Clinically relevant humanized mouse models of metastatic prostate cancer to evaluate cancer therapies.


Journal

bioRxiv : the preprint server for biology
Titre abrégé: bioRxiv
Pays: United States
ID NLM: 101680187

Informations de publication

Date de publication:
17 Oct 2023
Historique:
pubmed: 31 10 2023
medline: 31 10 2023
entrez: 31 10 2023
Statut: epublish

Résumé

There is tremendous need for improved prostate cancer (PCa) models. The mouse prostate does not spontaneously form tumors and is anatomically and developmentally different from the human prostate. Engineered mouse models lack the heterogeneity of human cancer and rarely establish metastatic growth. Human xenografts represent an alternative but rely on an immunocompromised host. Accordingly, we generated PCa murine xenograft models with an intact human immune system (huNOG and huNOG-EXL mice) to test whether humanizing tumor-immune interactions would improve modeling of metastatic PCa and the impact of hormonal and immunotherapies. These mice maintain multiple human cell lineages, including functional human T-cells and myeloid cells. In 22Rv1 xenografts, subcutaneous tumor size was not significantly altered across conditions; however, metastasis to secondary sites differed in castrate huNOG vs background-matched immunocompromised mice treated with enzalutamide (enza). VCaP xenograft tumors showed decreases in growth with enza and anti-Programed-Death-1 treatments in huNOG mice, and no effect was seen with treatment in NOG mice. Enza responses in huNOG and NOG mice were distinct and associated with increased T-cells within tumors of enza treated huNOG mice, and increased T-cell activation. In huNOG-EXL mice, which support human myeloid development, there was a strong population of immunosuppressive regulatory T-cells and Myeloid-Derived-Suppressor-Cells (MDSCs), and enza treatment showed no difference in metastasis. Results illustrate, to our knowledge, the first model of human PCa that metastasizes to clinically relevant locations, has an intact human immune system, responds appropriately to standard-of-care hormonal therapies, and can model both an immunosuppressive and checkpoint-inhibition responsive immune microenvironment.

Identifiants

pubmed: 37904960
doi: 10.1101/2023.10.13.562280
pmc: PMC10614761
pii:
doi:

Types de publication

Preprint

Langues

eng

Références

Commun Integr Biol. 2010 Nov;3(6):508-12
pubmed: 21331226
Oncotarget. 2016 May 3;7(18):26259-74
pubmed: 27036029
Cold Spring Harb Perspect Med. 2018 May 1;8(5):
pubmed: 29038334
Neoplasia. 2020 Feb;22(2):111-119
pubmed: 31931431
Sci Rep. 2019 Feb 12;9(1):1853
pubmed: 30755715
Front Oncol. 2022 Jul 04;12:862416
pubmed: 35860573
JCO Precis Oncol. 2020;4:382-392
pubmed: 32671317
Cancer Immunol Res. 2020 Sep;8(9):1215-1227
pubmed: 32661092
Oncogene. 2012 Nov 8;31(45):4759-67
pubmed: 22266865
Cancer Metastasis Rev. 2014 Sep;33(2-3):377-97
pubmed: 24452759
Prostate Cancer Prostatic Dis. 2021 Sep;24(3):697-717
pubmed: 33820953
Clin Immunol. 2020 Sep;218:108515
pubmed: 32619646
Br J Cancer. 2023 Feb;128(3):451-458
pubmed: 36564565
N Engl J Med. 2018 Oct 04;379(14):1381
pubmed: 30281993
N Engl J Med. 2018 Jun 28;378(26):2465-2474
pubmed: 29949494
Prostate. 2013 Sep;73(12):1316-25
pubmed: 23775398
Urology. 1995 Nov;46(5):681-6; discussion 686-7
pubmed: 7495121
Eur J Immunol. 2017 Jun;47(6):946-953
pubmed: 28475283
J Immunother Cancer. 2023 May;11(5):
pubmed: 37147019
Blood. 2002 Nov 1;100(9):3175-82
pubmed: 12384415
Front Immunol. 2022 Oct 28;13:1018962
pubmed: 36389779
Ann Oncol. 2016 Jul;27(7):1190-8
pubmed: 26912558
Cancer Res. 2006 Sep 1;66(17):8598-607
pubmed: 16951173
Front Immunol. 2021 Oct 12;12:740890
pubmed: 34712230
Cancer Res. 2009 May 15;69(10):4434-42
pubmed: 19366804
Curr Protoc Immunol. 2008 May;Chapter 15:15.21.1-15.21.21
pubmed: 18491294
Oncoimmunology. 2012 Mar 1;1(2):152-161
pubmed: 22720236
Nat Med. 2021 Jan;27(1):152-164
pubmed: 33398162
J Biol Chem. 2005 Oct 28;280(43):36442-51
pubmed: 16055444
Commun Biol. 2022 Sep 1;5(1):897
pubmed: 36050516
Cancer Res. 2013 May 1;73(9):2718-36
pubmed: 23610450
Nature. 2014 Jun 12;510(7504):278-82
pubmed: 24759320
Onco Targets Ther. 2019 Oct 15;12:8437-8445
pubmed: 31686860
Nat Commun. 2023 Feb 7;14(1):663
pubmed: 36750562
Prostate. 2020 Apr;80(5):407-411
pubmed: 31972048
Nat Med. 2021 Mar;27(3):426-433
pubmed: 33664492
Br J Cancer. 2009 Mar 10;100(5):671-5
pubmed: 19223900
Nucleic Acids Res. 2020 May 21;48(9):4741-4755
pubmed: 32198885
PLoS One. 2013;8(1):e53701
pubmed: 23326489
Cancer Cell. 2017 Oct 9;32(4):474-489.e6
pubmed: 29017058
Nature. 2022 Jun;606(7915):791-796
pubmed: 35322234
Cell Immunol. 2015 Apr;294(2):87-94
pubmed: 25708485

Auteurs

Raymond J Kostlan (RJ)

Department of Cancer Biology, Loyola University Chicago, Maywood, IL 60153.
Integrated Program in Biomedical Science, Biochemistry, Molecular and Cancer Biology, Loyola University Chicago, Maywood, IL, USA.

John T Phoenix (JT)

Department of Cancer Biology, Loyola University Chicago, Maywood, IL 60153.
Integrated Program in Biomedical Science, Biochemistry, Molecular and Cancer Biology, Loyola University Chicago, Maywood, IL, USA.

Audris Budreika (A)

Department of Cancer Biology, Loyola University Chicago, Maywood, IL 60153.
Integrated Program in Biomedical Science, Biochemistry, Molecular and Cancer Biology, Loyola University Chicago, Maywood, IL, USA.

Marina G Ferrari (MG)

Department of Cancer Biology, Loyola University Chicago, Maywood, IL 60153.

Neetika Khurana (N)

Department of Cancer Biology, Loyola University Chicago, Maywood, IL 60153.

Jae Eun Cho (JE)

Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, MI, USA.
Department of Pathology, University of Michigan, Ann Arbor, MI, USA.
Rogel Cancer Center, University of Michigan, Ann Arbor, MI, USA.

Kristin Juckette (K)

Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, MI, USA.
Department of Pathology, University of Michigan, Ann Arbor, MI, USA.
Rogel Cancer Center, University of Michigan, Ann Arbor, MI, USA.

Brooke L McCollum (BL)

Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, MI, USA.
Department of Pathology, University of Michigan, Ann Arbor, MI, USA.
Rogel Cancer Center, University of Michigan, Ann Arbor, MI, USA.

Russell Moskal (R)

Department of Cancer Biology, Loyola University Chicago, Maywood, IL 60153.

Rahul Mannan (R)

Integrated Program in Biomedical Science, Biochemistry, Molecular and Cancer Biology, Loyola University Chicago, Maywood, IL, USA.
Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, MI, USA.
Department of Pathology, University of Michigan, Ann Arbor, MI, USA.

Yuanyuan Qiao (Y)

Integrated Program in Biomedical Science, Biochemistry, Molecular and Cancer Biology, Loyola University Chicago, Maywood, IL, USA.
Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, MI, USA.
Department of Pathology, University of Michigan, Ann Arbor, MI, USA.

Donald J Vander Griend (DJV)

Department of Pathology, University of Illinois at Chicago, Chicago, IL, USA.

Arul M Chinnaiyan (AM)

Integrated Program in Biomedical Science, Biochemistry, Molecular and Cancer Biology, Loyola University Chicago, Maywood, IL, USA.
Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, MI, USA.
Department of Pathology, University of Michigan, Ann Arbor, MI, USA.

Steven Kregel (S)

Department of Cancer Biology, Loyola University Chicago, Maywood, IL 60153.

Classifications MeSH