CB1 Cannabinoid receptor-dependent activation of mTORC1/Pax6 signaling drives Tbr2 expression and basal progenitor expansion in the developing mouse cortex

Cerebral Cortex

Volumn 25, Issue 9, 2015, Pages 2395-2408

  Díaz Alonso, Javier ^a   Aguado, Tania ^a   De Salas Quiroga, Adán ^a   Ortega, Zaira ^a   Guzmán, Manuel ^a   Galve Roperh, Ismael ^a  

^a INSTITUTO RAMÓN Y CAJAL DE INVESTIGACIÓN SANITARIA IRYCIS   (Spain)

Author keywords

Basal progenitors; Cannabinoid; Corticogenesis; Eomes; MTORC1

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BROXURIDINE; CANNABINOID 1 RECEPTOR; DEXANABINOL; EOMESODERMIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; RIMONABANT; TRANSCRIPTION FACTOR PAX6; EOMES PROTEIN, MOUSE; EYE PROTEIN; HOMEODOMAIN PROTEIN; KI 67 ANTIGEN; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; NERVE PROTEIN; PAIRED BOX TRANSCRIPTION FACTOR; REPRESSOR PROTEIN; SMALL INTERFERING RNA; T BOX TRANSCRIPTION FACTOR; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL COUNT; CELL CYCLE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DRUG EFFECT; EMBRYO; EMBRYO DEVELOPMENT; GENE SILENCING; LUCIFERASE ASSAY; MOLECULAR BIOLOGY; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL CULTURE; SUBVENTRICULAR ZONE; TELENCEPHALON; ANIMAL; CELL CULTURE TECHNIQUE; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAMMALIAN EMBRYO; METABOLISM; MUTATION; NEWBORN; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CELL CULTURE TECHNIQUES; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; KI-67 ANTIGEN; MICE; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; MUTATION; NERVE TISSUE PROTEINS; ORGAN CULTURE TECHNIQUES; PAIRED BOX TRANSCRIPTION FACTORS; RECEPTOR, CANNABINOID, CB1; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STEM CELLS; T-BOX DOMAIN PROTEINS; TOR SERINE-THREONINE KINASES;

EID: 84973413819     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu039     Document Type: Article

References (58)

1. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman M, Galve-Roperh I. 2005. The endocannabinoid system drives neural progenitor proliferation. FASEB J. 19:1704-1706.
2. Aguado T, Romero E, Monory K, Palazuelos J, Sendtner M, Marsicano G, Lutz B, Guzman M, Galve-Roperh I. 2007. The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. J Biol Chem. 282:23892-23898.
3. Arnold SJ, Huang GJ, Cheung AF, Era T, Nishikawa S, Bikoff EK, Molnar Z, Robertson EJ, Groszer M. 2008. The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev. 22:2479-2484.
4. Asami M, Pilz GA, Ninkovic J, Godinho L, Schroeder T, Huttner WB, Gotz M. 2011. The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex. Development. 138:5067-5078.
5. Baala L, Briault S, Etchevers HC, Laumonnier F, Natiq A, Amiel J, Boddaert N, Picard C, Sbiti A, Asermouh A et al. 2007. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat Genet. 39:454-456.
6. Ben-Ari Y. 2008. Neuro-archaeology: pre-symptomatic architecture and signature of neurological disorders. Trends Neurosci. 31:626-636.
7. Berger J, Berger S, Tuoc TC, D'Amelio M, Cecconi F, Gorski JA, Jones KR, Gruss P, Stoykova A. 2007. Conditional activation of Pax6 in the developing cortex of transgenic mice causes progenitor apoptosis. Development. 134:1311-1322.
8. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, Monory K, Marsicano G, Matteoli M, Canty A et al. 2007. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science. 316:1212-1216.
9. Bromberg KD, Ma'ayan A, Neves SR, Iyengar R. 2008. Design logic of a cannabinoid receptor signaling network that triggers neurite outgrowth. Science. 320:903-909.
10. Castillo PE, Younts TJ, Chavez AE, Hashimotodani Y. 2012. Endocannabinoid signaling and synaptic function. Neuron. 76:70-81.
11. Cloetta D, Thomanetz V, Baranek C, Lustenberger RM, Lin S, Oliveri F, Atanasoski S, Ruegg MA. 2013. Inactivation of mTORC1 in the developing brain causes microcephaly and affects gliogenesis. J Neurosci. 33:7799-7810.
12. Crino PB 2011. mTOR: a pathogenic signaling pathway in developmental brain malformations. Trends Mol Med. 17:734-742.
13. Diaz-Alonso J, Aguado T, Wu CS, Palazuelos J, Hofmann C, Garcez P, Guillemot F, Lu HC, Lutz B, Guzman M et al. 2012. The CB1 cannabinoid receptor drives corticospinal motor neuron differentiation through the Ctip2/Satb2 transcriptional regulation axis. J Neurosci. 32:16651-16665.
14. Elsen GE, Hodge RD, Bedogni F, Daza RA, Nelson BR, Shiba N, Reiner SL, Hevner RF. 2013. The protomap is propagated to cortical plate neurons through an Eomes-dependent intermediate map. Proc Natl Acad Sci USA. 110:4081-4086.
15. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF. 2005. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci. 25:247-251.
16. Estivill-Torrus G, Pearson H, van Heyningen V, Price DJ, Rashbass P. 2002. Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development. 129:455-466.
17. Franco SJ, Gil-Sanz C, Martinez-Garay I, Espinosa A, Harkins-Perry SR, Ramos C, Muller U. 2012. Fate-restricted neural progenitors in the mammalian cerebral cortex. Science. 337:746-749.
18. Gal JS, Morozov YM, Ayoub AE, Chatterjee M, Rakic P, Haydar TF. 2006. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J Neurosci. 26:1045-1056.
19. Galve-Roperh I, Chiurchiu V, Diaz-Alonso J, Bari M, Guzman M, Maccarrone M. 2013. Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Progress Lipid Res. 52:633-650.
20. Ge S, Pradhan DA, Ming GL, Song H. 2007. GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci. 30:1-8.
21. Georgala PA, Manuel M, Price DJ. 2011. The generation of superficial cortical layers is regulated by levels of the transcription factor Pax6. Cereb Cortex. 21:81-94.
22. Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA. 2006. Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis. 44:611-621.
23. Goncalves MB, Suetterlin P, Yip P, Molina-Holgado F, Walker DJ, Oudin MJ, Zentar MP, Pollard S, Yanez-Munoz RJ, Williams G et al. 2008. A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol Cell Neurosci. 38:526-536.
24. Guillemot F, Molnar Z, Tarabykin V, Stoykova A. 2006. Molecular mechanisms of cortical differentiation. Eur J Neurosci. 23:857-868.
25. Han JM, Sahin M. 2011. TSC1/TSC2 signaling in the CNS. FEBS Lett. 585:973-980.
26. Hansen DV, Lui JH, Parker PR, Kriegstein AR. 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature. 464:554-561.
27. Harkany T, Guzman M, Galve-Roperh I, Berghuis P, Devi LA, Mackie K. 2007. The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol Sci. 28:83-92.
28. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL. 2001. Tbr1 regulates differentiation of the preplate and layer 6. Neuron. 29:353-366.
29. Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO, Childs J, Greenberg DA. 2004. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol. 66:204-208.
30. Jutras-Aswad D, DiNieri JA, Harkany T, Hurd YL. 2009. Neurobiological consequences of maternal cannabis on human fetal development and its neuropsychiatric outcome. Eur Arch Psychiatry Clin Neurosci. 259:395-412.
31. Kim S, Lehtinen MK, Sessa A, Zappaterra MW, Cho SH, Gonzalez D, Boggan B, Austin CA, Wijnholds J, Gambello MJ et al. 2010. The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron. 66:69-84.
32. Magri L, Cambiaghi M, Cominelli M, Alfaro-Cervello C, Cursi M, Pala M, Bulfone A, Garcia-Verdugo JM, Leocani L, Minicucci F et al. 2011. Sustained activation of mTOR pathway in embryonic neural stem cells leads to development of tuberous sclerosis complex-associated lesions. Cell Stem Cell. 9:447-462.
33. Marchalant Y, Brothers HM, Wenk GL. 2009. New neuron production can be increased in the hippocampus of aged rats following cannabinoid treatment. Mol Psychiatry. 14:1067, 1068-1069.
34. Mi D, Carr CB, Georgala PA, Huang YT, Manuel MN, Jeanes E, Niisato E, Sansom SN, Livesey FJ, Theil T et al. 2013. Pax6 exerts regional control of cortical progenitor proliferation via direct repression of Cdk6 and hypophosphorylation of pRb. Neuron. 78:269-284.
35. Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M et al. 2006. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron. 51:455-466.
36. Morozov YM, Dominguez MH, Varela L, Shanabrough M, Koch M, Horvath TL, Rakic P. 2013. Antibodies to cannabinoid type 1 receptor co-react with stomatin-like protein 2 in mouse brain mitochondria. Eur J Neurosci. 38:2341-2348.
37. Mulder J, Aguado T, Keimpema E, Barabas K, Ballester Rosado CJ, Nguyen L, Monory K, Marsicano G, Di Marzo V, Hurd YL et al. 2008. Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proc Natl Acad Sci USA. 105:8760-8765.
38. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 7:136-144.
39. Orlova KA, Tsai V, Baybis M, Heuer GG, Sisodiya S, Thom M, Strauss K, Aronica E, Storm PB, Crino PB. 2010. Early progenitor cell marker expression distinguishes type II from type I focal cortical dysplasias. J Neuropath Exp Neur. 69:850-863.
40. Osumi N, Shinohara H, Numayama-Tsuruta K, Maekawa M. 2008. Concise review: Pax6 transcription factor contributes to both embryonic and adult neurogenesis as a multifunctional regulator. Stem Cells. 26:1663-1672.
41. Palazuelos J, Ortega Z, Diaz-Alonso J, Guzman M, Galve-Roperh I. 2012. CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. J Biol Chem. 287:1198-1209.
42. Paliouras GN, Hamilton LK, Aumont A, Joppe SE, Barnabe-Heider F, Fernandes KJ. 2012. Mammalian target of rapamycin signaling is a key regulator of the transit-amplifying progenitor pool in the adult and aging forebrain. J Neurosci. 32:15012-15026.
43. Pinto L, Drechsel D, Schmid MT, Ninkovic J, Irmler M, Brill MS, Restani L, Gianfranceschi L, Cerri C, Weber SN et al. 2009. AP2gamma regulates basal progenitor fate in a region- and layer-specific manner in the developing cortex. Nat Neurosci. 12:1229-1237.
44. Puighermanal E, Marsicano G, Busquets-Garcia A, Lutz B, Maldonado R, Ozaita A. 2009. Cannabinoid modulation of hippocampal longterm memory is mediated by mTOR signaling. Nat Neurosci. 12:1152-1158.
45. Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, Bulfone A, Hevner RF, West JD, Price DJ. 2007. Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev Biol. 302:50-65.
46. Ramocki MB, Zoghbi HY. 2008. Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature. 455:912-918.
47. Saito T, Hanai S, Takashima S, Nakagawa E, Okazaki S, Inoue T, Miyata R, Hoshino K, Akashi T, Sasaki M et al. 2011. Neocortical layer formation of human developing brains and lissencephalies: consideration of layer-specific marker expression. Cereb Cortex. 21:588-596.
48. Sansom SN, Griffiths DS, Faedo A, Kleinjan DJ, Ruan Y, Smith J, van Heyningen V, Rubenstein JL, Livesey FJ. 2009. The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 5:e1000511.
49. Sessa A, Mao CA, Hadjantonakis AK, Klein WH, Broccoli V. 2008. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron. 60:56-69.
50. Sisodiya SM, Free SL, Williamson KA, Mitchell TN, Willis C, Stevens JM, Kendall BE, Shorvon SD, Hanson IM, Moore AT et al. 2001. PAX6 haploinsufficiency causes cerebral malformation and olfactory dysfunction in humans. Nat Genet. 28:214-216.
51. Trazzi S, Steger M, Mitrugno VM, Bartesaghi R, Ciani E. 2010. CB1 cannabinoid receptors increase neuronal precursor proliferation through AKT/glycogen synthase kinase-3beta/beta-catenin signaling. J Biol Chem. 285:10098-10109.
52. Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG, Sahin M. 2012. Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature. 488:647-651.
53. Tuoc TC, Radyushkin K, Tonchev AB, Pinon MC, Ashery-Padan R, Molnar Z, Davidoff MS, Stoykova A. 2009. Selective cortical layering abnormalities and behavioral deficits in cortex-specific Pax6 knockout mice. J Neurosci. 29:8335-8349.
54. Tuoc TC, Stoykova A. 2008. Trim11 modulates the function of neurogenic transcription factor Pax6 through ubiquitin-proteosome system. Genes Dev. 22:1972-1986.
55. Tyler WA, Haydar TF. 2013. Multiplex genetic fate mapping reveals a novel route of neocortical neurogenesis, which is altered in the Ts65Dn mouse model of Down syndrome. J Neurosci. 33:5106-5119.
56. Walcher T, Xie Q, Sun J, Irmler M, Beckers J, Ozturk T, Niessing D, Stoykova A, Cvekl A, Ninkovic J et al. 2013. Functional dissection of the paired domain of Pax6 reveals molecular mechanisms of coordinating neurogenesis and proliferation. Development. 140:1123-1136.
57. Warren N, Caric D, Pratt T, Clausen JA, Asavaritikrai P, Mason JO, Hill RE, Price DJ. 1999. The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex. Cereb Cortex. 9:627-635.
58. Zurolo E, Iyer AM, Spliet WG, Van Rijen PC, Troost D, Gorter JA, Aronica E. 2010. CB1 and CB2 cannabinoid receptor expression during development and in epileptogenic developmental pathologies. Neuroscience. 170:28-41.