Photo-controlled release of paclitaxel and model drugs from RNA pyramids

doi:10.1007/s12274-018-2174-x

Title: Photo-controlled release of paclitaxel and model drugs from RNA pyramids

Abstract

Stimuli-responsive release of drugs from a nanocarrier in spatial-, temporal-, and dosage-controlled fashions is of great interest in the pharmaceutical industry. Paclitaxel is one of the most effective and popular chemotherapeutic drugs against a number of cancers such as metastatic or nonmetastatic breast cancer, non–small cell lung cancer, refractory ovarian cancer, AIDS-related Kaposi’s sarcoma, and head and neck cancers. Here, by taking the advantage of RNA nanotechnology in biomedical and material science, we developed a three-dimensional pyramid-shaped RNA nanocage for a photocontrolled release of cargo, using paclitaxel as a model drug. The light-triggered release of paclitaxel or fluorophore Cy5 was achieved by incorporation of photocleavable spacers into the RNA nanoparticles. Upon irradiation with ultraviolet light, cargos were rapidly released (within 5 min). In vitro treatment of breast cancer cells with the RNA nanoparticles harboring photocleavable paclitaxel showed higher cytotoxicity as compared to RNA nanoparticles without the photocleavable spacer. The methodology provides proof of concept for the application of the light-triggered controlled release of drugs from RNA nanocages.

Authors:

Xu, Congcong ^[1]; Li, Hui ^[1]; Zhang, Kaiming ^[2]; Binzel, Daniel W. ^[1]; Yin, Hongran ^[1]; Chiu, Wah ^[3]; Guo, Peixuan ^[1]

The Ohio State Univ., Columbus, OH (United States). Center for RNA Nanobiotechnology and Nanomedicine; The Ohio State Univ., Columbus, OH (United States). Division of Pharmaceutics and Pharmaceutical Chemistry, College of Pharmacy; The Ohio State Univ., Columbus, OH (United States). Dorothy M. Davis Heart and Lung Research Inst., College of Medicine and James Comprehensive Cancer Center
Stanford Univ., CA (United States). Dept. of Bioengineering, Microbiology and Immunology, and James H. Clark Center
Stanford Univ., CA (United States). Dept. of Bioengineering, Microbiology and Immunology, and James H. Clark Center; SLAC National Accelerator Lab., Menlo Park, CA (United States)

Publication Date:: 2018-09-17

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1490466

Grant/Contract Number:: AC02-76SF00515

Resource Type:: Accepted Manuscript

Journal Name:: Nano Research

Additional Journal Information:: Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1998-0124

Publisher:: Springer

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; 77 NANOSCIENCE AND NANOTECHNOLOGY; RNA nanotechnology; controlled release; paclitaxel; drug delivery; RNA nanoparticles; Phi29 three-way junction

Citation Formats


                    Xu, Congcong, Li, Hui, Zhang, Kaiming, Binzel, Daniel W., Yin, Hongran, Chiu, Wah, and Guo, Peixuan. Photo-controlled release of paclitaxel and model drugs from RNA pyramids.  United States: N. p., 2018. 
        Web.  doi:10.1007/s12274-018-2174-x.

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                    Xu, Congcong, Li, Hui, Zhang, Kaiming, Binzel, Daniel W., Yin, Hongran, Chiu, Wah, & Guo, Peixuan. Photo-controlled release of paclitaxel and model drugs from RNA pyramids.  United States.  doi:10.1007/s12274-018-2174-x.

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                    Xu, Congcong, Li, Hui, Zhang, Kaiming, Binzel, Daniel W., Yin, Hongran, Chiu, Wah, and Guo, Peixuan. Mon .  
        "Photo-controlled release of paclitaxel and model drugs from RNA pyramids".  United States.  doi:10.1007/s12274-018-2174-x.  https://www.osti.gov/servlets/purl/1490466.

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@article{osti_1490466,

  title        = {Photo-controlled release of paclitaxel and model drugs from RNA pyramids},

  author       = {Xu, Congcong and Li, Hui and Zhang, Kaiming and Binzel, Daniel W. and Yin, Hongran and Chiu, Wah and Guo, Peixuan},

  abstractNote = {Stimuli-responsive release of drugs from a nanocarrier in spatial-, temporal-, and dosage-controlled fashions is of great interest in the pharmaceutical industry. Paclitaxel is one of the most effective and popular chemotherapeutic drugs against a number of cancers such as metastatic or nonmetastatic breast cancer, non–small cell lung cancer, refractory ovarian cancer, AIDS-related Kaposi’s sarcoma, and head and neck cancers. Here, by taking the advantage of RNA nanotechnology in biomedical and material science, we developed a three-dimensional pyramid-shaped RNA nanocage for a photocontrolled release of cargo, using paclitaxel as a model drug. The light-triggered release of paclitaxel or fluorophore Cy5 was achieved by incorporation of photocleavable spacers into the RNA nanoparticles. Upon irradiation with ultraviolet light, cargos were rapidly released (within 5 min). In vitro treatment of breast cancer cells with the RNA nanoparticles harboring photocleavable paclitaxel showed higher cytotoxicity as compared to RNA nanoparticles without the photocleavable spacer. The methodology provides proof of concept for the application of the light-triggered controlled release of drugs from RNA nanocages.},

  doi          = {10.1007/s12274-018-2174-x},

  journal      = {Nano Research},

  number       = 1,

  volume       = 12,

  place        = {United States},

  year         = {2018},

  month        = {9}

}

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DOI: 10.1007/s12274-018-2174-x

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Title: Photo-controlled release of paclitaxel and model drugs from RNA pyramids

Abstract

Citation Formats

Stimuli-responsive nanocarriers for drug delivery journal, October 2013

Stimuli-Responsive Nanomaterials for Biomedical Applications journal, February 2015

Fabrication of 14 different RNA nanoparticles for specific tumor targeting without accumulation in normal organs journal, April 2013

Physicochemically Tunable Polyfunctionalized RNA Square Architecture with Fluorogenic and Ribozymatic Properties journal, July 2014

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RNA as a stable polymer to build controllable and defined nanostructures for material and biomedical applications journal, October 2015

Mechanism of three-component collision to produce ultrastable pRNA three-way junction of Phi29 DNA-packaging motor by kinetic assessment journal, September 2016

Smart micro/nanoparticles in stimulus-responsive drug/gene delivery systems journal, January 2016

A Light-Responsive Self-Assembly Formed by a Cationic Azobenzene Derivative and SDS as a Drug Delivery System journal, January 2017

In vitro assembly of cubic RNA-based scaffolds designed in silico journal, August 2010

Paclitaxel (Taxol) journal, April 1995

Understanding the structure and stability of paclitaxel nanocrystals journal, May 2010

An RNA motif that binds ATP journal, August 1993

Specific Delivery of MiRNA for High Efficient Inhibition of Prostate Cancer by RNA Nanotechnology journal, July 2016

Light-Triggered Release of Bioactive Molecules from DNA Nanostructures journal, March 2016

Entropy-Driven One-Step Formation of Phi29 pRNA 3WJ from Three RNA Fragments journal, April 2014

A phase I and pharmacokinetic study of NK105, a paclitaxel-incorporating micellar nanoparticle formulation journal, June 2007

Endogenous inspired biomineral-installed hyaluronan nanoparticles as pH-responsive carrier of methotrexate for rheumatoid arthritis journal, April 2017

PEG liposomalization of paclitaxel improved its in vivo disposition and anti-tumor efficacy journal, June 2011

Stable RNA nanoparticles as potential new generation drugs for cancer therapy journal, February 2014

Stimuli-Responsive DNA-Based Hydrogels: From Basic Principles to Applications journal, February 2017

Favorable biodistribution, specific targeting and conditional endosomal escape of RNA nanoparticles in cancer therapy journal, February 2018

Light-Responsive Nanoparticles for Highly Efficient Cytoplasmic Delivery of Anticancer Agents journal, October 2016

Photo-Modulated Therapeutic Protein Release from a Hydrogel Depot Using Visible Light journal, December 2016

Redox-sensitive micelles self-assembled from amphiphilic hyaluronic acid-deoxycholic acid conjugates for targeted intracellular delivery of paclitaxel journal, March 2012

Assessment and comparison of thermal stability of phosphorothioate-DNA, DNA, RNA, 2′-F RNA, and LNA in the context of Phi29 pRNA 3WJ journal, October 2017

Fabrication of RNA 3D Nanoprisms for Loading and Protection of Small RNAs and Model Drugs journal, October 2016

Programmable folding of fusion RNA in vivo and in vitro driven by pRNA 3WJ motif of phi29 DNA packaging motor journal, September 2013

Bacterial virus phi29 pRNA as a hammerhead ribozyme escort to destroy hepatitis B virus journal, July 2003

Nanoparticle orientation to control RNA loading and ligand display on extracellular vesicles for cancer regression journal, December 2017

Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles journal, September 2009

Photocontrolled Nanoparticle Delivery Systems for Biomedical Applications journal, August 2014

Self-Assembled DNA Nanoclews for the Efficient Delivery of CRISPR-Cas9 for Genome Editing journal, August 2015

Delivery of paclitaxel by physically loading onto poly(ethylene glycol) (PEG)-graftcarbon nanotubes for potent cancer therapeutics journal, January 2010

Folding of the Four-Way RNA Junction of the Hairpin Ribozyme † journal, December 1998

Spatio-temporal control strategy of drug delivery systems based nano structures journal, June 2017

Smart Nanostructures for Cargo Delivery: Uncaging and Activating by Light journal, March 2017

RNAi‐based therapeutics–current status, challenges and prospects journal, June 2009

A photoactivable multi-inhibitor nanoliposome for tumour control and simultaneous inhibition of treatment escape pathways journal, January 2016

Light-switchable systems for remotely controlled drug delivery journal, December 2017

The Spinach RNA Aptamer as a Characterization Tool for Synthetic Biology journal, September 2013

Photochemical reaction mechanisms of 2-nitrobenzyl compounds: 2-Nitrobenzyl alcohols form 2-nitroso hydrates by dual proton transfer journal, January 2005

Paclitaxel: A Review of its Pharmacodynamic and Pharmacokinetic Properties and Therapeutic Potential in the Treatment of Cancer journal, January 1994

Multifunctional, stimuli-sensitive nanoparticulate systems for drug delivery journal, October 2014

Phase II evaluation of paclitaxel by short intravenous infusion in metastatic melanoma journal, February 2004

Novel thermo-sensitive hydrogel system with paclitaxel nanocrystals: High drug-loading, sustained drug release and extended local retention guaranteeing better efficacy and lower toxicity journal, January 2014

Controllable Self-Assembly of RNA Tetrahedrons with Precise Shape and Size for Cancer Targeting journal, June 2016

Mechanism of action of taxol journal, January 1992

Stimuli-responsive polymers: Biomedical applications and challenges for clinical translation journal, January 2013

Binary Malachite Green Aptamer for Fluorescent Detection of Nucleic Acids journal, September 2005

Paclitaxel and its formulations journal, March 2002

Advancement of the Emerging Field of RNA Nanotechnology journal, February 2017

Hydrophobic Effect from Conjugated Chemicals or Drugs on In Vivo Biodistribution of RNA Nanoparticles journal, January 2018

Targeted Paclitaxel by Conjugation to Iron Oxide and Gold Nanoparticles journal, January 2009

Cell-targetable DNA nanocapsules for spatiotemporal release of caged bioactive small molecules journal, August 2017

The Smart Drug Delivery System and Its Clinical Potential journal, January 2016

In vivo evaluation of polymeric micellar paclitaxel formulation: toxicity and efficacy journal, May 2001

Thermodynamically stable RNA three-way junction for constructing multifunctional nanoparticles for delivery of therapeutics journal, September 2011

Systemic Delivery of Anti-miRNA for Suppression of Triple Negative Breast Cancer Utilizing RNA Nanotechnology journal, September 2015

Cremophor EL journal, September 2001

Streptavidin aptamers: Affinity tags for the study of RNAs and ribonucleoproteins journal, April 2001

Cocoon-Like Self-Degradable DNA Nanoclew for Anticancer Drug Delivery journal, October 2014

Regression of Gastric Cancer by Systemic Injection of RNA Nanoparticles Carrying both Ligand and siRNA journal, July 2015

Ultrastable synergistic tetravalent RNA nanoparticles for targeting to cancers journal, August 2012

RNA-based micelles: A novel platform for paclitaxel loading and delivery journal, April 2018

RNA nanoparticle as a vector for targeted siRNA delivery into glioblastoma mouse model journal, March 2015

Tuning the size, shape and structure of RNA nanoparticles for favorable cancer targeting and immunostimulation journal, August 2019

The Role of Photochemical Reactions in the Development of Advanced Soft Materials for Biomedical Applications journal, April 2019

Tuning the size, shape and structure of RNA nanoparticles for favorable cancer targeting and immunostimulation journal, August 2019

High-order structures from nucleic acids for biomedical applications journal, January 2020

Stimuli-responsive nanocarriers for drug delivery
journal, October 2013

Stimuli-Responsive Nanomaterials for Biomedical Applications
journal, February 2015

Fabrication of 14 different RNA nanoparticles for specific tumor targeting without accumulation in normal organs
journal, April 2013

Physicochemically Tunable Polyfunctionalized RNA Square Architecture with Fluorogenic and Ribozymatic Properties
journal, July 2014

Light activated liposomes: Functionality and prospects in ocular drug delivery
journal, December 2016

RNA as a stable polymer to build controllable and defined nanostructures for material and biomedical applications
journal, October 2015

Mechanism of three-component collision to produce ultrastable pRNA three-way junction of Phi29 DNA-packaging motor by kinetic assessment
journal, September 2016

Smart micro/nanoparticles in stimulus-responsive drug/gene delivery systems
journal, January 2016

A Light-Responsive Self-Assembly Formed by a Cationic Azobenzene Derivative and SDS as a Drug Delivery System
journal, January 2017

In vitro assembly of cubic RNA-based scaffolds designed in silico
journal, August 2010

Paclitaxel (Taxol)
journal, April 1995

Understanding the structure and stability of paclitaxel nanocrystals
journal, May 2010

An RNA motif that binds ATP
journal, August 1993

Specific Delivery of MiRNA for High Efficient Inhibition of Prostate Cancer by RNA Nanotechnology
journal, July 2016

Light-Triggered Release of Bioactive Molecules from DNA Nanostructures
journal, March 2016

Entropy-Driven One-Step Formation of Phi29 pRNA 3WJ from Three RNA Fragments
journal, April 2014

A phase I and pharmacokinetic study of NK105, a paclitaxel-incorporating micellar nanoparticle formulation
journal, June 2007

Endogenous inspired biomineral-installed hyaluronan nanoparticles as pH-responsive carrier of methotrexate for rheumatoid arthritis
journal, April 2017

PEG liposomalization of paclitaxel improved its in vivo disposition and anti-tumor efficacy
journal, June 2011

Stable RNA nanoparticles as potential new generation drugs for cancer therapy
journal, February 2014

Stimuli-Responsive DNA-Based Hydrogels: From Basic Principles to Applications
journal, February 2017

Favorable biodistribution, specific targeting and conditional endosomal escape of RNA nanoparticles in cancer therapy
journal, February 2018

Light-Responsive Nanoparticles for Highly Efficient Cytoplasmic Delivery of Anticancer Agents
journal, October 2016

Photo-Modulated Therapeutic Protein Release from a Hydrogel Depot Using Visible Light
journal, December 2016

Redox-sensitive micelles self-assembled from amphiphilic hyaluronic acid-deoxycholic acid conjugates for targeted intracellular delivery of paclitaxel
journal, March 2012

Assessment and comparison of thermal stability of phosphorothioate-DNA, DNA, RNA, 2′-F RNA, and LNA in the context of Phi29 pRNA 3WJ
journal, October 2017

Fabrication of RNA 3D Nanoprisms for Loading and Protection of Small RNAs and Model Drugs
journal, October 2016

Programmable folding of fusion RNA in vivo and in vitro driven by pRNA 3WJ motif of phi29 DNA packaging motor
journal, September 2013

Bacterial virus phi29 pRNA as a hammerhead ribozyme escort to destroy hepatitis B virus
journal, July 2003

Nanoparticle orientation to control RNA loading and ligand display on extracellular vesicles for cancer regression
journal, December 2017

Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles
journal, September 2009

Photocontrolled Nanoparticle Delivery Systems for Biomedical Applications
journal, August 2014

Self-Assembled DNA Nanoclews for the Efficient Delivery of CRISPR-Cas9 for Genome Editing
journal, August 2015

Delivery of paclitaxel by physically loading onto poly(ethylene glycol) (PEG)-graftcarbon nanotubes for potent cancer therapeutics
journal, January 2010

Folding of the Four-Way RNA Junction of the Hairpin Ribozyme ^†
journal, December 1998

Spatio-temporal control strategy of drug delivery systems based nano structures
journal, June 2017

Smart Nanostructures for Cargo Delivery: Uncaging and Activating by Light
journal, March 2017

RNAi‐based therapeutics–current status, challenges and prospects
journal, June 2009

A photoactivable multi-inhibitor nanoliposome for tumour control and simultaneous inhibition of treatment escape pathways
journal, January 2016

Light-switchable systems for remotely controlled drug delivery
journal, December 2017

The Spinach RNA Aptamer as a Characterization Tool for Synthetic Biology
journal, September 2013

Photochemical reaction mechanisms of 2-nitrobenzyl compounds: 2-Nitrobenzyl alcohols form 2-nitroso hydrates by dual proton transfer
journal, January 2005

Paclitaxel: A Review of its Pharmacodynamic and Pharmacokinetic Properties and Therapeutic Potential in the Treatment of Cancer
journal, January 1994

Multifunctional, stimuli-sensitive nanoparticulate systems for drug delivery
journal, October 2014

Phase II evaluation of paclitaxel by short intravenous infusion in metastatic melanoma
journal, February 2004

Novel thermo-sensitive hydrogel system with paclitaxel nanocrystals: High drug-loading, sustained drug release and extended local retention guaranteeing better efficacy and lower toxicity
journal, January 2014

Controllable Self-Assembly of RNA Tetrahedrons with Precise Shape and Size for Cancer Targeting
journal, June 2016

Mechanism of action of taxol
journal, January 1992

Stimuli-responsive polymers: Biomedical applications and challenges for clinical translation
journal, January 2013

Binary Malachite Green Aptamer for Fluorescent Detection of Nucleic Acids
journal, September 2005

Paclitaxel and its formulations
journal, March 2002

Advancement of the Emerging Field of RNA Nanotechnology
journal, February 2017

Hydrophobic Effect from Conjugated Chemicals or Drugs on In Vivo Biodistribution of RNA Nanoparticles
journal, January 2018

Targeted Paclitaxel by Conjugation to Iron Oxide and Gold Nanoparticles
journal, January 2009

Cell-targetable DNA nanocapsules for spatiotemporal release of caged bioactive small molecules
journal, August 2017

The Smart Drug Delivery System and Its Clinical Potential
journal, January 2016

In vivo evaluation of polymeric micellar paclitaxel formulation: toxicity and efficacy
journal, May 2001

Thermodynamically stable RNA three-way junction for constructing multifunctional nanoparticles for delivery of therapeutics
journal, September 2011

Systemic Delivery of Anti-miRNA for Suppression of Triple Negative Breast Cancer Utilizing RNA Nanotechnology
journal, September 2015

Cremophor EL
journal, September 2001

Streptavidin aptamers: Affinity tags for the study of RNAs and ribonucleoproteins
journal, April 2001

Cocoon-Like Self-Degradable DNA Nanoclew for Anticancer Drug Delivery
journal, October 2014

Regression of Gastric Cancer by Systemic Injection of RNA Nanoparticles Carrying both Ligand and siRNA
journal, July 2015

Ultrastable synergistic tetravalent RNA nanoparticles for targeting to cancers
journal, August 2012

RNA-based micelles: A novel platform for paclitaxel loading and delivery
journal, April 2018

RNA nanoparticle as a vector for targeted siRNA delivery into glioblastoma mouse model
journal, March 2015

Tuning the size, shape and structure of RNA nanoparticles for favorable cancer targeting and immunostimulation
journal, August 2019

The Role of Photochemical Reactions in the Development of Advanced Soft Materials for Biomedical Applications
journal, April 2019

Tuning the size, shape and structure of RNA nanoparticles for favorable cancer targeting and immunostimulation
journal, August 2019

High-order structures from nucleic acids for biomedical applications
journal, January 2020