bioRxiv Science⌕ Search

bioRxiv · 10.1101/2021.11.15.468612

MKK6 deficiency promotes cardiac dysfunction through MKK3-p38γ/δ-mTOR hyperactivation

Abstract

Stress-activated p38 kinases control a plethora of functions and their dysregulation has been linked to development of steatosis, obesity, immune disorders and cancer. Therefore, they have been identified as potential targets for novel therapeutic strategies. There are four p38 family members (p38, p38{beta}, p38{gamma}, and p38{delta}) that are activated by MKK3 and MKK6. Here we demonstrate that lack of MKK6 reduces the life span in mice. Longitudinal study of cardiac function in Mkk6-/- mice showed that young mice have cardiac hypertrophy which progresses to cardiac dilatation and fibrosis with age. Mechanistically, lack of MKK6 blunts p38 activation while causing MKK3-p38{gamma}/{delta} hyperphosphorylation and increased mTOR signaling, resulting in cardiac hypertrophy. Cardiac hypertrophy in Mkk6-/- mice is reverted by knocking out either p38{gamma} or p38{delta}, or by inhibiting mTOR pathway with rapamycin. In conclusion, we have identified a key role for the MKK3/6-p38{gamma}/{delta} pathway in the development of cardiac hypertrophy, which has important implications for the clinical use of p38 inhibitors in the long-term treatment since they might result in cardiotoxicity. eLifes Review ProcesseLife works to improve the process of peer review so that it more effectively conveys the assessment of expert reviewers to authors, readers and other interested parties. In the future we envision a system in which research is first published as a preprint and the outputs of peer review are the primary way research is assessed, rather than journal title. Our editorial process produces two outputs: i) an assessment by peers designed to be posted alongside a preprint for the benefit of the readers; ii) detailed feedback on the manuscript for the authors, including requests for revisions and suggestions for improvement. Therefore we want to change how we construct and write peer reviews to make them useful to both authors and readers in a way that better reflects the work you put into reading and thinking about a paper. eLife reviews now have three parts: O_LIAn evaluation summary (in two or three sentences) that captures the major conclusions of the review in a concise manner, accessible to a wide audience. C_LIO_LIA public review that details the strengths and weaknesses of the manuscript before you, and discusses whether the authors claims and conclusions are justified by their data. C_LIO_LIA set of private recommendations for the authors that outline how you think the science and its presentation could be strengthened. C_LI All three sections will be used as the basis for an eLife publishing decision, which will, as always, be made after a consultation among the reviewers and editor. Each of the public reviews will be published (anonymously) alongside the preprint, together with a response from the authors if they choose. In the case of papers we reject after review, the authors can choose to delay posting until their paper has been published elsewhere. If this is your first time going through this new process, we ask that you take some time to read our Reviewer Guide, which discusses how we see each section will be used, what it should contain, and what we hope it accomplishes. And we remind you that, with the shift of reviews from private correspondence to public discourse, it is more important than ever that reviews are written in a clear and constructive manner appropriate for a public audience and mindful of the impact language choices might have on the authors.

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Romero-Becerra, R., Mora, A., Manieri, E., Sanz, L., Nikolic, I., Santamans, A. M., Montalvo-Romeral, V., Cruz, F. M., Rodriguez, E., Leiva-Vega, L., Bondia, V., Filgueiras-Rama, D., Jimenez-Borreguero, L. J., Jalife, J., Gonzalez-Teran, B., Sabio, G.. 2021-11-16. MKK6 deficiency promotes cardiac dysfunction through MKK3-p38γ/δ-mTOR hyperactivation. https://doi.org/10.1101/2021.11.15.468612

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Trans-branching of polyubiquitin chains orchestrates the DNA replication stress response

Polyubiquitin chain geometry dictates functional consequences of ubiquitylation. Although branched polyubiquitin chains are abundant in cells, little is known about their functions. Here we show that branching on the DNA replication factor PCNA, mediated by the ubiquitin-conjugating enzyme UBE2K and involving lysines 63 and 48 of ubiquitin, orchestrates the sequence of events in response to replication stress. By inducing VCP-dependent extraction of PCNA from chromatin, branching promotes re-priming of stalled forks and necessitates a BRCA1-dependent pathway of daughter-strand gap repair. Our study identifies hyper-accumulation of daughter-strand gaps as the mechanistic basis underlying the toxicity of inhibitors of the PCNA-specific isopeptidase, USP1, in BRCA1-deficient cells. Moreover, an unexpected preference of UBE2K to operate in trans suggests a general timing mechanism to organize hierarchies amongst ubiquitin signals.

molecular biology↗

Impaired proteostasis is an early feature of the diabetic heart in humans and mice

Diabetes and obesity increase cardiac lipid levels leading to cardiomyopathy and heart failure. We hypothesized that intermittent fasting would reduce cardiac lipid levels. Surprisingly, intermittent fasting increased myocardial triglyceride content, but rescued mortality and attenuated cardiomyopathy in mice overexpressing cardiomyocyte acyl-CoA synthetase 1 (MHC-ACSL1). Lipid overload caused cardiomyocyte accumulation of polyubiquitinated protein aggregates containing desmin, a scaffolding intermediate filament protein, which intermittent fasting prevented. Furthermore, intermittent fasting reversed elevated myocardial C16:0 ceramide content, and knockdown of ceramide synthase CerS5 and CerS6 reduced palmitate-induced protein aggregation, highlighting a role for C16:0 ceramides in this pathology. Conversely, impairing aggrephagy with cardiomyocyte-specific p62 ablation induced heart failure in mice fed a high-fat diet, with paradoxically reduced cardiac lipid content. Crucially, non-failing diabetic human hearts also exhibited protein aggregate pathology. Taken together, these results demonstrate that impaired proteostasis characterizes cardiomyopathy from cardiac lipid overload and identify a promising new therapeutic target for this condition.

molecular biology↗

Spatial profiling and neurovascular communication in the developing and adolescent cortex following prenatal alcohol exposure

Fetal alcohol spectrum disorders (FASD) constitute a wide range of developmental, cognitive, and behavioral impairments caused by prenatal alcohol exposure (PAE). Although neuronal and vascular consequences of PAE have been studied, how alcohol affects the cerebrovasculature within the framework of the neurovascular unit (NVU) across development remains poorly understood. At minimum, the NVU comprises neurons, astrocyte endfeet, and endothelial cells (ECs), which coordinate to maintain brain homeostasis. Here, we used the NanoString Digital Spatial Profiling platform to characterize spatial transcriptomic data from neurons, astrocytes, and ECs from PAE and saccharin (SAC) control cortices at embryonic day 18 (E18) and postnatal day 28 (P28). Differentially expressed genes were then used for Ingenuity Pathway Analysis (IPA) to identify altered biological pathways and perform comparison analyses across developmental time points, while CellChat was used to infer cell cell communication networks. We uncovered thousands of differentially expressed genes and numerous altered pathways and biological processes in PAE cortices across development. Both IPA and CellChat analyses implicated dysregulation of vascular and extracellular matrix (ECM) remodeling, cell adhesion, and neuroinflammatory signaling. CellChat further predicted the loss of several key bidirectional relationships and altered ligand-receptor interactions among neurovascular cell types at E18 and P28. Overall, these findings identify PAE associated alterations in neurovascular gene expression and intercellular signaling across development, providing potential mechanisms by which PAE may disrupt neurodevelopment.

molecular biology↗