Citation: Zani, A.P.; Zani, C.P.; Din,
Z.U.; Rodrigues-Filho, E.;
Ueda-Nakamura, T.; Garcia, F.P.; de
Oliveira Silva, S.; Nakamura, C.V.
Dibenzylideneacetone Induces
Apoptosis in Cervical Cancer Cells
through Ros-Mediated Mitochondrial
Damage. Antioxidants 2023, 12, 317.
https://doi.org/10.3390/
antiox12020317
Academic Editors: Vito Pesce and
Angela Maria Serena Lezza
Received: 14 December 2022
Revised: 16 January 2023
Accepted: 25 January 2023
Published: 30 January 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/).
antioxidants
Article
Dibenzylideneacetone Induces Apoptosis in Cervical Cancer
Cells through Ros-Mediated Mitochondrial Damage
Aline Pinto Zani
1
, Caroline Pinto Zani
1
, Zia Ud Din
2
, Edson Rodrigues-Filho
2
,Tânia Ueda-Nakamura
1
,
Francielle Pelegrin Garcia
1
, Sueli de Oliveira Silva
1
and Celso Vataru Nakamura
1,
*
1
Laboratory of Technological Innovation in the Development of Pharmaceuticals and Cosmetics,
State University of Maringá, Maringá CEP 87020-900, PR, Brazil
2
LaBioMMi, Department of Chemistry, Federal University of São Carlos, CP 676,
São Carlos CEP 13565-905, SP, Brazil
* Correspondence: cvnakamura@uem.br; Tel.: +55-(044)-3011-5012; Fax: +55-(044)-3011-5046
Abstract: Cervical cancer is a health problem among women worldwide. Considering the limitations
of prevention and antineoplastic chemotherapy against cervical cancer, research is needed to discover
new, more effective, and safe antitumor agents. In the present study, we investigated the in vitro
cytotoxicity of a new synthetic dibenzylideneacetone derived from 1,5-diaryl-3-oxo-1,4-pentadienyl
(A3K2A3) against cervical cancer cells immortalized by HPV 16 (SiHa), and 18 (HeLa) by MTT assay.
Furthermore, we performed spectrofluorimetry, flow cytometry, and Western blot analyzes to explore
the inhibitory mechanism of A3K2A3 in cervical cancer cells. A3K2A3 showed cytotoxic activity
against both cell lines. Mitochondrial depolarization and reduction in intracellular ATP levels were
observed, which may be dependent on the redox imbalance between increased ROS and reduced
levels of the antioxidant defense. In addition, damage to the cell membrane and DNA, and effective
blocking of cell division in the G2/M phase were detected, which possibly led to the induction
of apoptosis. This result was further confirmed by the upregulation of apoptosis-related proteins
Bax, cytochrome C, and caspases 9 and 3. Our results provided the first evidence that A3K2A3
contributes to the suppression of cervical cancer in vitro, showing promise as a possible alternative
for the treatment of this cancer.
Keywords: dibenzylideneacetone; apoptosis; oxidative stress; HeLa cell; SiHa cell
1. Introduction
Cervical cancer is the fourth most common cancer among women worldwide, with an
estimated 604,000 new cases and 342,000 deaths in 2020. More than 95% of cervical cancer
cases are infection-related with high-risk for human papillomavirus (HPV) [1]. Among the
high-risk HPVs, HPV16 and HPV18 are responsible for almost 70% of these cases [2,3].
In the last decade, screening for HPV lesions through HPV and Pap smear tests,
and prevention through HPV vaccinations have been recognized as the most effective
interventions to control the mortality rate associated with this disease [3,4]. Despite these
screening and prevention programs, the incidence of cervical cancer is still one of the
leading causes of cancer-related death in women [5]. This scenario may be due to the fact
that screening tests are not widely available in many underdeveloped countries, a situation
related to poverty and the lack of resources and infrastructure [6]. Further, vaccination is
limited to young people to ensure effectiveness [7]. Even with recent advances, the clinical
treatments available for cervical cancer, including radiotherapy, chemotherapy, and surgery,
are still not wholly adequate due to the frequent occurrence of adverse effects, among other
limitations, such as systemic toxicity and chemoresistance [8,9].
The need to identify new, more effective, and safer antitumor agents becomes clearly
justifiable. In general, natural products have demonstrated advantages due to their avail-
ability and biological potential and, in recent decades, several natural products have been
Antioxidants 2023, 12, 317. https://doi.org/10.3390/antiox12020317 https://www.mdpi.com/journal/antioxidants