Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell dissemination

Abstract Background Metastatic hormone-naïve prostate cancer (mHNPC) is an infrequent form of this tumor type that is characterized by metastasis at the time of diagnosis and accounts for up to 50% of prostate cancer-related deaths. Despite the extensive characterization of localized and metastatic...

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Main Authors: Natalia Martin-Martin, Saioa Garcia-Longarte, Jon Corres-Mendizabal, Uxue Lazcano, Ianire Astobiza, Laura Bozal-Basterra, Nicolas Herranz, Hielke van Splunder, Onintza Carlevaris, Mikel Pujana-Vaquerizo, María Teresa Blasco, Ana M. Aransay, Antonio Rosino, Julian Tudela, Daniel Jimenez, Alberto Martinez, Andrei Salca, Aida Santos-Martín, Sofía Rey, Aitziber Ugalde-Olano, David Gonzalo, Mariona Graupera, Roger R. Gomis, Joaquin Mateo, Miguel Unda, Enrique Gonzalez-Billalabeitia, Ana Loizaga-Iriarte, Isabel Mendizabal, Arkaitz Carracedo
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Language:English
Published: BMC 2025-06-01
Series:Genome Biology
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Online Access:https://doi.org/10.1186/s13059-025-03623-5
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author Natalia Martin-Martin
Saioa Garcia-Longarte
Jon Corres-Mendizabal
Uxue Lazcano
Ianire Astobiza
Laura Bozal-Basterra
Nicolas Herranz
Hielke van Splunder
Onintza Carlevaris
Mikel Pujana-Vaquerizo
María Teresa Blasco
Ana M. Aransay
Antonio Rosino
Julian Tudela
Daniel Jimenez
Alberto Martinez
Andrei Salca
Aida Santos-Martín
Sofía Rey
Aitziber Ugalde-Olano
David Gonzalo
Mariona Graupera
Roger R. Gomis
Joaquin Mateo
Miguel Unda
Enrique Gonzalez-Billalabeitia
Ana Loizaga-Iriarte
Isabel Mendizabal
Arkaitz Carracedo
author_facet Natalia Martin-Martin
Saioa Garcia-Longarte
Jon Corres-Mendizabal
Uxue Lazcano
Ianire Astobiza
Laura Bozal-Basterra
Nicolas Herranz
Hielke van Splunder
Onintza Carlevaris
Mikel Pujana-Vaquerizo
María Teresa Blasco
Ana M. Aransay
Antonio Rosino
Julian Tudela
Daniel Jimenez
Alberto Martinez
Andrei Salca
Aida Santos-Martín
Sofía Rey
Aitziber Ugalde-Olano
David Gonzalo
Mariona Graupera
Roger R. Gomis
Joaquin Mateo
Miguel Unda
Enrique Gonzalez-Billalabeitia
Ana Loizaga-Iriarte
Isabel Mendizabal
Arkaitz Carracedo
author_sort Natalia Martin-Martin
collection DOAJ
description Abstract Background Metastatic hormone-naïve prostate cancer (mHNPC) is an infrequent form of this tumor type that is characterized by metastasis at the time of diagnosis and accounts for up to 50% of prostate cancer-related deaths. Despite the extensive characterization of localized and metastatic castration-resistant prostate cancer, the molecular characteristics of mHNPC remain largely unexplored. Results Here, we provide the first extensive transcriptomics characterization of primary tumor specimens from patients with mHNPC. We generate discovery and validation bulk and single-cell RNA-seq datasets and perform integrative computational analysis in combination with experimental studies. Our results provide unprecedented evidence of the distinctive transcriptional profile of mHNPC and identify stroma remodeling as a predominant feature of these tumors. Importantly, we discover a central role for the SRY-box transcription factor 11 (SOX11) in triggering a heterotypic communication that is associated with the acquisition of metastatic properties. Conclusions Our study will constitute an invaluable resource for a profound understanding of mHNPC that can influence patient management.
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spelling doaj-art-aadc768ef9d149eea54de13238e479f62025-08-20T02:05:38ZengBMCGenome Biology1474-760X2025-06-0126112310.1186/s13059-025-03623-5Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell disseminationNatalia Martin-Martin0Saioa Garcia-Longarte1Jon Corres-Mendizabal2Uxue Lazcano3Ianire Astobiza4Laura Bozal-Basterra5Nicolas Herranz6Hielke van Splunder7Onintza Carlevaris8Mikel Pujana-Vaquerizo9María Teresa Blasco10Ana M. Aransay11Antonio Rosino12Julian Tudela13Daniel Jimenez14Alberto Martinez15Andrei Salca16Aida Santos-Martín17Sofía Rey18Aitziber Ugalde-Olano19David Gonzalo20Mariona Graupera21Roger R. Gomis22Joaquin Mateo23Miguel Unda24Enrique Gonzalez-Billalabeitia25Ana Loizaga-Iriarte26Isabel Mendizabal27Arkaitz Carracedo28Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Vall Hebron Institute of Oncology, Hebron University Hospital CampusEndothelial Pathobiology and Microenviroment Group, Josep Carreras Leukemia Research Institute (IJC)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Cancer Science Program, Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and TechnologyCenter for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Department of Urology, Morales Meseguer University HospitalDepartment of Pathology, Morales Meseguer University HospitalDepartment of Urology, Morales Meseguer University HospitalBiobanco Nodo 3, Morales Meseguer University HospitalVall Hebron Institute of Oncology, Hebron University Hospital CampusDepartment of Urology, Basurto University HospitalDepartment of Urology, Basurto University HospitalDepartment of Pathology, Basurto University HospitalTraslational Prostate Cancer Research Lab, CIC bioGUNE-Basurto, Biobizkaia Health Research Institute Technology ParkCentro de Investigación Biomédica En Red de Cáncer (CIBERONC)Centro de Investigación Biomédica En Red de Cáncer (CIBERONC)Vall Hebron Institute of Oncology, Hebron University Hospital CampusCentro de Investigación Biomédica En Red de Cáncer (CIBERONC)Department of Urology, Morales Meseguer University HospitalCentro de Investigación Biomédica En Red de Cáncer (CIBERONC)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA)Abstract Background Metastatic hormone-naïve prostate cancer (mHNPC) is an infrequent form of this tumor type that is characterized by metastasis at the time of diagnosis and accounts for up to 50% of prostate cancer-related deaths. Despite the extensive characterization of localized and metastatic castration-resistant prostate cancer, the molecular characteristics of mHNPC remain largely unexplored. Results Here, we provide the first extensive transcriptomics characterization of primary tumor specimens from patients with mHNPC. We generate discovery and validation bulk and single-cell RNA-seq datasets and perform integrative computational analysis in combination with experimental studies. Our results provide unprecedented evidence of the distinctive transcriptional profile of mHNPC and identify stroma remodeling as a predominant feature of these tumors. Importantly, we discover a central role for the SRY-box transcription factor 11 (SOX11) in triggering a heterotypic communication that is associated with the acquisition of metastatic properties. Conclusions Our study will constitute an invaluable resource for a profound understanding of mHNPC that can influence patient management.https://doi.org/10.1186/s13059-025-03623-5Prostate cancerMetastatic driverCancer cell reprogrammingSingle-cell transcriptomicsHormone-naïveTumor-stromal heterotypic communication
spellingShingle Natalia Martin-Martin
Saioa Garcia-Longarte
Jon Corres-Mendizabal
Uxue Lazcano
Ianire Astobiza
Laura Bozal-Basterra
Nicolas Herranz
Hielke van Splunder
Onintza Carlevaris
Mikel Pujana-Vaquerizo
María Teresa Blasco
Ana M. Aransay
Antonio Rosino
Julian Tudela
Daniel Jimenez
Alberto Martinez
Andrei Salca
Aida Santos-Martín
Sofía Rey
Aitziber Ugalde-Olano
David Gonzalo
Mariona Graupera
Roger R. Gomis
Joaquin Mateo
Miguel Unda
Enrique Gonzalez-Billalabeitia
Ana Loizaga-Iriarte
Isabel Mendizabal
Arkaitz Carracedo
Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell dissemination
Genome Biology
Prostate cancer
Metastatic driver
Cancer cell reprogramming
Single-cell transcriptomics
Hormone-naïve
Tumor-stromal heterotypic communication
title Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell dissemination
title_full Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell dissemination
title_fullStr Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell dissemination
title_full_unstemmed Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell dissemination
title_short Transcriptional analysis of metastatic hormone-naïve prostate cancer primary tumor biopsies reveals a relevant role for SOX11 in prostate cancer cell dissemination
title_sort transcriptional analysis of metastatic hormone naive prostate cancer primary tumor biopsies reveals a relevant role for sox11 in prostate cancer cell dissemination
topic Prostate cancer
Metastatic driver
Cancer cell reprogramming
Single-cell transcriptomics
Hormone-naïve
Tumor-stromal heterotypic communication
url https://doi.org/10.1186/s13059-025-03623-5
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