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Endocrinology Vol. 138, No. 6 2569-2576
Copyright © 1997 by The Endocrine Society

ARTICLES

Leptin Prevents Fasting-Induced Suppression of Prothyrotropin-Releasing Hormone Messenger Ribonucleic Acid in Neurons of the Hypothalamic Paraventricular Nucleus1

Gábor Légrádi, Charles H. Emerson, Rexford S. Ahima, Jeffrey S. Flier and Ronald M. Lechan

Tupper Research Institute and Department of Medicine, Division of Endocrinology, Diabetes, Metabolism and Molecular Medicine, New England Medical Center (G.L., R.M.L.) and Department of Medicine, Division of Endocrinology, Beth Israel-Deaconess Medical Center (R.S.A., J.S.F.), Boston, Massachusetts 02111; University of Massachusetts Medical School (C.H.E.), Worcester, Massachusetts 01655; and Department of Neuroscience (R.M.L.), Tufts University School of Medicine, Boston, Massachusetts 02111

Address all correspondence and requests for reprints to: Ronald M. Lechan, M.D., Ph.D., Professor of Medicine, Division of Endocrinology, Box No. 268, New England Medical Center, 750 Washington Street, Boston, Massachusetts 02111.

Prolonged fasting is associated with a number of changes in the thyroid axis manifested by low serum T3 and T4 levels and, paradoxically, low or normal TSH. This response is, at least partly, caused by suppression of proTRH gene expression in neurons of the hypothalamic paraventricular nucleus (PVN) and reduced hypothalamic TRH release. Because the fall in thyroid hormone levels can be blunted in mice by the systemic administration of leptin, we raised the possibility that leptin may have an important role in the neuroendocrine regulation of the thyroid axis, through effects on hypophysiotropic neurons producing proTRH. Adult male, Sprague-Dawley rats were either fed normally, fasted for 3 days, or fasted and administered leptin at a dose of 0.5 µg/gm BW ip every 6 h. Fasted animals showed significant reduction in plasma total and free T4 and T3 levels compared with controls, that were restored toward normal by the administration of leptin. Percent free T4, but not percent free T3, increased during fasting, further suggesting a reduction in plasma transthyretin levels that did not return to fed levels after leptin administration. By semiquantitative analysis of in situ hybridization autoradiograms, proTRH messenger RNA in medial parvocellular PVN neurons was markedly suppressed in the fasting animals but was restored to normal by leptin administration [fed vs. fast vs. fast/leptin (density units x 108): 8.5 ± 0.4, 3.2 ± 0.2, 8.1 ± 0.8]. In contrast, proTRH messenger RNA in adjacent neurons in the lateral hypothalamus that do not have a hypophysiotropic function remained unchanged by any of the experimental manipulations. These findings indicate that leptin has a selective, central action to modulate the hypothalamic-pituitary-thyroid axis by regulating proTRH gene expression in the PVN but does not have peripheral effects on thyroid-binding proteins. We propose that the fall in circulating leptin levels during fasting resets the set point for feedback inhibition by thyroid hormones on the biosynthesis of hypophysiotropic proTRH, thereby allowing adaptation to starvation.




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C. Fekete, E. Mihaly, L.-G. Luo, J. Kelly, J. T. Clausen, Q. Mao, W. M. Rand, L. G. Moss, M. Kuhar, C. H. Emerson, et al.
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
J. Neurosci., December 15, 2000; 20(24): 9224 - 9234.
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 Am. J. Physiol. Endocrinol. Metab.Home page
J.-L. Wang, N. Chinookoswong, S. Yin, and Z.-Q. Shi
Calorigenic actions of leptin are additive to, but not dependent on, those of thyroid hormones
Am J Physiol Endocrinol Metab, December 1, 2000; 279(6): E1278 - E1285.
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E. Mihály, C. Fekete, J. B. Tatro, Z. Liposits, E. G. Stopa, and R. M. Lechan
Hypophysiotropic Thyrotropin-Releasing Hormone-Synthesizing Neurons in the Human Hypothalamus Are Innervated by Neuropeptide Y, Agouti-Related Protein, and {alpha}-Melanocyte-Stimulating Hormone
J. Clin. Endocrinol. Metab., July 1, 2000; 85(7): 2596 - 2603.
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 Pharmacol. Rev.Home page
A. Inui
Transgenic Approach to the Study of Body Weight Regulation
Pharmacol. Rev., March 1, 2000; 52(1): 35 - 62.
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C. Fekete, G. Legradi, E. Mihaly, Q.-H. Huang, J. B. Tatro, W. M. Rand, C. H. Emerson, and R. M. Lechan
alpha -Melanocyte-Stimulating Hormone Is Contained in Nerve Terminals Innervating Thyrotropin-Releasing Hormone-Synthesizing Neurons in the Hypothalamic Paraventricular Nucleus and Prevents Fasting-Induced Suppression of Prothyrotropin-Releasing Hormone Gene Expression
J. Neurosci., February 15, 2000; 20(4): 1550 - 1558.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
R. S. Ahima, J. Kelly, J. K. Elmquist, and J. S. Flier
Distinct Physiologic and Neuronal Responses to Decreased Leptin and Mild Hyperleptinemia
Endocrinology, November 1, 1999; 140(11): 4923 - 4931.
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 Endocr. Rev.Home page
E. A. Nillni and K. A. Sevarino
The Biology of pro-Thyrotropin-Releasing Hormone-Derived Peptides
Endocr. Rev., October 1, 1999; 20(5): 599 - 648.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
M. Ozata, I. C. Ozdemir, and J. Licinio
Human Leptin Deficiency Caused by a Missense Mutation: Multiple Endocrine Defects, Decreased Sympathetic Tone, and Immune System Dysfunction Indicate New Targets for Leptin Action, Greater Central than Peripheral Resistance to the Effects of Leptin, and Spontaneous Correction of Leptin-Mediated Defects
J. Clin. Endocrinol. Metab., October 1, 1999; 84(10): 3686 - 3695.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
T. M. Mizuno, H. Makimura, J. Silverstein, J. L. Roberts, T. Lopingco, and C. V. Mobbs
Fasting Regulates Hypothalamic Neuropeptide Y, Agouti-Related Peptide, and Proopiomelanocortin in Diabetic Mice Independent of Changes in Leptin or Insulin
Endocrinology, October 1, 1999; 140(10): 4551 - 4557.
[Abstract] [Full Text]

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 EndocrinologyHome page
L. Jacobson
Lower Weight Loss and Food Intake in Protein-Deprived, Corticotropin Releasing Hormone-Deficient Mice Correlate with Glucocorticoid Insufficiency
Endocrinology, August 1, 1999; 140(8): 3543 - 3551.
[Abstract] [Full Text]

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 EndocrinologyHome page
G. Légrádi and R. M. Lechan
Agouti-Related Protein Containing Nerve Terminals Innervate Thyrotropin-Releasing Hormone Neurons in the Hypothalamic Paraventricular Nucleus
Endocrinology, August 1, 1999; 140(8): 3643 - 3652.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
S. Reichlin
Editorial: Is Leptin a Secretion of the Brain?
J. Clin. Endocrinol. Metab., July 1, 1999; 84(7): 2267 - 2269.
[Full Text]

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 ANN INTERN MEDHome page
C. S. Mantzoros
The Role of Leptin in Human Obesity and Disease: A Review of Current Evidence
Ann Intern Med, April 20, 1999; 130(8): 671 - 680.
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 Physiol. Rev.Home page
E. Jequier and L. Tappy
Regulation of Body Weight in Humans
Physiol Rev, April 1, 1999; 79(2): 451 - 480.
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 J. Histochem. Cytochem.Home page
D. G. Baskin, M. W. Schwartz, R. J. Seeley, S. C. Woods, D. Porte , Jr., J. F. Breininger, Z. Jonak, J. Schaefer, M. Krouse, C. Burghardt, et al.
Leptin Receptor Long-form Splice-variant Protein Expression in Neuron Cell Bodies of the Brain and Co-localization with Neuropeptide Y mRNA in the Arcuate Nucleus
J. Histochem. Cytochem., March 1, 1999; 47(3): 353 - 362.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
M. P. Warren, F. Voussoughian, E. B. Geer, E. P. Hyle, C. L. Adberg, and R. H. Ramos
Functional Hypothalamic Amenorrhea: Hypoleptinemia and Disordered Eating
J. Clin. Endocrinol. Metab., March 1, 1999; 84(3): 873 - 877.
[Abstract] [Full Text]

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 EndocrinologyHome page
B. A. Henry, J. W. Goding, W. S. Alexander, A. J. Tilbrook, B. J. Canny, F. Dunshea, A. Rao, A. Mansell, and I. J. Clarke
Central Administration of Leptin to Ovariectomized Ewes Inhibits Food Intake without Affecting the Secretion of Hormones from the Pituitary Gland: Evidence for a Dissociation of Effects on Appetite and Neuroendocrine Function
Endocrinology, March 1, 1999; 140(3): 1175 - 1182.
[Abstract] [Full Text]

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T. L. Horvath, S. Diano, and A. N. van den Pol
Synaptic Interaction between Hypocretin (Orexin) and Neuropeptide Y Cells in the Rodent and Primate Hypothalamus: A Novel Circuit Implicated in Metabolic and Endocrine Regulations
J. Neurosci., February 1, 1999; 19(3): 1072 - 1087.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
H. Yang, P. Yuan, V. Wu, and Y. Taché
Feedback Regulation of Thyrotropin-Releasing Hormone Gene Expression by Thyroid Hormone in the Caudal Raphe Nuclei in Rats
Endocrinology, January 1, 1999; 140(1): 43 - 49.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
G. Van den Berghe, P. Wouters, L. Carlsson, R. C. Baxter, R. Bouillon, and C. Y. Bowers
Leptin Levels in Protracted Critical Illness: Effects of Growth Hormone-Secretagogues and Thyrotropin-Releasing Hormone
J. Clin. Endocrinol. Metab., September 1, 1998; 83(9): 3062 - 3070.
[Abstract] [Full Text]

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 EndocrinologyHome page
G. Legradi and R. M. Lechan
The Arcuate Nucleus Is the Major Source for Neuropeptide Y-Innervation of Thyrotropin-Releasing Hormone Neurons in the Hypothalamic Paraventricular Nucleus
Endocrinology, July 1, 1998; 139(7): 3262 - 3270.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
S. Diano, F. Naftolin, F. Goglia, and T. L. Horvath
Fasting-Induced Increase in Type II Iodothyronine Deiodinase Activity and Messenger Ribonucleic Acid Levels Is Not Reversed by Thyroxine in the Rat Hypothalamus
Endocrinology, June 1, 1998; 139(6): 2879 - 2884.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
J. S. Flier
What's in a Name? In Search of Leptin's Physiologic Role
J. Clin. Endocrinol. Metab., May 1, 1998; 83(5): 1407 - 1413.
[Full Text]

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 J. Clin. Endocrinol. Metab.Home page
R. Roubenoff, L. C. Rall, J. D. Veldhuis, J. J. Kehayias, C. Rosen, M. Nicolson, N. Lundgren, and S. Reichlin
The Relationship between Growth Hormone Kinetics and Sarcopenia in Postmenopausal Women: The Role of Fat Mass and Leptin
J. Clin. Endocrinol. Metab., May 1, 1998; 83(5): 1502 - 1506.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
J. K. Elmquist, R. S. Ahima, C. F. Elias, J. S. Flier, and C. B. Saper
Leptin activates distinct projections from the dorsomedial and ventromedial hypothalamic nuclei
PNAS, January 20, 1998; 95(2): 741 - 746.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
S.R. Bornstein, D.J. Torpy, G.P. Chrousos, J. Licinio, and L. Engelmann
Leptin Levels Are Elevated Despite Low Thyroid Hormone Levels in the "Euthyroid Sick" Syndromei
J. Clin. Endocrinol. Metab., December 1, 1997; 82(12): 4278 - 4279.
[Full Text] [PDF]

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 J. Biol. Chem.Home page
E. A. Nillni, C. Vaslet, M. Harris, A. Hollenberg, C. Bjorbak, and J. S. Flier
Leptin Regulates Prothyrotropin-releasing Hormone Biosynthesis. EVIDENCE FOR DIRECT AND INDIRECT PATHWAYS
J. Biol. Chem., November 10, 2000; 275(46): 36124 - 36133.
[Abstract] [Full Text] [PDF]


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