Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition

Post, Klara; Olson, Erik D.; Naufer, M. Nabuan; Gorelick, Robert J.; Rouzina, Ioulia; Williams, Mark C.; Musier-Forsyth, Karin; Levin, Judith G.

doi:10.1186/s12977-016-0322-5

Title: Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition

Abstract

The nucleocapsid (NC) domain of HIV-1 Gag is responsible for specific recognition and packaging of genomic RNA (gRNA) into new viral particles. This occurs through specific interactions between the Gag NC domain and the Psi packaging signal in gRNA. In addition to this critical function, NC proteins are also nucleic acid (NA) chaperone proteins that facilitate NA rearrangements during reverse transcription. Although the interaction with Psi and chaperone activity of HIV-1 NC have been well characterized in vitro, little is known about simian immunodeficiency virus (SIV) NC. Non-human primates are frequently used as a platform to study retroviral infection in vivo; thus, it is important to understand underlying mechanistic differences between HIV-1 and SIV NC.

Authors:

Post, Klara ^[1]; Olson, Erik D. ^[2]; Naufer, M. Nabuan ^[3]; Gorelick, Robert J. ^[4]; Rouzina, Ioulia ^[2];

^[5]; Musier-Forsyth, Karin ^[2];

^[1]

National Inst. of Health (NIH), Bethesda, MD (United States). Section on Viral Gene Regulation, Program in Genomics of Differentiation, Eunice Kennedy Shriver National Institute of Child Health and Human Development
The Ohio State Univ., Columbus, OH (United States). Department of Chemistry and Biochemistry, Center for Retrovirus Research, and Center for RNA Biology
Northeastern Univ., Boston, MA (United States). Department of Physics
Frederick National Laboratory for Cancer Research, Frederick, MD (United States). AIDS and Cancer Virus Program, Leidos Biomedical Research, Inc.,
Northeastern Univ., Boston, MA (United States). Department of Physics

Publication Date:: Thu Dec 29 00:00:00 EST 2016

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1626909

Grant/Contract Number:: AC02-05CH11231; R01‑GM065056; R01‑GM072462; HHSN261200800001E; R01‑GM105404

Resource Type:: Accepted Manuscript

Journal Name:: Retrovirology

Additional Journal Information:: Journal Volume: 13; Journal Issue: 1; Journal ID: ISSN 1742-4690

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: Virology; HIV 1; SIV; Nucleocapsid proteins; Nucleic acid chaperone activity; Psi RNA packaging signal; Minus strand transfer; Small angle X ray scattering; Single molecule DNA stretching; Nucleic acid binding; Reverse transcription

Citation Formats


                    Post, Klara, Olson, Erik D., Naufer, M. Nabuan, Gorelick, Robert J., Rouzina, Ioulia, Williams, Mark C., Musier-Forsyth, Karin, and Levin, Judith G. Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition.  United States: N. p., 2016. 
Web.  doi:10.1186/s12977-016-0322-5.

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                    Post, Klara, Olson, Erik D., Naufer, M. Nabuan, Gorelick, Robert J., Rouzina, Ioulia, Williams, Mark C., Musier-Forsyth, Karin, & Levin, Judith G. Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition.  United States.  https://doi.org/10.1186/s12977-016-0322-5

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                    Post, Klara, Olson, Erik D., Naufer, M. Nabuan, Gorelick, Robert J., Rouzina, Ioulia, Williams, Mark C., Musier-Forsyth, Karin, and Levin, Judith G. Thu .  
"Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition".  United States.  https://doi.org/10.1186/s12977-016-0322-5.  https://www.osti.gov/servlets/purl/1626909.

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@article{osti_1626909,

  title        = {Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition},

  author       = {Post, Klara and Olson, Erik D. and Naufer, M. Nabuan and Gorelick, Robert J. and Rouzina, Ioulia and Williams, Mark C. and Musier-Forsyth, Karin and Levin, Judith G.},

  abstractNote = {The nucleocapsid (NC) domain of HIV-1 Gag is responsible for specific recognition and packaging of genomic RNA (gRNA) into new viral particles. This occurs through specific interactions between the Gag NC domain and the Psi packaging signal in gRNA. In addition to this critical function, NC proteins are also nucleic acid (NA) chaperone proteins that facilitate NA rearrangements during reverse transcription. Although the interaction with Psi and chaperone activity of HIV-1 NC have been well characterized in vitro, little is known about simian immunodeficiency virus (SIV) NC. Non-human primates are frequently used as a platform to study retroviral infection in vivo; thus, it is important to understand underlying mechanistic differences between HIV-1 and SIV NC.},

  doi          = {10.1186/s12977-016-0322-5},

  journal      = {Retrovirology},

  number       = 1,

  volume       = 13,

  place        = {United States},

  year         = {Thu Dec 29 00:00:00 EST 2016},

  month        = {Thu Dec 29 00:00:00 EST 2016}

}

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Figures / Tables:

Fig. 1: Sequence and structural features of HIV‑1 and SIV NC proteins. a Schematic diagrams of NC proteins: HIV‑1 NL4‑3 NC and SIVmne NC. Basic residues are colored blue, acidic residues are colored red, the CCHC residues that coordinate the Zn²⁺ ions in the ZFs are colored gray, and themore »

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An RNA-binding compound that stabilizes the HIV-1 gRNA packaging signal structure and specifically blocks HIV-1 RNA encapsidation
journal, March 2018

Ingemarsdotter, Carin K.; Zeng, Jingwei; Long, Ziqi
Retrovirology, Vol. 15, Issue 1
DOI: 10.1186/s12977-018-0407-4

An RNA-binding compound that stabilizes the HIV-1 gRNA packaging signal structure and specifically blocks HIV-1 RNA encapsidation.
text, January 2018

Ingemarsdotter, Carin; Zeng, Jing; Long, Ziqi
Apollo - University of Cambridge Repository
DOI: 10.17863/cam.23382

An RNA-binding compound that stabilizes the HIV-1 gRNA packaging signal structure and specifically blocks HIV-1 RNA encapsidation
collection, January 2018

Ingemarsdotter, Carin K.; Zeng, Jingwei; Long, Ziqi
Apollo - University of Cambridge Repository
DOI: 10.17863/cam.21838

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Title: Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition

Abstract

Citation Formats

Figures / Tables:

Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins journal, January 2006

Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus journal, June 1990

Optical tweezers experiments resolve distinct modes of DNA-protein binding journal, April 2009

Initiation of HIV Reverse Transcription journal, January 2010

Targeted binding of nucleocapsid protein transforms the folding landscape of HIV-1 TAR RNA journal, October 2015

Aromatic residue mutations reveal direct correlation between HIV-1 nucleocapsid protein's nucleic acid chaperone activity and retroviral replication journal, February 2013

Kuru experiments triggered the emergence of pathogenic SIVmac journal, January 2006

Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription journal, November 2010

Nucleocapsid Protein Zinc-Finger Mutants of Simian Immunodeficiency Virus Strain Mne Produce Virions That Are Replication Defectivein Vitroandin Vivo journal, January 1999

Preparation of Recombinant HIV-1 Gag Protein and Assembly of Virus-Like Particles In Vitro book, January 2009

Distinct nucleic acid interaction properties of HIV-1 nucleocapsid protein precursor NCp15 explain reduced viral infectivity journal, May 2014

Identification of a Minimal Region of the HIV-1 5′-Leader Required for RNA Dimerization, NC Binding, and Packaging journal, March 2012

Distinct binding interactions of HIV-1 Gag to Psi and non-Psi RNAs: Implications for viral genomic RNA packaging journal, June 2013

A protein ballet around the viral genome orchestrated by HIV-1 reverse transcriptase leads to an architectural switch: From nucleocapsid-condensed RNA to Vpr-bridged DNA journal, February 2013

Fluorescence Anisotropy-Based Salt-Titration Approach to Characterize Protein–Nucleic Acid Interactions book, December 2014

Origins of HIV and the AIDS Pandemic journal, September 2011

HIV-1 Protease and Reverse Transcriptase Control the Architecture of Their Nucleocapsid Partner journal, August 2007

A Guanosine-Centric Mechanism for RNA Chaperone Function journal, March 2013

The matrix domain contributes to the nucleic acid chaperone activity of HIV-2 Gag journal, March 2016

Hybrid Origin of SIV in Chimpanzees journal, June 2003

Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS journal, May 1984

Visualizing the Formation and Collapse of DNA Toroids journal, May 2010

Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS journal, May 1984

The Simian Immunodeficiency Virus 5′ Untranslated Leader Sequence Plays a Role in Intracellular Viral Protein Accumulation and in RNA Packaging journal, June 2003

Rapid Kinetics of Protein–Nucleic Acid Interaction is a Major Component of HIV-1 Nucleocapsid Protein’s Nucleic Acid Chaperone Function journal, November 2006

On the Selective Packaging of Genomic RNA by HIV-1 journal, September 2016

The Choreography of HIV-1 Proteolytic Processing and Virion Assembly journal, October 2012

Lentivirus Vectors Using Human and Simian Immunodeficiency Virus Elements journal, April 1999

High-Throughput SAXS for the Characterization of Biomolecules in Solution: A Practical Approach book, October 2013

NMR Structure of the 101-nucleotide Core Encapsidation Signal of the Moloney Murine Leukemia Virus journal, March 2004

International AIDS Society global scientific strategy: towards an HIV cure 2016 journal, July 2016

Alteration of Nucleic Acid Structure and Stability Modulates the Efficiency of Minus-Strand Transfer Mediated by the HIV-1 Nucleocapsid Protein journal, July 2004

Orchestrating the Selection and Packaging of Genomic RNA by Retroviruses: An Ensemble of Viral and Host Factors journal, September 2016

Functional Equivalence of Retroviral MA Domains in Facilitating Psi RNA Binding Specificity by Gag journal, September 2016

New Paradigms for HIV/AIDS Vaccine Development journal, February 2012

Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus journal, September 2004

Conserved determinants of lentiviral genome dimerization journal, September 2015

Biophysical studies of the nucleic acid chaperone properties of the HIV-1 nucleocapsid protein journal, November 2010

Macaques Infected with Cloned Simian Immunodeficiency Virus Show RecurringnefGene Alterations journal, September 1998

Differential contribution of basic residues to HIV-1 nucleocapsid protein’s nucleic acid chaperone function and retroviral replication journal, November 2013

Human infection by genetically diverse SIVSM-related HIV-2 in West Africa journal, August 1992

Fundamental differences between the nucleic acid chaperone activities of HIV-1 nucleocapsid protein and Gag or Gag-derived proteins: Biological implications journal, September 2010

Initiation of HIV-1 reverse transcription and functional role of nucleocapsid-mediated tRNA/viral genome interactions journal, November 2012

Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strong-stop DNA. journal, January 1997

Retrospective on the all-in-one retroviral nucleocapsid protein journal, November 2014

Specific recognition of the HIV-1 genomic RNA by the Gag precursor journal, July 2014

Structure of the HIV-1 RNA packaging signal journal, May 2015

Flexible Nature and Specific Functions of the HIV-1 Nucleocapsid Protein journal, July 2011

The Complete Nucleotide Sequence of a Pathogenic Molecular Clone of Simian Immunodeficiency Virus journal, November 1990

Molecular mimicry of human tRNALys anti-codon domain by HIV-1 RNA genome facilitates tRNA primer annealing journal, December 2012

Nucleic Acid Binding Properties of the Simian Immunodeficiency Virus Nucleocapsid Protein NCp8 journal, March 2000

Impaired RNA incorporation and dimerization in live attenuated leader-variants of SIVmac239 journal, December 2006

Single aromatic residue location alters nucleic acid binding and chaperone function of FIV nucleocapsid protein journal, November 2014

Defects in Primer-Template Binding, Processive DNA Synthesis, and RNase H Activity Associated with Chimeric Reverse Transcriptases Having the Murine Leukemia Virus Polymerase Domain Joined to Escherichia coli RNase H journal, April 1995

Chimpanzee Reservoirs of Pandemic and Nonpandemic HIV-1 journal, July 2006

HIV Gag polyprotein: processing and early viral particle assembly journal, March 2013

Isolation of a new human retrovirus from West African patients with AIDS journal, July 1986

Nucleic Acid Chaperone Activity of HIV‐1 Nucleocapsid Protein: Critical Role in Reverse Transcription and Molecular Mechanism book, January 2005

Small-angle X-ray scattering-derived structure of the HIV-1 5′ UTR reveals 3D tRNA mimicry journal, February 2014

Requirements for efficient minus strand strong-stop DNA transfer in human immunodeficiency virus 1 journal, March 2011

An African primate lentivirus (SIVsmclosely related to HIV-2 journal, June 1989

Solution Structure of the Rous Sarcoma Virus Nucleocapsid Protein: μΨ RNA Packaging Signal Complex journal, January 2007

Identification of unique reciprocal and non reciprocal cross packaging relationships between HIV-1, HIV-2 and SIV reveals an efficient SIV/HIV-2 lentiviral vector system with highly favourable features for in vivo testing and clinical usage journal, September 2005

X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution journal, August 2007

The packaging signal of simian immunodeficiency virus is upstream of the major splice donor at a distance from the RNA cap site similar to that of human immunodeficiency virus types 1 and 2 journal, September 2003

Effects of nucleic acid local structure and magnesium ions on minus-strand transfer mediated by the nucleic acid chaperone activity of HIV-1 nucleocapsid protein journal, June 2007

The structural biology of HIV assembly journal, April 2008

New Structure Sheds Light on Selective HIV-1 Genomic RNA Packaging journal, August 2015

Zinc finger function of HIV-1 nucleocapsid protein is required for removal of 5′-terminal genomic RNA fragments: A paradigm for RNA removal reactions in HIV-1 reverse transcription journal, February 2013

Site-selective probing of cTAR destabilization highlights the necessary plasticity of the HIV-1 nucleocapsid protein to chaperone the first strand transfer journal, March 2013

Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) journal, July 2009

Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS) journal, May 1983

Similarities and differences in the nucleic acid chaperone activity of HIV-2 and HIV-1 nucleocapsid proteins in vitro journal, July 2014

Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates journal, January 1987

Cross-species transmission of simian retroviruses: how and why they could lead to the emergence of new diseases in the human population journal, January 2012

Comparison of SIV and HIV-1 Genomic RNA Structures Reveals Impact of Sequence Evolution on Conserved and Non-Conserved Structural Motifs journal, April 2013

Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins
journal, January 2006

Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus
journal, June 1990

Optical tweezers experiments resolve distinct modes of DNA-protein binding
journal, April 2009

Initiation of HIV Reverse Transcription
journal, January 2010

Targeted binding of nucleocapsid protein transforms the folding landscape of HIV-1 TAR RNA
journal, October 2015

Aromatic residue mutations reveal direct correlation between HIV-1 nucleocapsid protein's nucleic acid chaperone activity and retroviral replication
journal, February 2013

Kuru experiments triggered the emergence of pathogenic SIVmac
journal, January 2006

Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription
journal, November 2010

Nucleocapsid Protein Zinc-Finger Mutants of Simian Immunodeficiency Virus Strain Mne Produce Virions That Are Replication Defectivein Vitroandin Vivo
journal, January 1999

Preparation of Recombinant HIV-1 Gag Protein and Assembly of Virus-Like Particles In Vitro
book, January 2009

Distinct nucleic acid interaction properties of HIV-1 nucleocapsid protein precursor NCp15 explain reduced viral infectivity
journal, May 2014

Identification of a Minimal Region of the HIV-1 5′-Leader Required for RNA Dimerization, NC Binding, and Packaging
journal, March 2012

Distinct binding interactions of HIV-1 Gag to Psi and non-Psi RNAs: Implications for viral genomic RNA packaging
journal, June 2013

A protein ballet around the viral genome orchestrated by HIV-1 reverse transcriptase leads to an architectural switch: From nucleocapsid-condensed RNA to Vpr-bridged DNA
journal, February 2013

Fluorescence Anisotropy-Based Salt-Titration Approach to Characterize Protein–Nucleic Acid Interactions
book, December 2014

Origins of HIV and the AIDS Pandemic
journal, September 2011

HIV-1 Protease and Reverse Transcriptase Control the Architecture of Their Nucleocapsid Partner
journal, August 2007

A Guanosine-Centric Mechanism for RNA Chaperone Function
journal, March 2013

The matrix domain contributes to the nucleic acid chaperone activity of HIV-2 Gag
journal, March 2016

Hybrid Origin of SIV in Chimpanzees
journal, June 2003

Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS
journal, May 1984

Visualizing the Formation and Collapse of DNA Toroids
journal, May 2010

Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS
journal, May 1984

The Simian Immunodeficiency Virus 5′ Untranslated Leader Sequence Plays a Role in Intracellular Viral Protein Accumulation and in RNA Packaging
journal, June 2003

Rapid Kinetics of Protein–Nucleic Acid Interaction is a Major Component of HIV-1 Nucleocapsid Protein’s Nucleic Acid Chaperone Function
journal, November 2006

On the Selective Packaging of Genomic RNA by HIV-1
journal, September 2016

The Choreography of HIV-1 Proteolytic Processing and Virion Assembly
journal, October 2012

Lentivirus Vectors Using Human and Simian Immunodeficiency Virus Elements
journal, April 1999

High-Throughput SAXS for the Characterization of Biomolecules in Solution: A Practical Approach
book, October 2013

NMR Structure of the 101-nucleotide Core Encapsidation Signal of the Moloney Murine Leukemia Virus
journal, March 2004

International AIDS Society global scientific strategy: towards an HIV cure 2016
journal, July 2016

Alteration of Nucleic Acid Structure and Stability Modulates the Efficiency of Minus-Strand Transfer Mediated by the HIV-1 Nucleocapsid Protein
journal, July 2004

Orchestrating the Selection and Packaging of Genomic RNA by Retroviruses: An Ensemble of Viral and Host Factors
journal, September 2016

Functional Equivalence of Retroviral MA Domains in Facilitating Psi RNA Binding Specificity by Gag
journal, September 2016

New Paradigms for HIV/AIDS Vaccine Development
journal, February 2012

Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus
journal, September 2004

Conserved determinants of lentiviral genome dimerization
journal, September 2015

Biophysical studies of the nucleic acid chaperone properties of the HIV-1 nucleocapsid protein
journal, November 2010

Macaques Infected with Cloned Simian Immunodeficiency Virus Show RecurringnefGene Alterations
journal, September 1998

Differential contribution of basic residues to HIV-1 nucleocapsid protein’s nucleic acid chaperone function and retroviral replication
journal, November 2013

Human infection by genetically diverse SIVSM-related HIV-2 in West Africa
journal, August 1992

Fundamental differences between the nucleic acid chaperone activities of HIV-1 nucleocapsid protein and Gag or Gag-derived proteins: Biological implications
journal, September 2010

Initiation of HIV-1 reverse transcription and functional role of nucleocapsid-mediated tRNA/viral genome interactions
journal, November 2012

Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strong-stop DNA.
journal, January 1997

Retrospective on the all-in-one retroviral nucleocapsid protein
journal, November 2014

Specific recognition of the HIV-1 genomic RNA by the Gag precursor
journal, July 2014

Structure of the HIV-1 RNA packaging signal
journal, May 2015

Flexible Nature and Specific Functions of the HIV-1 Nucleocapsid Protein
journal, July 2011

The Complete Nucleotide Sequence of a Pathogenic Molecular Clone of Simian Immunodeficiency Virus
journal, November 1990

Molecular mimicry of human tRNALys anti-codon domain by HIV-1 RNA genome facilitates tRNA primer annealing
journal, December 2012

Nucleic Acid Binding Properties of the Simian Immunodeficiency Virus Nucleocapsid Protein NCp8
journal, March 2000

Impaired RNA incorporation and dimerization in live attenuated leader-variants of SIVmac239
journal, December 2006

Single aromatic residue location alters nucleic acid binding and chaperone function of FIV nucleocapsid protein
journal, November 2014

Defects in Primer-Template Binding, Processive DNA Synthesis, and RNase H Activity Associated with Chimeric Reverse Transcriptases Having the Murine Leukemia Virus Polymerase Domain Joined to Escherichia coli RNase H
journal, April 1995

Chimpanzee Reservoirs of Pandemic and Nonpandemic HIV-1
journal, July 2006

HIV Gag polyprotein: processing and early viral particle assembly
journal, March 2013

Isolation of a new human retrovirus from West African patients with AIDS
journal, July 1986

Nucleic Acid Chaperone Activity of HIV‐1 Nucleocapsid Protein: Critical Role in Reverse Transcription and Molecular Mechanism
book, January 2005

Small-angle X-ray scattering-derived structure of the HIV-1 5′ UTR reveals 3D tRNA mimicry
journal, February 2014

Requirements for efficient minus strand strong-stop DNA transfer in human immunodeficiency virus 1
journal, March 2011

An African primate lentivirus (SIVsmclosely related to HIV-2
journal, June 1989

Solution Structure of the Rous Sarcoma Virus Nucleocapsid Protein: μΨ RNA Packaging Signal Complex
journal, January 2007

Identification of unique reciprocal and non reciprocal cross packaging relationships between HIV-1, HIV-2 and SIV reveals an efficient SIV/HIV-2 lentiviral vector system with highly favourable features for in vivo testing and clinical usage
journal, September 2005

X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution
journal, August 2007

The packaging signal of simian immunodeficiency virus is upstream of the major splice donor at a distance from the RNA cap site similar to that of human immunodeficiency virus types 1 and 2
journal, September 2003

Effects of nucleic acid local structure and magnesium ions on minus-strand transfer mediated by the nucleic acid chaperone activity of HIV-1 nucleocapsid protein
journal, June 2007

The structural biology of HIV assembly
journal, April 2008

New Structure Sheds Light on Selective HIV-1 Genomic RNA Packaging
journal, August 2015

Zinc finger function of HIV-1 nucleocapsid protein is required for removal of 5′-terminal genomic RNA fragments: A paradigm for RNA removal reactions in HIV-1 reverse transcription
journal, February 2013

Site-selective probing of cTAR destabilization highlights the necessary plasticity of the HIV-1 nucleocapsid protein to chaperone the first strand transfer
journal, March 2013

Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS)
journal, July 2009

Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS)
journal, May 1983

Similarities and differences in the nucleic acid chaperone activity of HIV-2 and HIV-1 nucleocapsid proteins in vitro
journal, July 2014

Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates
journal, January 1987

Cross-species transmission of simian retroviruses: how and why they could lead to the emergence of new diseases in the human population
journal, January 2012

Comparison of SIV and HIV-1 Genomic RNA Structures Reveals Impact of Sequence Evolution on Conserved and Non-Conserved Structural Motifs
journal, April 2013

Comparative Structural Effects of HIV-1 Gag and Nucleocapsid Proteins in Binding to and Unwinding of the Viral RNA Packaging Signal
journal, April 2012

First Glimpses at Structure-function Relationships of the Nucleocapsid Protein of Retroviruses
journal, December 1995

Single-molecule stretching studies of RNA chaperones
journal, November 2010

Structural features in TAR RNA of human and simian immunodeficiency viruses: a phylogenetic analysis
journal, January 1992