Self-assembly of multi-stranded RNA motifs into lattices and tubular structures

Stewart, Jaimie Marie; Subramanian, Hari K. K.; Franco, Elisa

doi:10.1093/nar/gkx063

Title: Self-assembly of multi-stranded RNA motifs into lattices and tubular structures

Abstract

Rational design of nucleic acidmolecules yields selfassembling scaffolds with increasing complexity, size and functionality. It is an open question whether design methods tailored to build DNA nanostructures can be adapted to build RNA nanostructures with comparable features. We demonstrate the formation of RNA lattices and tubular assemblies from double crossover (DX) tiles, a canonical motif in DNA nanotechnology. Tubular structures can exceed 1 m in length, suggesting that this DX motif can produce very robust lattices. Some of these tubes spontaneously form with left-handed chirality. We obtain assemblies by using two methods: a protocol where gel-extracted RNA strands are slowly annealed, and a one-pot transcription and anneal procedure. We then identify the tile nick position as a structural requirement for lattice formation. These results demonstrate that stable RNA structures can be obtained with design tools imported from DNA nanotechnology. These large assemblies could be potentially integrated with a variety of functional RNA motifs for drug or nanoparticle delivery, or for colocalization of cellular components.

Authors:

Stewart, Jaimie Marie ^[1]; Subramanian, Hari K. K. ^[2]; Franco, Elisa ^[2]

Univ. of California, Riverside, CA (United States). Dept. of Bioengineering
Univ. of California, Riverside, CA (United States). Dept. of Mechanical Engineering

Publication Date:: Thu Feb 16 00:00:00 EST 2017

Research Org.:: Univ. of California, Riverside, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC); National Science Foundation (NSF)

OSTI Identifier:: 1389571

Grant/Contract Number:: SC0010595; DMR-1450747

Resource Type:: Accepted Manuscript

Journal Name:: Nucleic Acids Research

Additional Journal Information:: Journal Volume: 45; Journal Issue: 9; Journal ID: ISSN 0305-1048

Publisher:: Oxford University Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; dna; gel; rna

Citation Formats


                    Stewart, Jaimie Marie, Subramanian, Hari K. K., and Franco, Elisa. Self-assembly of multi-stranded RNA motifs into lattices and tubular structures.  United States: N. p., 2017. 
Web.  doi:10.1093/nar/gkx063.

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                    Stewart, Jaimie Marie, Subramanian, Hari K. K., & Franco, Elisa. Self-assembly of multi-stranded RNA motifs into lattices and tubular structures.  United States.  https://doi.org/10.1093/nar/gkx063

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                    Stewart, Jaimie Marie, Subramanian, Hari K. K., and Franco, Elisa. Thu .  
"Self-assembly of multi-stranded RNA motifs into lattices and tubular structures".  United States.  https://doi.org/10.1093/nar/gkx063.  https://www.osti.gov/servlets/purl/1389571.

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@article{osti_1389571,

  title        = {Self-assembly of multi-stranded RNA motifs into lattices and tubular structures},

  author       = {Stewart, Jaimie Marie and Subramanian, Hari K. K. and Franco, Elisa},

  abstractNote = {Rational design of nucleic acidmolecules yields selfassembling scaffolds with increasing complexity, size and functionality. It is an open question whether design methods tailored to build DNA nanostructures can be adapted to build RNA nanostructures with comparable features. We demonstrate the formation of RNA lattices and tubular assemblies from double crossover (DX) tiles, a canonical motif in DNA nanotechnology. Tubular structures can exceed 1 m in length, suggesting that this DX motif can produce very robust lattices. Some of these tubes spontaneously form with left-handed chirality. We obtain assemblies by using two methods: a protocol where gel-extracted RNA strands are slowly annealed, and a one-pot transcription and anneal procedure. We then identify the tile nick position as a structural requirement for lattice formation. These results demonstrate that stable RNA structures can be obtained with design tools imported from DNA nanotechnology. These large assemblies could be potentially integrated with a variety of functional RNA motifs for drug or nanoparticle delivery, or for colocalization of cellular components.},

  doi          = {10.1093/nar/gkx063},

  journal      = {Nucleic Acids Research},

  number       = 9,

  volume       = 45,

  place        = {United States},

  year         = {Thu Feb 16 00:00:00 EST 2017},

  month        = {Thu Feb 16 00:00:00 EST 2017}

}

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Liu, Di; Geary, Cody; Chen, GAnf
Nature Chemistry, Vol. 12, Issue 3
DOI: 10.26434/chemrxiv.7837610

T7 RNA polymerase non-specifically transcribes and induces disassembly of DNA nanostructures
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Nucleic Acids Research, Vol. 46, Issue 10
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Controlling the Self-Assembly of Biomolecules into Functional Nanomaterials through Internal Interactions and External Stimulations: A Review
journal, February 2019

Wang, Li; Gong, Coucong; Yuan, Xinzhu
Nanomaterials, Vol. 9, Issue 2
DOI: 10.3390/nano9020285

Advances in intracellular delivery through supramolecular self-assembly of oligonucleotides and peptides
journal, January 2019

Kim, Jeonghwan; Narayana, Ashwanikumar; Patel, Siddharth
Theranostics, Vol. 9, Issue 11
DOI: 10.7150/thno.33921

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Title: Self-assembly of multi-stranded RNA motifs into lattices and tubular structures

Abstract

Citation Formats

Structural DNA Nanotechnology: State of the Art and Future Perspective journal, July 2014

RNA Self-Assembly and RNA Nanotechnology journal, May 2014

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

A single-stranded architecture for cotranscriptional folding of RNA nanostructures journal, August 2014

Co-transcriptional Assembly of Chemically Modified RNA Nanoparticles Functionalized with siRNAs journal, September 2012

Designing DNA nanodevices for compatibility with the immune system of higher organisms journal, September 2015

Self-Assembling RNA Nanorings Based on RNAI/II Inverse Kissing Complexes journal, February 2011

Controlling RNA self-assembly to form filaments journal, March 2006

Controlled Spacing of Cationic Gold Nanoparticles by Nanocrown RNA journal, August 2005

Building Programmable Jigsaw Puzzles with RNA journal, December 2004

Organization of Intracellular Reactions with Rationally Designed RNA Assemblies journal, June 2011

Bottom-up Assembly of RNA Arrays and Superstructures as Potential Parts in Nanotechnology journal, September 2004

Design and Characterization of Programmable DNA Nanotubes journal, December 2004

From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal journal, September 2009

DNA brick crystals with prescribed depths journal, October 2014

DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires journal, September 2003

Control of Self-Assembly of DNA Tubules Through Integration of Gold Nanoparticles journal, January 2009

Algorithmic Self-Assembly of DNA Sierpinski Triangles journal, December 2004

NUPACK: Analysis and design of nucleic acid systems journal, November 2010

The building blocks and motifs of RNA architecture journal, June 2006

Inter-RNA Interaction of Phage φ29 pRNA to Form a Hexameric Complex for Viral DNA Transportation journal, July 1998

Controllable self-assembly of RNA dendrimers journal, April 2016

Using DNA to Power Nanostructures journal, January 2003

Integrating DNA strand-displacement circuitry with DNA tile self-assembly journal, June 2013

Dynamic DNA devices and assemblies formed by shape-complementary, non-base pairing 3D components journal, March 2015

Synergistic self-assembly of RNA and DNA molecules journal, October 2010

RNA–DNA hybrid origami: folding of a long RNA single strand into complex nanostructures using short DNA helper strands journal, January 2013

Preparation of Chemically Modified RNA Origami Nanostructures journal, October 2014

DNA double-crossover molecules journal, April 1993

UCSF Chimera?A visualization system for exploratory research and analysis journal, January 2004

De Novo Design of Sequences for Nucleic Acid Structural Engineering journal, December 1990

Paradigms for computational nucleic acid design journal, February 2004

Vienna RNA secondary structure server journal, July 2003

Stacked–Unstacked Equilibrium at the Nick Site of DNA journal, September 2004

Self-Assembly of Chiral DNA Nanotubes journal, December 2004

Kinetics of RNA Degradation by Specific Base Catalysis of Transesterification Involving the 2‘-Hydroxyl Group journal, June 1999

The reactivity of phosphodiester bonds within linear single-stranded oligoribonucleotides is strongly dependent on the base sequence journal, January 2002

Nucleic acid junctions and lattices journal, November 1982

TectoRNA: modular assembly units for the construction of RNA nano-objects journal, January 2001

In vivo co-localization of enzymes on RNA scaffolds increases metabolic production in a geometrically dependent manner journal, July 2014

Self-coded 3′-Extension of Run-off Transcripts Produces Aberrant Products during in Vitro Transcription with T7 RNA Polymerase journal, March 1995

In Vitro Studies of Transcript Initiation by Escherichia coli RNA Polymerase. 1. RNA Chain Initiation, Abortive Initiation, and Promoter Escape at Three Bacteriophage Promoters † journal, April 2003

Direct Detection of Abortive RNA Transcripts in Vivo journal, May 2009

Processivity in early stages of transcription by T7 RNA polymerase journal, May 1988

Negative Autoregulation Matches Production and Demand in Synthetic Transcriptional Networks journal, April 2014

Computational and experimental characterization of RNA cubic nanoscaffolds journal, May 2014

RNA2D3D: A program for Generating, Viewing, and Comparing 3-Dimensional Models of RNA journal, June 2008

DNA Origami Design of Dolphin-Shaped Structures with Flexible Tails journal, June 2008

Rapid prototyping of 3D DNA-origami shapes with caDNAno journal, June 2009

DNA nanotube formation based on normal mode analysis journal, February 2012

Programmable RNA microstructures for coordinated delivery of siRNAs journal, January 2016

DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response journal, March 2012

UCSF Chimera?A visualization system for exploratory research and analysis journal, January 2004

Stacked–Unstacked Equilibrium at the Nick Site of DNA journal, September 2004

Controllable self-assembly of RNA dendrimers journal, April 2016

The building blocks and motifs of RNA architecture journal, June 2006

Computational and experimental characterization of RNA cubic nanoscaffolds journal, May 2014

RNA Self-Assembly and RNA Nanotechnology journal, May 2014

DNA double-crossover molecules journal, April 1993

Processivity in early stages of transcription by T7 RNA polymerase journal, May 1988

In Vitro Studies of Transcript Initiation by Escherichia coli RNA Polymerase. 1. RNA Chain Initiation, Abortive Initiation, and Promoter Escape at Three Bacteriophage Promoters † journal, April 2003

Self-Assembly of Chiral DNA Nanotubes journal, December 2004

Design and Characterization of Programmable DNA Nanotubes journal, December 2004

Self-Assembling RNA Nanorings Based on RNAI/II Inverse Kissing Complexes journal, February 2011

Co-transcriptional Assembly of Chemically Modified RNA Nanoparticles Functionalized with siRNAs journal, September 2012

Triggering of RNA Interference with RNA–RNA, RNA–DNA, and DNA–RNA Nanoparticles journal, December 2014

DNA Origami Design of Dolphin-Shaped Structures with Flexible Tails journal, June 2008

From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal journal, September 2009

DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response journal, March 2012

DNA brick crystals with prescribed depths journal, October 2014

A polyhedron made of tRNAs journal, July 2010

Synergistic self-assembly of RNA and DNA molecules journal, October 2010

From form to function journal, May 2015

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

Correction: Programmable RNA microstructures for coordinated delivery of siRNAs journal, January 2017

De Novo Design of Sequences for Nucleic Acid Structural Engineering journal, December 1990

RNA2D3D: A program for Generating, Viewing, and Comparing 3-Dimensional Models of RNA journal, June 2008

Structural DNA Nanotechnology: State of the Art and Future Perspective
journal, July 2014

RNA Self-Assembly and RNA Nanotechnology
journal, May 2014

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

A single-stranded architecture for cotranscriptional folding of RNA nanostructures
journal, August 2014

Co-transcriptional Assembly of Chemically Modified RNA Nanoparticles Functionalized with siRNAs
journal, September 2012

Designing DNA nanodevices for compatibility with the immune system of higher organisms
journal, September 2015

Self-Assembling RNA Nanorings Based on RNAI/II Inverse Kissing Complexes
journal, February 2011

Controlling RNA self-assembly to form filaments
journal, March 2006

Controlled Spacing of Cationic Gold Nanoparticles by Nanocrown RNA
journal, August 2005

Building Programmable Jigsaw Puzzles with RNA
journal, December 2004

Organization of Intracellular Reactions with Rationally Designed RNA Assemblies
journal, June 2011

Bottom-up Assembly of RNA Arrays and Superstructures as Potential Parts in Nanotechnology
journal, September 2004

Design and Characterization of Programmable DNA Nanotubes
journal, December 2004

From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal
journal, September 2009

DNA brick crystals with prescribed depths
journal, October 2014

DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires
journal, September 2003

Control of Self-Assembly of DNA Tubules Through Integration of Gold Nanoparticles
journal, January 2009

Algorithmic Self-Assembly of DNA Sierpinski Triangles
journal, December 2004

NUPACK: Analysis and design of nucleic acid systems
journal, November 2010

The building blocks and motifs of RNA architecture
journal, June 2006

Inter-RNA Interaction of Phage φ29 pRNA to Form a Hexameric Complex for Viral DNA Transportation
journal, July 1998

Controllable self-assembly of RNA dendrimers
journal, April 2016

Using DNA to Power Nanostructures
journal, January 2003

Integrating DNA strand-displacement circuitry with DNA tile self-assembly
journal, June 2013

Dynamic DNA devices and assemblies formed by shape-complementary, non-base pairing 3D components
journal, March 2015

Synergistic self-assembly of RNA and DNA molecules
journal, October 2010

RNA–DNA hybrid origami: folding of a long RNA single strand into complex nanostructures using short DNA helper strands
journal, January 2013

Preparation of Chemically Modified RNA Origami Nanostructures
journal, October 2014

DNA double-crossover molecules
journal, April 1993

UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

De Novo Design of Sequences for Nucleic Acid Structural Engineering
journal, December 1990

Paradigms for computational nucleic acid design
journal, February 2004

Vienna RNA secondary structure server
journal, July 2003

Stacked–Unstacked Equilibrium at the Nick Site of DNA
journal, September 2004

Self-Assembly of Chiral DNA Nanotubes
journal, December 2004

Kinetics of RNA Degradation by Specific Base Catalysis of Transesterification Involving the 2‘-Hydroxyl Group
journal, June 1999

The reactivity of phosphodiester bonds within linear single-stranded oligoribonucleotides is strongly dependent on the base sequence
journal, January 2002

Nucleic acid junctions and lattices
journal, November 1982

TectoRNA: modular assembly units for the construction of RNA nano-objects
journal, January 2001

In vivo co-localization of enzymes on RNA scaffolds increases metabolic production in a geometrically dependent manner
journal, July 2014

Self-coded 3′-Extension of Run-off Transcripts Produces Aberrant Products during in Vitro Transcription with T7 RNA Polymerase
journal, March 1995

In Vitro Studies of Transcript Initiation by Escherichia coli RNA Polymerase. 1. RNA Chain Initiation, Abortive Initiation, and Promoter Escape at Three Bacteriophage Promoters ^†
journal, April 2003

Direct Detection of Abortive RNA Transcripts in Vivo
journal, May 2009

Processivity in early stages of transcription by T7 RNA polymerase
journal, May 1988

Negative Autoregulation Matches Production and Demand in Synthetic Transcriptional Networks
journal, April 2014

Computational and experimental characterization of RNA cubic nanoscaffolds
journal, May 2014

RNA2D3D: A program for Generating, Viewing, and Comparing 3-Dimensional Models of RNA
journal, June 2008

DNA Origami Design of Dolphin-Shaped Structures with Flexible Tails
journal, June 2008

Rapid prototyping of 3D DNA-origami shapes with caDNAno
journal, June 2009

DNA nanotube formation based on normal mode analysis
journal, February 2012

Programmable RNA microstructures for coordinated delivery of siRNAs
journal, January 2016

DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response
journal, March 2012

UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

Stacked–Unstacked Equilibrium at the Nick Site of DNA
journal, September 2004

Controllable self-assembly of RNA dendrimers
journal, April 2016

The building blocks and motifs of RNA architecture
journal, June 2006

Computational and experimental characterization of RNA cubic nanoscaffolds
journal, May 2014

RNA Self-Assembly and RNA Nanotechnology
journal, May 2014

DNA double-crossover molecules
journal, April 1993

Processivity in early stages of transcription by T7 RNA polymerase
journal, May 1988

In Vitro Studies of Transcript Initiation by Escherichia coli RNA Polymerase. 1. RNA Chain Initiation, Abortive Initiation, and Promoter Escape at Three Bacteriophage Promoters ^†
journal, April 2003

Self-Assembly of Chiral DNA Nanotubes
journal, December 2004

Design and Characterization of Programmable DNA Nanotubes
journal, December 2004

Self-Assembling RNA Nanorings Based on RNAI/II Inverse Kissing Complexes
journal, February 2011

Co-transcriptional Assembly of Chemically Modified RNA Nanoparticles Functionalized with siRNAs
journal, September 2012

Triggering of RNA Interference with RNA–RNA, RNA–DNA, and DNA–RNA Nanoparticles
journal, December 2014

DNA Origami Design of Dolphin-Shaped Structures with Flexible Tails
journal, June 2008

From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal
journal, September 2009

DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response
journal, March 2012

DNA brick crystals with prescribed depths
journal, October 2014

A polyhedron made of tRNAs
journal, July 2010

Synergistic self-assembly of RNA and DNA molecules
journal, October 2010

From form to function
journal, May 2015

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

Correction: Programmable RNA microstructures for coordinated delivery of siRNAs
journal, January 2017

De Novo Design of Sequences for Nucleic Acid Structural Engineering
journal, December 1990

RNA2D3D: A program for Generating, Viewing, and Comparing 3-Dimensional Models of RNA
journal, June 2008

The reactivity of phosphodiester bonds within linear single-stranded oligoribonucleotides is strongly dependent on the base sequence
journal, January 2002

Vienna RNA secondary structure server
journal, July 2003

Paradigms for computational nucleic acid design
journal, February 2004