Citation: Saar, M.; Jaal, J.; Meltsov, A.;
Laasfeld, T.; Lust, H.; Kasvandik, S.;
Lavogina, D. Exploring the Molecular
Players behind the Potentiation of
Chemotherapy Effects by
Durvalumab in Lung
Adenocarcinoma Cell Lines.
Pharmaceutics 2023, 15, 1485.
https://doi.org/10.3390/
pharmaceutics15051485
Academic Editor: Xiaoyong Wang
Received: 11 March 2023
Revised: 5 May 2023
Accepted: 9 May 2023
Published: 12 May 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/).
pharmaceutics
Article
Exploring the Molecular Players behind the Potentiation of
Chemotherapy Effects by Durvalumab in Lung
Adenocarcinoma Cell Lines
Marika Saar
1,2,3
, Jana Jaal
1,4
, Alvin Meltsov
5,6
,Tõnis Laasfeld
7,8
, Helen Lust
1
, Sergo Kasvandik
9
and Darja Lavogina
1,5,7,
*
1
Institute of Clinical Medicine, Faculty of Medicine, University of Tartu, 50406 Tartu, Estonia
2
Instituteof Pharmacy, University of Tartu, 50411 Tartu, Estonia
3
Pharmacy, Tartu University Hospital,50406 Tartu, Estonia
4
Haematology and Oncology Clinic, Tartu University Hospital, 50406 Tartu, Estonia
5
Competence Centre on Health Technologies, 50411 Tartu, Estonia
6
Department of Genetics and Cell Biology, GROW School for Oncology and Developmental Biology,
Maastricht University, 6200 MD Maastricht, The Netherlands
7
Instituteof Chemistry, University of Tartu, 50411 Tartu, Estonia
8
Department of Computer Science, University of Tartu, 51009 Tartu, Estonia
9
Proteomics Core Facility, Institute of Technology, University of Tartu, 50411 Tartu, Estonia
* Correspondence: darja.lavogina@ut.ee; Tel.: +372-737-5296
Abstract: Immune checkpoint inhibitors are increasingly used in combination with chemotherapy
for the treatment of non-small cell lung cancer, yet the success of combination therapies is relatively
limited. Thus, more detailed insight regarding the tumor molecular markers that may affect the
responsiveness of patients to therapy is required. Here, we set out to explore the proteome of two
lung adenocarcinoma cell lines (HCC-44 and A549) treated with cisplatin, pemetrexed, durvalumab,
and the corresponding mixtures to establish the differences in post-treatment protein expression that
can serve as markers of chemosensitivity or resistance. The mass spectrometry study showed that the
addition of durvalumab to the treatment mixture resulted in cell line- and chemotherapeutic agent-
dependent responses and confirmed the previously reported involvement of DNA repair machinery
in the potentiation of the chemotherapy effect. Further validation using immunofluorescence also
indicated that the potentiating effect of durvalumab in the case of cisplatin treatment was dependent
on the tumor suppressor RB-1 in the PD-L1 weakly positive cells. In addition, we identified aldehyde
dehydrogenase ALDH1A3 as the general putative resistance marker. Further studies in patient biopsy
samples will be required to confirm the clinical significance of these findings.
Keywords: lung adenocarcinoma; cisplatin; pemetrexed; durvalumab; proteomics; chemosensitiv-
ity; resistance
1. Introduction
Non-small cell lung cancer (NSCLC) is one of the leading and deadliest types of
cancer, causing annually 1.8 million deaths worldwide [1]. The treatment of NSCLC
depends on the stage, histology, and tumor cell features, including genetic driver alter-
ations and the expression of markers that predict the efficacy of immunotherapy (e.g.,
programmed death-ligand 1, PD-L1) [2]. Despite the emergence of targeted therapy strate-
gies, chemotherapy remains the backbone of neoadjuvant and adjuvant treatment before
and after surgery in early-stage NSCLC as well as the optimal first-line treatment option
in metastatic NSCLC [3,4]. In recent decades, however, the choice of therapies has been
complemented by PD-1/PD-L1 axis-targeting immune checkpoint inhibitors (ICIs), which
are frequently used in combination with chemotherapy.
Pharmaceutics 2023, 15, 1485. https://doi.org/10.3390/pharmaceutics15051485 https://www.mdpi.com/journal/pharmaceutics