Local Modulation of BMP-Signalling for Therapeutic Neovascularization using siSmad 6

https://doi.org/10.1007/s00392-024-02526-y

Tatjana Fricke (Freiburg im Breisgau)1, H. Schmitt (Freiburg im Breisgau)1, R. Süss (Freiburg im Breisgau)2, C. Grundmann (Freiburg im Breisgau)2, M. Moser (Bad Krozingen)3, J. Eßer (Freiburg im Breisgau)1, Q. Zhou (Basel)4

1Universitäts-Herzzentrum Freiburg - Bad Krozingen Klinik für Kardiologie und Angiologie Freiburg im Breisgau, Deutschland; 2Universitätsklinikum Freiburg Institut für Pharmakologie Freiburg im Breisgau, Deutschland; 3Universitäts-Herzzentrum Freiburg / Bad Krozingen Klinik für Kardiologie und Angiologie Bad Krozingen, Deutschland; 4Universitätsspital Basel Klinik für Innere Medizin Basel, Schweiz

 

Introduction:
Peripheral Artery Disease (PAD) affects around 20% of Europe's population older than 55 years of age, making it one of the most widespread cardiovascular diseases. Up until today, treatment options - especially non-interventional - remain unsatisfactory in both target and outcome. Bone Morphogenetic Proteins (BMPs) are members of the Transforming Growth Factor beta (TGF-beta) superfamily. Increasing evidence suggests their crucial role in vascular remodelling. Upon activation of the BMP ligand-receptor complex, the intracellular signalling pathway is activated through Smad proteins. While Smads 1/5/7 interact with Smad 4 to induce BMP-signalling, Smad 6 generally inhibits the pathway, resulting in an autoregulated system. Previous data shows that overexpression of Smad 6 inhibited Vascular Endothelial Growth Factor (VEGF)-stimulated neovascularization in endothelial cells. Therefore, the current project aims to target Smad 6 specifically using RNA - interference (RNAi) to promote endogenous neovascularization at sites of ischemia.

Methods and Results:
Six- to eight-week-old C57/BL6J wildtype mice were used for the study. The mice were treated with a unilateral femoral artery ligation combined with a sham procedure on the respective other hind limb. Sufficient ischemia was ensured by Laser Doppler Perfusion Imaging (LDPI). Silencing Smad 6 RNA (siSmad 6) or control (siNeg) embedded in hydrogel was subcutaneously injected around the surgical area. Post-interventional revascularization was evaluated on days 3, 7, 10, 14 and 21 using LDPI. In comparison to the control group, the mice injected with siSmad 6 demonstrated accelerated revascularization following day 7 after induction of ischemia, with an increase of perfusion by 40% on day 10. In immunofluorescent evaluation, a two-fold-increase in total capillary-quantity as well as a 1.6-fold-increase in inflammatory cells, i.e., leukocytes, could be demonstrated in ischemic regions. Molecular methods confirmed increased inflammatory responses as well as a significant increase in vascular smooth muscle gene transcription, thereby indicating increased arterialization of preformed capillaries. Western blots for downstream BMP-pathway regulators indicated a total increase in pathway activity following injection of siSmad 6. Immunofluorescent demonstration of significantly increased quantities of pERK-positive cells in the experimental group suggests the increase in pathway-activity to be linked to MAPK/ERK-pathway signalling.

Conclusion:
Our results demonstrate that local inhibition of Smad 6 promotes revascularization in a murine hindlimb ischemia model. This might open up new options in future PAD treatment.

Funding:
This project was funded by grants from the German Research Foundation (DFG) to J.S.E. (ES 582/3-1) and Q.Z. (ZH 231/5-1) as well as a dissertation scholarship from the German Cardiac Society (DGK) to T.F.
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