Direct interaction of TrkA/CD44v3 is essential for NGF-promoted aggressiveness of breast cancer cells.


Journal

Journal of experimental & clinical cancer research : CR
ISSN: 1756-9966
Titre abrégé: J Exp Clin Cancer Res
Pays: England
ID NLM: 8308647

Informations de publication

Date de publication:
28 Mar 2022
Historique:
received: 19 11 2021
accepted: 03 03 2022
entrez: 29 3 2022
pubmed: 30 3 2022
medline: 5 4 2022
Statut: epublish

Résumé

CD44 is a multifunctional membrane glycoprotein. Through its heparan sulfate chain, CD44 presents growth factors to their receptors. We have shown that CD44 and Tropomyosin kinase A (TrkA) form a complex following nerve growth factor (NGF) induction. Our study aimed to understand how CD44 and TrkA interact and the consequences of inhibiting this interaction regarding the pro-tumoral effect of NGF in breast cancer. After determining which CD44 isoforms (variants) are involved in forming the TrkA/CD44 complex using proximity ligation assays, we investigated the molecular determinants of this interaction. By molecular modeling, we isolated the amino acids involved and confirmed their involvement using mutations. A CD44v3 mimetic peptide was then synthesized to block the TrkA/CD44v3 interaction. The effects of this peptide on the growth, migration and invasion of xenografted triple-negative breast cancer cells were assessed. Finally, we investigated the correlations between the expression of the TrkA/CD44v3 complex in tumors and histo-pronostic parameters. We demonstrated that isoform v3 (CD44v3), but not v6, binds to TrkA in response to NGF stimulation. The final 10 amino acids of exon v3 and the TrkA H112 residue are necessary for the association of CD44v3 with TrkA. Functionally, the CD44v3 mimetic peptide impairs not only NGF-induced RhoA activation, clonogenicity, and migration/invasion of breast cancer cells in vitro but also tumor growth and metastasis in a xenograft mouse model. We also detected TrkA/CD44v3 only in cancerous cells, not in normal adjacent tissues. Collectively, our results suggest that blocking the CD44v3/TrkA interaction can be a new therapeutic option for triple-negative breast cancers.

Sections du résumé

BACKGROUND BACKGROUND
CD44 is a multifunctional membrane glycoprotein. Through its heparan sulfate chain, CD44 presents growth factors to their receptors. We have shown that CD44 and Tropomyosin kinase A (TrkA) form a complex following nerve growth factor (NGF) induction. Our study aimed to understand how CD44 and TrkA interact and the consequences of inhibiting this interaction regarding the pro-tumoral effect of NGF in breast cancer.
METHODS METHODS
After determining which CD44 isoforms (variants) are involved in forming the TrkA/CD44 complex using proximity ligation assays, we investigated the molecular determinants of this interaction. By molecular modeling, we isolated the amino acids involved and confirmed their involvement using mutations. A CD44v3 mimetic peptide was then synthesized to block the TrkA/CD44v3 interaction. The effects of this peptide on the growth, migration and invasion of xenografted triple-negative breast cancer cells were assessed. Finally, we investigated the correlations between the expression of the TrkA/CD44v3 complex in tumors and histo-pronostic parameters.
RESULTS RESULTS
We demonstrated that isoform v3 (CD44v3), but not v6, binds to TrkA in response to NGF stimulation. The final 10 amino acids of exon v3 and the TrkA H112 residue are necessary for the association of CD44v3 with TrkA. Functionally, the CD44v3 mimetic peptide impairs not only NGF-induced RhoA activation, clonogenicity, and migration/invasion of breast cancer cells in vitro but also tumor growth and metastasis in a xenograft mouse model. We also detected TrkA/CD44v3 only in cancerous cells, not in normal adjacent tissues.
CONCLUSION CONCLUSIONS
Collectively, our results suggest that blocking the CD44v3/TrkA interaction can be a new therapeutic option for triple-negative breast cancers.

Identifiants

pubmed: 35346305
doi: 10.1186/s13046-022-02314-4
pii: 10.1186/s13046-022-02314-4
pmc: PMC8962522
doi:

Substances chimiques

CD44V3,8-10 0
Hyaluronan Receptors 0
NTRK1 protein, human 0
Protein Isoforms 0
Nerve Growth Factor 9061-61-4
Receptor, trkA EC 2.7.10.1
tropomyosin kinase EC 2.7.11.28

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

110

Informations de copyright

© 2022. The Author(s).

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Auteurs

Sarah Trouvilliez (S)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Julien Cicero (J)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.
University Artois, UR 2465, Laboratoire de la Barrière Hémato-Encéphalique (LBHE), F-62300, Lens, France.

Romain Lévêque (R)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Léo Aubert (L)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Cyril Corbet (C)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Alexandre Van Outryve (A)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Karolin Streule (K)

Karlsruhe Institute of Technology, Institute of Toxicology and Genetics, 76344, Eggenstein-Leopoldshafen, Germany.

Pierre-Olivier Angrand (PO)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Pamela Völkel (P)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Romain Magnez (R)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Guillaume Brysbaert (G)

University Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle, F-59000, Lille, France.

Caroline Mysiorek (C)

University Artois, UR 2465, Laboratoire de la Barrière Hémato-Encéphalique (LBHE), F-62300, Lens, France.

Fabien Gosselet (F)

University Artois, UR 2465, Laboratoire de la Barrière Hémato-Encéphalique (LBHE), F-62300, Lens, France.

Roland Bourette (R)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Eric Adriaenssens (E)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Xavier Thuru (X)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Chann Lagadec (C)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Jérôme de Ruyck (J)

University Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle, F-59000, Lille, France.

Véronique Orian-Rousseau (V)

Karlsruhe Institute of Technology, Institute of Toxicology and Genetics, 76344, Eggenstein-Leopoldshafen, Germany.

Xuefen Le Bourhis (X)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France.

Robert-Alain Toillon (RA)

University Lille, CNRS, INSERM, CHU Lille, UMR9020-U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, F-59000, Lille, France. robert-alain.toillon@univ-lille.fr.
Université de Lille, Faculté des Sciences et Technologies, UMR CNRS 9020- INSERM U1277 - CANTHER - Cancer Heterogeneity Plasticity and Resistance to Therapies, Bâtiment SN3, 3ème étage, Cité scientifique, 59655, Villeneuve d'Ascq, France. robert-alain.toillon@univ-lille.fr.

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