Hypothalamic neuroglial plasticity is regulated by anti-Müllerian hormone and disrupted in polycystic ovary syndrome.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Apr 2023
Historique:
received: 20 12 2022
revised: 03 03 2023
accepted: 08 03 2023
medline: 18 4 2023
pubmed: 1 4 2023
entrez: 31 3 2023
Statut: ppublish

Résumé

Polycystic ovary syndrome (PCOS) is the most common reproductive-endocrine disorder affecting between 5 and 18% of women worldwide. An elevated frequency of pulsatile luteinizing hormone (LH) secretion and higher serum levels of anti-Müllerian hormone (AMH) are frequently observed in women with PCOS. The origin of these abnormalities is, however, not well understood. We studied brain structure and function in women with and without PCOS using proton magnetic resonance spectroscopy (MRS) and diffusion tensor imaging combined with fiber tractography. Then, using a mouse model of PCOS, we investigated by electron microscopy whether AMH played a role on the regulation of hypothalamic structural plasticity. Increased AMH serum levels are associated with increased hypothalamic activity/axonal-glial signalling in PCOS patients. Furthermore, we demonstrate that AMH promotes profound micro-structural changes in the murine hypothalamic median eminence (ME), creating a permissive environment for GnRH secretion. These include the retraction of the processes of specialized AMH-sensitive ependymo-glial cells called tanycytes, allowing more GnRH neuron terminals to approach ME blood capillaries both during the run-up to ovulation and in a mouse model of PCOS. We uncovered a central function for AMH in the regulation of fertility by remodeling GnRH terminals and their tanycytic sheaths, and provided insights into the pivotal role of the brain in the establishment and maintenance of neuroendocrine dysfunction in PCOS. INSERM (U1172), European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement n° 725149), CHU de Lille, France (Bonus H).

Sections du résumé

BACKGROUND BACKGROUND
Polycystic ovary syndrome (PCOS) is the most common reproductive-endocrine disorder affecting between 5 and 18% of women worldwide. An elevated frequency of pulsatile luteinizing hormone (LH) secretion and higher serum levels of anti-Müllerian hormone (AMH) are frequently observed in women with PCOS. The origin of these abnormalities is, however, not well understood.
METHODS METHODS
We studied brain structure and function in women with and without PCOS using proton magnetic resonance spectroscopy (MRS) and diffusion tensor imaging combined with fiber tractography. Then, using a mouse model of PCOS, we investigated by electron microscopy whether AMH played a role on the regulation of hypothalamic structural plasticity.
FINDINGS RESULTS
Increased AMH serum levels are associated with increased hypothalamic activity/axonal-glial signalling in PCOS patients. Furthermore, we demonstrate that AMH promotes profound micro-structural changes in the murine hypothalamic median eminence (ME), creating a permissive environment for GnRH secretion. These include the retraction of the processes of specialized AMH-sensitive ependymo-glial cells called tanycytes, allowing more GnRH neuron terminals to approach ME blood capillaries both during the run-up to ovulation and in a mouse model of PCOS.
INTERPRETATION CONCLUSIONS
We uncovered a central function for AMH in the regulation of fertility by remodeling GnRH terminals and their tanycytic sheaths, and provided insights into the pivotal role of the brain in the establishment and maintenance of neuroendocrine dysfunction in PCOS.
FUNDING BACKGROUND
INSERM (U1172), European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement n° 725149), CHU de Lille, France (Bonus H).

Identifiants

pubmed: 37001236
pii: S2352-3964(23)00100-7
doi: 10.1016/j.ebiom.2023.104535
pmc: PMC10070524
pii:
doi:

Substances chimiques

Luteinizing Hormone 9002-67-9
Anti-Mullerian Hormone 80497-65-0
Gonadotropin-Releasing Hormone 33515-09-2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104535

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests A.-L.B. received a honorarium from Merck-Serono for a booklet writing on the use of AMH in Assisted Reproductive Technology; G.K. was a recipient of a Research Grant from Société Française de Neuroradiologie that covered part of his salary. All the other authors have declared that no conflict of interest exists.

Auteurs

Anne-Laure Barbotin (AL)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France; CHU Lille, Institut de Biologie de la Reproduction-Spermiologie-CECOS, Lille F-59000, France.

Nour El Houda Mimouni (NEH)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France.

Grégory Kuchcinski (G)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France; CHU Lille, Department of Neuroradiology, Lille F-59000, France.

Renaud Lopes (R)

CHU Lille, Department of Neuroradiology, Lille F-59000, France.

Romain Viard (R)

Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, US 41 - UAR 2014 - PLBS, Lille F-59000, France.

Sowmyalakshmi Rasika (S)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France.

Daniele Mazur (D)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France.

Mauro S B Silva (MSB)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France.

Virginie Simon (V)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France.

Angèle Boursier (A)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France; CHU Lille, Institut de Biologie de la Reproduction-Spermiologie-CECOS, Lille F-59000, France.

Jean-Pierre Pruvo (JP)

CHU Lille, Department of Neuroradiology, Lille F-59000, France.

Qiang Yu (Q)

Experimental Pharmacology, Center for Molecular Signalling (PZMS), Saarland University School of Medicine, Homburg 66123, Germany.

Michael Candlish (M)

Experimental Pharmacology, Center for Molecular Signalling (PZMS), Saarland University School of Medicine, Homburg 66123, Germany.

Ulrich Boehm (U)

Experimental Pharmacology, Center for Molecular Signalling (PZMS), Saarland University School of Medicine, Homburg 66123, Germany.

Federica Dal Bello (FD)

Department of Molecular Biotechnology and Health Science, University of Turin, Turin 10125, Italy.

Claudio Medana (C)

Department of Molecular Biotechnology and Health Science, University of Turin, Turin 10125, Italy.

Pascal Pigny (P)

CHU Lille, Service de Biochimie et Hormonologie, Centre de Biologie Pathologie, Lille F-59000, France.

Didier Dewailly (D)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France.

Vincent Prevot (V)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France.

Sophie Catteau-Jonard (S)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France; CHU Lille, Service de Gynécologie Médicale, Hôpital Jeanne de Flandre, Lille F-59000, France.

Paolo Giacobini (P)

Univ. Lille, Inserm, CHU Lille, U1172 - LilNCog - Lille Neuroscience & Cognition, Lille F-59000, France. Electronic address: paolo.giacobini@inserm.fr.

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Classifications MeSH