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@ARTICLE{Ioannidis:270139,
author = {Ioannidis, Valentin and Pandey, Rakshita and Bauer, Helen
Friedericke and Schön, Michael and Bockmann, Jürgen and
Boeckers, Tobias M and Lutz, Anne-Kathrin},
title = {{D}isrupted extracellular matrix and cell cycle genes in
autism-associated {S}hank3 deficiency are targeted by
lithium.},
journal = {Molecular psychiatry},
volume = {29},
number = {3},
issn = {1359-4184},
address = {London},
publisher = {Macmillan},
reportid = {DZNE-2024-00739},
pages = {704 - 717},
year = {2024},
abstract = {The Shank3 gene encodes the major postsynaptic scaffolding
protein SHANK3. Its mutation causes a syndromic form of
autism spectrum disorder (ASD): Phelan-McDermid Syndrome
(PMDS). It is characterized by global developmental delay,
intellectual disorders (ID), ASD behavior, affective
symptoms, as well as extra-cerebral symptoms. Although
Shank3 deficiency causes a variety of molecular alterations,
they do not suffice to explain all clinical aspects of this
heterogenic syndrome. Since global gene expression
alterations in Shank3 deficiency remain inadequately
studied, we explored the transcriptome in vitro in primary
hippocampal cells from Shank3∆11(-/-) mice, under control
and lithium (Li) treatment conditions, and confirmed the
findings in vivo. The Shank3∆11(-/-) genotype affected the
overall transcriptome. Remarkably, extracellular matrix
(ECM) and cell cycle transcriptional programs were
disrupted. Accordingly, in the hippocampi of adolescent
Shank3∆11(-/-) mice we found proteins of the collagen
family and core cell cycle proteins downregulated. In vitro
Li treatment of Shank3∆11(-/-) cells had a rescue-like
effect on the ECM and cell cycle gene sets. Reversed ECM
gene sets were part of a network, regulated by common
transcription factors (TF) such as cAMP responsive element
binding protein 1 (CREB1) and β-Catenin (CTNNB1), which are
known downstream effectors of synaptic activity and targets
of Li. These TFs were less abundant and/or
hypo-phosphorylated in hippocampi of Shank3∆11(-/-) mice
and could be rescued with Li in vitro and in vivo. Our
investigations suggest the ECM compartment and cell cycle
genes as new players in the pathophysiology of Shank3
deficiency, and imply involvement of transcriptional
regulators, which can be modulated by Li. This work supports
Li as potential drug in the management of PMDS symptoms,
where a Phase III study is ongoing.},
keywords = {Animals / Nerve Tissue Proteins: genetics / Nerve Tissue
Proteins: metabolism / Hippocampus: metabolism /
Extracellular Matrix: metabolism / Mice / Mice, Knockout /
beta Catenin: metabolism / beta Catenin: genetics /
Chromosome Disorders: genetics / Chromosome Disorders:
metabolism / Chromosome Deletion / Cell Cycle: drug effects
/ Cell Cycle: genetics / Autistic Disorder: genetics /
Autistic Disorder: metabolism / Chromosomes, Human, Pair 22:
genetics / Cyclic AMP Response Element-Binding Protein:
metabolism / Cyclic AMP Response Element-Binding Protein:
genetics / Male / Transcriptome: genetics / Autism Spectrum
Disorder: genetics / Autism Spectrum Disorder: metabolism /
Autism Spectrum Disorder: drug therapy / Mice, Inbred C57BL
/ Lithium: pharmacology / Microfilament Proteins: metabolism
/ Microfilament Proteins: genetics / Cells, Cultured /
Shank3 protein, mouse (NLM Chemicals) / Nerve Tissue
Proteins (NLM Chemicals) / beta Catenin (NLM Chemicals) /
Creb1 protein, mouse (NLM Chemicals) / Cyclic AMP Response
Element-Binding Protein (NLM Chemicals) / CTNNB1 protein,
mouse (NLM Chemicals) / Lithium (NLM Chemicals) /
Microfilament Proteins (NLM Chemicals)},
cin = {AG Böckers},
ddc = {610},
cid = {I:(DE-2719)1910002},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pmc = {pmc:PMC11153165},
pubmed = {pmid:38123724},
doi = {10.1038/s41380-023-02362-y},
url = {https://pub.dzne.de/record/270139},
}