An autocatalytic multicomponent DNAzyme nanomachine for tumor-specific photothermal therapy sensitization in pancreatic cancer

Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polye...

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Published inNature communications Vol. 14; no. 1; pp. 6905 - 21
Main Authors Yan, Jiaqi, Ma, Xiaodong, Liang, Danna, Ran, Meixin, Zheng, Dongdong, Chen, Xiaodong, Zhou, Shichong, Sun, Weijian, Shen, Xian, Zhang, Hongbo
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 30.10.2023
Nature Publishing Group
Nature Portfolio
Subjects
14
14/19
14/32
147/135
147/143
59
631/61/350/354
631/61/54/152
631/67/1059/602
Biocompatibility
Calcium (intracellular)
Calcium (mitochondrial)
Calcium efflux
Calcium homeostasis
Calcium ions
Calcium phosphates
Cancer
Cancer therapies
Cell Line, Tumor
Curcumin
Curcumin - pharmacology
Deoxyribozymes
DNA, Catalytic
Efflux
Ethanolamine
Gene regulation
Gene therapy
Heat shock proteins
Homeostasis
Hsp70 protein
Humanities and Social Sciences
Humans
Hydrophobicity
Irradiation
Laser radiation
Micelles
MicroRNAs - genetics
Mineralization
miRNA
mRNA
multidisciplinary
Nanoparticles - chemistry
Neoplasms
Oligopeptides
Pancreatic cancer
Pancreatic Neoplasms
Pancreatic Neoplasms - therapy
Phototherapy - methods
Photothermal Therapy
Polyethylene glycol
Polyethylene Glycols - chemistry
PTEN protein
Science
Science (multidisciplinary)
Toxicity
Tumor suppressor genes
Tumors
Online AccessGet full text

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Abstract Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca 2+ under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca 2+ to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca 2+ homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation. Despite delivering gene-specific silencing, the use of deoxyribozymes (DNAzymes) for cancer therapy is limited by toxicity due to off-target effects. Here, the authors develop a multi-component DNAzyme, targeting both miRNA21 and HSP70, to induce tumour-specific sensitisation to photothermal therapy in preclinical models of pancreatic cancer.
AbstractList Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca 2+ under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca 2+ to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca 2+ homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation. Despite delivering gene-specific silencing, the use of deoxyribozymes (DNAzymes) for cancer therapy is limited by toxicity due to off-target effects. Here, the authors develop a multi-component DNAzyme, targeting both miRNA21 and HSP70, to induce tumour-specific sensitisation to photothermal therapy in preclinical models of pancreatic cancer.
Abstract Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca2+ under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca2+ to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca2+ homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation.
Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca 2+ under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca 2+ to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca 2+ homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation.
Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca2+ under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca2+ to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca2+ homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation.Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca2+ under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca2+ to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca2+ homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation.
Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca2+ under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca2+ to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca2+ homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation.Despite delivering gene-specific silencing, the use of deoxyribozymes (DNAzymes) for cancer therapy is limited by toxicity due to off-target effects. Here, the authors develop a multi-component DNAzyme, targeting both miRNA21 and HSP70, to induce tumour-specific sensitisation to photothermal therapy in preclinical models of pancreatic cancer.
Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic gene regulation has rarely been studied. Herein, Arginylglycylaspartic acid (RGD)-modified Distearyl acylphosphatidyl ethanolamine (DSPE)-polyethylene glycol (PEG) (DSPE-PEG-RGD) micelle is prepared with a DSPE hydrophobic core to load the photothermal therapy (PTT) dye IR780 and the calcium efflux pump inhibitor curcumin. Then, the MNAzyme is distributed into the hydrophilic PEG layer and sealed with calcium phosphate through biomineralization. Moreover, RGD is attached to the outer tail of PEG for tumor targeting. The constructed nanomachine can release MNAzyme and the cofactor Ca under acidic conditions and self-assemble into an active mode to cleave heat shock protein (HSP) mRNA by consuming the oncogene miRNA-21. Silencing miRNA-21 enhances the expression of the tumor suppressor gene PTEN, leading to PTT sensitization. Meanwhile, curcumin maintains high intracellular Ca to further suppress HSP-chaperone ATP by disrupting mitochondrial Ca homeostasis. Therefore, pancreatic cancer is triple-sensitized to IR780-mediated PTT. The in vitro and in vivo results show that the MNAzyme-based nanomachine can strongly regulate HSP and PTEN expression and lead to significant pancreatic tumor inhibition under laser irradiation.
ArticleNumber 6905
Author Chen, Xiaodong
Zhou, Shichong
Ma, Xiaodong
Sun, Weijian
Ran, Meixin
Shen, Xian
Zheng, Dongdong
Yan, Jiaqi
Liang, Danna
Zhang, Hongbo
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  surname: Yan
  fullname: Yan, Jiaqi
  organization: Joint Centre of Translational Medicine, Wenzhou Key Laboratory of Interdiscipline and Translational Medicine, The First Affiliated Hospital of Wenzhou Medical University, Department of General Surgery, The First Affiliated Hospital of Wenzhou Medical University, Pharmaceutical Sciences Laboratory, Faculty of Science and Engineering, Åbo Akademi University, Turku Bioscience Centre, University of Turku and Åbo Akademi University
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  givenname: Xiaodong
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  organization: Pharmaceutical Sciences Laboratory, Faculty of Science and Engineering, Åbo Akademi University, Turku Bioscience Centre, University of Turku and Åbo Akademi University
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  givenname: Danna
  orcidid: 0000-0002-8910-568X
  surname: Liang
  fullname: Liang, Danna
  organization: Department of Gastrointestinal Surgery, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University
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  givenname: Meixin
  surname: Ran
  fullname: Ran, Meixin
  organization: Joint Centre of Translational Medicine, Wenzhou Key Laboratory of Interdiscipline and Translational Medicine, The First Affiliated Hospital of Wenzhou Medical University, Department of General Surgery, The First Affiliated Hospital of Wenzhou Medical University, Pharmaceutical Sciences Laboratory, Faculty of Science and Engineering, Åbo Akademi University, Turku Bioscience Centre, University of Turku and Åbo Akademi University
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  givenname: Dongdong
  orcidid: 0000-0001-6189-9046
  surname: Zheng
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  organization: Department of Ultrasound, Fudan University Shanghai Cancer Center
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  givenname: Xiaodong
  surname: Chen
  fullname: Chen, Xiaodong
  organization: Joint Centre of Translational Medicine, Wenzhou Key Laboratory of Interdiscipline and Translational Medicine, The First Affiliated Hospital of Wenzhou Medical University, Department of General Surgery, The First Affiliated Hospital of Wenzhou Medical University
– sequence: 7
  givenname: Shichong
  surname: Zhou
  fullname: Zhou, Shichong
  organization: Department of Ultrasound, Fudan University Shanghai Cancer Center
– sequence: 8
  givenname: Weijian
  surname: Sun
  fullname: Sun, Weijian
  email: fame198288@126.com
  organization: Department of Gastrointestinal Surgery, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University
– sequence: 9
  givenname: Xian
  surname: Shen
  fullname: Shen, Xian
  email: shenxian@wmu.edu.cn
  organization: Joint Centre of Translational Medicine, Wenzhou Key Laboratory of Interdiscipline and Translational Medicine, The First Affiliated Hospital of Wenzhou Medical University, Department of General Surgery, The First Affiliated Hospital of Wenzhou Medical University
– sequence: 10
  givenname: Hongbo
  orcidid: 0000-0002-1071-4416
  surname: Zhang
  fullname: Zhang, Hongbo
  email: hongbo.zhang@abo.fi
  organization: Joint Centre of Translational Medicine, Wenzhou Key Laboratory of Interdiscipline and Translational Medicine, The First Affiliated Hospital of Wenzhou Medical University, Department of General Surgery, The First Affiliated Hospital of Wenzhou Medical University, Pharmaceutical Sciences Laboratory, Faculty of Science and Engineering, Åbo Akademi University, Turku Bioscience Centre, University of Turku and Åbo Akademi University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37903795$$D View this record in MEDLINE/PubMed
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Snippet Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve synergistic...
Abstract Multicomponent deoxyribozymes (MNAzymes) have great potential in gene therapy, but their ability to recognize disease tissue and further achieve...
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StartPage 6905
SubjectTerms 14
14/19
14/32
147/135
147/143
59
631/61/350/354
631/61/54/152
631/67/1059/602
Biocompatibility
Calcium (intracellular)
Calcium (mitochondrial)
Calcium efflux
Calcium homeostasis
Calcium ions
Calcium phosphates
Cancer
Cancer therapies
Cell Line, Tumor
Curcumin
Curcumin - pharmacology
Deoxyribozymes
DNA, Catalytic
Efflux
Ethanolamine
Gene regulation
Gene therapy
Heat shock proteins
Homeostasis
Hsp70 protein
Humanities and Social Sciences
Humans
Hydrophobicity
Irradiation
Laser radiation
Micelles
MicroRNAs - genetics
Mineralization
miRNA
mRNA
multidisciplinary
Nanoparticles - chemistry
Neoplasms
Oligopeptides
Pancreatic cancer
Pancreatic Neoplasms
Pancreatic Neoplasms - therapy
Phototherapy - methods
Photothermal Therapy
Polyethylene glycol
Polyethylene Glycols - chemistry
PTEN protein
Science
Science (multidisciplinary)
Toxicity
Tumor suppressor genes
Tumors
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Title An autocatalytic multicomponent DNAzyme nanomachine for tumor-specific photothermal therapy sensitization in pancreatic cancer
URI https://link.springer.com/article/10.1038/s41467-023-42740-2
https://www.ncbi.nlm.nih.gov/pubmed/37903795
https://www.proquest.com/docview/2884010388
https://www.proquest.com/docview/2884675789
https://pubmed.ncbi.nlm.nih.gov/PMC10616286
https://doaj.org/article/b81d72334b1c49568d7302bae009e320
Volume 14
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