3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors

There is a growing recognition that current preclinical models do not reflect the tumor microenvironment in cellular, biological, and biophysical content and this may have a profound effect on drug efficacy testing, especially in the era of molecular-targeted agents. Here, we describe a method to di...

Full description

Bibliographic Details
Main Authors: Onion, David, Argent, Richard H., Reece-Smith, Alex M., Craze, Madeleine L., Pineda, Robert G., Clarke, Philip A., Ratan, Hari L., Parsons, Simon L., Lobo, Dileep N., Duffy, John P., Atherton, John C., McKenzie, Andrew J., Kumari, Rajendra, King, Peter, Hall, Brett M., Grabowska, Anna M.
Format: Article
Published: American Association for Cancer Research 2016
Online Access:https://eprints.nottingham.ac.uk/40487/
_version_ 1848796070050529280
author Onion, David
Argent, Richard H.
Reece-Smith, Alex M.
Craze, Madeleine L.
Pineda, Robert G.
Clarke, Philip A.
Ratan, Hari L.
Parsons, Simon L.
Lobo, Dileep N.
Duffy, John P.
Atherton, John C.
McKenzie, Andrew J.
Kumari, Rajendra
King, Peter
Hall, Brett M.
Grabowska, Anna M.
author_facet Onion, David
Argent, Richard H.
Reece-Smith, Alex M.
Craze, Madeleine L.
Pineda, Robert G.
Clarke, Philip A.
Ratan, Hari L.
Parsons, Simon L.
Lobo, Dileep N.
Duffy, John P.
Atherton, John C.
McKenzie, Andrew J.
Kumari, Rajendra
King, Peter
Hall, Brett M.
Grabowska, Anna M.
author_sort Onion, David
building Nottingham Research Data Repository
collection Online Access
description There is a growing recognition that current preclinical models do not reflect the tumor microenvironment in cellular, biological, and biophysical content and this may have a profound effect on drug efficacy testing, especially in the era of molecular-targeted agents. Here, we describe a method to directly embed low-passage patient tumor–derived tissue into basement membrane extract, ensuring a low proportion of cell death to anoikis and growth complementation by coculture with patient-derived cancer-associated fibroblasts (CAF). A range of solid tumors proved amenable to growth and pharmacologic testing in this 3D assay. A study of 30 early-stage non–small cell lung cancer (NSCLC) specimens revealed high levels of de novo resistance to a large range of standard-of-care agents, while histone deacetylase (HDAC) inhibitors and their combination with antineoplastic drugs displayed high levels of efficacy. Increased resistance was seen in the presence of patient-derived CAFs for many agents, highlighting the utility of the assay for tumor microenvironment-educated drug testing. Standard-of-care agents showed similar responses in the 3D ex vivo and patient-matched in vivo models validating the 3D-Tumor Growth Assay (3D-TGA) as a high-throughput screen for close-to-patient tumors using significantly reduced animal numbers. Mol Cancer Ther; 15(4); 753–63. ©2016 AACR.
first_indexed 2025-11-14T19:42:08Z
format Article
id nottingham-40487
institution University of Nottingham Malaysia Campus
institution_category Local University
last_indexed 2025-11-14T19:42:08Z
publishDate 2016
publisher American Association for Cancer Research
recordtype eprints
repository_type Digital Repository
spelling nottingham-404872020-05-04T17:39:01Z https://eprints.nottingham.ac.uk/40487/ 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors Onion, David Argent, Richard H. Reece-Smith, Alex M. Craze, Madeleine L. Pineda, Robert G. Clarke, Philip A. Ratan, Hari L. Parsons, Simon L. Lobo, Dileep N. Duffy, John P. Atherton, John C. McKenzie, Andrew J. Kumari, Rajendra King, Peter Hall, Brett M. Grabowska, Anna M. There is a growing recognition that current preclinical models do not reflect the tumor microenvironment in cellular, biological, and biophysical content and this may have a profound effect on drug efficacy testing, especially in the era of molecular-targeted agents. Here, we describe a method to directly embed low-passage patient tumor–derived tissue into basement membrane extract, ensuring a low proportion of cell death to anoikis and growth complementation by coculture with patient-derived cancer-associated fibroblasts (CAF). A range of solid tumors proved amenable to growth and pharmacologic testing in this 3D assay. A study of 30 early-stage non–small cell lung cancer (NSCLC) specimens revealed high levels of de novo resistance to a large range of standard-of-care agents, while histone deacetylase (HDAC) inhibitors and their combination with antineoplastic drugs displayed high levels of efficacy. Increased resistance was seen in the presence of patient-derived CAFs for many agents, highlighting the utility of the assay for tumor microenvironment-educated drug testing. Standard-of-care agents showed similar responses in the 3D ex vivo and patient-matched in vivo models validating the 3D-Tumor Growth Assay (3D-TGA) as a high-throughput screen for close-to-patient tumors using significantly reduced animal numbers. Mol Cancer Ther; 15(4); 753–63. ©2016 AACR. American Association for Cancer Research 2016-04-01 Article PeerReviewed Onion, David, Argent, Richard H., Reece-Smith, Alex M., Craze, Madeleine L., Pineda, Robert G., Clarke, Philip A., Ratan, Hari L., Parsons, Simon L., Lobo, Dileep N., Duffy, John P., Atherton, John C., McKenzie, Andrew J., Kumari, Rajendra, King, Peter, Hall, Brett M. and Grabowska, Anna M. (2016) 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors. Molecular Cancer Therapeutics, 15 (4). pp. 753-763. ISSN 1538-8514 http://dx.doi.org/10.1158/1535-7163.MCT-15-0598 doi:10.1158/1535-7163.MCT-15-0598 doi:10.1158/1535-7163.MCT-15-0598
spellingShingle Onion, David
Argent, Richard H.
Reece-Smith, Alex M.
Craze, Madeleine L.
Pineda, Robert G.
Clarke, Philip A.
Ratan, Hari L.
Parsons, Simon L.
Lobo, Dileep N.
Duffy, John P.
Atherton, John C.
McKenzie, Andrew J.
Kumari, Rajendra
King, Peter
Hall, Brett M.
Grabowska, Anna M.
3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors
title 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors
title_full 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors
title_fullStr 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors
title_full_unstemmed 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors
title_short 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors
title_sort 3-dimensional patient-derived lung cancer assays reveal resistance to standards-of-care promoted by stromal cells but sensitivity to histone deacetylase inhibitors
url https://eprints.nottingham.ac.uk/40487/
https://eprints.nottingham.ac.uk/40487/
https://eprints.nottingham.ac.uk/40487/