Molecular events in neuroendocrine prostate cancer development

Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a su...

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Published inNature reviews. Urology Vol. 18; no. 10; pp. 581 - 596
Main Authors Wang, Yong, Wang, Yu, Ci, Xinpei, Choi, Stephen Y. C., Crea, Francesco, Lin, Dong, Wang, Yuzhuo
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.10.2021
Nature Publishing Group
Subjects
631/208/68/2486
631/67/589/466
Adenocarcinoma - drug therapy
Adenocarcinoma - genetics
Adenocarcinoma - metabolism
Adenocarcinoma - pathology
Androgen Antagonists - therapeutic use
Androgens
Antineoplastic Agents - therapeutic use
Care and treatment
Cell receptors
Cell Transdifferentiation
Development and progression
Disease Progression
Gene expression
Genetic aspects
Health aspects
Humans
Male
Medicine
Medicine & Public Health
Neuroendocrine Tumors - genetics
Neuroendocrine Tumors - metabolism
Neuroendocrine Tumors - pathology
Phenotype
Platinum Compounds - therapeutic use
Prostate cancer
Prostatic Neoplasms - drug therapy
Prostatic Neoplasms - genetics
Prostatic Neoplasms - metabolism
Prostatic Neoplasms - pathology
Prostatic Neoplasms, Castration-Resistant - drug therapy
Prostatic Neoplasms, Castration-Resistant - genetics
Prostatic Neoplasms, Castration-Resistant - metabolism
Prostatic Neoplasms, Castration-Resistant - pathology
Receptors, Androgen - metabolism
Review Article
Urology
Canada
Online AccessGet full text
ISSN1759-4812
1759-4820
1759-4820
DOI10.1038/s41585-021-00490-0

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Abstract Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a subject of debate. The survival of patients with NEPC is poor, and few effective treatment options are available. To improve clinical outcomes, understanding of the biology and molecular mechanisms regulating NEPC development is crucial. Various NEPC molecular drivers make temporal contributions during NEPC development, and despite the limited treatment options available, several novel targeted therapeutics are currently under research. Neuroendocrine prostate cancer predominantly develops from adenocarcinoma following a period of androgen suppressive treatment. Outcomes in patients with this disease are poor; the understanding of the molecular mechanisms behind its development will improve future targeted therapy options. Key points Neuroendocrine prostate cancer (NEPC) is an aggressive variant form that is characterized by low or absent androgen receptor (AR) expression, gain of the neuroendocrine phenotype and is not responsive to therapies targeting AR signalling. De novo NEPC accounts for less than 2% of all prostate cancers, but treatment-induced NEPC occurs in 10–17% of patients with castration-resistant prostate cancer by evolving from adenocarcinoma, probably as a result of a transdifferentiation process. Molecular mechanisms underlying NEPC development include genomic alterations, abnormal regulation of epigenetic regulators, transcription factors and other molecular pathways. The temporal contribution and co-operation of NEPC drivers during adenocarcinoma to NEPC transdifferentiation is largely unknown; thus, longitudinal study of serial patient samples and preclinical models that recapitulate the entire disease progression is warranted. Longitudinal analyses of the only clinically relevant patient-derived xenograft model with serial genomic and transcriptomic data available throughout the adenocarcinoma-to-NEPC transdifferentiation process (LTL331/331 R) could group NEPC-driving molecular alterations into early and terminal events, suggesting their roles during different phases of NEPC development. Platinum-based chemotherapy is the only treatment currently available for NEPC. Advances in NEPC research have led to new potential therapies that are undergoing investigation in clinical trials or in preclinical development.
AbstractList Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a subject of debate. The survival of patients with NEPC is poor, and few effective treatment options are available. To improve clinical outcomes, understanding of the biology and molecular mechanisms regulating NEPC development is crucial. Various NEPC molecular drivers make temporal contributions during NEPC development, and despite the limited treatment options available, several novel targeted therapeutics are currently under research. Neuroendocrine prostate cancer predominantly develops from adenocarcinoma following a period of androgen suppressive treatment. Outcomes in patients with this disease are poor; the understanding of the molecular mechanisms behind its development will improve future targeted therapy options. Key points Neuroendocrine prostate cancer (NEPC) is an aggressive variant form that is characterized by low or absent androgen receptor (AR) expression, gain of the neuroendocrine phenotype and is not responsive to therapies targeting AR signalling. De novo NEPC accounts for less than 2% of all prostate cancers, but treatment-induced NEPC occurs in 10-17% of patients with castration-resistant prostate cancer by evolving from adenocarcinoma, probably as a result of a transdifferentiation process. Molecular mechanisms underlying NEPC development include genomic alterations, abnormal regulation of epigenetic regulators, transcription factors and other molecular pathways. The temporal contribution and co-operation of NEPC drivers during adenocarcinoma to NEPC transdifferentiation is largely unknown; thus, longitudinal study of serial patient samples and preclinical models that recapitulate the entire disease progression is warranted. Longitudinal analyses of the only clinically relevant patient-derived xenograft model with serial genomic and transcriptomic data available throughout the adenocarcinoma-to-NEPC transdifferentiation process (LTL331/331 R) could group NEPC-driving molecular alterations into early and terminal events, suggesting their roles during different phases of NEPC development. Platinum-based chemotherapy is the only treatment currently available for NEPC. Advances in NEPC research have led to new potential therapies that are undergoing investigation in clinical trials or in preclinical development.
Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a subject of debate. The survival of patients with NEPC is poor, and few effective treatment options are available. To improve clinical outcomes, understanding of the biology and molecular mechanisms regulating NEPC development is crucial. Various NEPC molecular drivers make temporal contributions during NEPC development, and despite the limited treatment options available, several novel targeted therapeutics are currently under research.Neuroendocrine prostate cancer predominantly develops from adenocarcinoma following a period of androgen suppressive treatment. Outcomes in patients with this disease are poor; the understanding of the molecular mechanisms behind its development will improve future targeted therapy options.
Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a subject of debate. The survival of patients with NEPC is poor, and few effective treatment options are available. To improve clinical outcomes, understanding of the biology and molecular mechanisms regulating NEPC development is crucial. Various NEPC molecular drivers make temporal contributions during NEPC development, and despite the limited treatment options available, several novel targeted therapeutics are currently under research.
Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a subject of debate. The survival of patients with NEPC is poor, and few effective treatment options are available. To improve clinical outcomes, understanding of the biology and molecular mechanisms regulating NEPC development is crucial. Various NEPC molecular drivers make temporal contributions during NEPC development, and despite the limited treatment options available, several novel targeted therapeutics are currently under research.Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a subject of debate. The survival of patients with NEPC is poor, and few effective treatment options are available. To improve clinical outcomes, understanding of the biology and molecular mechanisms regulating NEPC development is crucial. Various NEPC molecular drivers make temporal contributions during NEPC development, and despite the limited treatment options available, several novel targeted therapeutics are currently under research.
Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from adenocarcinoma in response to drug-induced androgen receptor signalling inhibition, although the mechanisms behind this transdifferentiation are a subject of debate. The survival of patients with NEPC is poor, and few effective treatment options are available. To improve clinical outcomes, understanding of the biology and molecular mechanisms regulating NEPC development is crucial. Various NEPC molecular drivers make temporal contributions during NEPC development, and despite the limited treatment options available, several novel targeted therapeutics are currently under research. Neuroendocrine prostate cancer predominantly develops from adenocarcinoma following a period of androgen suppressive treatment. Outcomes in patients with this disease are poor; the understanding of the molecular mechanisms behind its development will improve future targeted therapy options. Key points Neuroendocrine prostate cancer (NEPC) is an aggressive variant form that is characterized by low or absent androgen receptor (AR) expression, gain of the neuroendocrine phenotype and is not responsive to therapies targeting AR signalling. De novo NEPC accounts for less than 2% of all prostate cancers, but treatment-induced NEPC occurs in 10–17% of patients with castration-resistant prostate cancer by evolving from adenocarcinoma, probably as a result of a transdifferentiation process. Molecular mechanisms underlying NEPC development include genomic alterations, abnormal regulation of epigenetic regulators, transcription factors and other molecular pathways. The temporal contribution and co-operation of NEPC drivers during adenocarcinoma to NEPC transdifferentiation is largely unknown; thus, longitudinal study of serial patient samples and preclinical models that recapitulate the entire disease progression is warranted. Longitudinal analyses of the only clinically relevant patient-derived xenograft model with serial genomic and transcriptomic data available throughout the adenocarcinoma-to-NEPC transdifferentiation process (LTL331/331 R) could group NEPC-driving molecular alterations into early and terminal events, suggesting their roles during different phases of NEPC development. Platinum-based chemotherapy is the only treatment currently available for NEPC. Advances in NEPC research have led to new potential therapies that are undergoing investigation in clinical trials or in preclinical development.
Audience Academic
Author Wang, Yu
Wang, Yuzhuo
Ci, Xinpei
Crea, Francesco
Lin, Dong
Choi, Stephen Y. C.
Wang, Yong
AuthorAffiliation 3 Department of Urology, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, China
5 School of Life Health and Chemical Sciences, The Open University, Milton Keynes, UK
2 Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Vancouver, BC, Canada
4 Department of Experimental Therapeutics, BC Cancer Agency, Vancouver, BC, Canada
1 Vancouver Prostate Centre, Vancouver, BC, Canada
6 These authors contributed equally: Yong Wang, Yu Wang
AuthorAffiliation_xml – name: 1 Vancouver Prostate Centre, Vancouver, BC, Canada
– name: 3 Department of Urology, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, China
– name: 2 Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Vancouver, BC, Canada
– name: 6 These authors contributed equally: Yong Wang, Yu Wang
– name: 4 Department of Experimental Therapeutics, BC Cancer Agency, Vancouver, BC, Canada
– name: 5 School of Life Health and Chemical Sciences, The Open University, Milton Keynes, UK
Author_xml – sequence: 1
  givenname: Yong
  surname: Wang
  fullname: Wang, Yong
  organization: Vancouver Prostate Centre, Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Department of Urology, Qilu Hospital, Cheeloo College of Medicine, Shandong University
– sequence: 2
  givenname: Yu
  surname: Wang
  fullname: Wang, Yu
  organization: Vancouver Prostate Centre, Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Department of Experimental Therapeutics, BC Cancer Agency
– sequence: 3
  givenname: Xinpei
  surname: Ci
  fullname: Ci, Xinpei
  organization: Vancouver Prostate Centre, Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Department of Experimental Therapeutics, BC Cancer Agency
– sequence: 4
  givenname: Stephen Y. C.
  surname: Choi
  fullname: Choi, Stephen Y. C.
  organization: Vancouver Prostate Centre, Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Department of Experimental Therapeutics, BC Cancer Agency
– sequence: 5
  givenname: Francesco
  surname: Crea
  fullname: Crea, Francesco
  organization: School of Life Health and Chemical Sciences, The Open University
– sequence: 6
  givenname: Dong
  orcidid: 0000-0002-0303-2599
  surname: Lin
  fullname: Lin, Dong
  email: dlin@bccrc.ca
  organization: Vancouver Prostate Centre, Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Department of Experimental Therapeutics, BC Cancer Agency
– sequence: 7
  givenname: Yuzhuo
  orcidid: 0000-0002-9749-8591
  surname: Wang
  fullname: Wang, Yuzhuo
  email: ywang@bccrc.ca
  organization: Vancouver Prostate Centre, Department of Urologic Sciences, Faculty of Medicine, University of British Columbia, Department of Experimental Therapeutics, BC Cancer Agency
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34290447$$D View this record in MEDLINE/PubMed
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10.1056/NEJMoa1014618
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10.1016/j.jtho.2021.02.009
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Yong W. and Yu W. researched data for the article, Yong W., Yu W., X.C. and D.L. wrote the article, Yuzhuo W., D.L., Yong W., Yu W., X.C., S.C. and F.C. made a substantial contribution to discussion of the content of the manuscript and Yuzhuo W., D.L., S.Y.C.C. and F.C. reviewed and edited the manuscript before submission.
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Snippet Neuroendocrine prostate cancer (NEPC) is a lethal subtype of prostate cancer. NEPC arises de novo only rarely; the disease predominantly develops from...
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SubjectTerms 631/208/68/2486
631/67/589/466
Adenocarcinoma - drug therapy
Adenocarcinoma - genetics
Adenocarcinoma - metabolism
Adenocarcinoma - pathology
Androgen Antagonists - therapeutic use
Androgens
Antineoplastic Agents - therapeutic use
Care and treatment
Cell receptors
Cell Transdifferentiation
Development and progression
Disease Progression
Gene expression
Genetic aspects
Health aspects
Humans
Male
Medicine
Medicine & Public Health
Neuroendocrine Tumors - genetics
Neuroendocrine Tumors - metabolism
Neuroendocrine Tumors - pathology
Phenotype
Platinum Compounds - therapeutic use
Prostate cancer
Prostatic Neoplasms - drug therapy
Prostatic Neoplasms - genetics
Prostatic Neoplasms - metabolism
Prostatic Neoplasms - pathology
Prostatic Neoplasms, Castration-Resistant - drug therapy
Prostatic Neoplasms, Castration-Resistant - genetics
Prostatic Neoplasms, Castration-Resistant - metabolism
Prostatic Neoplasms, Castration-Resistant - pathology
Receptors, Androgen - metabolism
Review Article
Urology
Title Molecular events in neuroendocrine prostate cancer development
URI https://link.springer.com/article/10.1038/s41585-021-00490-0
https://www.ncbi.nlm.nih.gov/pubmed/34290447
https://www.proquest.com/docview/2577912750
https://www.proquest.com/docview/2554350125
https://pubmed.ncbi.nlm.nih.gov/PMC10802813
Volume 18
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