Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functions

Summary: Noncanonical genomic imprinting can cause biased expression of one parental allele in a tissue; however, the functional relevance of such biases is unclear. To investigate ethological roles for noncanonical imprinting in dopa decarboxylase (Ddc) and tyrosine hydroxylase (Th), we use machine...

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Main Authors: Paul J. Bonthuis, Susan Steinwand, Cornelia N. Stacher Hörndli, Jared Emery, Wei-Chao Huang, Stephanie Kravitz, Elliott Ferris, Christopher Gregg
Format: Article
Language:English
Published: Elsevier 2022-03-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124722002364
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author Paul J. Bonthuis
Susan Steinwand
Cornelia N. Stacher Hörndli
Jared Emery
Wei-Chao Huang
Stephanie Kravitz
Elliott Ferris
Christopher Gregg
author_facet Paul J. Bonthuis
Susan Steinwand
Cornelia N. Stacher Hörndli
Jared Emery
Wei-Chao Huang
Stephanie Kravitz
Elliott Ferris
Christopher Gregg
author_sort Paul J. Bonthuis
collection DOAJ
description Summary: Noncanonical genomic imprinting can cause biased expression of one parental allele in a tissue; however, the functional relevance of such biases is unclear. To investigate ethological roles for noncanonical imprinting in dopa decarboxylase (Ddc) and tyrosine hydroxylase (Th), we use machine learning to decompose naturalistic foraging in maternal and paternal allele mutant heterozygous mice. We uncover distinct roles for the maternal versus paternal alleles on foraging, where maternal alleles affect sons while daughters are under paternal allelic control. Each parental allele controls specific action sequences reflecting decisions in naive or familiar contexts. The maternal Ddc allele is preferentially expressed in subsets of hypothalamic GABAergic neurons, while the paternal allele predominates in subsets of adrenal cells. Each Ddc allele affects distinct molecular and endocrine components of the brain-adrenal axis. Thus, monoaminergic noncanonical imprinting has ethological roles in foraging and endocrine functions and operates by affecting discrete subsets of cells.
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spelling doaj.art-80e897921e7743a7b88649d4a8a36b5e2022-12-22T01:10:31ZengElsevierCell Reports2211-12472022-03-013810110500Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functionsPaul J. Bonthuis0Susan Steinwand1Cornelia N. Stacher Hörndli2Jared Emery3Wei-Chao Huang4Stephanie Kravitz5Elliott Ferris6Christopher Gregg7Department of Comparative Biosciences, University of Illinois at Urbana-Champaign College of Veterinary Medicine, Urbana, IL, USADepartment of Neurobiology, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USADepartment of Neurobiology, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USADepartment of Neurobiology, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USADepartment of Neurobiology, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USADepartment of Neurobiology, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USA; Department of Human Genetics, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USADepartment of Neurobiology, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USADepartment of Neurobiology, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USA; Department of Human Genetics, University of Utah School of Medicine, Room 408B, Biopolymers Research Building, Bld. 570, 20 South 2030 East, Salt Lake City, UT 84112, USA; Corresponding authorSummary: Noncanonical genomic imprinting can cause biased expression of one parental allele in a tissue; however, the functional relevance of such biases is unclear. To investigate ethological roles for noncanonical imprinting in dopa decarboxylase (Ddc) and tyrosine hydroxylase (Th), we use machine learning to decompose naturalistic foraging in maternal and paternal allele mutant heterozygous mice. We uncover distinct roles for the maternal versus paternal alleles on foraging, where maternal alleles affect sons while daughters are under paternal allelic control. Each parental allele controls specific action sequences reflecting decisions in naive or familiar contexts. The maternal Ddc allele is preferentially expressed in subsets of hypothalamic GABAergic neurons, while the paternal allele predominates in subsets of adrenal cells. Each Ddc allele affects distinct molecular and endocrine components of the brain-adrenal axis. Thus, monoaminergic noncanonical imprinting has ethological roles in foraging and endocrine functions and operates by affecting discrete subsets of cells.http://www.sciencedirect.com/science/article/pii/S2211124722002364genomic imprintingepigeneticsforagingmonoamineadrenalinetyrosine hydroxylase
spellingShingle Paul J. Bonthuis
Susan Steinwand
Cornelia N. Stacher Hörndli
Jared Emery
Wei-Chao Huang
Stephanie Kravitz
Elliott Ferris
Christopher Gregg
Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functions
Cell Reports
genomic imprinting
epigenetics
foraging
monoamine
adrenaline
tyrosine hydroxylase
title Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functions
title_full Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functions
title_fullStr Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functions
title_full_unstemmed Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functions
title_short Noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain-adrenal axis functions
title_sort noncanonical genomic imprinting in the monoamine system determines naturalistic foraging and brain adrenal axis functions
topic genomic imprinting
epigenetics
foraging
monoamine
adrenaline
tyrosine hydroxylase
url http://www.sciencedirect.com/science/article/pii/S2211124722002364
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