed Web of Science ®Google Scholar
• Bock FJ, Tait SWG. Mitochondria as multifaceted regulators of cell death. Nat Rev Mol Cell Biol. 2020 Feb;21(2):85–100. Pubmed PMID: 31636403. doi: 10.1038/s41580-019-0173-8
   PubMed Web of Science ®Google Scholar
• Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012 Aug 31;337(6098):1062–1065. Pubmed PMID: 22936770. doi: 10.1126/science.1219855
   PubMed Web of Science ®Google Scholar
• Kruppa AJ, Buss F. Motor proteins at the mitochondria-cytoskeleton interface. J Cell Sci. 2021 Apr 1;134(7):jcs226084. Pubmed PMID: 33912943. doi: 10.1242/jcs.226084
   PubMed Web of Science ®Google Scholar
• Yapa NMB, Lisnyak V, Reljic B, et al. Mitochondrial dynamics in health and disease. FEBS Lett. 2021 Apr;595(8):1184–1204. Pubmed PMID: 33742459. doi: 10.1002/1873-3468.14077
   PubMed Web of Science ®Google Scholar
• Montava-Garriga L, Ganley IG. Outstanding questions in mitophagy: what we do and do not know. J Mol Biol. 2020 Jan 3;432(1):206–230. Pubmed PMID: 31299243. doi: 10.1016/j.jmb.2019.06.032
   PubMed Web of Science ®Google Scholar
• Ng MYW, Wai T, Simonsen A. Quality control of the mitochondrion. Developmental Cell. 2021 Apr 5;56(7):881–905. Pubmed PMID: 33662258. doi: 10.1016/j.devcel.2021.02.009
   PubMed Web of Science ®Google Scholar
• Lemasters JJ. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 2005;8(1):3–5. Spring Spring. doi: 10.1089/rej.2005.8.3
   PubMed Web of Science ®Google Scholar
• Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys. 2007 Jun 15;462(2):245–253. PubmedPMID: 17475204. doi: 10.1016/j.abb.2007.03.034
   PubMed Web of Science ®Google Scholar
• Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011 Jan;12(1):9–14. Pubmed PMID: 21179058. doi: 10.1038/nrm3028
   PubMed Web of Science ®Google Scholar
• Palikaras K, Lionaki E, Tavernarakis N. Mechanisms of mitophagy in cellular homeostasis, physiology and pathology. Nat Cell Biol. 2018 Sep;20(9):1013–1022. Pubmed PMID: 30154567. doi: 10.1038/s41556-018-0176-2
   PubMed Web of Science ®Google Scholar
• Zachari M, Ganley IG, Lane JD, et al. The mammalian ULK1 complex and autophagy initiation. Essays Biochem. 2017 Dec 12;61(6):585–596. Pubmed PMID: 29233870. doi: 10.1042/EBC20170021
   PubMed Web of Science ®Google Scholar
• Egan DF, Shackelford DB, Mihaylova MM, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science. 2011 Jan 28;331(6016):456–461. Pubmed PMID: 21205641. doi: 10.1126/science.1196371
   PubMed Web of Science ®Google Scholar
• Wu W, Tian W, Hu Z, et al. ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. EMBO Rep. 2014 May;15(5):566–575. Pubmed PMID: 24671035. doi: 10.1002/embr.201438501
   PubMed Web of Science ®Google Scholar
• Laker RC, Drake JC, Wilson RJ, et al. Ampk phosphorylation of Ulk1 is required for targeting of mitochondria to lysosomes in exercise-induced mitophagy. Nat Commun. 2017 Sep 15;8(1):548. Pubmed PMID: 28916822. doi: 10.1038/s41467-017-00520-9
   PubMed Web of Science ®Google Scholar
• Murakawa T, Okamoto K, Omiya S, et al. A mammalian mitophagy receptor, Bcl2-L-13, recruits the ULK1 complex to induce mitophagy. Cell Rep. 2019 Jan 8;26(2):338–345. Pubmed PMID: 30625316. doi: 10.1016/j.celrep.2018.12.050
   PubMed Web of Science ®Google Scholar
• Martens S, Fracchiolla D. Activation and targeting of ATG8 protein lipidation. Cell Discov. 2020 May 5;6(1):23. Pubmed PMID: 32377373. doi: 10.1038/s41421-020-0155-1
   PubMed Web of Science ®Google Scholar
• Tanida I, Mizushima N, Kiyooka M, et al. Apg7p/Cvt2p: a novel protein-activating enzyme essential for autophagy. Mol Biol Cell. 1999 May;10(5):1367–1379. Pubmed PMID: 10233150. doi: 10.1091/mbc.10.5.1367
   PubMed Web of Science ®Google Scholar
• Tanida I, Tanida-Miyake E, Ueno T, et al. The human homolog of Saccharomyces cerevisiae Apg7p is a Protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J Biol Chem. 2001 Jan 19;276(3):1701–1706. Pubmed PMID: 11096062. doi: 10.1074/jbc.C000752200
   PubMed Web of Science ®Google Scholar
• Komatsu M, Tanida I, Ueno T, et al. The C-terminal region of an Apg7p/Cvt2p is required for homodimerization and is essential for its E1 activity and E1-E2 complex formation. J Biol Chem. 2001 Mar 30;276(13):9846–9854. Pubmed PMID: 11139573. doi: 10.1074/jbc.M007737200
   PubMed Web of Science ®Google Scholar
• Honda S, Arakawa S, Nishida Y, et al. Ulk1-mediated Atg5-independent macroautophagy mediates elimination of mitochondria from embryonic reticulocytes. Nat Commun. 2014 Jun 4;5(1):4004. Pubmed PMID: 24895007. doi: 10.1038/ncomms5004
   PubMed Web of Science ®Google Scholar
• Hirota Y, Yamashita S, Kurihara Y, et al. Mitophagy is primarily due to alternative autophagy and requires the MAPK1 and MAPK14 signaling pathways. Autophagy. 2015;11(2):332–343. Pubmed PMID: 25831013. doi: 10.1080/15548627.2015.1023047
   PubMed Web of Science ®Google Scholar
• Wang L, Klionsky DJ, Shen HM. The emerging mechanisms and functions of microautophagy. Nat Rev Mol Cell Biol. 2022 Sep 12;24(3):186–203. Pubmed PMID: 36097284. doi: 10.1038/s41580-022-00529-z
   PubMed Web of Science ®Google Scholar
• Hammerling BC, Najor RH, Cortez MQ, et al. A Rab5 endosomal pathway mediates Parkin-dependent mitochondrial clearance. Nat Commun. 2017 Jan 30;8(1):14050. Pubmed PMID: 28134239. doi: 10.1038/ncomms14050
   PubMedGoogle Scholar
• Saito T, Nah J, Oka SI, et al. An alternative mitophagy pathway mediated by Rab9 protects the heart against ischemia. J Clin Invest. 2019 Feb 1;129(2):802–819. Pubmed PMID: 30511961. doi: 10.1172/JCI122035
   PubMed Web of Science ®Google Scholar
• Wong YC, Ysselstein D, Krainc D. Mitochondria-lysosome contacts regulate mitochondrial fission via RAB7 GTP hydrolysis. Nature. 2018;554(7692):382–386. Feb 15 Pubmed PMID: 29364868 doi: 10.1038/nature25486
   PubMed Web of Science ®Google Scholar
• McWilliams TG, Muqit MM. PINK1 and Parkin: emerging themes in mitochondrial homeostasis. Curr Opin Cell Biol. 2017 Apr;45:83–91. Pubmed PMID: 28437683. doi: 10.1016/j.ceb.2017.03.013
   PubMed Web of Science ®Google Scholar
• Narendra D, Tanaka A, Suen DF, et al. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Bio. 2008 Dec 1;183(5):795–803. Pubmed PMID: 19029340. doi: 10.1083/jcb.200809125
   PubMed Web of Science ®Google Scholar
• Narendra DP, Jin SM, Tanaka A, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010 Jan 26;8(1):e1000298. Pubmed PMID: 20126261. doi: 10.1371/journal.pbio.1000298
   PubMed Web of Science ®Google Scholar
• Wang Y, Serricchio M, Jauregui M, et al. Deubiquitinating enzymes regulate PARK2-mediated mitophagy. Autophagy. 2015 Apr 3;11(4):595–606. Pubmed PMID: 25915564. doi: 10.1080/15548627.2015.1034408
   PubMed Web of Science ®Google Scholar
• Bhujabal Z, Birgisdottir ÅB, Sjøttem E, et al. FKBP8 recruits LC3A to mediate Parkin-independent mitophagy. EMBO Rep. 2017 Jun;18(6):947–961. Pubmed PMID: 28381481. doi: 10.15252/embr.201643147
   PubMed Web of Science ®Google Scholar
• Opstad IS, Godtliebsen G, Ahluwalia BS, et al. Mitochondrial dynamics and quantification of mitochondria-derived vesicles in cardiomyoblasts using structured illumination microscopy. J Biophoto. 2022 Feb;15(2):e202100305. Pubmed PMID: 34766731. doi: 10.1002/jbio.202100305
   PubMed Web of Science ®Google Scholar
• Shaner NC, Steinbach PA, Tsien RY. A guide to choosing fluorescent proteins. Nat Methods. 2005 Dec;2(12):905–909. Pubmed PMID: 16299475. doi: 10.1038/nmeth819
   PubMed Web of Science ®Google Scholar
• Dott W, Mistry P, Wright J, et al. Modulation of mitochondrial bioenergetics in a skeletal muscle cell line model of mitochondrial toxicity. Redox Biol. 2014. Jan 10;2:224–233. Pubmed PMID: 24494197. doi: 10.1016/j.redox.2013.12.028.
   PubMed Web of Science ®Google Scholar
• Wu H, Chen Q. Hypoxia activation of mitophagy and its role in disease pathogenesis. Antioxid Redox Signal. 2015 Apr 20;22(12):1032–1046. Pubmed PMID: 25526784. doi: 10.1089/ars.2014.6204
   PubMed Web of Science ®Google Scholar
• Katayama H, Kogure T, Mizushima N, et al. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem Biol. 2011 Aug 26;18(8):1042–1052. Pubmed PMID: 21867919. doi: 10.1016/j.chembiol.2011.05.013
   PubMedGoogle Scholar
• Sun N, Malide D, Liu J, et al. A fluorescence-based imaging method to measure in vitro and in vivo mitophagy using mt-Keima. Nat Protoc. 2017 Aug;12(8):1576–1587. Pubmed PMID: 28703790. doi: 10.1038/nprot.2017.060
   PubMed Web of Science ®Google Scholar
• Twig G, Elorza A, Molina AJ, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. Embo J. 2008 Jan 23;27(2):433–446. Pubmed PMID: 18200046. doi: 10.1038/sj.emboj.7601963
   PubMed Web of Science ®Google Scholar
• Kleele T, Rey T, Winter J, et al. Distinct fission signatures predict mitochondrial degradation or biogenesis. Nature. 2021 May;593(7859):435–439. Pubmed PMID: 33953403. doi: 10.1038/s41586-021-03510-6
   PubMed Web of Science ®Google Scholar
• Sekh AA, Opstad IS, Godtliebsen G, et al. Physics-based machine learning for subcellular segmentation in living cells. Nat Mach Intell. 2021;3(12):1071–1080. doi: 10.1038/s42256-021-00420-0
   Google Scholar
• Punnakkal AR, Godtliebsen G, Somani A, et al. Analyzing mitochondrial morphology through simulation supervised learning. J Vis Exp. 2023 Mar 3;(193). Pubmed PMID: 36939264. doi: 10.3791/64880-v
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay P, Rajesh M, Haskó G, et al. Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc. 2007;2(9):2295–2301. Pubmed PMID: 17853886. doi: 10.1038/nprot.2007.327
   PubMed Web of Science ®Google Scholar
• Marroquin LD, Hynes J, Dykens JA, et al. Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants. Toxicol Sci. 2007 Jun;97(2):539–547. Pubmed PMID: 17361016. doi: 10.1093/toxsci/kfm052
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)1. Autophagy. 2021 Jan;17(1):1–382. Pubmed PMID: 33634751. doi: 10.1080/15548627.2020.1797280
   PubMed Web of Science ®Google Scholar
• Collier JJ, Suomi F, Oláhová M, et al. Emerging roles of ATG7 in human health and disease. EMBO Mol Med. 2021 Dec 7;13(12):e14824. Pubmed PMID: 34725936. doi: 10.15252/emmm.202114824
   PubMed Web of Science ®Google Scholar
• Zhao JF, Rodger CE, Allen GFG, et al. HIF1α-dependent mitophagy facilitates cardiomyoblast differentiation. Cell Stress. 2020 Mar 4;4(5):99–113. Pubmed PMID: 32420530. doi: 10.15698/cst2020.05.220
   PubMedGoogle Scholar
• Söderberg O, Gullberg M, Jarvius M, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006 Dec;3(12):995–1000. Pubmed PMID: 17072308. doi: 10.1038/nmeth947
   PubMed Web of Science ®Google Scholar
• Sun N, Yun J, Liu J, et al. Measuring in vivo mitophagy. Molecular Cell. 2015 Nov 19;60(4):685–696. Pubmed PMID: 26549682. doi: 10.1016/j.molcel.2015.10.009
   PubMed Web of Science ®Google Scholar
• McWilliams TG, Prescott AR, Allen GF, et al. Mito-QC illuminates mitophagy and mitochondrial architecture in vivo. J Cell Bio. 2016 Aug 1;214(3):333–345. Pubmed PMID: 27458135. doi: 10.1083/jcb.201603039
   PubMed Web of Science ®Google Scholar
• McWilliams TG, Prescott AR, Montava-Garriga L, et al. Basal mitophagy occurs independently of PINK1 in mouse tissues of high metabolic demand. Cell Metab. 2018 Feb 6;27(2):439–449.e5. Pubmed PMID: 29337137. doi: 10.1016/j.cmet.2017.12.008
   PubMed Web of Science ®Google Scholar
• Lee JJ, Sanchez-Martinez A, Martinez Zarate A, et al. Basal mitophagy is widespread in Drosophila but minimally affected by loss of Pink1 or parkin. J Cell Bio. 2018 May 7;217(5):1613–1622. Pubmed PMID: PMID: 29500189. doi: 10.1083/jcb.201801044
   PubMed Web of Science ®Google Scholar
• Cornelissen T, Vilain S, Vints K, et al. Deficiency of parkin and PINK1 impairs age-dependent mitophagy in Drosophila. Elife. 2018 May 29;7:e35878. Pubmed PMID: 29809156. doi: 10.7554/eLife.35878
   PubMed Web of Science ®Google Scholar
• Singh F, Prescott AR, Rosewell P, et al. Pharmacological rescue of impaired mitophagy in Parkinson’s disease-related LRRK2 G2019S knock-in mice. Elife. 2021 Aug 3;10:e67604. Pubmed PMID: 34340748. doi: 10.7554/eLife.67604
   PubMedGoogle Scholar
• Munson MJ, Mathai BJ, Ng MYW, et al. GAK and PRKCD are positive regulators of PRKN-independent mitophagy. Nat Commun. 2021 Oct 20;12(1):6101. Pubmed PMID: 34671015. doi: 10.1038/s41467-021-26331-7
   PubMed Web of Science ®Google Scholar
• Allen GF, Toth R, James J, et al. Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep. 2013 Dec;14(12):1127–1135. Pubmed PMID: 24176932. doi: 10.1038/embor.2013.168
   PubMed Web of Science ®Google Scholar
• Rojansky R, Cha MY, Chan DC. Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. Elife. 2016 Nov 17;5:e17896. Pubmed PMID: 27852436. doi: 10.7554/eLife.17896
   PubMed Web of Science ®Google Scholar
• Abudu YP, Shrestha BK, Zhang W, et al. SAMM50 acts with p62 in piecemeal basal- and OXPHOS-induced mitophagy of SAM and MICOS components. J Cell Bio. 2021 Aug 2;220(8):e202009092. Pubmed PMID: 34037656. doi: 10.1083/jcb.202009092
   PubMed Web of Science ®Google Scholar
• Montava-Garriga L, Singh F, Ball G, et al. Semi-automated quantitation of mitophagy in cells and tissues. Mech Ageing Dev. 2020 Jan;185:111196. Pubmed PMID: 31843465. doi: 10.1016/j.mad.2019.111196
   PubMed Web of Science ®Google Scholar
• Melser S, Chatelain EH, Lavie J, et al. Rheb regulates mitophagy induced by mitochondrial energetic status. Cell Metab. 2013 May 7;17(5):719–730. Pubmed PMID: 23602449. doi: 10.1016/j.cmet.2013.03.014
   PubMed Web of Science ®Google Scholar
• Guerroué F L, Eck F, Jung J, et al. Autophagosomal content profiling reveals an LC3C-Dependent piecemeal mitophagy pathway. Mol Cell. 2017 Nov 16;68(4):786–796.e6. Pubmed PMID: 29149599. doi: 10.1016/j.molcel.2017.10.029
   PubMed Web of Science ®Google Scholar
• Van Laar VS, Arnold B, Cassady SJ, et al. Bioenergetics of neurons inhibit the translocation response of Parkin following rapid mitochondrial depolarization. Hum Mol Genet. 2011 Mar 1;20(5):927–940. Pubmed PMID: 21147754. doi: 10.1093/hmg/ddq531
   PubMed Web of Science ®Google Scholar
• MacVicar TD, Lane JD. Impaired OMA1-dependent cleavage of OPA1 and reduced DRP1 fission activity combine to prevent mitophagy in cells that are dependent on oxidative phosphorylation. J Cell Sci. 2014 May 15;127(Pt 10):2313–2325. Pubmed PMID: 24634514. doi: 10.1242/jcs.144337
   PubMed Web of Science ®Google Scholar
• Lee S, Zhang C, Liu X. Role of glucose metabolism and ATP in maintaining PINK1 levels during Parkin-mediated mitochondrial damage responses. J Biol Chem. 2015 Jan 9;290(2):904–917. Pubmed PMID: 25404737. doi: 10.1074/jbc.M114.606798
   PubMed Web of Science ®Google Scholar
• Zhen Y, Spangenberg H, Munson MJ, et al. ESCRT-mediated phagophore sealing during mitophagy. Autophagy. 2020 May;16(5):826–841. Pubmed PMID: 31366282. doi: 10.1080/15548627.2019.1639301
   PubMed Web of Science ®Google Scholar
• Krantz S, Kim YM, Srivastava S, et al. Mitophagy mediates metabolic reprogramming of induced pluripotent stem cells undergoing endothelial differentiation. J Biol Chem. 2021 Dec;297(6):101410. Pubmed PMID: 34785214. doi: 10.1016/j.jbc.2021.101410
   PubMed Web of Science ®Google Scholar
• Jung M, Choi H, Kim J, et al. Correlative light and transmission electron microscopy showed details of mitophagy by mitochondria quality control in propionic acid treated SH-SY5Y cell. Materials. 2020 Sep 29;13(19):4336. Pubmed PMID: 33003589. doi: 10.3390/ma13194336
   PubMed Web of Science ®Google Scholar
• Li H, Doric Z, Berthet A, et al. Longitudinal tracking of neuronal mitochondria delineates PINK1/Parkin-dependent mechanisms of mitochondrial recycling and degradation. Sci Adv. 2021 Aug 6;7(32):eabf6580. Pubmed PMID: 34362731. doi: 10.1126/sciadv.abf6580
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012 Jun 28;9(7):676–682. Pubmed PMID: 22743772. doi: 10.1038/nmeth.2019
   PubMed Web of Science ®Google Scholar
• Paul-Gilloteaux P, Heiligenstein X, Belle M, et al. Ec-CLEM: flexible multidimensional registration software for correlative microscopies. Nat Methods. 2017 Jan 31;14(2):102–103. Pubmed PMID:28139674. doi: 10.1038/nmeth.4170
   PubMed Web of Science ®Google Scholar
• de Chaumont F, Dallongeville S, Chenouard N, et al. Icy: an open bioimage informatics platform for extended reproducible research. Nat Methods. 2012 Jun 28;9(7):690–696. Pubmed PMID:22743774. doi: 10.1038/nmeth.2075
   PubMed Web of Science ®Google Scholar
• Nunez-Iglesias J, Blanch AJ, Looker O, et al. A new Python library to analyse skeleton images confirms malaria parasite remodelling of the red blood cell membrane skeleton. PeerJ. 2018 Feb 15;6:e4312. Pubmed PMID: 29472997. doi: 10.7717/peerj.4312
   PubMed Web of Science ®Google Scholar