Genetic disruption of Met signaling impairs GABAergic striatal development and cognition

Neuroscience

Volumn 176, Issue , 2011, Pages 199-209

  Martins, G J ^a,b   Shahrokh, M ^b   Powell, E M ^a,b  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

GABAergic interneuron; Hepatocyte growth factor; Met tyrosine kinase receptor; Morris water maze; Reversal learning; Striatum

Indexed keywords

SCATTER FACTOR RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR DLX6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN CELL; COGNITION; CONTROLLED STUDY; GABAERGIC SYSTEM; GENE DISRUPTION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE LOCATION; GENE MUTATION; GENETIC SUSCEPTIBILITY; GILLES DE LA TOURETTE SYNDROME; INTERNEURON; LEARNING; MALE; MAZE TEST; MEMORY CONSOLIDATION; MITOSIS; MOTOR PERFORMANCE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; SIGNAL TRANSDUCTION; TASK PERFORMANCE; TELENCEPHALON;

ANIMALS; BLOTTING, WESTERN; COGNITION; CORPUS STRIATUM; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION;

EID: 79851508020     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.12.058     Document Type: Article

References (65)

1. Anderson S.A., Marin O., Horn C., Jennings K., Rubenstein J.L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 2001, 128:353-363.
2. Balleine B.W., O'Doherty J.P. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 2010, 35:48-69.
3. Birchmeier C., Gherardi E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol 1998, 8:404-410.
4. Bissonette G.B., Bae M.H., Suresh T., Jaffe D.E., Powell E.M. Astrocyte-mediated hepatocyte growth factor/scatter factor supplementation restores GABAergic interneurons and corrects reversal learning deficits in mice. J Neurosci 2010, 30:2918-2923.
5. Bissonette G.B., Martins G.J., Franz T.M., Harper E.S., Schoenbaum G., Powell E.M. Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J Neurosci 2008, 28:11124-11130.
6. Bothe G.W.M., Bolivar V.J., Vedder M.J., Geistfeld J.G. Genetic and behavioral differences among five inbred mouse strains commonly used in the production of transgenic and knockout mice. Genes Brain Behav 2004, 3:149-157.
7. Brown V.J., Robbins T.W. Elementary processes of response selection mediated by distinct regions of the striatum. J Neurosci 1989, 9:3760-3765.
8. Calabresi P., de Murtas M., Bernardi G. The neostriatum beyond the motor function: experimental and clinical evidence. Neuroscience 1997, 78:39-60.
9. Campbell D.B., Li C., Sutcliffe J.S., Persico A.M., Levitt P. Genetic evidence implicating multiple genes in the MET receptor tyrosine kinase pathway in autism spectrum disorder. Autism Res 2008, 1:159-168.
10. Campbell D.B., Sutcliffe J.S., Ebert P.J., Militerni R., Bravaccio C., Trillo S., Elia M., Schneider C., Melmed R., Sacco R., Persico A.M., Levitt P. A genetic variant that disrupts MET transcription is associated with autism. Proc Natl Acad Sci U S A 2006, 103:16834-16839.
11. Chiu C.S., Brickley S., Jensen K., Southwell A., McKinney S., Cull-Candy S., Mody I., Lester H.A. GABA transporter deficiency causes tremor, ataxia, nervousness, and increased GABA-induced tonic conductance in cerebellum. J Neurosci 2005, 25:3234-3245.
12. Clarke H.F., Robbins T.W., Roberts A.C. Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. J Neurosci 2008, 28:10972-10982.
13. Colacicco G., Welzl H., Lipp H.P., Wurbel H. Attentional set-shifting in mice: modification of a rat paradigm, and evidence for strain-dependent variation. Behav Brain Res 2002, 132:95-102.
14. Crawley J.N. What's wrong with my mouse?: behavioral phenotyping of transgenic and knockout mice 2000, Wiley-Liss, New York, NY.
15. Crawley J.N. Behavioral phenotyping strategies for mutant mice. Neuron 2008, 57:809-818.
16. DeCoteau W., Hoang L., Huff L., Stone A., Kesner R. Effects of hippocampus and medial caudate nucleus lesions on memory for direction information in rats. Behav Neurosci 2004, 118:540-545.
17. Depino A.M., Tsetsenis T., Gross C. GABA homeostasis contributes to the developmental programming of anxiety-related behavior. Brain Res 2008, 1210:189-199.
18. Devan B.D., Goad E.H., Petri H.L. Dissociation of hippocampal and striatal contributions to spatial navigation in the water maze. Neurobiol Learn Mem 1996, 66:305-323.
19. Devan B.D., McDonald R.J., White N.M. Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: relation to thigmotaxis. Behav Brain Res 1999, 100:5-14.
20. Díaz-Anzaldúa A., Joober R., Rivière J.B., Dion Y., Lespérance P., Chouinard S., Richer F., Rouleau G.A. Association between 7q31 markers and Tourette syndrome. Am J Med Genet A 2004, 127A:17-20.
21. Gerfen C.R. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 1992, 15:133-139.
22. Holmes A., Wrenn C.C., Harris A.P., Thayer K.E., Crawley J.N. Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Genes Brain Behav 2002, 1:55-69.
23. Homanics G.E., Quinlan J.J., Firestone L.L. Pharmacologic and behavioral responses of inbred C57BL/6J and strain 129/SvJ mouse lines. Pharmacol Biochem Behav 1999, 63:21-26.
24. Huh C.G., Factor V.M., Sanchez A., Uchida K., Conner E.A., Thorgeirsson S.S. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci U S A 2004, 101:4477-4482.
25. Judson M.C., Bergman M.Y., Campbell D.B., Eagleson K.L., Levitt P. Dynamic gene and protein expression patterns of the autism-associated met receptor tyrosine kinase in the developing mouse forebrain. J Comp Neurol 2009, 513:511-531.
26. Kalanithi P.S.A., Zheng W., Kataoka Y., DiFiglia M., Grantz H., Saper C.B., Schwartz M.L., Leckman J.F., Vaccarino F.M. Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc Natl Acad Sci U S A 2005, 102:13307-13312.
27. Kataoka Y., Kalanithi P.S., Grantz H., Schwartz M.L., Saper C., Leckman J.F., Vaccarino F.M. Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome. J Comp Neurol 2010, 518:277-291.
28. Kawaguchi Y., Wilson C.J., Augood S.J., Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 1995, 18:527-535.
29. Kroisel P.M., Petek E., Emberger W., Windpassinger C., Wladika W., Wagner K. Candidate region for Gilles de la Tourette syndrome at 7q31. Am J Med Genet 2001, 101:259-261.
30. Leckman J.F., Vaccarino F.M., Kalanithi P.S.A., Rothenberger A. Annotation: Tourette syndrome: a relentless drumbeat-driven by misguided brain oscillations. J Child Psychol Psychiatry 2006, 47:537-550.
31. Levitt P., Eagleson K.L., Powell E.M. Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci 2004, 27:400-406.
32. Liu F.C., Graybiel A.M. Transient calbindin-D28k-positive systems in the telencephalon: ganglionic eminence, developing striatum and cerebral cortex. J Neurosci 1992, 12:674-690.
33. Lopez-Huerta V., Tecuapetla F., Guzman J., Bargas J., Galarraga E. Presynaptic modulation by somatostatin in the neostriatum. Neurochem Res 2008, 33:1452-1458.
34. Marin O., Rubenstein J.L.R. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2001, 2:780-790.
35. Marin O., Rubenstein J.L.R. Cell migration in the forebrain. Annu Rev Neurosci 2003, 26:441-483.
36. Marsh R., Alexander G.M., Packard M.G., Zhu H., Wingard J.C., Quackenbush G., Peterson B.S. Habit learning in Tourette syndrome: a translational neuroscience approach to a developmental psychopathology. Arch Gen Psychiatry 2004, 61:1259-1268.
37. Martins G.J., Plachez C., Powell E.M. Loss of embryonic Met signaling alters profiles of hippocampal interneurons. Dev Neurosci 2007, 29:143-158.
38. Mathis C., Paul S., Crawley J.N. Characterization of benzodiazepine-sensitive behaviors in the A/J and C57BL/6J inbred strains of mice. Behav Genet 1994, 24:171-180.
39. Moll G.H., Heinrich H., Trott G., Wirth S., Rothenberger A. Deficient intracortical inhibition in drug-naive children with attention-deficit hyperactivity disorder is enhanced by methylphenidate. Neurosci Lett 2000, 284:121-125.
40. Nery S., Fishell G., Corbin J.G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 2002, 5:1279-1287.
41. Packard M., Cahill L., McGaugh J. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc Natl Acad Sci U S A 1994, 91:8477-8481.
42. Packard M.G. Exhumed from thought: Basal ganglia and response learning in the plus-maze. Behav Brain Res 2009, 199:24-31.
43. Packard M.G., Knowlton B.J. Learning and memory functions of the basal ganglia. Annu Rev Neurosci 2002, 25:563-593.
44. Packard M.G., Teather L.A. Double dissociation of hippocampal and dorsal-striatal memory systems by posttraining intracerebral injections of 2-amino-5-phosphonopentanoic acid. Behav Neurosci 1997, 111:543-551.
45. Parent A., Hazrati L.N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Rev 1995, 20:91-127.
46. Partyka A., Kłodzińska A., Szewczyk B., Wierońska J., Chojnacka-Wójcik E., Librowski T., Filipek B., Nowak G., Pilc A. Effects of GABAB receptor ligands in rodent tests of anxiety-like behavior. Pharmacol Rep 2007, 59:757-762.
47. Paxinos G., Franklin K. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego, CA.
48. Pisa M., Cyr J. Regionally selective roles of the rat's striatum in modality-specific discrimination learning and forelimb reaching. Behav Brain Res 1990, 37:281-292.
49. Pisa M., Schranz J. Dissociable motor roles of the rat's striatum conform to a somatotopic model. Behav Neurosci 1988, 102:429-440.
50. Powell E.M., Campbell D.B., Stanwood G.D., Davis C., Noebels J.L., Levitt P. Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J Neurosci 2003, 23:622-631.
51. Powell E.M., Mars W.M., Levitt P. Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 2001, 30:79-89.
52. Reading P., Dunnett S.B., Robbins T. Dissociable roles of the ventral, medial and lateral striatum on the acquisition and performance of a complex visual stimulus-response habit. Behav Brain Res 1991, 45:147-161.
53. Rossato J.I., Zinn C.G., Furini C., Bevilaqua L.R.M., Medina J.H., Cammarota M., Izquierdo I. A link between the hippocampal and the striatal memory systems of the brain. An Acad Bras Ciênc 2006, 78:515-523.
54. Stenman J., Toresson H., Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 2003, 23:167-174.
55. Stern E.R., Blair C., Peterson B.S. Inhibitory deficits in Tourette's syndrome. Dev Psychobiol 2008, 50:9-18.
56. Teather L., Packard M.G., Smith D., Ellis-Behnke R., Bazan N. Differential induction of c-Jun and Fos-like proteins in rat hippocampus and dorsal striatum after training in two water maze tasks. Neurolbiol Learn Mem 2005, 84:75-84.
57. Van de Berg W., Kwaijtaal M., de Louw A., Lissone N., Schmitz C., Faull R., Blokland A., Blanco C., Steinbusch H. Impact of perinatal asphyxia on the GABAergic and locomotor system. Neuroscience 2003, 117:83-96.
58. Voelbel G.T., Bates M.E., Buckman J.F., Pandina G., Hendren R.L. Caudate nucleus volume and cognitive performance: are they related in childhood psychopathology?. Biol Psychiatry 2006, 60:942-950.
59. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006, 1:848-858.
60. Wahlsten D., Coopera S.F., Crabbe J.C. Different rankings of inbred mouse strains on the Morris maze and a refined 4-arm water escape task. Behav Brain Res 2005, 165:36-51.
61. Wahlsten D., Metten P., Phillips T.J., Boehm S.L., Burkhart-Kasch S., Dorow J., Doerksen S., Downing C., Fogarty J., Rodd-Henricks K., Hen R., McKinnon C.S., Merrill C.M., Nolte C., Schalomon M., Schlumbohm J.P., Sibert J.R., Wenger C.D., Dudek B.C., Crabbe J.C. Different data from different labs: Lessons from studies of gene-environment interaction. J Neurobiol 2003, 54:283-311.
62. Whishaw I.Q., Mittlemana G., Buncha S.T., Dunnett S.B. Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats. Behav Brain Res 1987, 24:125-138.
63. Wolff M., Savova M., Malleret G., Segu L., Buhot M.C. Differential learning abilities of 129T2/Sv and C57BL/6J mice as assessed in three water maze protocols. Behav Brain Res 2002, 136:463-474.
64. Wu Y., Parent A. Striatal interneurons expressing calretinin, parvalbumin or NADPH-diaphorase: a comparative study in the rat, monkey and human. Brain Res 2000, 863:182-191.
65. Ziemann U., Paulus W., Rothenberger A. Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 1997, 154:1277-1284.