HIV-1 Gag co-opts a cellular complex containing DDX 6 , a helicase that facilitates capsid assembly

The Rockefeller University Press $30.00 J. Cell Biol. Vol. 198 No. 3 439–456 www.jcb.org/cgi/doi/10.1083/jcb.201111012 JCB 439 Correspondence to Jaisri R. Lingappa: jais@u.washington.edu Abbreviations used in this paper: AI, assembly intermediate; gRNA, genomic RNA; HFV, human foamy virus; HMW, high molecular weight; IEM, immunoelectron microscopy; IP, immunoprecipitation; KD, knockdown; LZ, leucine zipper; miRNA, microRNA; PB, processing body; PBP, PB protein; PM, plasma membrane; RCG, region of clustered Gag; RNP, ribonucleoprotein; VLP, viruslike particle; VS, velocity sedimentation; WB, Western blot; WT, wild type. Introduction

[1]  Stephan Wickles,et al.  Structural basis of highly conserved ribosome recycling in eukaryotes and archaea , 2012, Nature.

[2]  John H. Morris,et al.  Global landscape of HIV–human protein complexes , 2011, Nature.

[3]  Siok Ghee Ler,et al.  Quantitative mass spectrometry of DENV-2 RNA-interacting proteins reveals that the DEAD-box RNA helicase DDX6 binds the DB1 and DB2 3’ UTR structures , 2011, RNA biology.

[4]  M. Emerman,et al.  The DEAD-box RNA Helicase DDX6 is Required for Efficient Encapsidation of a Retroviral Genome , 2011, PLoS pathogens.

[5]  C. Lecellier,et al.  Retroviral GAG proteins recruit AGO2 on viral RNAs without affecting RNA accumulation and translation , 2011, Nucleic acids research.

[6]  Patrick Linder,et al.  From unwinding to clamping — the DEAD box RNA helicase family , 2011, Nature Reviews Molecular Cell Biology.

[7]  V. Chukkapalli,et al.  Molecular determinants that regulate plasma membrane association of HIV-1 Gag. , 2011, Journal of molecular biology.

[8]  Karin Musier-Forsyth,et al.  Diverse interactions of retroviral Gag proteins with RNAs. , 2011, Trends in biochemical sciences.

[9]  S. Neil,et al.  Host factors involved in retroviral budding and release , 2011, Nature Reviews Microbiology.

[10]  K. C. Klein,et al.  HIV Gag-Leucine Zipper Chimeras Form ABCE1-Containing Intermediates and RNase-Resistant Immature Capsids Similar to Those Formed by Wild-Type HIV-1 Gag , 2011, Journal of Virology.

[11]  P. Bieniasz,et al.  Analysis of the Initiating Events in HIV-1 Particle Assembly and Genome Packaging , 2010, PLoS pathogens.

[12]  S. Sandmeyer,et al.  Function of a retrotransposon nucleocapsid protein , 2010, RNA biology.

[13]  Narasimhan J. Venkatachari,et al.  P Body-Associated Protein Mov10 Inhibits HIV-1 Replication at Multiple Stages , 2010, Journal of Virology.

[14]  A. Telesnitsky,et al.  7SL RNA Is Retained in HIV-1 Minimal Virus-Like Particles as an S-Domain Fragment , 2010, Journal of Virology.

[15]  Chris M. Brown,et al.  Live cell visualization of the interactions between HIV-1 Gag and the cellular RNA-binding protein Staufen1 , 2010, Retrovirology.

[16]  E. Poeschla,et al.  Live-Cell Coimaging of the Genomic RNAs and Gag Proteins of Two Lentiviruses , 2010, Journal of Virology.

[17]  M. Curcio,et al.  5′ to 3′ mRNA Decay Factors Colocalize with Ty1 Gag and Human APOBEC3G and Promote Ty1 Retrotransposition , 2010, Journal of Virology.

[18]  W. Fu,et al.  Moloney Leukemia Virus 10 (MOV10) Protein Inhibits Retrovirus Replication* , 2010, The Journal of Biological Chemistry.

[19]  L. Ajamian,et al.  Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA , 2010, Journal of Cell Science.

[20]  P. Bieniasz,et al.  Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles , 2009, Proceedings of the National Academy of Sciences.

[21]  K. Nagashima,et al.  P-Body Components Are Required for Ty1 Retrotransposition during Assembly of Retrotransposition-Competent Virus-Like Particles , 2009, Molecular and Cellular Biology.

[22]  A. Noueiry,et al.  Translation and replication of hepatitis C virus genomic RNA depends on ancient cellular proteins that control mRNA fates , 2009, Proceedings of the National Academy of Sciences.

[23]  Hong Cao,et al.  Cellular microRNA and P bodies modulate host-HIV-1 interactions. , 2009, Molecular cell.

[24]  P. Bieniasz The cell biology of HIV-1 virion genesis. , 2009, Cell host & microbe.

[25]  R. Parker,et al.  Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. , 2009, Current opinion in cell biology.

[26]  M. A. Desbats,et al.  Mammalian Staufen 1 is recruited to stress granules and impairs their assembly , 2009, Journal of Cell Science.

[27]  Rachael M. Crist,et al.  Assembly Properties of Human Immunodeficiency Virus Type 1 Gag-Leucine Zipper Chimeras: Implications for Retrovirus Assembly , 2008, Journal of Virology.

[28]  Amy S. Espeseth,et al.  Genome-scale RNAi screen for host factors required for HIV replication. , 2008, Cell host & microbe.

[29]  R. König,et al.  Global Analysis of Host-Pathogen Interactions that Regulate Early-Stage HIV-1 Replication , 2008, Cell.

[30]  E. Koonin,et al.  Origins and evolution of eukaryotic RNA interference. , 2008, Trends in ecology & evolution.

[31]  Ruth R. Montgomery,et al.  RNA interference screen for human genes associated with West Nile virus infection , 2008, Nature.

[32]  Luc DesGroseillers,et al.  The host protein Staufen1 interacts with the Pr55Gag zinc fingers and regulates HIV-1 assembly via its N-terminus , 2008, Retrovirology.

[33]  C. Beckham,et al.  P bodies, stress granules, and viral life cycles. , 2008, Cell host & microbe.

[34]  J. Lieberman,et al.  Identification of Host Proteins Required for HIV Infection Through a Functional Genomic Screen , 2008, Science.

[35]  G. W. Hatfield,et al.  Ty3 Nucleocapsid Controls Localization of Particle Assembly , 2007, Journal of Virology.

[36]  G. Meister,et al.  Proteomic and functional analysis of Argonaute‐containing mRNA–protein complexes in human cells , 2007, EMBO reports.

[37]  N. Kato,et al.  DDX3 DEAD-Box RNA Helicase Is Required for Hepatitis C Virus RNA Replication , 2007, Journal of Virology.

[38]  Lorne W. Walker,et al.  T Cells Contain an RNase-Insensitive Inhibitor of APOBEC3G Deaminase Activity , 2007, PLoS pathogens.

[39]  Chris Sander,et al.  Cellular cofactors affecting hepatitis C virus infection and replication , 2007, Proceedings of the National Academy of Sciences.

[40]  G. W. Hatfield,et al.  Ty3 Capsid Mutations Reveal Early and Late Functions of the Amino-Terminal Domain , 2007, Journal of Virology.

[41]  L. Abrahamyan,et al.  The Host Protein Staufen1 Participates in Human Immunodeficiency Virus Type 1 Assembly in Live Cells by Influencing pr55Gag Multimerization , 2007, Journal of Virology.

[42]  Roy Parker,et al.  P bodies and the control of mRNA translation and degradation. , 2007, Molecular cell.

[43]  J. Lingappa,et al.  Host ABCE1 is at Plasma Membrane HIV Assembly Sites and Its Dissociation from Gag is Linked to Subsequent Events of Virus Production , 2007, Traffic.

[44]  T. Rana,et al.  Human Retroviral Host Restriction Factors APOBEC3G and APOBEC3F Localize to mRNA Processing Bodies , 2006, PLoS pathogens.

[45]  R. Parker,et al.  CAR-1 and Trailer hitch: driving mRNP granule function at the ER? , 2006, The Journal of cell biology.

[46]  N. Kedersha,et al.  RNA granules , 2006, The Journal of cell biology.

[47]  P. Kiser,et al.  Basic Residues in the Nucleocapsid Domain of Gag Are Required for Interaction of HIV-1 Gag with ABCE1 (HP68), a Cellular Protein Important for HIV-1 Capsid Assembly* , 2006, Journal of Biological Chemistry.

[48]  G. Lyons,et al.  CAR-1, a protein that localizes with the mRNA decapping component DCAP-1, is required for cytokinesis and ER organization in Caenorhabditis elegans embryos. , 2005, Molecular biology of the cell.

[49]  M. Buszczak,et al.  Efficient protein trafficking requires trailer hitch, a component of a ribonucleoprotein complex localized to the ER in Drosophila. , 2005, Developmental cell.

[50]  Pierre Baldi,et al.  Retroviruses and yeast retrotransposons use overlapping sets of host genes. , 2005, Genome research.

[51]  R. Parker,et al.  Processing bodies require RNA for assembly and contain nontranslating mRNAs. , 2005, RNA.

[52]  D. Pérez-Caballero,et al.  APOBEC3G Incorporation into Human Immunodeficiency Virus Type 1 Particles , 2004, Journal of Virology.

[53]  Nobutaka Hirokawa,et al.  Kinesin Transports RNA Isolation and Characterization of an RNA-Transporting Granule , 2004, Neuron.

[54]  M. Emerman,et al.  Capsid Is a Dominant Determinant of Retrovirus Infectivity in Nondividing Cells , 2004, Journal of Virology.

[55]  A. Gatignol,et al.  Identification of Staufen in the Human Immunodeficiency Virus Type 1 Gag Ribonucleoprotein Complex and a Role in Generating Infectious Viral Particles , 2004, Molecular and Cellular Biology.

[56]  J. Lingappa,et al.  Conservation of a Stepwise, Energy-Sensitive Pathway Involving HP68 for Assembly of Primate Lentivirus Capsids in Cells , 2004, Journal of Virology.

[57]  P. Ahlquist,et al.  Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Paul Ahlquist,et al.  Host Factors in Positive-Strand RNA Virus Genome Replication , 2003, Journal of Virology.

[59]  Circe W. Tsui,et al.  Functional genomics reveals relationships between the retrovirus-like Ty1 element and its host Saccharomyces cerevisiae. , 2003, Genetics.

[60]  Jianbo Chen,et al.  Yeast Lsm1p-7p/Pat1p Deadenylation-Dependent mRNA-Decapping Factors Are Required for Brome Mosaic Virus Genomic RNA Translation , 2003, Molecular and Cellular Biology.

[61]  Marc C. Johnson,et al.  Nucleic Acid-Independent Retrovirus Assembly Can Be Driven by Dimerization , 2002, Journal of Virology.

[62]  M. Carrington Faculty Opinions recommendation of Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. , 2002 .

[63]  Bonnie L. Firestein,et al.  Identification of a host protein essential for assembly of immature HIV-1 capsids , 2002, Nature.

[64]  Aalok R. Singh,et al.  Effect of mutations in Gag on assembly of immature human immunodeficiency virus type 1 capsids in a cell-free system. , 2001, Virology.

[65]  B. Strack,et al.  Efficient Particle Production by Minimal Gag Constructs Which Retain the Carboxy-Terminal Domain of Human Immunodeficiency Virus Type 1 Capsid-p2 and a Late Assembly Domain , 2000, Journal of Virology.

[66]  P. Ahlquist,et al.  Identification and characterization of a host protein required for efficient template selection in viral RNA replication. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[67]  E. Freed,et al.  Binding of Human Immunodeficiency Virus Type 1 Gag to Membrane: Role of the Matrix Amino Terminus , 1999, Journal of Virology.

[68]  A. Rein,et al.  In Vitro Assembly Properties of Human Immunodeficiency Virus Type 1 Gag Protein Lacking the p6 Domain , 1999, Journal of Virology.

[69]  E. Barklis,et al.  Analysis of the Assembly Function of the Human Immunodeficiency Virus Type 1 Gag Protein Nucleocapsid Domain , 1998, Journal of Virology.

[70]  M. Emerman,et al.  Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated beta-galactosidase gene , 1992, Journal of virology.

[71]  A. Smith,et al.  Human immunodeficiency virus type 1 Pr55gag and Pr160gag-pol expressed from a simian virus 40 late replacement vector are efficiently processed and assembled into viruslike particles , 1990, Journal of virology.

[72]  J. Sodroski,et al.  Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[73]  T. Connolly,et al.  Formation of a functional ribosome-membrane junction during translocation requires the participation of a GTP-binding protein , 1986, The Journal of cell biology.

[74]  C. Mcewen Tables for estimating sedimentation through linear concentration gradients of sucrose solution. , 1967, Analytical biochemistry.

[75]  Y. Lévy,et al.  Suppression of HIV-1 replication by microRNA effectors , 2009, Retrovirology.

[76]  C. Beckham,et al.  Virus-like particles of the Ty3 retrotransposon assemble in association with P-body components. , 2006, RNA.

[77]  Patrick Linder,et al.  Nucleic Acids Research Advance Access published August 26, 2006 SURVEY AND SUMMARY Dead-box proteins: a family affair—active and passive players in RNP-remodeling , 2006 .

[78]  L. Teysset,et al.  About the origin of retroviruses and the co-evolution of the gypsy retrovirus with the Drosophila flamenco host gene , 2004, Genetica.

[79]  E. Freed,et al.  Retrovirus budding. , 2004, Virus research.

[80]  S. Eastman,et al.  Particle assembly and genome packaging. , 2003, Current topics in microbiology and immunology.

[81]  L. Ratner,et al.  Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. , 1990, Proceedings of the National Academy of Sciences of the United States of America.