Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 3064016, 15 pages
https://doi.org/10.1155/2017/3064016
Research Article

Increased Mitochondrial Mass and Cytosolic Redox Imbalance in Hippocampal Astrocytes of a Mouse Model of Rett Syndrome: Subcellular Changes Revealed by Ratiometric Imaging of JC-1 and roGFP1 Fluorescence

1Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB), Georg-August-Universität Göttingen, Universitätsmedizin Göttingen, Göttingen, Germany
2Zentrum Physiologie und Pathophysiologie, Institut für Neuro- und Sinnesphysiologie, Humboldtallee, 23 Göttingen, Germany

Correspondence should be addressed to Michael Müller; ed.gdwg@7elleumm

Received 15 March 2017; Revised 16 June 2017; Accepted 27 June 2017; Published 13 August 2017

Academic Editor: Icksoo Lee

Copyright © 2017 Dörthe F. Bebensee et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Rett, “Über ein eigenartiges hirnatrophisches Syndrom bei Hyperammonämie im Kindesalter,” Wiener Medizinische Wochenschrift (1946), vol. 116, pp. 723–726, 1966. View at Google Scholar
  2. B. Hagberg, J. Aicardi, K. Dias, and O. Ramos, “A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett’s syndrome: report of 35 cases,” Annals of Neurology, vol. 14, pp. 471–479, 1983. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Chahrour and H. Y. Zoghbi, “The story of Rett syndrome: from clinic to neurobiology,” Neuron, vol. 56, pp. 422–437, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Hagberg, “Rett’s syndrome: prevalence and impact on progressive severe mental retardation in girls,” Acta Paediatrica Scandinavica, vol. 74, pp. 405–408, 1985. View at Google Scholar
  5. L. Villard, “MECP2 mutations in males,” Journal of Medical Genetics, vol. 44, pp. 417–423, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. R. E. Amir, I. B. Veyver, M. Wan, C. Q. Tran, U. Francke, and H. Y. Zoghbi, “Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2,” Nature Genetics, vol. 23, pp. 185–188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. X. Nan, S. Cross, and A. Bird, “Gene silencing by methyl-CpG-binding proteins,” Novartis Foundation Symposium, vol. 214, pp. 6–16, 1998, discussion 16-21, 46-50. View at Google Scholar
  8. M. Chahrour, S. Y. Jung, C. Shaw et al., “MeCP2, a key contributor to neurological disease, activates and represses transcription,” Science, vol. 320, pp. 1224–1229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Trappe, F. Laccone, J. Cobilanschi et al., “MECP2 mutations in sporadic cases of Rett syndrome are almost exclusively of paternal origin,” American Journal of Human Genetics, vol. 68, pp. 1093–1101, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Dragich, I. Houwink-Manville, and C. Schanen, “Rett syndrome: a surprising result of mutation in MECP2,” Human Molecular Genetics, vol. 9, pp. 2365–2375, 2000. View at Google Scholar
  11. B. Hagberg and I. Witt-Engerström, “Rett syndrome: a suggested staging system for describing impairment profile with increasing age towards adolescence,” American Journal of Medical Genetics Supplement, vol. 1, pp. 47–59, 1986. View at Google Scholar
  12. B. Hagberg, M. Berg, and U. Steffenburg, “Three decades of sociomedical experiences from West Swedish Rett females 4-60 years of age,” Brain dev, vol. 23, Supplement 1, pp. S28–S31, 2001. View at Google Scholar
  13. A. M. Kerr, D. D. Armstrong, R. J. Prescott, D. Doyle, and D. L. Kearney, “Rett syndrome: analysis of deaths in the British survey,” European Child & Adolescent Psychiatry, vol. 6, Supplement 1, pp. 71–74, 1997. View at Google Scholar
  14. C. A. Chapleau, J. Lane, L. Pozzo-Miller, and A. K. Percy, “Evaluation of current pharmacological treatment options in the management of Rett syndrome: from the present to future therapeutic alternatives,” Current Clinical Pharmacology, vol. 8, pp. 358–369, 2013. View at Google Scholar
  15. D. M. Katz, A. Bird, M. Coenraads et al., “Rett syndrome: crossing the threshold to clinical translation,” Trends in Neurosciences, vol. 39, pp. 100–113, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Lotan and S. Hanks, “Physical therapy intervention for individuals with Rett syndrome,” TheScientificWorldJOURNAL, vol. 6, pp. 1314–1338, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. S. B. Hanks, “The role of therapy in Rett syndrome,” American Journal of Medical Genetics Supplement, vol. 1, pp. 247–252, 1986. View at Google Scholar
  18. M. Müller and K. Can, “Aberrant redox homoeostasis and mitochondrial dysfunction in Rett syndrome,” Biochemical Society Transactions, vol. 42, pp. 959–964, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Shulyakova, A. C. Andreazza, L. R. Mills, and J. H. Eubanks, “Mitochondrial dysfunction in the pathogenesis of Rett syndrome: implications for mitochondria-targeted therapies,” Frontiers in Cellular Neuroscience, vol. 11, p. 58, 2017. View at Publisher · View at Google Scholar
  20. O. Eeg-Olofsson, A. G. al-Zuhair, A. S. Teebi et al., “Rett syndrome: a mitochondrial disease?” Journal of Child Neurology, vol. 5, pp. 210–214, 1990. View at Publisher · View at Google Scholar · View at Scopus
  21. O. Eeg-Olofsson, A. G. Al-Zuhair, A. S. Teebi, and M. M. Al-Essa, “Abnormal mitochondria in the Rett syndrome,” Brain and Development, vol. 10, pp. 260–262, 1988. View at Google Scholar
  22. M. E. Cornford, M. Philippart, B. Jacobs, A. B. Scheibel, and H. V. Vinters, “Neuropathology of Rett syndrome: case report with neuronal and mitochondrial abnormalities in the brain,” Journal of Child Neurology, vol. 9, pp. 424–431, 1994. View at Publisher · View at Google Scholar · View at Scopus
  23. M. T. Dotti, L. Manneschi, A. Malandrini, N. Stefano, F. Caznerale, and A. Federico, “Mitochondrial dysfunction in Rett syndrome. An ultrastructural and biochemical study,” Brain and Development, vol. 15, pp. 103–106, 1993. View at Google Scholar
  24. J. H. Gibson, B. Slobedman, K. N. Harikrishnan et al., “Downstream targets of methyl CpG binding protein 2 and their abnormal expression in the frontal cortex of the human Rett syndrome brain,” BMC Neuroscience, vol. 11, no. 1, p. 53, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Pecorelli, G. Leoni, F. Cervellati et al., “Genes related to mitochondrial functions, protein degradation, and chromatin folding are differentially expressed in lymphomonocytes of Rett syndrome patients,” Mediators of Inflammation, vol. 2013, Article ID 137629, 18 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Filippis, D. Valenti, L. Bari et al., “Mitochondrial free radical overproduction due to respiratory chain impairment in the brain of a mouse model of Rett syndrome: protective effect of CNF1,” Free Radical Biology and Medicine, vol. 83, pp. 167–177, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Kriaucionis, A. Paterson, J. Curtis, J. Guy, N. Macleod, and A. Bird, “Gene expression analysis exposes mitochondrial abnormalities in a mouse model of Rett syndrome,” Molecular and Cellular Biology, vol. 26, pp. 5033–5042, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Valenti, L. Bari, B. Filippis, A. Henrion-Caude, and R. A. Vacca, “Mitochondrial dysfunction as a central actor in intellectual disability-related diseases: an overview of Down syndrome, autism, Fragile X and Rett syndrome,” Neuroscience and Biobehavioral Reviews, vol. 46, Part 2, pp. 202–217, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. W. A. Gold, S. L. Williamson, S. Kaur et al., “Mitochondrial dysfunction in the skeletal muscle of a mouse model of Rett syndrome (RTT): implications for the disease phenotype,” Mitochondrion, vol. 15, pp. 10–17, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Forlani, E. Giarda, U. Ala et al., “The MeCP2/YY1 interaction regulates ANT1 expression at 4q35: novel hints for Rett syndrome pathogenesis,” Human Molecular Genetics, vol. 19, pp. 3114–3123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Cervellati, C. Sticozzi, A. Romani et al., “Impaired enzymatic defensive activity, mitochondrial dysfunction and proteasome activation are involved in RTT cell oxidative damage,” Biochimica et Biophysica Acta, vol. 1852, pp. 2066–2074, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Matsuishi, F. Urabe, A. K. Percy et al., “Abnormal carbohydrate metabolism in cerebrospinal fluid in Rett syndrome,” Journal of Child Neurology, vol. 9, pp. 26–30, 1994. View at Publisher · View at Google Scholar
  33. V. Saywell, A. Viola, S. Confort-Gouny, Y. Fur, L. Villard, and P. J. Cozzone, “Brain magnetic resonance study of Mecp2 deletion effects on anatomy and metabolism,” Biochemical and Biophysical Research Communications, vol. 340, pp. 776–783, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. P. O. Julu, A. M. Kerr, F. Apartopoulos et al., “Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder,” Archives of Disease in Childhood, vol. 85, pp. 29–37, 2001. View at Google Scholar
  35. G. M. Stettner, S. Zanella, P. Huppke, J. Gärtner, G. Hilaire, and M. Dutschmann, “Spontaneous central apneas occur in the C57BL/6J mouse strain,” Respiratory Physiology & Neurobiology, vol. 160, pp. 21–27, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. D. M. Katz, M. Dutschmann, J. M. Ramirez, and G. Hilaire, “Breathing disorders in Rett syndrome: progressive neurochemical dysfunction in the respiratory network after birth,” Respiratory Physiology & Neurobiology, vol. 168, pp. 101–108, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Sierra, M. A. Vilaseca, N. Brandi et al., “Oxidative stress in Rett syndrome,” Brain and Development, vol. 23, Supplement 1, pp. S236–S239, 2001. View at Google Scholar
  38. C. Felice, L. Ciccoli, S. Leoncini et al., “Systemic oxidative stress in classic Rett syndrome,” Free Radical Biology and Medicine, vol. 47, pp. 440–448, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Felice, F. Della Ragione, C. Signorini et al., “Oxidative brain damage in Mecp2-mutant murine models of Rett syndrome,” Neurobiology of Disease, vol. 68, pp. 66–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Großer, U. Hirt, O. A. Janc et al., “Oxidative burden and mitochondrial dysfunction in a mouse model of Rett syndrome,” Neurobiology of Disease, vol. 48, pp. 102–114, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. D. D. Armstrong, “Neuropathology of Rett syndrome,” Journal of Child Neurology, vol. 20, pp. 747–753, 2005. View at Publisher · View at Google Scholar
  42. P. V. Belichenko, E. E. Wright, N. P. Belichenko et al., “Widespread changes in dendritic and axonal morphology in Mecp2-mutant mouse models of Rett syndrome: evidence for disruption of neuronal networks,” The Journal of Comparative Neurology, vol. 514, pp. 240–258, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Moretti, J. M. Levenson, F. Battaglia et al., “Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome,” The Journal of Neuroscience, vol. 26, pp. 319–327, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Ballas, D. T. Lioy, C. Grunseich, and G. Mandel, “Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology,” Nature Neuroscience, vol. 12, pp. 311–317, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. D. T. Lioy, S. K. Garg, C. E. Monaghan et al., “A role for glia in the progression of Rett’s syndrome,” Nature, vol. 475, pp. 497–500, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. M. V. Nguyen, C. A. Felice, F. Du et al., “Oligodendrocyte lineage cells contribute unique features to Rett syndrome neuropathology,” The Journal of Neuroscience, vol. 33, pp. 18764–18774, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. I. Maezawa and L. W. Jin, “Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate,” The Journal of Neuroscience, vol. 30, pp. 5346–5356, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Guy, B. Hendrich, M. Holmes, J. E. Martin, and A. Bird, “A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome,” Nature Genetics, vol. 27, pp. 322–326, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Weller, K. M. Kizina, K. Can, G. Bao, and M. Müller, “Response properties of the genetically encoded optical H2O2 sensor HyPer,” Free Radical Biology and Medicine, vol. 76, pp. 227–241, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. T. J. Sick and M. A. Perez-Pinzon, “Optical methods for probing mitochondrial function in brain slices,” Methods, vol. 18, pp. 104–108, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. S. T. Smiley, M. Reers, C. Mottola-Hartshorn et al., “Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, pp. 3671–3675, 1991. View at Google Scholar
  52. M. R. Duchen, A. Surin, and J. Jacobson, “Imaging mitochondrial function in intact cells,” Methods in Enzymology, vol. 361, pp. 353–389, 2003. View at Google Scholar
  53. K. A. Foster, F. Galeffi, F. J. Gerich, D. A. Turner, and M. Müller, “Optical and pharmacological tools to investigate the role of mitochondria during oxidative stress and neurodegeneration,” Progress in Neurobiology, vol. 79, pp. 136–171, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. V. C. Keil, F. Funke, A. Zeug, D. Schild, and M. Müller, “Ratiometric high-resolution imaging of JC-1 fluorescence reveals the subcellular heterogeneity of astrocytic mitochondria,” Pflügers Archiv, vol. 462, pp. 693–708, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Reers, S. T. Smiley, C. Mottola-Hartshorn, A. Chen, M. Lin, and L. B. Chen, “Mitochondrial membrane potential monitored by JC-1 dye,” Methods in Enzymology, vol. 260, pp. 406–417, 1995. View at Google Scholar
  56. G. T. Hanson, R. Aggeler, D. Oglesbee et al., “Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators,” The Journal of Biological Chemistry, vol. 279, pp. 13044–13053, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Funke, F. J. Gerich, and M. Müller, “Dynamic, semi-quantitative imaging of intracellular ROS levels and redox status in rat hippocampal neurons,” NeuroImage, vol. 54, pp. 2590–2602, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. K. C. Wagener, B. Kolbrink, K. Dietrich et al., “Redox-indicator mice stably expressing genetically-encoded neuronal roGFP: versatile tools to decipher subcellular redox dynamics in neuropathophysiology,” Antioxidants & Redox Signaling, vol. 25, pp. 41–58, 2016. View at Publisher · View at Google Scholar · View at Scopus
  59. K. Can, S. Kügler, and M. Müller, “Live imaging of mitochondrial ROS production and dynamic redox balance in neurons,” in Techniques to Investigate Mitochondrial Function in Neurons, S. Strack and Y. M. Usachev, Eds., pp. 179–197, Springer Science+Business Media, 2017. View at Google Scholar
  60. C. T. Dooley, T. M. Dore, G. T. Hanson, W. C. Jackson, S. J. Remington, and R. Y. Tsien, “Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators,” The Journal of Biological Chemistry, vol. 279, pp. 22284–22293, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. A. J. Meyer and T. P. Dick, “Fluorescent protein-based redox probes,” Antioxidants & Redox Signaling, vol. 13, pp. 621–650, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Müller, J. Schmidt, S. L. Mironov, and D. W. Richter, “Construction and performance of a custom-built two-photon laser scanning system,” Journal of Physics D: Applied Physics, vol. 36, pp. 1747–1757, 2003. View at Google Scholar
  63. N. P. Belichenko, P. V. Belichenko, H. H. Li, W. C. Mobley, and U. Francke, “Comparative study of brain morphology in Mecp2 mutant mouse models of Rett syndrome,” The Journal of Comparative Neurology, vol. 508, pp. 184–195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Poot, Y. Z. Zhang, J. A. Kramer et al., “Analysis of mitochondrial morphology and function with novel fixable fluorescent stains,” The Journal of Histochemistry and Cytochemistry, vol. 44, pp. 1363–1372, 1996. View at Google Scholar
  65. P. Formichi, C. Battisti, M. T. Dotti, G. Hayek, M. Zappella, and A. Federico, “Vitamin E serum levels in Rett syndrome,” Journal of the Neurological Sciences, vol. 156, pp. 227–230, 1998. View at Google Scholar
  66. O. A. Janc and M. Müller, “The free radical scavenger Trolox dampens neuronal hyperexcitability, reinstates synaptic plasticity, and improves hypoxia tolerance in a mouse model of Rett syndrome,” Frontiers in Cellular Neuroscience, vol. 8, p. 56, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. O. A. Janc, M. A. Hüser, K. Dietrich et al., “Systemic radical scavenger treatment of a mouse model of Rett syndrome: merits and limitations of the vitamin E derivative Trolox,” Frontiers in Cellular Neuroscience, vol. 10, p. 266, 2016. View at Publisher · View at Google Scholar · View at Scopus
  68. J. W. Phillis, A. Y. Estevez, and M. H. O'Regan, “Protective effects of the free radical scavengers, dimethyl sulfoxide and ethanol, in cerebral ischemia in gerbils,” Neuroscience Letters, vol. 244, pp. 109–111, 1998. View at Google Scholar
  69. M. Fischer, J. Reuter, F. J. Gerich et al., “Enhanced hypoxia susceptibility in hippocampal slices from a mouse model of Rett syndrome,” Journal of Neurophysiology, vol. 101, pp. 1016–1032, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Müller, S. L. Mironov, M. V. Ivannikov, J. Schmidt, and D. W. Richter, “Mitochondrial organization and motility probed by two-photon microscopy in cultured mouse brainstem neurons,” Experimental Cell Research, vol. 303, pp. 114–127, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. G. L. Rintoul, A. J. Filiano, J. B. Brocard, G. J. Kress, and I. J. Reynolds, “Glutamate decreases mitochondrial size and movement in primary forebrain neurons,” The Journal of Neuroscience, vol. 23, pp. 7881–7888, 2003. View at Google Scholar
  72. V. P. Skulachev, “Mitochondrial filaments and clusters as intracellular power-transmitting cables,” Trends in Biochemical Sciences, vol. 26, pp. 23–29, 2001. View at Google Scholar
  73. E. A. Newman, D. A. Frambach, and L. L. Odette, “Control of extracellular potassium levels by retinal glial cell K+ siphoning,” Science, vol. 225, pp. 1174-1175, 1984. View at Google Scholar
  74. L. K. Bak, A. Schousboe, and H. S. Waagepetersen, “The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer,” Journal of Neurochemistry, vol. 98, pp. 641–653, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. R. C. Janzer and M. C. Raff, “Astrocytes induce blood-brain barrier properties in endothelial cells,” Nature, vol. 325, pp. 253–257, 1987. View at Publisher · View at Google Scholar
  76. A. Ruch, T. W. Kurczynski, and M. E. Velasco, “Mitochondrial alterations in Rett syndrome,” Pediatric Neurology, vol. 5, pp. 320–323, 1989. View at Google Scholar
  77. S. B. Coker and A. R. Melnyk, “Rett syndrome and mitochondrial enzyme deficiencies,” Journal of Child Neurology, vol. 6, pp. 164–166, 1991. View at Publisher · View at Google Scholar · View at Scopus
  78. L. W. Jin, M. Horiuchi, H. Wulff et al., “Dysregulation of glutamine transporter SNAT1 in Rett syndrome microglia: a mechanism for mitochondrial dysfunction and neurotoxicity,” The Journal of Neuroscience, vol. 35, pp. 2516–2529, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. Y. Li, H. Wang, J. Muffat et al., “Global transcriptional and translational repression in human-embryonic-stem-cell-derived Rett syndrome neurons,” Cell Stem Cell, vol. 13, pp. 446–458, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. N. O. Shulyakova, “Studies of mitochondrial dysfunction in models of Rett syndrome. Thesis,” Tech. Rep., Department of Physiology, University of Toronto, Toronto, Canada, 2016. View at Google Scholar
  81. C. Felice, C. Signorini, S. Leoncini et al., “The role of oxidative stress in Rett syndrome: an overview,” Annals of the New York Academy of Sciences, vol. 1259, pp. 121–135, 2012. View at Publisher · View at Google Scholar · View at Scopus
  82. D. F. Suen, K. L. Norris, and R. J. Youle, “Mitochondrial dynamics and apoptosis,” Genes & Development, vol. 22, pp. 1577–1590, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Kron and M. Müller, “Enhanced anoxia susceptibility of MeCP2-deficient CA1 neurons involves altered K+ conductances,” Society for Neuroscience, Abstract Viewer/Itinerary Planner, p. 732.736, 2009. View at Google Scholar
  84. M. Kron and M. Müller, “Impaired hippocampal Ca2+ homeostasis and concomitant K+ channel dysfunction in a mouse model of Rett syndrome during anoxia,” Neuroscience, vol. 171, pp. 300–315, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. M. Kron, J. L. Zimmermann, M. Dutschmann, F. Funke, and M. Müller, “Altered responses of MeCP2-deficient mouse brain stem to severe hypoxia,” Journal of Neurophysiology, vol. 105, pp. 3067–3079, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. A. Mathur, Y. Hong, B. K. Kemp, A. A. Barrientos, and J. D. Erusalimsky, “Evaluation of fluorescent dyes for the detection of mitochondrial membrane potential changes in cultured cardiomyocytes,” Cardiovascular Research, vol. 46, pp. 126–138, 2000. View at Google Scholar