Tbx1, a gene encoded in 22q11.2 copy number variant, is a link between alterations in fimbria myelination and cognitive speed in mice
Copy number variants (CNVs) have provided a reliable entry point to identify the structural correlates of atypical cognitive development. Hemizygous deletion of human chromosome 22q11.2 is associated with impaired cognitive function; however, the mechanisms by which the CNVs contribute to cognitive...
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Published in | Molecular psychiatry Vol. 27; no. 2; pp. 929 - 938 |
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Main Authors | , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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London
Nature Publishing Group UK
01.02.2022
Nature Publishing Group |
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Abstract | Copy number variants (CNVs) have provided a reliable entry point to identify the structural correlates of atypical cognitive development. Hemizygous deletion of human chromosome 22q11.2 is associated with impaired cognitive function; however, the mechanisms by which the CNVs contribute to cognitive deficits via diverse structural alterations in the brain remain unclear. This study aimed to determine the cellular basis of the link between alterations in brain structure and cognitive functions in mice with a heterozygous deletion of
Tbx1
, one of the 22q11.2-encoded genes. Ex vivo whole-brain diffusion-tensor imaging (DTI)–magnetic resonance imaging (MRI) in
Tbx1
heterozygous mice indicated that the fimbria was the only region with significant myelin alteration. Electron microscopic and histological analyses showed that
Tbx1
heterozygous mice exhibited an apparent absence of large myelinated axons and thicker myelin in medium axons in the fimbria, resulting in an overall decrease in myelin. The fimbria of
Tbx1
heterozygous mice showed reduced mRNA levels of
Ng2
, a gene required to produce oligodendrocyte precursor cells. Moreover, postnatal progenitor cells derived from the subventricular zone, a source of oligodendrocytes in the fimbria, produced fewer oligodendrocytes in vitro. Behavioral analyses of these mice showed selectively slower acquisition of spatial memory and cognitive flexibility with no effects on their accuracy or sensory or motor capacities. Our findings provide a genetic and cellular basis for the compromised cognitive speed in patients with 22q11.2 hemizygous deletion. |
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AbstractList | Copy number variants (CNVs) have provided a reliable entry point to identify the structural correlates of atypical cognitive development. Hemizygous deletion of human chromosome 22q11.2 is associated with impaired cognitive function; however, the mechanisms by which the CNVs contribute to cognitive deficits via diverse structural alterations in the brain remain unclear. This study aimed to determine the cellular basis of the link between alterations in brain structure and cognitive functions in mice with a heterozygous deletion of
Tbx1
, one of the 22q11.2-encoded genes. Ex vivo whole-brain diffusion-tensor imaging (DTI)–magnetic resonance imaging (MRI) in
Tbx1
heterozygous mice indicated that the fimbria was the only region with significant myelin alteration. Electron microscopic and histological analyses showed that
Tbx1
heterozygous mice exhibited an apparent absence of large myelinated axons and thicker myelin in medium axons in the fimbria, resulting in an overall decrease in myelin. The fimbria of
Tbx1
heterozygous mice showed reduced mRNA levels of
Ng2
, a gene required to produce oligodendrocyte precursor cells. Moreover, postnatal progenitor cells derived from the subventricular zone, a source of oligodendrocytes in the fimbria, produced fewer oligodendrocytes in vitro. Behavioral analyses of these mice showed selectively slower acquisition of spatial memory and cognitive flexibility with no effects on their accuracy or sensory or motor capacities. Our findings provide a genetic and cellular basis for the compromised cognitive speed in patients with 22q11.2 hemizygous deletion. Copy number variants (CNVs) have provided a reliable entry point to identify the structural correlates of atypical cognitive development. Hemizygous deletion of human chromosome 22q11.2 is associated with impaired cognitive function; however, the mechanisms by which the CNVs contribute to cognitive deficits via diverse structural alterations in the brain remain unclear. This study aimed to determine the cellular basis of the link between alterations in brain structure and cognitive functions in mice with a heterozygous deletion of Tbx1, one of the 22q11.2-encoded genes. Ex vivo whole-brain diffusion-tensor imaging (DTI)-magnetic resonance imaging (MRI) in Tbx1 heterozygous mice indicated that the fimbria was the only region with significant myelin alteration. Electron microscopic and histological analyses showed that Tbx1 heterozygous mice exhibited an apparent absence of large myelinated axons and thicker myelin in medium axons in the fimbria, resulting in an overall decrease in myelin. The fimbria of Tbx1 heterozygous mice showed reduced mRNA levels of Ng2, a gene required to produce oligodendrocyte precursor cells. Moreover, postnatal progenitor cells derived from the subventricular zone, a source of oligodendrocytes in the fimbria, produced fewer oligodendrocytes in vitro. Behavioral analyses of these mice showed selectively slower acquisition of spatial memory and cognitive flexibility with no effects on their accuracy or sensory or motor capacities. Our findings provide a genetic and cellular basis for the compromised cognitive speed in patients with 22q11.2 hemizygous deletion. |
Author | Nonaka, Hiroi Tanigaki, Kenji Sumiyoshi, Akira Hiroi, Noboru Ryoke, Rie Yamauchi, Takahira Kawashima, Ryuta Enomoto, Shingo Izumi, Takeshi Bhat, Manzoor A. Kang, Gina Shi, Qian Hiramoto, Takeshi |
Author_xml | – sequence: 1 givenname: Takeshi surname: Hiramoto fullname: Hiramoto, Takeshi organization: Department of Pharmacology, University of Texas Health Science Center at San Antonio – sequence: 2 givenname: Akira surname: Sumiyoshi fullname: Sumiyoshi, Akira organization: Institute of Development, Aging, and Cancer, Tohoku University, National Institutes for Quantum and Radiological Science and Technology – sequence: 3 givenname: Takahira surname: Yamauchi fullname: Yamauchi, Takahira organization: Department of Pharmacology, University of Texas Health Science Center at San Antonio – sequence: 4 givenname: Kenji surname: Tanigaki fullname: Tanigaki, Kenji organization: Research Institute, Shiga Medical Center – sequence: 5 givenname: Qian surname: Shi fullname: Shi, Qian organization: Department of Cellular and Integrative Physiology, University of Texas Health Science Center at San Antonio – sequence: 6 givenname: Gina surname: Kang fullname: Kang, Gina organization: Department of Pharmacology, University of Texas Health Science Center at San Antonio – sequence: 7 givenname: Rie surname: Ryoke fullname: Ryoke, Rie organization: Institute of Development, Aging, and Cancer, Tohoku University – sequence: 8 givenname: Hiroi surname: Nonaka fullname: Nonaka, Hiroi organization: Institute of Development, Aging, and Cancer, Tohoku University – sequence: 9 givenname: Shingo surname: Enomoto fullname: Enomoto, Shingo organization: Department of Psychiatry and Behavioral Sciences, Albert Einstein College of Medicine – sequence: 10 givenname: Takeshi surname: Izumi fullname: Izumi, Takeshi organization: Department of Pharmacology, Health Sciences University of Hokkaido, Advanced Research Promotion Center, Health Sciences University of Hokkaido – sequence: 11 givenname: Manzoor A. orcidid: 0000-0003-0989-1498 surname: Bhat fullname: Bhat, Manzoor A. organization: Department of Cellular and Integrative Physiology, University of Texas Health Science Center at San Antonio – sequence: 12 givenname: Ryuta surname: Kawashima fullname: Kawashima, Ryuta organization: Institute of Development, Aging, and Cancer, Tohoku University – sequence: 13 givenname: Noboru orcidid: 0000-0002-6846-5969 surname: Hiroi fullname: Hiroi, Noboru email: hiroi@uthscsa.edu organization: Department of Pharmacology, University of Texas Health Science Center at San Antonio, Department of Cellular and Integrative Physiology, University of Texas Health Science Center at San Antonio, Department of Cell Systems and Anatomy, University of Texas Health Science Center at San Antonio |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34737458$$D View this record in MEDLINE/PubMed |
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Title | Tbx1, a gene encoded in 22q11.2 copy number variant, is a link between alterations in fimbria myelination and cognitive speed in mice |
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