Rac1 and Rac3 GTPases control synergistically the development of cortical and hippocampal GABAergic interneurons

Cerebral Cortex

Volumn 24, Issue 5, 2014, Pages 1247-1258

  Vaghi, Valentina ^a   Pennucci, Roberta ^a   Talpo, Francesca ^b   Corbetta, Sara ^a   Montinaro, Valentina ^a   Barone, Cinzia ^a   Croci, Laura ^a   Spaiardi, Paolo ^b   Consalez, G Giacomo ^a   Biella, Gerardo ^b   De Curtis, Ivan ^a,c  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

cortex; GABAergic interneurons; hippocampus; neuronal migration; Rac GTPases

Indexed keywords

4 AMINOBUTYRIC ACID; GUANOSINE TRIPHOSPHATASE; PARVALBUMIN; RAC1 PROTEIN; RAC3 PROTEIN; UNCLASSIFIED DRUG; 3-(2-CARBOXYPIPERAZIN-4-YL)PROPYL-1-PHOSPHONIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOPYRIDINE; AMINO ACID RECEPTOR BLOCKING AGENT; BICUCULLINE; PIPERAZINE DERIVATIVE; POTASSIUM CHANNEL BLOCKING AGENT; RAC PROTEIN; RAC3 PROTEIN, MOUSE; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VIAAT PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; CELL COUNT; CELL MATURATION; CELL MOTILITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; INHIBITORY SYNAPSE; INTERNEURON; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; SYNAPSE; ANIMAL; CELL MOTION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; INHIBITORY POSTSYNAPTIC POTENTIAL; KNOCKOUT MOUSE; METABOLISM; NEWBORN; PHYSIOLOGY;

4-AMINOPYRIDINE; ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; CELL MOVEMENT; CEREBRAL CORTEX; EXCITATORY AMINO ACID ANTAGONISTS; GABA-A RECEPTOR ANTAGONISTS; GABAERGIC NEURONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MICE; MICE, KNOCKOUT; PIPERAZINES; POTASSIUM CHANNEL BLOCKERS; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84898911671     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs402     Document Type: Article

References (49)

1. Albertinazzi C, Gilardelli D, Paris S, Longhi R, de Curtis I. 1998. Over-expression of a neural-specific rho family GTPase, cRac1B, selectively induces enhanced neuritogenesis and neurite branching in primary neurons. J Cell Biol. 142:815-825.
2. Albertinazzi C, Za L, Paris S, de Curtis I. 2003. ADP-ribosylation factor 6 and a functional PIX/p95-APP1 complex are required for Rac1B-mediated neurite outgrowth. Mol Biol Cell. 14:1295-1307.
3. Alcantara S, de Lecea L, Del Rio JA, Ferrer I, Soriano E. 1996. Transient colocalization of parvalbumin and calbindin D28k in the postnatal cerebral cortex: evidence for a phenotypic shift in developing nonpyramidal neurons. Eur J Neurosci. 8:1329-1339.
4. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science. 278:474-476.
5. Anderson SA, Marín O, Horn C, Jennings K, Rubenstein JL. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development. 128:353-363.
6. Ang ES Jr, Haydar TF, Gluncic V, Rakic P. 2003. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J Neurosci. 23:5805-5815.
7. Batista-Brito R, Fishell G. 2009. The developmental integration of cortical interneurons into a functional network. Curr Top Dev Biol. 87:81-118.
8. Bolis A, Corbetta S, Cioce A, de Curtis I. 2003. Differential distribution of Rac1 and Rac3 GTPases in the developing mouse brain: implications for a role of Rac3 in Purkinje cell differentiation. Eur J Neurosci. 18:2417-2424.
9. Brooks-Kayal A. 2011. Molecular mechanisms of cognitive and behavioral comorbidities of epilepsy in children. Epilepsia. 52(Suppl. 1):13-20.
10. Chen L, Liao G, Waclaw RR, Burns KA, Linquist D, Campbell K, Zheng Y, Kuan CY. 2007. Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J Neurosci. 27:3884-3893.
11. Cobos I, Borello U, Rubenstein JL. 2007. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron. 54:873-888.
12. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL. 2005. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci. 8:1059-1068.
13. Corbetta S, Gualdoni S, Albertinazzi C, Paris S, Croci L, Consalez GG, de Curtis I. 2005. Generation and characterization of Rac3 knockout mice. Mol Cell Biol. 25:5763-5776.
14. Corbetta S, Gualdoni S, Ciceri G, Monari M, Zuccaro E, Tybulewicz VL, de Curtis I. 2009. Essential role of Rac1 and Rac3 GTPases in neuronal development. FASEB J. 23:1347-1357.
15. Danglot L, Triller A, Marty S. 2006. The development of hippocampal interneurons in rodents. Hippocampus. 16:1032-1060.
16. de Curtis I. 2008. Functions of Rac GTPases during neuronal development. Dev Neurosci. 30:47-58.
17. Flames N, Pla R, Gelman DM, Rubenstein JLR, Puelles L, Marín O. 2007. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci. 27:9682-9695.
18. Fogarty M, Grist M, Gelman D, Marín O, Pachnis V, Kessaris N. 2007. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J Neurosci. 27:10935-10946.
19. Gelman DM, Marín O. 2010. Generation of interneuron diversity in the mouse cerebral cortex. Eur J Neurosci. 31:2136-2141.
20. Grigoriou M, Tucker AS, Sharpe PT, Pachnis V. 1998. Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodo-main encoding genes, suggests a role in mammalian head development. Development. 125:2063-2074.
21. Haataja L, Groffen J, Heisterkamp N. 1997. Characterization of RAC3, a novel member of the Rho family. J Biol Chem. 272:20384-20388.
22. Hernández-Miranda LR, Parnavelas JG, Chiara F. 2010. Molecules and mechanisms involved in the generation and migration of cortical interneurons. ASN Neuro. 2:e00031.
23. Hevner RF, Daza RA, Englund C, Kohtz J, Fink A. 2004. Postnatal shifts of interneuron position in the neocortex of normal and reeler mice: evidence for inward radial migration. Neuroscience. 124:605-618.
24. Hoesche C, Sauerwald A, Veh RW, Krippl B, Kilimann MW. 1993. The 5′-flanking region of the rat synapsin I gene directs neuron-specific and developmentally regulated reporter gene expression in transgenic mice. J Biol Chem. 268:26494-26502.
25. Inan M, Welagen J, Anderson SA. 2012. Spatial and temporal bias in the mitotic origins of somatostatin-and parvalbumin-expressing interneuron subgroups and the chandelier subtype in the medial ganglionic eminence. Cereb Cortex. 22:820-827.
26. Lewis DA, Hashimoto T, Volk DW. 2005. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 6:312-324.
27. Malosio ML, Gilardelli D, Paris S, Albertinazzi C, de Curtis I. 1997. Differential expression of distinct members of Rho family GTP-binding proteins during neuronal development: identification of Rac1B, a new neural-specific member of the family. J Neurosci. 17:6717-6728.
28. Marín O. 2012. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci. 13:107-120.
29. Martini FJ, Valiente M, López-Bendito G, Szabó G, Moya F, Valdeol-millos M, Marín O. 2009. Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration. Development. 136:41-50.
30. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G. 2010. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci. 30:1582-1594.
31. Nadarajah B, Alifragis P, Wong RO, Parnavelas JG. 2002. Ventricle-directed migration in the developing cerebral cortex. Nat Neurosci. 5:218-224.
32. Orekhova EV, Stroganova TA, Nygren G, Tsetlin MM, Posikera IN, Gillberg C, Elam M. 2007. Excess of high frequency electroencephalogram oscillations in boys with autism. Biol Psychiatry. 62:1022-1029.
33. Pennucci R, Tavano S, Tonoli D, Gualdoni S, de Curtis I. 2011. Rac1 and Rac3 GTPases regulate the development of hilar mossy cells by affecting the migration of their precursors to the hilus. PLoS One. 6:e24819.
34. Pla R, Borrell V, Flames N, Marín O. 2006. Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J Neurosci. 26:6924-6934.
35. Schaeren-Wiemers N, Gerfin-Moser A. 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry. 100:431-440.
36. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 21:70-71.
37. Stoop R, Pralong E. 2000. Functional connections and epileptic spread between hippocampus, entorhinal cortex and amygdala in a modified horizontal slice preparation of the rat brain. Eur J Neurosci. 12:3651-3663.
38. Stühmer T, Puelles L, Ekker M, Rubenstein JL. 2002. Expression from a Dlx Gene Enhancer Marks Adult Mouse Cortical GABAergic neurons. Cereb Cortex. 12:75-85.
39. Tanaka DH, Maekawa K, Yanagawa Y, Obata K, Murakami F. 2006. Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex. Development. 133:2167-2176.
40. Tanaka DH, Nakajima K. 2012. Migratory pathways of GABAergic interneurons when they enter the neocortex. Eur J Neurosci. 35:1655-1660.
41. Tricoire L, Pelkey KA, Erkkila BE, Jeffries BW, Yuan X, McBain CJ. 2011. A blueprint for the spatiotemporal origins of mouse hippo-campal interneuron diversity. J Neurosci. 31:10948-10970.
42. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, Khazipov R. 2003. Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol. 90:2964-2972.
43. Velíšek L, Shang E, Velíšková J, Chachua T, Macchiarulo S, Maglakelidze G, Wolgemuth DJ, Greenberg DA. 2011. GABAergic neuron deficit as an idiopathic generalized epilepsy mechanism: the role of BRD2 hap-loinsufficiency in juvenile myoclonic epilepsy. PLoS One. 6:e23656.
44. Vidaki M, Tivodar S, Doulgeraki K, Tybulewicz V, Kessaris N, Pachnis V, Karagogeos D. 2012. Rac1-dependent cell cycle exit of MGE precursors and GABAergic interneuron migration to the cortex. Cereb Cortex. 22:680-692.
45. Walmsley MJ, Ooi SK, Reynolds LF, Smith SH, Ruf S, Mathiot A, Vanes L, Williams DA, Cancro MP, Tybulewicz VL. 2003. Critical roles for Rac1 and Rac2 GTPases in B cell development and signaling. Science. 302:459-462.
46. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat Rev Neurosci. 7:687-696.
47. Wonders CP, Taylor L, Welagen J, Mbata IC, Xiang JZ, Anderson SA. 2008. A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev Biol. 314: 127-136.
48. Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL. 2008. Distinct molecular pathways for development of telencepha-lic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol. 510:79-99.
49. Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, Rushing EJ, Marth JD, Parada LF. 2001. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev. 15:859-876.