C-terminal DxD-containing sequences within paramyxovirus nucleocapsid proteins determine matrix protein compatibility and can direct foreign proteins into budding particles

Greeshma Ray, Phuong Tieu Schmitt, Anthony Paul Schmitt

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Paramyxovirus particles are formed by a budding process coordinated by viral matrix (M) proteins. Mproteins coalesce at sites underlying infected cell membranes and induce other viral components, including viral glycoproteins and viral ribonucleoprotein complexes (vRNPs), to assemble at these locations from which particles bud. Mproteins interact with the nucleocapsid (NP or N) components of vRNPs, and these interactions enable production of infectious, genome-containing virions. For the paramyxoviruses parainfluenza virus 5 (PIV5) and mumps virus, M-NP interaction also contributes to efficient production of virus-like particles (VLPs) in transfected cells. A DLD sequence near the C-terminal end of PIV5 NP protein was previously found to be necessary for M-NP interaction and efficient VLP production. Here, we demonstrate that 15-residue-long, DLDcontaining sequences derived from either the PIV5 or Nipah virus nucleocapsid protein C-terminal ends are sufficient to direct packaging of a foreign protein, Renilla luciferase, into budding VLPs. Mumps virus NP protein harborsDWDin place of the DLD sequence found in PIV5 NP protein, and consequently, PIV5 NP protein is incompatible with mumps virusMprotein. A single amino acid change converting DLD toDWDwithin PIV5 NP protein induced compatibility between these proteins and allowed efficient production of mumps VLPs. Our data suggest a model in which paramyxoviruses share an overall common strategy for directing M-NP interactions but with important variations contained within DLD-like sequences that play key roles in defining M/NP protein compatibilities.

Original languageEnglish (US)
Pages (from-to)3650-3660
Number of pages11
JournalJournal of virology
Volume90
Issue number7
DOIs
StatePublished - Jan 1 2016

Fingerprint

nucleocapsid proteins
Respirovirus
Nucleocapsid Proteins
Parainfluenza virus 5
Parainfluenza Virus 5
Virion
Mumps virus
virus-like particles
Proteins
Viral Matrix Proteins
proteins
Viral Structures
Ribonucleoproteins
ribonucleoproteins
Nipah Virus
Renilla Luciferases
Nipah virus
Nucleocapsid
Mumps
nucleocapsid

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Immunology
  • Insect Science
  • Virology

Cite this

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title = "C-terminal DxD-containing sequences within paramyxovirus nucleocapsid proteins determine matrix protein compatibility and can direct foreign proteins into budding particles",
abstract = "Paramyxovirus particles are formed by a budding process coordinated by viral matrix (M) proteins. Mproteins coalesce at sites underlying infected cell membranes and induce other viral components, including viral glycoproteins and viral ribonucleoprotein complexes (vRNPs), to assemble at these locations from which particles bud. Mproteins interact with the nucleocapsid (NP or N) components of vRNPs, and these interactions enable production of infectious, genome-containing virions. For the paramyxoviruses parainfluenza virus 5 (PIV5) and mumps virus, M-NP interaction also contributes to efficient production of virus-like particles (VLPs) in transfected cells. A DLD sequence near the C-terminal end of PIV5 NP protein was previously found to be necessary for M-NP interaction and efficient VLP production. Here, we demonstrate that 15-residue-long, DLDcontaining sequences derived from either the PIV5 or Nipah virus nucleocapsid protein C-terminal ends are sufficient to direct packaging of a foreign protein, Renilla luciferase, into budding VLPs. Mumps virus NP protein harborsDWDin place of the DLD sequence found in PIV5 NP protein, and consequently, PIV5 NP protein is incompatible with mumps virusMprotein. A single amino acid change converting DLD toDWDwithin PIV5 NP protein induced compatibility between these proteins and allowed efficient production of mumps VLPs. Our data suggest a model in which paramyxoviruses share an overall common strategy for directing M-NP interactions but with important variations contained within DLD-like sequences that play key roles in defining M/NP protein compatibilities.",
author = "Greeshma Ray and Schmitt, {Phuong Tieu} and Schmitt, {Anthony Paul}",
year = "2016",
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T1 - C-terminal DxD-containing sequences within paramyxovirus nucleocapsid proteins determine matrix protein compatibility and can direct foreign proteins into budding particles

AU - Ray, Greeshma

AU - Schmitt, Phuong Tieu

AU - Schmitt, Anthony Paul

PY - 2016/1/1

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N2 - Paramyxovirus particles are formed by a budding process coordinated by viral matrix (M) proteins. Mproteins coalesce at sites underlying infected cell membranes and induce other viral components, including viral glycoproteins and viral ribonucleoprotein complexes (vRNPs), to assemble at these locations from which particles bud. Mproteins interact with the nucleocapsid (NP or N) components of vRNPs, and these interactions enable production of infectious, genome-containing virions. For the paramyxoviruses parainfluenza virus 5 (PIV5) and mumps virus, M-NP interaction also contributes to efficient production of virus-like particles (VLPs) in transfected cells. A DLD sequence near the C-terminal end of PIV5 NP protein was previously found to be necessary for M-NP interaction and efficient VLP production. Here, we demonstrate that 15-residue-long, DLDcontaining sequences derived from either the PIV5 or Nipah virus nucleocapsid protein C-terminal ends are sufficient to direct packaging of a foreign protein, Renilla luciferase, into budding VLPs. Mumps virus NP protein harborsDWDin place of the DLD sequence found in PIV5 NP protein, and consequently, PIV5 NP protein is incompatible with mumps virusMprotein. A single amino acid change converting DLD toDWDwithin PIV5 NP protein induced compatibility between these proteins and allowed efficient production of mumps VLPs. Our data suggest a model in which paramyxoviruses share an overall common strategy for directing M-NP interactions but with important variations contained within DLD-like sequences that play key roles in defining M/NP protein compatibilities.

AB - Paramyxovirus particles are formed by a budding process coordinated by viral matrix (M) proteins. Mproteins coalesce at sites underlying infected cell membranes and induce other viral components, including viral glycoproteins and viral ribonucleoprotein complexes (vRNPs), to assemble at these locations from which particles bud. Mproteins interact with the nucleocapsid (NP or N) components of vRNPs, and these interactions enable production of infectious, genome-containing virions. For the paramyxoviruses parainfluenza virus 5 (PIV5) and mumps virus, M-NP interaction also contributes to efficient production of virus-like particles (VLPs) in transfected cells. A DLD sequence near the C-terminal end of PIV5 NP protein was previously found to be necessary for M-NP interaction and efficient VLP production. Here, we demonstrate that 15-residue-long, DLDcontaining sequences derived from either the PIV5 or Nipah virus nucleocapsid protein C-terminal ends are sufficient to direct packaging of a foreign protein, Renilla luciferase, into budding VLPs. Mumps virus NP protein harborsDWDin place of the DLD sequence found in PIV5 NP protein, and consequently, PIV5 NP protein is incompatible with mumps virusMprotein. A single amino acid change converting DLD toDWDwithin PIV5 NP protein induced compatibility between these proteins and allowed efficient production of mumps VLPs. Our data suggest a model in which paramyxoviruses share an overall common strategy for directing M-NP interactions but with important variations contained within DLD-like sequences that play key roles in defining M/NP protein compatibilities.

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