Ephrin-A binding and EphA receptor expression delineate the matrix compartment of the striatum

Journal of Neuroscience

Volumn 19, Issue 12, 1999, Pages 4962-4971

  Janis, L Scott ^a   Cassidy, Robert M ^a   Kromer, Lawrence F ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Development; EphA4; EphA7; Matrix; Prosencephalon; Rat; Striosomes; Tyrosine kinase receptor

Indexed keywords

CELL SURFACE PROTEIN; PROTEIN TYROSINE KINASE;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELLULAR DISTRIBUTION; CORPUS STRIATUM; FEMALE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SENSORY NERVE;

EID: 0033564406     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-12-04962.1999     Document Type: Article

References (93)

1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
2. Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid and corticopetal components of substantia innominata. Neuroscience 27:1-39.
3. Arnauld E, Arsaut J, Tafani JA, Demotes-Mainard J (1995) Dopaminergic control of gene transcription during striatal ontogeny: c-fos induction by D1 receptor activation in the developing striosomes. Mol Brain Res 30:223-232.
4. Arvidsson U, Riedl M, Chakrabarti S, Lee J-H, Nakano AH, Dado RJ, Loh HH, Law P-Y, Wessendorf MW, Elde R (1995) Distribution and targeting of a μ-opioid receptor (MOR1) in brain and spinal cord. J Neurosci 15:3328-3341.
5. Becker N, Scitanidou T, Murphy P, Mattei MG, Topilko P, Nieto MA, Wilkinson DG, Charnay P, Gilardi-Hebenstreit P (1994) Several receptor tyrosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain. Mech Dev 47:3-17.
6. Berendse HW, Groenewegen HJ (1990) Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J Comp Neurol 299:187-228.
7. Bergemann AD, Cheng HJ, Brambilla R, Klein R, Flanagan JG (1995) ELF-2, a new member of the Eph ligand family, is segmentally expressed in mouse embryos in the region of the hindbrain and newly forming somites. Mol Cell Biol 15:4921-4929.
8. Bishop GA, Chang HT, Kitai ST (1982) Morphological and physiological properties of neostriatal neurons: an intracellular horseradish peroxidase study in the rat. Neuroscience 7:179-191.
9. Bruckner K, Pasquale EB, Klein R (1997) Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 275:1640-1643.
10. Carlsson M, Carlsson A (1990) Interactions between glutamatergic and monoaminergic systems within the basal ganglia - implication for schizophrenia and Parkinson's disease. Trends Neurosci 13:272-276.
11. Cassidy RM, Holst PL, Fox GM, Kromer LF (1996) Rek-4 receptor expression is developmentally regulated in the rodent forebrain. Soc Neurosci Abstr 22:1478.
12. Cheng H, Flanagan JG (1994) Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek4 and Sek receptor tyrosine kinases. Cell 79:157-168.
13. Cheng HJ, Nakamoto M, Bergemann AD, Flanagan JG (1995) Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82:371-381.
14. Ciossek T, Ullrich A (1997) Identification of Elf-1 and B61 as high affinity ligands for the receptor tyrosine kinase MDK1. Oncogene 14:35-43.
15. Davenport RW, Thies E, Zhou R, Nelson PG (1998) Cellular localization of ephrin-A2, ephrin-A5, and other functional guidance cues underlies retinotopic development across species. J Neurosci 18:975-986.
16. 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.
17. Delfs JM, Kong H, Mestek A, Chen Y, Yu L, Reisine T, Chesselet MF (1994) Expression of mu opioid receptor mRNA in rat brain: an in situ hybridization study at the single cell level. J Comp Neurol 345:46-68.
18. Desban M, Gauchy C, Kernel ML, Besson MJ, Glowinski J (1989) Three-dimensional organization of the striosomal compartment and patchy distribution of striatonigral projections in the matrix of the cat caudate nucleus. Neuroscience 29:551-566.
19. Desban M, Gauchy C, Glowinski J, Kernel ML (1995) Heterogeneous topographical distribution of the striatonigral and striatopallidal neurons in the matrix compartment of the cat caudate nucleus. J Comp Neurol 352:117-133.
20. Drescher U, Kremoser C, Handwerker C, Loschinger J, Noda M, Bonhoeffer F (1995) In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-370.
21. Durbin L, Brennan C, Shiomi K, Cooke J, Barrios A, Shanmugalingam S, Guthrie B, Lindberg R, Holder N (1998) Eph signaling is required for segmentation and differentiation of the somites. Genes Dev 12:3096-3109.
22. Eblen F, Graybiel AM (1995) Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J Neurosci 15:5999-6013.
23. Ellis C, Kasmi F, Ganju P, Walls E, Panayotou G, Reith AD (1996) A juxtamembrane autophosphorylation site in the Eph family receptor tyrosine kinase, Sek, mediates high affinity interaction with p59fyn. Oncogene 12:1727-1736.
24. Ellis J, Liu Q, Breitman M, Jenkins NA, Gilbert DJ, Copeland NG, Tempest HV, Warren S, Muir E, Schilling H, Fletcher FA, Ziegler SF, Rogers JH (1995) Embryo brain kinase: a novel gene of the eph/elk receptor tyrosine kinase family. Mech Dev 52:319-341.
25. Fishell G, van der Kooy D (1987) Pattern formation in the striatum: developmental changes in the distribution of striatonigral neurons. J Neurosci 7:1969-1978.
26. Flanagan JG, Vanderhaeghen P (1998) The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309-345.
27. Flenniken AM, Gale NW, Yancopoulos GD, Wilkinson DG (1996) Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis. Dev Biol 179:382-401.
28. Fox GM, Holst PL, Chute HT, Lindberg RA, Janssen AM, Basu R, Welcher AA (1995) cDNA cloning and tissue distribution of five human Eph-like receptor protein-tyrosine kinases. Oncogene 10:897-905.
29. Friedman GC, O'Leary D (1996) Eph receptor tyrosine kinases and their ligands in neural development. Curr Opin Neurobiol 6:127-133.
30. Fryer RH, Kaplan DR, Feinstein SC, Radeke MJ, Grayson DR, Kromer LF (1996) Developmental and mature expression of full-length and truncated trkB receptors in the rat forebrain. J Comp Neurol 374:21-40.
31. Gale MW, Yancopoulos GD (1997) Ephrins and their receptors: a repulsive topic? Cell Tissue Res 290:227-241.
32. Gale NW, Flenniken A, Compton DC, Jenkins N, Copeland NG, Gilbert DJ, Davis S, Wilkinson DG, Yancopoulos GD (1996a) Elk-L3, a novel transmembrane ligand for the Eph family of receptor tyrosine kinases, expressed in embryonic floor plate, roof plate and hindbrain segments. Oncogene 13:1343-1352.
33. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD (1996b) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9-19.
34. Gao PP, Zhang JH, Yokoyama M, Racey B, Dreyfus CF, Black IB, Zhou R (1996) Regulation of topographic projection in the brain: Elf-1 in the hippocamposeptal system. Proc Natl Acad Sci USA 93:11161-11166.
35. Gao PP, Yue Y, Zhang JH, Cerretti DP, Levitt P, Zhou R (1998) Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: implications in the development of thalamocortical projections. Proc Natl Acad Sci USA 95:5329-5334.
36. Gerfen CR (1984) The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311:461-464.
37. Gerfen CR (1989) The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246:385-388.
38. Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 15:285-320.
39. Gerfen CR, Herkenham M, Thibault J (1987) The neostriatal mosaic. II. Patch-and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 7:3915-3934.
40. Gilardi-Hebenstreit P, Nieto MA, Frain M, Mattei M-G, Chestier A, Wilkinson DG, Charnay P (1992) An Eph-related receptor protein tryosine kinase gene segmentally expressed in the developing mouse hindbrain. Oncogene 7:2499-2506.
41. Gimenez-Amaya JM, Graybiel AM (1991) Modular organization of projection neurons in the matrix compartment of the primate striatum. J Neurosci 11:779-791.
42. Goldman PS, Nauta WJ (1977) An intricately patterned prefrontocaudate projection in the rhesus monkey. J Comp Neurol 72:369-386.
43. Goldman-Rakic PS (1981) Prenatal formation of cortical input and development of cytoarchitectonic compartments in the neostriatum of the rhesus monkey. J Neurosci 1:721-735.
44. Graybiel AM (1984) Correspondence between the dopamine islands and striosomes of the mammalian striatum. Neuroscience 13:1157-1187.
45. Harris WA, Holt CE (1995) From tags to RAGS: chemoaffinity finally has receptors and ligands. Neuron 15:241-244.
46. Heimer L, Zahm DS, Alheid GF (1995) Basal ganglia. In: The rat nervous system (Paxinos G, ed), pp 579-628. San Diego: Academic.
47. Henkemeyer M, Marengere LEM, McGlade J, Olivier JP, Conlon RA, Holmyard DP, Letwin K, Pawson T (1994) Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene 9:1001-1014.
48. Herkenham M, Pert CB (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 291:415-418.
49. Holland SJ, Gale NW, Mbamalu G, Yancopoulos GD, Henkemeyer M, Pawson T (1996) Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 383:722-725.
50. Holland SJ, Gale NW, Gish GD, Roth RA, Songyang Z, Cantley LC, Henkemeyer M, Yancopoulos GD, Pawson T (1997) Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells. EMBO J 16:3877-3888.
51. Janis LS, Kromer LF (1997) Differential expression of Mek-4, an EphA3 tyrosine kinase receptor, in the developing rat CNS. Soc Neurosci Abstr 23:324.
52. Jimenez-Castellanos J, Graybiel AM (1989) Compartmental origins of striatal efferent projections in the cat. Neuroscience 32:297-321.
53. Kincaid AE, Wilson CJ (1996) Corticostriatal innervation of the patch and matrix in the rat neostriatum. J Comp Neurol 374:578-592.
54. Krull CE, Lansford R, Gale NW, Collazo A, Marcelle C, Yancopoulos GD, Fraser SE, Bronner-Fraser M (1997) Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Curr Biol 7:571-580.
55. Lanca AJ, Boyd S, Kolb BE, van der Kooy D (1986) The development of a patchy organization of the rat striatum. Dev Brain Res 27:1-10.
56. Loizou LA (1972) The postnatal ontogeny of monoamine-containing neurones in the central nervous system of the albino rat. Brain Res 40:395-418.
57. Maisonpierre PC, Barrequeta NX, Yancopoulos GD (1993) Ehk-1 and Ehk-2: two novel members of the Eph receptor-like tyrosine kinase family with distinctive structures and neuronal expression. Oncogene 8:3277-3288.
58. Malach R, Graybiel AM (1986) Mosaic architecture of the somatic sensory-recipient sector of the cat's striatum. J Neurosci 6:3436-3458.
59. Mansour A, Fox CA, Thompson RC, Akil H, Watson SJ (1994) μ-Opioid receptor mRNA expression in the rat CNS: comparison to μ-receptor binding. Brain Res 643:245-265.
60. Marsden CD (1981) The basal ganglia and the control of movement: motor activity and the outputs of the basal ganglia. Trends Neurosci 4:124-125.
61. Martone ME, Holash JA, Bayardo A, Pasquale EB, Ellisman MH (1997) Immunolocalization of the receptor tyrosine kinase EphA4 in the adult rat central nervous system. Brain Res 771:238-250.
62. Meima L, Kljavin IJ, Moran P, Shih A, Winslow JW, Caras IW (1997) AL-1-induced growth cone collapse of rat cortical neurons is correlated with Rek7 expression and rearrangement of actin cytoskeleton. Eur J Neurosci 9:177-188.
63. Monschau B, Kremoser C, Ohta K, Tanaka H, Kaneko T, Yamada T, Handwerker C, Hornberger MR, Loschinger J, Pasquale EB, Siever DA, Verderame MF, Muller BK, Bonhoeffer F, Drescher U (1997) Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. EMBO J 16:1258-1267.
64. Mori T, Wanaka A, Taguchi A, Matsumoto K, Tohyama M (1995a) Differential expressions of the eph family of receptor tyrosine kinase genes (sek, elk, eck) in the developing nervous system of the mouse. Mol Brain Res 29:325-335.
65. Mori T, Wanaka A, Taguchi A, Matsumoto K, Tohyama M (1995b) Localization of novel receptor tyrosine kinase genes of the eph family, MDK1 and its splicing variant, in the developing mouse nervous system. Mol Brain Res 34:154-160.
66. Murrin LC, Ferrer JR (1984) Ontogeny of the rat striatum: correspondence of dopamine terminals, opiate receptors and acetylcholinesterase. Neurosci Lett 47:155-160.
67. Murrin LC, Zeng WY (1989) Dopamine D1 receptor development in the rat striatum: early localization in striosomes. Brain Res 480:170-177.
68. Murrin LC, Zeng WY (1990) Ontogeny of dopamine D1 receptors in rat forebrain: a quantitative autoradiographic study. Dev Brain Res 57:7-13.
69. Nastuk MA, Graybiel AM (1985) Patterns of muscarinic cholinergic binding in the striatum and their relation to dopamine islands and striosomes. J Comp Neurol 237:176-194.
70. Nastuk MA, Graybiel AM (1988) Autoradiographic localization and biochemical characteristics of M1 and M2 muscarinic binding sites in the striatum of the cat, monkey, and human. J Neurosci 8:1052-1062.
71. Nieto MA, Gilardi-Hebenstreit P, Charnay P, Wilkinson DG (1992) A receptor protein tryosine kinase implicated in the segmental patterning of the hindbrain and mesoderm. Development 116:1137-1150.
72. Olson L, Seiger A, Fuxe K (1972) Heterogeneity of striatal and limbic dopamine innervation: highly fluorescent islands in developing and adult rats. Brain Res 44:283-288.
73. Parent A, Hazrati L-N (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-cortical loop. Brain Res Rev 20:91-127.
74. Park S, Sanchez MP (1997) The Eek receptor, a member of the Eph family of tyrosine protein kinases, can be activated by three different Eph family ligands. Oncogene 14:533-542.
75. Penney Jr JB, Young AB (1993) Speculation on the functional anatomy of basal ganglia disorders. Annu Rev Neurosci 6:73-94.
76. Penny GR, Wilson CJ, Kitai ST (1988) Relationship of the axonal and dendritic geometry of spiny projection neurons to the compartmental organization of the neostriatum. J Comp Neurol 269:275-289.
77. Ruiz JC, Roberston EJ (1994) The expression of the receptor-protein tyrosine kinase gene, eck, is highly restricted during early mouse development. Mech Dev 46:87-100.
78. Schoen SW, Graybiel AM (1992) 5′-Nucleotidase: a new marker for striosomal organization in the rat caudoputamen. J Comp Neurol 322:566-576.
79. Taneja R, Thisse B, Rijli FM, Thisse C, Bouillet P, Dolle P, Chambon P (1996) The expression pattern of the mouse receptor tyrosine kinase gene MDK1 is conserved through evolution and requires Hoxa-2 for rhombomere-specific expression in mouse embryos. Dev Biol 177:397-412.
80. Tessier-Lavigne M (1995) Eph receptor tyrosine kinases, axon repulsion, and the development of topographic maps. Cell 82:345-348.
81. van der Kooy D, Fishell G (1987) Neuronal birthdate underlies the development of striatal compartments. Brain Res 401:155-161.
82. Voorn P, Kalsbeek A, Jorritsma-Byham B, Groenewegen HJ (1988) The pre-and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striaturn of the rat. Neuroscience 25:857-887.
83. Walker RH, Arbuthnott GW, Baughman RW, Graybiel AM (1993) Dendritic domains of medium spiny neurons in the primate striatum: relationships to striosomal borders. J Comp Neurol 337:614-628.
84. 5-enkephalin in the patch compartment of the rat caudate-putamen nucleus. J Comp Neurol 375:659-674.
85. Wang HU, Anderson DJ (1997) Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18:383-396.
86. Wilson CJ, Groves PM (1980) Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular inject of horseradish peroxidase. J Comp Neurol 194:599-615.
87. Winning RS, Sargent TD (1994) Pagliaccio, a member of the Eph family of receptor tyrosine kinase genes, has localized expression in a subset of neural crest and neural tissues in Xenopus laevis embryos. Mech Dev 46:219-229.
88. Xu Q, Alldus G, Holder N, Wilkinson DG (1995) Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 121:4005-4016.
89. Zhang J, Pimenta AF, Levitt P, Zhou R (1997) Dynamic expression suggests multiple roles of the eph family receptor brain-specific kinase (Bsk) during mouse neurogenesis. Mol Brain Res 47:202-214.
90. Zhang JH, Cerretti DP, Yu T, Flanagan JG, Zhou R (1996) Detection of ligands in regions anatomically connected to neurons expressing the Eph receptor Bsk: potential roles in neuron-target interaction. J Neurosci 16:7182-7192.
91. Zhou R (1998) The Eph family receptors and ligands. Pharmacol Ther 77:151-181.
92. Zisch AH, Pasquale EB (1997) The Eph family: a multitude of receptors that mediate cell recognition signals. Cell Tissue Res 290:217-226.
93. Zisch AH, Kalo MS, Chong LD, Pasquale EB (1998) Complex formation between EphB2 and Src requires phosphorylation of tyrosine 611 in the EphB2 juxtamembrane region. Oncogene 16:2657-2670.