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Dual pH/redox-responsive hyperbranched polymeric nanocarriers with TME-trigger size shrinkage and charge reversible ability for amplified chemotherapy of breast cancer

Badparvar, Fahimeh, Marjani, Ahmad Poursattar, Salehi, Roya, Ramezani, Fatemeh·2024·Scientific Reports
DOI 10.1038/s41598-024-57296-4PMC PMC11349913
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Abstract

A novel pH/redox-responsive hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) nanoparticles (NPs) were designed with size shrinkage and charge-reversible potential for targeted delivery of docetaxel (DTX) to MDA-MB-231 cell lines. In the tumor microenvironment (TME), amine protonation induces charge reversal and disulfide bond cleavage under high TME GSH concentration causing size shrinkage, improved deep tumor penetration, and active targeting of the therapeutic agents. These nano drug delivery systems (NDDSs) significantly promoted cancer cell uptake (~ 100% at 0.5 h), facilitating site-specific delivery and deep tumor penetration. The MTT assay revealed significantly higher cytotoxicity ( P value < 0.0001) for DTX-loaded NPs compared to free DTX. Cell cycle analysis revealed G2/M (58.3 ± 2.1%) and S (21.5 ± 1.3%) arrest for DTX-loaded NPs, while free DTX caused G2/M (67.9 ± 1.1%) and sub-G1 (10.3 ± 0.8%) arrest. DTX-loaded NPs induced higher apoptosis ( P value < 0.001) in MDA-MB-231 cells (71.5 ± 2.8%) compared to free DTX (42.3 ± 3.1%). Western blotting and RT-PCR assays confirmed significant up-regulation of protein levels and apoptotic genes by DTX-loaded NPs compared to free DTX. In conclusion, TME-responsive charge reversal and size-shrinkable smart NDDSs designed based on low pH, and high glutathione (GSH), offer more effective site-specific delivery of therapeutic agents to tumors.

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Figure 1 Graphical representation showing the size and charges reversible smart pH/redox dual-stimuli hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) nano-vehicle for promoted breast cancer tumor targeting and dual pH/redox triggered DTX release. Created with BioRender.com.
Figure 1 Graphical representation showing the size and charges reversible smart pH/redox dual-stimuli hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) nano-vehicle for promoted breast cancer tumor targeting and dual pH/redox triggered DTX release. Created with BioRender.com.CC BY · PubMed Central
Figure 2 Synthesis route of acrylate-terminated poly(β-amino ester)s through the Michael-type addition from 3 synthetic steps from Bis(2-hydroxyethyl)disulfide (product of step 1) and 2,2′-dithiodiethanol diacrylate (DSDA) (product of step 2).
Figure 2 Synthesis route of acrylate-terminated poly(β-amino ester)s through the Michael-type addition from 3 synthetic steps from Bis(2-hydroxyethyl)disulfide (product of step 1) and 2,2′-dithiodiethanol diacrylate (DSDA) (product of step 2).CC BY · PubMed Central
Figure 3 Synthesis route of bromine-terminal MeO-PEG from MeO-PEG and alpha-bromoisobutyryl bromide (α-BriBr) as an ATRP macroinitiator (MeO-PEG-Br).
Figure 3 Synthesis route of bromine-terminal MeO-PEG from MeO-PEG and alpha-bromoisobutyryl bromide (α-BriBr) as an ATRP macroinitiator (MeO-PEG-Br).CC BY · PubMed Central
Figure 4 Synthesis route of hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) copolymer through ATRP approach.
Figure 4 Synthesis route of hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) copolymer through ATRP approach.CC BY · PubMed Central
Figure 5 The 1H-NMR spectra of MeO-PEG-β-(NIPAAm-co-PBAE) copolymer.
Figure 5 The 1H-NMR spectra of MeO-PEG-β-(NIPAAm-co-PBAE) copolymer.CC BY · PubMed Central
Figure 6 The SEM images (A) and EDS analysis of hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) copolymeric blank NPs (B).
Figure 6 The SEM images (A) and EDS analysis of hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) copolymeric blank NPs (B).CC BY · PubMed Central
Figure 7 The hydrodynamic size of blank (A), and Drug-loaded (B) MeO-PEG-b-( NIPAAm-co-PBAE) NPs; The hydrodynamic size of Blank NPs after 1 mount incubation in distilled water (C) and PBS buffer (pH = 7.4) (D).
Figure 7 The hydrodynamic size of blank (A), and Drug-loaded (B) MeO-PEG-b-( NIPAAm-co-PBAE) NPs; The hydrodynamic size of Blank NPs after 1 mount incubation in distilled water (C) and PBS buffer (pH = 7.4) (D).CC BY · PubMed Central
Figure 8 In vitro, dual pH/redox triggered DTX release from MeO-PEG-b-(NIPAAm-co-PBAE) NPs at pH = 6.4 with 10 mM GSH (green), pH = 6.4, without GSH (red), pH = 7.4 with 10 µM GSH (black), pH = 7.4 without GSH (orange) (A). pH/redox-responsive size alteration assessment at PBS buffer with a pH of 7.4 without GSH and PBS buffer with 10 Mm GSH and pH of 6.4 at different time intervals (0.5, 3, and 24 h) (B).
Figure 8 In vitro, dual pH/redox triggered DTX release from MeO-PEG-b-(NIPAAm-co-PBAE) NPs at pH = 6.4 with 10 mM GSH (green), pH = 6.4, without GSH (red), pH = 7.4 with 10 µM GSH (black), pH = 7.4 without GSH (orange) (A). pH/redox-responsive size alteration assessment at PBS buffer with a pH of 7.4 without GSH and PBS buffer with 10 Mm GSH and pH of 6.4 at different time intervals (0.5, 3, and 24 h) (B).CC BY · PubMed Central
Figure 9 Flow cytometry diagrams for intracellular uptake indicating quantitatively examine fluorescence intensity at pH = 6.4 (A), and pH = 7.4 (B); And comparison graphs of mean fluorescence intensity (%) of intracellular uptake at pH 7.4 and 6.4 (Pvalue ˂0.0001) (C) of MDA-MB-231 cells after treatment with RhB-labeled DTX-loaded MeO-PEG-b-(NIPAAm-co-PBAE) NPs and, RhB-labeled copolymeric Blank NPs in various time intervals: 0.5, and 3 h.
Figure 9 Flow cytometry diagrams for intracellular uptake indicating quantitatively examine fluorescence intensity at pH = 6.4 (A), and pH = 7.4 (B); And comparison graphs of mean fluorescence intensity (%) of intracellular uptake at pH 7.4 and 6.4 (Pvalue ˂0.0001) (C) of MDA-MB-231 cells after treatment with RhB-labeled DTX-loaded MeO-PEG-b-(NIPAAm-co-PBAE) NPs and, RhB-labeled copolymeric Blank NPs in various time intervals: 0.5, and 3 h.CC BY · PubMed Central
Figure 10 Qualitative image by Cytation 5 cell imaging of MDA-MB-231 cells after treatment with RhB-labeled DTX-loaded MeO-PEG-b-(NIPAAm-co-PBAE) NPs and, RhB-labeled copolymeric NPs in various time intervals: 0.5, and 3 h at TME.
Figure 10 Qualitative image by Cytation 5 cell imaging of MDA-MB-231 cells after treatment with RhB-labeled DTX-loaded MeO-PEG-b-(NIPAAm-co-PBAE) NPs and, RhB-labeled copolymeric NPs in various time intervals: 0.5, and 3 h at TME.CC BY · PubMed Central
Figure 11 The viability of MDA-MB-231 cells incubated with different concentrations of free DTX and DTX-loaded NPs for 48 h was determined by the MTT method. Data are presented as the average ± SD (n = 6) (Pvalue < 0.0001).
Figure 11 The viability of MDA-MB-231 cells incubated with different concentrations of free DTX and DTX-loaded NPs for 48 h was determined by the MTT method. Data are presented as the average ± SD (n = 6) (Pvalue < 0.0001).CC BY · PubMed Central
Figure 12 Cellular interaction for cell cycle analysis of all formulation (DTX-loaded NPs, free DTX, blank NPs, and control cells) with MDA-MB-231 cells, by flow cytometry technique: Histograms of cell cycle distribution (A) and quantitative diagram of the related flow-cytometry diagram's cell population (%) profile in cell cycle phases (Sub G1, G2/M, S, and G0/G1) (B).
Figure 12 Cellular interaction for cell cycle analysis of all formulation (DTX-loaded NPs, free DTX, blank NPs, and control cells) with MDA-MB-231 cells, by flow cytometry technique: Histograms of cell cycle distribution (A) and quantitative diagram of the related flow-cytometry diagram's cell population (%) profile in cell cycle phases (Sub G1, G2/M, S, and G0/G1) (B).CC BY · PubMed Central
Figure 13 Cytogram of cellular apoptosis against MDA-MB-231 cells induced by free DTX and DTX-loaded NPs in their IC50 dose in comparison to the blank hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) copolymeric NPs as positive control and non-treated cells as a negative control. The flow cytometric diagram divided cells into four sections (viable, early apoptotic, late apoptotic, and necrotic) and the percent of counted cells in each area is illustrated on the quadrant charts (Pvalue < 0.001) (A). Quantitative results of apoptotic effects evaluated by Annexin V/FITC assay (B).
Figure 13 Cytogram of cellular apoptosis against MDA-MB-231 cells induced by free DTX and DTX-loaded NPs in their IC50 dose in comparison to the blank hyperbranched MeO-PEG-b-(NIPAAm-co-PBAE) copolymeric NPs as positive control and non-treated cells as a negative control. The flow cytometric diagram divided cells into four sections (viable, early apoptotic, late apoptotic, and necrotic) and the percent of counted cells in each area is illustrated on the quadrant charts (Pvalue < 0.001) (A). Quantitative results of apoptotic effects evaluated by Annexin V/FITC assay (B).CC BY · PubMed Central
Figure 14 Results of apoptotic effect of free DTX and DTX-loaded NPs treated MDA-MB-231 cells assessed by real-time PCR analyses at the gene level. Untreated cells are considered as control. (Pvalue < 0.0001).
Figure 14 Results of apoptotic effect of free DTX and DTX-loaded NPs treated MDA-MB-231 cells assessed by real-time PCR analyses at the gene level. Untreated cells are considered as control. (Pvalue < 0.0001).CC BY · PubMed Central
Figure 15 Western blotting images (A), and western blotting plot of protein state alterations attributed to the control group (protein state = 1) (B) of the MDA-MB-231 cells incubated with free DTX and DTX-loaded NPs with a concentration of IC50 dose. Proteins: Bcl-2, Bax, caspases 9, 7, and 3, cleaved-caspases 9, 7, and 3, and GAPDH as internal control, n = 2.
Figure 15 Western blotting images (A), and western blotting plot of protein state alterations attributed to the control group (protein state = 1) (B) of the MDA-MB-231 cells incubated with free DTX and DTX-loaded NPs with a concentration of IC50 dose. Proteins: Bcl-2, Bax, caspases 9, 7, and 3, cleaved-caspases 9, 7, and 3, and GAPDH as internal control, n = 2.CC BY · PubMed Central

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Authors
Badparvar, F., Marjani, A. P., Salehi, R., & Ramezani, F.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2024-04-12
Volume
14
Issue
1
ISSN
2045-2322
DOI
10.1038/s41598-024-57296-4
PMC
PMC11349913
Cited by
48
References
0
Language
en
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Badparvar, F., Marjani, A. P., Salehi, R., & Ramezani, F. (2024). Dual pH/redox-responsive hyperbranched polymeric nanocarriers with TME-trigger size shrinkage and charge reversible ability for amplified chemotherapy of breast cancer. Scientific Reports. https://doi.org/10.1038/s41598-024-57296-4