Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancer

Abstract Triple‐negative breast cancer (TNBC) is notoriously difficult to treat due to the lack of targetable receptors and sometimes poor response to chemotherapy. The transforming growth factor beta (TGFβ) family of proteins and their receptors (TGFRs) are highly expressed in TNBC and implicated i...

Full description

Saved in:
Bibliographic Details
Main Authors: Natasha Vinod, Duhyeong Hwang, Sloane Christian Fussell, Tyler Cannon Owens, Olaoluwa Christopher Tofade, Thad S. Benefield, Sage Copling, Jacob D. Ramsey, Patrick D. Rädler, Hannah M. Atkins, Eric E. Livingston, J. Ashley Ezzell, Marina Sokolsky‐Papkov, Hong Yuan, Charles M. Perou, Alexander V. Kabanov
Format: Article
Language:English
Published: Wiley 2024-09-01
Series:Bioengineering & Translational Medicine
Online Access:https://doi.org/10.1002/btm2.10681
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846167964092465152
author Natasha Vinod
Duhyeong Hwang
Sloane Christian Fussell
Tyler Cannon Owens
Olaoluwa Christopher Tofade
Thad S. Benefield
Sage Copling
Jacob D. Ramsey
Patrick D. Rädler
Hannah M. Atkins
Eric E. Livingston
J. Ashley Ezzell
Marina Sokolsky‐Papkov
Hong Yuan
Charles M. Perou
Alexander V. Kabanov
author_facet Natasha Vinod
Duhyeong Hwang
Sloane Christian Fussell
Tyler Cannon Owens
Olaoluwa Christopher Tofade
Thad S. Benefield
Sage Copling
Jacob D. Ramsey
Patrick D. Rädler
Hannah M. Atkins
Eric E. Livingston
J. Ashley Ezzell
Marina Sokolsky‐Papkov
Hong Yuan
Charles M. Perou
Alexander V. Kabanov
author_sort Natasha Vinod
collection DOAJ
description Abstract Triple‐negative breast cancer (TNBC) is notoriously difficult to treat due to the lack of targetable receptors and sometimes poor response to chemotherapy. The transforming growth factor beta (TGFβ) family of proteins and their receptors (TGFRs) are highly expressed in TNBC and implicated in chemotherapy‐induced cancer stemness. Here, we evaluated combination treatments using experimental TGFR inhibitors (TGFβi), SB525334 (SB), and LY2109761 (LY) with paclitaxel (PTX) chemotherapy. These TGFβi target TGFR‐I (SB) or both TGFR‐I and TGFR‐II (LY). Due to the poor water solubility of these drugs, we incorporated each of them in poly(2‐oxazoline) (POx) high‐capacity polymeric micelles (SB‐POx and LY‐POx). We assessed their anticancer effect as single agents and in combination with micellar PTX (PTX‐POx) using multiple immunocompetent TNBC mouse models that mimic human subtypes (4T1, T11‐Apobec and T11‐UV). While either TGFβi or PTX showed a differential effect in each model as single agents, the combinations were consistently effective against all three models. Genetic profiling of the tumors revealed differences in the expression levels of genes associated with TGFβ, epithelial to mesenchymal transition (EMT), TLR‐4, and Bcl2 signaling, alluding to the susceptibility to specific gene signatures to the treatment. Taken together, our study suggests that TGFβi and PTX combination therapy using high‐capacity POx micelle delivery provides a robust antitumor response in multiple TNBC subtype mouse models.
format Article
id doaj-art-4d3e5270f8a24f30a1b80e2ded6ba463
institution Kabale University
issn 2380-6761
language English
publishDate 2024-09-01
publisher Wiley
record_format Article
series Bioengineering & Translational Medicine
spelling doaj-art-4d3e5270f8a24f30a1b80e2ded6ba4632024-11-14T12:22:22ZengWileyBioengineering & Translational Medicine2380-67612024-09-0195n/an/a10.1002/btm2.10681Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancerNatasha Vinod0Duhyeong Hwang1Sloane Christian Fussell2Tyler Cannon Owens3Olaoluwa Christopher Tofade4Thad S. Benefield5Sage Copling6Jacob D. Ramsey7Patrick D. Rädler8Hannah M. Atkins9Eric E. Livingston10J. Ashley Ezzell11Marina Sokolsky‐Papkov12Hong Yuan13Charles M. Perou14Alexander V. Kabanov15Division of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USADivision of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USADepartment of Biology, Department of Chemistry University of North Carolina at Chapel Hill Chapel Hill North Carolina USADivision of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USADivision of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USADepartment of Radiology University of North Carolina at Chapel Hill Chapel Hill North Carolina USADivision of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USADivision of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USALineberger Comprehensive Cancer Center University of North Carolina Chapel Hill North Carolina USALineberger Comprehensive Cancer Center University of North Carolina Chapel Hill North Carolina USADepartment of Radiology, Biomedical Research Imaging Center, UNC Lineberger Comprehensive Cancer Center University of North Carolina at Chapel Hill Chapel Hill North Carolina USAHistology Research Core University of North Carolina Chapel Hill North Carolina USADivision of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USADepartment of Radiology, Biomedical Research Imaging Center, UNC Lineberger Comprehensive Cancer Center University of North Carolina at Chapel Hill Chapel Hill North Carolina USALineberger Comprehensive Cancer Center University of North Carolina Chapel Hill North Carolina USADivision of Pharmacoengineering and Molecular Pharmaceutics, Center for Nanotechnology in Drug Delivery, Eshelman School of Pharmacy University of North Carolina at Chapel Hill Chapel Hill North Carolina USAAbstract Triple‐negative breast cancer (TNBC) is notoriously difficult to treat due to the lack of targetable receptors and sometimes poor response to chemotherapy. The transforming growth factor beta (TGFβ) family of proteins and their receptors (TGFRs) are highly expressed in TNBC and implicated in chemotherapy‐induced cancer stemness. Here, we evaluated combination treatments using experimental TGFR inhibitors (TGFβi), SB525334 (SB), and LY2109761 (LY) with paclitaxel (PTX) chemotherapy. These TGFβi target TGFR‐I (SB) or both TGFR‐I and TGFR‐II (LY). Due to the poor water solubility of these drugs, we incorporated each of them in poly(2‐oxazoline) (POx) high‐capacity polymeric micelles (SB‐POx and LY‐POx). We assessed their anticancer effect as single agents and in combination with micellar PTX (PTX‐POx) using multiple immunocompetent TNBC mouse models that mimic human subtypes (4T1, T11‐Apobec and T11‐UV). While either TGFβi or PTX showed a differential effect in each model as single agents, the combinations were consistently effective against all three models. Genetic profiling of the tumors revealed differences in the expression levels of genes associated with TGFβ, epithelial to mesenchymal transition (EMT), TLR‐4, and Bcl2 signaling, alluding to the susceptibility to specific gene signatures to the treatment. Taken together, our study suggests that TGFβi and PTX combination therapy using high‐capacity POx micelle delivery provides a robust antitumor response in multiple TNBC subtype mouse models.https://doi.org/10.1002/btm2.10681
spellingShingle Natasha Vinod
Duhyeong Hwang
Sloane Christian Fussell
Tyler Cannon Owens
Olaoluwa Christopher Tofade
Thad S. Benefield
Sage Copling
Jacob D. Ramsey
Patrick D. Rädler
Hannah M. Atkins
Eric E. Livingston
J. Ashley Ezzell
Marina Sokolsky‐Papkov
Hong Yuan
Charles M. Perou
Alexander V. Kabanov
Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancer
Bioengineering & Translational Medicine
title Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancer
title_full Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancer
title_fullStr Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancer
title_full_unstemmed Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancer
title_short Combination of polymeric micelle formulation of TGFβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of Triple‐negative breast cancer
title_sort combination of polymeric micelle formulation of tgfβ receptor inhibitors and paclitaxel produces consistent response across different mouse models of triple negative breast cancer
url https://doi.org/10.1002/btm2.10681
work_keys_str_mv AT natashavinod combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT duhyeonghwang combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT sloanechristianfussell combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT tylercannonowens combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT olaoluwachristophertofade combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT thadsbenefield combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT sagecopling combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT jacobdramsey combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT patrickdradler combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT hannahmatkins combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT ericelivingston combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT jashleyezzell combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT marinasokolskypapkov combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT hongyuan combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT charlesmperou combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer
AT alexandervkabanov combinationofpolymericmicelleformulationoftgfbreceptorinhibitorsandpaclitaxelproducesconsistentresponseacrossdifferentmousemodelsoftriplenegativebreastcancer