Neurite outgrowth deficits caused by rare PLXNB1 mutation in pediatric bipolar disorder
Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5–1% of children and teens in the United States. It is associated with recurrent episodes of mania and depression and an increased risk of suicidality. However, the genetics and neuropathology of PBD are largely...
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Published in | Molecular psychiatry Vol. 28; no. 6; pp. 2525 - 2539 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Nature Publishing Group UK
01.06.2023
Nature Publishing Group |
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Abstract | Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5–1% of children and teens in the United States. It is associated with recurrent episodes of mania and depression and an increased risk of suicidality. However, the genetics and neuropathology of PBD are largely unknown. Here, we used a combinatorial family-based approach to characterize cellular, molecular, genetic, and network-level deficits associated with PBD. We recruited a PBD patient and three unaffected family members from a family with a history of psychiatric illnesses. Using resting-state functional magnetic resonance imaging (rs-fMRI), we detected altered resting-state functional connectivity in the patient as compared to an unaffected sibling. Using transcriptomic profiling of patient and control induced pluripotent stem cell (iPSC)-derived telencephalic organoids, we found aberrant signaling in the molecular pathways related to neurite outgrowth. We corroborated the presence of neurite outgrowth deficits in patient iPSC-derived cortical neurons and identified a rare homozygous loss-of-function
PLXNB1
variant (c.1360C>C; p.Ser454Arg) responsible for the deficits in the patient. Expression of wild-type
PLXNB1
, but not the variant, rescued neurite outgrowth in patient neurons, and expression of the variant caused the neurite outgrowth deficits in cortical neurons from
PlxnB1
knockout mice. These results indicate that dysregulated PLXNB1 signaling may contribute to an increased risk of PBD and other mood dysregulation-related disorders by disrupting neurite outgrowth and functional brain connectivity. Overall, this study established and validated a novel family-based combinatorial approach for studying cellular and molecular deficits in psychiatric disorders and identified dysfunctional PLXNB1 signaling and neurite outgrowth as potential risk factors for PBD. |
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AbstractList | Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5-1% of children and teens in the United States. It is associated with recurrent episodes of mania and depression and an increased risk of suicidality. However, the genetics and neuropathology of PBD are largely unknown. Here, we used a combinatorial family-based approach to characterize cellular, molecular, genetic, and network-level deficits associated with PBD. We recruited a PBD patient and three unaffected family members from a family with a history of psychiatric illnesses. Using resting-state functional magnetic resonance imaging (rs-fMRI), we detected altered resting-state functional connectivity in the patient as compared to an unaffected sibling. Using transcriptomic profiling of patient and control induced pluripotent stem cell (iPSC)-derived telencephalic organoids, we found aberrant signaling in the molecular pathways related to neurite outgrowth. We corroborated the presence of neurite outgrowth deficits in patient iPSC-derived cortical neurons and identified a rare homozygous loss-of-function PLXNB1 variant (c.1360C>C; p.Ser454Arg) responsible for the deficits in the patient. Expression of wild-type PLXNB1, but not the variant, rescued neurite outgrowth in patient neurons, and expression of the variant caused the neurite outgrowth deficits in cortical neurons from PlxnB1 knockout mice. These results indicate that dysregulated PLXNB1 signaling may contribute to an increased risk of PBD and other mood dysregulation-related disorders by disrupting neurite outgrowth and functional brain connectivity. Overall, this study established and validated a novel family-based combinatorial approach for studying cellular and molecular deficits in psychiatric disorders and identified dysfunctional PLXNB1 signaling and neurite outgrowth as potential risk factors for PBD.Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5-1% of children and teens in the United States. It is associated with recurrent episodes of mania and depression and an increased risk of suicidality. However, the genetics and neuropathology of PBD are largely unknown. Here, we used a combinatorial family-based approach to characterize cellular, molecular, genetic, and network-level deficits associated with PBD. We recruited a PBD patient and three unaffected family members from a family with a history of psychiatric illnesses. Using resting-state functional magnetic resonance imaging (rs-fMRI), we detected altered resting-state functional connectivity in the patient as compared to an unaffected sibling. Using transcriptomic profiling of patient and control induced pluripotent stem cell (iPSC)-derived telencephalic organoids, we found aberrant signaling in the molecular pathways related to neurite outgrowth. We corroborated the presence of neurite outgrowth deficits in patient iPSC-derived cortical neurons and identified a rare homozygous loss-of-function PLXNB1 variant (c.1360C>C; p.Ser454Arg) responsible for the deficits in the patient. Expression of wild-type PLXNB1, but not the variant, rescued neurite outgrowth in patient neurons, and expression of the variant caused the neurite outgrowth deficits in cortical neurons from PlxnB1 knockout mice. These results indicate that dysregulated PLXNB1 signaling may contribute to an increased risk of PBD and other mood dysregulation-related disorders by disrupting neurite outgrowth and functional brain connectivity. Overall, this study established and validated a novel family-based combinatorial approach for studying cellular and molecular deficits in psychiatric disorders and identified dysfunctional PLXNB1 signaling and neurite outgrowth as potential risk factors for PBD. Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5-1% of children and teens in the United States. It is associated with recurrent episodes of mania and depression and an increased risk of suicidality. However, the genetics and neuropathology of PBD are largely unknown. Here, we used a combinatorial family-based approach to characterize cellular, molecular, genetic, and network-level deficits associated with PBD. We recruited a PBD patient and three unaffected family members from a family with a history of psychiatric illnesses. Using resting-state functional magnetic resonance imaging (rs-fMRI), we detected altered resting-state functional connectivity in the patient as compared to an unaffected sibling. Using transcriptomic profiling of patient and control induced pluripotent stem cell (iPSC)-derived telencephalic organoids, we found aberrant signaling in the molecular pathways related to neurite outgrowth. We corroborated the presence of neurite outgrowth deficits in patient iPSC-derived cortical neurons and identified a rare homozygous loss-of-function PLXNB1 variant (c.1360C>C; p.Ser454Arg) responsible for the deficits in the patient. Expression of wild-type PLXNB1, but not the variant, rescued neurite outgrowth in patient neurons, and expression of the variant caused the neurite outgrowth deficits in cortical neurons from PlxnB1 knockout mice. These results indicate that dysregulated PLXNB1 signaling may contribute to an increased risk of PBD and other mood dysregulation-related disorders by disrupting neurite outgrowth and functional brain connectivity. Overall, this study established and validated a novel family-based combinatorial approach for studying cellular and molecular deficits in psychiatric disorders and identified dysfunctional PLXNB1 signaling and neurite outgrowth as potential risk factors for PBD. Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5–1% of children and teens in the United States. It is associated with recurrent episodes of mania and depression and an increased risk of suicidality. However, the genetics and neuropathology of PBD are largely unknown. Here, we used a combinatorial family-based approach to characterize cellular, molecular, genetic, and network-level deficits associated with PBD. We recruited a PBD patient and three unaffected family members from a family with a history of psychiatric illnesses. Using resting-state functional magnetic resonance imaging (rs-fMRI), we detected altered resting-state functional connectivity in the patient as compared to an unaffected sibling. Using transcriptomic profiling of patient and control induced pluripotent stem cell (iPSC)-derived telencephalic organoids, we found aberrant signaling in the molecular pathways related to neurite outgrowth. We corroborated the presence of neurite outgrowth deficits in patient iPSC-derived cortical neurons and identified a rare homozygous loss-of-function PLXNB1 variant (c.1360C>C; p.Ser454Arg) responsible for the deficits in the patient. Expression of wild-type PLXNB1 , but not the variant, rescued neurite outgrowth in patient neurons, and expression of the variant caused the neurite outgrowth deficits in cortical neurons from PlxnB1 knockout mice. These results indicate that dysregulated PLXNB1 signaling may contribute to an increased risk of PBD and other mood dysregulation-related disorders by disrupting neurite outgrowth and functional brain connectivity. Overall, this study established and validated a novel family-based combinatorial approach for studying cellular and molecular deficits in psychiatric disorders and identified dysfunctional PLXNB1 signaling and neurite outgrowth as potential risk factors for PBD. |
Author | Libowitz, Mark Yang, Guang Coon, Hilary Anderson, Jeffrey S. King, Jace B. Yandell, Mark Parker, Ethan Maguire, Colin Ullah, H. M. Arif Gorsi, Bushra Lopez-Larson, Melissa Shcheglovitov, Alex |
Author_xml | – sequence: 1 givenname: Guang orcidid: 0000-0001-9754-3543 surname: Yang fullname: Yang, Guang organization: Department of Neurobiology, University of Utah, Neuroscience Graduate Program, University of Utah – sequence: 2 givenname: H. M. Arif orcidid: 0000-0001-6874-3095 surname: Ullah fullname: Ullah, H. M. Arif organization: Department of Neurobiology, University of Utah – sequence: 3 givenname: Ethan surname: Parker fullname: Parker, Ethan organization: Department of Biomedical Engineering, University of Utah – sequence: 4 givenname: Bushra surname: Gorsi fullname: Gorsi, Bushra organization: Department of Human Genetics, University of Utah, Utah Center for Genetic Discovery – sequence: 5 givenname: Mark surname: Libowitz fullname: Libowitz, Mark organization: Department of Neurobiology, University of Utah – sequence: 6 givenname: Colin surname: Maguire fullname: Maguire, Colin organization: Clinical & Translational Research Core, Utah Clinical & Translational Research Institute – sequence: 7 givenname: Jace B. surname: King fullname: King, Jace B. organization: Department of Radiology, University of Utah – sequence: 8 givenname: Hilary surname: Coon fullname: Coon, Hilary organization: Department of Psychiatry, University of Utah – sequence: 9 givenname: Melissa surname: Lopez-Larson fullname: Lopez-Larson, Melissa organization: Department of Psychiatry, University of Utah, Lopez-Larson and Associates – sequence: 10 givenname: Jeffrey S. orcidid: 0000-0002-9669-3846 surname: Anderson fullname: Anderson, Jeffrey S. organization: Department of Radiology, University of Utah – sequence: 11 givenname: Mark orcidid: 0000-0002-9497-4505 surname: Yandell fullname: Yandell, Mark organization: Department of Human Genetics, University of Utah – sequence: 12 givenname: Alex orcidid: 0000-0001-8359-9650 surname: Shcheglovitov fullname: Shcheglovitov, Alex email: alexsh@neuro.utah.edu organization: Department of Neurobiology, University of Utah, Neuroscience Graduate Program, University of Utah, Department of Biomedical Engineering, University of Utah, Clinical & Translational Research Core, Utah Clinical & Translational Research Institute, Department of Psychiatry, University of Utah |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37032361$$D View this record in MEDLINE/PubMed |
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Snippet | Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5–1% of children and teens in the United States. It is associated with... Pediatric bipolar disorder (PBD) is a severe mood dysregulation condition that affects 0.5-1% of children and teens in the United States. It is associated with... |
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Title | Neurite outgrowth deficits caused by rare PLXNB1 mutation in pediatric bipolar disorder |
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