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Monnier, P. P.

Publications and source records attributed to Monnier, P. P..

6 recordsLinked to original sources

Unbiased Long-Read Whole-Genome Sequencing Enables High-Resolution Mapping of Transgene Concatenation and Off-target Genomic Disruption in a Mouse Model

Transgenic mouse models are indispensable for dissecting disease mechanisms; yet, their interpretability is frequently compromised by cryptic genomic alterations introduced during transgenesis. Thus, robust quality control strategies are needed to elucidate integration architecture and evaluate model performance when such unintended events occur. Here, we applied unbiased whole-genome long-read sequencing using the PacBio Revio to investigate a mouse model exhibiting unexpected transgene silencing, originally designed to recapitulate autosomal-dominant hereditary macular dystrophy driven by upregulation of a ZZEF1-ALOX15 fusion gene. Long-read sequencing analysis revealed a [≥]29-kb head-to-tail concatemer containing more than three copies of the transgene vector. Reconstruction of transgene-genome junctions revealed off-target integration of the concatemer into the calcium-sensing receptor gene (Casr), along with exogenous E. coli DNA, that together defined final transgene architecture. 5-methylcytosine profiling identified hypermethylation of the transgene promoter and additional phenotyping indicated disruption of endogenous Casr function resulting from the rearrangement. Our workflow enabled direct detection of transgene concatenation and off-target mapping. These findings establish long-read sequencing as a powerful and scalable quality control standard for genetically engineered animal models, uniquely capable of uncovering hidden genomic complexity, resolving aberrant phenotypes, and enhancing the reliability of in vivo disease modelling.

genomics↗

Segregated localization of target-SNARE proteins within presynaptic terminals of Munc18-1 deficient photoreceptors

Sec1/Munc18 family proteins are essential for SNARE-mediated vesicular exocytosis. However, where SNARE proteins are localized in Munc18-1 deficient presynaptic terminals remains unclear due to the rapid degeneration of neurons lacking Munc18-1. Here, we found that removing Munc18-1 from photoreceptor cells did not result in major cellular loss until postnatal day 14, which allowed us to investigate the role of Munc18-1 in endogenous presynaptic terminals. In the absence of Munc18-1, even before major photoreceptor cell degeneration, functional impairments were present. While Munc18-1 was not required for the pre-synaptic enrichment of the t-SNARE proteins syntaxin-3 and SNAP-25, it played a critical role in their proper localization. In wild-type conditions, t-SNAREs are highly colocalized. However, in the absence of Munc18-1, their distribution becomes strikingly segregated. Immuno-electron microscopy revealed that without Munc18-1, syntaxin-3 is retained within various organelle membranes rather than being targeted to synaptic plasma membranes. These findings provide the first evidence that Munc18-1 is important to prevent segregation of syntaxin-3 and SNAP-25 within presynaptic terminals.

neuroscience↗

SNAP-25, but not SNAP-23, is essential for photoreceptor function and survival in mice

Vesicular transport plays critical roles in photopigment delivery at photoreceptor outer segments and glutamate exocytosis at photoreceptor synapses. Previous studies into the role of photoreceptor SNAP proteins are limited in their characterizations into only gene/protein expression and do not delve further into their functional role. Here, we examine the expression and localization of SNAP-23 and SNAP-25 mRNA and protein. Using SNAP-23 and SNAP-25 conditional knockout mice, we further evaluated the morphological and functional consequences that the absence of these proteins has on vision. Although we found that the ubiquitously expressed SNAP-23 showed weak mRNA expression in photoreceptors, removal of SNAP-23 did not result in any observable phenotype. We found that neuronal SNAP-25 is developmentally regulated and SNAP-25 mRNA undergoes mRNA trafficking to the photoreceptor inner segments coinciding with the development of photoreceptor outer segments. Removal of SNAP-25 in photoreceptor cells led to changes in both outer segment protein trafficking and synaptic integrity, resulting in a complete loss of vision in SNAP-25 cKO mice. Our results conclude that SNAP-25, but not SNAP-23, is the essential isoform for photoreceptor survival and function.

neuroscience↗

Mouse model of multiple sclerosis induced by disrupting vesicular transport in oligodendrocytes

Multiple Sclerosis is an autoimmune demyelination disorder with unknown etiology. Despite the myelin damage, the roles of myelinating oligodendrocytes in driving disease progression remain unknown. We hypothesize that disrupting vesicular transport in oligodendrocytes during adolescence will disrupt myelin integrity and causes neuroinflammation. By creating a mouse model of SNAP-23 conditional knockout in mature oligodendrocytes, we showed that impairment in vesicular trafficking in oligodendrocytes causes demyelination. Neuroinflammation with infiltration of peripheral immune T cells into the central nervous system was observed accompanied by demyelination. Mechanistically, SNAP-23 removal in oligodendrocytes caused abnormal axon-myelin structures and impaired myelin protein trafficking, both can contribute to autoimmune activation and demyelination. With our novel animal model, we propose that oligodendrocyte injury is an endogenous early event in triggering Multiple Sclerosis. One-Sentence SummaryImpaired vesicular transport in oligodendrocytes in adults caused demyelination and inflammation driving Multiple Sclerosis

neuroscience↗

Double open syntaxin and UNC-18 P334A mutation leads to excitatory-inhibitory imbalance and impairs multiple aspects of C. elegans behavior

SNARE and Sec/Munc18 proteins are essential in synaptic vesicle exocytosis. Open form t-SNARE syntaxin and UNC-18 P334A are well-studied exocytosis-enhancing mutants. Here we investigate the interrelationship between the two mutations by generating double mutants in various genetic backgrounds in C. elegans. While each single mutation rescued the motility of CAPS/unc-31 and synaptotagmin/snt-1 mutants significantly, double mutations unexpectedly worsened motility or lost their rescuing effects. Electrophysiological analyses revealed that simultaneous mutations of open syntaxin and gain-of-function P334A UNC-18 induces a strong imbalance of excitatory over inhibitory transmission. In liposome fusion assays performed with mammalian proteins, the enhancement of fusion caused by the two mutations individually was abolished when the two mutations were introduced simultaneously, consistent with what we observed in C. elegans. We conclude that open syntaxin and P334A UNC-18 do not have additive beneficial effects, and this extends to C. elegans characteristics such as motility, growth, offspring bared, body size, and exocytosis, as well as liposome fusion in vitro. Our results also reveal unexpected differences between the regulation of exocytosis in excitatory versus inhibitory synapses.

neuroscience↗

Neuronal SNAP-23 scales hippocampal synaptic plasticity and memory

Soluble NSF Attachment protein REceptor (SNARE)-mediated membrane fusion plays a crucial role not only in presynaptic vesicle exocytosis but also in postsynaptic receptor delivery. The latter is considered particularly important for long-term synaptic plasticity and learning and memory, yet underlying mechanisms including the identity of the key SNARE proteins remain elusive. Here, we investigate the role of neuronal Synaptosomal-Associated Protein-23 (SNAP-23) by analyzing pyramidal-neuron specific SNAP-23 conditional knockout (cKO) mice. SNAP-23 immunostaining in postsynaptic spines was effectively decreased in the SNAP-23 cKO hippocampus. Electrophysiological analysis of SNAP-23 deficient neurons using acute hippocampal slices showed normal basal neurotransmission in CA3-CA1 synapses with unchanged AMPA and NMDA currents. Nevertheless, we found theta-burst stimulation induced long-term potentiation (LTP) was vastly diminished in SNAP-23 cKO. Moreover, unlike syntaxin-4 cKO mice in which both basal neurotransmission and LTP decrease manifested changes in a broad set of behavioral tasks, deficits of SNAP-23 cKO is more limited to spatial memory. Our data reveal that neuronal SNAP-23 is selectively crucial for synaptic plasticity and spatial memory without affecting basal glutamate receptor function.

neuroscience↗