In mammalian skeletal muscle, phosphorylation of TOMM22 by protein kinase CSNK2/CK2 controls mitophagy

References

• Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell. 2012;148:1145–1159. doi:10.1016/j.cell.2012.02.035. PMID:22424226
   PubMed Web of Science ®Google Scholar
• Harbauer AB, Zahedi RP, Sickmann A, Pfanner N, Meisinger C. The protein import machinery of mitochondria-a regulatory hub in metabolism, stress, and disease. Cell Metab. 2014;19:357–372. doi:10.1016/j.cmet.2014.01.010. PMID:24561263
   PubMed Web of Science ®Google Scholar
• Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. Importing mitochondrial proteins: machineries and mechanisms. Cell. 2009;138:628–644. doi:10.1016/j.cell.2009.08.005. PMID:19703392
   PubMed Web of Science ®Google Scholar
• Neupert W, Herrmann JM. Translocation of proteins into mitochondria. Annu Rev Biochem. 2007;76:723–749. doi:10.1146/annurev.biochem.76.052705.163409. PMID:17263664
   PubMed Web of Science ®Google Scholar
• Brix J, Dietmeier K, Pfanner N. Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, and Tom70. J Biol Chem. 1997;272:20730–20735. doi:10.1074/jbc.272.33.20730. PMID:9252394
   PubMed Web of Science ®Google Scholar
• Brix J, Rudiger S, Bukau B, Schneider-Mergener J, Pfanner N. Distribution of binding sequences for the mitochondrial import receptors Tom20, Tom22, and Tom70 in a presequence-carrying preprotein and a non-cleavable preprotein. J Biol Chem. 1999;274:16522–16530. doi:10.1074/jbc.274.23.16522. PMID:10347216
   PubMed Web of Science ®Google Scholar
• Young JC, Hoogenraad NJ, Hartl FU. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell. 2003;112:41–50. doi:10.1016/S0092-8674(02)01250-3. PMID:12526792
   PubMed Web of Science ®Google Scholar
• Dolezal P, Likic V, Tachezy J, Lithgow T. Evolution of the molecular machines for protein import into mitochondria. Science. 2006;313:314–318. doi:10.1126/science.1127895. PMID:16857931
   PubMed Web of Science ®Google Scholar
• Schmidt O, Harbauer AB, Rao S, Eyrich B, Zahedi RP, Stojanovski D, Schönfisch B, Guiard B, Sickmann A, Pfanner N, et al. Regulation of mitochondrial protein import by cytosolic kinases. Cell. 2011;144:227–239. doi:10.1016/j.cell.2010.12.015. PMID:21215441
   PubMed Web of Science ®Google Scholar
• Gerbeth C, Schmidt O, Rao S, Harbauer AB, Mikropoulou D, Opalinska M, Guiard B, Pfanner N, Meisinge C. Glucose-Induced Regulation of Protein Import Receptor Tom22 by Cytosolic and Mitochondria-Bound Kinases. Cell Metab. 2013;18:578–587. doi:10.1016/j.cmet.2013.09.006. PMID:24093680
   PubMed Web of Science ®Google Scholar
• Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337:1062–1065. doi:10.1126/science.1219855. PMID:22936770
   PubMed Web of Science ®Google Scholar
• Rugarli EI, Langer T. Mitochondrial quality control: a matter of life and death for neurons. EMBO J. 2012;31:1336–1349. doi:10.1038/emboj.2012.38. PMID:22354038
   PubMed Web of Science ®Google Scholar
• Exner N, Lutz AK, Haass C, Winklhofer KF. Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J. 2012;31:3038–3062. doi:10.1038/emboj.2012.170. PMID:22735187
   PubMed Web of Science ®Google Scholar
• Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011;12:9–14. doi:10.1038/nrm3028. PMID:21179058
   PubMed Web of Science ®Google Scholar
• de Lau LM, Breteler MM. Epidemiology of Parkinson's disease. Lancet Neurol. 2006;5:525–535. doi:10.1016/S1474-4422(06)70471-9. PMID:16713924
   PubMed Web of Science ®Google Scholar
• Bekris LM, Mata IF, Zabetian CP. The genetics of Parkinson disease. J Geriatr Psychiatry Neurol. 2010;23:228–242. doi:10.1177/0891988710383572. PMID:20938043
   PubMed Web of Science ®Google Scholar
• Burbulla LF, Kruger R. Converging environmental and genetic pathways in the pathogenesis of Parkinson's disease. J Neurol Sci. 2011;306:1–8. doi:10.1016/j.jns.2011.04.005. PMID:21513949
   PubMed Web of Science ®Google Scholar
• Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Turco DD, Bentivoglio AR, Healy DG, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science. 2004;304:1158–1160. doi:10.1126/science.1096284. PMID:15087508
   PubMed Web of Science ®Google Scholar
• 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;392:605–608. doi:10.1038/33416. PMID:9560156
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1371/journal.pbio.1000298. PMID:20126261
   PubMed Web of Science ®Google Scholar
• Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet. 2010;19:4861–4870. doi:10.1093/hmg/ddq419. PMID:20871098
   PubMed Web of Science ®Google Scholar
• 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;13:378–385. doi:10.1038/embor.2012.14. PMID:22354088
   PubMed Web of Science ®Google Scholar
• Kato H, Lu Q, Rapaport D, Kozjak-Pavlovic V. Tom70 is essential for PINK1 import into mitochondria. PLoS One. 2013;8:e58435. doi:10.1371/journal.pone.0058435. PMID:23472196
   PubMed Web of Science ®Google Scholar
• Yamano K, Youle RJ. PINK1 is degraded through the N-end rule pathway. Autophagy. 2013;9:1758–1769. doi:10.4161/auto.24633. PMID:24121706
   PubMed Web of Science ®Google Scholar
• Fedorowicz MA, de Vries-Schneider RL, Rub C, Becker D, Huang Y, Zhou C, Alessi Wolken DM, Voos W, Liu Y, Przedborski S. Cytosolic cleaved PINK1 represses Parkin translocation to mitochondria and mitophagy. EMBO Rep. 2013. PMID:24357652
   PubMed Web of Science ®Google Scholar
• Hasson SA, Kane LA, Yamano K, Huang CH, Sliter DA, Buehler E, Wang C, Heman-Ackah SM, Hessa T, Guha R, et al. High-content genome-wide RNAi screens identify regulators of parkin upstream of mitophagy. Nature. 2013;504:291–295. doi:10.1038/nature12748. PMID:24270810
   PubMed Web of Science ®Google Scholar
• Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, Sou Y-S, 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;189:211–221. doi:10.1083/jcb.200910140. PMID:20404107
   PubMed Web of Science ®Google Scholar
• Koyano F, Okatsu K, Kosako H, Tamura Y, Go E, Kimura M, Kimura Y, Tsuchiya H, Yoshihara H, Hirokawa T, et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature. 2014;510:162–166. PMID:24784582
   PubMed Web of Science ®Google Scholar
• Kane LA, Lazarou M, Fogel AI, Li Y, Yamano K, Sarraf SA, Banerjee S, Youle RJ. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol. 2014;205:143–153. doi:10.1083/jcb.201402104. PMID:24751536
   PubMed Web of Science ®Google Scholar
• 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;191:933–942. doi:10.1083/jcb.201008084. PMID:21115803
   PubMed Web of Science ®Google Scholar
• Becker D, Richter J, Tocilescu MA, Przedborski S, Voos W. Pink1 kinase and its membrane potential (Deltapsi)-dependent cleavage product both localize to outer mitochondrial membrane by unique targeting mode. J Biol Chem. 2012;287:22969–22987. doi:10.1074/jbc.M112.365700. PMID:22547060
   PubMed Web of Science ®Google Scholar
• Silvestri L, Caputo V, Bellacchio E, Atorino L, Dallapiccola B, Valente EM, Casari G. Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum Mol Genet. 2005;14:3477–3492. doi:10.1093/hmg/ddi377. PMID:16207731
   PubMed Web of Science ®Google Scholar
• 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;22:320–333. doi:10.1016/j.devcel.2011.12.014. PMID:22280891
   PubMed Web of Science ®Google Scholar
• Litchfield DW. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem J. 2003;369:1–15. doi:10.1042/bj20021469. PMID:12396231
   PubMed Web of Science ®Google Scholar
• Cheusova T, Khan MA, Schubert SW, Gavin AC, Buchou T, Jacob G, Sticht H, Allende J, Boldyreff B, Brenner HR, et al. Casein kinase 2-dependent serine phosphorylation of MuSK regulates acetylcholine receptor aggregation at the neuromuscular junction. Genes Dev. 2006;20:1800–1816. doi:10.1101/gad.375206. PMID:16818610
   PubMed Web of Science ®Google Scholar
• Herrmann D, Straubinger M, Hashemolhosseini S. Protein kinase CK2 interacts at the neuromuscular synapse with Rapsyn, Rac1, 14-3-3gamma, and Dok-7 proteins and phosphorylates the latter two. J Biol Chem. 2015;290:22370–22384. doi:10.1074/jbc.M115.647610. PMID:26198629
   PubMed Web of Science ®Google Scholar
• Escher P, Lacazette E, Courtet M, Blindenbacher A, Landmann L, Bezakova G, Lloyd KC, Mueller U, Brenner HR. Synapses form in skeletal muscles lacking neuregulin receptors. Science. 2005;308:1920–1923. doi:10.1126/science.1108258. PMID:15976301
   PubMed Web of Science ®Google Scholar
• Leu M, Bellmunt E, Schwander M, Farinas I, Brenner HR, Muller U. Erbb2 regulates neuromuscular synapse formation and is essential for muscle spindle development. Development. 2003;130:2291–2301. doi:10.1242/dev.00447. PMID:12702645
   PubMed Web of Science ®Google Scholar
• Meggio F, Pinna LA. One-thousand-and-one substrates of protein kinase CK2? Faseb J. 2003;17:349–368. doi:10.1096/fj.02-0473rev. PMID:12631575
   PubMed Web of Science ®Google Scholar
• Eiber N, Simeone L, Hashemolhosseini S. Ablation of protein kinase CK2beta in skeletal muscle fibers interferes with their oxidative capacity. Pharmaceuticals (Basel). 2017;10:13.
   Google Scholar
• Abe T, Kiyonari H, Shioi G, Inoue K, Nakao K, Aizawa S, Fujimori T. Establishment of conditional reporter mouse lines at ROSA26 locus for live cell imaging. Genesis. 2011;49:579–590. doi:10.1002/dvg.20753. PMID:21445964
   PubMed Web of Science ®Google Scholar
• Schapira AH. Mitochondrial disease. Lancet. 2006;368:70–82. doi:10.1016/S0140-6736(06)68970-8. PMID:16815381
   PubMed Web of Science ®Google Scholar
• Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y, Milan G, Masiero E, Piccolo PD, Foretz M, et al. Mitochondrial fission and remodelling contributes to muscle atrophy. Embo J. 2010;29:1774–1785. doi:10.1038/emboj.2010.60. PMID:20400940
   PubMed Web of Science ®Google Scholar
• Jin SM, Youle RJ. PINK1- and Parkin-mediated mitophagy at a glance. J Cell Sci. 2012;125:795–799. doi:10.1242/jcs.093849. PMID:22448035
   PubMed Web of Science ®Google Scholar
• Zhou C, Huang Y, Shao Y, May J, Prou D, Perier C, Dauer W, Schon EA, Przedborski S. The kinase domain of mitochondrial PINK1 faces the cytoplasm. Proc Natl Acad Sci U S A. 2008;105:12022–12027. doi:10.1073/pnas.0802814105. PMID:18687899
   PubMed Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000;19:5720–5728. doi:10.1093/emboj/19.21.5720. PMID:11060023
   PubMed Web of Science ®Google Scholar
• Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402:672–676. doi:10.1038/45257. PMID:10604474
   PubMed Web of Science ®Google Scholar
• Zhang J, Ney PA. Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 2009;16:939–946. doi:10.1038/cdd.2009.16. PMID:19229244
   PubMed Web of Science ®Google Scholar
• Geisler S, Holmstrom 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;12:119–131. doi:10.1038/ncb2012. PMID:20098416
   PubMed Web of Science ®Google Scholar
• 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;6:1090–1106. doi:10.4161/auto.6.8.13426. PMID:20890124
   PubMed Web of Science ®Google Scholar
• Katayama H, Kogure T, Mizushima N, Yoshimori T, Miyawaki A. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem Biol. 2011;18:1042–1052. doi:10.1016/j.chembiol.2011.05.013. PMID:21867919
   PubMed Web of Science ®Google Scholar
• Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132:27–42. doi:10.1016/j.cell.2007.12.018. PMID:18191218
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140:313–326. doi:10.1016/j.cell.2010.01.028. PMID:20144757
   PubMed Web of Science ®Google Scholar
• Irwin WA, Bergamin N, Sabatelli P, Reggiani C, Megighian A, Merlini L, Braghetta P, Columbaro M, Volpin D, Bressan GM, et al. Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat Genet. 2003;35:367–371. doi:10.1038/ng1270. PMID:14625552
   PubMed Web of Science ®Google Scholar
• Nicholls DG, Ward MW. Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts. Trends Neurosci. 2000;23:166–174. doi:10.1016/S0166-2236(99)01534-9. PMID:10717676
   PubMed Web of Science ®Google Scholar
• Gnad F, Forner F, Zielinska DF, Birney E, Gunawardena J, Mann M. Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria. Mol Cell Proteomics. 2010;9:2642–2653. doi:10.1074/mcp.M110.001594. PMID:20688971
   PubMed Web of Science ®Google Scholar
• Zhang XJ, Chen S, Huang KX, Le WD. Why should autophagic flux be assessed? Acta Pharmacol Sin. 2013;34:595–599. doi:10.1038/aps.2012.184. PMID:23474710
   PubMed Web of Science ®Google Scholar
• Miniou P, Tiziano D, Frugier T, Roblot N, Le Meur M, Melki J. Gene targeting restricted to mouse striated muscle lineage. Nucleic Acids Res. 1999;27:e27. doi:10.1093/nar/27.19.e27. PMID:10481039
   PubMed Web of Science ®Google Scholar
• Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, Bertaggia E, Blaauw B, Urciuolo A, Tiepolo T, Merlini L, et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med. 2010;16:1313–1320. doi:10.1038/nm.2247. PMID:21037586
   PubMed Web of Science ®Google Scholar
• Morais VA, Haddad D, Craessaerts K, De Bock PJ, Swerts J, Vilain S, Aerts L, Overbergh L, Grünewald A, Seibler P, et al. PINK1 loss-of-function mutations affect mitochondrial complex I activity via NdufA10 ubiquinone uncoupling. Science. 2014;344:203–207. doi:10.1126/science.1249161. PMID:24652937
   PubMed Web of Science ®Google Scholar
• Murakawa T, Yamaguchi O, Hashimoto A, Hikoso S, Takeda T, Oka T, Yasui H, Ueda H, Akazawa Y, Nakayama H, et al. Bcl-2-like protein 13 is a mammalian Atg32 homologue that mediates mitophagy and mitochondrial fragmentation. Nat Commun. 2015;6:7527. doi:10.1038/ncomms8527. PMID:26146385
   PubMed Web of Science ®Google Scholar
• Kanki T, Kurihara Y, Jin X, Goda T, Ono Y, Aihara M, Hirota Y, Saigusa T, Aoki Y, Uchiumi T, et al. Casein kinase 2 is essential for mitophagy. EMBO Rep. 2013. doi:10.1038/embor.2013.114. PMID:23897086
   PubMed Web of Science ®Google Scholar
• Chen G, Han Z, Feng D, Chen Y, Chen L, Wu H, Huang L, Zhou C, Cai X, Fu C, et al. A Regulatory Signaling Loop Comprising the PGAM5 Phosphatase and CK2 Controls Receptor-Mediated Mitophagy. Mol Cell. 2014;54:362–377. doi:10.1016/j.molcel.2014.02.034. PMID:24746696
   PubMed Web of Science ®Google Scholar
• Hashemolhosseini S, Moore C, Landmann L, Sander A, Schwarz H, Witzemann V, Sakmann B, Brenner HR. Electrical activity and postsynapse formation in adult muscle: gamma-AChRs are not required. Mol Cell Neurosci. 2000;16:697–707. doi:10.1006/mcne.2000.0911. PMID:11124891
   PubMed Web of Science ®Google Scholar
• Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell. 2010;141:280–289. doi:10.1016/j.cell.2010.02.026. PMID:20403324
   PubMed Web of Science ®Google Scholar
• Buchou T, Vernet M, Blond O, Jensen HH, Pointu H, Olsen BB, Cochet C, Issinger OG, Boldyreff B. Disruption of the regulatory beta subunit of protein kinase CK2 in mice leads to a cell-autonomous defect and early embryonic lethality. Mol Cell Biol. 2003;23:908–915. doi:10.1128/MCB.23.3.908-915.2003. PMID:12529396
   PubMed Web of Science ®Google Scholar
• Milan G, Romanello V, Pescatore F, Armani A, Paik JH, Frasson L, Seydel A, Zhao J, Abraham R, Goldberg AL, et al. Regulation of autophagy and the ubiquitin-proteasome system by the FoxO transcriptional network during muscle atrophy. Nat Commun. 2015;6:6670. doi:10.1038/ncomms7670. PMID:25858807
   PubMed Web of Science ®Google Scholar
• Rudolf R, Mongillo M, Magalhaes PJ, Pozzan T. In vivo monitoring of Ca(2+) uptake into mitochondria of mouse skeletal muscle during contraction. J Cell Biol. 2004;166:527–536. doi:10.1083/jcb.200403102. PMID:15314066
   PubMed Web of Science ®Google Scholar
• Frezza C, Cipolat S, Scorrano L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc. 2007;2:287–295. doi:10.1038/nprot.2006.478. PMID:17406588
   PubMed Web of Science ®Google Scholar
• Wittig I, Braun HP, Schagger H. Blue native PAGE. Nat Protoc. 2006;1:418–428. doi:10.1038/nprot.2006.62. PMID:17406264
   PubMed Web of Science ®Google Scholar
• Messina A, Reina S, Guarino F, De Pinto V. VDAC isoforms in mammals. Biochim Biophys Acta. 2012;1818:1466–1476. doi:10.1016/j.bbamem.2011.10.005. PMID:22020053
   PubMed Web of Science ®Google Scholar
• Stojanovski D, Pfanner N, Wiedemann N. Import of proteins into mitochondria. Methods Cell Biol. 2007;80:783–806. doi:10.1016/S0091-679X(06)80036-1. PMID:17445722
   PubMed Web of Science ®Google Scholar
• Buttgereit A, Weber C, Garbe CS, Friedrich O. From chaos to split-ups–SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle. J Pathol. 2013;229:477–485. doi:10.1002/path.4136. PMID:23132094
   PubMed Web of Science ®Google Scholar
• Guth SI, Schmidt K, Hess A, Wegner M. Adult-onset degeneration of adipose tissue in mice deficient for the Sox8 transcription factor. J Lipid Res. 2009;50:1269–1280. doi:10.1194/jlr.M800531-JLR200. PMID:19286648
   PubMed Web of Science ®Google Scholar
• Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007;6:458–471. doi:10.1016/j.cmet.2007.11.001. PMID:18054315
   PubMed Web of Science ®Google Scholar
• Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007;6:472–483. doi:10.1016/j.cmet.2007.11.004. PMID:18054316
   PubMed Web of Science ®Google Scholar
• Liley AW. An investigation of spontaneous activity at the neuromuscular junction of the rat. J Physiol. 1956;132:650–666. doi:10.1113/jphysiol.1956.sp005555. PMID:13332600
   PubMed Web of Science ®Google Scholar
• Plomp JJ, van Kempen GT, Molenaar PC. Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in alpha-bungarotoxin-treated rats. J Physiol. 1992;458:487–499. doi:10.1113/jphysiol.1992.sp019429. PMID:1302275
   PubMed Web of Science ®Google Scholar
• Rogozhin AA, Pang KK, Bukharaeva E, Young C, Slater CR. Recovery of mouse neuromuscular junctions from single and repeated injections of botulinum neurotoxin A. J Physiol. 2008;586:3163–3182. doi:10.1113/jphysiol.2008.153569. PMID:18467364
   PubMed Web of Science ®Google Scholar