Citation: Huang, K.; Pitman, M.;
Oladosu, O.; Echesabal-Chen, J.;
Vojtech, L.; Esobi, I.; Larsen, J.; Jo, H.;
Stamatikos, A. The Impact of
MiR-33a-5p Inhibition in
Pro-Inflammatory Endothelial Cells.
Diseases 2023, 11, 88. https://
doi.org/10.3390/diseases11030088
Academic Editors: Diana Díaz-García
and Santiago Gómez-Ruiz
Received: 13 May 2023
Revised: 18 June 2023
Accepted: 21 June 2023
Published: 24 June 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
diseases
Article
The Impact of MiR-33a-5p Inhibition in Pro-Inflammatory
Endothelial Cells
Kun Huang
1
, Mark Pitman
2
, Olanrewaju Oladosu
1
, Jing Echesabal-Chen
1
, Lucia Vojtech
3
, Ikechukwu Esobi
1
,
Jessica Larsen
2,4
, Hanjoong Jo
5
and Alexis Stamatikos
1,
*
1
Department of Food, Nutrition, and Packaging Sciences, Clemson University, Clemson, SC 29634, USA;
kunh@g.clemson.edu (K.H.); oolados@g.clemson.edu (O.O.); jchen11@clemson.edu (J.E.-C.);
iesobi@g.clemson.edu (I.E.)
2
Department of Chemical and Biomolecular Engineering, Clemson University, Clemson, SC 29634, USA;
pitman@g.clemson.edu (M.P.); larsenj@clemson.edu (J.L.)
3
Department of Obstetrics & Gynecology, University of Washington, Seattle, WA 98109, USA; luciav@uw.edu
4
Department of Bioengineering, Clemson University, Clemson, SC 29634, USA
5
Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University,
Atlanta, GA 30322, USA; hjo@emory.edu
* Correspondence: adstama@clemson.edu
Abstract: Evidence suggests cholesterol accumulation in pro-inflammatory endothelial cells (EC)
contributes to triggering atherogenesis and driving atherosclerosis progression. Therefore, inhibit-
ing miR-33a-5p within inflamed endothelium may prevent and treat atherosclerosis by enhancing
apoAI-mediated cholesterol efflux by upregulating ABCA1. However, it is not entirely elucidated
whether inhibition of miR-33a-5p in pro-inflammatory EC is capable of increasing ABCA1-dependent
cholesterol efflux. In our study, we initially transfected LPS-challenged, immortalized mouse aortic
EC (iMAEC) with either pAntimiR33a5p plasmid DNA or the control plasmid, pScr. We detected
significant increases in both ABCA1 protein expression and apoAI-mediated cholesterol efflux in
iMAEC transfected with pAntimiR33a5p when compared to iMAEC transfected with pScr. We subse-
quently used polymersomes targeting inflamed endothelium to deliver either pAntimiR33a5p or pScr
to cultured iMAEC and showed that the polymersomes were selective in targeting pro-inflammatory
iMAEC. Moreover, when we exposed LPS-challenged iMAEC to these polymersomes, we observed a
significant decrease in miR-33a-5p expression in iMAEC incubated with polymersomes containing
pAntimR33a5p versus control iMAEC. We also detected non-significant increases in both ABCA1 pro-
tein and apoAI-mediated cholesterol in iMAEC exposed to polymersomes containing pAntimR33a5p
when compared to control iMAEC. Based on our results, inhibiting miR-33a-5p in pro-inflammatory
EC exhibits atheroprotective effects, and so precisely delivering anti-miR-33a-5p to these cells is a
promising anti-atherogenic strategy.
Keywords: endothelial activation; endothelial dysfunction; HDL; microRNA; nanoparticle; nanother-
apy; reverse cholesterol transport; vascular inflammation; VCAM-1
1. Introduction
Atherosclerotic cardiovascular disease is a condition that kills more people worldwide
than any other disease [1]. While the pathophysiology of atherosclerotic cardiovascular
disease is complex and poorly understood [2], endothelial cell (EC) inflammation is rec-
ognized to contribute to both atherogenesis and atherosclerosis progression [3]. Indeed,
vascular inflammation is an intriguing component of atherosclerosis, as inflammation
in the EC facilitates monocyte/macrophage intimal entry, which allows macrophages to
engulf intimal cholesterol [4]. This in turn may result in the accumulation of lipid-laden
macrophages within the intima, leading to atherosclerosis formation [5].
Endothelial dysfunction and activation are strongly linked with EC inflammation [6,7].
Interestingly, an acknowledged precursor to endothelial dysfunction/activation is EC
Diseases 2023, 11, 88. https://doi.org/10.3390/diseases11030088 https://www.mdpi.com/journal/diseases