Comparative transcriptomics reveals a mixed basal, club, and hillock epithelial cell identity in castration-resistant prostate cancer

S Samuel P. Pitzen (Masonic Cancer Center, University of Minnesota) A Amber N. Rudenick (Masonic Cancer Center, University of Minnesota) Y Yinjie Qiu (Minnesota Supercomputing Institute, University of Minnesota) W Weijie Zhang S Sarah A. Munro (Minnesota Supercomputing Institute, University of Minnesota) B Braedan M. McCluskey (Minnesota Supercomputing Institute, University of Minnesota) C Colleen Forster (Department of Laboratory Medicine and Pathology, University of Minnesota Medical School) H Hannah E. Bergom (Division of Hematology, Oncology and Transplantation, University of Minnesota) A Atef Ali (Division of Hematology, Oncology and Transplantation, University of Minnesota) E Ella Boytim (Division of Hematology, Oncology and Transplantation, University of Minnesota) J John T. Lafin (Department of Urology, University of Texas Southwestern Medical Center) S Simon Linder (Division on Oncogenomics, Oncode Institute, The Netherlands Cancer Institute) M Mazlina Ismail (Department of Oncology, University College London Cancer Institute) W Wout Devlies (Department of Urology, University Hospitals Leuven) C Conner J. Sessions (Department of Urology, University of Washington) F Frank Claessens S Steven Joniau (Department of Urology, University Hospitals Leuven) G Gerhardt Attard W Wilbert Zwart P Peter S. Nelson (Division of Hematology and Oncology, University of Washington, Fred Hutchinson Cancer Center) E Eva Corey (Department of Urology, University of Washington) Y Yuzhuo Wang (Department of Urologic Sciences, Faculty of Medicine, Vancouver Prostate Centre, University of British Columbia) J Joshua M. Lang (Department of Medicine, University of Wisconsin-Madison) H Himisha Beltran D Douglas Strand (Department of Urology, University of Texas Southwestern Medical Center) E Emmanuel S. Antonarakis (Masonic Cancer Center, University of Minnesota) J Justin Hwang (Masonic Cancer Center, University of Minnesota) P Paari Murugan (Department of Laboratory Medicine and Pathology, University of Minnesota Medical School) R R. Stephanie Huang (Masonic Cancer Center, University of Minnesota) S Scott M. Dehm (Masonic Cancer Center, University of Minnesota)

Abstract

Inhibiting the androgen receptor (AR) is effective for treatment of advanced prostate cancers because of their AR-dependent luminal epithelial cell identity. Tumors progress during therapy to castration-resistant prostate cancer (CRPC) by restoring AR signaling and maintaining luminal identity or by converting through lineage plasticity to a neuroendocrine (NE) identity or double-negative CRPC (DNPC) lacking luminal or NE identities. Here, we show that DNPC cells express genes defining basal, club, and hillock epithelial cells from benign prostate. We identified KLF5 as a regulator of genes defining this mixed basal, club, and hillock cell identity in DNPC models. KLF5-mediated upregulation of RARG uncovered a DNPC sensitivity to growth inhibition by retinoic acid receptor agonists, which down-regulated KLF5 and up-regulated AR. These findings offer CRPC classifications based on prostate epithelial cell identities and nominate KLF5 and RARG as therapeutic targets for CRPC displaying a mixed basal, club, and hillock identity.

Article Details

Volume / Issue Vol. 122, Issue 6
Published February 11, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (30)

S

Samuel P. Pitzen

Masonic Cancer Center, University of Minnesota

A

Amber N. Rudenick

Masonic Cancer Center, University of Minnesota

Y

Yinjie Qiu

Minnesota Supercomputing Institute, University of Minnesota

W

Weijie Zhang

S

Sarah A. Munro

Minnesota Supercomputing Institute, University of Minnesota

B

Braedan M. McCluskey

Minnesota Supercomputing Institute, University of Minnesota

C

Colleen Forster

Department of Laboratory Medicine and Pathology, University of Minnesota Medical School

H

Hannah E. Bergom

Division of Hematology, Oncology and Transplantation, University of Minnesota

A

Atef Ali

Division of Hematology, Oncology and Transplantation, University of Minnesota

E

Ella Boytim

Division of Hematology, Oncology and Transplantation, University of Minnesota

J

John T. Lafin

Department of Urology, University of Texas Southwestern Medical Center

S

Simon Linder

Division on Oncogenomics, Oncode Institute, The Netherlands Cancer Institute

M

Mazlina Ismail

Department of Oncology, University College London Cancer Institute

W

Wout Devlies

Department of Urology, University Hospitals Leuven

C

Conner J. Sessions

Department of Urology, University of Washington

F

Frank Claessens

S

Steven Joniau

Department of Urology, University Hospitals Leuven

G

Gerhardt Attard

W

Wilbert Zwart

P

Peter S. Nelson

Division of Hematology and Oncology, University of Washington, Fred Hutchinson Cancer Center

E

Eva Corey

Department of Urology, University of Washington

Y

Yuzhuo Wang

Department of Urologic Sciences, Faculty of Medicine, Vancouver Prostate Centre, University of British Columbia

J

Joshua M. Lang

Department of Medicine, University of Wisconsin-Madison

H

Himisha Beltran

D

Douglas Strand

Department of Urology, University of Texas Southwestern Medical Center

E

Emmanuel S. Antonarakis

Masonic Cancer Center, University of Minnesota

J

Justin Hwang

Masonic Cancer Center, University of Minnesota

P

Paari Murugan

Department of Laboratory Medicine and Pathology, University of Minnesota Medical School

R

R. Stephanie Huang

Masonic Cancer Center, University of Minnesota

S

Scott M. Dehm

Masonic Cancer Center, University of Minnesota