Deficiency of GABAergic synaptic inhibition in the Kölliker-Fuse area underlies respiratory dysrhythmia in a mouse model of Rett syndrome

Journal of Physiology

Volumn 594, Issue 1, 2016, Pages 223-237

  Abdala, Ana Paula ^a   Toward, Marie A ^a   Dutschmann, Mathias ^b   Bissonnette, John M ^c   Paton, Julian F R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; METHYL CPG BINDING PROTEIN 2; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APNEA; ARTICLE; BREATHING PATTERN; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GABAERGIC TRANSMISSION; HETEROZYGOTE; INSPIRATORY CAPACITY; KOLLIKER FUSE NUCLEUS; MALE; MECP2 GENE; MOLECULAR PATHOLOGY; MOUSE; NEUROBIOLOGY; NONHUMAN; OSCILLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; RAT; RECEPTOR BLOCKING; RESPIRATORY DYSRHYTHMIA; RESPIRATORY TRACT DISEASE; RETT SYNDROME; SYNAPTIC INHIBITION; UPPER RESPIRATORY TRACT; ANIMAL; BREATHING; GENETICS; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; FEMALE; GABA ANTAGONISTS; INHIBITORY POSTSYNAPTIC POTENTIALS; KOLLIKER-FUSE NUCLEUS; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; RECEPTORS, GABA-A; RESPIRATION; RETT SYNDROME;

EID: 84952865541     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270966     Document Type: Article

References (75)

1. Abdala AP, Bissonnette JM & Newman-Tancredi A (2014a). Pinpointing brainstem mechanisms responsible for autonomic dysfunction in Rett syndrome: therapeutic perspectives for 5-HT1A agonists. Front Physiol 5, 205.
2. Abdala AP, Dutschmann M, Bissonnette JM & Paton JF (2010). Correction of respiratory disorders in a mouse model of Rett syndrome. Proc Natl Acad Sci USA 107, 18208-18213.
3. Abdala AP, Lioy DT, Garg SK, Knopp SJ, Paton JF & Bissonnette JM (2014b). Effect of Sarizotan, a 5-HT1a and D2-like receptor agonist, on respiration in three mouse models of Rett syndrome. Am J Respir Cell Mol Biol 50, 1031-1039.
4. Alheid GF, Gray PA, Jiang MC, Feldman JL & McCrimmon DR (2002). Parvalbumin in respiratory neurons of the ventrolateral medulla of the adult rat. J Neurocytol 31, 693-717.
5. 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.
6. Bautista TG & Dutschmann M (2014). Ponto-medullary nuclei involved in the generation of sequential pharyngeal swallowing and concomitant protective laryngeal adduction in situ. J Physiol 592, 2605-2623.
7. 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.
8. 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.
9. Blue ME, Naidu S & Johnston MV (1999a). Altered development of glutamate and GABA receptors in the basal ganglia of girls with Rett syndrome. Exp Neurol 156, 345-352.
10. Blue ME, Naidu S & Johnston MV (1999b). Development of amino acid receptors in frontal cortex from girls with Rett syndrome. Ann Neurol 45, 541-545.
11. /+ mouse brain. Hum Mol Genet 13, 1275-1286.
12. Carotenuto M, Esposito M, D'Aniello A, Rippa CD, Precenzano F, Pascotto A, Bravaccio C & Elia M (2012). Polysomnographic findings in Rett syndrome: a case-control study. Sleep Breath 17, 93-98.
13. Chamberlin NL & Saper CB (1994). Topographic organization of respiratory responses to glutamate microstimulation of the parabrachial nucleus in the rat. J Neurosci 14, 6500-6510.
14. Champagnat J, Denavit-Saubie M, Moyanova S & Rondouin G (1982). Involvement of amino acids in periodic inhibitions of bulbar respiratory neurones. Brain Res 237, 351-365.
15. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, Gong S, Lu HC, Heintz N, Ekker M, Rubenstein JL, Noebels JL, Rosenmund C & Zoghbi HY (2010). Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468, 263-269.
16. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E & Huang ZJ (2004). Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24, 9598-9611.
17. Cohen MI (1971). Switching of the respiratory phases and evoked phrenic responses produced by rostral pontine electrical stimulation. J Physiol 217, 133-158.
18. Damasceno RS, Takakura AC & Moreira TS (2014). Regulation of the chemosensory control of breathing by Kolliker-Fuse neurons. Am J Physiol Regul Integr Comp Physiol 307, R57-67.
19. Dhingra RR, Zhu Y, Jacono FJ, Katz DM, Galan RF & Dick TE (2013). Decreased Hering-Breuer input-output entrainment in a mouse model of Rett syndrome. Front Neural Circuits 7, 42.
20. Dick TE, Bellingham MC & Richter DW (1994). Pontine respiratory neurons in anesthetized cats. Brain Res 636, 259-269.
21. Downs J, Wong K, Ravikumara M, Ellaway C, Elliott EJ, Christodoulou J, Jacoby P & Leonard H (2014). Experience of gastrostomy using a quality care framework: the example of Rett syndrome. Medicine (Baltimore) 93, e328.
22. Dutschmann M & Dick TE (2012). Pontine mechanisms of respiratory control. Compr Physiol 2, 2443-2469.
23. A receptors in the rat Kolliker-Fuse area control cardiorespiratory responses evoked by trigeminal ethmoidal nerve stimulation. J Physiol 510, 793-804.
24. Dutschmann M & Herbert H (2006). The Kolliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur J Neurosci 24, 1071-1084.
25. Ezure K & Tanaka I (2004). GABA, in some cases together with glycine, is used as the inhibitory transmitter by pump cells in the Hering-Breuer reflex pathway of the rat. Neuroscience 127, 409-417.
26. Ezure K, Tanaka I & Kondo M (2003a). Glycine is used as a transmitter by decrementing expiratory neurons of the ventrolateral medulla in the rat. J Neurosci 23, 8941-8948.
27. Ezure K, Tanaka I & Miyazaki M (1998). Pontine projections of pulmonary slowly adapting receptor relay neurons in the cat. Neuroreport 9, 411-414.
28. Ezure K, Tanaka I & Saito Y (2003b). Brainstem and spinal projections of augmenting expiratory neurons in the rat. Neurosci Res 45, 41-51.
29. Ezure K, Tanaka I, Saito Y & Otake K (2002). Axonal projections of pulmonary slowly adapting receptor relay neurons in the rat. J Comp Neurol 446, 81-94.
30. Forbes-Lorman RM, Kurian JR & Auger AP (2014). MeCP2 regulates GFAP expression within the developing brain. Brain Res 1543, 151-158.
31. Fortuna MG, West GH, Stornetta RL & Guyenet PG (2008). Botzinger expiratory-augmenting neurons and the parafacial respiratory group. J Neurosci 28, 2506-2515.
32. Franklin KBJ & Paxinos G (2007). The Mouse Brain in Stereotaxic Coordinates. Elsevier, Amsterdam.
33. Gautier H & Bertrand F (1975). Respiratory effects of pneumotaxic center lesions and subsequent vagotomy in chronic cats. Resp Physiol 23, 71-85.
34. Goyal M, O'Riordan MA & Wiznitzer M (2004). Effect of topiramate on seizures and respiratory dysrhythmia in Rett syndrome. J Child Neurol 19, 588-591.
35. A receptor subunits, and GAD mRNAs in the rat parabrachial and Kolliker-Fuse nuclei. J Comp Neurol 400, 229-243.
36. Haji A, Takeda R & Remmers JE (1992). Evidence that glycine and GABA mediate postsynaptic inhibition of bulbar respiratory neurons in the cat. J Appl Physiol (1985) 73, 2333-2342.
37. Hayward LF, Castellanos M & Davenport PW (2004). Parabrachial neurons mediate dorsal periaqueductal gray evoked respiratory responses in the rat. J Appl Physiol (1985) 96, 1146-1154.
38. Horike S, Cai S, Miyano M, Cheng JF & Kohwi-Shigematsu T (2005). Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat Genet 37, 31-40.
39. Isaacs JS, Murdock M, Lane J & Percy AK (2003). Eating difficulties in girls with Rett syndrome compared with other developmental disabilities. J Am Diet Assoc 103, 224-230.
40. Johnson CM, Cui N, Zhong W, Oginsky MF & Jiang C (2015). Breathing abnormalities in a female mouse model of Rett syndrome. J Physiol Sci 65, 451-459.
41. 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.
42. Kline DD, Ogier M, Kunze DL & Katz DM (2010). Exogenous brain-derived neurotrophic factor rescues synaptic dysfunction in Mecp2-null mice. J Neurosci 30, 5303-5310.
43. Krajnc N (2014). Severe respiratory dysrhythmia in Rett syndrome treated with topiramate. J Child Neurol 29, NP118-121.
44. 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.
45. Kron M, Zimmermann JL, Dutschmann M, Funke F & Muller M (2011). Altered responses of MeCP2-deficient mouse brain stem to severe hypoxia. J Neurophysiol 105, 3067-3079.
46. Lugaresi E, Cirignotta F & Montagna P (1985). Abnormal breathing in the Rett syndrome. Brain Dev 7, 329-333.
47. Maezawa I & Jin LW (2010). Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J Neurosci 30, 5346-5356.
48. Medrihan L, Tantalaki E, Aramuni G, Sargsyan V, Dudanova I, Missler M & Zhang W (2008). Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome. J Neurophysiol 99, 112-121.
49. Moerschel M & Dutschmann M (2009). Pontine respiratory activity involved in inspiratory/expiratory phase transition. Philos Trans R Soc Lond B Biol Sci 364, 2517-2526.
50. Morton RE, Bonas R, Minford J, Kerr A & Ellis RE (1997). Feeding ability in Rett syndrome. Dev Med Child Neurol 39, 331-335.
51. Morton RE, Pinnington L & Ellis RE (2000). Air swallowing in Rett syndrome. Dev Med Child Neurol 42, 271-275.
52. 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.
53. Paton JFR (1995). A working heart-brain-stem preparation of the mature mouse. J Physiol 489.P, 155P-155P.
54. Paton JF & Kasparov S (1999). Differential effects of angiotensin II on cardiorespiratory reflexes mediated by nucleus tractus solitarii - a microinjection study in the rat. J Physiol 521, 213-225.
55. 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.
56. Ren J, Ding X, Funk GD & Greer JJ (2012). Anxiety-related mechanisms of respiratory dysfunction in a mouse model of Rett syndrome. J Neurosci 32, 17230-17240.
57. Richter DW, Manzke T, Wilken B & Ponimaskin E (2003). Serotonin receptors: guardians of stable breathing. Trends Mol Med 9, 542-548.
58. A receptors shape the discharge pattern of bulbar respiratory neurons. Brain Res 710, 150-160.
59. Schreihofer AM, Stornetta RL & Guyenet PG (1999). Evidence for glycinergic respiratory neurons: Botzinger neurons express mRNA for glycinergic transporter 2. J Comp Neurol 407, 583-597.
60. Song G, Tin C, Giacometti E & Poon CS (2011). Habituation without NMDA receptor-dependent desensitization of Hering-Breuer apnea reflex in a Mecp2 mutant mouse model of Rett syndrome. Front Integr Neurosci 5, 6.
61. Song G, Wang H, Xu H & Poon CS (2012). Kolliker-Fuse neurons send collateral projections to multiple hypoxia-activated and nonactivated structures in rat brainstem and spinal cord. Brain Struct Funct 217, 835-858.
62. /y knockout mice. J Physiol 579, 863-876.
63. Stettner GM, Zanella S, Hilaire G & Dutschmann M (2008a). 8-OH-DPAT suppresses spontaneous central apneas in the C57BL/6 J mouse strain. Respir Physiol Neurobiol 161, 10-15.
64. Stettner GM, Zanella S, Huppke P, Gartner J, Hilaire G & Dutschmann M (2008b). Spontaneous central apneas occur in the C57BL/6 J mouse strain. Respir Physiol Neurobiol 160, 21-27.
65. Stornetta RL, Rosin DL, Wang H, Sevigny CP, Weston MC & Guyenet PG (2003). A group of glutamatergic interneurons expressing high levels of both neurokinin-1 receptors and somatostatin identifies the region of the pre-Botzinger complex. J Comp Neurol 455, 499-512.
66. Tan W, Pagliardini S, Yang P, Janczewski WA & Feldman JL (2010). Projections of preBotzinger complex neurons in adult rats. J Comp Neurol 518, 1862-1878.
67. 2 chemosensitivity in methyl-CpG-binding protein 2 (Mecp2)-deficient mice. Exp Physiol 98, 842-849.
68. Viemari JC, Roux JC, Tryba AK, Saywell V, Burnet H, Pena F, Zanella S, Bevengut 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.
69. Voituron N & Hilaire G (2011). The benzodiazepine Midazolam mitigates the breathing defects of Mecp2-deficient mice. Respir Physiol Neurobiol 177, 56-60.
70. Voituron N, Menuet C, Dutschmann M & Hilaire G (2010). Physiological definition of upper airway obstructions in mouse model for Rett syndrome. Respir Physiol Neurobiol 173, 146-156.
71. 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.
72. Yamashita Y, Matsuishi T, Ishibashi M, Kimura A, Onishi Y, Yonekura Y & Kato H (1998). Decrease in benzodiazepine receptor binding in the brains of adult patients with Rett syndrome. J Neurol Sci 154, 146-150.
73. Yasui DH, Xu H, Dunaway KW, Lasalle JM, Jin LW & Maezawa I (2013). MeCP2 modulates gene expression pathways in astrocytes. Mol Autism 4, 3.
74. Yokota S, Tsumori T, Oka T, Nakamura S & Yasui Y (2008). GABAergic neurons in the ventrolateral subnucleus of the nucleus tractus solitarius are in contact with Kolliker-Fuse nucleus neurons projecting to the rostral ventral respiratory group and phrenic nucleus in the rat. Brain Res 1228, 113-126.
75. Zhang X, Su J, Cui N, Gai H, Wu Z & Jiang C (2011). The disruption of central CO2 chemosensitivity in a mouse model of Rett syndrome. Am J Physiol Cell Physiol 301, C729-738.