Species-specific patterns of glycoprotein expression in the developing rodent caudoputamen: Association of 5′-nucleotidase activity with dopamine islands and striosomes in rat, but with extrastriosomal matrix in mouse

The glycoprotein 5′‐nucleotidase is a cell surface phosphatase and represents a new marker for striosomes in the adult rat caudoputamen. We report here on its developmental expression in the rat and mouse striatum, and show an unexpected converse 5′‐nucleotidase chemoarchitecture of the caudoputamen...

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Veröffentlicht in:Journal of comparative neurology (1911) 1993-07, Vol.333 (4), p.578-596
Hauptverfasser: Schoen, Siegfried W., Graybiel, Ann M.
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description The glycoprotein 5′‐nucleotidase is a cell surface phosphatase and represents a new marker for striosomes in the adult rat caudoputamen. We report here on its developmental expression in the rat and mouse striatum, and show an unexpected converse 5′‐nucleotidase chemoarchitecture of the caudoputamen in these closely related species. In the rat, 5′‐nucleotidase activity was first visible as neuropil staining in tyrosine hydroxylase‐positive dopamine islands of the midstriatum on postnatal day 1, and by the end of the first postnatal week, 5′‐nucleotidase‐positive dopamine islands also appeared rostrally. This compartmental pattern persisted thereafter, so that in adult animals, in all but the caudal caudoputamen, zones of enhanced 5′‐nucleotidase staining were restricted to calbindin‐D28k‐poor striosomes. Weak 5′‐nucleotidase activity also emerged in the matrix. In striking contrast, in the mouse striatum, enhanced 5′‐nucleotidase activity was preferentially associated with extrastriosomal tissue. Enzymatic reaction first appeared on embryonic day 18, and developed over the first postnatal week into a mosaic pattern in which the matrix was stained but the dopamine islands were unstained. The matrix staining itself was heterogeneous. After the second postnatal week, most of the caudoputamen was stained, and in adult mice only rostral striosomes expressed low 5′‐nucleotidase activity. We conclude that in rats, 5′‐nucleotidase represents one of the few substances that maintains a preferential dopamine island/striosome distribution during striatal development. In mice, 5′‐nucleotidase activity is expressed preferentially in the matrix during development, and its compartmental pattern is gradually lost with maturation, except very rostrally. These findings do not suggest an instructive role of the enzyme in striatal compartment formation in either species, but do suggest the possibility that 5′‐nucleotidase contributes to the differentiation of striatal compartments during development. © 1993 Wiley‐Liss, Inc.
doi_str_mv 10.1002/cne.903330410
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We report here on its developmental expression in the rat and mouse striatum, and show an unexpected converse 5′‐nucleotidase chemoarchitecture of the caudoputamen in these closely related species. In the rat, 5′‐nucleotidase activity was first visible as neuropil staining in tyrosine hydroxylase‐positive dopamine islands of the midstriatum on postnatal day 1, and by the end of the first postnatal week, 5′‐nucleotidase‐positive dopamine islands also appeared rostrally. This compartmental pattern persisted thereafter, so that in adult animals, in all but the caudal caudoputamen, zones of enhanced 5′‐nucleotidase staining were restricted to calbindin‐D28k‐poor striosomes. Weak 5′‐nucleotidase activity also emerged in the matrix. In striking contrast, in the mouse striatum, enhanced 5′‐nucleotidase activity was preferentially associated with extrastriosomal tissue. 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Comp. Neurol</addtitle><description>The glycoprotein 5′‐nucleotidase is a cell surface phosphatase and represents a new marker for striosomes in the adult rat caudoputamen. We report here on its developmental expression in the rat and mouse striatum, and show an unexpected converse 5′‐nucleotidase chemoarchitecture of the caudoputamen in these closely related species. In the rat, 5′‐nucleotidase activity was first visible as neuropil staining in tyrosine hydroxylase‐positive dopamine islands of the midstriatum on postnatal day 1, and by the end of the first postnatal week, 5′‐nucleotidase‐positive dopamine islands also appeared rostrally. This compartmental pattern persisted thereafter, so that in adult animals, in all but the caudal caudoputamen, zones of enhanced 5′‐nucleotidase staining were restricted to calbindin‐D28k‐poor striosomes. Weak 5′‐nucleotidase activity also emerged in the matrix. In striking contrast, in the mouse striatum, enhanced 5′‐nucleotidase activity was preferentially associated with extrastriosomal tissue. Enzymatic reaction first appeared on embryonic day 18, and developed over the first postnatal week into a mosaic pattern in which the matrix was stained but the dopamine islands were unstained. The matrix staining itself was heterogeneous. After the second postnatal week, most of the caudoputamen was stained, and in adult mice only rostral striosomes expressed low 5′‐nucleotidase activity. We conclude that in rats, 5′‐nucleotidase represents one of the few substances that maintains a preferential dopamine island/striosome distribution during striatal development. In mice, 5′‐nucleotidase activity is expressed preferentially in the matrix during development, and its compartmental pattern is gradually lost with maturation, except very rostrally. These findings do not suggest an instructive role of the enzyme in striatal compartment formation in either species, but do suggest the possibility that 5′‐nucleotidase contributes to the differentiation of striatal compartments during development. © 1993 Wiley‐Liss, Inc.</description><subject>5'-Nucleotidase - immunology</subject><subject>5'-Nucleotidase - metabolism</subject><subject>adenosine</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>basal ganglia</subject><subject>Biochemistry and metabolism</subject><subject>Biological and medical sciences</subject><subject>Caudate Nucleus - embryology</subject><subject>Caudate Nucleus - growth &amp; development</subject><subject>Caudate Nucleus - metabolism</subject><subject>cell adhesion</subject><subject>Central nervous system</subject><subject>development</subject><subject>Dopamine - physiology</subject><subject>Female</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>glia</subject><subject>Glycoproteins - biosynthesis</subject><subject>Immunohistochemistry</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred Strains</subject><subject>Organelles - enzymology</subject><subject>Pregnancy</subject><subject>Putamen - embryology</subject><subject>Putamen - growth &amp; development</subject><subject>Putamen - metabolism</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Species Specificity</subject><subject>synaptic plasticity</subject><subject>Tyrosine 3-Monooxygenase - immunology</subject><subject>Tyrosine 3-Monooxygenase - metabolism</subject><subject>Vertebrates: nervous system and sense organs</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1993</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc2O0zAUhSMEGsrAkiWSF4gVGezacRJ2o2ooSKMi_tSl5TjXM4YkDr7OTLvjmXgddjwJLi0VK9j4R_c79x77ZNljRs8YpfMXZoCzmnLOqWD0TjZjtJZ5XUl2N5ulOsvrWpb3sweInymldc2rk-ykYpSXFZ1lPz6MYBxgjrvdOkNGHSOEAYm35KrbGj8GH8ENBDZjAETnB5Ju8RpICzfQ-dENVyT4FoZIjJ5aP05R9zC8JOeI3jgdd5LUrfj57Xs-TKYDH12rEYg20d24uCW3Ll6TpNS9G4A47PTQIkkLwRicR98D7qYGHZ-TZop7AWxi0H8A3ZFep_Nmx_V-QniY3bO6Q3h02E-zT68uPi5e55dvl28W55e5EVzQ3EDFRMOsNLqwoHlZ8oLZgkkQnLfUMt1YKoADNYIxXjdlNafWNkyAkEVR8dPs2b5v-qmvE2BUvUMDXXoEJB-qLOpCUEH_CzIpi3LOZQLzPWiCRwxg1Rhcr8NWMap2qauUujqmnvgnh8ZT00N7pA8xp_rTQ12j0Z0NejAOj5io5lL-9lfusVvXwfbfM9VidfG3gYNhhxE2R6UOX5QseVmo9Wqplu-rcr1az9U7_gt5ndvi</recordid><startdate>19930722</startdate><enddate>19930722</enddate><creator>Schoen, Siegfried W.</creator><creator>Graybiel, Ann M.</creator><general>Wiley Subscription Services, Inc., A Wiley Company</general><general>Wiley-Liss</general><scope>BSCLL</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope></search><sort><creationdate>19930722</creationdate><title>Species-specific patterns of glycoprotein expression in the developing rodent caudoputamen: Association of 5′-nucleotidase activity with dopamine islands and striosomes in rat, but with extrastriosomal matrix in mouse</title><author>Schoen, Siegfried W. ; Graybiel, Ann M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4340-ce814b1f6ca5fea377351f516e433d0f1abf04e3e0c41139b7820ffb14e465583</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1993</creationdate><topic>5'-Nucleotidase - immunology</topic><topic>5'-Nucleotidase - metabolism</topic><topic>adenosine</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>basal ganglia</topic><topic>Biochemistry and metabolism</topic><topic>Biological and medical sciences</topic><topic>Caudate Nucleus - embryology</topic><topic>Caudate Nucleus - growth &amp; development</topic><topic>Caudate Nucleus - metabolism</topic><topic>cell adhesion</topic><topic>Central nervous system</topic><topic>development</topic><topic>Dopamine - physiology</topic><topic>Female</topic><topic>Fundamental and applied biological sciences. 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Comp. Neurol</addtitle><date>1993-07-22</date><risdate>1993</risdate><volume>333</volume><issue>4</issue><spage>578</spage><epage>596</epage><pages>578-596</pages><issn>0021-9967</issn><eissn>1096-9861</eissn><coden>JCNEAM</coden><abstract>The glycoprotein 5′‐nucleotidase is a cell surface phosphatase and represents a new marker for striosomes in the adult rat caudoputamen. We report here on its developmental expression in the rat and mouse striatum, and show an unexpected converse 5′‐nucleotidase chemoarchitecture of the caudoputamen in these closely related species. In the rat, 5′‐nucleotidase activity was first visible as neuropil staining in tyrosine hydroxylase‐positive dopamine islands of the midstriatum on postnatal day 1, and by the end of the first postnatal week, 5′‐nucleotidase‐positive dopamine islands also appeared rostrally. This compartmental pattern persisted thereafter, so that in adult animals, in all but the caudal caudoputamen, zones of enhanced 5′‐nucleotidase staining were restricted to calbindin‐D28k‐poor striosomes. Weak 5′‐nucleotidase activity also emerged in the matrix. In striking contrast, in the mouse striatum, enhanced 5′‐nucleotidase activity was preferentially associated with extrastriosomal tissue. Enzymatic reaction first appeared on embryonic day 18, and developed over the first postnatal week into a mosaic pattern in which the matrix was stained but the dopamine islands were unstained. The matrix staining itself was heterogeneous. After the second postnatal week, most of the caudoputamen was stained, and in adult mice only rostral striosomes expressed low 5′‐nucleotidase activity. We conclude that in rats, 5′‐nucleotidase represents one of the few substances that maintains a preferential dopamine island/striosome distribution during striatal development. In mice, 5′‐nucleotidase activity is expressed preferentially in the matrix during development, and its compartmental pattern is gradually lost with maturation, except very rostrally. These findings do not suggest an instructive role of the enzyme in striatal compartment formation in either species, but do suggest the possibility that 5′‐nucleotidase contributes to the differentiation of striatal compartments during development. © 1993 Wiley‐Liss, Inc.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc., A Wiley Company</pub><pmid>8103780</pmid><doi>10.1002/cne.903330410</doi><tpages>19</tpages></addata></record>
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subjects 5'-Nucleotidase - immunology
5'-Nucleotidase - metabolism
adenosine
Animals
Animals, Newborn
basal ganglia
Biochemistry and metabolism
Biological and medical sciences
Caudate Nucleus - embryology
Caudate Nucleus - growth & development
Caudate Nucleus - metabolism
cell adhesion
Central nervous system
development
Dopamine - physiology
Female
Fundamental and applied biological sciences. Psychology
glia
Glycoproteins - biosynthesis
Immunohistochemistry
Mice
Mice, Inbred BALB C
Mice, Inbred Strains
Organelles - enzymology
Pregnancy
Putamen - embryology
Putamen - growth & development
Putamen - metabolism
Rats
Rats, Sprague-Dawley
Species Specificity
synaptic plasticity
Tyrosine 3-Monooxygenase - immunology
Tyrosine 3-Monooxygenase - metabolism
Vertebrates: nervous system and sense organs
title Species-specific patterns of glycoprotein expression in the developing rodent caudoputamen: Association of 5′-nucleotidase activity with dopamine islands and striosomes in rat, but with extrastriosomal matrix in mouse
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