L’Organisation Mondiale de la Santé a évalué qu’au moins 15 millions de nouveau-nés naissent prématurément chaque année (37 ou 40 semaines avant le terme). Mondialement, cela représente environ 1 nourrisson prématuré sur 10. Sur ces 15 millions de nourrissons nés prématurément, environ 1 million ne survivra pas et une large proportion des survivants présentera des déficiences neurocomportementales permanentes (Harrison et Goldenberg, 2016; Liu et al., 2016). Les nourrissons nés prématurément semblent posséder un QI inférieur et moins performant que leurs congénères du même âge nés à terme dans certains domaines cognitifs tels que les fonctions exécutives, le traitement du langage et le fonctionnement de la mémoire (Cheong et al., 2017; Doyle et al., 2015; Moore et al., 2012; Pascoe et al., 2013; Raju et al., 2017; Spittle et al., 2017). Ces déficiences commencent à s’observer au début de l’enfance et sont permanentes ; ces observations ont été faites dans de grands groupes de nourrissons nés prématurément jusqu’à l’adolescence et à l’âge adulte tardif (Healy et al., 2013; Heinonen et al., 2015). La gravité des résultats de ces personnes nées prématurément est directement liée à la gravité de la naissance prématurée et elle est modulée par de nombreux facteurs qui seront étudiés ci-après (c.-à-d. inflammation, stress, génétique). De plus, comparé aux enfants nés à terme, les prématurés extrêmes (naissance 28 semaines avant le terme de la grossesse) ont entre 10 et 17 fois plus de risque de développer un TSA (Joseph et al., 2017; Leviton et al., 2018; Limperopoulos et al., 2008a). Les enfants prématurés et nés à terme atteints d’un TSA ne présentent pas exactement les mêmes phénotypes : les enfants prématurés présentent généralement un sous-type de TSA avec des troubles de la communication et sociaux mais ils ne présentent pas de comportements répétés et stéréotypés (Johnson et al., 2010).
Chez les nourrissons nés à terme, il est largement reconnu qu’un TSA est lié à une association de facteurs génétiques et environnementaux dont la proportion de chacun de ces facteurs est différente selon l’individu (Kim and Leventhal, 2015). Chez les enfants prématurés, une lésion cérébrale, appelée « encéphalopathie du prématuré », est souvent la conséquence d’une neuro-inflammation, générée par les cellules microgliales et les astrocytes. L’encéphalopathie du prématuré est en partie caractérisée par des anomalies de la substance blanche et des troubles synaptiques (Kinney, 2009). À l’instar d’un nombre significatif de nouveau-nés prématurés, les nourrissons nés à terme de la même famille développeront un TSA (notre argument principal est que l’exposition à une neuro-inflammation sur l’équivalent du dernier trimestre est un facteur environnemental important dans le développement d’un TSA). En effet, le seul facteur de risque principal pour une naissance prématurée est l’infection/inflammation entre la mère et le fœtus : entre 25 et 40 % des naissances prématurées sont liées à des infections dues, soit à la rupture prématurée des membranes, soit à un diagnostic non établi. De plus, les nouveau-nés prématurés sont souvent exposés à des infections néonatales telles que la septicémie néonatale, la ventilation mécanique et l’entérocolite nécrotique (Hagberg et al., 2015; Joseph et al., 2017; Kuban et al., 2015; Leviton et al., 2018). En réponse à l’infection à l’inflammation, les cellules immunitaires du système produisent une multitude de cytokines et de chimiokines (McElrath et al., 2011; Menon et al., 2009). Grâce à un mécanisme pas tout à fait connu qui impliquerait vraisemblablement la cyclooxygénase inductible des cellules endothéliales et le nerf vague, l’inflammation du système induit une neuroinflammation principalement générée par les cellules microgliales et les astrocytes. Cette neuroinflammation joue un rôle central dans la pathogenèse de l’encéphalopathie du prématuré.
Les marqueurs neuropathologiques de l’encéphalopathie du prématuré ainsi que l’imagerie rappellent ce qui a été décrit dans des études post-mortem chez les patients atteints d’un TSA : trouble de la myélinisation liée à un trouble de la maturation des oligodendrocytes, connectivité réduite, anomalie de la fonction synaptique et diminution de certaines classes d’interneurones (Billiards et al., 2008; Buser et al., 2012; Verney et al., 2012a, Ball et al., 2013b; Eaton-Rosen et al., 2017; Garcia et al., 2018; Kelly et al., 2015; Vinall et al., 2013).
Les cellules microgliales sont les cellules immunitaires résiduelles du cerveau et de la moelle épinière dérivées de progéniteurs myéloïdes du sac vitellin qui migrent vers le neuro-épithélium lors du développement embryonnaire précoce pour devenir effecteurs du développement et de l’homéostasie du cerveau (Ginhoux et al., 2010; Kierdorf et al., 2013; Tay et al., 2017b). Les cellules microgliales expriment une multitude de récepteurs tels que les récepteurs des cytokines/chimiokines, et de récepteurs membranaires reconnaissant des motifs moléculaires associés aux dégâts cellulaires et des motifs moléculaires associés à des pathogènes de façon à détecter les modifications environnementales. En plus de leurs fonctions immunitaires, les cellules microgliales ont un rôle à la fois spécifique et critique durant le développement normal du cerveau et tout au long de la vie . Lors de la neurogenèse, les cellules microgliales favorisent la mort sélective des cellules progénitrices neuronales dans différentes régions en produisant des DRO et en phagocytant les cellules étrangères (Sierra et al., 2010). Par opposition, les cellules microgliales favorisent la survie des neurones de la couche V (Ueno et al., 2013) ainsi que le niveau de fonctionnement de maturation en exprimant le gène IGF1 (Wlodarczyk et al., 2017). Dans la substance blanche, les cellules microgliales sont connues pour favoriser la fasciculation axonale, tandis que les axones voisins qui se déplacent simultanément adhèrent l’un à l’autre. Les cellules microgliales sont également importantes pour assurer la myélinisation normale (Wlodarczyk et al., 2017). Les cellules microgliales contribuent également à l’assemblage de circuits en contrôlant la position laminaire d’interneurones somatosensoriels (Pont-Lezica et al., 2014; Squarzoni et al., 2014; Ueno et al., 2013). Une autre fonction principale des cellules microgliales lors du développement est leur interférence au niveau de mécanismes de formation et d’élagage synaptiques. De récentes études ont démontré que les cellules microgliales de P8 à P10 favorisaient le rôle des filopodia dans la formation synaptique induite par le Ca2+ (Miyamoto et al., 2016). De plus, de P8 à P21, les cellules microgliales induisent l’élagage synaptique en marquant les synapses les plus faibles avec un système complémentaire. Elles sont ensuite phagocytées (Paolicelli et al., 2011). Cala renforce la résistance et la plasticité des synapses.
Le fait que chaque perturbation de ces fonctions neuro-développementales normales soit associée à un TSA ne signifie rien (Fernandez de Cossio et al., 2017; Jawaid et al., 2018; Li and Barres, 2018; Miyamoto et al., 2016; Pierre et al., 2017; Tay et al., 2017a; Tay et al., 2017b; Thion and Garel, 2017). Dans les cerveaux des prématurés post-mortem, notre équipe a antérieurement démontré que les lésions kystiques étaient plus entourées par des cellules microgliales, comparé aux cerveaux des personnes nées à terme. Cela suggère que l’activation des cellules microgliales pourrait être un élément clef dans les anomalies de la substance blanche et de la substance grise (Hagberg et al., 2016; Hagberg et al., 2002; Verney et al., 2012a; Verney et al., 2010b). Cette association entre microgliose et lésion a été observée et étudiée dans des modèles de lésion cérébrale périnatale (Baud et al., 2004; Dean et al., 2009; Favrais et al., 2011; Fleiss et al., 2012; Kaur et al., 2013; Ophelders et al., 2016; Schmitz et al., 2014; Tahraoui et al., 2001)(Baburamani et al., 2014).
L’analyse transcriptomique des cellules microgliales chez une souris atteinte d’encéphalopathie du prématuré a révélé que non seulement ces cellules étaient polarisées vers un phénotype proinflammatoire mais également que de nombreuses transcriptions correspondant à la fonction normale des cellules microgliales durant le développement du cerveau étaient significativement inhibées (Krishnan et al., 2017). Cela suggère que ces cellules microgliales immatures perdent leurs fonctions développementale et homéostatique suite à un stimulus inflammatoire.
Pierre GRESSENS
PROTECT, INSERM
Université Paris Diderot,
Sorbonne Paris Cité, F-75019 Paris, France
Centre for the Developing Brain
Department of Division of Imaging Sciences and
Biomedical Engineering
King’s College London, King’s Health Partners
St. Thomas’ Hospital, London, SE1 7EH,
France – United Kingdom
Article extrait du :
LIVRE BLANC SCIENTIFIQUE INTERNATIONAL DE L’AUTISME – ENG_FR
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