Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin Expression

Prostate cancer is a major public health concern and one of the most prevalent forms of cancer worldwide. The definition of altered signaling pathways implicated in this complex disease is thus essential. In this context, abnormal expression of the receptor of Macrophage Colony-Stimulating Factor-1...

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Main Authors: Alexandra Mougel, Eric Adriaenssens, Boris Guyot, Lu Tian, Stéphanie Gobert, Thierry Chassat, Philippe Persoons, David Hannebique, Hélène Bauderlique-Le Roy, Jérôme Vicogne, Xuefen Le Bourhis, Roland P. Bourette
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:International Journal of Molecular Sciences
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Online Access:https://www.mdpi.com/1422-0067/23/24/16028
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author Alexandra Mougel
Eric Adriaenssens
Boris Guyot
Lu Tian
Stéphanie Gobert
Thierry Chassat
Philippe Persoons
David Hannebique
Hélène Bauderlique-Le Roy
Jérôme Vicogne
Xuefen Le Bourhis
Roland P. Bourette
author_facet Alexandra Mougel
Eric Adriaenssens
Boris Guyot
Lu Tian
Stéphanie Gobert
Thierry Chassat
Philippe Persoons
David Hannebique
Hélène Bauderlique-Le Roy
Jérôme Vicogne
Xuefen Le Bourhis
Roland P. Bourette
author_sort Alexandra Mougel
collection DOAJ
description Prostate cancer is a major public health concern and one of the most prevalent forms of cancer worldwide. The definition of altered signaling pathways implicated in this complex disease is thus essential. In this context, abnormal expression of the receptor of Macrophage Colony-Stimulating Factor-1 (M-CSF or CSF-1) has been described in prostate cancer cells. Yet, outcomes of this expression remain unknown. Using mouse and human prostate cancer cell lines, this study has investigated the functionality of the wild-type CSF-1 receptor in prostate tumor cells and identified molecular mechanisms underlying its ligand-induced activation. Here, we showed that upon CSF-1 binding, the receptor autophosphorylates and activates multiple signaling pathways in prostate tumor cells. Biological experiments demonstrated that the CSF-1R/CSF-1 axis conferred significant advantages in cell growth and cell invasion in vitro. Mouse xenograft experiments showed that CSF-1R expression promoted the aggressiveness of prostate tumor cells. In particular, we demonstrated that the ligand-activated CSF-1R increased the expression of <i>spp1</i> transcript encoding for osteopontin, a key player in cancer development and metastasis. Therefore, this study highlights that the CSF-1 receptor is fully functional in a prostate cancer cell and may be a potential therapeutic target for the treatment of prostate cancer.
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spelling doaj.art-4abd2f9f4c0e43af8c357e0f93cfb0372023-11-24T15:31:45ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-12-0123241602810.3390/ijms232416028Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin ExpressionAlexandra Mougel0Eric Adriaenssens1Boris Guyot2Lu Tian3Stéphanie Gobert4Thierry Chassat5Philippe Persoons6David Hannebique7Hélène Bauderlique-Le Roy8Jérôme Vicogne9Xuefen Le Bourhis10Roland P. Bourette11University of Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, FranceUniversity of Lille, CNRS, Inserm, CHU Lille, UMR9020-UMR1277—CANTHER—Cancer Heterogeneity, Plasticity and Resistance to Therapies, F-59000 Lille, FranceCentre de Recherche en Cancérologie de Lyon, Department of Cancer Initiation and Tumor Cell Identity CNRS UMR5286, Inserm U1052, Lyon 1 University, F-69000 Lyon, FranceUniversity of Lille, CNRS, Inserm, CHU Lille, UMR9020-UMR1277—CANTHER—Cancer Heterogeneity, Plasticity and Resistance to Therapies, F-59000 Lille, FranceUniversity of Lyon, Universiteé Claude Bernard Lyon 1, CNRS UMR-5305, Laboratoire de Biologie Tissulaire et Ingeénierie Theérapeutique, F-69367 Lyon, FranceInstitut Pasteur de Lille—PLEHTA (Plateforme d’Expérimentation et de Haute Technologie Animale), F-59019 Lille, FranceInstitut Pasteur de Lille—PLEHTA (Plateforme d’Expérimentation et de Haute Technologie Animale), F-59019 Lille, FranceInstitut Pasteur de Lille—PLEHTA (Plateforme d’Expérimentation et de Haute Technologie Animale), F-59019 Lille, FranceCNRS, Inserm, CHU Lille, Institut Pasteur de Lille, US41-UMS 2014-PLBS, University of Lille, F-59000 Lille, FranceUniversity of Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, FranceUniversity of Lille, CNRS, Inserm, CHU Lille, UMR9020-UMR1277—CANTHER—Cancer Heterogeneity, Plasticity and Resistance to Therapies, F-59000 Lille, FranceUniversity of Lille, CNRS, Inserm, CHU Lille, UMR9020-UMR1277—CANTHER—Cancer Heterogeneity, Plasticity and Resistance to Therapies, F-59000 Lille, FranceProstate cancer is a major public health concern and one of the most prevalent forms of cancer worldwide. The definition of altered signaling pathways implicated in this complex disease is thus essential. In this context, abnormal expression of the receptor of Macrophage Colony-Stimulating Factor-1 (M-CSF or CSF-1) has been described in prostate cancer cells. Yet, outcomes of this expression remain unknown. Using mouse and human prostate cancer cell lines, this study has investigated the functionality of the wild-type CSF-1 receptor in prostate tumor cells and identified molecular mechanisms underlying its ligand-induced activation. Here, we showed that upon CSF-1 binding, the receptor autophosphorylates and activates multiple signaling pathways in prostate tumor cells. Biological experiments demonstrated that the CSF-1R/CSF-1 axis conferred significant advantages in cell growth and cell invasion in vitro. Mouse xenograft experiments showed that CSF-1R expression promoted the aggressiveness of prostate tumor cells. In particular, we demonstrated that the ligand-activated CSF-1R increased the expression of <i>spp1</i> transcript encoding for osteopontin, a key player in cancer development and metastasis. Therefore, this study highlights that the CSF-1 receptor is fully functional in a prostate cancer cell and may be a potential therapeutic target for the treatment of prostate cancer.https://www.mdpi.com/1422-0067/23/24/16028M-CSFCSF-1 receptorprostateC2H cell lineTRAMPosteopontin
spellingShingle Alexandra Mougel
Eric Adriaenssens
Boris Guyot
Lu Tian
Stéphanie Gobert
Thierry Chassat
Philippe Persoons
David Hannebique
Hélène Bauderlique-Le Roy
Jérôme Vicogne
Xuefen Le Bourhis
Roland P. Bourette
Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin Expression
International Journal of Molecular Sciences
M-CSF
CSF-1 receptor
prostate
C2H cell line
TRAMP
osteopontin
title Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin Expression
title_full Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin Expression
title_fullStr Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin Expression
title_full_unstemmed Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin Expression
title_short Macrophage-Colony-Stimulating Factor Receptor Enhances Prostate Cancer Cell Growth and Aggressiveness In Vitro and In Vivo and Increases Osteopontin Expression
title_sort macrophage colony stimulating factor receptor enhances prostate cancer cell growth and aggressiveness in vitro and in vivo and increases osteopontin expression
topic M-CSF
CSF-1 receptor
prostate
C2H cell line
TRAMP
osteopontin
url https://www.mdpi.com/1422-0067/23/24/16028
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