Fragile X and autism: Intertwined at the molecular level leading to targeted treatments - PubMed (original) (raw)
Fragile X and autism: Intertwined at the molecular level leading to targeted treatments
Randi Hagerman et al. Mol Autism. 2010.
Abstract
Fragile X syndrome (FXS) is caused by an expanded CGG repeat (> 200 repeats) in the 5' untranslated portion of the fragile mental retardation 1 gene (FMR1), leading to deficiency or absence of the FMR1 protein (FMRP). FMRP is an RNA carrier protein that controls the translation of several other genes that regulate synaptic development and plasticity. Autism occurs in approximately 30% of FXS cases, and pervasive developmental disorder, not otherwise specified (PDD-NOS) occurs in an additional 30% of cases. Premutation repeat expansions (55 to 200 CGG repeats) may also give rise to autism spectrum disorders (ASD), including both autism and PDD-NOS, through a different molecular mechanism that involves a direct toxic effect of the expanded CGG repeat FMR1 mRNA. RNA toxicity can also lead to aging effects including tremor, ataxia and cognitive decline, termed fragile X-associated tremor ataxia syndrome (FXTAS), in premutation carriers in late life. In studies of mice bearing premutation expansions, there is evidence of early postnatal neuronal cell toxicity, presenting as reduced cell longevity, decreased dendritic arborization and altered synaptic morphology. There is also evidence of mitochondrial dysfunction in premutation carriers. Many of the problems with cellular dysregulation in both premutation and full mutation neurons also parallel the cellular abnormalities that have been documented in autism without fragile X mutations. Research regarding dysregulation of neurotransmitter systems in FXS, including the metabotropic glutamate receptor (mGluR)1/5 pathway and γ aminobutyric acid (GABA)A pathways, have led to new targeted treatments for FXS. Preliminary evidence suggests that these new targeted treatments will also be beneficial in non-fragile X forms of autism.
Figures
Figure 1
Overview of the behavioral/cognitive phenotype of fragile X syndrome (FXS). The interrelationships among cognitive, behavioral and attentional deficits in FXS are modified by additional environmental influences and genetic background effects. Environmental influences include seizures, trauma, abuse and socioeconomic status. Genetic influences include allelic variations, additional genetic disorders and variation in the expression levels of genes important for the phenotype of FXS.
Figure 2
Molecular overlap between autism, fragile x syndrome (FXS) and premutation disorders. Absence of the FMR1 protein (FMRP) leads to the dysregulation of several proteins including those involved with synapse formation and plasticity, glutamate and γ aminobuyric acid (GABA) neurotransmission and mammalian target of rapamycin (mTOR) and phosphatase and tensin homolog (PTEN) pathways. A premutation is associated with elevation of FMR1 mRNA, leading to sequestration of proteins and mitochondrial dysfunction. Many of these same molecular changes can also occur in some types of autism. Some patients with FXS have mosaicism of premutation and full cells, so there is overlap of the molecular mechanisms among all three disorders.
Figure 3
Potential mechanisms of FMR1 mRNA toxicity. Although numerous studies point to RNA toxicity as the underlying pathogenic trigger in fragile X-associated tremor ataxia syndrome (FXTAS), the specific mechanism for such toxicity is not known. Possibilities include (1) sequestration of one or more proteins that bind to the RNA, thus attenuating their other cell functions; (2) protein activation upon binding to the CGG-repeat RNA, leading to dysregulation of one or more signaling cascades; and (3) various co-transcriptional process, such as R-loop formation, that lead to DNA damage/repair signaling and consequent cellular dysregulation.
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