Manipulations of MeCP2 in glutamatergic neurons highlight their contributions to rett and other neurological disorders

eLife

Volumn 5, Issue JUN2016, 2016, Pages

  Meng, Xiangling ^a,b   Wang, Wei ^a,b   Lu, Hui ^a,b   He, Ling Jie ^a,b   Chen, Wu ^a,c   Chao, Eugene S ^a,c   Fiorotto, Marta L ^a   Tang, Bin ^a,b   Herrera, Jose A ^a,b   Seymour, Michelle L ^a   Neul, Jeffrey L ^b,d   Pereira, Fred A ^a   Tang, Jianrong ^a,b   Xue, Mingshan ^a,c   Zoghbi, Huda Y ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Texas Children's Hospital   (United States)

^c Cain Foundation Laboratories   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHYL CPG BINDING PROTEIN 2; MECP2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; ATAXIA; COGNITION; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; EVOKED BRAIN STEM AUDITORY RESPONSE; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; FOOT SLIP TEST; GENE DELETION; GLUTAMATERGIC SYNAPSE; HOLE BOARD ASSAY; IMPAIRED ACOUSTIC STARTLE RESPONSE; LETHALITY; MALE; MAZE TEST; MOUSE; NERVOUS SYSTEM PARAMETERS; NONHUMAN; OBESITY; PARTITION TEST; PHENOTYPE; RETT SYNDROME; ROTAROD TEST; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; TREMOR; ANIMAL; DEFICIENCY; GENE EXPRESSION; GENETICS; METABOLISM; NERVE CELL; NEUROLOGIC DISEASE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; GENE EXPRESSION; METHYL-CPG-BINDING PROTEIN 2; MICE; NERVOUS SYSTEM DISEASES; NEURONS;

EID: 84979650408     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.14199     Document Type: Article

References (52)

1. Amir RE, Van den 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. Nature Genetics 23: 185-188. doi: 10.1038/13810
2. Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT, Edwards RH, Storm-Mathisen J, Chaudhry FA. 2004. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. The Journal of Comparative Neurology 480: 264-280. doi: 10.1002/cne.20354
3. Cai T, Seymour ML, Zhang H, Pereira FA, Groves AK. 2013. Conditional deletion of Atoh1 reveals distinct critical periods for survival and function of hair cells in the organ of Corti. Journal of Neuroscience 33: 10110-10122. doi: 10.1523/JNEUROSCI.5606-12.2013
4. Cardoza B, Clarke A, Wilcox J, Gibbon F, Smith PE, Archer H, Hryniewiecka-Jaworska A, Kerr M. 2011. Epilepsy in Rett syndrome: association between phenotype and genotype, and implications for practice. Seizure 20: 646-649. doi: 10.1016/j.seizure.2011.06.010
5. 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. doi: 10.1038/nature09582
6. Chao HT, Zoghbi HY, Rosenmund C. 2007. MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56: 58-65. doi: 10.1016/j.neuron.2007.08.018
7. Chapleau CA, Calfa GD, Lane MC, Albertson AJ, Larimore JL, Kudo S, Armstrong DL, Percy AK, Pozzo-Miller L. 2009. Dendritic spine pathologies in hippocampal pyramidal neurons from Rett syndrome brain and after expression of Rett-associated MECP2 mutations. Neurobiology of Disease 35: 219-233. doi: 10.1016/j.nbd.2009.05.001
8. Cooper RA, Kerr AM, Amos PM. 1998. Rett syndrome: critical examination of clinical features, serial EEG and video-monitoring in understanding and management. European Journal of Paediatric Neurology 2: 127-135. doi: 10.1016/S1090-3798(98)80028-7
9. Crino PB. 2013. Evolving neurobiology of tuberous sclerosis complex. Acta Neuropathologica 125: 317-332. doi: 10.1007/s00401-013-1085-x
10. D’Cruz JA, Wu C, Zahid T, El-Hayek Y, Zhang L, Eubanks JH. 2010. Alterations of cortical and hippocampal EEG activity in MeCP2-deficient mice. Neurobiology of Disease 38: 8-16. doi: 10.1016/j.nbd.2009.12.018
11. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB. 2005. Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proceedings of the National Academy of Sciences of the United States of America 102: 12560-12565. doi: 10.1073/pnas.0506071102
12. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, Licatalosi DD, Richter JD, Darnell RB. 2011. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146: 247-261. doi: 10.1016/j.cell.2011.06.013
13. Fremeau RT, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH. 2004. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304: 1815-1819. doi: 10.1126/science.1097468
14. Fyffe SL, Neul JL, Samaco RC, Chao HT, Ben-Shachar S, Moretti P, McGill BE, Goulding EH, Sullivan E, Tecott LH, Zoghbi HY. 2008. Deletion of Mecp2 in Sim1-expressing neurons reveals a critical role for MeCP2 in feeding behavior, aggression, and the response to stress. Neuron 59: 947-958. doi: 10.1016/j.neuron.2008.07.030
15. Gemelli T, Berton O, Nelson ED, Perrotti LI, Jaenisch R, Monteggia LM. 2006. Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biological Psychiatry 59: 468-476. doi: 10.1016/j.biopsych.2005.07.025
16. Goffin D, Brodkin ES, Blendy JA, Siegel SJ, Zhou Z. 2014. Cellular origins of auditory event-related potential deficits in Rett syndrome. Nature Neuroscience 17: 804-806. doi: 10.1038/nn.3710
17. 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. doi: 10.1126/science.1138389
18. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. 2001. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nature Genetics 27: 322-326. doi: 10.1038/85899
19. Hao S, Tang B, Wu Z, Ure K, Sun Y, Tao H, Gao Y, Patel AJ, Curry DJ, Samaco RC, Zoghbi HY, Tang J. 2015. Forniceal deep brain stimulation rescues hippocampal memory in Rett syndrome mice. Nature 526: 430-434. doi: 10.1038/nature15694
20. Heckman LD, Chahrour MH, Zoghbi HY. 2014. Rett-causing mutations reveal two domains critical for MeCP2 function and for toxicity in MECP2 duplication syndrome mice. eLife 3: e02676. doi: 10.7554/eLife.02676
21. Hodgkin AL, Huxley AF. 1990. A quantitative description of membrane current and its application to conduction and excitation in nerve. 1952. Bulletin of Mathematical Biology 52: 25-71. doi: 10.1007/BF02459568
22. Ito-Ishida A, Ure K, Chen H, Swann JW, Zoghbi HY. 2015. Loss of MeCP2 in parvalbumin-and somatostatin-expressing neurons in mice leads to distinct rett syndrome-like phenotypes. Neuron 88: 651-658. doi: 10.1016/j.neuron.2015.10.029
23. Julu PO, Kerr AM, Apartopoulos F, Al-Rawas S, Engerström IW, Engerström L, Jamal GA, Hansen S. 2001. Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder. Archives of Disease in Childhood 85: 29-37. doi: 10.1136/adc.85.1.29
24. Klauck SM, Lindsay S, Beyer KS, Splitt M, Burn J, Poustka A. 2002. A mutation hot spot for nonspecific X-linked mental retardation in the MECP2 gene causes the PPM-X syndrome. American Journal of Human Genetics 70: 1034-1037. doi: 10.1086/339553
25. Koch M, Schnitzler HU. 1997. The acoustic startle response in rats-circuits mediating evocation, inhibition and potentiation. Behavioural Brain Research 89: 35-49. doi: 10.1016/S0166-4328(97)02296-1
26. Kodama T, Guerrero S, Shin M, Moghadam S, Faulstich M, du Lac S. 2012. Neuronal classification and marker gene identification via single-cell expression profiling of brainstem vestibular neurons subserving cerebellar learning. Journal of Neuroscience 32: 7819-7831. doi: 10.1523/JNEUROSCI.0543-12.2012
27. Lyst MJ, Bird A. 2015. Rett syndrome: a complex disorder with simple roots. Nature Reviews Genetics 16: 261-275. doi: 10.1038/nrg3897
28. Ma X, Lin L, Qin G, Lu X, Fiorotto M, Dixit VD, Sun Y. 2011. Ablations of ghrelin and ghrelin receptor exhibit differential metabolic phenotypes and thermogenic capacity during aging. PLoS ONE 6: e16391. doi: 10.1371/journal.pone.0016391
29. Mabb AM, Judson MC, Zylka MJ, Philpot BD. 2011. Angelman syndrome: insights into genomic imprinting and neurodevelopmental phenotypes. Trends in Neurosciences 34: 293-303. doi: 10.1016/j.tins.2011.04.001
30. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, Chen G, Gage FH, Muotri AR. 2010. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143: 527-539. doi: 10.1016/j.cell.2010.10.016
31. Miyazaki T, Fukaya M, Shimizu H, Watanabe M. 2003. Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. The European Journal of Neuroscience 17: 2563-2572. doi: 10.1046/j.1460-9568.2003.02698.x
32. Nelson SB, Valakh V. 2015. Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders. Neuron 87: 684-698. doi: 10.1016/j.neuron.2015.07.033
33. Pelka GJ, Watson CM, Radziewic T, Hayward M, Lahooti H, Christodoulou J, Tam PP. 2006. Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 129: 887-898. doi: 10.1093/brain/awl022
34. Qiu S, Anderson CT, Levitt P, Shepherd GM. 2011. Circuit-specific intracortical hyperconnectivity in mice with deletion of the autism-associated Met receptor tyrosine kinase. Journal of Neuroscience 31: 5855-5864. doi: 10.1523/JNEUROSCI.6569-10.2011
35. Roze E, Cochen V, Sangla S, Bienvenu T, Roubergue A, Leu-Semenescu S, Vidaihet M. 2007. Rett syndrome: an overlooked diagnosis in women with stereotypic hand movements, psychomotor retardation, Parkinsonism, and dystonia? Movement Disorders 22: 387-389. doi: 10.1002/mds.21276
36. Rubenstein JL, Merzenich MM. 2003. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes, Brain, and Behavior 2: 255-267. doi: 10.1034/j.1601-183X.2003.00037.x
37. Samaco RC, McGraw CM, Ward CS, Sun Y, Neul JL, Zoghbi HY. 2013. Female Mecp2(+/-) mice display robust behavioral deficits on two different genetic backgrounds providing a framework for pre-clinical studies. Human Molecular Genetics 22: 96-109. doi: 10.1093/hmg/dds406
38. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, Armstrong D, Paylor R, Zoghbi H. 2002. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35: 243-254. doi: 10.1016/S0896-6273(02)00768-7
39. Stearns NA, Schaevitz LR, Bowling H, Nag N, Berger UV, Berger-Sweeney J. 2007. Behavioral and anatomical abnormalities in Mecp2 mutant mice: a model for Rett syndrome. Neuroscience 146: 907-921. doi: 10.1016/j.neuroscience.2007.02.009
40. Steffenburg U, Hagberg G, Hagberg B. 2001. Epilepsy in a representative series of Rett syndrome. Acta Paediatrica 90: 34-39. doi: 10.1111/j.1651-2227.2001.tb00252.x
41. Telfeian AE, Tseng HC, Baybis M, Crino PB, Dichter MA. 2003. Differential expression of GABA and glutamate-receptor subunits and enzymes involved in GABA metabolism between electrophysiologically identified hippocampal CA1 pyramidal cells and interneurons. Epilepsia 44: 143-149. doi: 10.1046/j.1528-1157.2003.06102.x
42. Trappe R, Laccone F, Cobilanschi J, Meins M, Huppke P, Hanefeld F, Engel W. 2001. MECP2 mutations in sporadic cases of Rett syndrome are almost exclusively of paternal origin. American Journal of Human Genetics 68: 1093-1101. doi: 10.1086/320109
43. Tschöp MH, Speakman JR, Arch JRS, Auwerx J, Brüning JC, Chan L, Eckel RH, Farese RV, Galgani JE, Hambly C, Herman MA, Horvath TL, Kahn BB, Kozma SC, Maratos-Flier E, Müller TD, Münzberg H, Pfluger PT, Plum L, Reitman ML, et al. 2012. A guide to analysis of mouse energy metabolism. Nature Methods 9: 57-63. doi: 10.1038/nmeth.1806
44. Turrigiano G. 2011. Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annual Review of Neuroscience 34: 89-103. doi: 10.1146/annurev-neuro-060909-153238
45. Ure K, Lu H, Wang W, Ito-Ishida A, Wu Z, He LJ, Sztainberg Y, Chen W, Tang J, Zoghbi HY. 2016. Restoration of Mecp2 expression in GABAergic neurons is sufficient to rescue multiple disease features in a mouse model of Rett Syndrome. eLife 5: e14198. doi: 10.7554/eLife.14198
46. Vong L, Ye C, Yang Z, Choi B, Chua S, Lowell BB. 2011. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71: 142-154. doi: 10.1016/j.neuron.2011.05.028
47. Ward CS, Arvide EM, Huang TW, Yoo J, Noebels JL, Neul JL. 2011. MeCP2 is critical within HoxB1-derived tissues of mice for normal lifespan. Journal of Neuroscience 31: 10359-10370. doi: 10.1523/JNEUROSCI.0057-11.2011
48. 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. Pediatric Research 60: 443-449. doi: 10.1203/01.pdr.0000238302.84552.d0
49. Wiesmann UN, DiDonato S, Herschkowitz NN, Ma X LL, Qin G, Lu X, Fiorotto M, Dixit VD, Sun Y. 1975. Effect of chloroquine on cultured fibroblasts: release of lysosomal hydrolases and inhibition of their uptake. Biochemical and Biophysical Research Communications 66: e16391. doi: 10.1016/0006-291X(75)90506-9
50. Wood L, Gray NW, Zhou Z, Greenberg ME, Shepherd GM. 2009. Synaptic circuit abnormalities of motor-frontal layer 2/3 pyramidal neurons in an RNA interference model of methyl-CpG-binding protein 2 deficiency. Journal of Neuroscience 29: 12440-12448. doi: 10.1523/JNEUROSCI.3321-09.2009
51. Young JI, Zoghbi HY. 2004. X-chromosome inactivation patterns are unbalanced and affect the phenotypic outcome in a mouse model of rett syndrome. American Journal of Human Genetics 74: 511-520. doi: 10.1086/382228
52. Zhang W, Peterson M, Beyer B, Frankel WN, Zhang ZW. 2014. Loss of MeCP2 from forebrain excitatory neurons leads to cortical hyperexcitation and seizures. Journal of Neuroscience 34: 2754-2763. doi: 10.1523/JNEUROSCI.4900-12.2014