Coating of chitosan on poly D,L-lactic-co-glycolic acid thymoquinone nanoparticles enhances the anti-tumor activity in triple-negative breast cancer

Jingrong Gao; Ankita Kumari; Xin An Zeng; Siewyin Chan; Muhammad Adil Farooq; Mahafooj Alee; Shaheer Hasan Khan; Abdul Rahaman; Shan He; Xiong Xin; Tariq Mehmood

doi:10.3389/fchem.2023.1044953

Coating of chitosan on poly D,L-lactic-co-glycolic acid thymoquinone nanoparticles enhances the anti-tumor activity in triple-negative breast cancer

Jingrong Gao, Ankita Kumari, Xin An Zeng, Siewyin Chan, Muhammad Adil Farooq, Mahafooj Alee, Shaheer Hasan Khan, Abdul Rahaman, Shan He, Xiong Xin, Tariq Mehmood

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Abstract

Breast cancer is the second most common cancer around the world. Triple-negative breast cancer (TNBC) is characterized by the absence of three receptors: progesterone, estrogen, and human epidermal growth factor-2 receptor (HER2). Various synthetic chemotherapies have gained attention but they caused unwanted side effects. Therefore, some secondary therapies are now becoming famous against this disease. For instance, natural compounds have been extensively researched against many diseases. However, enzymatic degradation and low solubility remain a major concern. To combat these issues, various nanoparticles have been synthesized and optimized from time to time, which increases its solubility and hence therapeutic potential of a particular drug increases. In this study, we have synthesized Poly D,L-lactic-co-glycolic acid (PLGA) loaded thymoquinone (TQ) nanoparticle (PLGA-TQ-NPs) and then coated them by chitosan (CS) (PLGA-CS-TQ-NPs), which was characterized by different methods. Size of non-coated NPs was 105 nm with PDI value of 0.3 and the size of coated NPs was 125 nm with PDI value of 0.4. Encapsulation efficiency (EE%) and Drug loading (DL%) was found to be 70.5 ± 2.33 and 3.38 for non-coated and 82.3 ± 3.11 and 2.66 for coated NPs respectively. We have also analysed their cell viability against MDA-MB-231 and SUM-149 TNBC cell lines. The resultant, nanoformulations exhibit anti-cancerous activity in a dose and time-dependent manner for MDA-MB-231 and SUM-149 cell lines with an IC₅₀ value of (10.31 ± 1.15, 15.60 ± 1.25, 28.01 ± 1.24) and (23.54 ± 1.24, 22.37 ± 1.25, 35 ± 1.27) for TQ free, PLGA-TQ-NPs and PLGA-CS-TQ-NPs respectively. For the first time, we have developed a nanoformulations of PLGA loaded TQ coated with CS NPs (PLGA-CS-TQ-NPs) against TNBC which led to their enhanced anti-cancerous effects.

Original language	English
Article number	1044953
Pages (from-to)	1-13
Number of pages	13
Journal	Frontiers in Chemistry
Volume	11
DOIs	https://doi.org/10.3389/fchem.2023.1044953
Publication status	Published - 8 Feb 2023

Bibliographical note

Funding Information:
The study was funded by the National Natural Science Foundation of China (32150410363, 32172348, 31972205); S&T projects of Guangzhou City (project No. 202102020731, 202102080346); the 111 Project (B17018); The S&T Project of Yangjiang (SDZX20200010); the R&D projects in key areas of Guangdong Province (2019B020212004); Guangzhou City University Alliance Fundamental Research Fund (Fund No. 20210210486), and the S&T projects of China’s Ministry (QN2021163001L). The authors are also thankful for the funding provided by the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft) as part of Germany’s Excellence Strategy—EXC 2050/1—Project ID 390696704—Cluster of Excellence, “Centre for Tactile Internet with Human-in-the Loop” (CeTI) of Technische University Dresden.

Publisher Copyright:
Copyright © 2023 Gao, Kumari, Zeng, Chan, Farooq, Alee, Khan, Rahaman, He, Xin and Mehmood.

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Gao, J., Kumari, A., Zeng, X. A., Chan, S., Farooq, M. A., Alee, M., Khan, S. H., Rahaman, A., He, S., Xin, X., & Mehmood, T. (2023). Coating of chitosan on poly D,L-lactic-co-glycolic acid thymoquinone nanoparticles enhances the anti-tumor activity in triple-negative breast cancer. Frontiers in Chemistry, 11, 1-13. Article 1044953. https://doi.org/10.3389/fchem.2023.1044953

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title = "Coating of chitosan on poly D,L-lactic-co-glycolic acid thymoquinone nanoparticles enhances the anti-tumor activity in triple-negative breast cancer",

abstract = "Breast cancer is the second most common cancer around the world. Triple-negative breast cancer (TNBC) is characterized by the absence of three receptors: progesterone, estrogen, and human epidermal growth factor-2 receptor (HER2). Various synthetic chemotherapies have gained attention but they caused unwanted side effects. Therefore, some secondary therapies are now becoming famous against this disease. For instance, natural compounds have been extensively researched against many diseases. However, enzymatic degradation and low solubility remain a major concern. To combat these issues, various nanoparticles have been synthesized and optimized from time to time, which increases its solubility and hence therapeutic potential of a particular drug increases. In this study, we have synthesized Poly D,L-lactic-co-glycolic acid (PLGA) loaded thymoquinone (TQ) nanoparticle (PLGA-TQ-NPs) and then coated them by chitosan (CS) (PLGA-CS-TQ-NPs), which was characterized by different methods. Size of non-coated NPs was 105 nm with PDI value of 0.3 and the size of coated NPs was 125 nm with PDI value of 0.4. Encapsulation efficiency (EE%) and Drug loading (DL%) was found to be 70.5 ± 2.33 and 3.38 for non-coated and 82.3 ± 3.11 and 2.66 for coated NPs respectively. We have also analysed their cell viability against MDA-MB-231 and SUM-149 TNBC cell lines. The resultant, nanoformulations exhibit anti-cancerous activity in a dose and time-dependent manner for MDA-MB-231 and SUM-149 cell lines with an IC50 value of (10.31 ± 1.15, 15.60 ± 1.25, 28.01 ± 1.24) and (23.54 ± 1.24, 22.37 ± 1.25, 35 ± 1.27) for TQ free, PLGA-TQ-NPs and PLGA-CS-TQ-NPs respectively. For the first time, we have developed a nanoformulations of PLGA loaded TQ coated with CS NPs (PLGA-CS-TQ-NPs) against TNBC which led to their enhanced anti-cancerous effects.",

keywords = "chitosan, hybrid nanoparticles, polylactic acid, polymeric nanoparticles, thymoquinone, triple negative breast cancer",

author = "Jingrong Gao and Ankita Kumari and Zeng, {Xin An} and Siewyin Chan and Farooq, {Muhammad Adil} and Mahafooj Alee and Khan, {Shaheer Hasan} and Abdul Rahaman and Shan He and Xiong Xin and Tariq Mehmood",

note = "Funding Information: The study was funded by the National Natural Science Foundation of China (32150410363, 32172348, 31972205); S&T projects of Guangzhou City (project No. 202102020731, 202102080346); the 111 Project (B17018); The S&T Project of Yangjiang (SDZX20200010); the R&D projects in key areas of Guangdong Province (2019B020212004); Guangzhou City University Alliance Fundamental Research Fund (Fund No. 20210210486), and the S&T projects of China{\textquoteright}s Ministry (QN2021163001L). The authors are also thankful for the funding provided by the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft) as part of Germany{\textquoteright}s Excellence Strategy—EXC 2050/1—Project ID 390696704—Cluster of Excellence, “Centre for Tactile Internet with Human-in-the Loop” (CeTI) of Technische University Dresden. Publisher Copyright: Copyright {\textcopyright} 2023 Gao, Kumari, Zeng, Chan, Farooq, Alee, Khan, Rahaman, He, Xin and Mehmood.",

year = "2023",

month = feb,

day = "8",

doi = "10.3389/fchem.2023.1044953",

language = "English",

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journal = "Frontiers in Chemistry",

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T1 - Coating of chitosan on poly D,L-lactic-co-glycolic acid thymoquinone nanoparticles enhances the anti-tumor activity in triple-negative breast cancer

AU - Gao, Jingrong

AU - Kumari, Ankita

AU - Zeng, Xin An

AU - Chan, Siewyin

AU - Farooq, Muhammad Adil

AU - Alee, Mahafooj

AU - Khan, Shaheer Hasan

AU - Rahaman, Abdul

AU - He, Shan

AU - Xin, Xiong

AU - Mehmood, Tariq

N1 - Funding Information: The study was funded by the National Natural Science Foundation of China (32150410363, 32172348, 31972205); S&T projects of Guangzhou City (project No. 202102020731, 202102080346); the 111 Project (B17018); The S&T Project of Yangjiang (SDZX20200010); the R&D projects in key areas of Guangdong Province (2019B020212004); Guangzhou City University Alliance Fundamental Research Fund (Fund No. 20210210486), and the S&T projects of China’s Ministry (QN2021163001L). The authors are also thankful for the funding provided by the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft) as part of Germany’s Excellence Strategy—EXC 2050/1—Project ID 390696704—Cluster of Excellence, “Centre for Tactile Internet with Human-in-the Loop” (CeTI) of Technische University Dresden. Publisher Copyright: Copyright © 2023 Gao, Kumari, Zeng, Chan, Farooq, Alee, Khan, Rahaman, He, Xin and Mehmood.

PY - 2023/2/8

Y1 - 2023/2/8

N2 - Breast cancer is the second most common cancer around the world. Triple-negative breast cancer (TNBC) is characterized by the absence of three receptors: progesterone, estrogen, and human epidermal growth factor-2 receptor (HER2). Various synthetic chemotherapies have gained attention but they caused unwanted side effects. Therefore, some secondary therapies are now becoming famous against this disease. For instance, natural compounds have been extensively researched against many diseases. However, enzymatic degradation and low solubility remain a major concern. To combat these issues, various nanoparticles have been synthesized and optimized from time to time, which increases its solubility and hence therapeutic potential of a particular drug increases. In this study, we have synthesized Poly D,L-lactic-co-glycolic acid (PLGA) loaded thymoquinone (TQ) nanoparticle (PLGA-TQ-NPs) and then coated them by chitosan (CS) (PLGA-CS-TQ-NPs), which was characterized by different methods. Size of non-coated NPs was 105 nm with PDI value of 0.3 and the size of coated NPs was 125 nm with PDI value of 0.4. Encapsulation efficiency (EE%) and Drug loading (DL%) was found to be 70.5 ± 2.33 and 3.38 for non-coated and 82.3 ± 3.11 and 2.66 for coated NPs respectively. We have also analysed their cell viability against MDA-MB-231 and SUM-149 TNBC cell lines. The resultant, nanoformulations exhibit anti-cancerous activity in a dose and time-dependent manner for MDA-MB-231 and SUM-149 cell lines with an IC50 value of (10.31 ± 1.15, 15.60 ± 1.25, 28.01 ± 1.24) and (23.54 ± 1.24, 22.37 ± 1.25, 35 ± 1.27) for TQ free, PLGA-TQ-NPs and PLGA-CS-TQ-NPs respectively. For the first time, we have developed a nanoformulations of PLGA loaded TQ coated with CS NPs (PLGA-CS-TQ-NPs) against TNBC which led to their enhanced anti-cancerous effects.

AB - Breast cancer is the second most common cancer around the world. Triple-negative breast cancer (TNBC) is characterized by the absence of three receptors: progesterone, estrogen, and human epidermal growth factor-2 receptor (HER2). Various synthetic chemotherapies have gained attention but they caused unwanted side effects. Therefore, some secondary therapies are now becoming famous against this disease. For instance, natural compounds have been extensively researched against many diseases. However, enzymatic degradation and low solubility remain a major concern. To combat these issues, various nanoparticles have been synthesized and optimized from time to time, which increases its solubility and hence therapeutic potential of a particular drug increases. In this study, we have synthesized Poly D,L-lactic-co-glycolic acid (PLGA) loaded thymoquinone (TQ) nanoparticle (PLGA-TQ-NPs) and then coated them by chitosan (CS) (PLGA-CS-TQ-NPs), which was characterized by different methods. Size of non-coated NPs was 105 nm with PDI value of 0.3 and the size of coated NPs was 125 nm with PDI value of 0.4. Encapsulation efficiency (EE%) and Drug loading (DL%) was found to be 70.5 ± 2.33 and 3.38 for non-coated and 82.3 ± 3.11 and 2.66 for coated NPs respectively. We have also analysed their cell viability against MDA-MB-231 and SUM-149 TNBC cell lines. The resultant, nanoformulations exhibit anti-cancerous activity in a dose and time-dependent manner for MDA-MB-231 and SUM-149 cell lines with an IC50 value of (10.31 ± 1.15, 15.60 ± 1.25, 28.01 ± 1.24) and (23.54 ± 1.24, 22.37 ± 1.25, 35 ± 1.27) for TQ free, PLGA-TQ-NPs and PLGA-CS-TQ-NPs respectively. For the first time, we have developed a nanoformulations of PLGA loaded TQ coated with CS NPs (PLGA-CS-TQ-NPs) against TNBC which led to their enhanced anti-cancerous effects.

KW - chitosan

KW - hybrid nanoparticles

KW - polylactic acid

KW - polymeric nanoparticles

KW - thymoquinone

KW - triple negative breast cancer

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JO - Frontiers in Chemistry

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M1 - 1044953

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Coating of chitosan on poly D,L-lactic-co-glycolic acid thymoquinone nanoparticles enhances the anti-tumor activity in triple-negative breast cancer

Abstract

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