Impaired CO2 sensitivity of astrocytes in a mouse model of Rett syndrome

Journal of Physiology

Volumn 593, Issue 14, 2015, Pages 3159-3168

  Turovsky, Egor ^a,b   Karagiannis, Anastassios ^a   Abdala, Ana Paula ^c   Gourine, Alexander V ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INSTITUTE OF CELL BIOPHYSICS   (Russian Federation)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARBON DIOXIDE; LACTIC ACID; METHYL CPG BINDING PROTEIN 2; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CALCIUM; MESP2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN SLICE; CELL METABOLISM; CHEMOSENSITIVITY; EXTRACELLULAR SPACE; FEMALE; GENE DELETION; HYPOXIA; KNOCKOUT MOUSE; MALE; MEDULLA OBLONGATA; MOUSE; MOUSE MODEL; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RESPIRATORY FUNCTION; RETT SYNDROME; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; GENETICS; METABOLISM;

ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM; CARBON DIOXIDE; CEREBRAL CORTEX; LACTIC ACID; MEDULLA OBLONGATA; MICE; RETT SYNDROME;

EID: 84948383311     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270369     Document Type: Article

References (68)

1. Abdala AP, Dutschmann M, Bissonnette JM & Paton JF (2010). Correction of respiratory disorders in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A 107, 18208-18213.
2. Amaral MD, Chapleau CA & Pozzo-Miller L (2007). Transient receptor potential channels as novel effectors of brain-derived neurotrophic factor signaling: potential implications for Rett syndrome. Pharmacol Ther 113, 394-409.
3. Amir RE, Vanden Veyver IB, Wan M, Tran CQ, Francke U & Zoghbi HY (1999). Rett syndrome is caused by mutations in X-linked MeCP2, encoding methyl-CpG-binding protein 2. Nat Genet 23, 185-188.
4. Andaku DK, Mercadante MT & Schwartzman JS (2005). Buspirone in Rett syndrome respiratory dysfunction. Brain Dev 27, 437-438.
5. Armstrong DD (1995). The neuropathology of Rett syndrome- overview 1994. Neuropediatrics 26, 100-104.
6. Ballas N, Lioy DT, Grunseich C & Mandel G (2009). Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 12, 311-317.
7. Bauman ML, Kemper TL & Arin DM (1995). Pervasive neuroanatomic abnormalities of the brain in three cases of Rett's syndrome. Neurology 45, 1581-1586.
8. Bissonnette JM, Garg SK, Lioy DT, Knopp SJ & Mandel G (2012). Depletion of methyl-CpG-binding protein 2 (MeCP2) in astrocytes depresses chemosensitivity. Program No. 897.19. 2012 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2012. Online.
9. Bissonnette JM & Knopp SJ (2006). Separate respiratory phenotypes in methyl-CpG-binding protein 2 (Mecp2) deficient mice. Pediatr Res 59(4), 513-518.
10. Bissonnette JM & Knopp SJ (2008). Effect of inspired oxygen on periodic breathing in methy-CpG-binding protein 2 (Mecp2) deficient mice. J Appl Physiol 104, 198-204.
11. Bissonnette JM, Schaevitz LR, Knopp SJ & Zhou Z (2014). Respiratory phenotypes are distinctly affected in mice with common Rett syndrome mutations MeCP2 T158A and R168X. Neuroscience 267, 166-176.
12. -/+ mouse brain. Hum Mol Genet 13, 1275-1286.
13. Carotenuto M, Esposito M, D'Aniello A, Rippa CD, Precenzano F, Pascotto A, Bravaccio C & Elia M (2013). Polysomnographic findings in Rett syndrome: a case-control study. Sleep Breath 17, 93-98.
14. Chang Q, Khare G, Dani V, Nelson S & Jaenisch R (2006). The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49, 341-348.
15. Chen WG, Chang Q, Lin Y, Meissner A, West AE, Griffith EC, Jaenisch R & Greenberg ME (2003). Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302, 885-889.
16. Cornford ME, Philippart M, Jacobs B, Scheibel AB & Vinters HV (1994). Neuropathology of Rett syndrome: case report with neuronal and mitochondrial abnormalities in the brain. J Child Neurol 9, 424-431.
17. Cuddapah VA, Nwaobi S, Thompson C & Olsen M (2013). Methyl-CpG-binding protein 2 (MeCP2) deficiency leads to altered astrocyte function. Program No. 718.09. 2013 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2013. Online.
18. DeFelice C, Della Ragione F, Signorini C, Leoncini S, Pecorelli A, Ciccoli L, Scalabrì F, Marracino F, Madonna M, Belmonte G, Ricceri L, DeFilippis B, Laviola G, Valacchi G, Durand T, Galano JM, Oger C, Guy A, Bultel-Poncé V, Guy J, Filosa S, Hayek J & D'Esposito M (2014). Oxidative brain damage in Mecp2-mutant murine models of Rett syndrome. Neurobiol Dis 68, 66-77.
19. DeFelice C, Rossi M, Leoncini S, Chisci G, Signorini C, Lonetti G, Vannuccini L, Spina D, Ginori A, Iacona I, Cortelazzo A, Pecorelli A, Valacchi G, Ciccoli L, Pizzorusso T & Hayek J (2014). Inflammatory lung disease in Rett syndrome. Mediators Inflamm 2014, 560120.
20. DeFelice C, Signorini C, Leoncini S, Pecorelli A, Durand T, Valacchi G, Ciccoli L & Hayek J (2012). The role of oxidative stress in Rett syndrome: an overview. Ann N Y Acad Sci 1259, 121-135.
21. Forbes-Lorman RM, Kurian JR & Auger AP (2014). MeCP2 regulates GFAP expression within the developing brain. Brain Res 1543, 151-158.
22. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K & Kasparov S (2010). Astrocytes control breathing through pH-dependent release of ATP. Science 329, 571-575.
23. Gourine AV, Llaudet E, Dale N & Spyer KM (2005). ATP is a mediator of chemosensory transduction in the central nervous system. Nature 436, 108-111.
24. Guy J, Gan J, Selfridge J, Cobb S & Bird A (2007). Reversal of neurological defects in a mouse model of Rett syndrome. Science 315, 1143-1147.
25. Guy J, Hendrich B, Holmes M, Martin JE & Bird A (2001). A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27, 322-326.
26. Guyenet PG (2014). Regulation of breathing and autonomic outflows by chemoreceptors. Compr Physiol 4, 1511-1562.
27. Hagebeuk EE, Bijlmer RP, Koelman JH & Poll-The BT (2012). Respiratory disturbances in Rett syndrome: don't forget to evaluate upper airway obstruction. J Child Neurol 27, 888-892.
28. Harms L, Finta M, Tschöpl M & Illes P (1992). Depolarization of rat locus coeruleus neurons by adenosine 5′-triphosphate. Neuroscience 48, 941-952.
29. 2-dependent opening of connexin 26 and related beta connexins. J Physiol 588, 3921-3931.
30. 2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J Physiol 588, 3901-3920.
31. Julu PO, Kerr AM, Apartopoulos F, Al-Rawas S, Engerstrom IW, Engerstrom L, Jamal GA & Hansen S (2001). Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder. Arch Dis Child 85, 29-37.
32. Kasymov V, Larina O, Castaldo C, Marina N, Patrushev M, Kasparov S & Gourine AV (2013). Differential sensitivity of brainstem versus cortical astrocytes to changes in pH reveals functional regional specialization of astroglia. J Neurosci 33, 435-441.
33. Kron M, Lang M, Adams IT, Sceniak M, Longo F & Katz DM (2014). A BDNF loop-domain mimetic acutely reverses spontaneous apneas and respiratory abnormalities during behavioral arousal in a mouse model of Rett syndrome. Dis Model Mech 7, 1047-1055.
34. Lappalainen R & Riikonen RS (1994). Elevated CSF lactate in the Rett syndrome: cause or consequence? Brain Dev 16, 399-401.
35. Lawson-Yuen A, Liu D, Han L, Jiang ZI, Tsai GE, Basu AC, Picker J, Feng J & Coyle JT (2007). Ube3a mRNA and protein expression are not decreased in Mecp2R168X mutant mice. Brain Res 1180, 1-6.
36. Lioy DT, Garg SK, Monaghan CE, Raber J, Foust KD, Kaspar BK, Hirrlinger PG, Kirchhoff F, Bissonnette JM, Ballas N & Mandel G (2011). A role for glia in the progression of Rett's syndrome. Nature 475, 497-500.
37. Maezawa I & Jin LW (2010). Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J Neurosci 30, 5346-5356.
38. Maezawa I, Swanberg S, Harvey D, LaSalle JM & Jin LW (2009). Rett syndrome astrocytes are abnormal and spread MeCP2 deficiency through gap junctions. J Neurosci 29, 5051-5061.
39. Magistretti PJ, Sorg O, Naichen Y, Pellerin L, deRham S & Martin JL (1994). Regulation of astrocyte energy metabolism by neurotransmitters. Ren Physiol Biochem 17, 168-171.
40. Magistretti PJ, Sorg O, Yu N, Martin JL & Pellerin L (1993). Neurotransmitters regulate energy metabolism in astrocytes: implications for the metabolic trafficking between neural cells. Dev Neurosci 15, 306-312.
41. Marina N, Abdala AP, Trapp S, Li A, Nattie EE, Hewinson J, Smith JC, Paton JF & Gourine AV (2010). Essential role of Phox2b-expressing ventrolateral brainstem neurons in the chemosensory control of inspiration and expiration. J Neurosci 30, 12466-12473.
42. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G & Sun YE (2003). DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302, 890-893.
43. Matsuishi T, Urabe F, Komori H, Yamashita Y, Naito E, Kuroda Y, Horikawa M & Ohtaki E (1992). The Rett syndrome and CSF lactic acid patterns. Brain Dev 14, 68-70.
44. Matsuishi T, Urabe F, Percy AK, Komori H, Yamashita Y, Schultz RS, Ohtani Y, Kuriya N & Kato H (1994). Abnormal carbohydrate metabolism in cerebrospinal fluid in Rett syndrome. J Child Neurol 9, 26-30.
45. + sensing by astrocytes in the retrotrapezoid nucleus and their possible contribution to respiratory drive. Exp Physiol 96, 400-406.
46. Nwaobi SE, Lin E, Peramsetty SR & Olsen ML (2014). DNA methylation functions as a critical regulator of Kir4.1 expression during CNS development. Glia 62, 411-427.
47. Okabe Y, Takahashi T, Mitsumasu C, Kosai K, Tanaka E & Matsuishi T (2012). Alterations of gene expression and glutamate clearance in astrocytes derived from an MeCP2-null mouse model of Rett syndrome. PLoS One 7, e35354.
48. Pellerin L & Magistretti PJ (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91, 10625-10629.
49. Ramirez JM, Ward CS & Neul JL (2013). Breathing challenges in Rett syndrome: lessons learned from humans and animal models. Respir Physiol Neurobiol 189, 280-287.
50. Schmid DA, Yang T, Ogier M, Adams I, Mirakhur Y, Wang Q, Massa SM, Longo FM & Katz DM (2012). A TrkB small molecule partial agonist rescues TrkB phosphorylation deficits and improves respiratory function in a mouse model of Rett syndrome. J Neurosci 32, 1803-1810.
51. Schurr A, Payne RS, Miller JJ & Rigor BM (1997a). Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J Neurochem 69, 423-426.
52. Schurr A, Payne RS, Miller JJ & Rigor BM (1997b). Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res 744, 105-111.
53. Schurr A, Payne RS, Miller JJ & Rigor BM (1997c). Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia. Brain Res 774, 221-224.
54. Shigetomi E, Jackson-Weaver O, Huckstepp RT, O'Dell TJ & Khakh BS (2013). TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J Neurosci 33, 10143-10153.
55. Smeets EE, Julu PO, vanWaardenburg D, Engerstrom IW, Hansen S, Apartopoulos F, Curfs LM & Schrander-Stumpel CT (2006). Management of a severe forceful breather with Rett syndrome using carbogen. Brain Dev 28, 625-632.
56. Schnell C, Hagos Y & Hülsmann S (2012). Active sulforhodamine 101 uptake into hippocampal astrocytes. PLoS One 7, e49398.
57. Southall DP, Kerr AM, Tirosh E, Amos P, Lang MH & Stephenson JB (1988). Hyperventilation in the awake state: potentially treatable component of Rett syndrome. Arch Dis Child 63, 1039-1048.
58. Tang F, Lane S, Korsak A, Paton JF, Gourine AV, Kasparov S & Teschemacher AG (2014). Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat Commun 5, 3284.
59. 2 chemosensitivity in methyl-CpG-binding protein 2 (Mecp2)-deficient mice. Exp Physiol 98, 842-849.
60. Trapp S, Tucker SJ & Gourine AV (2011). Respiratory responses to hypercapnia and hypoxia in mice with genetic ablation of Kir5.1 (Kcnj16). Exp Physiol 96, 451-459.
61. Viemari JC, Roux JC, Tryba AK, Saywell V, Burnet H, Peña F, Zanella S, Bévengut M, Barthelemy-Requin M, Herzing LB, Moncla A, Mancini J, Ramirez JM, Villard L & Hilaire G (2005). Mecp2 deficiency disrupts norepinephrine and respiratory systems in mice. J Neurosci 25, 11521-11530.
62. Voituron N, Zanella S, Menuet C, Dutschmann M & Hilaire G (2009). Early breathing defects after moderate hypoxia or hypercapnia in a mouse model of Rett syndrome. Respir Physiol Neurobiol 168, 109-118.
63. Wang H, Chan SA, Ogier M, Hellard D, Wang Q, Smith C & Katz DM (2006). Dysregulation of brain-derived neurotrophic factor expression and neurosecretory function in Mecp2 null mice. J Neurosci 26, 10911-10915.
64. Weese-Mayer DE, Lieske SP, Boothby CM, Kenny AS, Bennett HL, Silvestri JM & Ramirez JM (2006). Autonomic nervous system dysregulation: breathing and heart rate perturbation during wakefulness in young girls with Rett syndrome. Pediatr Res 60, 443-449.
65. + by inhibition of a Kir4.1-Kir5.1-like current and may contribute to chemoreception by a purinergic mechanism. J Neurophysiol 104, 3042-3052.
66. +-sensitive neurons by purinergic signalling. J Physiol 590, 2137-2150.
67. Yasui DH, Xu H, Dunaway KW, Lasalle JM, Jin LW & Maezawa I (2013). MeCP2 modulates gene expression pathways in astrocytes. Mol Autism 4, 3.
68. 2 chemosensitivity in a mouse model of Rett syndrome. Am J Physiol Cell Physiol 301, C729-738.