Changes in immediate early gene expression during postnatal development of cat cortex and cerebellum

doi:10.1016/0169-328X(92)90087-R

Molecular Brain Research

Volume 12, Issues 1–3, January 1992, Pages 215-223

https://doi.org/10.1016/0169-328X(92)90087-R Get rights and content

Abstract

Postnatal brain development involves interactions between extracellular signals and preprogrammed genetic events. Immediate early genes (IEGs) are a group of genes that are induced by extracellular signals and their protein products alter transcription by binding regulatory elements in other genes. Using Northern and slot blot analysis of total RNA isolated from visual cortex, frontal cortex, and cerebellum of cats, we have determined the postnatal developmental patterns of mRNA expression for 5 of these genes, c-fos, egr-1, c-jun, jun-B, and c-myc. Each gene had a distinct developmental pattern of mRNA expression, and for a given gene, these patterns were often different in different brain structures. These results suggest that temporal changes in the combinational interaction of different IEGs during early postnatal life are important for normal brain development.

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Recently, the effect of binocular central retinal lesions on the expression of immediate early genes in the visual system of adult cats was demonstrated using in situ hybridization and immunocytochemistry [2]. The present study was undertaken to quantify cat c-fos mRNA expression differences in the cat primary visual cortex after sensory deafferentation. Prior to quantification, DNA fragments obtained using reverse transcription-polymerase chain reaction (RT-PCR) in combination with rapid amplification of complementary DNA ends (RACE) were cloned and sequenced. This provided us with the necessary sequence¹ information to prepare cat-specific c-fos primers for the development of a new quantitative RT-PCR assay. We optimized a reverse transcription-competitive polymerase chain reaction (RT-cPCR) method with a heterologous DNA fragment (competitor) as external standard to quantify relative amounts of cat c-fos mRNA expression levels. Internal standardization was accomplished by quantifying, in a parallel RT-cPCR, a well-characterized housekeeping gene, glyceraldehyde-3-phosphate dehydrogenase (GAPDH). This cat-specific RT-cPCR assay allowed us to measure c-fos mRNA expression levels in central and peripheral regions of primary visual cortex in normal and retinal lesion cats.
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The central expression of Krox-20, a C₂H₂-type zinc-finger transcription factor and immediate early gene, is primarily studied in the young embryo, where it contributes to rhombomere (r) r3 and r5 development. Data regarding the cellular localization and developmental regulation of Krox-20 protein expression in brainstem neurons are lacking. Our interest in brainstem development, coupled with findings from our lab and others that demonstrate a profound impact of a Krox-20 null mutation on brainstem-mediated behaviors, led us to investigate the spatiotemporal expression of Krox-20 protein in brainstem and cerebellar neurons to gain insight into potential cellular targets of the mutation. Understanding the cellular localization of Krox-20 is important in light of studies showing the impact of immediate early gene expression on neuronal function. Krox-20 immunohistochemistry experiments were conducted on animals at embryonic days (E) 17.0 and 18.5 and postnatal days (P) 0–1, 3–4, 7, 14, 22, and adulthood. Krox-20 expression is developmentally regulated in motoneurons, somatosensory-related neurons, Purkinje cells, and components of auditory circuitry. Neurons in the ventral cochlear nucleus and inferior colliculus show a sustained Krox-20 expression. Ultrastructural data demonstrate Krox-20 expression in somata and dendrites of central neurons. Our identification of Krox-20 expressing neurons provides us a better understanding of the behavioral consequences of the mutation. Furthermore, our results suggest that Krox-20 protein has a role in the maturation of particular brainstem and cerebellar neurons and fluctuations in Krox-20 protein expression coincide with the development of circuitry underlying brainstem-mediated behaviors.
Immediate early gene expression in the visual cortex of normal and dark reared cats: Differences between fos and egr-1
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Northern blotting indicated that the level of induced fos was higher in normal than dark reared cat visual cortex (VC) at 5 weeks of age, comparable at 10 weeks, and higher in dark reared than normal cat visual cortex at 20 weeks. Fos egr-1, induction was higher in dark reared visual cortex at all ages. Thus, dark rearing has similar effects on fos, but not egr-1, expression as it has on physiological neuronal plasticity during the VC critical period.
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This chapter discusses the way molecular mapping strategies have been used to address fundamental questions of sensory function in the mammalian nervous system. Immediate-early genes (IEGs), c-fos and zif268, are popular neurobiological tools for mapping functional activity in the brain. The various members of the IEG family are known to encode proteins with diverse cellular functions. In the brain, IEGs linked to neural activity and having mapping applications generally encode proteins that serve as transcription factors—that is, complexes that bind to the promoter regions of certain genes and then either activate or repress their expression. These so-called “inducible transcription factors” (ITFs) are distinguished from other proteins that normally reside in the nucleus and that serve as regulators of ongoing transcriptional activity. The ITFs, c-Fos and Zif268, are both induced in neurons after extracellular stimulation by neurotransmitters and trophic substances. The sequence of events that leads to ITF induction is largely coordinated by Ca²⁺ influx into the cell.
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The first several months of life are a critical period for neuronal plasticity in the visual cortex, during which anatomical and physiological development depends upon visual experience. Rearing in darkness slows the time course of this critical period, such that at 5 weeks normal cats are more plastic than dark-reared cats, while at 20 weeks dark-reared cats are more plastic. This study reports the identification of a subset of mitochondrial genes that are regulated in this manner. Opponent patterns of bidirectional expression were found: several genes (ATPase 6, cytochrome b, NADH dehydrogenase subunits 4 and 2) showed elevation in normal cats at 5 weeks and in dark-reared cats at 20 weeks (“plasticity” genes); others (NADH dehydrogenase subunits 3 and 5) showed the opposite (“anti-plasticity” genes). These findings add a new dimension to the growing evidence that changes in mitochondrial gene expression are involved in the neuroplastic response.
Developmental changes in the expression of GABA<inf>A</inf> receptor subunits (α<inf>1</inf>, α<inf>2</inf>, α<inf>3</inf>) in the cat visual cortex and the effects of dark rearing
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The present study used Western blots and Northern slot blots to determine changes in the level of expression of GABA_A receptor subunits α₁, α₂, and α₃, in relation to the ‘critical period’ in cat visual cortex. Levels of the GABA_A α₁ subunit were lowest at 1 week, increased four-fold to a maximum at 10 weeks, and declined slightly (35%) into adulthood. Levels of the GABA_A α₂ and α₃ subunits were highest at 1 week of age, decreased two-fold by 10 weeks of age and were constant thereafter. Comparison between visual cortex from normal and dark-reared cats at 5 weeks and 20 weeks showed that α₁ and α₃ subunit expression was elevated in dark-reared animals by approximately 50% at both ages. α₂ expression was not affected. These results implicate the importance of a shift from putative immature to mature GABA_A receptor subunits during the critical period of visual cortex and in conjunction with parallel analysis of NMDA receptor subunit maturation, further support the notion that a changing excitatory/inhibitory balance is critical for neuronal plasticity.

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Changes in immediate early gene expression during postnatal development of cat cortex and cerebellum

Abstract

Cell

Cell

Cell

Cell

Anal. Biochem.

Cell

J. Biol. Chem.

Cell

Cell

Cell

Cell

Cell

Cell

Cell

Neuron

Cell

Dev. Brain Res.

Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction

Genes Dev.

Postnatal changes in the distribution of acetylcholinesterase in kitten visual cortex

J. Comp. Neurol.

Innate and environmental factors in the development of the kitten's visual cortex

J. Physiol.

c-fos proto-oncogene expression in the nervous system during mouse development

Mol. Cell Biol.

pp60c-src expression in the developing rat brain

A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with ‘zinc finger’ sequences

The development of synapses in the visual system of the cat

J. Comp. Neurol.

Early development of visual cortical cells in normal and dark-reared kittens: relationship between orientation selectivity and ocular dominance

J. Physiol.

The laminar distribution and postnatal development of serotonin-immunoreactive axons in the cat primary visual cortex

Exp. Brain Res.

Variations in c-fos gene expression during rat brain development

Mol. Brain Res.

A FOS protein is present in a complex that binds a negative regulator of MYC

Genes Dev.

pp60^c-src expression in the developing rat brain