Temozolomide-Acquired Resistance Is Associated with Modulation of the Integrin Repertoire in Glioblastoma, Impact of α5β1 Integrin

Despite extensive treatment, glioblastoma inevitably recurs, leading to an overall survival of around 16 months. Understanding why and how tumours resist to radio/chemotherapies is crucial to overcome this unmet oncological challenge. Primary and acquired resistance to Temozolomide (TMZ), the standa...

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Published inCancers Vol. 14; no. 2; p. 369
Main Authors Sani, Saidu, Pallaoro, Nikita, Messe, Mélissa, Bernhard, Chloé, Etienne-Selloum, Nelly, Kessler, Horst, Marinelli, Luciana, Entz-Werle, Natacha, Foppolo, Sophie, Martin, Sophie, Reita, Damien, Dontenwill, Monique
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 12.01.2022
MDPI
Subjects
Amino acids
Apoptosis
Biochemistry, Molecular Biology
Brain cancer
Brain tumors
Cancer
Cell culture
Cell growth
Cell migration
Cell proliferation
Chemotherapy
Clinical trials
Genomics
Glioblastoma
Glioblastoma cells
Glioma cells
Integrins
Life Sciences
MDM2 protein
Medical prognosis
Neurobiology
Neurons and Cognition
Pharmaceutical sciences
Pharmacology
Proteins
Senescence
Temozolomide
Therapeutic targets
Transcriptomics
Tumors
France
integrins
temozolomide resistance
glioblastoma
p53 reactivation
Online AccessGet full text
ISSN2072-6694
2072-6694
DOI10.3390/cancers14020369

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Abstract Despite extensive treatment, glioblastoma inevitably recurs, leading to an overall survival of around 16 months. Understanding why and how tumours resist to radio/chemotherapies is crucial to overcome this unmet oncological challenge. Primary and acquired resistance to Temozolomide (TMZ), the standard-of-care chemotherapeutic drug, have been the subjects of several studies. This work aimed to evaluate molecular and phenotypic changes occurring during and after TMZ treatment in a glioblastoma cell model, the U87MG. These initially TMZ-sensitive cells acquire long-lasting resistance even after removal of the drug. Transcriptomic analysis revealed that profound changes occurred between parental and resistant cells, particularly at the level of the integrin repertoire. Focusing on α5β1 integrin, which we proposed earlier as a glioblastoma therapeutic target, we demonstrated that its expression was decreased in the presence of TMZ but restored after removal of the drug. In this glioblastoma model of recurrence, α5β1 integrin plays an important role in the proliferation and migration of tumoral cells. We also demonstrated that reactivating p53 by MDM2 inhibitors concomitantly with the inhibition of this integrin in recurrent cells may overcome the TMZ resistance. Our results may explain some integrin-based targeted therapy failure as integrin expressions are highly switchable during the time of treatment. We also propose an alternative way to alter the viability of recurrent glioblastoma cells expressing a high level of α5β1 integrin.
AbstractList Despite extensive treatment, glioblastoma inevitably recurs, leading to an overall survival of around 16 months. Understanding why and how tumours resist to radio/chemotherapies is crucial to overcome this unmet oncological challenge. Primary and acquired resistance to Temozolomide (TMZ), the standard-of-care chemotherapeutic drug, have been the subjects of several studies. This work aimed to evaluate molecular and phenotypic changes occurring during and after TMZ treatment in a glioblastoma cell model, the U87MG. These initially TMZ-sensitive cells acquire long-lasting resistance even after removal of the drug. Transcriptomic analysis revealed that profound changes occurred between parental and resistant cells, particularly at the level of the integrin repertoire. Focusing on α5β1 integrin, which we proposed earlier as a glioblastoma therapeutic target, we demonstrated that its expression was decreased in the presence of TMZ but restored after removal of the drug. In this glioblastoma model of recurrence, α5β1 integrin plays an important role in the proliferation and migration of tumoral cells. We also demonstrated that reactivating p53 by MDM2 inhibitors concomitantly with the inhibition of this integrin in recurrent cells may overcome the TMZ resistance. Our results may explain some integrin-based targeted therapy failure as integrin expressions are highly switchable during the time of treatment. We also propose an alternative way to alter the viability of recurrent glioblastoma cells expressing a high level of α5β1 integrin.
Despite extensive treatment, glioblastoma inevitably recurs, leading to an overall survival of around 16 months. Understanding why and how tumours resist to radio/chemotherapies is crucial to overcome this unmet oncological challenge. Primary and acquired resistance to Temozolomide (TMZ), the standard-of-care chemotherapeutic drug, have been the subjects of several studies. This work aimed to evaluate molecular and phenotypic changes occurring during and after TMZ treatment in a glioblastoma cell model, the U87MG. These initially TMZ-sensitive cells acquire long-lasting resistance even after removal of the drug. Transcriptomic analysis revealed that profound changes occurred between parental and resistant cells, particularly at the level of the integrin repertoire. Focusing on α5β1 integrin, which we proposed earlier as a glioblastoma therapeutic target, we demonstrated that its expression was decreased in the presence of TMZ but restored after removal of the drug. In this glioblastoma model of recurrence, α5β1 integrin plays an important role in the proliferation and migration of tumoral cells. We also demonstrated that reactivating p53 by MDM2 inhibitors concomitantly with the inhibition of this integrin in recurrent cells may overcome the TMZ resistance. Our results may explain some integrin-based targeted therapy failure as integrin expressions are highly switchable during the time of treatment. We also propose an alternative way to alter the viability of recurrent glioblastoma cells expressing a high level of α5β1 integrin.Despite extensive treatment, glioblastoma inevitably recurs, leading to an overall survival of around 16 months. Understanding why and how tumours resist to radio/chemotherapies is crucial to overcome this unmet oncological challenge. Primary and acquired resistance to Temozolomide (TMZ), the standard-of-care chemotherapeutic drug, have been the subjects of several studies. This work aimed to evaluate molecular and phenotypic changes occurring during and after TMZ treatment in a glioblastoma cell model, the U87MG. These initially TMZ-sensitive cells acquire long-lasting resistance even after removal of the drug. Transcriptomic analysis revealed that profound changes occurred between parental and resistant cells, particularly at the level of the integrin repertoire. Focusing on α5β1 integrin, which we proposed earlier as a glioblastoma therapeutic target, we demonstrated that its expression was decreased in the presence of TMZ but restored after removal of the drug. In this glioblastoma model of recurrence, α5β1 integrin plays an important role in the proliferation and migration of tumoral cells. We also demonstrated that reactivating p53 by MDM2 inhibitors concomitantly with the inhibition of this integrin in recurrent cells may overcome the TMZ resistance. Our results may explain some integrin-based targeted therapy failure as integrin expressions are highly switchable during the time of treatment. We also propose an alternative way to alter the viability of recurrent glioblastoma cells expressing a high level of α5β1 integrin.
Simple SummaryGlioblastomas are the deadliest brain tumours. The standard of care associates surgery, radio- and chemotherapy with Temozolomide as the reference drug. Despite this treatment, most of the tumours recur. The characterization of resistance mechanisms is of paramount importance to enable the proposal of more effective therapies. In this work we aimed to evaluate the molecular changes occurring during and after Temozolomide treatment in a glioma cell line. A high plasticity in the integrin repertoire exists in these cells. As an example, variations of the α5β1 integrin expression were observed with a reduction during the treatment and re-expression after removal of the drug. The association of integrin antagonists with p53 reactivators appears to be efficient in recurrent tumours. Specific integrins may thus be particularly targetable at different time points of glioblastoma treatment and combination therapies evaluated according to their time-dependent expression.AbstractDespite extensive treatment, glioblastoma inevitably recurs, leading to an overall survival of around 16 months. Understanding why and how tumours resist to radio/chemotherapies is crucial to overcome this unmet oncological challenge. Primary and acquired resistance to Temozolomide (TMZ), the standard-of-care chemotherapeutic drug, have been the subjects of several studies. This work aimed to evaluate molecular and phenotypic changes occurring during and after TMZ treatment in a glioblastoma cell model, the U87MG. These initially TMZ-sensitive cells acquire long-lasting resistance even after removal of the drug. Transcriptomic analysis revealed that profound changes occurred between parental and resistant cells, particularly at the level of the integrin repertoire. Focusing on α5β1 integrin, which we proposed earlier as a glioblastoma therapeutic target, we demonstrated that its expression was decreased in the presence of TMZ but restored after removal of the drug. In this glioblastoma model of recurrence, α5β1 integrin plays an important role in the proliferation and migration of tumoral cells. We also demonstrated that reactivating p53 by MDM2 inhibitors concomitantly with the inhibition of this integrin in recurrent cells may overcome the TMZ resistance. Our results may explain some integrin-based targeted therapy failure as integrin expressions are highly switchable during the time of treatment. We also propose an alternative way to alter the viability of recurrent glioblastoma cells expressing a high level of α5β1 integrin.
Author Etienne-Selloum, Nelly
Dontenwill, Monique
Marinelli, Luciana
Martin, Sophie
Sani, Saidu
Reita, Damien
Kessler, Horst
Messe, Mélissa
Entz-Werle, Natacha
Foppolo, Sophie
Bernhard, Chloé
Pallaoro, Nikita
AuthorAffiliation 3 Department of Pharmacy, Institut de Cancérologie Strasbourg Europe (ICANS), 67200 Strasbourg, France
6 Pediatric Onco-Hematology Unit, University Hospital of Strasbourg, 67098 Strasbourg, France
7 Département de Génétique Moléculaire des Cancers, Oncologie Moléculaire & Pharmacogénétique, University Hospital of Strasbourg, 67000 Strasbourg, France
4 Department of Chemistry, Institute for Advanced Study, Technical University of Munich, 85748 Garching, Germany; kessler@tum.de
5 Dipartimento di Farmacia, Università degli Studi di Napoli “Federico II”, 80131 Naples, Italy; lmarinel@unina.it
2 Cancer and Diabetic Research Group, Department of Biochemistry, Faculty of Biological Science, Federal University Ndufu-Alike Ikwo, Abakaliki 482131, Nigeria
1 Laboratoire de Bioimagerie et Pathologies (LBP), UMR CNRS 7021, Faculté de Pharmacie, Université de Strasbourg, 67401 Illkirch, France; Sanisaidu96@gmail.com (S.S.); npallaoro@unistra.fr (N.P.); melissa.messe@etu.unistra.fr (M.M.); chloe.bernhard@e
AuthorAffiliation_xml – name: 5 Dipartimento di Farmacia, Università degli Studi di Napoli “Federico II”, 80131 Naples, Italy; lmarinel@unina.it
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– name: 3 Department of Pharmacy, Institut de Cancérologie Strasbourg Europe (ICANS), 67200 Strasbourg, France
– name: 1 Laboratoire de Bioimagerie et Pathologies (LBP), UMR CNRS 7021, Faculté de Pharmacie, Université de Strasbourg, 67401 Illkirch, France; Sanisaidu96@gmail.com (S.S.); npallaoro@unistra.fr (N.P.); melissa.messe@etu.unistra.fr (M.M.); chloe.bernhard@etu.unistra.fr (C.B.); nelly.etienne-selloum@unistra.fr (N.E.-S.); Natacha.Entz-Werle@chru-strasbourg.fr (N.E.-W.); sophie.foppolo@unistra.fr (S.F.); sophie.martin@unistra.fr (S.M.); damien.reita@gmail.com (D.R.)
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Keywords integrins
temozolomide resistance
glioblastoma
p53 reactivation
Language English
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Snippet Despite extensive treatment, glioblastoma inevitably recurs, leading to an overall survival of around 16 months. Understanding why and how tumours resist to...
Simple SummaryGlioblastomas are the deadliest brain tumours. The standard of care associates surgery, radio- and chemotherapy with Temozolomide as the...
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SubjectTerms Amino acids
Apoptosis
Biochemistry, Molecular Biology
Brain cancer
Brain tumors
Cancer
Cell culture
Cell growth
Cell migration
Cell proliferation
Chemotherapy
Clinical trials
Genomics
Glioblastoma
Glioblastoma cells
Glioma cells
Integrins
Life Sciences
MDM2 protein
Medical prognosis
Neurobiology
Neurons and Cognition
Pharmaceutical sciences
Pharmacology
Proteins
Senescence
Temozolomide
Therapeutic targets
Transcriptomics
Tumors
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Title Temozolomide-Acquired Resistance Is Associated with Modulation of the Integrin Repertoire in Glioblastoma, Impact of α5β1 Integrin
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Volume 14
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