Budding of a Retrovirus: Some Assemblies Required

One of the most important steps in any viral lifecycle is the production of progeny virions. For retroviruses as well as other viruses, this step is a highly organized process that occurs with exquisite spatial and temporal specificity on the cellular plasma membrane. To facilitate this process, retroviruses encode short peptide motifs, or L domains, that hijack host factors to ensure completion of this critical step. One such cellular machinery targeted by viruses is known as the Endosomal Sorting Complex Required for Transport (ESCRTs). Typically responsible for vesicular trafficking within the cell, ESCRTs are co-opted by the retroviral Gag polyprotein to assist in viral particle assembly and release of infectious virions. This review in the Viruses Special Issue “The 11th International Retroviral Nucleocapsid and Assembly Symposium”, details recent findings that shed light on the molecular details of how ESCRTs and the ESCRT adaptor protein ALIX, facilitate retroviral dissemination at sites of viral assembly.

[1]  J. Hurley,et al.  A helical assembly of human ESCRT-I scaffolds reverse-topology membrane scission , 2020, bioRxiv.

[2]  Marc C. Johnson,et al.  Structures of immature EIAV Gag lattices reveal a conserved role for IP6 in lentivirus assembly , 2020, PLoS pathogens.

[3]  H. Stenmark,et al.  The many functions of ESCRTs , 2019, Nature Reviews Molecular Cell Biology.

[4]  B. Chait,et al.  Asymmetric Molecular Architecture of the Human γ-Tubulin Ring Complex , 2019, Cell.

[5]  E. Freed,et al.  Genomic tagging of endogenous human ESCRT-I complex preserves ESCRT-mediated membrane-remodeling functions , 2019, The Journal of Biological Chemistry.

[6]  J. Briggs,et al.  Structure and architecture of immature and mature murine leukemia virus capsids , 2018, Proceedings of the National Academy of Sciences.

[7]  V. Larue,et al.  The NC domain of HIV-1 Gag contributes to the interaction of Gag with TSG101. , 2018, Biochimica et biophysica acta. General subjects.

[8]  D. Goldman,et al.  ESCRT membrane scission revealed by optical tweezers. , 2018 .

[9]  N. Tjandra,et al.  Tsg101 chaperone function revealed by HIV-1 assembly inhibitors , 2017, Nature Communications.

[10]  J. Briggs,et al.  An atomic model of HIV-1 capsid-SP1 reveals structures regulating assembly and maturation , 2016, Science.

[11]  M. Bendjennat,et al.  The Race against Protease Activation Defines the Role of ESCRTs in HIV Budding , 2016, PLoS pathogens.

[12]  K. Liestøl,et al.  ALIX and ESCRT-I/II function as parallel ESCRT-III recruiters in cytokinetic abscission , 2016, The Journal of cell biology.

[13]  B. Meng,et al.  Evidence that the endosomal sorting complex required for transport-II (ESCRT-II) is required for efficient human immunodeficiency virus-1 (HIV-1) production , 2015, Retrovirology.

[14]  N. Loncle,et al.  An ESCRT module is required for neuron pruning , 2015, Scientific Reports.

[15]  C. Bräuchle,et al.  Super-Resolution Imaging of ESCRT-Proteins at HIV-1 Assembly Sites , 2015, PLoS pathogens.

[16]  Michelle S Itano,et al.  Temporal and spatial organization of ESCRT protein recruitment during HIV-1 budding , 2014, Proceedings of the National Academy of Sciences.

[17]  A. Cashikar,et al.  Structure of cellular ESCRT-III spirals and their relationship to HIV budding , 2014, eLife.

[18]  K. Nagashima,et al.  Ubiquitin conjugation to Gag is essential for ESCRT-mediated HIV-1 budding , 2013, Retrovirology.

[19]  Klaus Schulten,et al.  Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics , 2013, Nature.

[20]  T. Xiao,et al.  Two distinct binding modes define the interaction of Brox with the C-terminal tails of CHMP5 and CHMP4B. , 2012, Structure.

[21]  K. Nagashima,et al.  Budding of Retroviruses Utilizing Divergent L Domains Requires Nucleocapsid , 2012, Journal of Virology.

[22]  W. Sundquist,et al.  Structure of the Bro1 Domain Protein BROX and Functional Analyses of the ALIX Bro1 Domain in HIV-1 Budding , 2011, PloS one.

[23]  T. Xiao,et al.  The Phe105 loop of Alix Bro1 domain plays a key role in HIV-1 release. , 2011, Structure.

[24]  J. Hurley,et al.  Proline‐Rich Regions and Motifs in Trafficking: From ESCRT Interaction to Viral Exploitation , 2011, Traffic.

[25]  K. Nagashima,et al.  Basic Residues in the Nucleocapsid Domain of Gag Are Critical for Late Events of HIV-1 Budding , 2010, Journal of Virology.

[26]  N. Gov,et al.  Retroviral assembly and budding occur through an actin-driven mechanism. , 2009, Biophysical journal.

[27]  Kunio Nagashima,et al.  The Nucleocapsid Region of HIV-1 Gag Cooperates with the PTAP and LYPXnL Late Domains to Recruit the Cellular Machinery Necessary for Viral Budding , 2009, PLoS pathogens.

[28]  Aleksandr Mironov,et al.  The Bro1-related protein HD-PTP/PTPN23 is required for endosomal cargo sorting and multivesicular body morphogenesis , 2008, Proceedings of the National Academy of Sciences.

[29]  M. Maki,et al.  Brox, a novel farnesylated Bro1 domain‐containing protein that associates with charged multivesicular body protein 4 (CHMP4) , 2008, The FEBS journal.

[30]  Michio Inoue,et al.  Human Immunodeficiency Virus Type 1 Gag Engages the Bro1 Domain of ALIX/AIP1 through the Nucleocapsid , 2007, Journal of Virology.

[31]  S. Gygi,et al.  Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis , 2007, The EMBO journal.

[32]  J. Martin-Serrano,et al.  Parallels Between Cytokinesis and Retroviral Budding: A Role for the ESCRT Machinery , 2007, Science.

[33]  J. Hurley,et al.  Molecular Architecture and Functional Model of the Complete Yeast ESCRT-I Heterotetramer , 2007, Cell.

[34]  H. Göttlinger,et al.  Potent Rescue of Human Immunodeficiency Virus Type 1 Late Domain Mutants by ALIX/AIP1 Depends on Its CHMP4 Binding Site , 2007, Journal of Virology.

[35]  R. D. Fisher,et al.  Structural and Biochemical Studies of ALIX/AIP1 and Its Role in Retrovirus Budding , 2007, Cell.

[36]  R. D. Fisher,et al.  Human ESCRT-II Complex and Its Role in Human Immunodeficiency Virus Type 1 Release , 2006, Journal of Virology.

[37]  S. Emr,et al.  ESCRT-I Core and ESCRT-II GLUE Domain Structures Reveal Role for GLUE in Linking to ESCRT-I and Membranes , 2006, Cell.

[38]  J. Hurley,et al.  Structural and Functional Organization of the ESCRT-I Trafficking Complex , 2006, Cell.

[39]  J. Hurley,et al.  Structural basis for endosomal targeting by the Bro1 domain. , 2005, Developmental cell.

[40]  I. Dikic,et al.  Src Phosphorylation of Alix/AIP1 Modulates Its Interaction with Binding Partners and Antagonizes Its Activities* , 2005, Journal of Biological Chemistry.

[41]  W. Sundquist,et al.  The Human Endosomal Sorting Complex Required for Transport (ESCRT-I) and Its Role in HIV-1 Budding*♦ , 2004, Journal of Biological Chemistry.

[42]  A. Calistri,et al.  AIP1/ALIX Is a Binding Partner for HIV-1 p6 and EIAV p9 Functioning in Virus Budding , 2003, Cell.

[43]  P. Bieniasz,et al.  Role of ESCRT-I in Retroviral Budding , 2003, Journal of Virology.

[44]  P. Bieniasz,et al.  HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress , 2001, Nature Medicine.

[45]  L. Verplank,et al.  Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55Gag , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Woodman,et al.  TSG101/Mammalian VPS23 and Mammalian VPS28 Interact Directly and Are Recruited to VPS4-induced Endosomes* , 2001, The Journal of Biological Chemistry.

[47]  A. Patnaik,et al.  Ubiquitin is part of the retrovirus budding machinery. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Xiao-Fang Yu,et al.  Proline Residues in Human Immunodeficiency Virus Type 1 p6Gag Exert a Cell Type-Dependent Effect on Viral Replication and Virion Incorporation of Pol Proteins , 1999, Journal of Virology.

[49]  C. Flexner,et al.  Mutations of the Human Immunodeficiency Virus Type 1 p6Gag Domain Result in Reduced Retention of Pol Proteins during Virus Assembly , 1998, Journal of Virology.

[50]  H. Kräusslich,et al.  Sequential Steps in Human Immunodeficiency Virus Particle Maturation Revealed by Alterations of Individual Gag Polyprotein Cleavage Sites , 1998, Journal of Virology.

[51]  J. Wills,et al.  Equine infectious anemia virus utilizes a YXXL motif within the late assembly domain of the Gag p9 protein , 1997, Journal of virology.

[52]  L. Arthur,et al.  Cytoskeletal proteins inside human immunodeficiency virus type 1 virions , 1996, Journal of virology.

[53]  K. Köhrer,et al.  Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. , 1996, Molecular biology of the cell.

[54]  E. Freed,et al.  p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease , 1995, Journal of virology.