Citation: Ilari, A.; Cogliati, V.; Sherif,
N.; Grassilli, E.; Ramazzotti, D.;
Cordani, N.; Cazzaniga, G.; Di Bella,
C.; Lavitrano, M.; Cazzaniga, M.E.;
et al. Differential Expression of
NOTCH-1 and Its Molecular Targets
in Response to Metronomic Followed
by Conventional Therapy in a Patient
with Advanced Triple-Negative Breast
Cancer. Biomedicines 2024, 12, 272.
https://doi.org/10.3390/
biomedicines12020272
Academic Editors: Daniela Carlisi and
Anna De Blasio
Received: 8 December 2023
Revised: 19 January 2024
Accepted: 23 January 2024
Published: 25 January 2024
Copyright: © 2024 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/).
biomedicines
Article
Differential Expression of NOTCH-1 and Its Molecular Targets
in Response to Metronomic Followed by Conventional Therapy
in a Patient with Advanced Triple-Negative Breast Cancer
Alice Ilari
1
, Viola Cogliati
2
, Noorhan Sherif
1
, Emanuela Grassilli
1
, Daniele Ramazzotti
1
, Nicoletta Cordani
1
,
Giorgio Cazzaniga
3
, Camillo Di Bella
3
, Marialuisa Lavitrano
1
, Marina Elena Cazzaniga
1,2
and Maria Grazia Cerrito
1,
*
1
School of Medicine and Surgery, Milano-Bicocca University, 20900 Monza, Italy;
a.ilari@campus.unimib.it (A.I.); n.sherif@campus.unimib.it (N.S.); emanuela.grassilli@unimib.it (E.G.);
daniele.ramazzotti@unimib.it (D.R.); nicoletta.cordani@unimib.it (N.C.);
marialuisa.lavitrano@unimib.it (M.L.); marina.cazzaniga@unimib.it (M.E.C.)
2
Phase 1 Research Centre, Fondazione IRCCS San Gerardo dei Tintori, Via Pergolesi 33, 20900 Monza, Italy;
viola.cogliati@irccs-sangerardo.it
3
Department of Pathology, Fondazione IRCCS San Gerardo dei Tintori, Via Pergolesi 33, 20900 Monza, Italy;
giorgio9cazzaniga@gmail.com (G.C.); camillo.dibella@irccs-sangerardo.it (C.D.B.)
* Correspondence: mariagrazia.cerrito@unimib.it; Tel.: +39-0264488339
Abstract: A group of 27 patients diagnosed with metastatic triple-negative breast cancer (mTNBC)
was randomly distributed into two groups and underwent different lines of metronomic treatment
(mCHT). The former group (N 14) received first-line mCHT and showed a higher overall survival
rate than the second group (N 13), which underwent second-line mCHT. Analysis of one patient still
alive from the first group, diagnosed with mTNBC in 2019, showed a complete metabolic response
(CMR) after a composite approach implicating first-line mCHT followed by second-line epirubicin
and third-line nab-paclitaxel, and was chosen for subsequent molecular characterization. We found
altered expression in the cancer stemness-associated gene NOTCH-1 and its corresponding protein.
Additionally, we found changes in the expression of oncogenes, such as MYC and AKT, along with
their respective proteins. Overall, our data suggest that a first-line treatment with mCHT followed
by MTD might be effective by negatively regulating stemness traits usually associated with the
emergence of drug resistance.
Keywords: metastatic triple-negative breast cancer (mTNBC); metronomic therapy (mCHT); cancer
stem cells (CSCs); NOTCH-1; c-MYC; pAKT
1. Introduction
Triple-negative breast cancer (TNBC) represents 10–20% of all breast cancers and is
characterized by the absence of the expression of estrogen receptors (ER), progesterone
receptors (PR), and the absence of amplification/over-expression of the human epidermal
growth factor receptor 2 (HER2) [1]. These receptors are common targets for breast cancer
therapies, and their absence in TNBC makes it more challenging to treat compared to other
types of breast cancer. Chemotherapy and surgery have represented for years the only
possible treatment approach for these patients [2], who very often relapse or have a spread
of the tumor to other organs [3]. Currently, immune checkpoint inhibitors [4] and the new
class of antibody–drug conjugates have provided valuable options for the treatment of
TNBC [5,6]. Nevertheless, better therapeutic options are needed, both in terms of new
drugs and methods of administering chemotherapy treatments. Many efforts are underway
to identify new therapeutic targets and treatment strategies for TNBC.
Metronomic chemotherapy (mCHT), consisting of continuous administration of
chemotherapy drugs at reduced doses, has been explored in selected patients as an alterna-
Biomedicines 2024, 12, 272. https://doi.org/10.3390/biomedicines12020272 https://www.mdpi.com/journal/biomedicines