A monolayer hiPSC culture system for autophagy/mitophagy studies in human dopaminergic neurons

References

• The prevalence and incidence of Parkinson’s in the UK. Accessed 14 March 2020. Available from: https://www.parkinsons.org.uk/sites/default/files/2018-01/CS2960%20Incidence%20and%20prevalence%20report%20branding%20summary%20report.pdf.
   Google Scholar
• Teismann P, Schulz JB. Cellular pathology of Parkinson’s disease: astrocytes, microglia and inflammation. Cell Tissue Res. 2004 Oct;318(1):149–161.
   PubMed Web of Science ®Google Scholar
• Hirsch E, Graybiel AM, Agid YA. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson’s disease. Nature. 1988 Jul 28;334(6180):345–348.
   PubMed Web of Science ®Google Scholar
• Bohnen NI, Albin RL. The cholinergic system and Parkinson disease. Behav Brain Res. 2011 Aug 10;221(2):564–573.
   PubMed Web of Science ®Google Scholar
• Chinta SJ, Andersen JK. Dopaminergic neurons. Int J Biochem Cell Biol. 2005 May;37(5):942–946.
   PubMed Web of Science ®Google Scholar
• Hirsch EC, Jenner P, Przedborski S. Pathogenesis of Parkinson’s disease. Mov Disord. 2013 Jan;28(1):24–30..
   PubMed Web of Science ®Google Scholar
• Lesage S, Brice A. Parkinson’s disease: from monogenic forms to genetic susceptibility factors. Hum Mol Genet. 2009 Apr 15;18(R1):R48–59.
   PubMed Web of Science ®Google Scholar
• Chang D, Nalls MA, Hallgrimsdottir IB, et al. A meta-analysis of genome-wide association studies identifies 17 new Parkinson’s disease risk loci. Nat Genet. 2017 Oct;49(10):1511–1516.
   PubMed Web of Science ®Google Scholar
• Kalinderi K, Bostantjopoulou S, Fidani L. The genetic background of Parkinson’s disease: current progress and future prospects. Acta Neurol Scand. 2016 Nov;134(5):314–326.
   PubMed Web of Science ®Google Scholar
• Shults CW. Lewy bodies. Proc Natl Acad Sci U S A. 2006 Feb 07;103(6):1661–1668.
   PubMed Web of Science ®Google Scholar
• Karabiyik C, Lee MJ, Rubinsztein DC. Autophagy impairment in Parkinson’s disease. Essays Biochem. 2017 Dec 12;61(6):711–720.
   PubMed Web of Science ®Google Scholar
• Surmeier DJ, Obeso JA, Halliday GM. Selective neuronal vulnerability in Parkinson disease. Nat Rev Neurosci. 2017 Jan 20;18(2):101–113.
   PubMed Web of Science ®Google Scholar
• Pacelli C, Giguere N, Bourque MJ, et al. Elevated mitochondrial bioenergetics and axonal arborization size are key contributors to the vulnerability of dopamine neurons. Curr Biol. 2015 Sep 21;25(18):2349–2360.
   PubMed Web of Science ®Google Scholar
• Chan CS, Gertler TS, Surmeier DJ. Calcium homeostasis, selective vulnerability and Parkinson’s disease. Trends Neurosci. 2009 May;32(5):249–256.
   PubMed Web of Science ®Google Scholar
• Surmeier DJ, Schumacker PT. Calcium, bioenergetics, and neuronal vulnerability in Parkinson’s disease. J Biol Chem. 2013 Apr 12;288(15):10736–10741.
   PubMed Web of Science ®Google Scholar
• Foehring RC, Zhang XF, Lee JC, et al. Endogenous calcium buffering capacity of substantia nigral dopamine neurons. J Neurophysiol. 2009 Oct;102(4):2326–2333.
   PubMed Web of Science ®Google Scholar
• Guzman JN, Sanchez-Padilla J, Chan CS, et al. Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci. 2009 Sep 2;29(35):11011–11019.
   PubMed Web of Science ®Google Scholar
• Philippart F, Destreel G, Merino-Sepulveda P, et al. Differential somatic Ca2+ channel profile in midbrain dopaminergic neurons. J Neurosci. 2016 Jul 6;36(27):7234–7245.
   PubMed Web of Science ®Google Scholar
• Federico A, Cardaioli E, Da Pozzo P, et al. Mitochondria, oxidative stress and neurodegeneration. J Neurol Sci. 2012 Nov 15;322(1–2):254–262.
   PubMed Web of Science ®Google Scholar
• Williams ET, Chen X, Moore DJ. VPS35, the retromer complex and parkinson’s disease. J Parkinsons Dis. 2017;7(2):219–233.
   PubMedGoogle Scholar
• Tang FL, Erion JR, Tian Y, et al. VPS35 in dopamine neurons is required for endosome-to-Golgi retrieval of Lamp2a, a receptor of chaperone-mediated autophagy that is critical for alpha-synuclein degradation and prevention of pathogenesis of Parkinson’s disease. J Neurosci. 2015 Jul 22;35(29):10613–10628.
   PubMed Web of Science ®Google Scholar
• Zavodszky E, Seaman MN, Moreau K, et al. Mutation in VPS35 associated with Parkinson’s disease impairs WASH complex association and inhibits autophagy. Nat Commun. 2014 May 13;5:3828.
   PubMed Web of Science ®Google Scholar
• Wang W, Wang X, Fujioka H, et al. Parkinson’s disease-associated mutant VPS35 causes mitochondrial dysfunction by recycling DLP1 complexes. Nat Med. 2016 Jan;22(1):54–63.
   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 Biol. 2008 Dec 01;183(5):795–803.
   PubMed Web of Science ®Google Scholar
• Clark IE, Dodson MW, Jiang C, et al. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature. 2006 Jun 29;441(7097):1162–1166.
   PubMed Web of Science ®Google Scholar
• Kane LA, Lazarou M, Fogel AI, et al. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol. 2014 Apr 28;205(2):143–153.
   PubMed Web of Science ®Google Scholar
• Kazlauskaite A, Kondapalli C, Gourlay R, et al. Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J. 2014 May 15;460(1):127–139.
   PubMed Web of Science ®Google Scholar
• Koyano F, Okatsu K, Kosako H, et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature. 2014 Jun 5;510(7503):162–166.
   PubMed Web of Science ®Google Scholar
• Lazarou M, Sliter DA, Kane LA, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015 Aug 20;524(7565):309–314.
   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 Web of Science ®Google Scholar
• Lee JJ, Sanchez-Martinez A, Zarate AM, et al. Basal mitophagy is widespread in Drosophila but minimally affected by loss of Pink1 or parkin. J Cell Biol. 2018 May 7;217(5):1613–1622.
   PubMed Web of Science ®Google Scholar
• Arenas E, Denham M, Villaescusa JC. How to make a midbrain dopaminergic neuron. Development. 2015 Jun 1;142(11):1918–1936.
   PubMed Web of Science ®Google Scholar
• Ardhanareeswaran K, Mariani J, Coppola G, et al. Human induced pluripotent stem cells for modelling neurodevelopmental disorders. Nat Rev Neurol. 2017 May;13(5):265–278.
   PubMed Web of Science ®Google Scholar
• Hamazaki T, El Rouby N, Fredette NC, et al. Concise review: induced pluripotent stem cell research in the era of precision medicine. Stem Cells. 2017 Mar;35(3):545–550.
   PubMed Web of Science ®Google Scholar
• Li M, Izpisua Belmonte JC. Looking to the future following 10 years of induced pluripotent stem cell technologies. Nat Protoc. 2016 Sep;11(9):1579–1585.
   PubMed Web of Science ®Google Scholar
• Shi Y, Inoue H, Wu JC, et al. Induced pluripotent stem cell technology: a decade of progress. Nat Rev Drug Discov. 2017 Feb;16(2):115–130.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006 Aug 25;126(4):663–676.
   PubMed Web of Science ®Google Scholar
• Ali F, Stott SR, Barker RA. Stem cells and the treatment of Parkinson’s disease. Exp Neurol. 2014 Oct;260:3–11.
   PubMed Web of Science ®Google Scholar
• Jimenez-Moreno N, Stathakos P, Caldwell MA, et al. Induced pluripotent stem cell neuronal models for the study of autophagy pathways in human neurodegenerative disease. Cells. 2017 Aug 11;6(3):24.
   Web of Science ®Google Scholar
• Crompton LA, Byrne ML, Taylor H, et al. Stepwise, non-adherent differentiation of human pluripotent stem cells to generate basal forebrain cholinergic neurons via hedgehog signaling. Stem Cell Res. 2013;Nov;11(3):1206–1221.
   PubMed Web of Science ®Google Scholar
• Gregg C, Weiss S. Generation of functional radial glial cells by embryonic and adult forebrain neural stem cells. J Neurosci. 2003 Dec 17;23(37):11587–11601.
   PubMed Web of Science ®Google Scholar
• Kuhn HG, Winkler J, Kempermann G, et al. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci. 1997 Aug 1;17(15):5820–5829.
   PubMed Web of Science ®Google Scholar
• Yan J, Studer L, McKay RD. Ascorbic acid increases the yield of dopaminergic neurons derived from basic fibroblast growth factor expanded mesencephalic precursors. J Neurochem. 2001 Jan;76(1):307–311.
   PubMed Web of Science ®Google Scholar
• Hyman C, Hofer M, Barde YA, et al. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature. 1991 Mar 21;350(6315):230–232.
   PubMed Web of Science ®Google Scholar
• Massa SM, Yang T, Xie Y, et al. Small molecule BDNF mimetics activate TrkB signaling and prevent neuronal degeneration in rodents. J Clin Invest. 2010 May;120(5):1774–1785.
   PubMed Web of Science ®Google Scholar
• Lin LF, Doherty DH, Lile JD, et al. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science. 1993 May 21;260(5111):1130–1132.
   PubMed Web of Science ®Google Scholar
• Chen X, Xu L, Radcliffe P, et al. Activation of tyrosine hydroxylase mRNA translation by cAMP in midbrain dopaminergic neurons. Mol Pharmacol. 2008 Jun;73(6):1816–1828.
   PubMed Web of Science ®Google Scholar
• Mourlevat S, Troadec JD, Ruberg M, et al. Prevention of dopaminergic neuronal death by cyclic AMP in mixed neuronal/glial mesencephalic cultures requires the repression of presumptive astrocytes. Mol Pharmacol. 2003 Sep;64(3):578–586.
   PubMed Web of Science ®Google Scholar
• Troadec JD, Marien M, Mourlevat S, et al. Activation of the mitogen-activated protein kinase (ERK(1/2)) signaling pathway by cyclic AMP potentiates the neuroprotective effect of the neurotransmitter noradrenaline on dopaminergic neurons. Mol Pharmacol. 2002 Nov;62(5):1043–1052.
   PubMed Web of Science ®Google Scholar
• Crawford TQ, Roelink H. The notch response inhibitor DAPT enhances neuronal differentiation in embryonic stem cell-derived embryoid bodies independently of sonic hedgehog signaling. Dev Dyn. 2007 Mar;236(3):886–892.
   PubMed Web of Science ®Google Scholar
• Poulsen KT, Armanini MP, Klein RD, et al. TGF beta 2 and TGF beta 3 are potent survival factors for midbrain dopaminergic neurons. Neuron. 1994 Nov;13(5):1245–1252.
   PubMed Web of Science ®Google Scholar
• Jaeger I, Arber C, Risner-Janiczek JR, et al. Temporally controlled modulation of FGF/ERK signaling directs midbrain dopaminergic neural progenitor fate in mouse and human pluripotent stem cells. Development. 2011 Oct;138(20):4363–4374.
   PubMed Web of Science ®Google Scholar
• Kirkeby A, Grealish S, Wolf DA, et al. Generation of regionally specified neural progenitors and functional neurons from human embryonic stem cells under defined conditions. Cell Rep. 2012 Jun 28;1(6):703–714.
   PubMed Web of Science ®Google Scholar
• Nistor PA, May PW, Tamagnini F, et al. Long-term culture of pluripotent stem-cell-derived human neurons on diamond–A substrate for neurodegeneration research and therapy. Biomaterials. 2015 Aug;61:139–149.
   PubMed Web of Science ®Google Scholar
• Shi Y, Kirwan P, Livesey FJ. Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat Protoc. 2012 Oct;7(10):1836–1846.
   PubMed Web of Science ®Google Scholar
• Grealish S, Diguet E, Kirkeby A, et al. Human ESC-derived dopamine neurons show similar preclinical efficacy and potency to fetal neurons when grafted in a rat model of Parkinson’s disease. Cell Stem Cell. 2014 Nov 06;15(5):653–665.
   PubMed Web of Science ®Google Scholar
• Briscoe J, Small S. Morphogen rules: design principles of gradient-mediated embryo patterning. Development. 2015 Dec 1;142(23):3996–4009.
   PubMed Web of Science ®Google Scholar
• Doi D, Samata B, Katsukawa M, et al. Isolation of human induced pluripotent stem cell-derived dopaminergic progenitors by cell sorting for successful transplantation. Stem Cell Reports. 2014 Mar 11;2(3):337–350.
   PubMed Web of Science ®Google Scholar
• Sanchez-Danes A, Richaud-Patin Y, Carballo-Carbajal I, et al. Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson’s disease. EMBO Mol Med. 2012 May;4(5):380–395.
   PubMed Web of Science ®Google Scholar
• Chung S, Leung A, Han BS, et al. Wnt1-lmx1a forms a novel autoregulatory loop and controls midbrain dopaminergic differentiation synergistically with the SHH-FoxA2 pathway. Cell Stem Cell. 2009 Dec 4;5(6):646–658.
   PubMed Web of Science ®Google Scholar
• Kadkhodaei B, Ito T, Joodmardi E, et al. Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J Neurosci. 2009 Dec 16;29(50):15923–15932.
   PubMed Web of Science ®Google Scholar
• Guo S, Liang Y, Murphy SF, et al. A rapid and high content assay that measures cyto-ID-stained autophagic compartments and estimates autophagy flux with potential clinical applications. Autophagy. 2015;11(3):560–572.
   PubMed Web of Science ®Google Scholar
• He M, Ding Y, Chu C, et al. Autophagy induction stabilizes microtubules and promotes axon regeneration after spinal cord injury. Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):11324–11329.
   PubMed Web of Science ®Google Scholar
• Pendergrass W, Wolf N, Poot M. Efficacy of MitoTracker Green and CMXrosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry A. 2004 Oct;61(2):162–169.
   PubMed Web of Science ®Google Scholar
• Jungverdorben J, Till A, Brustle O. Induced pluripotent stem cell-based modeling of neurodegenerative diseases: a focus on autophagy. J Mol Med (Berl). 2017 Jul;95(7):705–718.
   PubMed Web of Science ®Google Scholar
• Poon A, Zhang Y, Chandrasekaran A, et al. Modeling neurodegenerative diseases with patient-derived induced pluripotent cells: possibilities and challenges. N Biotechnol. 2017 Oct 25;39(Pt B):190–198.
   PubMedGoogle Scholar
• Weykopf B, Haupt S, Jungverdorben J, et al. Induced pluripotent stem cell-based modeling of mutant LRRK2-associated Parkinson’s Disease. Eur J Neurosci. 2019 Jan;49:561–589.
   PubMed Web of Science ®Google Scholar
• Orenstein SJ, Kuo SH, Tasset I, et al. Interplay of LRRK2 with chaperone-mediated autophagy. Nat Neurosci. 2013 Apr;16(4):394–406.
   PubMed Web of Science ®Google Scholar
• Chambers SM, Fasano CA, Papapetrou EP, et al. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol. 2009 Mar;27(3):275–280.
   PubMed Web of Science ®Google Scholar
• Kriks S, Shim JW, Piao J, et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease. Nature. 2011 Nov 06;480(7378):547–551.
   PubMed Web of Science ®Google Scholar
• Fernandes HJ, Hartfield EM, Christian HC, et al. ER stress and autophagic perturbations lead to elevated extracellular alpha-synuclein in GBA-N370S Parkinson’s iPSC-derived dopamine neurons. Stem Cell Reports. 2016 Mar 08;6(3):342–356.
   PubMed Web of Science ®Google Scholar
• Seibler P, Graziotto J, Jeong H, et al. Mitochondrial Parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells. J Neurosci. 2011 Apr 20;31(16):5970–5976.
   PubMed Web of Science ®Google Scholar
• Chung SY, Kishinevsky S, Mazzulli JR, et al. Parkin and PINK1 patient iPSC-derived midbrain dopamine neurons exhibit mitochondrial dysfunction and alpha-synuclein accumulation. Stem Cell Reports. 2016 Oct 11;7(4):664–677.
   PubMed Web of Science ®Google Scholar
• Suzuki S, Akamatsu W, Kisa F, et al. Efficient induction of dopaminergic neuron differentiation from induced pluripotent stem cells reveals impaired mitophagy in PARK2 neurons. Biochem Biophys Res Commun. 2017 Jan 29;483(1):88–93.
   PubMed Web of Science ®Google Scholar
• Burbulla LF, Song P, Mazzulli JR, et al. Dopamine oxidation mediates mitochondrial and lysosomal dysfunction in Parkinson’s disease. Science. 2017 Sep 22;357(6357):1255–1261.
   PubMed Web of Science ®Google Scholar
• Hsieh CH, Shaltouki A, Gonzalez AE, et al. Functional impairment in miro degradation and mitophagy is a shared feature in familial and sporadic parkinson’s disease. Cell Stem Cell. 2016 Dec 01;19(6):709–724.
   PubMed Web of Science ®Google Scholar
• Devine MJ, Ryten M, Vodicka P, et al. Parkinson’s disease induced pluripotent stem cells with triplication of the alpha-synuclein locus. Nat Commun. 2011 Aug;23(2):440.
   Web of Science ®Google Scholar
• Aflatoonian B, Ruban L, Shamsuddin S, et al. Generation of Sheffield (Shef) human embryonic stem cell lines using a microdrop culture system. In Vitro Cell Dev Biol Anim. 2010 Apr;46(3–4):236–241.
   PubMed Web of Science ®Google Scholar
• Ross PJ, Suhr ST, Rodriguez RM, et al. Human-induced pluripotent stem cells produced under xeno-free conditions. Stem Cells Dev. 2010 Aug;19(8):1221–1229.
   PubMed Web of Science ®Google Scholar
• Stathakos P, Jimenez-Moreno N, Crompton L, et al. Imaging autophagy in hipsc-derived midbrain dopaminergic neuronal cultures for Parkinson’s disease research. Methods Mol Biol. 2019;1880:257–280.
   PubMedGoogle Scholar
• Betin VM, Singleton BK, Parsons SF, et al. Autophagy facilitates organelle clearance during differentiation of human erythroblasts: evidence for a role for ATG4 paralogs during autophagosome maturation. Autophagy. 2013 Jun 01;9(6):881–893.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001 Dec;25(4):402–408.
   PubMed Web of Science ®Google Scholar