A subpopulation of embryonic microglia respond to maternal stress and influence nearby neural progenitors

Rosin, Jessica M.; Sinha, Sarthak; Biernaskie, Jeff; Kurrasch, Deborah M.

doi:10.1016/j.devcel.2021.03.018

Cited by 32 publications

(41 citation statements)

References 80 publications

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“…It is very interesting to note, that the year after, using the same chemical agent (PLX5622), another research group reached the opposite conclusion [43]. In effect, in this study the authors show that depleting microglia after contusive SCI enhances functional recovery [44]. Interestingly, in this article, the authors explore a new field of investigation at the border between regenerative and cognitive sciences.…”

Section: Modulation Of the Spinal Cord Plasticitymentioning

confidence: 68%

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Plasticity of the Injured Spinal Cord

Guérout

2021

Cells

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Complete spinal cord injury (SCI) leads to permanent motor, sensitive and sensory deficits. In humans, there is currently no therapy to promote recovery and the only available treatments include surgical intervention to prevent further damage and symptomatic relief of pain and infections in the acute and chronic phases, respectively. Basically, the spinal cord is classically viewed as a nonregenerative tissue with limited plasticity. Thereby the establishment of the “glial” scar which appears within the SCI is mainly described as a hermetic barrier for axon regeneration. However, recent discoveries have shed new light on the intrinsic functional plasticity and endogenous recovery potential of the spinal cord. In this review, we will address the different aspects that the spinal cord plasticity can take on. Indeed, different experimental paradigms have demonstrated that axonal regrowth can occur even after complete SCI. Moreover, recent articles have demonstrated too that the “glial” scar is in fact composed of several cellular populations and that each of them exerts specific roles after SCI. These recent discoveries underline the underestimation of the plasticity of the spinal cord at cellular and molecular levels. Finally, we will address the modulation of this endogenous spinal cord plasticity and the perspectives of future therapeutic opportunities which can be offered by modulating the injured spinal cord microenvironment.

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Section: Modulation Of the Spinal Cord Plasticitymentioning

confidence: 68%

“…The role played by microglia on behavior, according to the sex, has been underlined recently [43]. Indeed, in this publication, the authors describe that gestational cold stress alters social behavior in adult male mice in a microglia-dependent manner [44].…”

Section: Modulation Of the Spinal Cord Plasticitymentioning

confidence: 97%

Plasticity of the Injured Spinal Cord

Guérout

2021

Cells

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“…Furthermore, maternal inflammation causes abnormal microglial distribution and motility in the embryonic stage (Squarzoni et al 2014 ; Ozaki et al 2020 ). Maternal cold stress affects microglial effects on nearby neural progenitors in a sexually dimorphic manner in the embryonic hypothalamus (Rosin et al 2021 ). Taken together, these findings suggest that microglial characterization is determined through both an intrinsic transcriptional program and extrinsic environmental factors.…”

Section: Discussionmentioning

confidence: 99%

The behavior and functions of embryonic microglia

Hattori

2021

Anat Sci Int

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Microglia are the resident immune cells of the central nervous system. Microglial progenitors are generated in the yolk sac during the early embryonic stage. Once microglia enter the brain primordium, these cells colonize the structure through migration and proliferation during brain development. Microglia account for a minor population among the total cells that constitute the developing cortex, but they can associate with many surrounding neural lineage cells by extending their filopodia and through their broad migration capacity. Of note, microglia change their distribution in a stage-dependent manner in the developing brain: microglia are homogenously distributed in the pallium in the early and late embryonic stages, whereas these cells are transiently absent from the cortical plate (CP) from embryonic day (E) 15 to E16 and colonize the ventricular zone (VZ), subventricular zone (SVZ), and intermediate zone (IZ). Previous studies have reported that microglia positioned in the VZ/SVZ/IZ play multiple roles in neural lineage cells, such as regulating neurogenesis, cell survival and neuronal circuit formation. In addition to microglial functions in the zones in which microglia are replenished, these cells indirectly contribute to the proper maturation of post-migratory neurons by exiting the CP during the mid-embryonic stage. Overall, microglial time-dependent distributional changes are necessary to provide particular functions that are required in specific regions. This review summarizes recent advances in the understanding of microglial colonization and multifaceted functions in the developing brain, especially focusing on the embryonic stage, and discuss the molecular mechanisms underlying microglial behaviors.

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“…Increased microglial-mediated neuroinflammation has been seen in numerous NDDs, including ASD (Morgan et al, 2010;Tetreault et al, 2012;Suzuki et al, 2013;Gupta et al, 2014;Lee et al, 2017), schizophrenia (Garey, 2010;Sellgren et al, 2019;Chini et al, 2020), ADHD (Anand et al, 2017), and TS (Lennington et al, 2016). Microglia in the developing brain are also sensitive to external perturbations such as maternal infections (Smolders et al, 2015;Bernstein et al, 2016;Rosin et al, 2021a;Rosin et al, 2021b). Microglia are thought to initiate an immune response to protect the brain, but altered microglial activity has also been implicated in disorders of neurodevelopment and neurodegeneration through an upregulation of neuroinflammation (Kettenmann et al, 2011;Salter and Stevens, 2017).…”

Section: Microglia and Neuroinflammationmentioning

confidence: 99%

Histamine, Neuroinflammation and Neurodevelopment: A Review

Carthy

Ellender

2021

Front. Neurosci.

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The biogenic amine, histamine, has been shown to critically modulate inflammatory processes as well as the properties of neurons and synapses in the brain, and is also implicated in the emergence of neurodevelopmental disorders. Indeed, a reduction in the synthesis of this neuromodulator has been associated with the disorders Tourette’s syndrome and obsessive-compulsive disorder, with evidence that this may be through the disruption of the corticostriatal circuitry during development. Furthermore, neuroinflammation has been associated with alterations in brain development, e.g., impacting synaptic plasticity and synaptogenesis, and there are suggestions that histamine deficiency may leave the developing brain more vulnerable to proinflammatory insults. While most studies have focused on neuronal sources of histamine it remains unclear to what extent other (non-neuronal) sources of histamine, e.g., from mast cells and other sources, can impact brain development. The few studies that have started exploring this in vitro, and more limited in vivo, would indicate that non-neuronal released histamine and other preformed mediators can influence microglial-mediated neuroinflammation which can impact brain development. In this Review we will summarize the state of the field with regard to non-neuronal sources of histamine and its impact on both neuroinflammation and brain development in key neural circuits that underpin neurodevelopmental disorders. We will also discuss whether histamine receptor modulators have been efficacious in the treatment of neurodevelopmental disorders in both preclinical and clinical studies. This could represent an important area of future research as early modulation of histamine from neuronal as well as non-neuronal sources may provide novel therapeutic targets in these disorders.

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A subpopulation of embryonic microglia respond to maternal stress and influence nearby neural progenitors

Cited by 32 publications

References 80 publications

Plasticity of the Injured Spinal Cord

Plasticity of the Injured Spinal Cord

The behavior and functions of embryonic microglia

Histamine, Neuroinflammation and Neurodevelopment: A Review

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