Engrailed2 modulates cerebellar granule neuron precursor proliferation, differentiation and insulin-like growth factor 1 signaling during postnatal development

Molecular Autism

Volumn 5, Issue 1, 2014, Pages

  Rossman, Ian T ^a,b,c   Lin, Lulu ^a   Morgan, Katherine M ^a,b   Digiovine, Marissa ^a,d   Van Buskirk, Elise K ^a,e   Kamdar, Silky ^a   Millonig, James H ^a,f   Dicicco Bloom, Emanuel ^a,b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e DUKE UNIVERSITY   (United States)

^f RUTGERS UNIVERSITY   (United States)

Author keywords

Autism; Cell cycle; Cerebellum; Engrailed2; IGF1; Neurodevelopment; Phospho S6 kinase; Proliferation

Indexed keywords

COMPLEMENTARY DNA; ENGRAILED 2 PROTEIN; FIBROBLAST GROWTH FACTOR 2; HOMEODOMAIN PROTEIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; S6 KINASE; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL CYCLE; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVATION; GENE OVEREXPRESSION; GENE SILENCING; GRANULE CELL; GRANULE NEURON PRECURSOR; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

EID: 84896730301     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/2040-2392-5-9     Document Type: Article

References (113)

1. Expression of the homeo box-containing gene En-2 delineates a specific region of the developing mouse brain. Davis CA, Noble-Topham SE, Rossant J, Joyner AL, Genes Dev 1988 2 361 371 10.1101/gad.2.3.361 2454212
2. Engrailed, Wnt and Pax genes regulate midbrain-hindbrain development. Joyner AL, Trends Genet 1996 12 15 20 10.1016/0168-9525(96)81383-7 8741855 (Pubitemid 26031160)
3. Neuroanatomic observations of the brain in autism: a review and future directions. Bauman ML, Kemper TL, Int J Dev Neurosci 2005 23 183 187 10.1016/j.ijdevneu.2004.09.006 15749244 (Pubitemid 40313551)
4. An MRI study of autism: the cerebellum revisited. Piven J, Saliba K, Bailey J, Arndt S, Neurology 1997 49 546 551 10.1212/WNL.49.2.546 9270594 (Pubitemid 27368899)
5. A comprehensive volumetric analysis of the cerebellum in children and adolescents with autism spectrum disorder. Scott JA, Schumann CM, Goodlin-Jones BL, Amaral DG, Autism Res 2009 2 246 257 10.1002/aur.97 19885834
6. Consensus paper: pathological role of the cerebellum in autism. Fatemi SH, Aldinger KA, Ashwood P, Bauman ML, Blaha CD, Blatt GJ, Chauhan A, Chauhan V, Dager SR, Dickson PE, et al. Cerebellum 2012 11 777 807 10.1007/s12311-012- 0355-9 22370873
7. Support for the homeobox transcription factor gene ENGRAILED 2 as an autism spectrum disorder susceptibility locus. Benayed R, Gharani N, Rossman I, Mancuso V, Lazar G, Kamdar S, Bruse SE, Tischfield S, Smith BJ, Zimmerman RA, et al. Am J Hum Genet 2005 77 851 868 10.1086/497705 16252243 (Pubitemid 41513285)
8. Heterogeneous association between Engrailed-2 and autism in the CPEA network. Brune CW, Korvatska E, Allen-Brady K, Cook EH Jr, Dawson G, Devlin B, Estes A, Hennelly M, Hyman SL, McMahon WM, et al. Am J Med Genet B Neuropsychiatr Genet 2008 147B 187 193 10.1002/ajmg.b.30585 17948868 (Pubitemid 351355279)
9. Association of the homeobox transcription factor, ENGRAILED 2, with autism spectrum disorder. Gharani N, Benayed R, Mancuso V, Brzustowicz LM, Millonig JH, Mol Psychiatry 2004 9 474 484 10.1038/sj.mp.4001498 15024396 (Pubitemid 38903503)
10. Family-based studies indicate association of Engrailed 2 gene with autism in an Indian population. Sen B, Singh AS, Sinha S, Chatterjee A, Ahmed S, Ghosh S, Usha R, Genes Brain Behav 2010 9 248 255 10.1111/j.1601-183X.2009.00556.x 20050924
11. Association of the ENGRAILED 2 (EN2) gene with autism in Chinese Han population. Wang L, Jia M, Yue W, Tang F, Qu M, Ruan Y, Lu T, Zhang H, Yan H, Liu J, et al. Am J Med Genet B Neuropsychiatr Genet 2008 147B 434 438 10.1002/ajmg.b.30623 17948901 (Pubitemid 351830799)
12. Intronic single nucleotide polymorphisms of engrailed homeobox 2 modulate the disease vulnerability of autism in a Han Chinese population. Yang P, Shu BC, Hallmayer JF, Lung FW, Neuropsychobiology 2010 62 104 115 10.1159/000315441 20523082
13. Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. Joyner AL, Herrup K, Auerbach BA, Davis CA, Rossant J, Science 1991 251 1239 1243 10.1126/science.1672471 1672471 (Pubitemid 21926222)
14. Abnormal embryonic cerebellar development and patterning of postnatal foliation in two mouse Engrailed-2 mutants. Millen KJ, Wurst W, Herrup K, Joyner AL, Development 1994 120 695 706 7909289 (Pubitemid 24071210)
15. A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. Millen KJ, Hui CC, Joyner AL, Development 1995 121 3935 3945 8575294 (Pubitemid 26007345)
16. Pattern deformities and cell loss in Engrailed-2 mutant mice suggest two separate patterning events during cerebellar development. Kuemerle B, Zanjani H, Joyner A, Herrup K, J Neurosci 1997 17 7881 7889 9315908 (Pubitemid 27426225)
17. Engrailed homeobox genes regulate establishment of the cerebellar afferent circuit map. Sillitoe RV, Vogel MW, Joyner AL, J Neurosci 2010 30 10015 10024 10.1523/JNEUROSCI.0653-10.2010 20668186
18. Ectopic overexpression of Engrailed-2 in cerebellar Purkinje cells causes restricted cell loss and retarded external germinal layer development at lobule junctions. Baader SL, Sanlioglu S, Berrebi AS, Parker-Thornburg J, Oberdick J, J Neurosci 1998 18 1763 1773 9465001 (Pubitemid 28103084)
19. Selective disruption of "late onset" sagittal banding patterns by ectopic expression of Engrailed-2 in cerebellar Purkinje cells. Baader SL, Vogel MW, Sanlioglu S, Zhang X, Oberdick J, J Neurosci 1999 19 5370 5379 10377347 (Pubitemid 29300203)
20. Engrailed-2 negatively regulates the onset of perinatal Purkinje cell differentiation. Jankowski J, Holst MI, Liebig C, Oberdick J, Baader SL, J Comp Neurol 2004 472 87 99 10.1002/cne.20059 15024754 (Pubitemid 38393309)
21. Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene Int-1 diverge during mouse development. Davis CA, Joyner AL, Genes Dev 1988 2 1736 1744 10.1101/gad.2.12b.1736 2907320
22. Spatially restricted and developmentally dynamic expression of engrailed genes in multiple cerebellar cell types. Wilson SL, Kalinovsky A, Orvis GD, Joyner AL, Cerebellum 2011 10 356 372 10.1007/s12311-011-0254-5 21431469
23. Quantitative analysis of cell proliferation and differentiation in the cortex of the postnatal mouse cerebellum. Fujita S, J Cell Biol 1967 32 277 287 10.1083/jcb.32.2.277 10976221
24. Heintz N, The GENSAT Project at Rockefeller University 2013 In http://www.gensat.org/index.html
25. Concordance for the syndrome of autism in 40 pairs of afflicted twins. Ritvo ER, Freeman BJ, Mason-Brothers A, Mo A, Ritvo AM, Am J Psychiatry 1985 142 74 77 4038442 (Pubitemid 15189523)
26. Infantile autism: a genetic study of 21 twin pairs. Folstein S, Rutter M, J Child Psychol Psychiatry 1977 18 297 321 10.1111/j.1469-7610.1977.tb00443.x 562353
27. 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)
28. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Deng W, Aimone JB, Gage FH, Nat Rev Neurosci 2010 11 339 350 10.1038/nrn2822 20354534
29. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Ming GL, Song H, Neuron 2011 70 687 702 10.1016/j.neuron.2011.05.001 21609825
30. Autism and abnormal development of brain connectivity. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ, J Neurosci 2004 24 9228 9231 10.1523/JNEUROSCI.3340-04.2004 15496656 (Pubitemid 39426157)
31. Brain structural abnormalities in young children with autism spectrum disorder. Sparks BF, Friedman SD, Shaw DW, Aylward EH, Echelard D, Artru AA, Maravilla KR, Giedd JN, Munson J, Dawson G, Dager SR, Neurology 2002 59 184 192 10.1212/WNL.59.2.184 12136055 (Pubitemid 34779175)
32. Functional and anatomical cortical underconnectivity in autism: evidence from an fMRI study of an executive function task and corpus callosum morphometry. Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ, Cereb Cortex 2007 17 951 961 16772313 (Pubitemid 46434636)
33. Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. McAlonan GM, Cheung V, Cheung C, Suckling J, Lam GY, Tai KS, Yip L, Murphy DG, Chua SE, Brain 2005 128 268 276 15548557 (Pubitemid 40222596)
34. Bridging the gap between MRI and postmortem research in autism. Schumann CM, Nordahl CW, Brain Res 2010 1380 175 186 20869352
35. Autism in tuberous sclerosis complex is related to both cortical and subcortical dysfunction. Asano E, Chugani DC, Muzik O, Behen M, Janisse J, Rothermel R, Mangner TJ, Chakraborty PK, Chugani HT, Neurology 2001 57 1269 1277 10.1212/WNL.57.7.1269 11591847 (Pubitemid 32947387)
36. Dating the development of human cerebellum. Friede RL, Acta Neuropathol 1973 23 48 58 10.1007/BF00689004 4698523
37. Neurogenesis in neonatal rat brain is regulated by peripheral injection of basic fibroblast growth factor (bFGF). Tao Y, Black IB, DiCicco-Bloom E, J Comp Neurol 1996 376 653 663 10.1002/(SICI)1096-9861(19961223)376:4<653::AID- CNE11>3.0.CO;2-N 8978476 (Pubitemid 27009846)
38. Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. Nicot A, Lelievre V, Tam J, Waschek JA, DiCicco-Bloom E, J Neurosci 2002 22 9244 9254 12417650 (Pubitemid 35356168)
39. Neuronal regulation of astroglial morphology and proliferation in vitro. Hatten ME, J Cell Biol 1985 100 384 396 10.1083/jcb.100.2.384 3881455 (Pubitemid 15173244)
40. Cerebellar granule cell neurogenesis is regulated by cell-cell interactions in vitro. Gao WO, Heintz N, Hatten ME, Neuron 1991 6 705 715 10.1016/0896-6273(91)90168-Y 2025426
41. Insulin-like growth factors cross the blood-brain barrier. Reinhardt RR, Bondy CA, Endocrinology 1994 135 1753 1761 7525251 (Pubitemid 24363863)
42. Neuroblast mitosis in dissociated culture: regulation and relationship to differentiation. DiCicco-Bloom E, Townes-Anderson E, Black IB, J Cell Biol 1990 110 2073 2086 10.1083/jcb.110.6.2073 2190991 (Pubitemid 20183165)
43. Vasoactive intestinal peptide regulates mitosis, differentiation and survival of cultured sympathetic neuroblasts. Pincus DW, DiCicco-Bloom EM, Black IB, Nature 1990 343 564 567 10.1038/343564a0 2300207 (Pubitemid 20042718)
44. Basic fibroblast growth factor exhibits dual and rapid regulation of cyclin D1 and p27 to stimulate proliferation of rat cerebral cortical precursors. Li B, DiCicco-Bloom E, Dev Neurosci 2004 26 197 207 10.1159/000082137 15711060 (Pubitemid 40867975)
45. DNAse I pre-treatment markedly enhances detection of nuclear cyclin-dependent kinase inhibitor p57Kip2 and BrdU double immunostaining in embryonic rat brain. Ye W, Mairet-Coello G, Dicicco-Bloom E, Histochem Cell Biol 2007 127 195 203 10.1007/s00418-006-0238-6 17024454 (Pubitemid 46147273)
46. Pituitary adenylate cyclase activating polypeptide anti-mitogenic signaling in cerebral cortical progenitors is regulated by p57Kip2-dependent CDK2 activity. Carey RG, Li B, DiCicco-Bloom E, J Neurosci 2002 22 1583 1591 11880488 (Pubitemid 35386277)
47. Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. Wagner JP, Black IB, DiCicco-Bloom E, J Neurosci 1999 19 6006 6016 10407038 (Pubitemid 29327934)
48. A single peripheral injection of basic fibroblast growth factor (bFGF) stimulates granule cell production and increases cerebellar growth in newborn rats. Cheng Y, Tao Y, Black IB, DiCicco-Bloom E, J Neurobiol 2001 46 220 229 10.1002/1097-4695(20010215)46:3<220::AID-NEU1004>3.0.CO;2-P 11169507 (Pubitemid 32105833)
49. Local control of granule cell generation by cerebellar Purkinje cells. Smeyne RJ, Chu T, Lewin A, Bian F, Sanlioglu S, Kunsch C, Lira SA, Oberdick J, Mol Cell Neurosci 1995 6 230 251 10.1006/mcne.1995.1019 7496629
50. Sonic hedgehog signaling is required for expansion of granule neuron precursors and patterning of the mouse cerebellum. Lewis PM, Gritli-Linde A, Smeyne R, Kottmann A, McMahon AP, Dev Biol 2004 270 393 410 10.1016/j.ydbio. 2004.03.007 15183722 (Pubitemid 38748561)
51. Pituitary adenylate cyclase-activating polypeptide promotes cell survival and neurite outgrowth in rat cerebellar neuroblasts. Gonzalez BJ, Basille M, Vaudry D, Fournier A, Vaudry H, Neuroscience 1997 78 419 430 10.1016/S0306-4522(96)00617-3 9145799 (Pubitemid 27170334)
52. Insulin-like growth factor I (IGF-I) is a critical trophic factor for developing cerebellar granule cells. Lin X, Bulleit RF, Brain Res 1997 99 234 242 10.1016/S0165-3806(97)00015-1 (Pubitemid 27151899)
53. Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurons through Smad5 signaling. Rios I, Alvarez-Rodriguez R, Marti E, Pons S, Development 2004 131 3159 3168 10.1242/dev.01188 15197161 (Pubitemid 39077439)
54. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Kenney AM, Cole MD, Rowitch DH, Development 2003 130 15 28 10.1242/dev.00182 12441288 (Pubitemid 36113940)
55. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Wallace VA, Curr Biol 1999 9 445 448 10226030 (Pubitemid 29205791)
56. The nature and regulation of the receptors for insulin-like growth factors. Rechler MM, Nissley SP, Annu Rev Physiol 1985 47 425 442 10.1146/annurev.ph.47.030185.002233 2986537 (Pubitemid 15142390)
57. Interactions of IGF-1 with the blood-brain barrier in vivo and in situ. Pan W, Kastin AJ, Neuroendocrinology 2000 72 171 178 10.1159/000054584 11025411
58. Cerebellar granule cells elaborate neurites before mitosis. Wolf E, Wagner JP, Black IB, DiCicco-Bloom E, Brain Res Dev Brain Res 1997 102 305 308 10.1016/S0165-3806(97)00111-9 9352115 (Pubitemid 27435952)
59. FGF inhibits neurite outgrowth over monolayers of astrocytes and fibroblasts expressing transfected cell adhesion molecules. Williams EJ, Mittal B, Walsh FS, Doherty P, J Cell Sci 1995 108 Pt 11 3523 3530 8586663
60. Signaling by insulin-like growth factor 1 in brain. Bondy CA, Cheng CM, Eur J Pharmacol 2004 490 25 31 10.1016/j.ejphar.2004.02.042 15094071 (Pubitemid 38482159)
61. PI3K/Akt-dependent regulation of the transcription factor myocyte enhancer factor-2 in insulin-like growth factor-1- and membrane depolarization-mediated survival of cerebellar granule neurons. Wiedmann M, Wang X, Tang X, Han M, Li M, Mao Z, J Neurosci Res 2005 81 226 234 10.1002/jnr.20556 15931671 (Pubitemid 41153336)
62. Inhibition of glycogen synthase kinase 3beta activity regulates proliferation of cultured cerebellar granule cells. Cui H, Meng Y, Bulleit RF, Dev Brain Res 1998 111 177 188 10.1016/S0165-3806(98)00136-9 (Pubitemid 28561724)
63. Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization- and insulin-like growth factor I-mediated survival of cerebellar granule cells. Miller TM, Tansey MG, Johnson EM Jr, Creedon DJ, J Biol Chem 1997 272 9847 9853 10.1074/jbc.272.15.9847 9092520 (Pubitemid 27171651)
64. Survival of cultured cerebellar granule neurons can be maintained by Akt-dependent and Akt-independent signaling pathways. Chin PC, D'Mello SR, Brain Res 2004 127 140 145 10.1016/j.molbrainres.2004.02.029 (Pubitemid 39078601)
65. In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: evidence that IGF-I increases proliferation of granule cell progenitors. Ye P, Xing Y, Dai Z, D'Ercole AJ, Brain Res 1996 95 44 54 10.1016/0165-3806(96)00492-0 (Pubitemid 26259821)
66. Insulin-like growth factor-I modulation of cerebellar cell populations is developmentally stage-dependent and mediated by specific intracellular pathways. Torres-Aleman I, Villalba M, Nieto-Bona MP, Neuroscience 1998 83 321 334 9460743 (Pubitemid 28062625)
67. Co-activation of the phosphatidylinositol-3-kinase/Akt signaling pathway by N-methyl-D-aspartate and TrkB receptors in cerebellar granule cell neurons. Zhu D, Lipsky RH, Marini AM, Amino Acids 2002 23 11 17 10.1007/s00726-001-0103-9 12373512
68. Activation of mitogen-activated protein kinase and p70S6 kinase is not correlated with cerebellar granule cell survival. Gunn-Moore FJ, Williams AG, Toms NJ, Tavare JM, Biochem J 1997 324 Pt 2 365 369 9182692 (Pubitemid 27267976)
69. The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. Shahbazian D, Roux PP, Mieulet V, Cohen MS, Raught B, Taunton J, Hershey JW, Blenis J, Pende M, Sonenberg N, EMBO J 2006 25 2781 2791 10.1038/sj.emboj.7601166 16763566 (Pubitemid 43980385)
70. Development of the olivocerebellar projection in the rat: I. Transient biochemical compartmentation of the inferior olive. Wassef M, Chedotal A, Cholley B, Thomasset M, Heizmann CW, Sotelo C, J Comp Neurol 1992 323 519 536 10.1002/cne.903230405 1430320
71. Development of the olivocerebellar projection in the rat: II. Matching of the developmental compartmentations of the cerebellum and inferior olive through the projection map. Wassef M, Cholley B, Heizmann CW, Sotelo C, J Comp Neurol 1992 323 537 550 10.1002/cne.903230406 1430321
72. Cloning and sequence comparison of the mouse, human, and chicken engrailed genes reveal potential functional domains and regulatory regions. Logan C, Hanks MC, Noble-Topham S, Nallainathan D, Provart NJ, Joyner AL, Dev Genet 1992 13 345 358 10.1002/dvg.1020130505 1363401 (Pubitemid 23061772)
73. Evaluation of cell proliferation in rat tissues with BrdU, PCNA, Ki-67(MIB-5) immunohistochemistry and in situ hybridization for histone mRNA. Muskhelishvili L, Latendresse JR, Kodell RL, Henderson EB, J Histochem Cytochem 2003 51 1681 1688 10.1177/002215540305101212 14623936 (Pubitemid 37475441)
74. Joint regulation of the MAP1B promoter by HNF3beta/Foxa2 and Engrailed is the result of a highly conserved mechanism for direct interaction of homeoproteins and Fox transcription factors. Foucher I, Montesinos ML, Volovitch M, Prochiantz A, Trembleau A, Development 2003 130 1867 1876 10.1242/dev.00414 12642491 (Pubitemid 36575913)
75. Neurotrophic activity of pituitary adenylate cyclase-activating polypeptide on rat cerebellar cortex during development. Vaudry D, Gonzalez BJ, Basille M, Fournier A, Vaudry H, Proc Natl Acad Sci USA 1999 96 9415 9420 10.1073/pnas.96.16.9415 10430957 (Pubitemid 29374769)
76. Cell intrinsic mechanisms regulate mouse cerebellar granule neuron differentiation. Lin X, Bulleit RF, Neurosci Lett 1996 220 81 84 10.1016/S0304-3940(96)13214-6 8981478 (Pubitemid 26426589)
77. PACAP type I receptor activation promotes cerebellar neuron survival through the cAMP/PKA signaling pathway. Kienlen Campard P, Crochemore C, Rene F, Monnier D, Koch B, Loeffler JP, DNA Cell Biol 1997 16 323 333 10.1089/dna.1997.16.323 9115641
78. Sonic hedgehog regulates the growth and patterning of the cerebellum. Dahmane N, Ruiz i Altaba A, Development 1999 126 3089 3100 10375501 (Pubitemid 29378174)
79. Insulin-like growth factor I (IGF-I) regulates IGF binding protein-5 gene expression in the brain. Ye P, D'Ercole J, Endocrinology 1998 139 65 71 9421399 (Pubitemid 28166292)
80. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J, Mol Cell Biol 2004 24 200 216 10.1128/MCB.24.1.200-216.2004 14673156 (Pubitemid 38010048)
81. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, et al. Cancer Res 2006 66 1500 1508 10.1158/0008-5472.CAN-05-2925 16452206 (Pubitemid 43259931)
82. Emx2 homeodomain transcription factor interacts with eukaryotic translation initiation factor 4E (eIF4E) in the axons of olfactory sensory neurons. Nedelec S, Foucher I, Brunet I, Bouillot C, Prochiantz A, Trembleau A, Proc Natl Acad Sci USA 2004 101 10815 10820 10.1073/pnas.0403824101 15247416 (Pubitemid 38955825)
83. Phosphorylation and activation of p70s6k by PDK1. Pullen N, Dennis PB, Andjelkovic M, Dufner A, Kozma SC, Hemmings BA, Thomas G, Science 1998 279 707 710 10.1126/science.279.5351.707 9445476 (Pubitemid 28144550)
84. Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. Tremblay F, Brule S, Hee Um S, Li Y, Masuda K, Roden M, Sun XJ, Krebs M, Polakiewicz RD, Thomas G, Marette A, Proc Natl Acad Sci USA 2007 104 14056 14061 10.1073/pnas.0706517104 17709744 (Pubitemid 350003334)
85. Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells. Alder J, Lee KJ, Jessell TM, Hatten ME, Nat Neurosci 1999 2 535 540 10.1038/9189 10448218 (Pubitemid 30491234)
86. Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma. Flora A, Klisch TJ, Schuster G, Zoghbi HY, Science 2009 326 1424 1427 10.1126/science.1181453 19965762
87. Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Corrales JD, Rocco GL, Blaess S, Guo Q, Joyner AL, Development 2004 131 5581 5590 10.1242/dev.01438 15496441 (Pubitemid 39625202)
88. Zic2 controls cerebellar development in cooperation with Zic1. Aruga J, Inoue T, Hoshino J, Mikoshiba K, J Neurosci 2002 22 218 225 11756505 (Pubitemid 34033499)
89. Immunolocalization of Zic2 expression in the developing mouse forebrain. Brown LY, Kottmann AH, Brown S, Gene Expr Patterns 2003 3 361 367 10.1016/S1567-133X(03)00043-7 12799086 (Pubitemid 36676006)
90. Reciprocal actions of ATF5 and Shh in proliferation of cerebellar granule neuron progenitor cells. Lee HY, Angelastro JM, Kenney AM, Mason CA, Greene LA, Dev Neurobiol 2012 72 789 804 10.1002/dneu.20979 22095825
91. RP58/ZNF238 directly modulates proneurogenic gene levels and is required for neuronal differentiation and brain expansion. Xiang C, Baubet V, Pal S, Holderbaum L, Tatard V, Jiang P, Davuluri RV, Dahmane N, Cell Death Differ 2012 19 692 702 10.1038/cdd.2011.144 22095278
92. ZNF238 is expressed in postmitotic brain cells and inhibits brain tumor growth. Tatard VM, Xiang C, Biegel JA, Dahmane N, Cancer Res 2010 70 1236 1246 10.1158/0008-5472.CAN-09-2249 20103640
93. Migration from a mitogenic niche promotes cell-cycle exit. Choi Y, Borghesani PR, Chan JA, Segal RA, J Neurosci 2005 25 10437 10445 10.1523/JNEUROSCI.1559-05.2005 16280582 (Pubitemid 41628447)
94. Evidence for a genetically encoded map of functional development in the cerebellum. Oberdick J, Histochemistry 1994 102 1 14 10.1007/BF00271044 7814265
95. Transverse zones in the vermis of the mouse cerebellum. Ozol K, Hayden JM, Oberdick J, Hawkes R, J Comp Neurol 1999 412 95 111 10.1002/(SICI)1096- 9861(19990913)412:1<95::AID-CNE7>3.0.CO;2-Y 10440712 (Pubitemid 29380327)
96. Engrailed homeobox genes determine the organization of Purkinje cell sagittal stripe gene expression in the adult cerebellum. Sillitoe RV, Stephen D, Lao Z, Joyner AL, J Neurosci 2008 28 12150 12162 10.1523/JNEUROSCI.2059-08.2008 19020009
97. Pontocerebellar axon guidance: neuropilin-1- and semaphorin 3A-sensitivity gradients across basilar pontine nuclei and semaphorin 3A variation across cerebellum. Solowska JM, Mazurek A, Weinberger L, Baird DH, Mol Cell Neurosci 2002 21 266 284 10.1006/mcne.2002.1187 12401447 (Pubitemid 35333816)
98. The compartmentalization of the cerebellum. Herrup K, Kuemerle B, Annu Rev Neurosci 1997 20 61 90 10.1146/annurev.neuro.20.1.61 9056708 (Pubitemid 27106376)
99. Autism-associated haplotype affects the regulation of the homeobox gene, ENGRAILED 2. Benayed R, Choi J, Matteson PG, Gharani N, Kamdar S, Brzustowicz LM, Millonig JH, Biol Psychiatry 2009 66 911 917 10.1016/j.biopsych.2009.05.027 19615670
100. Autism Associated Gene, ENGRAILED2, and Flanking Gene Levels Are Altered in Post-Mortem Cerebellum. Choi J, Ababon MR, Soliman M, Lin Y, Brzustowicz LM, Matteson PG, Millonig JH, PLoS One 2014 9 2 87208 doi: 10.1371/journal.pone. 0087208 10.1371/journal.pone.0087208 24520327
101. Neuroanatomy of autism. Amaral DG, Schumann CM, Nordahl CW, Trends Neurosci 2008 31 137 145 10.1016/j.tins.2007.12.005 18258309
102. Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2 years. Hazlett HC, Poe M, Gerig G, Smith RG, Provenzale J, Ross A, Gilmore J, Piven J, Arch Gen Psychiatry 2005 62 1366 1376 10.1001/archpsyc.62.12.1366 16330725 (Pubitemid 41746614)
103. Reduced cerebellar hemisphere size and its relationship to vermal hypoplasia in autism. Murakami JW, Courchesne E, Press GA, Yeung-Courchesne R, Hesselink JR, Arch Neurol 1989 46 689 694 10.1001/archneur.1989.00520420111032 2730382 (Pubitemid 19150951)
104. The cerebellum and neuropsychiatric disorders. Villanueva R, Psychiat Res 2012 198 527 532 10.1016/j.psychres.2012.02.023
105. Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG, Sahin M, Nature 2012 488 647 651 10.1038/nature11310 22763451
106. The role of the cerebellum in the pathophysiology and treatment of neuropsychiatric disorders: a review. Hoppenbrouwers SS, Schutter DJ, Fitzgerald PB, Chen R, Daskalakis ZJ, Brain Res Rev 2008 59 185 200 10.1016/j.brainresrev. 2008.07.005 18687358
107. Cerebrospinal fluid insulin-like growth factors IGF-1 and IGF-2 in infantile autism. Riikonen R, Makkonen I, Vanhala R, Turpeinen U, Kuikka J, Kokki H, Dev Med Child Neurol 2006 48 751 755 10.1017/S0012162206001605 16904022 (Pubitemid 44227167)
108. Altered mTOR signaling and enhanced CYFIP2 expression levels in subjects with fragile X syndrome. Hoeffer CA, Sanchez E, Hagerman RJ, Mu Y, Nguyen DV, Wong H, Whelan AM, Zukin RS, Klann E, Tassone F, Genes Brain Behav 2012 11 332 341 10.1111/j.1601-183X.2012.00768.x 22268788
109. Reduced AKT/mTOR signaling and protein synthesis dysregulation in a Rett syndrome animal model. Ricciardi S, Boggio EM, Grosso S, Lonetti G, Forlani G, Stefanelli G, Calcagno E, Morello N, Landsberger N, Biffo S, et al. Hum Mol Genet 2011 20 1182 1196 10.1093/hmg/ddq563 21212100
110. Equivalent benefit of mTORC1 blockade and combined PI3K-mTOR blockade in a mouse model of tuberous sclerosis. Pollizzi K, Malinowska-Kolodziej I, Stumm M, Lane H, Kwiatkowski D, Mol Cancer 2009 8 38 10.1186/1476-4598-8-38 19527517
111. Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice. Tropea D, Giacometti E, Wilson NR, Beard C, McCurry C, Fu DD, Flannery R, Jaenisch R, Sur M, Proc Natl Acad Sci USA 2009 106 2029 2034 10.1073/pnas.0812394106 19208815
112. Insulin-like growth factor-1 rescues synaptic and motor deficits in a mouse model of autism and developmental delay. Bozdagi O, Tavassoli T, Buxbaum JD, Molecular autism 2013 4 9 10.1186/2040-2392-4-9 23621888
113. Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Zoghbi HY, Bear MF, Cold Spring Harb Perspect Biol 2012 4 doi:10.1101/cshperspect.a009886