MeCP2-mediated alterations of striatal features accompany psychomotor deficits in a mouse model of Rett syndrome

Brain Structure and Function

Volumn 220, Issue 1, 2015, Pages 419-434

  Kao, Fang Chi ^a   Su, San Hua ^a   Carlson, Gregory C ^b   Liao, Wenlin ^a  

^a NATIONAL CHENGCHI UNIVERSITY   (Taiwan)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Autism spectrum disorders; Calbindin; Dopamine; Parvalbumin; Striatum; Opioid receptor

Indexed keywords

CALBINDINS; DOPAMINE; MECP2 PROTEIN, MOUSE; METHYL-CPG-BINDING PROTEIN 2; NERVE TISSUE PROTEINS; RECEPTORS, DOPAMINE; RECEPTORS, OPIOID, MU; RNA, MESSENGER; TYROSINE 3-MONOOXYGENASE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPLICATION; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; LEARNING; MALE; METABOLISM; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PATHOLOGY; PHYSIOLOGY; PSYCHOMOTOR DISORDERS; RETT SYNDROME; ROTAROD PERFORMANCE TEST;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CALBINDINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; LEARNING; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PSYCHOMOTOR DISORDERS; RECEPTORS, DOPAMINE; RECEPTORS, OPIOID, MU; RETT SYNDROME; RNA, MESSENGER; ROTAROD PERFORMANCE TEST; TYROSINE 3-MONOOXYGENASE;

EID: 84887070692     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0664-x     Document Type: Article

References (74)

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. Nat Genet 23:185–188
2. Amir RE, Van den Veyver IB, Schultz R, Malicki DM, Tran CQ, Dahle EJ, Philippi A, Timar L, Percy AK, Motil KJ, Lichtarge O, Smith EO, Glaze DG, Zoghbi HY (2000) Influence of mutation type and X chromosome inactivation on Rett syndrome phenotypes. Ann Neurol 47:670–679
3. Anzalone A, Lizardi-Ortiz JE, Ramos M, De MC, Hopf FW, Iaccarino C, Halbout B, Jacobsen J, Kinoshita C, Welter M, Caron MG, Bonci A, Sulzer D, Borrelli E (2012) Dual control of dopamine synthesis and release by presynaptic and postsynaptic dopamine D2 receptors. J Neurosci 32:9023–9034
4. Barmack NH, Qian Z, Yakhnittsa V (2010) Climbing fibers induce microRNA transcription in cerebellar Purkinje cells. Neuroscience 171(3):655–665
5. Burkett JP, Spiegel LL, Inoue K, Murphy AZ, Young LJ (2011) Activation of mu-opioid receptors in the dorsal striatum is necessary for adult social attachment in monogamous prairie voles. Neuropsychopharmacology 36:2200–2210
6. Canales JJ, Graybiel AM (2000) A measure of striatal function predicts motor stereotypy. Nat Neurosci 3:377–383
7. Chahrour M, Zoghbi HY (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron 56:422–437
8. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320:1224–1229
9. 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
10. Chen RZ, Akbarian S, Tudor M, Jaenisch R (2001) Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27:327–331
11. Chiron C, Bulteau C, Loc’h C, Raynaud C, Garreau B, Syrota A, Maziere B (1993) Dopaminergic D2 receptor SPECT imaging in Rett syndrome: increase of specific binding in striatum. J Nucl Med 34:1717–1721
12. Collin T, Chat M, Lucas MG, Moreno H, Racay P, Schwaller B, Marty A, Llano I (2005) Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling. J Neurosci 25:96–107
13. Crittenden JR, Graybiel AM (2011) Basal ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front Neuroanat 5:59
14. Deng JV, Rodriguiz RM, Hutchinson AN, Kim IH, Wetsel WC, West AE (2010) MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nat Neurosci 13:1128–1136
15. Di CG, Imperato A (1988) Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J Pharmacol Exp Ther 244:1067–1080
16. Dumas TC, Powers EC, Tarapore PE, Sapolsky RM (2004) Overexpression of calbindin D (28k) in dentate gyrus granule cells alters mossy fiber presynaptic function and impairs hippocampal-dependent memory. Hippocampus 14:701–709
17. Dunn HG, Stoessl AJ, Ho HH, MacLeod PM, Poskitt KJ, Doudet DJ, Schulzer M, Blackstock D, Dobko T, Koop B, de Amorim GV (2002) Rett syndrome: investigation of nine patients, including PET scan. Can J Neurol Sci 29:345–357
18. Enomoto H, Hendy GN, Andrews GK, Clemens TL (1992) Regulation of avian calbindin-D28K gene expression in primary chick kidney cells: importance of posttranscriptional mechanisms and calcium ion concentration. Endocrinology 130:3467–3474
19. Figueredo-Cardenas G, Harris CL, Anderson KD, Reiner A (1998) Relative resistance of striatal neurons containing calbindin or parvalbumin to quinolinic acid-mediated excitotoxicity compared to other striatal neuron types. Exp Neurol 149:356–372
20. Fujiyama F, Unzai T, Nakamura K, Nomura S, Kaneko T (2006) Difference in organization of corticostriatal and thalamostriatal synapses between patch and matrix compartments of rat neostriatum. Eur J Neurosci 24:2813–2824
21. Gantz SC, Ford CP, Neve KA, Williams JT (2011) Loss of Mecp2 in substantia nigra dopamine neurons compromises the nigrostriatal pathway. J Neurosci 31:12629–12637
22. 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. Biol Psychiatry 59:468–476
23. Gittis AH, Hang GB, LaDow ES, Shoenfeld LR, Atallah BV, Finkbeiner S, Kreitzer AC (2011) Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 71:858–868
24. Goffin D, Allen M, Zhang L, Amorim M, Wang IT, Reyes AR, Mercado-Berton A, Ong C, Cohen S, Hu L, Blendy JA, Carlson GC, Siegel SJ, Greenberg ME, Zhou Z (2012) Rett syndrome mutation MeCP2 T158A disrupts DNA binding, protein stability and ERP responses. Nat Neurosci 15:274–283
25. Graybiel AM (1984) Correspondence between the dopamine islands and striosomes of the mammalian striatum. Neuroscience 13:1157–1187
26. 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
27. Hagberg B, Aicardi J, Dias K, Ramos O (1983) A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett’s syndrome: report of 35 cases. Ann Neurol 14:471–479
28. Herkenham M, Pert CB (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 291:415–418
29. Hilario M, Holloway T, Jin X, Costa RM (2012) Different dorsal striatum circuits mediate action discrimination and action generalization. Eur J Neurosci 35:1105–1114
30. Hontanilla B, de las HS, Gimenez-Amaya JM (1996) A topographic re-evaluation of the nigrostriatal projections to the caudate nucleus in the cat with multiple retrograde tracers. Neuroscience 72:485–503
31. 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
32. Hwang CK, Song KY, Kim CS, Choi HS, Guo XH, Law PY, Wei LN, Loh HH (2009) Epigenetic programming of mu-opioid receptor gene in mouse brain is regulated by MeCP2 and Brg1 chromatin remodelling factor. J Cell Mol Med 13:3591–3615
33. Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488
34. Jouvenceau A, Potier B, Poindessous-Jazat F, Dutar P, Slama A, Epelbaum J, Billard JM (2002) Decrease in calbindin content significantly alters LTP but not NMDA receptor and calcium channel properties. Neuropharmacology 42:444–458
35. Jung MY, Hof PR, Schmauss C (2000) Targeted disruption of the dopamine D(2) and D(3) receptor genes leads to different alterations in the expression of striatal calbindin-D(28k). Neuroscience 97:495–504
36. Kimchi EY, Laubach M (2009) Dynamic encoding of action selection by the medial striatum. J Neurosci 29:3148–3159
37. Koos T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467–472
38. Kreitzer AC, Malenka RC (2008) Striatal plasticity and basal ganglia circuit function. Neuron 60:543–554
39. Lang M, Wither RG, Brotchie JM, Wu C, Zhang L, Eubanks JH (2013) Selective preservation of MeCP2 in catecholaminergic cells is sufficient to improve the behavioral phenotype of male and female Mecp2-deficient mice. Hum Mol Genet 22:358–371
40. Lawhorn C, Smith DM, Brown LL (2009) Partial ablation of mu-opioid receptor rich striosomes produces deficits on a motor-skill learning task. Neuroscience 163:109–119
41. Liao WL, Tsai HC, Wang HF, Chang J, Lu KM, Wu HL, Lee YC, Tsai TF, Takahashi H, Wagner M, Ghyselinck NB, Chambon P, Liu FC (2008) Modular patterning of structure and function of the striatum by retinoid receptor signaling. Proc Natl Acad Sci USA 105:6765–6770
42. Lindgren N, Xu ZQ, Herrera-Marschitz M, Haycock J, Hokfelt T, Fisone G (2001) Dopamine D(2) receptors regulate tyrosine hydroxylase activity and phosphorylation at Ser40 in rat striatum. Eur J Neurosci 13:773–780
43. Liu FC, Graybiel AM (1992) Transient calbindin-D28k-positive systems in the telencephalon: ganglionic eminence, developing striatum and cerebral cortex. J Neurosci 12:674–690
44. Miralves J, Magdeleine E, Joly E (2007) Design of an improved set of oligonucleotide primers for genotyping MeCP2tm1.1Bird KO mice by PCR. Mol Neurodegener 2:16
45. Miura M, Saino-Saito S, Masuda M, Kobayashi K, Aosaki T (2007) Compartment-specific modulation of GABAergic synaptic transmission by mu-opioid receptor in the mouse striatum with green fluorescent protein-expressing dopamine islands. J Neurosci 27:9721–9728
46. Moles A, Kieffer BL, D’Amato FR (2004) Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science 304:1983–1986
47. Moore AE, Cicchetti F, Hennen J, Isacson O (2001) Parkinsonian motor deficits are reflected by proportional A9/A10 dopamine neuron degeneration in the rat. Exp Neurol 172:363–376
48. Mosconi MW, Takarae Y, Sweeney JA (2011) Motor functioning and dyspraxia in autism spectrum disorders. In: Amaral DG, Dawson G, Geschwind DH (eds) Autism spectrum disorders. Oxford University Press Inc, New York, pp 355–380
49. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389
50. Pan PY, Ryan TA (2012) Calbindin controls release probability in ventral tegmental area dopamine neurons. Nat Neurosci 15:813–815
51. Panayotis N, Pratte M, Borges-Correia A, Ghata A, Villard L, Roux JC (2011) Morphological and functional alterations in the substantia nigra pars compacta of the Mecp2-null mouse. Neurobiol Dis 41:385–397
52. Paxinos and Franklin (2004) The mouse brain in stereotaxic coordinates. Compact second edition. Elsevier, London
53. Piepponen TP, Honkanen A, Kivastik T, Zharkovsky A, Turtia A, Mikkola JA, Ahtee L (1999) Involvement of opioid mu1-receptors in opioid-induced acceleration of striatal and limbic dopaminergic transmission. Pharmacol Biochem Behav 63:245–252
54. Reiss AL, Faruque F, Naidu S, Abrams M, Beaty T, Bryan RN, Moser H (1993) Neuroanatomy of Rett syndrome: a volumetric imaging study. Ann Neurol 34:227–234
55. Samaco RC, Mandel-Brehm C, Chao HT, Ward CS, Fyffe-Maricich SL, Ren J, Hyland K, Thaller C, Maricich SM, Humphreys P, Greer JJ, Percy A, Glaze DG, Zoghbi HY, Neul JL (2009) Loss of MeCP2 in aminergic neurons causes cell-autonomous defects in neurotransmitter synthesis and specific behavioral abnormalities. Proc Natl Acad Sci USA 106:21966–21971
56. Samaco RC, Mandel-Brehm C, McGraw CM, Shaw CA, McGill BE, Zoghbi HY (2012) Crh and Oprm1 mediate anxiety-related behavior and social approach in a mouse model of MECP2 duplication syndrome. Nat Genet 44:206–211
57. Schmidt H (2012) Three functional facets of calbindin D-28k. Front Mol Neurosci 5:25
58. Shahbazian MD, Antalffy B, Armstrong DL, Zoghbi HY (2002a) Insight into Rett syndrome: MeCP2 levels display tissue-and cell-specific differences and correlate with neuronal maturation. Hum Mol Genet 11:115–124
59. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, Armstrong D, Paylor R, Zoghbi H (2002b) Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35:243–254
60. 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
61. Sterling L, McLaughlin A, King BH (2011) Stereotypy and self-injury. In: Amaral DG, Dawson G, Geschwind DH (eds) Autism spectrum disorder. Oxford University Press Inc, New York, pp 339–354
62. Szulwach KE, Li X, Smrt RD, Li Y, Luo Y, Lin L, Santistevan NJ, Li W, Zhao X, Jin P (2010) Cross talk between microRNA and epigenetic regulation in adult neurogenesis. J Cell Biol 189(1):127–141
63. Temudo T, Ramos E, Dias K, Barbot C, Vieira JP, Moreira A, Calado E, Carrilho I, Oliveira G, Levy A, Fonseca M, Cabral A, Cabral P, Monteiro JP, Borges L, Gomes R, Santos M, Sequeiros J, Maciel P (2008) Movement disorders in Rett syndrome: an analysis of 60 patients with detected MECP2 mutation and correlation with mutation type. Mov Disord 23:1384–1390
64. Thorn CA, Atallah H, Howe M, Graybiel AM (2010) Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 66:781–795
65. Ungerstedt U, Herrera-Marschitz M, Stahle L, Tossman U, Zetterstrom T (1985) Functional classification of different dopamine receptors. Psychopharmacology Suppl 2:19–30
66. van der Kooy D, Fishell G (1992) Embryonic lesions of the substantia nigra prevent the patchy expression of opiate receptors, but not the segregation of patch and matrix compartment neurons, in the developing rat striatum. Brain Res Dev Brain Res 66:141–145
67. Wang Y, Dye CA, Sohal V, Long JE, Estrada RC, Roztocil T, Lufkin T, Deisseroth K, Baraban SC, Rubenstein JL (2010) Dlx5 and Dlx6 regulate the development of parvalbumin-expressing cortical interneurons. J Neurosci 30:5334–5345
68. Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N (2012) Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74:858–873
69. Wood L, Shepherd GM (2010) Synaptic circuit abnormalities of motor-frontal layer 2/3 pyramidal neurons in a mutant mouse model of Rett syndrome. Neurobiol Dis 38:281–287
70. 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. J Neurosci 29:12440–12448
71. Wu Y, Parent A (2000) Striatal interneurons expressing calretinin, parvalbumin or NADPH-diaphorase: a comparative study in the rat, monkey and human. Brain Res 863:182–191
72. Wu X, Fu Y, Knott G, Lu J, Di CG, Huang ZJ (2012) GABA signaling promotes synapse elimination and axon pruning in developing cortical inhibitory interneurons. J Neurosci 32:331–343
73. Yenari MA, Minami M, Sun GH, Meier TJ, Kunis DM, McLaughlin JR, Ho DY, Sapolsky RM, Steinberg GK (2001) Calbindin d28k overexpression protects striatal neurons from transient focal cerebral ischemia. Stroke 32:1028–1035
74. Yin HH, Mulcare SP, Hilario MR, Clouse E, Holloway T, Davis MI, Hansson AC, Lovinger DM, Costa RM (2009) Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci 12:333–341