Identification of an intracellular trafficking and assembly pathway for HIV-1 Gag

Traffic

Volumn 7, Issue 6, 2006, Pages 731-745

  Perlman, Mira ^a   Resh, Marilyn D ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Gag; HIV 1; Membranes; Multivesicular body exocytosis; Viral particle assembly

Indexed keywords

CALCIUM ION; CD63 ANTIGEN; GAG PROTEIN; GREEN FLUORESCENT PROTEIN; IONOMYCIN; MEMBRANE PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; EXOCYTOSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMAGE ANALYSIS; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REGULATORY MECHANISM; RETROVIRUS; SECRETORY VESICLE; VIRUS ASSEMBLY; VIRUS PARTICLE;

ANIMALS; ARSENICALS; BASE SEQUENCE; CALCIUM SIGNALING; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLOHEXIMIDE; DNA, VIRAL; FLUORESCENT DYES; GENE PRODUCTS, GAG; HELA CELLS; HIV-1; HUMANS; MICROSCOPY, ELECTRON; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT; TRANSFECTION; VIRUS ASSEMBLY;

EID: 33646410462     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1398-9219.2006.00428.x     Document Type: Article

References (48)

1. Freed EO. HIV-1 gag proteins: Diverse functions in the virus life cycle. Virology 1998; 251: 1-15.
2. Gottlinger HG. The HIV-1 assembly machine. Aids 2001; 15 (Suppl. 5): S13-S20.
3. Resh MD. Intracellular trafficking of HIV-1 Gag: How Gag interacts with cell membranes and makes viral particles. AIDS Rev 2005; 7: 84-91.
4. Zhou W, Parent LJ, Wills JW, Resh MD. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J Virol 1994; 68: 2556-2569.
5. Burniston MT, Cimarelli A, Colgan J, Curtis SP, Luban J. Human immunodeficiency virus type 1 Gag polyprotein multimerization requires the nucleocapsid domain and RNA and is promoted by the capsid-dimer interface and the basic region of matrix protein. J Virol 1999; 73: 8527-8540.
6. Cimarelli A, Sandin S, Hoglund S, Luban J. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J Virol 2000; 74: 3046-3057.
7. Freed EO. The HIV-TSG101 interface: Recent advances in a budding field. Trends Microbiol 2003; 11: 56-59.
8. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, Myszka DG, Sundquist WI. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001; 107: 55-65.
9. VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55 (Gag). Proc Natl Acad Sci USA 2001; 98: 7724-7729.
10. Martin-Serrano J, Zang T, Bieniasz PD. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat Med 2001; 7: 1313-1319.
11. Demirov DG, Ono A, Orenstein JM, Freed EO. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc Natl Acad Sci USA 2002; 99: 955-960.
12. Babst M, Odorizzi G, Estepa EJ, Emr SD. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 2000; 1: 248-258.
13. Katzmann DJ, Babst M, Emr SD. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 2001; 106: 145-155.
14. Katzmann DJ, Odorizzi G, Emr SD. Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 2002; 3: 893-905.
15. Patnaik A, Chau V, Wills JW. Ubiquitin is part of the retrovirus budding machinery. Proc Natl Acad Sci USA 2000; 97: 13069-13074.
16. Hermida-Matsumoto L, Resh MD. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J Virol 2000; 74: 8670-8679.
17. Raposo G, Moore M, Innes D, Leijendekker R, Leigh-Brown A, Benaroch P, Geuze H. Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic 2002; 3: 718-729.
18. Pelchen-Matthews A, Kramer B, Marsh M. Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol 2003; 162: 443-455.
19. Ono A, Ablan SD, Lockett SJ, Nagashima K, Freed EO. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc Natl Acad Sci USA 2004; 101: 14889-14894.
20. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Ingmundson A, Horner SM, Cicchetti G, Allen PG, Pypaert M, Cunningham JM, Mothes W. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 2003; 4: 785-801.
21. Nydegger S, Foti M, Derdowski A, Spearman P, Thali M. HIV-1 egress is gated through late endosomal membranes. Traffic 2003; 4: 902-910.
22. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH. Multicolor and electron microscopic imaging of connexin trafficking. Science 2002; 296: 503-507.
23. Adams SR, Campbell RE, Gross LA, Martin BR, Walkup GK, Yao Y, Llopis J, Tsien RY. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: Synthesis and biological applications. J Am Chem Soc 2002; 124: 6063-6076.
24. Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, Payne M, He GP, Wang HE, Morham SG, Sundquist WI. HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J Cell Biol 2003; 162: 425-434.
25. Lindwasser OW, Resh MD. Human immunodeficiency virus type 1 Gag contains a dileucine-like motif that regulates association with multivesicular bodies. J Virol 2004; 78: 6013-6023.
26. Tritel M, Resh MD. Kinetic analysis of human immunodeficiency virus type 1 assembly reveals the presence of sequential intermediates. J Virol 2000; 74: 5845-5855.
27. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000; 404: 770-774.
28. Lindwasser OW, Resh MD. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J Virol 2001; 75: 7913-7924.
29. Dong X, Li H, Derdowski A, Ding L, Burnett A, Chen X, Peters TR, Dermody TS, Woodruff E, Wang JJ, Spearman P. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 2005; 120: 663-674.
30. Rudner L, Nydegger S, Coren LV, Nagashima K, Thali M, Ott DE. Dynamic fluorescent imaging of human immunodeficiency virus type 1 gag in live cells by biarsenical labeling. J Virol 2005; 79: 4055-4065.
31. Poole E, Strappe P, Mok HP, Hicks R, Lever AM. HIV-1 Gag-RNA interaction occurs at a perinuclear/centrosomal site; analysis by confocal microscopy and FRET. Traffic 2005; 6: 741-755.
32. Nermut MV, Zhang WH, Francis G, Ciampor F, Morikawa Y, Jones IM. Time course of Gag protein assembly in HIV-1-infected cells: A study by immunoelectron microscopy. Virology 2003; 305: 219-227.
33. Jaiswal JK, Andrews NW, Simon SM. Membrane proximal lysosomes are the major vesicles responsible for calcium-dependent exocytosis in nonsecretory cells. J Cell Biol 2002; 159: 625-635.
34. Gerber SH, Sudhof TC. Molecular determinants of regulated exocytosis. Diabetes 2002; 51 (Suppl. 1): S3-S11.
35. Borgonovo B, Cocucci E, Racchetti G, Podini P, Bachi A, Meldolesi J. Regulated exocytosis: A novel, widely expressed system. Nat Cell Biol 2002; 4: 955-962.
36. Pryor PR, Mullock BM, Bright NA, Gray SR, Luzio JP. The role of intraorganellar Ca (2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol 2000; 149: 1053-1062.
37. Piper RC, Luzio JP. CUPpling calcium to lysosomal biogenesis. Trends Cell Biol 2004; 14: 471-473.
38. Savina A, Fader CM, Damiani MT, Colombo MI. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic 2005; 6: 131-143.
39. Blott EJ, Griffiths GM. Secretory lysosomes. Nat Rev Mol Cell Biol 2002; 3: 122-131.
40. Rodriguez A, Webster P, Ortego J, Andrews NW. Lysosomes behave as Ca2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J Cell Biol 1997; 137: 93-104.
41. Andrews NW. Lysosomes and the plasma membrane: Trypanosomes reveal a secret relationship. J Cell Biol 2002; 158: 389-394.
42. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G. The biogenesis and functions of exosomes. Traffic 2002; 3: 321-330.
43. Michaux G, Cutler DF. How to roll an endothelial cigar: The biogenesis of Weibel-Palade bodies. Traffic 2004; 5: 69-78.
44. Beuret N, Stettler H, Renold A, Rutishauser J, Spiess M. Expression of regulated secretory proteins is sufficient to generate granule-like structures in constitutively secreting cells. J Biol Chem 2004; 279: 20242-20249.
45. Gould SJ, Booth AM, Hildreth JE. The Trojan exosome hypothesis. Proc Natl Acad Sci USA 2003; 100: 10592-10597.
46. Basyuk E, Galli T, Mougel M, Blanchard JM, Sitbon M, Bertrand E. Retroviral genomic RNAs are transported to the plasma membrane by endosomal vesicles. Dev Cell 2003; 5: 161-174.
47. Blot V, Perugi F, Gay B, Prevost MC, Briant L, Tangy F, Abriel H, Staub O, Dokhelar MC, Pique C. Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding. J Cell Sci 2004; 117: 2357-2367.
48. Kolesnikova L, Bamberg S, Berghofer B, Becker S. The matrix protein of Marburg virus is transported to the plasma membrane along cellular membranes: Exploiting the retrograde late endosomal pathway. J Virol 2004; 78: 2382-2393.