Vol.:(0123456789) 1 3
Parasitology Research (2024) 123:60
https://doi.org/10.1007/s00436-023-08031-x
REVIEW
Apoptosis and its pathways as targets for intracellular pathogens
to persist in cells
Jorge Rodríguez‑González
1,2
· Laila Gutiérrez‑Kobeh
1
Received: 7 March 2023 / Accepted: 10 November 2023
© The Author(s) 2023
Abstract
Apoptosis is a fnely programmed process of cell death in which cells silently dismantle and actively participate in several
operations such as immune response, diferentiation, and cell growth. It can be initiated by three main pathways: the extrin-
sic, the perforin granzyme, and the intrinsic that culminate in the activation of several proteins in charge of tearing down the
cell. On the other hand, apoptosis represents an ordeal for pathogens that live inside cells and maintain a strong dependency
with them; thus, they have evolved multiple strategies to manipulate host cell apoptosis on their behalf. It has been widely
documented that diverse intracellular bacteria, fungi, and parasites can interfere with most steps of the host cell apoptotic
machinery to inhibit or induce apoptosis. Indeed, the inhibition of apoptosis is considered a virulence property shared by many
intracellular pathogens to ensure productive replication. Some pathogens intervene at an early stage by interfering with the
sensing of extracellular signals or transduction pathways. Others sense cellular stress or target the apoptosis regulator proteins
of the Bcl-2 family or caspases. In many cases, the exact molecular mechanisms leading to the interference with the host cell
apoptotic cascade are still unknown. However, intense research has been conducted to elucidate the strategies employed by
intracellular pathogens to modulate host cell death. In this review, we summarize the main routes of activation of apoptosis
and present several processes used by diferent bacteria, fungi, and parasites to modulate the apoptosis of their host cells.
Keywords Apoptosis · Bacteria · Fungi · Intracellular pathogens · Parasites · Signaling pathways
Introduction
Human health is continuously threatened by pathogens and
in response to this, the immune system orchestrates multi-
faceted defense strategies. As a result, pathogens have devel-
oped multiple schemes to overcome human defense mecha-
nisms. Among these, cell death is very important for the host
because it eliminates infected cells and activates the immune
system. However, cell death can become a double-edged
sword: if uncontrolled, it may also lead to tissue damage,
which might subsequently activate the pathogen dissemina-
tion procedures. To avoid this, the major cell death pathways
(apoptosis, pyroptosis, and necroptosis) are highly regulated.
Recently, these three programed cell death pathways have
been included in an entity named PANoptosis directed by a
PANoptosome. The PANoptosome is a multimeric protein
complex responsible for recruiting all the molecules neces-
sary to carry out any of the three types of programmed cell
death (Bedoui et al. 2020; D'Arcy 2019; Samir et al. 2020).
Of these three types of programmed cell death, apoptosis
has typically been described through morphological mark-
ers such as chromatin condensation, cytoplasm contraction,
formation and separation of apoptotic bodies, and the lack
of infammation. Nevertheless, the Committee for Nomen-
clature of Cell Death has determined that to have a clearer
characterization of the diferent types of cell death quantif-
able biochemical parameters must be used instead of mor-
phological ones (Galluzzi et al. 2014).
Handling Editor: Una Ryan
* Laila Gutiérrez-Kobeh
lgutierr@unam.mx
1
Unidad de Investigación UNAM-INC, División de
Investigación, Facultad de Medicina, Universidad
Nacional Autónoma de México-Instituto Nacional de
Cardiología “Ignacio Chávez,”, Juan Badiano No. 1, Col.
Belisario Domínguez, Sección XVI, Delegación Tlalpan,
C.P. 14080 Ciudad de México, México
2
Present Address: Laboratorio de Estudios Epidemiológicos,
Clínicos, Diseños Experimentales e Investigación, Facultad
de Ciencias Químicas, Universidad Autónoma “Benito
Juárez” de Oaxaca, Oaxaca, Mexico