Structure, function and dynamics in adenovirus maturation

Mangel, Walter F.; San Martín, Carmen

doi:10.3390/v6114536

Title: Structure, function and dynamics in adenovirus maturation

Abstract

Here we review the current knowledge on maturation of adenovirus, a non-enveloped icosahedral eukaryotic virus. The adenovirus dsDNA genome fills the capsid in complex with a large amount of histone-like viral proteins, forming the core. Maturation involves proteolytic cleavage of several capsid and core precursor proteins by the viral protease (AVP). AVP uses a peptide cleaved from one of its targets as a “molecular sled” to slide on the viral genome and reach its substrates, in a remarkable example of one-dimensional chemistry. Immature adenovirus containing the precursor proteins lacks infectivity because of its inability to uncoat. The immature core is more compact and stable than the mature one, due to the condensing action of unprocessed core polypeptides; shell precursors underpin the vertex region and the connections between capsid and core. Maturation makes the virion metastable, priming it for stepwise uncoating by facilitating vertex release and loosening the condensed genome and its attachment to the icosahedral shell. The packaging scaffold protein L1 52/55k is also a substrate for AVP. Proteolytic processing of L1 52/55k disrupts its interactions with other virion components, providing a mechanism for its removal during maturation. In conclusion, possible roles for maturation of the terminal protein are discussed.

Authors:

Mangel, Walter F. ^[1]; San Martín, Carmen ^[2]

Brookhaven National Lab. (BNL), Upton, NY (United States)
Centro Nacional de Biotechnologica, Madrid (Spain)

Publication Date:: Fri Nov 21 00:00:00 EST 2014

Research Org.:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Org.:: National Institutes of Health (NIH)

OSTI Identifier:: 1167152

Report Number(s):: BNL-107242-2014-JA
Journal ID: ISSN 1999-4915; VIRUBR; 400412000

Grant/Contract Number:: SC00112704

Resource Type:: Accepted Manuscript

Journal Name:: Viruses

Additional Journal Information:: Journal Volume: 6; Journal Issue: 11; Journal ID: ISSN 1999-4915

Publisher:: MDPI

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; protease; DNA sliding; virus stability; uncoating; adenovirus; infectivity

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                    Mangel, Walter F., and San Martín, Carmen. Structure, function and dynamics in adenovirus maturation.  United States: N. p., 2014. 
Web.  doi:10.3390/v6114536.

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                    Mangel, Walter F., & San Martín, Carmen. Structure, function and dynamics in adenovirus maturation.  United States.  https://doi.org/10.3390/v6114536

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                    Mangel, Walter F., and San Martín, Carmen. Fri .  
"Structure, function and dynamics in adenovirus maturation".  United States.  https://doi.org/10.3390/v6114536.  https://www.osti.gov/servlets/purl/1167152.

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@article{osti_1167152,

  title        = {Structure, function and dynamics in adenovirus maturation},

  author       = {Mangel, Walter F. and San Martín, Carmen},

  abstractNote = {Here we review the current knowledge on maturation of adenovirus, a non-enveloped icosahedral eukaryotic virus. The adenovirus dsDNA genome fills the capsid in complex with a large amount of histone-like viral proteins, forming the core. Maturation involves proteolytic cleavage of several capsid and core precursor proteins by the viral protease (AVP). AVP uses a peptide cleaved from one of its targets as a “molecular sled” to slide on the viral genome and reach its substrates, in a remarkable example of one-dimensional chemistry. Immature adenovirus containing the precursor proteins lacks infectivity because of its inability to uncoat. The immature core is more compact and stable than the mature one, due to the condensing action of unprocessed core polypeptides; shell precursors underpin the vertex region and the connections between capsid and core. Maturation makes the virion metastable, priming it for stepwise uncoating by facilitating vertex release and loosening the condensed genome and its attachment to the icosahedral shell. The packaging scaffold protein L1 52/55k is also a substrate for AVP. Proteolytic processing of L1 52/55k disrupts its interactions with other virion components, providing a mechanism for its removal during maturation. In conclusion, possible roles for maturation of the terminal protein are discussed.},

  doi          = {10.3390/v6114536},

  journal      = {Viruses},

  number       = 11,

  volume       = 6,

  place        = {United States},

  year         = {Fri Nov 21 00:00:00 EST 2014},

  month        = {Fri Nov 21 00:00:00 EST 2014}

}

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Title: Structure, function and dynamics in adenovirus maturation

Abstract

Citation Formats

Adenovirus Composition, Proteolysis, and Disassembly Studied by In-depth Qualitative and Quantitative Proteomics journal, March 2014

The structure of nucleoprotein cores released from adenovirions journal, January 1983

Biological and Structural Studies with an Adenovirus Type 2 Temperature-Sensitive Mutant Defective for Uncoating journal, January 1983

The active adenovirus protease is the intact L3 23K protein journal, July 1993

Infectious Adenovirus Type 2 Transport Through Early but not Late Endosomes journal, December 2008

Discovery of a new inhibitor lead of adenovirus proteinase: steps toward selective, irreversible inhibitors of cysteine proteinases journal, August 2001

DNA Binding Provides a Molecular Strap Activating the Adenovirus Proteinase journal, June 2004

Structure of adenovirus chromatin journal, January 1982

Current Issues and Future Directions of Oncolytic Adenoviruses journal, February 2010

Accurate single-day titration of adenovirus vectors based on equivalence of protein VII nuclear dots and infectious particles journal, August 2009

Identification of proteins and protein domains that contact DNA within adenovirus nucleoprotein cores by ultraviolet light crosslinking of oligonucleotides 32P-labelled in vivo journal, March 1986

Technical Reports: Mapping a Functional Viral Protein in Solution Using Synchrotron X-ray Footprinting Technology journal, January 2005

Nonspecifically bound proteins spin while diffusing along DNA journal, November 2009

Drifting Motions of the Adenovirus Receptor CAR and Immobile Integrins Initiate Virus Uncoating and Membrane Lytic Protein Exposure journal, August 2011

Rhodamine-based compounds as fluorogenic substrates for serine proteinases journal, February 1983

Identification of a protein linked to the ends of adenovirus DNA journal, June 1977

Role of preterminal protein processing in adenovirus replication. journal, January 1997

Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: II. ADENOVIRUS PROTEINASE IS ACTIVATED IN AN UNUSUAL ONE-DIMENSIONAL BIOCHEMICAL REACTION journal, October 2012

Reduced Infectivity of Adenovirus Type 5 Particles and Degradation of Entering Viral Genomes Associated with Incomplete Processing of the Preterminal Protein journal, October 2012

Characterization of Three Components of Human Adenovirus Proteinase Activity in Vitro journal, January 1996

Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: I. BINDING TO DNA AND TO HEXON OF THE PRECURSOR TO PROTEIN VI, pVI, OF HUMAN ADENOVIRUS journal, October 2012

Interaction of the adenovirus major core protein precursor, pVII, with the viral DNA packaging machinery journal, April 2005

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

New Insights on Adenovirus as Vaccine Vectors journal, August 2009

Molecular composition of the adenovirus type 2 virion. journal, January 1985

Viral DNA and a viral peptide can act as cofactors of adenovirus virion proteinase activity journal, January 1993

Integrins αvβ3 and αvβ5 promote adenovirus internalization but not virus attachment journal, April 1993

Adenovirus receptors: implications for targeting of viral vectors journal, August 2012

Poliovirus Cell Entry: Common Structural Themes in Viral Cell Entry Pathways journal, October 2002

Characterization of Empty Adenovirus Particles Assembled in the Absence of a Functional Adenovirus IVa2 Protein journal, March 2011

Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: III. ATOMIC RESOLUTION STRUCTURE OF THE NASCENT FORM OF THE ADENOVIRUS PROTEINASE journal, October 2012

In the Virion, the 11-Amino-Acid Peptide Cofactor pVIc Is Covalently Linked to the Adenovirus Proteinase journal, May 2002

Encapsidation of Viral DNA Requires the Adenovirus L1 52/55-Kilodalton Protein journal, October 1998

Adenovirus Infections in Human Immunodeficiency Virus-Positive Patients: Clinical Features and Molecular Epidemiology journal, September 1995

The adenovirus protease is activated by a virus-coded disulphide-linked peptide journal, January 1993

Respiratory Diseases among U.S. Military Personnel: Countering Emerging Threats journal, June 1999

Organization of the Avian Adenovirus Genome and the Structure of Its Endopeptidase journal, September 1993

Interaction of the Human Adenovirus Proteinase with Its 11-Amino Acid Cofactor pVIc † journal, October 2001

The role of the nuclear pore complex in adenovirus DNA entry journal, October 1997

T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton journal, September 2000

Different modes of inhibition of human adenovirus proteinase, probably a cysteine proteinase, by bovine pancreatic trypsin inhibitor journal, June 1996

An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature journal, June 2010

Localization of the N-Terminus of Minor Coat Protein IIIa in the Adenovirus Capsid journal, November 2008

Microtubule-dependent Plus- and Minus End–directed Motilities Are Competing Processes for Nuclear Targeting of Adenovirus journal, February 1999

Characterization of the Adenovirus Proteinase: Development and Use of a Specific Peptide Assay journal, December 1989

A precursor terminal protein-trinucleotide intermediate during initiation of adenovirus DNA replication: regeneration of molecular ends in vitro by a jumping back mechanism. journal, December 1994

Modern Biomolecular Mass Spectrometry and its Role in Studying Virus Structure, Dynamics, and Assembly journal, July 2011

Infectious Adenovirus Type 2 Transport Through Early but not Late Endosomes journal, December 2008

The Role of Capsid Maturation on Adenovirus Priming for Sequential Uncoating journal, July 2012

Adenovirus Structural Protein IIIa Is Involved in the Serotype Specificity of Viral DNA Packaging journal, June 2011

Interaction of the adenovirus major core protein precursor, pVII, with the viral DNA packaging machinery journal, April 2005

Anatomy of hot spots in protein interfaces journal, July 1998

Characterization of the Adenovirus Proteinase: Development and Use of a Specific Peptide Assay journal, December 1989

Respiratory Diseases among U.S. Military Personnel: Countering Emerging Threats journal, June 1999

New Insights on Adenovirus as Vaccine Vectors journal, August 2009

Role of the nuclear matrix in adenovirus maturation journal, June 1986

Gene and mRNA for precursor polypeptide VI from adenovirus type 2. journal, January 1981

Monitoring dynamics of human adenovirus disassembly induced by mechanical fatigue journal, March 2013

An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature journal, June 2010

Adenoviruses: update on structure and function journal, January 2009

Virus Maturation journal, June 2012

Current Issues and Future Directions of Oncolytic Adenoviruses journal, February 2010

Interaction of the Adenovirus Proteinase with Protein Cofactors with High Negative Charge Densities † journal, June 2005

Isolation and properties of adenovirus type 2 proteinase. journal, January 1993

Cleavage Efficiency by Adenovirus Protease Is Site-dependent journal, December 1996

The polypeptides of adenovirus journal, February 1974

Different modes of inhibition of human adenovirus proteinase, probably a cysteine proteinase, by bovine pancreatic trypsin inhibitor journal, June 1996

Structure and Uncoating of Immature Adenovirus journal, September 2009

Progressive reorganization of the host cell cytoskeleton during adenovirus infection. journal, January 1986

First generation inhibitors of the adenovirus proteinase journal, May 2013

The adenovirus L3 23-kilodalton proteinase cleaves the amino-terminal head domain from cytokeratin 18 and disrupts the cytokeratin network of HeLa cells. journal, January 1993

Adenovirus Transport via Direct Interaction of Cytoplasmic Dynein with the Viral Capsid Hexon Subunit journal, December 2009

The Cleaved N-Terminus of pVI Binds Peripentonal Hexons in Mature Adenovirus journal, May 2014

Subtilisin. Stereochemical mechanism involving transition-state stabilization journal, November 1972

Binding of chloromethyl ketone substrate analogs to crystalline papain journal, August 1976

Infections in 18, 000 Infants and Children in a Controlled Study of Respiratory Tract Disease. i. Adenovirus Pathogenicity in Relation to Serologic type and Illness Syndrome1 journal, December 1969

Poliovirus Cell Entry: Common Structural Themes in Viral Cell Entry Pathways journal, October 2002

Adenovirus Composition, Proteolysis, and Disassembly Studied by In-depth Qualitative and Quantitative Proteomics
journal, March 2014

The structure of nucleoprotein cores released from adenovirions
journal, January 1983

Biological and Structural Studies with an Adenovirus Type 2 Temperature-Sensitive Mutant Defective for Uncoating
journal, January 1983

The active adenovirus protease is the intact L3 23K protein
journal, July 1993

Infectious Adenovirus Type 2 Transport Through Early but not Late Endosomes
journal, December 2008

Discovery of a new inhibitor lead of adenovirus proteinase: steps toward selective, irreversible inhibitors of cysteine proteinases
journal, August 2001

DNA Binding Provides a Molecular Strap Activating the Adenovirus Proteinase
journal, June 2004

Structure of adenovirus chromatin
journal, January 1982

Current Issues and Future Directions of Oncolytic Adenoviruses
journal, February 2010

Accurate single-day titration of adenovirus vectors based on equivalence of protein VII nuclear dots and infectious particles
journal, August 2009

Identification of proteins and protein domains that contact DNA within adenovirus nucleoprotein cores by ultraviolet light crosslinking of oligonucleotides 32P-labelled in vivo
journal, March 1986

Technical Reports: Mapping a Functional Viral Protein in Solution Using Synchrotron X-ray Footprinting Technology
journal, January 2005

Nonspecifically bound proteins spin while diffusing along DNA
journal, November 2009

Drifting Motions of the Adenovirus Receptor CAR and Immobile Integrins Initiate Virus Uncoating and Membrane Lytic Protein Exposure
journal, August 2011

Rhodamine-based compounds as fluorogenic substrates for serine proteinases
journal, February 1983

Identification of a protein linked to the ends of adenovirus DNA
journal, June 1977

Role of preterminal protein processing in adenovirus replication.
journal, January 1997

Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: II. ADENOVIRUS PROTEINASE IS ACTIVATED IN AN UNUSUAL ONE-DIMENSIONAL BIOCHEMICAL REACTION
journal, October 2012

Reduced Infectivity of Adenovirus Type 5 Particles and Degradation of Entering Viral Genomes Associated with Incomplete Processing of the Preterminal Protein
journal, October 2012

Characterization of Three Components of Human Adenovirus Proteinase Activity in Vitro
journal, January 1996

Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: I. BINDING TO DNA AND TO HEXON OF THE PRECURSOR TO PROTEIN VI, pVI, OF HUMAN ADENOVIRUS
journal, October 2012

Interaction of the adenovirus major core protein precursor, pVII, with the viral DNA packaging machinery
journal, April 2005

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

New Insights on Adenovirus as Vaccine Vectors
journal, August 2009

Molecular composition of the adenovirus type 2 virion.
journal, January 1985

Viral DNA and a viral peptide can act as cofactors of adenovirus virion proteinase activity
journal, January 1993

Integrins αvβ3 and αvβ5 promote adenovirus internalization but not virus attachment
journal, April 1993

Adenovirus receptors: implications for targeting of viral vectors
journal, August 2012

Poliovirus Cell Entry: Common Structural Themes in Viral Cell Entry Pathways
journal, October 2002

Characterization of Empty Adenovirus Particles Assembled in the Absence of a Functional Adenovirus IVa2 Protein
journal, March 2011

Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: III. ATOMIC RESOLUTION STRUCTURE OF THE NASCENT FORM OF THE ADENOVIRUS PROTEINASE
journal, October 2012

In the Virion, the 11-Amino-Acid Peptide Cofactor pVIc Is Covalently Linked to the Adenovirus Proteinase
journal, May 2002

Encapsidation of Viral DNA Requires the Adenovirus L1 52/55-Kilodalton Protein
journal, October 1998

Adenovirus Infections in Human Immunodeficiency Virus-Positive Patients: Clinical Features and Molecular Epidemiology
journal, September 1995

The adenovirus protease is activated by a virus-coded disulphide-linked peptide
journal, January 1993

Respiratory Diseases among U.S. Military Personnel: Countering Emerging Threats
journal, June 1999

Organization of the Avian Adenovirus Genome and the Structure of Its Endopeptidase
journal, September 1993

Interaction of the Human Adenovirus Proteinase with Its 11-Amino Acid Cofactor pVIc ^†
journal, October 2001

The role of the nuclear pore complex in adenovirus DNA entry
journal, October 1997

T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton
journal, September 2000

Different modes of inhibition of human adenovirus proteinase, probably a cysteine proteinase, by bovine pancreatic trypsin inhibitor
journal, June 1996

An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature
journal, June 2010

Localization of the N-Terminus of Minor Coat Protein IIIa in the Adenovirus Capsid
journal, November 2008

Microtubule-dependent Plus- and Minus End–directed Motilities Are Competing Processes for Nuclear Targeting of Adenovirus
journal, February 1999

Characterization of the Adenovirus Proteinase: Development and Use of a Specific Peptide Assay
journal, December 1989

A precursor terminal protein-trinucleotide intermediate during initiation of adenovirus DNA replication: regeneration of molecular ends in vitro by a jumping back mechanism.
journal, December 1994

Modern Biomolecular Mass Spectrometry and its Role in Studying Virus Structure, Dynamics, and Assembly
journal, July 2011

Infectious Adenovirus Type 2 Transport Through Early but not Late Endosomes
journal, December 2008

The Role of Capsid Maturation on Adenovirus Priming for Sequential Uncoating
journal, July 2012

Adenovirus Structural Protein IIIa Is Involved in the Serotype Specificity of Viral DNA Packaging
journal, June 2011

Interaction of the adenovirus major core protein precursor, pVII, with the viral DNA packaging machinery
journal, April 2005

Anatomy of hot spots in protein interfaces
journal, July 1998

Characterization of the Adenovirus Proteinase: Development and Use of a Specific Peptide Assay
journal, December 1989

Respiratory Diseases among U.S. Military Personnel: Countering Emerging Threats
journal, June 1999

New Insights on Adenovirus as Vaccine Vectors
journal, August 2009

Role of the nuclear matrix in adenovirus maturation
journal, June 1986

Gene and mRNA for precursor polypeptide VI from adenovirus type 2.
journal, January 1981

Monitoring dynamics of human adenovirus disassembly induced by mechanical fatigue
journal, March 2013

An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature
journal, June 2010

Adenoviruses: update on structure and function
journal, January 2009

Virus Maturation
journal, June 2012

Current Issues and Future Directions of Oncolytic Adenoviruses
journal, February 2010

Interaction of the Adenovirus Proteinase with Protein Cofactors with High Negative Charge Densities ^†
journal, June 2005

Isolation and properties of adenovirus type 2 proteinase.
journal, January 1993

Cleavage Efficiency by Adenovirus Protease Is Site-dependent
journal, December 1996

The polypeptides of adenovirus
journal, February 1974

Different modes of inhibition of human adenovirus proteinase, probably a cysteine proteinase, by bovine pancreatic trypsin inhibitor
journal, June 1996

Structure and Uncoating of Immature Adenovirus
journal, September 2009

Progressive reorganization of the host cell cytoskeleton during adenovirus infection.
journal, January 1986

First generation inhibitors of the adenovirus proteinase
journal, May 2013

The adenovirus L3 23-kilodalton proteinase cleaves the amino-terminal head domain from cytokeratin 18 and disrupts the cytokeratin network of HeLa cells.
journal, January 1993

Adenovirus Transport via Direct Interaction of Cytoplasmic Dynein with the Viral Capsid Hexon Subunit
journal, December 2009

The Cleaved N-Terminus of pVI Binds Peripentonal Hexons in Mature Adenovirus
journal, May 2014

Subtilisin. Stereochemical mechanism involving transition-state stabilization
journal, November 1972

Binding of chloromethyl ketone substrate analogs to crystalline papain
journal, August 1976

Infections in 18, 000 Infants and Children in a Controlled Study of Respiratory Tract Disease. i. Adenovirus Pathogenicity in Relation to Serologic type and Illness Syndrome1
journal, December 1969

Poliovirus Cell Entry: Common Structural Themes in Viral Cell Entry Pathways
journal, October 2002

Classification of single-projection reconstructions for cryo-electron microscopy data of icosahedral viruses
journal, July 2005

Genetic identification of a endoproteinase endoded by the adenovirus genome
journal, June 1983

Characterization of the Adenovirus Proteinase: Substrate Specificity
journal, December 1989