Molecular mechanisms controlling the migration of striatal interneurons

Journal of Neuroscience

Volumn 35, Issue 23, 2015, Pages 8718-8729

  Villar Cerviño, Verona ^a   Kappeler, Caroline ^a   Nóbrega Pereira, Sandrina ^a,d   Henkemeyer, Mark ^b   Rago, Luciano ^a   Nieto, M Angela ^a   Marín, Oscar ^a,c  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF LISBON   (Portugal)

Author keywords

Eph; ErbB4; GABAergic; Interneuron; Migration; Striatum

Indexed keywords

BETA TUBULIN; EPHRIN RECEPTOR B1; EPIDERMAL GROWTH FACTOR RECEPTOR 4; MYOSIN HEAVY CHAIN ALPHA; NEU DIFFERENTIATION FACTOR; TATA BINDING PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR NKX2.2; EPHRIN RECEPTOR B3; ERBB4 PROTEIN, HUMAN; NUCLEAR PROTEIN; THYROID NUCLEAR FACTOR 1; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORPUS STRIATUM; DNA FOOTPRINTING; ELECTROPORATION; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; LUCIFERASE ASSAY; MALE; MEDIAN EMINENCE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL DIFFERENTIATION; CELL MOTION; CEREBELLUM CORTEX; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; IN VITRO STUDY; METABOLISM; MUTATION; NERVE TRACT; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TELENCEPHALON; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CELL MOVEMENT; CEREBELLAR CORTEX; CORPUS STRIATUM; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IN VITRO TECHNIQUES; INTERNEURONS; MICE; MICE, INBRED C57BL; MUTATION; NEURAL PATHWAYS; NUCLEAR PROTEINS; ORGAN CULTURE TECHNIQUES; RECEPTOR, EPHB1; RECEPTOR, EPHB3; RECEPTOR, ERBB-4; SIGNAL TRANSDUCTION; TELENCEPHALON; TRANSCRIPTION FACTORS;

EID: 84930911567     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4317-14.2015     Document Type: Article

References (45)

1. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476. CrossRef Medline
2. Backman M, Machon O, Mygland L, van den Bout CJ, Zhong W, TaketoMM, Krauss S (2005) Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev Biol 279:155-168. CrossRef Medline
3. Butt SJ, Sousa VH, Fuccillo MV, Hjerling-Leffler J, Miyoshi G, Kimura S, Fishell G (2008) The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59:722-732. CrossRef Medline
4. Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, Pawson T, Goldfarb M, Yancopoulos GD (1994) Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266:816-819. CrossRef Medline
5. De Felipe J, López-Cruz PL, Benavides-Piccione R, Bielza C, Larrañaga P, Anderson S, Burkhalter A, Cauli B, Fairén A, Feldmeyer D, Fishell G, Fitzpatrick D, Freund TF, González-Burgos G, Hestrin S, Hill S, Hof PR, Huang J, Jones EG, Kawaguchi, Y, et al. (2013) New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14:202-216. CrossRef Medline
6. Du T, Xu Q, Ocbina PJ, Anderson SA (2008) NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 135:1559 -1567. CrossRef Medline
7. Elenius K, Corfas G, Paul S, Choi CJ, Rio C, Plowman GD, Klagsbrun M (1997) A novel juxtamembrane domain isoform of HER4/ErbB4. Isoform-specific tissue distribution and differential processing in response to phorbol ester. J Biol Chem 272:26761-26768. CrossRef Medline
8. Elenius K, Choi CJ, Paul S, Santiestevan E, Nishi E, Klagsbrun M (1999) Characterization of a naturally occurring ErbB4 isoform that does not bind or activate phosphatidyl inositol 3-kinase. Oncogene 18:2607-2615. CrossRef Medline
9. Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C, Lai C, Rubenstein JL, Marín O (2004) Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44:251-261. CrossRef Medline
10. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marín O (2007) Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 27:9682-9695. CrossRef Medline
11. Flandin P, Kimura S, Rubenstein JL (2010) The progenitor zone of the ventral medial ganglionic eminence requires Nkx2-1 to generate most of the globus pallidus but few neocortical interneurons. J Neurosci 30:2812- 2823. CrossRef Medline
12. Fox IJ, Kornblum HI (2005) Developmental profile of ErbB receptors in murine central nervous system: implications for functional interactions. J Neurosci Res 79:584 -597. CrossRef Medline
13. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R, Lemke G (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378:390 -394. CrossRef Medline
14. Hadjantonakis AK, Macmaster S, Nagy A (2002) Embryonic stem cells and mice expressing different GFP variants for multiple noninvasive reporter usage within a single animal. BMC Biotechnol 2:11. CrossRef Medline
15. Hernández-Miranda LR, Cariboni A, Faux C, Ruhrberg C, Cho JH, Cloutier JF, Eickholt BJ, Parnavelas JG, Andrews WD (2011) Robo1 regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain. J Neurosci 31:6174-6187. CrossRef Medline
16. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923. Medline
17. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638 -2655. Medline
18. Kepecs A, Fishell G (2014) Interneuron cell types are fit to function. Nature 505:318 -326. CrossRef Medline
19. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881-7888. Medline
20. Lee BJ, Cho GJ, Norgren RB, Junier MP, Hill DF, Tapia V, Costa ME, Ojeda SR (2001) TTF-1, a homeodomain gene required for diencephalic morphogenesis, is postnatally expressed in the neuroendocrine brain in a developmentally regulated and cell-specific fashion. Mol Cell Neurosci 17:107-126. CrossRef Medline
21. Li L, Tasic B, Micheva KD, Ivanov VM, Spletter ML, Smith SJ, Luo L (2010) Visualizing the distribution of synapses from individual neurons in the mouse brain. PLoS One 5:e11503. CrossRef Medline
22. Liodis P, Denaxa M, Grigoriou M, Akufo-Addo C, Yanagawa Y, Pachnis V (2007) Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J Neurosci 27:3078 -3089. CrossRef Medline
23. Marín O (2013) Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur J Neurosci 38:2019 -2029. CrossRef Medline
24. Marín O, Anderson SA, Rubenstein JL (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063- 6076. Medline
25. Marín O, Yaron A, Bagri A, Tessier-Lavigne M, Rubenstein JL (2001) Sorting of striatal and cortical interneurons regulated by semaphorin/neuropilin interactions. Science 293:872- 875. CrossRef Medline
26. Marín O, Plump AS, Flames N, Sánchez-Camacho C, Tessier-Lavigne M, Rubenstein JL (2003) Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction. Development 130:1889 -1901. CrossRef Medline
27. Nóbrega-Pereira S, Kessaris N, Du T, Kimura S, Anderson SA, Marín O (2008) Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 59:733- 745. CrossRef Medline
28. Ovcharenko I, Nobrega MA, Loots GG, Stubbs L (2004) ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res 32:W280-286. CrossRef Medline
29. Passante L, Gaspard N, Degraeve M, Frisén J, Kullander K, De Maertelaer V, Vanderhaeghen P (2008) Temporal regulation of ephrin/Eph signaling is required for the spatial patterning of the mammalian striatum. Development 135:3281-3290. CrossRef Medline
30. Powell EM, Mars WM, Levitt P (2001) Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30:79-89. CrossRef Medline
31. Pozas E, Ibáñez CF (2005) GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45:701- 713. CrossRef Medline
32. Rakiæ S, Kanatani S, Hunt D, Faux C, Cariboni A, Chiara F, Khan S, Wansbury O, Howard B, Nakajima K, Nikoliæ M, Parnavelas JG (2015) Cdk5 Phosphorylation of ErbB4 is Required for Tangential Migration of Cortical Interneurons. Cereb Cortex 25:991-1003. CrossRef Medline
33. Rudolph J, Zimmer G, Steinecke A, Barchmann S, Bolz J (2010) Ephrins guide migrating cortical interneurons in the basal telencephalon. Cell Adh Migr 4:400-408. CrossRef Medline
34. Stein E, Lane AA, Cerretti DP, Schoecklmann HO, Schroff AD, Van Etten RL, Daniel TO (1998) Eph receptors discriminate specific ligand oligomers to determine alternative signaling complexes, attachment, and assembly responses. Genes Dev 12:667- 678. CrossRef Medline
35. Sussel L, Marin O, Kimura S, Rubenstein JL (1999) Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126:3359 -3370. Medline
36. Tidcombe H, Jackson-Fisher A, Mathers K, Stern DF, Gassmann M, Golding JP (2003) Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc Natl Acad Sci U S A 100:8281- 8286. CrossRef Medline
37. Villar-Cerviño V, Molano-Mazón M, Catchpole T, Valdeolmillos M, Henkemeyer M, Martínez LM, Borrell V, Marín O (2013) Contact repulsion controls the dispersion and final distribution of Cajal-Retzius cells. Neuron 77:457- 471. CrossRef Medline
38. Villasenor A, Marty-Santos L, Dravis C, Fletcher P, Henkemeyer M, Cleaver O (2012) EphB3 marks delaminating endocrine progenitor cells in the developing pancreas. Dev Dyn 241:1008 -1019. CrossRef Medline
39. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759- 3771. Medline
40. Wichterle H, Alvarez-DoladoM,Erskine L, Alvarez-BuyllaA (2003) Permissive corridor and diffusible gradients direct medial ganglionic eminence cell migration to the neocortex. Proc Natl Acad Sci U S A 100:727-732. CrossRef Medline
41. Xu Q, Tam M, Anderson SA (2008) Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J Comp Neurol 506:16 -29. CrossRef Medline
42. Yau HJ, Wang HF, Lai C, Liu FC (2003) Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tangentially migrating from the ganglionic eminences. Cereb Cortex 13:252-264. CrossRef Medline
43. Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL (2008) Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol 510:79 -99. CrossRef Medline
44. Zimmer G, Garcez P, Rudolph J, Niehage R, Weth F, Lent R, Bolz J (2008) Ephrin-A5 acts as a repulsive cue for migrating cortical interneurons. Eur J Neurosci 28:62-73. CrossRef Medline
45. Zimmer G, Rudolph J, Landmann J, Gerstmann K, Steinecke A, Gampe C, Bolz J (2011) Bidirectional ephrinB3/EphA4 signaling mediates the segregation of medial ganglionic eminence- and preoptic area-derived interneurons in the deep and superficial migratory stream. J Neurosci 31: 18364-18380. CrossRef Medline