Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human
Preterm brain injury, occurring in approximately 30% of infants born <32 weeks gestational age, is associated with an increased risk of neurodevelopmental disorders, such as autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (ADHD). The mechanism of gray matter injury...
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Frontiers Media S.A.
2019-07-01
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Series: | Frontiers in Physiology |
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Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2019.00955/full |
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doaj-1c1f74d1b6ef498f92faa6f6306eddb8 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Helen B. Stolp Helen B. Stolp Bobbi Fleiss Bobbi Fleiss Bobbi Fleiss Yoko Arai Veena Supramaniam Regina Vontell Regina Vontell Sebastian Birtles Abi G. Yates Abi G. Yates Ana A. Baburamani Claire Thornton Claire Thornton Mary Rutherford A. David Edwards Pierre Gressens Pierre Gressens |
spellingShingle |
Helen B. Stolp Helen B. Stolp Bobbi Fleiss Bobbi Fleiss Bobbi Fleiss Yoko Arai Veena Supramaniam Regina Vontell Regina Vontell Sebastian Birtles Abi G. Yates Abi G. Yates Ana A. Baburamani Claire Thornton Claire Thornton Mary Rutherford A. David Edwards Pierre Gressens Pierre Gressens Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human Frontiers in Physiology parvalbumin perineuronal nets neuroinflammation mouse human |
author_facet |
Helen B. Stolp Helen B. Stolp Bobbi Fleiss Bobbi Fleiss Bobbi Fleiss Yoko Arai Veena Supramaniam Regina Vontell Regina Vontell Sebastian Birtles Abi G. Yates Abi G. Yates Ana A. Baburamani Claire Thornton Claire Thornton Mary Rutherford A. David Edwards Pierre Gressens Pierre Gressens |
author_sort |
Helen B. Stolp |
title |
Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human |
title_short |
Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human |
title_full |
Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human |
title_fullStr |
Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human |
title_full_unstemmed |
Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human |
title_sort |
interneuron development is disrupted in preterm brains with diffuse white matter injury: observations in mouse and human |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Physiology |
issn |
1664-042X |
publishDate |
2019-07-01 |
description |
Preterm brain injury, occurring in approximately 30% of infants born <32 weeks gestational age, is associated with an increased risk of neurodevelopmental disorders, such as autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (ADHD). The mechanism of gray matter injury in preterm born children is unclear and likely to be multifactorial; however, inflammation, a high predictor of poor outcome in preterm infants, has been associated with disrupted interneuron maturation in a number of animal models. Interneurons are important for regulating normal brain development, and disruption in interneuron development, and the downstream effects of this, has been implicated in the etiology of neurodevelopmental disorders. Here, we utilize postmortem tissue from human preterm cases with or without diffuse white matter injury (WMI; PMA range: 23+2 to 28+1 for non-WMI group, 26+6 to 30+0 for WMI group, p = 0.002) and a model of inflammation-induced preterm diffuse white matter injury (i.p. IL-1β, b.d., 10 μg/kg/injection in male CD1 mice from P1–5). Data from human preterm infants show deficits in interneuron numbers in the cortex and delayed growth of neuronal arbors at this early stage of development. In the mouse, significant reduction in the number of parvalbumin-positive interneurons was observed from postnatal day (P) 10. This decrease in parvalbumin neuron number was largely rectified by P40, though there was a significantly smaller number of parvalbumin positive cells associated with perineuronal nets in the upper cortical layers. Together, these data suggest that inflammation in the preterm brain may be a contributor to injury of specific interneuron in the cortical gray matter. This may represent a potential target for postnatal therapy to reduce the incidence and/or severity of neurodevelopmental disorders in preterm infants. |
topic |
parvalbumin perineuronal nets neuroinflammation mouse human |
url |
https://www.frontiersin.org/article/10.3389/fphys.2019.00955/full |
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doaj-1c1f74d1b6ef498f92faa6f6306eddb82020-11-25T00:19:15ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-07-011010.3389/fphys.2019.00955450351Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and HumanHelen B. Stolp0Helen B. Stolp1Bobbi Fleiss2Bobbi Fleiss3Bobbi Fleiss4Yoko Arai5Veena Supramaniam6Regina Vontell7Regina Vontell8Sebastian Birtles9Abi G. Yates10Abi G. Yates11Ana A. Baburamani12Claire Thornton13Claire Thornton14Mary Rutherford15A. David Edwards16Pierre Gressens17Pierre Gressens18Department for Comparative Biomedical Sciences, Royal Veterinary College, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomUniversité de Paris, NeuroDiderot, Inserm, Paris, FranceSchool of Health and Biomedical Sciences, RMIT University, Melbourne, VIC, AustraliaUniversité de Paris, NeuroDiderot, Inserm, Paris, FranceDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Neurology, University of Miami, Miller School of Medicine, Miami, FL, United StatesDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Pharmacology, University of Oxford, Oxford, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment for Comparative Biomedical Sciences, Royal Veterinary College, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomDepartment of Perinatal Imaging & Health, Centre for the Developing Brain, School of Biomedical Engineering and Imaging Science, King’s College London, London, United KingdomUniversité de Paris, NeuroDiderot, Inserm, Paris, FrancePreterm brain injury, occurring in approximately 30% of infants born <32 weeks gestational age, is associated with an increased risk of neurodevelopmental disorders, such as autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (ADHD). The mechanism of gray matter injury in preterm born children is unclear and likely to be multifactorial; however, inflammation, a high predictor of poor outcome in preterm infants, has been associated with disrupted interneuron maturation in a number of animal models. Interneurons are important for regulating normal brain development, and disruption in interneuron development, and the downstream effects of this, has been implicated in the etiology of neurodevelopmental disorders. Here, we utilize postmortem tissue from human preterm cases with or without diffuse white matter injury (WMI; PMA range: 23+2 to 28+1 for non-WMI group, 26+6 to 30+0 for WMI group, p = 0.002) and a model of inflammation-induced preterm diffuse white matter injury (i.p. IL-1β, b.d., 10 μg/kg/injection in male CD1 mice from P1–5). Data from human preterm infants show deficits in interneuron numbers in the cortex and delayed growth of neuronal arbors at this early stage of development. In the mouse, significant reduction in the number of parvalbumin-positive interneurons was observed from postnatal day (P) 10. This decrease in parvalbumin neuron number was largely rectified by P40, though there was a significantly smaller number of parvalbumin positive cells associated with perineuronal nets in the upper cortical layers. Together, these data suggest that inflammation in the preterm brain may be a contributor to injury of specific interneuron in the cortical gray matter. This may represent a potential target for postnatal therapy to reduce the incidence and/or severity of neurodevelopmental disorders in preterm infants.https://www.frontiersin.org/article/10.3389/fphys.2019.00955/fullparvalbuminperineuronal netsneuroinflammationmousehuman |