Impairment of fragile X mental retardation protein-metabotropic glutamate receptor 5 signaling and its downstream cognates ras-related C3 botulinum toxin substrate 1, amyloid beta A4 precursor protein, striatal-enriched protein tyrosine phosphatase, and homer 1, in autism: A postmortem study in cerebellar vermis and superior frontal cortex

Molecular Autism

Volumn 4, Issue 1, 2013, Pages

  Fatemi, S Hossein ^a   Folsom, Timothy D ^a   Kneeland, Rachel E ^a   Yousefi, Mahtab K ^a   Liesch, Stephanie B ^a   Thuras, Paul D ^b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b VA MEDICAL CENTER   (United States)

Author keywords

Adults; APP; Autism; BA9; Cerebellar vermis; Children; Homer 1; RAC1; STEP

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ANTICONVULSIVE AGENT; BETA ACTIN; FRAGILE X MENTAL RETARDATION PROTEIN; METABOTROPIC RECEPTOR 5; PROTEIN HOMER 1; PROTEIN TYROSINE PHOSPHATASE; RAC1 PROTEIN; STRIATAL ENRICHED PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ARTICLE; AUTISM; CEREBELLUM VERMIS; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; HUMAN; MALE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHOOL CHILD; SUPERIOR FRONTAL CORTEX; WESTERN BLOTTING;

EID: 84879434002     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/2040-2392-4-21     Document Type: Article

References (104)

1. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders Washington, DC: APA Press 4 1994
2. Minicolumnar pathology in autism. Casanova MF, Buxhoeveden DP, Switala AE, Roy E, Neurology 2002 58 428 432 10.1212/WNL.58.3.428 11839843 (Pubitemid 34150918)
3. Neuropathological findings in autism. Palmen SJ, van Engeland H, Hof PR, Schmitz C, Brain 2004 127 2572 2583 10.1093/brain/awh287 15329353 (Pubitemid 39627367)
4. Macrocephaly and the control of brain growth in autistic disorders. McCaffrey P, Deutsch CK, Prog Neurobiol 2005 77 38 56 10.1016/j.pneurobio.2005. 10.005 16280193 (Pubitemid 41654772)
5. Prevalence of autism spectrum disorders-Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008. Autism and Developmental Disabilities Monitoring Network Surveillance Year 2008 Principal Investigators; Centers for Disease Control and Prevention, MMWR Surveill Summ 2012 61 1 19 23235338
6. Epilepsy in autism spectrum disorders. Canitano R, Eur Child Adolesc Psychiatry 2006 16 61 66 16932856 (Pubitemid 46648358)
7. Selective cognitive impairment during focal and generalized epileptiform EEG activity. Aarts JH, Binnie CD, Smit AM, Wilkins AJ, Brain 1984 107 293 308 10.1093/brain/107.1.293 6421454 (Pubitemid 14162914)
8. Cognitive impairment during epileptiform discharges: is it ever justifiable to treat the EEG? Binnie CD, Lancet Neurol 2003 2 725 730 10.1016/S1474-4422(03)00584-2 14636777 (Pubitemid 37443514)
9. Autism: many genes, common pathways? Geschwind DH, Cell 2008 135 391 395 10.1016/j.cell.2008.10.016 18984147
10. Advances in autism genetics: on the threshold of a new neurobiology. Abrahams BS, Geschwind DH, Nat Rev Genet 2008 9 341 355 10.1038/nrg2346 18414403 (Pubitemid 351556064)
11. Protein interactome reveals converging molecular pathways among autism disorders. Sakai Y, Shaw CA, Dawson BC, Dugas DV, Al-Mohtaseb Z, Hill DE, Zoghbi HY, Sci Transl Med 2011 3 86ra49 10.1126/scitranslmed.3002166 21653829
12. Identification of risk factors for autism spectrum disorders in tuberous sclerosis complex. Numis AL, Major P, Montenegro MA, Muzykewicz DA, Pulsifer MB, Thiele EA, Neurology 2011 76 981 987 10.1212/WNL.0b013e3182104347 21403110
13. FMR1 premutation and full mutation molecular mechanisms related to autism. Hagerman R, Au J, Hagerman P, J Neurodev Disord 2011 3 211 224 10.1007/s11689-011-9084-5 21617890
14. Methyl-CpG-binding protein 2 polymorphisms and vulnerability to autism. Loat CS, Curran S, Lewis CM, Duvall J, Geschwind D, Bolton P, Craig IW, Genes Brain Behav 2008 7 754 760 10.1111/j.1601-183X.2008.00414.x 19125863
15. Evaluation of autism traits in Angelman syndrome: a resource to unfold autism genes. Bonati MT, Russo S, Finelli P, Valsecchi MR, Cavalleri F, Roberts W, Elia M, Larizza L, Neurogenetics 2007 8 169 178 10.1007/s10048-007-0086-0 17415598 (Pubitemid 47051010)
16. Autistic behavior in children with Fragile X syndrome: prevalence, stability, and the impact of FMRP. Hatton DD, Sideris J, Skinner M, Mankowski J, Bailey DB Jr, Roberts J, Mirrett P, Am J Med Genet A 2006 140A 1804 1813 10.1002/ajmg.a.31286 16700053 (Pubitemid 44330644)
17. Autism spectrum disorder in fragile X syndrome: Communication, social interaction, and specific behaviors. Kauffman WE, Cortell R, Kau A, Bukelis I, Tierney E, Gray R, Cox C, Capone G, Stanard P, Am J Med Genet A 2004 129A 225 234 10.1002/ajmg.a.30229 15326621 (Pubitemid 39166187)
18. Learning-disabled males with a fragile X CGG expansion in the upper premutation size range. Hagerman RJ, Staley LW, O'Conner R, Lugenbeel K, Nelson D, McLean SD, Taylor A, Pediatrics 1996 97 122 126 8545206 (Pubitemid 26012623)
19. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Bassell GJ, Warren ST, Neuron 2008 60 201 214 10.1016/j.neuron.2008.10.004 18957214
20. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. 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, Cell 2011 146 247 261 10.1016/j.cell.2011.06.013 21784246
21. The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of a fragile X premutation. Devys D, Lutz Y, Rouyer N, Bellocq JP, Mandel JL, Nat Genet 1993 4 335 340 10.1038/ng0893-335 8401578 (Pubitemid 23231479)
22. Developmental expression of FMRP in the astrocyte lineage: implications for fragile X syndrome. Pacey LK, Doering LC, Glia 2007 55 1601 1609 10.1002/glia.20573 17823967 (Pubitemid 47556263)
23. Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Weiler IJ, Irwin SA, Klintsova AY, Spencer CM, Brazelton AD, Miyashiro K, Comery TA, Patel B, Eberwine J, Greenough WT, Proc Natl Acad Sci U S A 1997 94 5395 5400 10.1073/pnas.94.10.5395 9144248 (Pubitemid 27214794)
24. Immunocytochemical and biochemical characterization of FMRP, FXR1P, and FXR2P in the mouse. Bakker CE, de Diego OY, Bontekoe C, Raghoe P, Luteijn T, Hoogeveen AT, Oostra BA, Willemsen R, Exp Cell Res 2000 258 162 170 10.1006/excr.2000.4932 10912798 (Pubitemid 30461118)
25. The mGluR theory of fragile X syndrome. Krueger DD, Bear MF, Autism Spectrum Disorders New York: Oxford University Press, USA, Amaral DG, Dawson G, Geschwind DH, 2011 1239 1258
26. The mGluR theory of Fragile X mental retardation. Bear MF, Huber KM, Warren ST, Trends Neurosci 2004 27 370 377 10.1016/j.tins.2004.04.009 15219735 (Pubitemid 38829251)
27. Hippocampal pyramidal cells in adult Fmr1 knockout mice exhibit an immature-appearing profile of dendritic spines. Grossman AW, Elisseou NM, McKinney BC, Greenough WT, Brain Res 2006 1084 158 164 10.1016/j.brainres.2006. 02.044 16574084 (Pubitemid 44262070)
28. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Hutsler JJ, Zhang H, Brain Res 2010 1309 83 94 19896929
29. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Irwin SA, Patel B, Idupulapati M, Harris JB, Crisostomo RA, Larsen BP, Kooy F, Willems PJ, Cras P, Kozlowski PB, Swain RA, Weiler IJ, Greenough WT, Am J Med Genet 2001 98 161 171 10.1002/1096-8628(20010115)98:2<161::AID-AJMG1025>3.0. CO;2-B 11223852
30. Dysregulation of fragile X mental retardation protein and metabotropic glutamate receptor 5 in superior frontal cortex of subjects with autism: a postmortem brain study. Fatemi SH, Folsom TD, Mol Autism 2011 2 6 10.1186/2040-2392-2-6 21548960
31. Metabotropic glutamate receptor 5 upregulation in children with autism is associated with underexpression of both Fragile X mental retardation protein and GABA§ssub§A§esub§ receptor beta 3 in adults with autism. Fatemi SH, Folsom TD, Kneeland RE, Liesch SB, Anat Rec 2011 294 1635 1645 10.1002/ar.21299
32. GABA(A) Receptor downregulation in brains of subjects with autism. Fatemi SH, Reutiman TJ, Folsom TD, Thuras PD, J Autism Dev Disord 2009 39 223 230 10.1007/s10803-008-0646-7 18821008
33. Expression of GABA(B) receptors is altered in brains of subjects with autism. Fatemi SH, Folsom TD, Reutiman TJ, Thuras PD, Cerebellum 2009 8 64 69 10.1007/s12311-008-0075-3 19002745
34. mRNA and Protein levels for GABA(A) alpha 4, alpha 5, beta 1, and GABA(B)R1 receptors are altered in brains from subjects with autism. Fatemi SH, Reutiman TJ, Folsom TD, Rooney RJ, Patel DH, Thuras PD, J Autism Dev Disord 2010 40 743 750 10.1007/s10803-009-0924-z 20066485
35. A power primer. Cohen J, Psychol Bull 1992 112 155 159 19565683
36. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, Mill J, Cantor RM, Blencowe BJ, Geschwind DH, Nature 2011 474 380 384 10.1038/nature10110 21614001
37. GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. Bustelo XR, Sauzeau V, Berenjeno IM, Bioessays 2007 29 356 370 10.1002/bies.20558 17373658 (Pubitemid 46597867)
38. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Kaibuchi K, Kuroda S, Amano M, Annu Rev Biochem 1999 68 459 486 10.1146/annurev.biochem.68.1.459 10872457 (Pubitemid 29449200)
39. Essential role of Rac1 and Rac3 GTPases in neuronal development. Corbetta S, Gualdoni S, Ciceri G, Monari M, Zuccaro E, Tybulewicz VL, de Curtis I, FASEB J 2009 23 1347 1357 10.1096/fj.08-121574 19126596
40. Rho family GTPases and dendrite plasticity. Negishi M, Katoh H, Neuroscientist 2005 11 187 191 10.1177/1073858404268768 15911868 (Pubitemid 40686719)
41. Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility. Tashiro A, Yuste R, Mol Cell Neurosci 2004 26 429 440 10.1016/j.mcn.2004.04.001 15234347 (Pubitemid 38968436)
42. Rac1 induces the clustering of AMPA receptors during spinogenesis. Wiens KM, Lin H, Liao D, J Neurosci 2005 25 10627 10636 10.1523/JNEUROSCI.1947-05.2005 16291935 (Pubitemid 41681910)
43. Yuste R, Dendritic Spines Cambridge, MA: The MIT Press 2010
44. Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Billuart P, Bienvenu T, Ronce N, Des Portes V, Vinet MC, Zemni R, Roest Crollius H, Carrié A, Fauchereau F, Cherry M, Briault S, Hamel B, Fryns JP, Beldjord C, Kahn A, Moraine C, Chelly J, Nature 1998 392 923 926 10.1038/31940 9582072 (Pubitemid 28232063)
45. Excessive expression of synaptojanin in brains with Down syndrome. Arai Y, Ijuin T, Takenawa T, Becker LE, Takashima S, Brain Dev 2002 24 67 72 10.1016/S0387-7604(01)00405-3 11891094 (Pubitemid 34224905)
46. A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Schenck A, Bardoni B, Moro A, Bagni C, Mandel JL, Proc Natl Acad Sci U S A 2001 98 8844 8849 10.1073/pnas.151231598 11438699 (Pubitemid 32678115)
47. CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Schenck A, Bardoni B, Langmann C, Harden N, Mandel JL, Giangrande A, Neuron 2003 38 887 898 10.1016/S0896-6273(03) 00354-4 12818175 (Pubitemid 36782381)
48. FMRP interferes with the Rac1 pathway and controls actin cytoskeleton dynamics in murine fibroblasts. Castets M, Schaeffer C, Bechara E, Schenck A, Khandjian EW, Luche S, Moine H, Rabilloud T, Mandel JL, Bardoni B, Hum MolGenet 2005 14 835 844 (Pubitemid 40403279)
49. Modulation of dendritic spines and synaptic function by Rac1: A possible link to fragile X syndrome pathology. Bongmba OY, Martinez LA, Elhardt ME, Butler K, Tejada-Simon MV, Brain Res 2011 1399 79 95 21645877
50. Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Luo L, Hensch TK, Ackerman L, Barbel S, Jan LY, Jan YN, Nature 1996 379 837 840 10.1038/379837a0 8587609 (Pubitemid 26067727)
51. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. Nakayama AY, Harms MB, Luo L, J Neurosci 2000 20 5329 5338 10884317 (Pubitemid 30457730)
52. Astrocyte stellation, a process dependent on Rac1 is sustained by the regulated exocytosis of enlargeosomes. Racchetti G, D'Alessandro R, Meldolesi J, Glia 2012 60 465 475 10.1002/glia.22280 22144092
53. Hyaluronan-CD44 interaction stimulates Rac1 signaling and PKN gamma kinase activation leading to cytoskeleton function and cell migration in astrocytes. Bourguignon LY, Gilad E, Peyrollier K, Brightman A, Swanson RA, J Neurochem 2007 101 1002 1017 10.1111/j.1471-4159.2007.04485.x 17403031 (Pubitemid 46683879)
54. Glial fibrillary acidic protein is elevated in superior frontal, parietal and cerebellar cortices of autistic subjects. Laurence JA, Fatemi SH, Cerebellum 2005 4 201 210
55. High levels of Alzheimer beta-amyloid precursor protein (APP) in children with severely autistic behavior and aggression. Sokol DK, Chen D, Farlow MR, Dunn DW, Maloney B, Zimmer JA, Lahiri DK, J Child Neurol 2006 21 444 449 16948926 (Pubitemid 44069791)
56. Peripheral biomarkers in autism: Secreted amyloid precursor protein-alpha as a probable key player in early diagnosis. Bailey AR, Giunta BN, Obregon D, Nikolic WV, Tian J, Sanberg CD, Sutton DT, Tan J, Int J Clin Exp Med 2008 1 338 344 19079679
57. Increased secreted amyloid precursor protein-α (sAPPα) in severe autism: proposal of a specific, anabolic pathway and putative biomarker. Ray B, Long JM, Sokol DK, Lahiri DK, PLoS One 2011 6 20405 10.1371/journal.pone. 0020405 21731612
58. Autism, Alzheimer disease, and fragile X: APP, FMRP, and mGluR5 are molecular links. Sokol DK, Maloney B, Long JM, Ray B, Lahiri DK, Neurology 2011 76 344 1352
59. FMRP mediates mGluR5-dependent translation of amyloid precursor protein. Westmark CJ, Malter JS, PLoS Biol 2007 5 52 10.1371/journal.pbio.0050052 17298186 (Pubitemid 46422979)
60. Olanzapine and quetiapine protect PC12 cells from beta-amyloid peptide(25-35)-induced oxidative stress and the ensuing apoptosis. Wang H, Xu H, Dyck LE, Li XM, J Neurosci Res 2005 81 572 580 10.1002/jnr.20570 15948179 (Pubitemid 41297394)
61. Imipramine, in part through tumor necrosis factor alpha inhibition, prevents cognitive decline and beta-amyloid accumulation in a mouse model of Alzheimer's disease. Chavant F, Deguil J, Pain S, Ingrand I, Milin S, Fauconneau B, Pérault-Pochat MC, Lafay- Chebassier C, J Pharmacol Exp Ther 2010 332 505 514 10.1124/jpet.109.162164 19889791
62. Proteomic analysis of the presynaptic active zone. Volknandt W, Karas M, Exp Brain Res 2012 217 449 461 10.1007/s00221-012-3031-x 22354101
63. NMDA receptor/amyloid precursor protein interactions: a comparison between wild-type and amyloid precursor protein mutations associated with familial Alzheimer's disease. Innocent N, Cousins SL, Stephenson FA, Neurosci Lett 2012 515 131 136 10.1016/j.neulet.2012.03.029 22450047
64. Amyloid precursor protein 695 associates with assembled NR2A- and NR2B-containing NMDA receptors to result in the enhancement of their cell surface delivery. Cousins SL, Hoey SE, Stephenson FA, Perkinton MS, J Neurochem 2009 111 1501 1513 10.1111/j.1471-4159.2009.06424.x 19811606
65. The effects of amyloid precursor protein on postsynaptic composition and activity. Hoe HS, Fu Z, Makarova A, Lee JY, Lu C, Feng L, Pajoohesh-Ganji A, Matsuoka Y, Hyman BT, Ehlers MD, Vicini S, Pak DT, Rebeck GW, J Biol Chem 2009 284 8495 8506 19164281
66. Reversal of fragile X phenotypes by manipulation of AβPP/Aβ levels in Fmr1KO mice. Westmark CJ, Westmark PR, O'Riordan KJ, Ray BC, Hervey CM, Salamat MS, Abozeid SH, Stein KM, Stodola LA, Tranfaglia M, Burger C, Berry-Kravis EM, Malter JS, PLoS One 2011 6 26549 10.1371/journal.pone.0026549 22046307
67. Expression of APP pathway mRNAs and proteins in Alzheimer's disease. Matsui T, Ingelsson M, Fukumoto H, Ramasamy K, Kowa H, Frosch MP, Irizarry MC, Hyman BT, Brain Res 2007 1161 116 123 17586478 (Pubitemid 47068429)
68. Aberrant early-phase ERK inactivation impedes neuronal function in fragile X syndrome. Kim SH, Markham JA, Weiler IJ, Greenough WT, Proc Natl Acad Sci U S A 2008 105 4429 4434 10.1073/pnas.0800257105 18332424 (Pubitemid 351754397)
69. Compartmentalization of the MAPK scaffold protein KSR1 modulates synaptic plasticity in hippocampal neurons. Canal F, Palygin O, Pankratov Y, Corrêa SA, Müller J, FASEB 2011 25 2362 2372 10.1096/fj.10-173153
70. The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation. Zhang Y, Venkitaramani DV, Gladding CM, Zhang Y, Kurup P, Molnar E, Collingridge GL, Lombroso PJ, J Neurosci 2008 28 10561 10566 10.1523/JNEUROSCI.2666-08.2008 18923032
71. Identification of two alternatively spliced transcripts of STEP: a subfamily of brain-enriched protein tyrosine phosphatases. Sharma E, Zhao F, Bult A, Lambroso PJ, Brain Res Mol Brain Res 1995 32 87 93 10.1016/0169-328X(95) 00066-2 7494467
72. STEP: a family of brain-enriched PTPs. Alternative splicing produces transmembrane, cytosolic and truncated isoforms. Bult A, Zhao F, Dirkx R Jr, Raghunathan A, Solimena M, Lombroso PJ, Eur J Cell Biol 1997 72 337 344 9127733 (Pubitemid 27170630)
73. Genetic manipulation of STEP reverses behavioral abnormalities in a fragile X syndrome mouse model. Goebel-Goody SM, Wilson-Wallis ED, Royston S, Tagliatela SM, Naegele JR, Lombroso PJ, Genes Brain Behav 2012 11 586 600 10.1111/j.1601-183X.2012.00781.x 22405502
74. The Role of Striatal-Enriched Protein Tyrosine Phosphatase (STEP) in Cognition. Fitzpatrick CJ, Lombroso P, Front Neuroanat 2011 5 47 21863137
75. The tyrosine phosphatase STEP: implications in schizophrenia and the molecular mechanism underlying antipsychotic medications. Carty NC, Xu J, Kurup P, Brouillette J, Goebel-Goody SM, Austin DR, Yuan P, Chen G, Correa PR, Haroutunian V, Pittenger C, Lombroso PJ, Transl Psychiatry 2012 2 137 10.1038/tp.2012.63 22781170
76. Abeta-mediated NMDA receptor endocytosis in Alzheimer's disease involves ubiquitination of the tyrosine phosphatase STEP61. Kurup P, Zhang Y, Xu J, Venkitaramani DV, Haroutunian V, Greengard P, Nairn AC, Lombroso PJ, J Neurosci 2010 30 5948 5957 10.1523/JNEUROSCI.0157-10.2010 20427654
77. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Huber KM, Gallagher SM, Warren ST, Bear MF, Proc Acad Natl Sci U S A 2002 99 7746 7750 10.1073/pnas.122205699 (Pubitemid 34568762)
78. Genetic reduction of striatal-enriched tyrosine phosphatase (STEP) reverses cognitive and cellular deficits in an Alzheimer's disease mouse model. Zhang Y, Kurup P, Xu J, Carty N, Fernandez SM, Nygaard HB, Pittenger C, Greengard P, Strittmatter SM, Nairn AC, Lombroso PJ, Proc Natl Acad Sci U S A 2010 107 19014 19019 10.1073/pnas.1013543107 20956308
79. Expression of neuron specific phosphatase, striatal enriched phosphatase (STEP) in reactive astrocytes after transient forebrain ischemia. Hasegawa S, Morioka M, Goto S, Korematsu K, Okamura A, Yano S, Kai Y, Hamada JI, Ushio Y, Glia 2000 29 316 329 10.1002/(SICI)1098-1136(20000215)29:4<316::AID- GLIA3>3.0.CO;2-O 10652442 (Pubitemid 30121422)
80. STEP regulation of seizure thresholds in the hippocampus. Briggs SW, Walker J, Asik K, Lombroso P, Naegele J, Aaron G, Epilepsia 2011 52 497 506 10.1111/j.1528-1167.2010.02912.x 21204826
81. Homer binds a novel prolin-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K, Li M, Linden DJ, Worley PF, Neuron 1998 21 717 726 10.1016/S0896-6273(00)80589-9 9808459 (Pubitemid 28498781)
82. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density protein. Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, Aakalu VK, Lanahan AA, Sheng M, Worley PF, Neuron 1999 23 583 592 10.1016/S0896-6273(00)80810-7 10433269 (Pubitemid 29359928)
83. A reduced number of metabotropic glutamate subtype 5 receptors are associated with constitutive homer proteins in a mouse model of fragile X syndrome. Giuffrida R, Musumeci S, D'Antoni S, Bonaccorso CM, Giuffrida-Stella AM, Oostra BA, Catania MV, J Neurosci 2005 25 8908 8916 10.1523/JNEUROSCI.0932- 05.2005 16192381 (Pubitemid 41384459)
84. Homer-dependent cell surface expression of metabotropic glutamate receptor type 5 in neurons. Ango F, Robbe D, Muller T, Tu JC, Xiao B, Worley PF, Pin JP, Bockaert J, Fagni L, Mol Cell Neurosci 2002 20 323 329 10.1006/mcne.2002.1100 12093163 (Pubitemid 34762140)
85. Endogenous homer proteins regulate metabotropic glutamate receptor signaling in neurons. Kammermeier PJ, J Neurosci 2008 28 8560 8567 10.1523/JNEUROSCI.1830-08.2008 18716215
86. Receptor activation and Homer differentially control the lateral mobility of metabotropic glutamate receptor 5 in the neuronal membrane. Sergé A, Fourgeaud L, Hémar A, Choquet D, J Neurosci 2002 22 3910 3920 12019310 (Pubitemid 37465699)
87. Homer interactions are necessary for metabotropic glutamate receptor-induced long-term depression and translational activation. Ronesi JA, Huber KM, J Neurosci 2008 28 543 547 10.1523/JNEUROSCI.5019-07.2008 18184796
88. High-throughput sequencing of mGluR signaling pathway genes reveals enrichment of rare variants in autism. Kelleher RJ 3rd, Geigenmüller U, Hovhannisyan H, Trautman E, Pinard R, Rathmell B, Carpenter R, Margulies D, PLoS One 2012 7 35003 10.1371/journal.pone.0035003 22558107
89. Chronic treatment with lithium or valproate modulates the expression of Homer1b/c and its related genes Shank and Inositol 1,4,5-trisphosphate receptor. de Bartolomeis A, Tomasetti C, Cicale M, Yuan PX, Manji HK, Eur Neuropsychopharmacol 2012 22 527 535 10.1016/j.euroneuro.2011.11.006 22245542
90. Decreased GABA§ssub§A§esub§ receptor expression in the seizure-prone fragile X mouse. El Idrissi A, Ding XH, Scalia J, Trenkner E, Brown WT, Dobkin C, Neurosci Lett 2005 377 141 146 10.1016/j.neulet.2004.11.087 15755515 (Pubitemid 40332346)
91. Decreased expression of the GABA§ssub§A§esub§ receptor in fragile X syndrome. D'Hulst C, De Geest N, Reeve SP, Van Dam D, De Deyn PP, Hassan BA, Kooy RF, Brain Res 2006 1121 238 245 10.1016/j.brainres. 2006.08.115 17046729 (Pubitemid 44708899)
92. Expression profiling suggests underexpression of the GABAA receptor subunit delta in the fragile X knockout mouse model. Gantois I, Vandescompele J, Speleman F, Reyniers E, D'Hooge R, Severijnen LA, Willemsen R, Tassone F, Kooy RF, Neurobiol Dis 2006 21 346 357 10.1016/j.nbd.2005.07.017 16199166 (Pubitemid 43099858)
93. Downregulation of GABA(A) β subunits is transcriptionally controlled by Fmr1p. Hong A, Zhang A, Ke Y, El Idrissi A, Shen CH, J Mol Neurosci 2012 46 272 275 10.1007/s12031-011-9531-5 21547530
94. Dysregulation of Reelin and Bcl-2 proteins in autistic cerebellum. Fatemi SH, Stary JM, Halt AR, Realmuto GR, J Autism Dev Disord 2001 31 529 535 10.1023/A:1013234708757 11814262 (Pubitemid 37490147)
95. Reduced blood levels of reelin as a vulnerability factor in pathophysiology of autistic disorder. Fatemi SH, Stary JM, Egan EA, Cell Mol Neurobiol 2002 22 139 152 10.1023/A:1019857620251 12363196
96. Reelin signaling is impaired in autism. Fatemi SH, Snow AV, Stary JM, Araghi-Niknam M, Reutiman TJ, Lee S, Brooks AI, Pearce DA, Biol Psychiatry 2005 57 777 787 10.1016/j.biopsych.2004.12.018 15820235 (Pubitemid 40487922)
97. The role of fragile X mental retardation protein in major mental disorders. Fatemi SH, Folsom TD, Neuropharmacology 2012 60 1221 1226
98. The translation of translational control by FMRP: therapeutic targets for FXS. Darnell JC, Klann E, Nat Neurosci 2013 10.1038/nn.3379
99. Rescue of behavioral phenotype and neuronal protrusion morphology in Fmr1 KO mice. de Vrij FM, Levenga J, van der Linde HC, Koekkoek SK, De Zeeuw CI, Nelson DL, Oostra BA, Willemsen R, Neurobiol Dis 2008 31 127 132 10.1016/j.nbd.2008.04.002 18571098 (Pubitemid 351822560)
100. AFQ506, a new mGluR5 antagonist for treatment of fragile X syndrome. Levenga J, Hayashi S, de Vrij FM, Koekkoek SK, van der Linde HC, Nieuwenhuizen I, Song C, Buijsen RA, Pop AS, Gomezmancilla B, Nelson DL, Willemsen R, Gasparini F, Oostra BA, Trends Mol Med 2011 16 516 527
101. Chronic pharmacological mGlu5 inhibition corrects fragile X in adult mice. Michalon A, Sidorov M, Ballard TM, Ozmen L, Spooren W, Wettstein JG, Jaeschke G, Bear MF, Lindemann L, Neuron 2012 74 49 56 10.1016/j.neuron.2012.03. 009 22500629
102. Inhibitory effect of minocycline on amyloid beta fibril formation and human microglial activation. Familian A, Boshuizen RS, Eikelenboom P, Veerhuis R, Glia 2006 53 233 240 10.1002/glia.20268 16220550 (Pubitemid 43221345)
103. Minocycline inhibits neuronal death and glial activation induced by beta-amyloid peptide in rat hippocampus. Ryu JK, Franciosi S, Sattayaprasert P, Kim SU, McLarnon JG, Glia 2004 48 85 90 10.1002/glia.20051 15326618 (Pubitemid 39390851)
104. Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. Bilousova TV, Dansie L, Ngo M, Aye J, Charles JR, Ethell DW, Ethell IM, J Med Genet 2009 46 94 102 18835858 Development Development