Vascular Pharmacology 140 (2021) 106873
Available online 13 May 2021
1537-1891/© 2021 Elsevier Inc. All rights reserved.
Extracellular vesicles (EVs) in ischemic conditioning and angiogenesis:
Focus on endothelial derived EVs
Edoardo Alfì
a
, Cecilia Thairi
a
, Saveria Femmin` o
b
, Giuseppe Alloatti
c
, Francesco Moccia
d
,
Maria F. Brizzi
b
, Pasquale Pagliaro
a, *
, Claudia Penna
a
a
Department of Clinical and Biological Sciences, University of Turin, Regione Gonzole 10, 10043 Orbassano, TO, Italy
b
Department of Medical Sciences, University of Turin, Corso Dogliotti 14, 10126 Turin, Italy
c
Uni-Astiss, Polo Universitario Rita Levi Montalcini, 14100 Asti, Italy
d
Department of Biology and Biotechnology, University of Pavia, Laboratory of General Physiology, 27100 Pavia, Italy
A R T I C L E INFO
Keywords:
Endothelial cells
Cardioprotection
Biomarkers
Remote ischemic conditioning
ABSTRACT
During myocardial ischemia, timely reperfusion is critical to limit infarct area and the overall loss of cardiac
contractile function. However, reperfusion further exacerbates the damage of the ischemic heart. This type of
injury is known as ischemia-reperfusion injury (IRI). Ischemic conditioning is a procedure which consists of brief
cycles of ischemia and reperfusion in order to protect the myocardium against IRI. Remote ischemic conditioning
(RIC), namely transient brief episodes of ischemia at a remote site before a subsequent damaging ischemia/
reperfusion procedure of the target organ (e.g., the heart), protects against IRI. However, how the stimulus of RIC
is transduced from the remote organ to the ischemic heart is still unknown. Recently, extracellular vesicles (EVs)
have been proposed to have a role in the RIC procedure. The endothelium releases EVs and is also one of the
tissues mostly exposed to EVs during their journey to the target organ. Moreover, EVs may have important roles
in angiogenesis and, therefore, in the remodeling of post-ischemic organs. Here we analyze how EVs may
contribute to the overall cardioprotective effect and the implication of the endothelium and its EVs in RIC
mediated acute cardioprotection as well as in angiogenesis.
1. Introduction
The paradigm of cardioprotection induced by ischemic pre-
conditioning (IPC) was established by Murry and colleagues [1]. These
authors demonstrated that brief cycles of 5 min coronary occlusion
interspersed with 5 min of reperfusion immediately prior to 40 min of
coronary occlusion were able to signifcantly reduce infarct size (IS).
Subsequently remote ischemic conditioning (RIC) was described [2].
Unlike IPC, which protects only those districts directly subjected to
initial ischemia by coronary occlusion, in RIC the ischemic insult is
applied to distant areas within the heart or distant organs. Among
distant organs limbs [3] are included. RIC gained popularity for this
intriguing feature and it is believed a more applicable type of
conditioning for cardioprotection in humans. RIC can be applied before
ischemia, that is remote preconditioning (RIPC), during organ ischemia,
namely remote per-conditioning (RIPerC) and/or after organ ischemia,
that is remote post-conditioning (RIPostC). All these procedures,
collectively known as RIC, showed similar cardioprotective effects [4].
Several evidence suggest that many organs can undergo RIC in order
to protect the heart from ischemia/reperfusion (I/R) injury (IRI).
Indeed, cardioprotection can be evoked by ischemic episodes in distant
organs, such as liver [5], small intestine [6], and kidney [7]. Different
interesting mechanisms have been proposed to explain the car-
dioprotective effect of RIC [8] including: i) the RIC as a trigger of specifc
mediators in the preconditioned remote organ/limb, ii) the transfer of
such mediators from remote organ/limb to the heart, and fnally iii) the
Abbreviations: AMI, Acute myocardial infarction; EC, Endothelial cells; ECFCs, Endothelial colony forming cells; EEs, Early endosomes; EPC, Endothelial pro-
genitor cells; eNOS, Endothelial nitric oxide synthase; ESCRT, Endosomal sorting complex required for transport; EVs, Extracellular vesicles; HUVECs, Human
umbilical vein endothelial cells; ILVs, Intraluminal vesicles; I/R, Ischemia reperfusion; IRI, Ischemia reperfusion injury; IPC, Ischemic preconditioning; LEs, Late
endosomes; MMP, Matrix metalloprotease; MS, Metabolic syndrome; MSCs, Mesenchymal stem cells; MVBs, Multivesicular bodies; PI3K, Phosphoinositide-3-kinase;
RIC, Remote ischemic conditioning; RIPC, Remote ischemic preconditioning; RIPerC, Remote ischemic perconditioning; RIPostC, Remote ischemic post conditioning.
* Corresponding author.
E-mail address: pasquale.pagliaro@unito.it (P. Pagliaro).
Contents lists available at ScienceDirect
Vascular Pharmacology
journal homepage: www.elsevier.com/locate/vph
https://doi.org/10.1016/j.vph.2021.106873
Received 10 April 2021; Received in revised form 7 May 2021; Accepted 11 May 2021