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Upf3b gene underlies intellectual disability

Abnormalities in RNA processing can lead to learning and memory impairment...

In humans, mutations in the UPF3B gene cause intellectual disability and are strongly associated with (1) autism spectrum disorder, (2) attention deficit hyperactivity disorder and (3) schizophrenia. This is because UPF3B regulates nonsense-mediated RNA decay (NMD), which is the "volume control" for many genes.

Now, researchers at University of California San Diego School of Medicine have developed the first mouse without the Upf3b gene. This mouse provided researchers the opportunity to identify Upf3b's role in neurodevelopment. Their findings are now published in the September 26, 2017 edition of Molecular Psychiatry.
"These observations about UPF3B made us wonder if nonsense-mediated RNA decay (NMD) is important to mammalian brain development."

Miles Wilkinson PhD, Professor, Reproductive Medicine, School of Medicine, University of California, San Diego, USA and senior author.

NMD acts on messenger RNAs (mRNAs) as they carryout gene blueprints. Each blueprint must be translated into an essential protein in order for the body to function. Initially, NMD was thought to serve only as a quality control mechanism useful for degrading mRNAs that might code for harmful proteins. Recently though, NMD is seen to also degrade normal mRNAs in specific cell types to eliminate mRNAs if needed.
NMD plays an important part in several biological processes, including fetal and neonatal development - a time when cells must be especially careful about how they coordinate and time production of mRNAs (and the proteins they encode).

Wilkinson's team found how Upf3b-deficient mice are different from normal mice in that their neural stem cells do not specialize into functional neurons. Neurons that they create do not form dendrites with dendritic spines, structures critical in neuron-to-neuron communication. Upf3b deficient mice also have specific memory and learning defects associated around the fear response. Their way of sensory processing is often found in schizophrenia and similar brain disorders. Comparing RNA sequences in the frontal cortex of normal mice to those in Upf3b deficient mice, researchers found that Upf3b regulates how RNAs encode proteins neurons need in order to develop and mature normally.

"In many ways, the behavioral impairments in mice lacking Upf3b mimicked those found in human patients with UPF3B mutations. This new model will be critical in determining precisely how defects in NMD can lead to specific learning and sensory processing defects."span>

Miles Wilkinson PhD

Nonsense-mediated RNA decay (NMD) is a highly conserved and selective RNA degradation pathway that acts on RNAs terminating their reading frames in specific contexts. NMD is regulated in a tissue-specific and developmentally controlled manner, raising the possibility that it influences developmental events. Indeed, loss or depletion of NMD factors have been shown to disrupt developmental events in organisms spanning the phylogenetic scale. In humans, mutations in the NMD factor gene, UPF3B, cause intellectual disability (ID) and are strongly associated with autism spectrum disorder (ASD), attention deficit hyperactivity disorder (ADHD) and schizophrenia (SCZ). Here, we report the generation and characterization of mice harboring a null Upf3b allele. These Upf3b-null mice exhibit deficits in fear-conditioned learning, but not spatial learning. Upf3b-null mice also have a profound defect in prepulse inhibition (PPI), a measure of sensorimotor gating commonly deficient in individuals with SCZ and other brain disorders. Consistent with both their PPI and learning defects, cortical pyramidal neurons from Upf3b-null mice display deficient dendritic spine maturation in vivo. In addition, neural stem cells from Upf3b-null mice have impaired ability to undergo differentiation and require prolonged culture to give rise to functional neurons with electrical activity. RNA sequencing (RNAseq) analysis of the frontal cortex identified UPF3B-regulated RNAs, including direct NMD target transcripts encoding proteins with known functions in neural differentiation, maturation and disease. We suggest Upf3b-null mice serve as a novel model system to decipher cellular and molecular defects underlying ID and neurodevelopmental disorders.

Co-authors of this study are: L Huang, E Y Shum, S H Jones, C-H Lou, J Dumdie, H Kim, A J Roberts, L A Jolly, J L Espinoza, D M Skarbrevik, M H Phan, H Cook-Andersen, N R Swerdlow, J Gecz and M F Wilkinson

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Cartoon of mRNA being translated into protein chain.
Image Credit: National Institute of General Medical Studies

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