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The Journal of Neuroscience, December 15, 2000, 20(24):9224-9234

Association of Cocaine- and Amphetamine-Regulated Transcript-Immunoreactive Elements with Thyrotropin-Releasing Hormone-Synthesizing Neurons in the Hypothalamic Paraventricular Nucleus and Its Role in the Regulation of the Hypothalamic-Pituitary-Thyroid Axis during Fasting

Csaba Fekete^{1, 2}, Emese Mihály¹, Lu-Guang Luo³, Joseph Kelly¹, Jes Thorn Clausen⁴, QuanFu Mao³, William M. Rand⁵, Larry Gene Moss¹, Michael Kuhar⁷, Charles H. Emerson⁸, Ivor M. D. Jackson³, and Ronald M. Lechan^{1, 6}

¹ Tupper Research Institute and Department of Medicine, Division of Endocrinology, Diabetes, Metabolism and Molecular Medicine, New England Medical Center, Boston, Massachusetts 02111, ² Department of Neurobiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary 1083, ³ Division of Endocrinology, Rhode Island Hospital and Brown University, Providence, Rhode Island 02903, ⁴ Novo Nordisk A/S, Department of Assay and Cell Technology, Novo Alle, DK-2880 Bagsvaerd, Denmark, Departments of ⁵ Community Health and ⁶ Neuroscience, Tufts University School of Medicine, Boston, Massachusetts 02111, ⁷ Yerkes Regional Primate Center, Emory University, Atlanta, Georgia 30329, and ⁸ Department of Medicine, Division of Endocrinology, University of Massachusetts Medical School, Worcester, Massachusetts 01655

Because cocaine- and amphetamine-regulated transcript (CART) coexists with -melanocyte stimulating hormone (-MSH) in the arcuate nucleus neurons and we have recently demonstrated that -MSH innervates TRH-synthesizing neurons in the hypothalamic paraventricular nucleus (PVN), we raised the possibility that CART may also be contained in fibers that innervate hypophysiotropic thyrotropin-releasing hormone (TRH) neurons and modulate TRH gene expression. Triple-labeling fluorescent in situ hybridization and immunofluorescence were performed to reveal the morphological relationships between pro-TRH mRNA-containing neurons and CART- and -MSH-immunoreactive (IR) axons. CART-IR axons densely innervated the majority of pro-TRH mRNA-containing neurons in all parvocellular subdivisions of the PVN and established asymmetric synaptic specializations with pro-TRH neurons. However, whereas all -MSH-IR axons in the PVN contained CART-IR, only a portion of CART-IR axons in contact with pro-TRH neurons were immunoreactive for -MSH. In the medial and periventricular parvocellular subdivisions of the PVN, CART was co-contained in ~80% of pro-TRH neuronal perikarya, whereas colocalization with pro-TRH was found in <10% of the anterior parvocellular subdivision neurons. In addition, >80% of TRH/CART neurons in the periventricular and medial parvocellular subdivisions accumulated Fluoro-Gold after systemic administration, suggesting that CART may serve as a marker for hypophysiotropic TRH neurons. CART prevented fasting-induced suppression of pro-TRH in the PVN when administered intracerebroventricularly and increased the content of TRH in hypothalamic cell cultures. These studies establish an anatomical association between CART and pro-TRH-producing neurons in the PVN and demonstrate that CART has a stimulatory effect on hypophysiotropic TRH neurons by increasing pro-TRH gene expression and the biosynthesis of TRH.

Key words: thyrotropin-releasing hormone; thyroid axis; CART; -MSH; fasting; leptin

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20249224-11$05.00/0

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