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Neurons can choose to activate mom or dad's genes

For over a century, scientists have thought most of our cells use genes from both parents' pretty equally throughout life. But our biology is more nuanced, say scientists who invented a screen to measure specific genes from each parent.

Researchers report that in rodent, monkey, and human brains, it's not unusual for individual neurons to silence genes from one parent or the other. The work is published in the February 23 issue of Neuron.

Surprisingly, differential activation of maternal and paternal gene copies was observed most often in the developing brain, impacting about 85% of genes. Gradually, as the brain matures, neurons increasingly express both parents' genes equally. However, for at least 10% of genes, maternal and paternal copies continue to be differentially expressed in the adult brain, revealing that this imbalance exists throughout an organism's lifetime for many genes in the brain.

"This story has its roots in understanding why we reproduce sexually. Normally, having two copies of a gene acts as a protective buffer in case one is defective. Our findings suggest that in periods when the healthy gene copy is turned off — could provide a critical window during which cells are particularly vulnerable to a mutation in the other copy."

Christopher Gregg PhD, Robertson Neuroscience Investigator, Departments of Neurobiology & Anatomy, Department of Human Genetics, New York Stem Cell Foundation and senior author.

Often mutations causing mental illness are heterozygous, meaning the impact is felt from just one gene copy. The Gregg lab is now exploring whether the effects they uncovered explain why the same gene can be associated with a wide range of mental illnesses, from autism to schizophrenia. Also in question, does variation in the severity of disease symptoms, or risk, depend on the same gene variant.

The study demonstrates it is possible for some brain cells to predominately express a mutant copy of a gene while others don't.

Scientists have known for decades that some specific classes of genes activate their maternal or paternal copy in the brain. However, Gregg's lab has uncovered a vast, new landscape of parental brain differential affects. Differences can be seen in activation of maternal or paternal gene copy according to an individual's age, a particular cell type, or region of the brain, or even tissue type.

This raises the possibility of more undiscovered mechanisms for how cells decide which parent gene to shut off. It's known that children inherit epigenetic imprints from parents signalling whether a particular gene should be expressed. For example, in all females, each cell inactivates one X of the two female X chromosomes. Finding the mechanisms that cause gene selectivity and subsequent gene shutoff, could lead to new therapeutic approaches to activate silent healthy gene copies in the brain and other systems.

"The screens revealed a new landscape of effects on maternal and paternal gene copies in the brain that were not due to imprinting and not due to X inactivation but took on all kinds of different form.

"Some effects are age specific, some are stable after birth, some impact most brain cells, some are more cell specific, some involved antagonistic effects where the maternal gene would go up and the paternal gene would go down, while others took on a different pattern."

Christopher Gregg PhD

Gregg and his team at the University of Utah are now focused on understanding how differences in parental gene expression shapes brain function and disease risk.

While specifically looking at brain cells and mental illness, the screen they developed is now available to the scientific community, and could provide insights across many cell types.

•In vivo genome-wide screen uncovers diverse non-genetic allelic effects
•Non-genetic allelic effects are prevalent in the neonatal mouse brain
•Allelic effects cause mosaics of mutant and wild-type cells for heterozygous mutations
•Allelic effects exist in the primate brain and impact genes linked to mental illness

Interactions between genetic and epigenetic effects shape brain function, behavior, and the risk for mental illness. Random X inactivation and genomic imprinting are epigenetic allelic effects that are well known to influence genetic architecture and disease risk. Less is known about the nature, prevalence, and conservation of other potential epigenetic allelic effects in vivo in the mouse and primate brain. Here we devise genomics, in situ hybridization, and mouse genetics strategies to uncover diverse allelic effects in the brain that are not caused by imprinting or genetic variation. We found allelic effects that are developmental stage and cell type specific, that are prevalent in the neonatal brain, and that cause mosaics of monoallelic brain cells that differentially express wild-type and mutant alleles for heterozygous mutations. Finally, we show that diverse non-genetic allelic effects that impact mental illness risk genes exist in the macaque and human brain. Our findings have potential implications for mammalian brain genetics.Abstract

This work has been supported by the National Institutes of Health, a Simons Foundation Autism Research Initiative Explorer Award, a University of Utah Seed Grant, and a New York Stem Cell Foundation Robertson-Neuroscience Award.

Neuron, Huang and Ferris et al.: "Diverse Non-Genetic Allele Specific Expression Effects Shape Genetic Architecture at the Cellular Level in the Mammalian Brain" http://www.cell.com/neuron/fulltext/S0896-6273(17)30057-0

Neuron (@NeuroCellPress), published by Cell Press, is a bimonthly journal that has established itself as one of the most influential and relied upon journals in the field of neuroscience and one of the premier intellectual forums of the neuroscience community. It publishes interdisciplinary articles that integrate biophysical, cellular, developmental, and molecular approaches with a systems approach to sensory, motor, and higher-order cognitive functions. Visit: http://www.cell.com/neuron. To receive Cell Press media alerts, contact press@cell.com.
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Feb 28, 2017   Fetal Timeline   Maternal Timeline   News   News Archive   

Above: Non-genetic allelles — a form of gene arising via mutation and found at the same place
on a chromosome — found in many autosomal genes in the mouse and primate brain.
Maternal (RED) and Paternal (BLUE) copies of a chromosome can be seen in three neurons.
Difference in chromosome expression (function) is seen in two alleles due to epigenetic effects,
One allele is MUTATED (RED) and one is HEALTHY (BLUE).

In the brightly highlighted yellow neuron, the gene is monoallelic and only expresses a healthy, wildtype allele. In the more dimly highlighted neuron, the gene is biallelic and expresses both the healthy and the mutated allele. Finally, in the dark neuron, only the mutated allele is expressed.

Non-genetic allelic effects can shape gene architecture at the cellular level in the brain,
potentially creating a complex picture of genetics for brain disorders.
Image Credit: Gregg Lab


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