Developmental regulation of α-amino-3-hydroxy-5-methyl-4-isoxazole- propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex

Delia M. Talos, Rachel E. Fishman, Hyun Kyung Park, Rebecca D. Folkerth, Pamela L. Follett, Joseph J. Volpe, Frances E. Jensen

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Abstract

This is the first part of a two-part study to investigate the cellular distribution and temporal regulation of α-amino-3-hydroxy-5-methyl-4- isoxazole-propionic acid receptor (AMPAR) subunits in the developing white matter and cortex in rat (part I) and human (part II). Western blot and immunocytochemistry were used to evaluate the differential expression of AMPAR subunits on glial and neuronal subtypes during the first 3 postnatal weeks in the Long Evans and Sprague Dawley rat strains. In Long Evans rats during the first postnatal week, GluR2-lacking AMPARs were expressed predominantly on white matter cells, including radial glia, premyelinating oligodendrocytes, and subplate neurons, whereas, during the second postnatal week, these AMPARs were highly expressed on cortical neurons, coincident with decreased expression on white matter cells. Immunocytochemical analysis revealed that cell-specific developmental changes in AMPAR expression occurred 2-3 days earlier by chronological age in Sprague Dawley rats compared with Long Evans rats, despite overall similar temporal sequencing. In both white and gray matter, the periods of high GluR2 deficiency correspond to those of regional susceptibility to hypoxic/ischemic injury in each of the two rat strains, supporting prior studies suggesting a critical role for Ca2+-permeable AMPARs in excitotoxic cellular injury and epileptogenesis. The developmental regulation of these receptor subunits strongly suggests that Ca2+ influx through GluR2-lacking AMPARs may play an important role in neuronal and glial development and injury in the immature brain. Moreover, as demonstrated in part II, there are striking similarities between rat and human in the regional and temporal maturational regulation of neuronal and glial AMPAR expression.

Original languageEnglish
Pages (from-to)42-60
Number of pages19
JournalJournal of Comparative Neurology
Volume497
Issue number1
DOIs
StatePublished - 2006 Jul 1

Fingerprint

Isoxazoles
Prosencephalon
Neuroglia
Rodentia
Long Evans Rats
Wounds and Injuries
Sprague Dawley Rats
Neurons
Oligodendroglia
Western Blotting
Immunohistochemistry
White Matter
propionic acid
Brain

Keywords

  • Excitotoxicity
  • Glutamate receptor
  • Neuron
  • Oligodendrocyte
  • Perinatal
  • Seizure

Cite this

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title = "Developmental regulation of α-amino-3-hydroxy-5-methyl-4-isoxazole- propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex",
abstract = "This is the first part of a two-part study to investigate the cellular distribution and temporal regulation of α-amino-3-hydroxy-5-methyl-4- isoxazole-propionic acid receptor (AMPAR) subunits in the developing white matter and cortex in rat (part I) and human (part II). Western blot and immunocytochemistry were used to evaluate the differential expression of AMPAR subunits on glial and neuronal subtypes during the first 3 postnatal weeks in the Long Evans and Sprague Dawley rat strains. In Long Evans rats during the first postnatal week, GluR2-lacking AMPARs were expressed predominantly on white matter cells, including radial glia, premyelinating oligodendrocytes, and subplate neurons, whereas, during the second postnatal week, these AMPARs were highly expressed on cortical neurons, coincident with decreased expression on white matter cells. Immunocytochemical analysis revealed that cell-specific developmental changes in AMPAR expression occurred 2-3 days earlier by chronological age in Sprague Dawley rats compared with Long Evans rats, despite overall similar temporal sequencing. In both white and gray matter, the periods of high GluR2 deficiency correspond to those of regional susceptibility to hypoxic/ischemic injury in each of the two rat strains, supporting prior studies suggesting a critical role for Ca2+-permeable AMPARs in excitotoxic cellular injury and epileptogenesis. The developmental regulation of these receptor subunits strongly suggests that Ca2+ influx through GluR2-lacking AMPARs may play an important role in neuronal and glial development and injury in the immature brain. Moreover, as demonstrated in part II, there are striking similarities between rat and human in the regional and temporal maturational regulation of neuronal and glial AMPAR expression.",
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Developmental regulation of α-amino-3-hydroxy-5-methyl-4-isoxazole- propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. / Talos, Delia M.; Fishman, Rachel E.; Park, Hyun Kyung; Folkerth, Rebecca D.; Follett, Pamela L.; Volpe, Joseph J.; Jensen, Frances E.

In: Journal of Comparative Neurology, Vol. 497, No. 1, 01.07.2006, p. 42-60.

Research output: Contribution to journalArticleResearchpeer-review

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