Cortical interneurons require JNK1 to enter and navigate the developing cerebral cortex

Journal of Neuroscience

Volumn 34, Issue 23, 2014, Pages 7787-7801

  Myers, Abigail K ^a   Meechan, Daniel W ^b   Adney, Danielle R ^a   Tucker, Eric S ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Development; Forebrain; GABAergic interneuron; Intracellular signaling; Neuronal migration; Psychiatric disorder

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; COMPLEMENTARY DNA; MITOGEN ACTIVATED PROTEIN KINASE 9; STRESS ACTIVATED PROTEIN KINASE 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL FUNCTION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTERNEURON; MENTAL DISEASE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION;

DEVELOPMENT; FOREBRAIN; GABAERGIC INTERNEURON; INTRACELLULAR SIGNALING; NEURONAL MIGRATION; PSYCHIATRIC DISORDER;

ANIMALS; ANIMALS, NEWBORN; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASE 9; ORGAN CULTURE TECHNIQUES; PREGNANCY; TIME FACTORS;

EID: 84901752019     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4695-13.2014     Document Type: Article

References (58)

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. Bellion A, Baudoin JP, Alvarez C, Bornens M, Métin C (2005) Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J Neurosci 25:5691-5699. CrossRef Medline
3. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, Bhagwat SS, Manning AM, Anderson DW (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 98:13681-13686. CrossRef Medline
4. Carboni S, Hiver A, Szyndralewiez C, Gaillard P, Gotteland JP, Vitte PA (2004) AS601245 (1,3-benzothiazol-2-yl(2-{ 2-(3-pyridinyl)ethyl amino}-4 pyrimidinyl) acetonitrile): a c-Jun NH2-terminal protein kinase inhibitor with neuroprotective properties. J Pharmacol Exp Ther 310:25-32. CrossRef Medline
5. Das M, Jiang F, Sluss HK, Zhang C, Shokat KM, Flavell RA, Davis RJ (2007) Suppression of p53-dependent senescence by the JNK signal transduction pathway. Proc Natl Acad Sci U S A 104:15759-15764. CrossRef Medline
6. Dong C, Yang DD, Wysk M, Whitmarsh AJ, Davis RJ, Flavell RA (1998) Defective T cell differentiation in the absence of Jnk1. Science 282:2092-2095. CrossRef Medline
7. Faux C, Rakic S, Andrews W, Britto JM (2012) Neurons on the move: migration and lamination of cortical interneurons. Neurosignals 20:168-189. CrossRef Medline
8. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trzaskos JM (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623-18632. CrossRef Medline
9. Fine SE, Weissman A, Gerdes M, Pinto-Martin J, Zackai EH, McDonald-McGinn DM, Emanuel BS (2005) Autism spectrum disorders and symptoms in children with molecularly confirmed 22q11.2 deletion syndrome. J Autism Dev Disord 35:461-470. CrossRef Medline
10. 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
11. Friocourt G, Liu JS, Antypa M, Rakic S, Walsh CA, Parnavelas JG (2007) Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci 27:3875-3883. CrossRef Medline
12. Gdalyahu A, Ghosh I, Levy T, Sapir T, Sapoznik S, Fishler Y, Azoulai D, Reiner O (2004) DCX, a new mediator of the JNK pathway. EMBO J 23:823-832. CrossRef Medline
13. Godin JD, Thomas N, Laguesse S, Malinouskaya L, Close P, Malaise O, Purnelle A, Raineteau O, Campbell K, Fero M, Moonen G, Malgrange B, Chariot A, Metin C, Besson A, Nguyen L (2012) p27(Ki P1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration. Dev Cell 23:729-744. CrossRef Medline
14. Gopal PP, Simonet JC, Shapiro W, Golden JA (2010) Leading process branch instability in Lis1(+/-) nonradially migrating interneurons. Cereb Cortex 20:1497-1505. CrossRef Medline
15. Haeusgen W, Boehm R, Zhao Y, Herdegen T, Waetzig V (2009) Specific activities of individual c-jun n-terminal kinases in the brain. Neuroscience 161:951-959. CrossRef Medline
16. Hirai S, Cui de F, Miyata T, Ogawa M, Kiyonari H, Suda Y, Aizawa S, Banba Y, Ohno S (2006) The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J Neurosci 26:11992-12002. CrossRef Medline
17. Jin J, Suzuki H, Hirai S, Mikoshiba K, Ohshima T (2010) JNK phosphorylates Ser332 of doublecortin and regulates its function in neurite extension and neuronal migration. Dev Neurobiol 70:929-942. CrossRef Medline
18. Kappeler C, Saillour Y, Baudoin JP, Tuy FP, Alvarez C, Houbron C, Gaspar P, Hamard G, Chelly J, Métin C, Francis F (2006) Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum Mol Genet 15:1387-1400. CrossRef Medline
19. Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22:667-676. CrossRef Medline
20. Kunde SA, Rademacher N, Tzschach A, Wiedersberg E, Ullmann R, Kalscheuer VM, Shoichet SA (2013) Characterisation of de novo MAPK10/JNK3 truncation mutations associated with cognitive disorders in two unrelated patients. Hum Genet 132:461-471. CrossRef Medline
21. 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
22. Li G, Adesnik H, Li J, Long J, Nicoll RA, Rubenstein JL, Pleasure SJ (2008) Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J Neurosci 28:1085-1098. CrossRef Medline
23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402-408. CrossRef Medline
24. López-Bendito G, Sánchez-Alcañiz JA, Pla R, Borrell V, Picó E, Valdeolmillos M, Marín O (2008) Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J Neurosci 28: 1613-1624. CrossRef Medline
25. Marín O (2012) Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 13:107-120. CrossRef Medline
26. Marín O (2013) Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur J Neurosci 38:2019-2029. CrossRef Medline
27. Marín O, Yaron A, Bagri A, Tessier-Lavigne M, Rubenstein JL (2001) Sorting of striatal and cortical interneurons regulated by semaphorinneuropilin interactions. Science 293:872-875. CrossRef Medline
28. Martini FJ, Valiente M, López Bendito G, Szabó G, Moya F, Valdeolmillos M, Marín O (2009) Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration. Development 136:41-50. CrossRef Medline
29. Meechan DW, Tucker ES, Maynard TM, La Mantia AS (2009) Diminished dosage of 22q11 genes disrupts neurogenesis and cortical development in a mouse model of 22q11 deletion/Di George syndrome. Proc Natl Acad Sci U S A 106:16434-16445. CrossRef Medline
30. Meechan DW, Tucker ES, Maynard TM, La Mantia AS (2012) Cxcr4 regulation of interneuron migration is disrupted in 22q11.2 deletion syndrome. Proc Natl Acad Sci U S A 109:18601-18606. CrossRef Medline
31. 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. CrossRef Medline
32. Murphy KC, Jones LA, Owen MJ (1999) High rates of schizophrenia in adults with velo-cardio-facial syndrome. Arch Gen Psychiatry 56:940-945. Medline
33. Nery S, Fishell G, Corbin JG (2002) The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279-1287. CrossRef Medline
34. Niklasson L, Rasmussen P, Oskarsdóttir S, Gillberg C (2009) Autism, ADHD, mental retardation and behavior problems in 100 individuals with 22q11 deletion syndrome. Res Dev Disabil 30:763-773. CrossRef Medline
35. Polleux F, Ghosh A (2002) The slice overlay assay: a versatile tool to study the influence of extracellular signals on neuronal development. Sci STKE 2002:pl9-pl9. Medline
36. Polleux F, Whitford KL, Dijkhuizen PA, Vitalis T, Ghosh A (2002) Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129:3147-3160. Medline
37. 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
38. Pozas E, Ibáñez CF (2005) GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45:701-713. CrossRef Medline
39. Qu C, Li W, Shao Q, Dwyer T, Huang H, Yang T, Liu G (2013) c-Jun N-terminal kinase 1 (JNK1) is required for coordination of netrin signaling in axon guidance. J Biol Chem 288:1883-1895. CrossRef Medline
40. Sabapathy K, Jochum W, Hochedlinger K, Chang L, Karin M, Wagner EF (1999) Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech Dev 89:115-124. CrossRef Medline
41. Sánchez-Alcañiz JA, Haege S, Mueller W, Pla R, Mackay F, Schulz S, López-Bendito G, Stumm R, Marín O (2011) Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron 69:77-90. CrossRef Medline
42. Stenman J, Toresson H, Campbell K (2003) Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167-174. Medline
43. Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Höllt V, Schulz S (2003) CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 23:5123-5130. Medline
44. Stumm R, Kolodziej A, Schulz S, Kohtz JD, Höllt V (2007) Patterns of SDF-1 alpha and SDF-1 gamma m RNAs, migration pathways, and phenotypes of CXCR4-expressing neurons in the developing rat telencephalon. J Comp Neurol 502:382-399. CrossRef Medline
45. 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
46. Tahirovic S, Hellal F, Neukirchen D, Hindges R, Garvalov BK, Flynn KC, Stradal TE, Chrostek-Grashoff A, Brakebusch C, Bradke F (2010) Rac1 regulates neuronal polarization through the WAVE complex. J Neurosci 30:6930-6943. CrossRef Medline
47. Tiveron MC, Rossel M, Moepps B, Zhang YL, Seidenfaden R, Favor J, König N, Cremer H (2006) Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. J Neurosci 26:13273-13278. CrossRef Medline
48. Tivodar S, Kalemaki K, Kounoupa Z, Vidaki M, Theodorakis K, Denaxa M, Kessaris N, Decurtis I, Pachnis V, Karagogeos D (2014) Rac-GTPases regulate microtubule stability and axon growth of cortical GABAergic interneurons. Cereb Cortex. Advance online publication. doi:10.1093/ cercor/bhu037. CrossRef
49. Toritsuka M, Kimoto S, Muraki K, Landek-Salgado MA, Yoshida A, Yamamoto N, Horiuchi Y, Hiyama H, Tajinda K, Keni N, Illingworth E, Iwamoto T, Kishimoto T, Sawa A, Tanigaki K (2013) Deficits in micro RNA-mediated Cxcr4/Cxcl12 signaling in neurodevelopmental deficits in a 22q11 deletion syndrome mouse model. Proc Natl Acad Sci U S A 110:17552-17557. CrossRef Medline
50. Tucker ES, Polleux F, La Mantia AS (2006) Position and time specify the migration of a pioneering population of olfactory bulb interneurons. Dev Biol 297:387-401. CrossRef Medline
51. Wang X, Nadarajah B, Robinson AC, McColl BW, Jin JW, Dajas-Bailador F, Boot-Handford RP, Tournier C (2007) Targeted deletion of the mitogen-activated protein kinase kinase 4 gene in the nervous system causes severe brain developmental defects and premature death. Mol Cell Biol 27:7935-7946. CrossRef Medline
52. Wang Y, Li G, Stanco A, Long JE, Crawford D, Potter GB, Pleasure SJ, Behrens T, Rubenstein JL (2011) CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 69:61-76. CrossRef Medline
53. Westerlund N, Zdrojewska J, Padzik A, Komulainen E, Björkblom B, Rannikko E, Tararuk T, Garcia-Frigola C, Sandholm J, Nguyen L, Kallunki T, Courtney MJ, Coffey ET (2011) Phosphorylation of SCG10/stathmin-2 determines multipolar stage exit and neuronal migration rate. Nat Neurosci 14:305-313. CrossRef Medline
54. 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
55. Yamasaki T, Kawasaki H, Arakawa S, Shimizu K, Shimizu S, Reiner O, Okano H, Nishina S, Azuma N, Penninger JM, Katada T, Nishina H (2011) Stress-activated protein kinase MKK7 regulates axon elongation in the developing cerebral cortex. J Neurosci 31:16872-16883. CrossRef Medline
56. Yamasaki T, Kawasaki H, Nishina H (2012) Diverse roles of JNK and MKK pathways in the brain. J Signal Transduct 2012:459265-459265. CrossRef Medline
57. Yang DD, Conze D, Whitmarsh AJ, Barrett T, Davis RJ, Rincón M, Flavell RA (1998) Differentiation of CD4(+) T cells to Th1 cells requires MAP kinase JNK2. Immunity 9:575-585. CrossRef Medline
58. Yau HJ, Wang HF, Lai C, Liu FC (2003) Neural development of the neuregulin receptor Erb B4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tangentially migrating from the ganglionic eminences. Cereb Cortex 13:252-264. CrossRef Medline