Reevaluation of the Requirement for TIP47 in Human Immunodeficiency Virus Type 1 Envelope Glycoprotein Incorporation

ABSTRACT Incorporation of the human immunodeficiency virus type 1 (HIV-1) envelope glycoproteins into assembling particles is crucial for virion infectivity. Genetic and biochemical data indicate that the matrix (MA) domain of Gag and the cytoplasmic tail of the transmembrane glycoprotein gp41 play an important role in coordinating Env incorporation; however, the molecular mechanism and possible role of host factors in this process remain to be defined. Recent studies suggested that Env incorporation is mediated by interactions between matrix and tail-interacting protein of 47 kDa (TIP47; also known as perilipin-3 and mannose-6-phosphate receptor-binding protein 1), a member of the perilipin, adipophilin, TIP47 (PAT) family of proteins implicated in protein sorting and lipid droplet biogenesis. We have confirmed by nuclear magnetic resonance spectroscopy titration experiments and surface plasmon resonance that MA binds TIP47. We also reevaluated the role of TIP47 in HIV-1 Env incorporation in HeLa cells and in the Jurkat T-cell line. In HeLa cells, TIP47 overexpression or RNA interference (RNAi)-mediated depletion had no significant effect on HIV-1 Env incorporation, virus release, or particle infectivity. Similarly, depletion of TIP47 in Jurkat cells did not impair HIV-1 Env incorporation, virus release, infectivity, or replication. Our results thus do not support a role for TIP47 in HIV-1 Env incorporation or virion infectivity.

[1]  Tanaka,et al.  The role of , 2021, Journal of insect physiology.

[2]  J. Trewhella,et al.  Solution structure studies of monomeric human TIP47/perilipin‐3 reveal a highly extended conformation , 2012, Proteins.

[3]  W. Sundquist,et al.  HIV-1 assembly, budding, and maturation. , 2012, Cold Spring Harbor perspectives in medicine.

[4]  E. Freed,et al.  New insights into HIV assembly and trafficking. , 2011, Physiology.

[5]  E. Freed,et al.  HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. , 2011, Journal of molecular biology.

[6]  Marc C. Johnson.  Mechanisms for Env glycoprotein acquisition by retroviruses. , 2011, AIDS research and human retroviruses.

[7]  E. Freed,et al.  The Role of Lipids in Retrovirus Replication , 2010, Viruses.

[8]  Kunio Nagashima,et al.  The capsid-spacer peptide 1 Gag processing intermediate is a dominant-negative inhibitor of HIV-1 maturation. , 2010, Virology.

[9]  F. Mammano,et al.  TIP47 is required for the production of infectious HIV-1 particles from primary macrophages , 2009, Retrovirology.

[10]  M. Welte,et al.  PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. , 2009, Biochimica et biophysica acta.

[11]  M. Rudolph,et al.  TIP47 functions in the biogenesis of lipid droplets , 2009, The Journal of cell biology.

[12]  J. Manrique,et al.  In vitro binding of simian immunodeficiency virus matrix protein to the cytoplasmic domain of the envelope glycoprotein. , 2008, Virology.

[13]  K. Nagashima,et al.  Molecular Characterization of Feline Immunodeficiency Virus Budding , 2007, Journal of Virology.

[14]  P. Loll,et al.  Ligation independent cloning vectors for expression of SUMO fusions. , 2007, Protein expression and purification.

[15]  R. Benarous,et al.  Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions , 2006, Proceedings of the National Academy of Sciences.

[16]  F. Studier,et al.  Protein production by auto-induction in high density shaking cultures. , 2005, Protein expression and purification.

[17]  S. Pfeffer,et al.  Rab9 GTPase regulates late endosome size and requires effector interaction for its stability. , 2004, Molecular biology of the cell.

[18]  T. Hodge,et al.  High Resolution Crystal Structure of Human Rab9 GTPase , 2004, Journal of Biological Chemistry.

[19]  J. Hurley,et al.  Structure of a lipid droplet protein; the PAT family member TIP47. , 2004, Structure.

[20]  M. Summers,et al.  Entropic switch regulates myristate exposure in the HIV-1 matrix protein. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Benarous,et al.  Targeting of the Human Immunodeficiency Virus Type 1 Envelope to the trans-Golgi Network through Binding to TIP47 Is Required for Env Incorporation into Virions and Infectivity , 2003, Journal of Virology.

[22]  S. Pfeffer,et al.  Self‐Assembly Is Important for TIP47 Function in Mannose 6‐Phosphate Receptor Transport , 2003, Traffic.

[23]  S. Pfeffer,et al.  Identification of residues in TIP47 essential for Rab9 binding , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Brasaemle,et al.  TIP47 Associates with Lipid Droplets* , 2001, The Journal of Biological Chemistry.

[25]  S. Pfeffer,et al.  Quantitative Analysis of TIP47-Receptor Cytoplasmic Domain Interactions , 2000, The Journal of Biological Chemistry.

[26]  S. Pfeffer,et al.  Recognition of the 300-kDa mannose 6-phosphate receptor cytoplasmic domain by 47-kDa tail-interacting protein. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  H. Akari,et al.  Cell-Dependent Requirement of Human Immunodeficiency Virus Type 1 gp41 Cytoplasmic Tail for Env Incorporation into Virions , 2000, Journal of virology.

[28]  E. Freed,et al.  Genetic Evidence for an Interaction between Human Immunodeficiency Virus Type 1 Matrix and α-Helix 2 of the gp41 Cytoplasmic Tail , 2000, Journal of Virology.

[29]  E. Freed,et al.  The long cytoplasmic tail of gp41 is required in a cell type-dependent manner for HIV-1 envelope glycoprotein incorporation into virions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Pfeffer,et al.  TIP47: A Cargo Selection Device for Mannose 6-Phosphate Receptor Trafficking , 1998, Cell.

[31]  H. Gelderblom,et al.  Efficient HIV‐1 replication can occur in the absence of the viral matrix protein , 1998, The EMBO journal.

[32]  E. Freed,et al.  Role of Matrix in an Early Postentry Step in the Human Immunodeficiency Virus Type 1 Life Cycle , 1998, Journal of Virology.

[33]  F. Gage,et al.  In Vivo Gene Delivery and Stable Transduction of Nondividing Cells by a Lentiviral Vector , 1996, Science.

[34]  E. Freed,et al.  Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions , 1996, Journal of virology.

[35]  S. Grzesiek,et al.  NMRPipe: A multidimensional spectral processing system based on UNIX pipes , 1995, Journal of biomolecular NMR.

[36]  E. Freed,et al.  Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection , 1995, Journal of virology.

[37]  J. Sodroski,et al.  Rescue of human immunodeficiency virus type 1 matrix protein mutants by envelope glycoproteins with short cytoplasmic domains , 1995, Journal of virology.

[38]  E. Freed,et al.  Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific, single amino acid substitutions in the human immunodeficiency virus type 1 matrix , 1995, Journal of virology.

[39]  W. Sundquist,et al.  Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein. , 1994, Journal of molecular biology.

[40]  J. Burns,et al.  A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Pfeffer,et al.  Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network , 1994, The Journal of cell biology.

[42]  E. Freed,et al.  Evidence for a functional interaction between the V1/V2 and C4 domains of human immunodeficiency virus type 1 envelope glycoprotein gp120 , 1994, Journal of virology.

[43]  W. Haseltine,et al.  Role of the matrix protein in the virion association of the human immunodeficiency virus type 1 envelope glycoprotein , 1994, Journal of virology.

[44]  Y. Goda,et al.  Rab9 functions in transport between late endosomes and the trans Golgi network. , 1993, The EMBO journal.

[45]  Z. Matsuda,et al.  The matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions , 1992, Journal of virology.

[46]  D. Littman,et al.  Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity , 1990, Journal of virology.

[47]  J. Bonifacino,et al.  Biosynthesis, cleavage, and degradation of the human immunodeficiency virus 1 envelope glycoprotein gp160. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[48]  H. Gendelman,et al.  Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone , 1986, Journal of virology.

[49]  S. Pfeffer,et al.  Purification and analysis of TIP47 function in Rab9-dependent mannose 6-phosphate receptor trafficking. , 2005, Methods in enzymology.

[50]  Bruce A Johnson,et al.  Using NMRView to visualize and analyze the NMR spectra of macromolecules. , 2004, Methods in molecular biology.

[51]  M. Emerman,et al.  HIV-1 infection of non-dividing cells , 1994, Nature.

[52]  Xian-Yang Zhang,et al.  LSU Digital Commons LSU Digital Commons Altering the tropism of lentiviral vectors through pseudotyping Altering the tropism of lentiviral vectors through pseudotyping , 2022 .