Citation: Yong, J.; Gröger, S.;
von Bremen, J.; Meyle, J.; Ruf, S.
Immunorthodontics: PD-L1, a
Novel Immunomodulator in
Cementoblasts, Is Regulated by
HIF-1α under Hypoxia. Cells 2022,
11, 2350. https://doi.org/10.3390/
cells11152350
Academic Editors: Li Xiao and
Takeo Tsutsui
Received: 1 July 2022
Accepted: 28 July 2022
Published: 30 July 2022
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2022 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/).
cells
Article
Immunorthodontics: PD-L1, a Novel Immunomodulator in
Cementoblasts, Is Regulated by HIF-1α under Hypoxia
Jiawen Yong
1,2,3,
* , Sabine Gröger
1,2
, Julia von Bremen
1
, Joerg Meyle
2
and Sabine Ruf
1
1
Department of Orthodontics, Faculty of Medicine, Justus Liebig University Giessen, 35392 Giessen, Germany;
sabine.e.groeger@dentist.med.uni-giessen.de (S.G.); julia.v.bremen@dentist.med.uni-giessen.de (J.v.B.);
sabine.ruf@dentist.med.uni-giessen.de (S.R.)
2
Department of Periodontology, Faculty of Medicine, Justus Liebig University Giessen,
35392 Giessen, Germany; joerg.meyle@dentist.med.uni-giessen.de
3
Stomatology Hospital, School of Stomatology, Zhejiang University School of Medicine, Zhejiang Provincial
Clinical Research Center for Oral Diseases, Key Laboratory of Oral Biomedical Research of Zhejiang Province,
Cancer Center of Zhejiang University, Hangzhou 310003, China
* Correspondence: jiawen.yong@dentist.med.uni-giessen.de or yongjiawen.ggl@gmail.com;
Tel.: +49-641-99-46131
Abstract: Recent studies have revealed that hypoxia alters the PD-L1 expression in periodontal cells.
HIF-1α is a key regulator for PD-L1. As hypoxia presents a hallmark of an orthodontically induced
microenvironment, hypoxic stimulation of PD-L1 expression may play vital roles in immunorthodon-
tics and orthodontically induced inflammatory root resorption (OIIRR). This study aims to investigate
the hypoxic regulation of PD-L1 in cementoblasts, and its interaction with hypoxia-induced HIF-1α
expression. The cementoblast (OCCM-30) cells (M. Somerman, NIH, NIDCR, Bethesda, Maryland)
were cultured in the presence and absence of cobalt (II) chloride (CoCl
2
). Protein expression of
PD-L1 and HIF-1α as well as their gene expression were evaluated by Western blotting and RT-qPCR.
Immunofluorescence was applied to visualize the localization of the proteins within cells. The HIF-1α
inhibitor (HY-111387, MedChemExpress) was added, and CRISPR/Cas9 plasmid targeting HIF-1α
was transferred for further investigation by flow cytometry analysis. Under hypoxic conditions,
cementoblasts undergo an up-regulation of PD-L1 expression at protein and mRNA levels. Silencing
of HIF-1α using CRISPR/Cas9 indicated a major positive correlation with HIF-1α in regulating
PD-L1 expression. Taken together, these findings show the influence of hypoxia on PD-L1 expression
is modulated in a HIF-1α dependent manner. The HIF-1α/PD-L1 pathway may play a role in the
immune response of cementoblasts. Thus, combined HIF-1α/PD-L1 inhibition could be of possible
therapeutic relevance for OIIRR prevention.
Keywords: cementoblasts; hypoxia; PD-L1; HIF-1α; orthodontic; immunorthodontics
1. Introduction
Orthodontic tooth movement (OTM) takes place as a direct consequence of connective
tissue remodeling within the periodontium which occurs through a localized inflamma-
tory response induced by external mechanical forces [1] when using removable or fixed
orthodontic appliances [2]. The compressive force results in an altered homeostasis of
the periodontal ligament (PDL) cells and the host immune response [3]. This orthodontic
force causes capillary vasodilatation within the blood vessels of the PDL, in turn resulting
in migration of immune cells and the expression of various cytokines such as GAS-6 [4].
These soluble cytokines regulate the process of cementum resorption, so-called orthodontic-
induced inflammatory root resorption (OIIRR), in response to orthodontic force [5]. Ce-
mentum seems to be able to protect the tooth root from OIIRR [6]. PDL cells (mainly
cementoblasts) are capable of repairing resorption pits with new cementum [7,8] and play
an immunomodulatory role under hypoxic conditions [9].
Cells 2022, 11, 2350. https://doi.org/10.3390/cells11152350 https://www.mdpi.com/journal/cells