Self-Assembly of a Designed Nucleoprotein Architecture through Multimodal Interactions

Subramanian, Rohit H.; Smith, Sarah J.; Alberstein, Robert G.; Bailey, Jake B.; Zhang, Ling; Cardone, Giovanni; Suominen, Lauri; Chami, Mohamed; Stahlberg, Henning; Baker, Timothy S.; Tezcan, F. Akif

doi:10.1021/acscentsci.8b00745

Title: Self-Assembly of a Designed Nucleoprotein Architecture through Multimodal Interactions

Abstract

The co-self-assembly of proteins and nucleic acids (NAs) produces complex biomolecular machines (e.g., ribosomes and telomerases) that represent some of the most daunting targets for biomolecular design. Despite significant advances in protein and DNA or RNA nanotechnology, the construction of artificial nucleoprotein complexes has largely been limited to cases that rely on the NA-mediated spatial organization of protein units, rather than a cooperative interplay between protein- and NA-mediated interactions that typify natural nucleoprotein assemblies. We report here a structurally well-defined synthetic nucleoprotein assembly that forms through the synergy of three types of intermolecular interactions: Watson–Crick base pairing, NA–protein interactions, and protein–metal coordination. The fine thermodynamic balance between these interactions enables the formation of a crystalline architecture under highly specific conditions.

Authors:

^[1];

^[1]; Alberstein, Robert G. ^[1]; Bailey, Jake B. ^[1]; Zhang, Ling ^[1]; Cardone, Giovanni ^[1]; Suominen, Lauri ^[1]; Chami, Mohamed ^[2]; Stahlberg, Henning ^[2]; Baker, Timothy S. ^[3];

^[4]

Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, California 92093, United States
C−CINA, Biozentrum, University of Basel, Mattenstrasse 26, 4058 Basel, Switzerland
Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, California 92093, United States, Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093, United States
Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, California 92093, United States, Materials Science and Engineering, University of California, San Diego, La Jolla, California 92093, United States

Publication Date:: Thu Nov 15 00:00:00 EST 2018

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

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Inst. of Health (NIH) (United States)

OSTI Identifier:: 1482287

Alternate Identifier(s):: OSTI ID: 1508780

Grant/Contract Number:: SC0003844; AC02-76SF00515; DMR-1602537; T32GM112584-01; R01-GM033050

Resource Type:: Published Article

Journal Name:: ACS Central Science

Additional Journal Information:: Journal Name: ACS Central Science Journal Volume: 4 Journal Issue: 11; Journal ID: ISSN 2374-7943

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats


                    Subramanian, Rohit H., Smith, Sarah J., Alberstein, Robert G., Bailey, Jake B., Zhang, Ling, Cardone, Giovanni, Suominen, Lauri, Chami, Mohamed, Stahlberg, Henning, Baker, Timothy S., and Tezcan, F. Akif. Self-Assembly of a Designed Nucleoprotein Architecture through Multimodal Interactions.  United States: N. p., 2018. 
Web.  doi:10.1021/acscentsci.8b00745.

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                    Subramanian, Rohit H., Smith, Sarah J., Alberstein, Robert G., Bailey, Jake B., Zhang, Ling, Cardone, Giovanni, Suominen, Lauri, Chami, Mohamed, Stahlberg, Henning, Baker, Timothy S., & Tezcan, F. Akif. Self-Assembly of a Designed Nucleoprotein Architecture through Multimodal Interactions.  United States.  https://doi.org/10.1021/acscentsci.8b00745

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                    Subramanian, Rohit H., Smith, Sarah J., Alberstein, Robert G., Bailey, Jake B., Zhang, Ling, Cardone, Giovanni, Suominen, Lauri, Chami, Mohamed, Stahlberg, Henning, Baker, Timothy S., and Tezcan, F. Akif. Thu .  
"Self-Assembly of a Designed Nucleoprotein Architecture through Multimodal Interactions".  United States.  https://doi.org/10.1021/acscentsci.8b00745.

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@article{osti_1482287,

  title        = {Self-Assembly of a Designed Nucleoprotein Architecture through Multimodal Interactions},

  author       = {Subramanian, Rohit H. and Smith, Sarah J. and Alberstein, Robert G. and Bailey, Jake B. and Zhang, Ling and Cardone, Giovanni and Suominen, Lauri and Chami, Mohamed and Stahlberg, Henning and Baker, Timothy S. and Tezcan, F. Akif},

  abstractNote = {The co-self-assembly of proteins and nucleic acids (NAs) produces complex biomolecular machines (e.g., ribosomes and telomerases) that represent some of the most daunting targets for biomolecular design. Despite significant advances in protein and DNA or RNA nanotechnology, the construction of artificial nucleoprotein complexes has largely been limited to cases that rely on the NA-mediated spatial organization of protein units, rather than a cooperative interplay between protein- and NA-mediated interactions that typify natural nucleoprotein assemblies. We report here a structurally well-defined synthetic nucleoprotein assembly that forms through the synergy of three types of intermolecular interactions: Watson–Crick base pairing, NA–protein interactions, and protein–metal coordination. The fine thermodynamic balance between these interactions enables the formation of a crystalline architecture under highly specific conditions.},

  doi          = {10.1021/acscentsci.8b00745},

  journal      = {ACS Central Science},

  number       = 11,

  volume       = 4,

  place        = {United States},

  year         = {Thu Nov 15 00:00:00 EST 2018},

  month        = {Thu Nov 15 00:00:00 EST 2018}

}

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https://doi.org/10.1021/acscentsci.8b00745

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Cited by: 20 works

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Figures / Tables:

Figure 1: Design of RIDC3−10a/b. (a) Schematic of RIDC3−DNA hybrids. Metal-binding residues are shown as cyan sticks on the RIDC3 surface. (b) Potential self-assembly outcomes for the RIDC3−DNA hybrids.

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Title: Self-Assembly of a Designed Nucleoprotein Architecture through Multimodal Interactions

Abstract

Citation Formats

Figures / Tables:

A designed supramolecular protein assembly with in vivo enzymatic activity journal, December 2014

Generation of protein lattices by fusing proteins with matching rotational symmetry journal, July 2011

Semisynthetic DNA-Protein Conjugates for Biosensing and Nanofabrication journal, January 2010

Nanohedra: Using symmetry to design self assembling protein cages, layers, crystals, and filaments journal, February 2001

Self-Assembly of Proteins into Designed Networks journal, October 2003

Reconfiguration of DNA molecular arrays driven by information relay journal, June 2017

A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity journal, June 2012

Computational Design of Self-Assembling Protein Nanomaterials with Atomic Level Accuracy journal, May 2012

Computational design of co-assembling protein–DNA nanowires journal, September 2015

Exceptionally stable, redox-active supramolecular protein assemblies with emergent properties journal, February 2014

Gigadalton-scale shape-programmable DNA assemblies journal, December 2017

Folding DNA to create nanoscale shapes and patterns journal, March 2006

Engineering a 2D Protein-DNA Crystal journal, May 2005

Multi-enzyme complexes on DNA scaffolds capable of substrate channelling with an artificial swinging arm journal, May 2014

Metal-Directed Protein Self-Assembly journal, May 2010

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

Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays journal, March 2012

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

A universal telomerase RNA core structure includes structured motifs required for binding the telomerase reverse transcriptase protein journal, September 2004

Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly journal, October 2007

DNA Origami: Scaffolds for Creating Higher Order Structures journal, June 2017

Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals journal, May 2016

Designed proteins induce the formation of nanocage-containing extracellular vesicles journal, November 2016

Modulating Nanoparticle Superlattice Structure Using Proteins with Tunable Bond Distributions journal, January 2017

Protein Nanotube Selectively Cleavable with DNA: Supramolecular Polymerization of “DNA-Appended Molecular Chaperones” journal, December 2017

Single-stranded DNA and RNA origami journal, December 2017

DNA nanotechnology journal, November 2017

Self-assembly of genetically encoded DNA-protein hybrid nanoscale shapes journal, March 2017

DNA-mediated engineering of multicomponent enzyme crystals journal, March 2015

Evolution of a designed protein assembly encapsulating its own RNA genome journal, December 2017

Three-Dimensional Structures Self-Assembled from DNA Bricks journal, November 2012

Designed, Helical Protein Nanotubes with Variable Diameters from a Single Building Block journal, August 2015

X-ray Crystal Structures of 70S Ribosome Functional Complexes journal, September 1999

A designed supramolecular protein assembly with in vivo enzymatic activity
journal, December 2014

Generation of protein lattices by fusing proteins with matching rotational symmetry
journal, July 2011

Semisynthetic DNA-Protein Conjugates for Biosensing and Nanofabrication
journal, January 2010

Nanohedra: Using symmetry to design self assembling protein cages, layers, crystals, and filaments
journal, February 2001

Self-Assembly of Proteins into Designed Networks
journal, October 2003

Reconfiguration of DNA molecular arrays driven by information relay
journal, June 2017

A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity
journal, June 2012

Computational Design of Self-Assembling Protein Nanomaterials with Atomic Level Accuracy
journal, May 2012

Computational design of co-assembling protein–DNA nanowires
journal, September 2015

Exceptionally stable, redox-active supramolecular protein assemblies with emergent properties
journal, February 2014

Gigadalton-scale shape-programmable DNA assemblies
journal, December 2017

Folding DNA to create nanoscale shapes and patterns
journal, March 2006

Engineering a 2D Protein-DNA Crystal
journal, May 2005

Multi-enzyme complexes on DNA scaffolds capable of substrate channelling with an artificial swinging arm
journal, May 2014

Metal-Directed Protein Self-Assembly
journal, May 2010

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

Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays
journal, March 2012

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

A universal telomerase RNA core structure includes structured motifs required for binding the telomerase reverse transcriptase protein
journal, September 2004

Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly
journal, October 2007

DNA Origami: Scaffolds for Creating Higher Order Structures
journal, June 2017

Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals
journal, May 2016

Designed proteins induce the formation of nanocage-containing extracellular vesicles
journal, November 2016

Modulating Nanoparticle Superlattice Structure Using Proteins with Tunable Bond Distributions
journal, January 2017

Protein Nanotube Selectively Cleavable with DNA: Supramolecular Polymerization of “DNA-Appended Molecular Chaperones”
journal, December 2017

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journal, March 2017

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journal, March 2015

Evolution of a designed protein assembly encapsulating its own RNA genome
journal, December 2017

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journal, November 2012

Designed, Helical Protein Nanotubes with Variable Diameters from a Single Building Block
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X-ray Crystal Structures of 70S Ribosome Functional Complexes
journal, September 1999