Intertwining DNA-RNA nanocapsules loaded with tumor neoantigens as synergistic nanovaccines for cancer immunotherapy

Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we report self-assembled intertwining DNA-RNA nanocapsules (iDR-NCs) that efficiently delivered synergistic DNA CpG and short hairpin RNA (shRNA) adjuvants...

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Published inNature communications Vol. 8; no. 1; pp. 1482 - 13
Main Authors Zhu, Guizhi, Mei, Lei, Vishwasrao, Harshad D, Jacobson, Orit, Wang, Zhantong, Liu, Yijing, Yung, Bryant C, Fu, Xiao, Jin, Albert, Niu, Gang, Wang, Qin, Zhang, Fuwu, Shroff, Hari, Chen, Xiaoyuan
Format Journal Article
LanguageEnglish
Published England Nature Publishing Group 14.11.2017
Nature Publishing Group UK
Nature Portfolio
Subjects
Adjuvants
Antigen presentation
Antigen-presenting cells
Antigens
Cancer
Cancer immunotherapy
CD8 antigen
CpG islands
Deoxyribonucleic acid
DNA
Immunological memory
Immunotherapy
Lymph nodes
Lymphocytes
Lymphocytes T
Memory cells
Neoantigens
Peptides
Polyethylene glycol
Polypeptides
Precision medicine
Ribonucleic acid
RNA
Transcription
Tumors
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Abstract Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we report self-assembled intertwining DNA-RNA nanocapsules (iDR-NCs) that efficiently delivered synergistic DNA CpG and short hairpin RNA (shRNA) adjuvants, as well as tumor-specific peptide neoantigens into antigen presenting cells (APCs) in lymph nodes for cancer immunotherapy. These nanovaccines were prepared by (1) producing tandem CpG and shRNA via concurrent rolling circle replication and rolling circle transcription, (2) self-assembling CpG and shRNA into DNA-RNA microflowers, (3) shrinking microflowers into iDR-NCs using PEG-grafted cationic polypeptides, and (4) physically loading neoantigen into iDR-NCs. CpG and shRNA in iDR-NCs synergistically activate APCs for sustained antigen presentation. Remarkably, iDR-NC/neoantigen nanovaccines elicit 8-fold more frequent neoantigen-specific peripheral CD8 T cells than CpG, induce T cell memory, and significantly inhibit the progression of neoantigen-specific colorectal tumors. Collectively, iDR-NCs represent potential DNA/RNA/peptide triple-co-delivery nanocarriers and synergistic tumor immunotherapeutic nanovaccines.
AbstractList Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we report self-assembled intertwining DNA-RNA nanocapsules (iDR-NCs) that efficiently delivered synergistic DNA CpG and short hairpin RNA (shRNA) adjuvants, as well as tumor-specific peptide neoantigens into antigen presenting cells (APCs) in lymph nodes for cancer immunotherapy. These nanovaccines were prepared by (1) producing tandem CpG and shRNA via concurrent rolling circle replication and rolling circle transcription, (2) self-assembling CpG and shRNA into DNA-RNA microflowers, (3) shrinking microflowers into iDR-NCs using PEG-grafted cationic polypeptides, and (4) physically loading neoantigen into iDR-NCs. CpG and shRNA in iDR-NCs synergistically activate APCs for sustained antigen presentation. Remarkably, iDR-NC/neoantigen nanovaccines elicit 8-fold more frequent neoantigen-specific peripheral CD8+ T cells than CpG, induce T cell memory, and significantly inhibit the progression of neoantigen-specific colorectal tumors. Collectively, iDR-NCs represent potential DNA/RNA/peptide triple-co-delivery nanocarriers and synergistic tumor immunotherapeutic nanovaccines.
Abstract Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we report self-assembled intertwining DNA-RNA nanocapsules (iDR-NCs) that efficiently delivered synergistic DNA CpG and short hairpin RNA (shRNA) adjuvants, as well as tumor-specific peptide neoantigens into antigen presenting cells (APCs) in lymph nodes for cancer immunotherapy. These nanovaccines were prepared by (1) producing tandem CpG and shRNA via concurrent rolling circle replication and rolling circle transcription, (2) self-assembling CpG and shRNA into DNA-RNA microflowers, (3) shrinking microflowers into iDR-NCs using PEG-grafted cationic polypeptides, and (4) physically loading neoantigen into iDR-NCs. CpG and shRNA in iDR-NCs synergistically activate APCs for sustained antigen presentation. Remarkably, iDR-NC/neoantigen nanovaccines elicit 8-fold more frequent neoantigen-specific peripheral CD8 + T cells than CpG, induce T cell memory, and significantly inhibit the progression of neoantigen-specific colorectal tumors. Collectively, iDR-NCs represent potential DNA/RNA/peptide triple-co-delivery nanocarriers and synergistic tumor immunotherapeutic nanovaccines.
Nucleic acid nanomedicines are promising for cancer drug delivery. Here, the authors show using a mouse model the tumor immunotherapeutic efficacy of nanovaccines based on intertwining DNA-RNA nanocapsules loaded with DNA CpG, Stat3-silencing short hairpin RNA and tumor-specific peptide neoantigens.
Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we report self-assembled intertwining DNA-RNA nanocapsules (iDR-NCs) that efficiently delivered synergistic DNA CpG and short hairpin RNA (shRNA) adjuvants, as well as tumor-specific peptide neoantigens into antigen presenting cells (APCs) in lymph nodes for cancer immunotherapy. These nanovaccines were prepared by (1) producing tandem CpG and shRNA via concurrent rolling circle replication and rolling circle transcription, (2) self-assembling CpG and shRNA into DNA-RNA microflowers, (3) shrinking microflowers into iDR-NCs using PEG-grafted cationic polypeptides, and (4) physically loading neoantigen into iDR-NCs. CpG and shRNA in iDR-NCs synergistically activate APCs for sustained antigen presentation. Remarkably, iDR-NC/neoantigen nanovaccines elicit 8-fold more frequent neoantigen-specific peripheral CD8 + T cells than CpG, induce T cell memory, and significantly inhibit the progression of neoantigen-specific colorectal tumors. Collectively, iDR-NCs represent potential DNA/RNA/peptide triple-co-delivery nanocarriers and synergistic tumor immunotherapeutic nanovaccines. Nucleic acid nanomedicines are promising for cancer drug delivery. Here, the authors show using a mouse model the tumor immunotherapeutic efficacy of nanovaccines based on intertwining DNA-RNA nanocapsules loaded with DNA CpG, Stat3 -silencing short hairpin RNA and tumor-specific peptide neoantigens.
Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we report self-assembled intertwining DNA-RNA nanocapsules (iDR-NCs) that efficiently delivered synergistic DNA CpG and short hairpin RNA (shRNA) adjuvants, as well as tumor-specific peptide neoantigens into antigen presenting cells (APCs) in lymph nodes for cancer immunotherapy. These nanovaccines were prepared by (1) producing tandem CpG and shRNA via concurrent rolling circle replication and rolling circle transcription, (2) self-assembling CpG and shRNA into DNA-RNA microflowers, (3) shrinking microflowers into iDR-NCs using PEG-grafted cationic polypeptides, and (4) physically loading neoantigen into iDR-NCs. CpG and shRNA in iDR-NCs synergistically activate APCs for sustained antigen presentation. Remarkably, iDR-NC/neoantigen nanovaccines elicit 8-fold more frequent neoantigen-specific peripheral CD8 T cells than CpG, induce T cell memory, and significantly inhibit the progression of neoantigen-specific colorectal tumors. Collectively, iDR-NCs represent potential DNA/RNA/peptide triple-co-delivery nanocarriers and synergistic tumor immunotherapeutic nanovaccines.
ArticleNumber 1482
Author Wang, Zhantong
Vishwasrao, Harshad D
Niu, Gang
Zhang, Fuwu
Liu, Yijing
Fu, Xiao
Zhu, Guizhi
Jacobson, Orit
Mei, Lei
Chen, Xiaoyuan
Yung, Bryant C
Shroff, Hari
Jin, Albert
Wang, Qin
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  surname: Zhu
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– sequence: 2
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  surname: Mei
  fullname: Mei, Lei
  organization: Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland, College Park, MD, 20742, USA
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  givenname: Harshad D
  surname: Vishwasrao
  fullname: Vishwasrao, Harshad D
  organization: Advanced Imaging and Microscopy Resource, NIH, Bethesda, MD, 20892, USA
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  surname: Jacobson
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  surname: Wang
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  organization: Laboratory of Molecular Imaging and Nanomedicine, National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health (NIH), Bethesda, MD, 20892, USA
– sequence: 6
  givenname: Yijing
  surname: Liu
  fullname: Liu, Yijing
  organization: Laboratory of Molecular Imaging and Nanomedicine, National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health (NIH), Bethesda, MD, 20892, USA
– sequence: 7
  givenname: Bryant C
  surname: Yung
  fullname: Yung, Bryant C
  organization: Laboratory of Molecular Imaging and Nanomedicine, National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health (NIH), Bethesda, MD, 20892, USA
– sequence: 8
  givenname: Xiao
  surname: Fu
  fullname: Fu, Xiao
  organization: Laboratory of Cellular Imaging and Macromolecular Biophysics, NIBIB, NIH, Bethesda, MD, 20892, USA
– sequence: 9
  givenname: Albert
  orcidid: 0000-0003-3826-1081
  surname: Jin
  fullname: Jin, Albert
  organization: Laboratory of Cellular Imaging and Macromolecular Biophysics, NIBIB, NIH, Bethesda, MD, 20892, USA
– sequence: 10
  givenname: Gang
  surname: Niu
  fullname: Niu, Gang
  organization: Laboratory of Molecular Imaging and Nanomedicine, National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health (NIH), Bethesda, MD, 20892, USA
– sequence: 11
  givenname: Qin
  surname: Wang
  fullname: Wang, Qin
  organization: Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland, College Park, MD, 20742, USA
– sequence: 12
  givenname: Fuwu
  surname: Zhang
  fullname: Zhang, Fuwu
  email: fuwu.zhang@nih.gov
  organization: Laboratory of Molecular Imaging and Nanomedicine, National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health (NIH), Bethesda, MD, 20892, USA. fuwu.zhang@nih.gov
– sequence: 13
  givenname: Hari
  surname: Shroff
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– sequence: 14
  givenname: Xiaoyuan
  orcidid: 0000-0002-9622-0870
  surname: Chen
  fullname: Chen, Xiaoyuan
  email: shawn.chen@nih.gov
  organization: Laboratory of Molecular Imaging and Nanomedicine, National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health (NIH), Bethesda, MD, 20892, USA. shawn.chen@nih.gov
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29133898$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2017. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
The Author(s) 2017
Copyright_xml – notice: 2017. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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SSID ssj0000391844
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Snippet Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we report...
Abstract Nanomedicines that co-deliver DNA, RNA, and peptide therapeutics are highly desirable yet remain underdeveloped for cancer theranostics. Herein, we...
Nucleic acid nanomedicines are promising for cancer drug delivery. Here, the authors show using a mouse model the tumor immunotherapeutic efficacy of...
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StartPage 1482
SubjectTerms Adjuvants
Antigen presentation
Antigen-presenting cells
Antigens
Cancer
Cancer immunotherapy
CD8 antigen
CpG islands
Deoxyribonucleic acid
DNA
Immunological memory
Immunotherapy
Lymph nodes
Lymphocytes
Lymphocytes T
Memory cells
Neoantigens
Peptides
Polyethylene glycol
Polypeptides
Precision medicine
Ribonucleic acid
RNA
Transcription
Tumors
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Title Intertwining DNA-RNA nanocapsules loaded with tumor neoantigens as synergistic nanovaccines for cancer immunotherapy
URI https://www.ncbi.nlm.nih.gov/pubmed/29133898
https://www.proquest.com/docview/1963433281/abstract/
https://search.proquest.com/docview/1964273045
https://pubmed.ncbi.nlm.nih.gov/PMC5684198
https://doaj.org/article/c51e8ed297cd4c9da385abee4fc19f46
Volume 8
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