Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma

Pancreatic ductal adenocarcinoma (PDAC) is a lethal disease where standard-of-care chemotherapeutic drugs have limited efficacy due to the development of drug resistance and poor drug delivery caused by a highly desmoplastic tumor microenvironment. Combining multiple drugs in a tumor-targeting carri...

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Main Authors: Naga Malleswara Rao Nakka, Hari Krishnareddy Rachamala, Ramcharan Singh Angom, Nagamalleswara Rao Indla, Shamit Kumar Dutta, Enfeng Wang, Santanu Bhattacharya, Annadanam V. Sesha Sainath, Hani Babiker, Krishnendu Pal, Debabrata Mukhopadhyay
Format: Article
Language:English
Published: Elsevier 2024-10-01
Series:Materials Today Bio
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Online Access:http://www.sciencedirect.com/science/article/pii/S2590006424002606
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author Naga Malleswara Rao Nakka
Hari Krishnareddy Rachamala
Ramcharan Singh Angom
Nagamalleswara Rao Indla
Shamit Kumar Dutta
Enfeng Wang
Santanu Bhattacharya
Annadanam V. Sesha Sainath
Hani Babiker
Krishnendu Pal
Debabrata Mukhopadhyay
author_facet Naga Malleswara Rao Nakka
Hari Krishnareddy Rachamala
Ramcharan Singh Angom
Nagamalleswara Rao Indla
Shamit Kumar Dutta
Enfeng Wang
Santanu Bhattacharya
Annadanam V. Sesha Sainath
Hani Babiker
Krishnendu Pal
Debabrata Mukhopadhyay
author_sort Naga Malleswara Rao Nakka
collection DOAJ
description Pancreatic ductal adenocarcinoma (PDAC) is a lethal disease where standard-of-care chemotherapeutic drugs have limited efficacy due to the development of drug resistance and poor drug delivery caused by a highly desmoplastic tumor microenvironment. Combining multiple drugs in a tumor-targeting carrier would be a favorable approach to overcome these limitations. Hence, a tumor-targeted peptide (TTP) conjugated amphiphilic tri-block copolymer was developed to make targeted polymer nanoparticles (TTP-PNPs) serving as a vehicle for carrying gemcitabine (Gem), paclitaxel (PTX), and their combination (Gem + PTX). The TTP-PNPs in the form of empty polymer (P), single drug-loaded [P(Gem) and P(PTX)], and dual drug-loaded [P(Gem + PTX)] polymer nanoformulations exhibited stable and homogenous spherical shapes with 110–160 nm size. These nanoformulations demonstrated excellent stability under in vitro physiological conditions and led to an efficient release of the drugs in the presence of reduced glutathione (GSH). The efficacy of these nanoparticles was thoroughly evaluated in vitro and in vivo, demonstrating a notable capacity to selectively target and restrict PDAC cells (PANC-1 and KPC) growth. The cellular uptake and biodistribution study showed a significantly higher tumor-targeting ability of TTP-PNPs than PNPs without TTP. Notably, P(Gem + PTX) exhibited the lowest IC50 compared to all other controls and showed heightened synergistic effects in both cell lines. Furthermore, P(Gem + PTX) showed a significantly better tumor reduction and median overall survival in mouse models than single drug-loaded TTP-PNPs or a combination of free drugs (Gem + PTX). In summary, our TTP-PNP system shows great promise as a novel platform for delivering Gem + PTX specifically to pancreatic cancer (PC), maximizing the therapeutic benefits with lower concentrations of the drugs and potentially reducing toxic side effects.
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spelling doaj-art-af4e9d5dd2c4413bb0f9e1232ea4f2ba2025-08-20T01:54:45ZengElsevierMaterials Today Bio2590-00642024-10-012810119910.1016/j.mtbio.2024.101199Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinomaNaga Malleswara Rao Nakka0Hari Krishnareddy Rachamala1Ramcharan Singh Angom2Nagamalleswara Rao Indla3Shamit Kumar Dutta4Enfeng Wang5Santanu Bhattacharya6Annadanam V. Sesha Sainath7Hani Babiker8Krishnendu Pal9Debabrata Mukhopadhyay10Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USADepartment of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USADepartment of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USAPolymers and Functional Materials and Fluoro-Agrochemicals Department, CSIR-Indian Institute of Chemical Technology, Uppal Road, Hyderabad, 500007, India; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, 201002, IndiaDepartment of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USADepartment of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USADepartment of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USA; Department of Physiology and Biomedical Engineering, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USAPolymers and Functional Materials and Fluoro-Agrochemicals Department, CSIR-Indian Institute of Chemical Technology, Uppal Road, Hyderabad, 500007, India; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, 201002, IndiaDepartment of Medicine, Division of Hematology-Oncology, Mayo Clinic Florida, Jacksonville, FL, 32224, USADepartment of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USADepartment of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USA; Department of Physiology and Biomedical Engineering, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USA; Corresponding author. Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine and Sciences, Jacksonville, FL, 32224, USA.Pancreatic ductal adenocarcinoma (PDAC) is a lethal disease where standard-of-care chemotherapeutic drugs have limited efficacy due to the development of drug resistance and poor drug delivery caused by a highly desmoplastic tumor microenvironment. Combining multiple drugs in a tumor-targeting carrier would be a favorable approach to overcome these limitations. Hence, a tumor-targeted peptide (TTP) conjugated amphiphilic tri-block copolymer was developed to make targeted polymer nanoparticles (TTP-PNPs) serving as a vehicle for carrying gemcitabine (Gem), paclitaxel (PTX), and their combination (Gem + PTX). The TTP-PNPs in the form of empty polymer (P), single drug-loaded [P(Gem) and P(PTX)], and dual drug-loaded [P(Gem + PTX)] polymer nanoformulations exhibited stable and homogenous spherical shapes with 110–160 nm size. These nanoformulations demonstrated excellent stability under in vitro physiological conditions and led to an efficient release of the drugs in the presence of reduced glutathione (GSH). The efficacy of these nanoparticles was thoroughly evaluated in vitro and in vivo, demonstrating a notable capacity to selectively target and restrict PDAC cells (PANC-1 and KPC) growth. The cellular uptake and biodistribution study showed a significantly higher tumor-targeting ability of TTP-PNPs than PNPs without TTP. Notably, P(Gem + PTX) exhibited the lowest IC50 compared to all other controls and showed heightened synergistic effects in both cell lines. Furthermore, P(Gem + PTX) showed a significantly better tumor reduction and median overall survival in mouse models than single drug-loaded TTP-PNPs or a combination of free drugs (Gem + PTX). In summary, our TTP-PNP system shows great promise as a novel platform for delivering Gem + PTX specifically to pancreatic cancer (PC), maximizing the therapeutic benefits with lower concentrations of the drugs and potentially reducing toxic side effects.http://www.sciencedirect.com/science/article/pii/S2590006424002606Pancreatic ductal adenocarcinomaTumor-targeted therapyAmphiphilic tri-block copolymerGemcitabinePaclitaxelPolymer nanoparticles
spellingShingle Naga Malleswara Rao Nakka
Hari Krishnareddy Rachamala
Ramcharan Singh Angom
Nagamalleswara Rao Indla
Shamit Kumar Dutta
Enfeng Wang
Santanu Bhattacharya
Annadanam V. Sesha Sainath
Hani Babiker
Krishnendu Pal
Debabrata Mukhopadhyay
Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma
Materials Today Bio
Pancreatic ductal adenocarcinoma
Tumor-targeted therapy
Amphiphilic tri-block copolymer
Gemcitabine
Paclitaxel
Polymer nanoparticles
title Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma
title_full Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma
title_fullStr Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma
title_full_unstemmed Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma
title_short Dual drug-loaded tumor-targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma
title_sort dual drug loaded tumor targeted polymeric nanoparticles for enhancing therapeutic response in pancreatic ductal adenocarcinoma
topic Pancreatic ductal adenocarcinoma
Tumor-targeted therapy
Amphiphilic tri-block copolymer
Gemcitabine
Paclitaxel
Polymer nanoparticles
url http://www.sciencedirect.com/science/article/pii/S2590006424002606
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