Abstract
The present study examines the developmentally regulated expression pattern of an Ig superfamily member, KG-CAM, in the neostriatum of the rat. KG-CAM is a 90-kDa glycoprotein that is related to the DM-GRASP/Neurolin family of adhesion molecules. In the embryonic and early postnatal neostriatum, the distribution of KG-CAM correlates with the distribution of dopaminergic terminals. Early in neostriatal development, KG-CAM is found in the tyrosine hydroxylase-positive patches. In the maturing neostriatum, the levels of KG-CAM remain high within the patches, and KG-CAM upregulates in the matrix compartment. As the neostriatum is reaching its adult morphology, 5 weeks postnatal, the expression of KG-CAM in the matrix is approximately equal to that of the patches. When the distribution of KG-CAM is examined at the ultrastructural level, the immunoreactivity is localized to the external surface of neuronal and glial profiles in the neuropil. KG-CAM does not appear to be associated with the guidance of dopaminergic axons from the substantia nigra to the striatum, for this pathway is not immunopositive for this member of the Ig superfamily. The present study identifies an Ig superfamily member, KG-CAM, that appears to play a major role in the development of the neostriatum. Furthermore, the high levels of KG-CAM in the adult neostriatum suggest that this Ig superfamily member may be involved in maintaining the integrity of this structure in the adult rat.
Similar content being viewed by others
References
Albelda SM, Buck CA (1990) Integrins and other cell adhesion molecules. FASEB J 4:2868–2880
Beckstead RM (1985) Complementary mosaic distributions of thalamic and nigral axons in the caudate nucleus of the cat: double anterograde labeling combining autoradiography and wheat germ-HRP histochemistry. Brain Res 335:153–159
Boylan MK, Levine MS, Buchwald NA, Fisher RS (1990) Patterns of tachykinin expression and localization in developing feline neostriatum. J Comp Neurol 293:151–163
Burns FR, Kannen S von, Guy L, Raper JA, Kamholz J, Chang S (1991) DM-GRASP, a novel immunoglobulin superfamily axonal surface protein that supports neurite extension. Neuron 7:209–220
Caboche J, Rogard M, Besson MJ (1991) Comparative development of Dl-dopamine and mu opiate receptors in normal and in 6-hydroxydopamine-lesioned neonatal rat striatum: dopaminergic fibers regulate mu but not Dl receptor distribution. Dev Brain Res 58:111–122
Chun JJM, Shatz CJ (1988) A fibronectin-like molecule is present in the developing cat cerebral cortex and is correlated with subplate neurons. J Cell Biol 106:857–872
Chuong C-M, Crossin KL, Edelman GM (1987) Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers. J Cell Biol 104:331–342
Crossin KL, Hoffman S, Tan SS, Edelman GM (1989) Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse. Dev Biol 136:381–392
Dodd J, Jessell TM (1988) Axon guidance and the patterning of neuronal projections in vertebrates. Science 242:692–699
Donoghue JP, Herkenham M (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res 365:397–403
Edley SM, Herkenham M (1984) Comparative development of striatal opiate receptors and dopamine revealed by autoradiography and histofluorescence. Brain Res 305:27–42
El-Deeb S, Thompson SC, Covault J (1992) Characterization of a cell surface adhesion molecule expressed by a subset of developing chick neurons. Dev Biol 149:213–227
Faissner A, Kruse J (1990) J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5:627–637
Foster GA, Schultzberg M, Hoekfelt T, Goldstein M, Hemmings HC Jr, Ouimet CC, Walaas SI, Greengard P (1987) Development of a dopamine-and cyclic adenosine 3′:5′-monophosphate-regulated phosphoprotein (DARPP-32) in the prenatal rat central nervous system, and its relationship to the arrival of presumptive dopaminergic innervation. J Neurosci 7:1994–2018
Geisert EE Jr, Bidanset DJ (1993) A central nervous system keratan sulfate proteoglycan: localization to boundaries in the neonatal rat brain. Dev Brain Res 75:163–173
Gerfen CR (1984) The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311:461–464
Gerfen CR (1985) The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J Comp Neurol 236:454–476
Gerfen CR, Baimbridge KG, Miller JJ (1985) The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci USA 82:8780–8784
Gerfen CR, Herkenham M, Thibault J (1987a) The neostriatal mosaic. II. Patch-and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 7:3915–3934
Gerfen CR, Baimbridge KG, Thibault J (1987b) The neostriatal mosaic. III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems. J Neurosci 7:3935–3944
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
Graybiel AM (1990) Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13:244–254
Graybiel AM, Hickey TL (1982) Chemospecificity of ontogenetic units in the striatum: demonstration by combining [3H]thymidine neuronography and histochemical staining. Proc Natl Acad Sci USA 79:198–202
Hatten ME, Furie MB, Rifkin DB (1982) Binding of developing mouse cerebellar cells to fibronectin: a possible mechanism for the formation of the external granular layer. J Neurosci 2:1195–1206
Herkenham M, Pert CB (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 291:415–418
Kooy D van der (1984) Developmental relationships between opiate receptors and dopamine in the formation of caudate-putamen patches. Dev Brain Res 14:300–303
Kooy D van der, Fishell G (1987) Neuronal birthdate underlies the development of striatal compartments. Brain Res 401:155–161
Kooy D van der, Fishell G (1992) Embryonic lesions of the substantia nigra prevent the patchy expression of opiate receptors, but not the segregation of patch and matrix compartment neurons, in the developing rat striatum. Dev Brain Res 66:141–145
Krushel LA, Kooy D van der (1993) Pattern formation in the developing mammalian forebrain: selective adhesion of early but not late postmitotic cortical and striatal neurons within forebrain reaggregate cultures. Dev Biol 158:145–162
Krushel LA, Prieto AL, Cunningham BA, Edelman GM (1993) Expression patterns of the cell adhesion molecule Nr-CAM during histogenesis of the chick nervous system. Neuroscience 53:797–812
Lagunowich LA, Schneider JC, Chasen S, Grunwald GB (1992) Immunohistochemical and biochemical analysis of N-cadherin expression during CNS development. J Neurosci Res 32:202–208
Lança AJ, Boyd S, Kolb BE, Kooy D van der (1986) The development of a patchy organization of the rat striatum. Dev Brain Res 27:1–10
Liesi P, Silver J (1988) Is astrocyte laminin involved in axon guidance in the mammalian CNS? Dev Biol 130:774–785
Lindner J, Rathjen FG, Schachner M (1983) L1 mono-and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305:427–430
Liu FC, Graybiel AM (1992) Heterogeneous development of calbindin-D28K expression in the striatal matrix. J Comp Neurol 320:304–322
Marchand R, Lajoie L (1986) Histogenesis of the striopallidal system in the rat. Neurogenesis of its neurons. Neuroscience 17:573–590
McGeer PL, Zhu SG, Dedhar S (1990) Immunostaining of human brain capillaries by antibodies to very late antigens. J Neuroimmunol 26:213–218
McLoon SC, McLoon LK, Palm SL, Furcht LT (1988) Transient expression of laminin in the optic nerve of the developing rat. J Neurosci 8:1981–1990
Newman-Gage H, Graybiel AM (1988) Expression of calcium/ calmodulin-dependent protein kinase in relation to dopamine islands and synaptic maturation in the cat striatum. J Neurosci 8:3360–3375
O'Brien TF, Faissner A, Schachner M, Steindler DA (1992) Afferent-boundary interactions in the developing neostriatal mosaic. Dev Brain Res 65:259–267
O'Shea KS, Rheinheimer JST, Dixit VM (1990) Deposition and role of thrombospondin in the histogenesis of the cerebellar cortex. J Cell Biol 110:1275–1283
Paschke KA, Lottspeich F, Stuermer CAO (1992) Neurolin, a cell surface glycoprotein on growing retinal axons in the goldfish visual system, is reexpressed during retinal axonal regeneration. J Cell Biol 117:863–875
Peduzzi JD, Irwin MG, Geisert EE Jr. (1994) Distribution and characteristics of a 90-kDa protein, KG-CAM, in the rat CNS. Brain Res 640:296–307
Persohn E, Schachner M (1987) Immunoelectron microscopic localization of the neural cell adhesion molecules L1 and N-CAM during postnatal development of the mouse cerebellum. J Cell Biol 105:569–576
Pourquié O, Corbel C, Le Caer J-P, Rossier J, Le Douarin NM (1992) BEN, a surface glycoprotein of the immunoglobulin superfamily, is expressed in a variety of developing systems. Proc Natl Acad Sci USA 89:5261–5265
Prince JT, Nishiyama A, Healy PA, Beasley L, Stallcup WB (1992) Expression of the F84.1 glycoprotein in the spinal cord and cranial nerves of the developing rat. Dev Brain Res 68:193–201
Saffell JL, Ashton SV, Walsh FS, Doherty P (1992) The changing role of NCAM as a neurite outgrowth-promoting molecule during development. Biochem Soc Trans 20:410–412
Scarisbrick IA, Jones EG (1993) NCAM immunoreactivity during major developmental events in the rat maxillary nerve-whisker system. Dev Brain Res 71:121–135
Sheppard AM, Hamilton SK, Pearlman AL (1991) Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J Neurosci 11:3928–3942
Shults CW, Kimber TA (1993) Thy-1 immunoreactivity distinguishes patches/striosomes from matrix in the early postnatal striatum of the rat. Dev Brain Res 75:136–140
Shults CW, Alberti L, Kimber TA, Stallcup WB (1992) Mesostriatal dopaminergic axons transiently express high levels of NILE during development. Exp Neurol 116:275–285
Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J (1990) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111–130
Snyder-Keller AM (1991) Development of striatal compartmentalization following pre- or postnatal dopamine depletion. J Neurosci 11:810–821
Steindler DA, O'Brien TF, Cooper NGF (1988) Glycoconjugate boundaries during early postnatal development of the neostriatal mosaic. J Comp Neurol 267:357–369
Steindler DA, Cooper NGF, Faissner A, Schachner M (1989) Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Dev Biol 131:243–260
Steindler DA, O'Brien TF, Laywell E, Harrington K, Faissner A, Schachner M (1990) Boundaries during normal and abnormal brain development: in vivo and in vitro studies of glia and glycoconjugates. Exp Neurol 109:35–56
Stewart GR, Pearlman AL (1987) Fibronectin-like immunoreactivity in the developing cerebral cortex. J Neurosci 7:3325–3333
Stitt TN, Gasser UE, Hatten ME (1991) Molecular mechanisms of glial-guided neuronal migration. Ann N Y Acad Sci 633:113–121
Tanaka H, Matsui T, Agata A, Tomura M, Kubota I, McFarland KC, Kohr B, Lee A, Phillips HS, Shelton DL (1991) Molecular cloning and expression of a novel adhesion molecule, SC1. Neuron 7:535–545
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 striatum of the rat. Neuroscience 25:857–887
Zahm DS, Eggerman KW, Sprung RF, Wesche DE, Payne E (1990) Postnatal development of striatal neurotensin immunoreactivity in relation to clusters of substance P-immunoreactive neurons and the “dopamine islands” in the rat. J Comp Neurol 296:403–414
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kuga, Y., Geisert, E.E., Kono, T. et al. Developmental expression of KG-CAM in the rat neostriatum. Anat Embryol 191, 191–201 (1995). https://doi.org/10.1007/BF00187818
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00187818