Meningiomas from a developmental perspective: exploring the crossroads between meningeal embryology and tumorigenesis

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REVIEW ARTICLE - TUMOR - MENINGIOMA

Meningiomas from a developmental perspective: exploring the crossroads between meningeal embryology and tumorigenesis Julien Boetto 1

&

Matthieu Peyre 2 & Michel Kalamarides 2

Received: 12 October 2020 / Accepted: 12 November 2020 # Springer-Verlag GmbH Austria, part of Springer Nature 2020

Abstract Meningiomas are tumors arising from the meninges and represent the most frequent central nervous system tumors in adults. Recent large-scale genetic studies and preclinical meningioma mouse modelling led to a better comprehension of meningioma development and suggested evidences of close relationships between meningeal embryology and tumorigenesis. In this nonsystematic review, we summarize the current knowledge on meningeal embryology and developmental biology, and illustrate how meningioma tumorigenesis is deeply related to meningeal embryology, concerning the potential cell of origin, the role of reactivation of embryonic stem cells, the influence of the embryonic tissue of origin, and the parallelism between topographydependant molecular pathways involved in normal meninges and in meningioma development. Our study emphasizes why future studies on meningeal embryology are mandatory to affine our comprehension of mechanisms underlying meningioma initiation and development. Keywords Meningioma . Embryological development

Introduction The human central nervous system (CNS) is surrounded by three layers of membranes called the meninges. They are divided primarily into the dura mater (or pachymeninx) and the arachnoid and pia mater (leptomeninges) [24]. The meninges provide a mechanical protection to the underlying soft neural tissue of the brain and the spinal cord and contain space through which cerebrospinal fluid (CSF) travels around the CNS. In addition to this structural role, leptomeninges have complex functions as barriers and facilitators for the movement of fluid, solutes, and cell at the surface and within the CNS, playing a fundamental role in nutrition [74]. During the embryonic period, there are evidences that meninges are This article is part of the Topical Collection on Tumor - Meningioma * Julien Boetto [email protected] 1

Neurosurgery Department, Gui de Chauliac Hospital, Montpellier University Medical Center, 91 avenue Augustin Fliche, 34090 Montpellier, France

2

APHP, Groupe Hospitalo-Universitaire Pitié-Salpétrière, Neurosurgery Department, Sorbonne Université, Paris, France

actively involved in development of the brain and the calvaria and serve as a stem cell niche postnatally [2, 17, 66]. Tumors arising from the meninges are called meningiomas and represent the most common primary CNS tumor in adults [56]. One of the most intriguing characteristics of meningiomas is the huge diversity of their histologic subtypes (15 different subtypes are described in the WHO classification of brain tumors): meningiomas are classified into three prognostic histological groups following the WHO classification: grade I (65–80%), grade II (20–35%, atypical), and grade