Insets show nTg mice with no hTDP-43 expression and nuclear h+mTDP-43 expression. vulnerable forebrain regions, corticospinal tract degeneration, and motor spasticity recapitulating key aspects of FTLD and primary lateral sclerosis. Only rare cytoplasmic phosphorylated and ubiquitinated TDP-43 inclusions were seen in hTDP-43-NLS mice, suggesting that cytoplasmic inclusions were not required to induce neuronal death. Instead, neurodegeneration in hTDP-43 and hTDP-43-NLSCexpressing neurons was accompanied by a dramatic downregulation of the endogenous mouse TDP-43. Moreover, mice expressing hTDP-43-NLS exhibited profound changes in gene expression in cortical neurons. Our data suggest that perturbation of endogenous nuclear TDP-43 results in loss of normal TDP-43 function(s) and gene regulatory pathways, culminating in degeneration of selectively vulnerable affected neurons. Introduction Frontotemporal lobar degeneration (FTLD) and amyotrophic lateral sclerosis (ALS) are characterized by the presence of ubiquitin-positive inclusions (1). These inclusions are found in the brain and spinal cord of ALS patients as well as in patients with a major subtype of FTLD designated FTLD-TDP because these inclusions were shown to be comprised of the TAR-DNA binding protein 43 (TDP-43) (2). Since (a) cognitive abnormalities or dementia consistent with FTLD are increasingly recognized in ALS patients, (b) some FTLD patients develop MND, and (c) cytoplasmic TDP-43 aggregates are found in the brain and spinal cord of both ALS and FTLD-TDP patients, TDP-43 pathology appears to define a single neurodegenerative disorder (TDP-43 proteinopathy) with a spectrum of clinical manifestations (3C5). The importance of TDP-43 in the pathogenesis of these diseases is supported by the presence of autosomal dominant mutations in the gene associated with ALS and FTLD (6). Human TDP-43 (hTDP-43) is a highly conserved and ubiquitously expressed 414Camino acid nuclear protein that binds to both DNA and RNA (7, 8). TDP-43 is implicated in repression of gene transcription, regulation of exon splicing, and nuclear body functions (for a summary see recent reviews, refs. 4 and 6). Pathological TDP-43 XMD8-92 can be abnormally cleaved, phosphorylated, and ubiquitinated, and most TDP-43 aggregates are mislocalized outside the nucleus within the XMD8-92 cytoplasm or neurites (2). Interestingly, cells that develop TDP-43 accumulations show a dramatic depletion of normal nuclear TDP-43. Thus, both gain and loss of functions are potential disease mechanisms, either due to the loss of normal nuclear TDP-43 expression, cytoplasmic mislocalization, or cytoplasmic aggregation (2, 9, 10). To mimic this nuclear clearance and to model the formation of TDP-43 cytoplasmic aggregates, we have shown that expression of hTDP-43 with mutated nuclear localization signals (hTDP-43-NLS) Kl in cultured cells reduces endogenous nuclear TDP-43 and accumulates as cytoplasmic aggregates (11). In vivo mouse models with TDP-43 knockout or overexpression have also been reported. null mice exhibit rapid postnatal death associated with aberrations in fat metabolism (15). Tg mice with overexpression of human or mouse TDP-43-WT as well as mice expressing TDP-43 harboring disease-associated mutations have been reported to show TDP-43 pathologies associated with motor neuron degeneration reminiscent of ALS or FTLD-TDP (16C20). However, the effects of cytoplasmic TDP-43 expression on the formation of cytoplasmic aggregates, neurotoxicity, and normal nuclear TDP-43 protein on initiating neurodegeneration have not been addressed in vivo. Here, we generated Tg mice with inducible forebrain overexpression of hTDP-43-NLS using the Camk2a tetracycline transactivator (Camk2a tetO) to specifically model cytoplasmic mislocalization of TDP-43 XMD8-92 and interrogate the consequences of this abnormal distribution of TDP-43 in the presence or absence of TDP-43 aggregates. We found profound neuron loss in specific regions, in particular, cortex (including motor cortex) and hippocampus, with corticospinal tract (CST) degeneration and a spastic motoric phenotype, all of which recapitulate key aspects of FTLD and primary lateral sclerosis (PLS). However, only small numbers of phosphorylated and ubiquitinated cytoplasmic hTDP-43 aggregates are found in hTDP-43-NLS Tg mice, and they do not correlate with the observed profound neurotoxicity. Instead, a dramatic loss of endogenous nuclear mouse TDP-43 (mTDP-43) was the only correlate to neurodegeneration in hTDP-43-NLSCexpressing mice. Significantly, this was connected with a strikingly selective and abnormal upregulation of chromatin assembly genes in hTDP-43-NLS Tg mice. We conclude that endogenous nuclear TDP-43 is normally highly regulated which perturbation of nuclear TDP-43 is normally associated with deep modifications in gene appearance and cell loss of life. Outcomes Era of Tg mice overexpressing hTDP-43-NLS and hTDP-43-WT protein. To make conditional mouse types of TDP-43 proteinopathies, we produced Tg mice expressing hTDP-43-NLS and its own control counterpart hTDP-43-WT using CaMK2 promoter components to operate a vehicle tet-off tTA (Camk2a-tTA) and a tetracycline reactive promoter to operate a vehicle hTDP-43 appearance (tetO-hTDP-43; Figure ?Amount1A)1A) (21C23). Bigenic mice (Camk2a-tTA x tetO-hTDP-43) had been preserved on Doxycycline (Dox) to inhibit transgene appearance until 28 times of age if they had been turned to a Dox-free diet plan and sacrificed on the designated time factors off Dox (Amount ?(Figure1B). 1B)..
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