Direct hypothalamic control of vasoactive intestinal peptide (VIP) levels in the developing rat ovary

Juan P. Advis, Carol E. Ahmed, Sergio Ojeda

    Research output: Contribution to journalArticle

    27 Citations (Scopus)

    Abstract

    We have previously identified the neurotransmitter vasoactive intestinal peptide (VIP) in nerve fibers of the immature rat ovary and showed that it stimulates steroid release by a mechanism involving increased synthesis of the components of the cholesterol side-chain cleavage enzyme complex. The present experiments were undertaken to study the ontogeny of ovarian VIP levels and to determine if they change in relation to the initiation of puberty. VIP was already detected in 2-day-old ovaries; levels remained constant at approximately 4.5 pg/mg ovary until the end of juvenile development (day 30). Thereafter, and preceding the peripubertal activation of the ovary, VIP levels increased two-fold, decreased gradually towards the first proestrus, and returned to juvenile values after the first ovulation. Transection of the ovarian nerves eliminated radioimmunoassayable VIP levels in both intact and hypophysectomized rats, indicating that ovarian VIP derives mostly from the extrinsic innervation of the gland. Treatment of hypophysectomized immature female rats with human chorionic gonadotropin (hCG), follicle stimulating hormone (FSH), growth hormone (GH), prolactin (Prl), estradiol, or their combination, failed to reproduce the peripubertal increase in VIP. In contrast, unilateral direct anodal current lesions of the left preoptic-anterior hypothalamic area (POA-AHA) of hypophysectomized juvenile rats led to a significant increase in VIP in the ipsilateral ovary. Surprisingly, both bilateral lesions and lesions of the right POA-AHA also increased VIP levels in the left ovary suggesting the existence of a marked asymmetry in the hypothalamic control of ovarian VIP. Lesions of the ventromedial nucleus, dorsal AHA or small lesions of the AHA were ineffective. The results suggest that: a) in prepubertal rats ovarian VIP levels are controlled by a pituitary-independent, neurally-mediated, mechanism which involves the POA-AHA region of the hypothalamus; b) this control is markedly asymmetric; and c) the lesion-induced increase in ovarian VIP levels may not result from the loss of a discrete inhibitory center, but rather may be the consequence of compensatory reactivity of the areas surrounding the lesion.

    Original languageEnglish (US)
    Pages (from-to)605-610
    Number of pages6
    JournalBrain Research Bulletin
    Volume22
    Issue number4
    DOIs
    StatePublished - 1989

    Fingerprint

    Vasoactive Intestinal Peptide
    Ovary
    Anterior Hypothalamic Nucleus
    Cholesterol Side-Chain Cleavage Enzyme
    Proestrus
    Follicle Stimulating Hormone
    Chorionic Gonadotropin
    Puberty
    Ovulation
    Nerve Fibers
    Prolactin
    Growth Hormone
    Hypothalamus
    Neurotransmitter Agents
    Estradiol
    Steroids

    Keywords

    • Female puberty
    • Hypothalamic lesions
    • Hypothalamus
    • Ovarian innervation
    • Vasoactive intestinal peptide

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    Direct hypothalamic control of vasoactive intestinal peptide (VIP) levels in the developing rat ovary. / Advis, Juan P.; Ahmed, Carol E.; Ojeda, Sergio.

    In: Brain Research Bulletin, Vol. 22, No. 4, 1989, p. 605-610.

    Research output: Contribution to journalArticle

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    N2 - We have previously identified the neurotransmitter vasoactive intestinal peptide (VIP) in nerve fibers of the immature rat ovary and showed that it stimulates steroid release by a mechanism involving increased synthesis of the components of the cholesterol side-chain cleavage enzyme complex. The present experiments were undertaken to study the ontogeny of ovarian VIP levels and to determine if they change in relation to the initiation of puberty. VIP was already detected in 2-day-old ovaries; levels remained constant at approximately 4.5 pg/mg ovary until the end of juvenile development (day 30). Thereafter, and preceding the peripubertal activation of the ovary, VIP levels increased two-fold, decreased gradually towards the first proestrus, and returned to juvenile values after the first ovulation. Transection of the ovarian nerves eliminated radioimmunoassayable VIP levels in both intact and hypophysectomized rats, indicating that ovarian VIP derives mostly from the extrinsic innervation of the gland. Treatment of hypophysectomized immature female rats with human chorionic gonadotropin (hCG), follicle stimulating hormone (FSH), growth hormone (GH), prolactin (Prl), estradiol, or their combination, failed to reproduce the peripubertal increase in VIP. In contrast, unilateral direct anodal current lesions of the left preoptic-anterior hypothalamic area (POA-AHA) of hypophysectomized juvenile rats led to a significant increase in VIP in the ipsilateral ovary. Surprisingly, both bilateral lesions and lesions of the right POA-AHA also increased VIP levels in the left ovary suggesting the existence of a marked asymmetry in the hypothalamic control of ovarian VIP. Lesions of the ventromedial nucleus, dorsal AHA or small lesions of the AHA were ineffective. The results suggest that: a) in prepubertal rats ovarian VIP levels are controlled by a pituitary-independent, neurally-mediated, mechanism which involves the POA-AHA region of the hypothalamus; b) this control is markedly asymmetric; and c) the lesion-induced increase in ovarian VIP levels may not result from the loss of a discrete inhibitory center, but rather may be the consequence of compensatory reactivity of the areas surrounding the lesion.

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