Development and Dynamic Regulation of Mitochondrial Network in Human Midbrain Dopaminergic Neurons Differentiated from iPSCs

Stem Cell Reports

Volumn 7, Issue 4, 2016, Pages 678-692

  Fang, Du ^a   Qing, Yu ^a,b   Yan, Shijun ^a   Chen, Doris ^a   Yan, Shirley ShiDu ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE; BIOLOGICAL MARKER; DOPAMINE TRANSPORTER; ENGRAILED 1 PROTEIN; HEPATOCYTE NUCLEAR FACTOR 3BETA; LIM HOMEOBOX TRANSCRIPTION FACTOR 1 ALPHA; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; OCTAMER TRANSCRIPTION FACTOR 4; PEPTIDES AND PROTEINS; POTASSIUM CYANIDE; ROTENONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR PAX6; TUJ1 PROTEIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER 2;

ARTICLE; CELL FUNCTION; CELL MATURATION; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOPAMINERGIC NERVE CELL; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPTOGENESIS; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; ELECTROPHYSIOLOGY; MESENCEPHALON; METABOLISM; MITOCHONDRION; PHENOTYPE; SYNAPSE;

BIOMARKERS; CELL DIFFERENTIATION; CELL MOVEMENT; DOPAMINERGIC NEURONS; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESENCEPHALON; MITOCHONDRIA; PHENOTYPE; SYNAPSES;

EID: 84992184182     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2016.08.014     Document Type: Article

References (39)

1. Andersson, E., Tryggvason, U., Deng, Q., Friling, S., Alekseenko, Z., Robert, B., Perlmann, T., Ericson, J., Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124 (2006), 393–405.
2. Ang, S.L., Transcriptional control of midbrain dopaminergic neuron development. Development 133 (2006), 3499–3506.
3. Armstrong, L., Tilgner, K., Saretzki, G., Atkinson, S.P., Stojkovic, M., Moreno, R., Przyborski, S., Lako, M., Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells. Stem Cells 28 (2010), 661–673.
4. Asensi, K.D., Fortunato, R.S., dos Santos, D.S., Pacheco, T.S., de Rezende, D.F., Rodrigues, D.C., Mesquita, F.C., Kasai-Brunswick, T.H., de Carvalho, A.C., Carvalho, D.P., et al. Reprogramming to a pluripotent state modifies mesenchymal stem cell resistance to oxidative stress. J. Cell Mol. Med. 18 (2014), 824–831.
5. Beers, J., Gulbranson, D.R., George, N., Siniscalchi, L.I., Jones, J., Thomson, J.A., Chen, G., Passaging and colony expansion of human pluripotent stem cells by enzyme-free dissociation in chemically defined culture conditions. Nat. Protoc. 7 (2012), 2029–2040.
6. Birsa, N., Norkett, R., Higgs, N., Lopez-Domenech, G., Kittler, J.T., Mitochondrial trafficking in neurons and the role of the Miro family of GTPase proteins. Biochem. Soc. Trans. 41 (2013), 1525–1531.
7. Bjorklund, L.M., Sanchez-Pernaute, R., Chung, S., Andersson, T., Chen, I.Y., McNaught, K.S., Brownell, A.L., Jenkins, B.G., Wahlestedt, C., Kim, K.S., et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. USA 99 (2002), 2344–2349.
8. Bukowiecki, R., Adjaye, J., Prigione, A., Mitochondrial function in pluripotent stem cells and cellular reprogramming. Gerontology 60 (2014), 174–182.
9. Chandel, N.S., Maltepe, E., Goldwasser, E., Mathieu, C.E., Simon, M.C., Schumacker, P.T., Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 95 (1998), 11715–11720.
10. Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E., Chan, D.C., Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160 (2003), 189–200.
11. Cho, Y.M., Kwon, S., Pak, Y.K., Seol, H.W., Choi, Y.M., Park do, J., Park, K.S., Lee, H.K., Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem. Biophys. Res. Commun. 348 (2006), 1472–1478.
12. Colon-Ramos, D.A., Synapse formation in developing neural circuits. Curr. Top. Dev. Biol. 87 (2009), 53–79.
13. Cooper, O., Seo, H., Andrabi, S., Guardia-Laguarta, C., Graziotto, J., Sundberg, M., McLean, J.R., Carrillo-Reid, L., Xie, Z., Osborn, T., et al. Pharmacological rescue of mitochondrial deficits in iPSC-derived neural cells from patients with familial Parkinson's disease. Sci. Transl. Med., 4, 2012, 141ra190.
14. Genova, M.L., Pich, M.M., Bernacchia, A., Bianchi, C., Biondi, A., Bovina, C., Falasca, A.I., Formiggini, G., Castelli, G.P., Lenaz, G., The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann. N. Y. Acad. Sci. 1011 (2004), 86–100.
15. Hartfield, E.M., Yamasaki-Mann, M., Ribeiro Fernandes, H.J., Vowles, J., James, W.S., Cowley, S.A., Wade-Martins, R., Physiological characterisation of human iPS-derived dopaminergic neurons. PLoS One, 9, 2014, e87388.
16. Kim, J., Su, S.C., Wang, H., Cheng, A.W., Cassady, J.P., Lodato, M.A., Lengner, C.J., Chung, C.Y., Dawlaty, M.M., Tsai, L.H., et al. Functional integration of dopaminergic neurons directly converted from mouse fibroblasts. Cell Stem Cell 9 (2011), 413–419.
17. Martinez, C., Cornejo, V.H., Lois, P., Ellis, T., Solis, N.P., Wainwright, B.J., Palma, V., Proliferation of murine midbrain neural stem cells depends upon an endogenous sonic hedgehog (Shh) source. PLoS One, 8, 2013, e65818.
18. Mattson, M.P., Gleichmann, M., Cheng, A., Mitochondria in neuroplasticity and neurological disorders. Neuron 60 (2008), 748–766.
19. Millet, S., Bloch-Gallego, E., Simeone, A., Alvarado-Mallart, R.M., The caudal limit of Otx2 gene expression as a marker of the midbrain/hindbrain boundary: a study using in situ hybridisation and chick/quail homotopic grafts. Development 122 (1996), 3785–3797.
20. Nakatani, T., Kumai, M., Mizuhara, E., Minaki, Y., Ono, Y., Lmx1a and Lmx1b cooperate with Foxa2 to coordinate the specification of dopaminergic neurons and control of floor plate cell differentiation in the developing mesencephalon. Dev. Biol. 339 (2010), 101–113.
21. O'Brien, L.C., Keeney, P.M., Bennett, J.P. Jr., Differentiation of human neural stem cells into motor neurons stimulates mitochondrial biogenesis and decreases glycolytic flux. Stem Cells Dev. 24 (2015), 1984–1994.
22. Perier, C., Vila, M., Mitochondrial biology and Parkinson's disease. Cold Spring Harbor Perspect. Med., 2, 2012, a009332.
23. Prigione, A., Lichtner, B., Kuhl, H., Struys, E.A., Wamelink, M., Lehrach, H., Ralser, M., Timmermann, B., Adjaye, J., Human induced pluripotent stem cells harbor homoplasmic and heteroplasmic mitochondrial DNA mutations while maintaining human embryonic stem cell-like metabolic reprogramming. Stem Cells 29 (2011), 1338–1348.
24. Sena, L.A., Chandel, N.S., Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48 (2012), 158–167.
25. Simon, H.H., Saueressig, H., Wurst, W., Goulding, M.D., O'Leary, D.D., Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J. Neurosci. 21 (2001), 3126–3134.
26. St John, J.C., Ramalho-Santos, J., Gray, H.L., Petrosko, P., Rawe, V.Y., Navara, C.S., Simerly, C.R., Schatten, G.P., The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 7 (2005), 141–153.
27. Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006), 663–676.
28. Tapia, P.C., Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients: “Mitohormesis” for health and vitality. Med. Hypotheses 66 (2006), 832–843.
29. Teslaa, T., Teitell, M.A., Pluripotent stem cell energy metabolism: an update. EMBO J. 34 (2015), 138–153.
30. Varum, S., Momcilovic, O., Castro, C., Ben-Yehudah, A., Ramalho-Santos, J., Navara, C.S., Enhancement of human embryonic stem cell pluripotency through inhibition of the mitochondrial respiratory chain. Stem Cell Res. 3 (2009), 142–156.
31. Varum, S., Rodrigues, A.S., Moura, M.B., Momcilovic, O., Easley, C.A.t., Ramalho-Santos, J., Van Houten, B., Schatten, G., Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One, 6, 2011, e20914.
32. Vazquez-Martin, A., Cufi, S., Corominas-Faja, B., Oliveras-Ferraros, C., Vellon, L., Menendez, J.A., Mitochondrial fusion by pharmacological manipulation impedes somatic cell reprogramming to pluripotency: new insight into the role of mitophagy in cell stemness. Aging 4 (2012), 393–401.
33. Wang, L., Ye, X., Zhao, Q., Zhou, Z., Dan, J., Zhu, Y., Chen, Q., Liu, L., Drp1 is dispensable for mitochondria biogenesis in induction to pluripotency but required for differentiation of embryonic stem cells. Stem Cells Dev. 23 (2014), 2422–2434.
34. Wu, Y., Zhang, X., Kang, X., Li, N., Wang, R., Hu, T., Xiang, M., Wang, X., Yuan, W., Chen, A., et al. Oxidative stress inhibits adhesion and transendothelial migration, and induces apoptosis and senescence of induced pluripotent stem cells. Clin. Exp. Pharmacol. Physiol. 40 (2013), 626–634.
35. Xu, X., Duan, S., Yi, F., Ocampo, A., Liu, G.H., Izpisua Belmonte, J.C., Mitochondrial regulation in pluripotent stem cells. Cell Metab. 18 (2013), 325–332.
36. Xu, X.L., Yi, F., Pan, H.Z., Duan, S.L., Ding, Z.C., Yuan, G.H., Qu, J., Zhang, H.C., Liu, G.H., Progress and prospects in stem cell therapy. Acta Pharmacol. Sin. 34 (2013), 741–746.
37. Yamaoka, S., Nakajima, M., Fujimoto, M., Tsutsumi, N., MIRO1 influences the morphology and intracellular distribution of mitochondria during embryonic cell division in Arabidopsis. Plant Cell Rep. 30 (2011), 239–244.
38. Yang, D., Zhang, Z.J., Oldenburg, M., Ayala, M., Zhang, S.C., Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells 26 (2008), 55–63.
39. Yoon, Y., Krueger, E.W., Oswald, B.J., McNiven, M.A., The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell Biol. 23 (2003), 5409–5420.