A sex-related difference in the developmental expression of class II β-tubulin messenger RNA in rat hypothalamus

Lisa C. Rogers, Marie Pierre Junier, Stephen R. Farmer, Sergio Ojeda

    Research output: Contribution to journalArticle

    21 Citations (Scopus)

    Abstract

    Axonal elongation, neurite outgrowth, and synaptogenesis are key events of mammalian brain development. The neuronal cytoskeleton plays a fundamental role in these changes, which are influenced by gonadal steroids in brain regions bearing the appropriate receptors. Microtubules, which constitute a major portion of the cytoskeleton, are composed of α- and β-tubulin polypeptide heterodimers encoded by multigene families. Of the five β-tubulin isotypes described, the genes encoding Class II and IV are preferentially expressed in brain. Expression of the mRNA encoding Class II β-tubulin isotype is selectively increased during neuronal development and regeneration, whereas that of Class IV increases later in development and does not change during regeneration. The present study was undertaken to characterize the expression of these mRNAs during hypothalamic development and to determine if the well-known process of steroid-dependent sexual differentiation of this brain region is accompanied by related differences in β-tubulin mRNA expression. In addition, we examined the developmental profile of mRNAs encoding two protein constituents of neurofllaments (NF), the other major component of the neuronal cytoskeleton. The levels of Class II β-tubulin mRNA (RBTZ) were elevated in the medial basal hypothalamus (MBH) and preoptic area (POA) of both males and females during the late fetal-early postnatal period (i.e., Fetal Day 16-Postnatal Day 2) and decreased markedly thereafter. The initial decrease, detected between Postnatal Days 2 and 12, was more pronounced in females than in males, the difference being more clear in the POA than in the MBH. No such sexrelated differences were found in the cerebral cortex (Cc) or cerebellum (Cb). Castration of male rats on the day of birth reduced RBTZ mRNA levels in the POA and MBH toward female values when measured on Day 12. Analysis of the Class IV β-tubulin mRNA (RBT2) developmental profile revealed that RBTZ mRNA is expressed throughout development (Fetal Day 20-Postnatal Day 25) in the POA and MBH, without sex-related differences. Although levels of expression increased during the fourth week of life, the increase was less conspicuous than in the Cb. Levels of the two mRNAs encoding the 68-kDa protein of neurofilaments (NF68) increased moderately between Fetal Day 16 and the day of birth in both the POA and MBH, remaining relatively constant thereafter, without detectable sex differences. Levels of NF145 mRNA, which encodes the 145-kDa protein of neurofilaments, were already maximally elevated by Fetal Day 16 (the earliest age studied) and showed no sex-related differences during development. Since RBTZ, but not RBT2 or NF, mRNA expression is known to be induced during neuronal development, the results provide molecular evidence for the concept that an extended period of axonal elongation/neurite outgrowth underlies the steroid-dependent morphological differentiation of the rat hypothalamus.

    Original languageEnglish (US)
    Pages (from-to)130-138
    Number of pages9
    JournalMolecular and Cellular Neuroscience
    Volume2
    Issue number2
    DOIs
    StatePublished - 1991

    Fingerprint

    Tubulin
    Sex Characteristics
    Hypothalamus
    Middle Hypothalamus
    Messenger RNA
    Preoptic Area
    Cytoskeleton
    Steroids
    Brain
    Cerebellum
    Regeneration
    Parturition
    Neurofilament Proteins
    Sex Differentiation
    MHC Class II Genes
    Orchiectomy
    Multigene Family
    Fetal Development
    Microtubules
    Cerebral Cortex

    ASJC Scopus subject areas

    • Molecular Biology
    • Cellular and Molecular Neuroscience
    • Developmental Neuroscience

    Cite this

    A sex-related difference in the developmental expression of class II β-tubulin messenger RNA in rat hypothalamus. / Rogers, Lisa C.; Junier, Marie Pierre; Farmer, Stephen R.; Ojeda, Sergio.

    In: Molecular and Cellular Neuroscience, Vol. 2, No. 2, 1991, p. 130-138.

    Research output: Contribution to journalArticle

    @article{f357291ca8334c0c8fccc804c134bd2d,
    title = "A sex-related difference in the developmental expression of class II β-tubulin messenger RNA in rat hypothalamus",
    abstract = "Axonal elongation, neurite outgrowth, and synaptogenesis are key events of mammalian brain development. The neuronal cytoskeleton plays a fundamental role in these changes, which are influenced by gonadal steroids in brain regions bearing the appropriate receptors. Microtubules, which constitute a major portion of the cytoskeleton, are composed of α- and β-tubulin polypeptide heterodimers encoded by multigene families. Of the five β-tubulin isotypes described, the genes encoding Class II and IV are preferentially expressed in brain. Expression of the mRNA encoding Class II β-tubulin isotype is selectively increased during neuronal development and regeneration, whereas that of Class IV increases later in development and does not change during regeneration. The present study was undertaken to characterize the expression of these mRNAs during hypothalamic development and to determine if the well-known process of steroid-dependent sexual differentiation of this brain region is accompanied by related differences in β-tubulin mRNA expression. In addition, we examined the developmental profile of mRNAs encoding two protein constituents of neurofllaments (NF), the other major component of the neuronal cytoskeleton. The levels of Class II β-tubulin mRNA (RBTZ) were elevated in the medial basal hypothalamus (MBH) and preoptic area (POA) of both males and females during the late fetal-early postnatal period (i.e., Fetal Day 16-Postnatal Day 2) and decreased markedly thereafter. The initial decrease, detected between Postnatal Days 2 and 12, was more pronounced in females than in males, the difference being more clear in the POA than in the MBH. No such sexrelated differences were found in the cerebral cortex (Cc) or cerebellum (Cb). Castration of male rats on the day of birth reduced RBTZ mRNA levels in the POA and MBH toward female values when measured on Day 12. Analysis of the Class IV β-tubulin mRNA (RBT2) developmental profile revealed that RBTZ mRNA is expressed throughout development (Fetal Day 20-Postnatal Day 25) in the POA and MBH, without sex-related differences. Although levels of expression increased during the fourth week of life, the increase was less conspicuous than in the Cb. Levels of the two mRNAs encoding the 68-kDa protein of neurofilaments (NF68) increased moderately between Fetal Day 16 and the day of birth in both the POA and MBH, remaining relatively constant thereafter, without detectable sex differences. Levels of NF145 mRNA, which encodes the 145-kDa protein of neurofilaments, were already maximally elevated by Fetal Day 16 (the earliest age studied) and showed no sex-related differences during development. Since RBTZ, but not RBT2 or NF, mRNA expression is known to be induced during neuronal development, the results provide molecular evidence for the concept that an extended period of axonal elongation/neurite outgrowth underlies the steroid-dependent morphological differentiation of the rat hypothalamus.",
    author = "Rogers, {Lisa C.} and Junier, {Marie Pierre} and Farmer, {Stephen R.} and Sergio Ojeda",
    year = "1991",
    doi = "10.1016/1044-7431(91)90005-9",
    language = "English (US)",
    volume = "2",
    pages = "130--138",
    journal = "Molecular and Cellular Neuroscience",
    issn = "1044-7431",
    publisher = "Academic Press Inc.",
    number = "2",

    }

    TY - JOUR

    T1 - A sex-related difference in the developmental expression of class II β-tubulin messenger RNA in rat hypothalamus

    AU - Rogers, Lisa C.

    AU - Junier, Marie Pierre

    AU - Farmer, Stephen R.

    AU - Ojeda, Sergio

    PY - 1991

    Y1 - 1991

    N2 - Axonal elongation, neurite outgrowth, and synaptogenesis are key events of mammalian brain development. The neuronal cytoskeleton plays a fundamental role in these changes, which are influenced by gonadal steroids in brain regions bearing the appropriate receptors. Microtubules, which constitute a major portion of the cytoskeleton, are composed of α- and β-tubulin polypeptide heterodimers encoded by multigene families. Of the five β-tubulin isotypes described, the genes encoding Class II and IV are preferentially expressed in brain. Expression of the mRNA encoding Class II β-tubulin isotype is selectively increased during neuronal development and regeneration, whereas that of Class IV increases later in development and does not change during regeneration. The present study was undertaken to characterize the expression of these mRNAs during hypothalamic development and to determine if the well-known process of steroid-dependent sexual differentiation of this brain region is accompanied by related differences in β-tubulin mRNA expression. In addition, we examined the developmental profile of mRNAs encoding two protein constituents of neurofllaments (NF), the other major component of the neuronal cytoskeleton. The levels of Class II β-tubulin mRNA (RBTZ) were elevated in the medial basal hypothalamus (MBH) and preoptic area (POA) of both males and females during the late fetal-early postnatal period (i.e., Fetal Day 16-Postnatal Day 2) and decreased markedly thereafter. The initial decrease, detected between Postnatal Days 2 and 12, was more pronounced in females than in males, the difference being more clear in the POA than in the MBH. No such sexrelated differences were found in the cerebral cortex (Cc) or cerebellum (Cb). Castration of male rats on the day of birth reduced RBTZ mRNA levels in the POA and MBH toward female values when measured on Day 12. Analysis of the Class IV β-tubulin mRNA (RBT2) developmental profile revealed that RBTZ mRNA is expressed throughout development (Fetal Day 20-Postnatal Day 25) in the POA and MBH, without sex-related differences. Although levels of expression increased during the fourth week of life, the increase was less conspicuous than in the Cb. Levels of the two mRNAs encoding the 68-kDa protein of neurofilaments (NF68) increased moderately between Fetal Day 16 and the day of birth in both the POA and MBH, remaining relatively constant thereafter, without detectable sex differences. Levels of NF145 mRNA, which encodes the 145-kDa protein of neurofilaments, were already maximally elevated by Fetal Day 16 (the earliest age studied) and showed no sex-related differences during development. Since RBTZ, but not RBT2 or NF, mRNA expression is known to be induced during neuronal development, the results provide molecular evidence for the concept that an extended period of axonal elongation/neurite outgrowth underlies the steroid-dependent morphological differentiation of the rat hypothalamus.

    AB - Axonal elongation, neurite outgrowth, and synaptogenesis are key events of mammalian brain development. The neuronal cytoskeleton plays a fundamental role in these changes, which are influenced by gonadal steroids in brain regions bearing the appropriate receptors. Microtubules, which constitute a major portion of the cytoskeleton, are composed of α- and β-tubulin polypeptide heterodimers encoded by multigene families. Of the five β-tubulin isotypes described, the genes encoding Class II and IV are preferentially expressed in brain. Expression of the mRNA encoding Class II β-tubulin isotype is selectively increased during neuronal development and regeneration, whereas that of Class IV increases later in development and does not change during regeneration. The present study was undertaken to characterize the expression of these mRNAs during hypothalamic development and to determine if the well-known process of steroid-dependent sexual differentiation of this brain region is accompanied by related differences in β-tubulin mRNA expression. In addition, we examined the developmental profile of mRNAs encoding two protein constituents of neurofllaments (NF), the other major component of the neuronal cytoskeleton. The levels of Class II β-tubulin mRNA (RBTZ) were elevated in the medial basal hypothalamus (MBH) and preoptic area (POA) of both males and females during the late fetal-early postnatal period (i.e., Fetal Day 16-Postnatal Day 2) and decreased markedly thereafter. The initial decrease, detected between Postnatal Days 2 and 12, was more pronounced in females than in males, the difference being more clear in the POA than in the MBH. No such sexrelated differences were found in the cerebral cortex (Cc) or cerebellum (Cb). Castration of male rats on the day of birth reduced RBTZ mRNA levels in the POA and MBH toward female values when measured on Day 12. Analysis of the Class IV β-tubulin mRNA (RBT2) developmental profile revealed that RBTZ mRNA is expressed throughout development (Fetal Day 20-Postnatal Day 25) in the POA and MBH, without sex-related differences. Although levels of expression increased during the fourth week of life, the increase was less conspicuous than in the Cb. Levels of the two mRNAs encoding the 68-kDa protein of neurofilaments (NF68) increased moderately between Fetal Day 16 and the day of birth in both the POA and MBH, remaining relatively constant thereafter, without detectable sex differences. Levels of NF145 mRNA, which encodes the 145-kDa protein of neurofilaments, were already maximally elevated by Fetal Day 16 (the earliest age studied) and showed no sex-related differences during development. Since RBTZ, but not RBT2 or NF, mRNA expression is known to be induced during neuronal development, the results provide molecular evidence for the concept that an extended period of axonal elongation/neurite outgrowth underlies the steroid-dependent morphological differentiation of the rat hypothalamus.

    UR - http://www.scopus.com/inward/record.url?scp=0002454999&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=0002454999&partnerID=8YFLogxK

    U2 - 10.1016/1044-7431(91)90005-9

    DO - 10.1016/1044-7431(91)90005-9

    M3 - Article

    AN - SCOPUS:0002454999

    VL - 2

    SP - 130

    EP - 138

    JO - Molecular and Cellular Neuroscience

    JF - Molecular and Cellular Neuroscience

    SN - 1044-7431

    IS - 2

    ER -