cancers
Article
Pimavanserin: A Novel Autophagy Modulator for Pancreatic
Cancer Treatment
Sharavan Ramachandran, Itishree S. Kaushik and Sanjay K. Srivastava *
Citation: Ramachandran, S.;
Kaushik, I.S.; Srivastava, S.K.
Pimavanserin: A Novel Autophagy
Modulator for Pancreatic Cancer
Treatment. Cancers 2021, 13, 5661.
https://doi.org/10.3390/cancers
13225661
Academic Editors: Subhash
C. Chauhan and David Wong
Received: 2 June 2021
Accepted: 5 November 2021
Published: 12 November 2021
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2021 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/).
Department of Immunotherapeutics and Biotechnology, Center for Tumor Immunology and Targeted
Cancer Therapy, Texas Tech University Health Sciences Center, Abilene, TX 79601, USA;
sharavan.ramachandran@ttuhsc.edu (S.R.); i.kaushik@ttuhsc.edu (I.S.K.)
* Correspondence: sanjay.srivastava@ttuhsc.edu; Tel.: +1-325-696-0464; Fax: +1-325-676-3875
Simple Summary: Pimavanserin a novel anti-psychotic drug suppresses the growth of pancreatic
tumors in vitro and in vivo and can be developed as a treatment option for pancreatic cancer.
Abstract: Pancreatic tumors exhibit high basal autophagy compared to that of other cancers. Several
studies including those from our laboratory reported that enhanced autophagy leads to apoptosis
in cancer cells. In this study, we evaluated the autophagy and apoptosis inducing effects of Pima-
vanserin tartrate (PVT). Autophagic effects of PVT were determined by Acridine Orange assay and
Transmission Electron Microscopy analysis. Clinical significance of ULK1 in normal and pancreatic
cancer patients was evaluated by R2 and GEPIA cancer genomic databases. Modulation of proteins in
autophagy signaling was assessed by Western blotting and Immunofluorescence. Apoptotic effects of
PVT was evaluated by Annexin-V/APC assay. Subcutaneous xenograft pancreatic tumor model was
used to evaluate the autophagy-mediated apoptotic effects of PVT in vivo. Autophagy was induced
upon PVT treatment in pancreatic ducal adenocarcinoma (PDAC) cells. Pancreatic cancer patients
exhibit reduced levels of autophagy initiator gene, ULK1, which correlated with reduced patient
survival. Interestingly, PVT induced the expression of autophagy markers ULK1, FIP200, Atg101,
Beclin-1, Atg5, LC3A/B, and cleavage of caspase-3, an indicator of apoptosis in several PDAC cells.
ULK1 agonist LYN-1604 enhanced the autophagic and apoptotic effects of PVT. On the other hand,
autophagy inhibitors chloroquine and bafilomycin blocked the autophagic and apoptotic effects of
PVT in PDAC cells. Notably, chloroquine abrogated the growth suppressive effects of PVT by 25% in
BxPC3 tumor xenografts in nude mice. Collectively, our results indicate that PVT mediated pancreatic
tumor growth suppression was associated with induction of autophagy mediated apoptosis.
Keywords: cancer; autophagy; cell death; drug repurposing; apoptosis
1. Introduction
Several stress elements including drug-induced stress activate intra-cellular survival
mechanisms such as autophagy to tolerate the harsh conditions or trigger cell death path-
ways [1,2]. Autophagy occurs in three forms such as; macroautophagy, microautophagy,
and chaperone-mediated autophagy. Macroautophagy, hereafter referred to as autophagy,
is the most prevalent form of autophagy in eukaryotes, and play a pivotal role in maintain-
ing tissue homeostasis. Autophagy is considered as an evolutionarily conserved catabolic
process, where the sequestered cellular organelles are delivered to lysosomes by the au-
tophagosomes for degradation. This ubiquitous process happens in five distinct stages:
initiation, vesicle nucleation, vesicle elongation, autophagosome expansion, and fusion
of autophagosome with lysosome for degradation. ULK1 orchestrates the initiation of
autophagy, where it assembles with Atg13, Atg101, and FIP200 to form the autophagy
initiation complex. Phosphorylation of ULK1 at Ser 757 prevents ULK1 in forming the
autophagy initiation complex, thereby inhibits autophagy. The ULK1 complex guides
the assembly of class-III PI3K or VPS34 complex comprising VPS34, Atg14, UVRAG and
Cancers 2021, 13, 5661. https://doi.org/10.3390/cancers13225661 https://www.mdpi.com/journal/cancers