ERα-36 regulates progesterone receptor activity in breast cancer.


Journal

Breast cancer research : BCR
ISSN: 1465-542X
Titre abrégé: Breast Cancer Res
Pays: England
ID NLM: 100927353

Informations de publication

Date de publication:
19 05 2020
Historique:
received: 16 12 2019
accepted: 13 04 2020
entrez: 21 5 2020
pubmed: 21 5 2020
medline: 6 11 2020
Statut: epublish

Résumé

Alterations in estrogen and progesterone signaling, via their respective receptors, estrogen receptor alpha (ERα) and progesterone receptor (PR), respectively, are largely involved in the development of breast cancer (BC). The recent identification of ERα-36, a splice variant of ERα, has uncovered a new facet of this pathology. Although ERα-36 expression is associated with poor prognosis, metastasis development, and resistance to treatment, its predictive value has so far not been associated with a BC subtype and its mechanisms of action remain understudied. To study ERα-36 expression in BC specimens, we performed immunochemical experiments. Next, the role of ERα-36 in progesterone signaling was investigated by generating KO clones using the CRISPR/CAS9 technology. PR signaling was also assessed by proximity ligation assay, Western blotting, RT-QPCR, and ChIP experiments. Finally, proliferation assays were performed with the IncuCyte technology and migration experiments using scratch assays. Here, we demonstrate that ERα-36 expression at the plasma membrane is correlated with a reduced disease-free survival in a cohort of 160 BC patients, particularly in PR-positive tumors, suggesting a crosstalk between ERα-36 and PR. Indeed, we show that ERα-36 interacts constitutively with PR in the nucleus of tumor cells. Moreover, it regulates PR expression and phosphorylation on key residues, impacting the biological effects of progesterone. ERα-36 is thus a regulator of PR signaling, interfering with its transcriptional activity and progesterone-induced anti-proliferative effects as well as migratory capacity. Hence, ERα-36 may constitute a new prognostic marker as well as a potential target in PR-positive BC.

Sections du résumé

BACKGROUND
Alterations in estrogen and progesterone signaling, via their respective receptors, estrogen receptor alpha (ERα) and progesterone receptor (PR), respectively, are largely involved in the development of breast cancer (BC). The recent identification of ERα-36, a splice variant of ERα, has uncovered a new facet of this pathology. Although ERα-36 expression is associated with poor prognosis, metastasis development, and resistance to treatment, its predictive value has so far not been associated with a BC subtype and its mechanisms of action remain understudied.
METHODS
To study ERα-36 expression in BC specimens, we performed immunochemical experiments. Next, the role of ERα-36 in progesterone signaling was investigated by generating KO clones using the CRISPR/CAS9 technology. PR signaling was also assessed by proximity ligation assay, Western blotting, RT-QPCR, and ChIP experiments. Finally, proliferation assays were performed with the IncuCyte technology and migration experiments using scratch assays.
RESULTS
Here, we demonstrate that ERα-36 expression at the plasma membrane is correlated with a reduced disease-free survival in a cohort of 160 BC patients, particularly in PR-positive tumors, suggesting a crosstalk between ERα-36 and PR. Indeed, we show that ERα-36 interacts constitutively with PR in the nucleus of tumor cells. Moreover, it regulates PR expression and phosphorylation on key residues, impacting the biological effects of progesterone.
CONCLUSIONS
ERα-36 is thus a regulator of PR signaling, interfering with its transcriptional activity and progesterone-induced anti-proliferative effects as well as migratory capacity. Hence, ERα-36 may constitute a new prognostic marker as well as a potential target in PR-positive BC.

Identifiants

pubmed: 32429997
doi: 10.1186/s13058-020-01278-7
pii: 10.1186/s13058-020-01278-7
pmc: PMC7238515
doi:

Substances chimiques

Biomarkers, Tumor 0
ESR1 protein, human 0
Estrogen Receptor alpha 0
Protein Isoforms 0
Receptors, Progesterone 0
ERBB2 protein, human EC 2.7.10.1
Receptor, ErbB-2 EC 2.7.10.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

50

Subventions

Organisme : INCA
ID : none
Pays : International
Organisme : Direction Générale de l'offre de Soins
ID : none
Pays : International
Organisme : Government ivory
ID : none
Pays : International
Organisme : Canceroloe CLARA
ID : none
Pays : International

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Auteurs

Henri-Philippe Konan (HP)

Université de Lyon, F-69000, Lyon, France.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France.

Loay Kassem (L)

Clinical Oncology Department, Faculty of Medicine, Cairo University, Cairo, Egypt.

Soleilmane Omarjee (S)

Université de Lyon, F-69000, Lyon, France.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France.
Cancer Research UK, Cambridge Institute, University of Cambridge, Cambridge, CB2 0RE, UK.

Ausra Surmieliova-Garnès (A)

Université de Lyon, F-69000, Lyon, France.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France.

Julien Jacquemetton (J)

Université de Lyon, F-69000, Lyon, France.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France.

Elodie Cascales (E)

genOway, 69007, Lyon, France.

Amélie Rezza (A)

genOway, 69007, Lyon, France.

Olivier Trédan (O)

Université de Lyon, F-69000, Lyon, France.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France.
Medical Oncology Department, Centre Léon Bérard, F-69000, Lyon, France.

Isabelle Treilleux (I)

Université de Lyon, F-69000, Lyon, France.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France.
Pathology Department, Centre Léon Bérard, F-69000, Lyon, France.

Coralie Poulard (C)

Université de Lyon, F-69000, Lyon, France.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France.

Muriel Le Romancer (M)

Université de Lyon, F-69000, Lyon, France. muriel.leromancer@lyon.unicancer.fr.
Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Bâtiment D, 28 rue Laennec, 69373 Lyon Cedex 08, F-69000, Lyon, France. muriel.leromancer@lyon.unicancer.fr.
CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon, F-69000, Lyon, France. muriel.leromancer@lyon.unicancer.fr.

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