Rab7A is required for efficient production of infectious HIV-1

PLoS Pathogens

Volumn 7, Issue 11, 2011, Pages

  Caillet, Marina ^a,b   Janvier, Katy ^a,b   Pelchen Matthews, Annegret ^c   Delcroix Genête, Delphine ^a,b   Camus, Grégory ^a,b   Marsh, Mark ^c   Berlioz Torrent, Clarisse ^a,b  

^a INSTITUT COCHIN   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; RAB PROTEIN; RAB7A PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; BST2 PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; LEUKOCYTE ANTIGEN; RAB7 PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; VIROLOGY; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION; BIOSYNTHESIS; CELL STRAIN HEK293; ENDOSOME; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELA CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PROTEIN TRANSPORT; RNA INTERFERENCE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIGENS, CD; CELL MEMBRANE; ENDOSOMES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GPI-LINKED PROTEINS; HEK293 CELLS; HELA CELLS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS RELEASE;

EID: 81755163007     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002347     Document Type: Article

References (82)

1. Goff SP, (2007) Host factors exploited by retroviruses. Nat Rev Microbiol 5: 253-263.
2. Malim MH, Emerman M, (2008) HIV-1 accessory proteins-ensuring viral survival in a hostile environment. Cell Host Microbe 3: 388-398.
3. Freed EO, (2004) HIV-1 and the host cell: an intimate association. Trends Microbiol 12: 170-177.
4. Fackler OT, Krausslich HG, (2006) Interactions of human retroviruses with the host cell cytoskeleton. Curr Opin Microbiol 9: 409-415.
5. Chu H, Wang JJ, Spearman P, (2009) Human immunodeficiency virus type-1 gag and host vesicular trafficking pathways. Curr Top Microbiol Immunol 339: 67-84.
6. Ono A, Ablan SD, Lockett SJ, Nagashima K, Freed EO, (2004) Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc Natl Acad Sci U S A 101: 14889-14894.
7. Saad JS, Miller J, Tai J, Kim A, Ghanam RH, et al. (2006) Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc Natl Acad Sci U S A 103: 11364-11369.
8. Bonifacino JS, Traub LM, (2003) Signals for Sorting of Transmembrane Proteins to Endosomes and Lysosomes. Annu Rev Biochem 72: 395-447.
9. Camus G, Segura-Morales C, Molle D, Lopez-Verges S, Begon-Pescia C, et al. (2007) The clathrin adaptor complex AP-1 binds HIV-1 and MLV Gag and facilitates their budding. Mol Biol Cell 18: 3193-3203.
10. Dong X, Li H, Derdowski A, Ding L, Burnett A, et al. (2005) AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 120: 663-674.
11. Azevedo C, Burton A, Ruiz-Mateos E, Marsh M, Saiardi A, (2009) Inositol pyrophosphate mediated pyrophosphorylation of AP3B1 regulates HIV-1 Gag release. Proc Natl Acad Sci U S A 106: 21161-21166.
12. Joshi A, Garg H, Nagashima K, Bonifacino JS, Freed EO, (2008) GGA and Arf proteins modulate retrovirus assembly and release. Mol Cell 30: 227-238.
13. Boge M, Wyss S, Bonifacino JS, Thali M, (1998) A membrane-proximal tyrosine-based signal mediates internalization of the HIV-1 envelope glycoprotein via interaction with the AP-2 clathrin adaptor. J Biol Chem 273: 15773-15778.
14. Byland R, Vance PJ, Hoxie JA, Marsh M, (2007) A Conserved Dileucine Motif Mediates Clathrin and AP-2-dependent Endocytosis of the HIV-1 Envelope Protein. Mol Biol Cell 18: 414-425.
15. Wyss S, Berlioz-Torrent C, Boge M, Blot G, Honing S, et al. (2001) The highly conserved C-terminal dileucine motif in the cytosolic domain of the human immunodeficiency virus type 1 envelope glycoprotein is critical for its association with the AP-1 clathrin adaptor [correction of adapter]. J Virol 75: 2982-2992.
16. Berlioz-Torrent C, Shacklett BL, Erdtmann L, Delamarre L, Bouchaert I, et al. (1999) Interactions of the cytoplasmic domains of human and simian retroviral transmembrane proteins with components of the clathrin adaptor complexes modulate intracellular and cell surface expression of envelope glycoproteins. J Virol 73: 1350-1361.
17. Ohno H, Aguilar RC, Fournier MC, Hennecke S, Cosson P, et al. (1997) Interaction of endocytic signals from the HIV-1 envelope glycoprotein complex with members of the adaptor medium chain family. Virology 238: 305-315.
18. Blot G, Janvier K, Le Panse S, Benarous R, Berlioz-Torrent C, (2003) 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. J Virol 77: 6931-6945.
19. Bauby H, Lopez-Verges S, Hoeffel G, Delcroix-Genete D, Janvier K, et al. (2010) TIP47 is required for the production of infectious HIV-1 particles from primary macrophages. Traffic 11: 455-467.
20. Lopez-Verges S, Camus G, Blot G, Beauvoir R, Benarous R, et al. (2006) Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions. Proc Natl Acad Sci U S A 103: 14947-14952.
21. Carlton JG, Martin-Serrano J, (2007) Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316: 1908-1912.
22. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP, et al. (2007) Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 26: 4215-4227.
23. Raiborg C, Stenmark H, (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458: 445-452.
24. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, et al. (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107: 55-65.
25. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, et al. (2003) The protein network of HIV budding. Cell 114: 701-713.
26. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG, (2003) AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114: 689-699.
27. Martin-Serrano J, Zang T, Bieniasz PD, (2001) HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat Med 7: 1313-1319.
28. Neil SJ, Zang T, Bieniasz PD, (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425-430.
29. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, et al. (2008) The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3: 245-252.
30. Janvier K, Pelchen-Matthews A, Renaud JB, Caillet M, Marsh M, et al. (2011) The ESCRT-0 Component HRS is Required for HIV-1 Vpu-Mediated BST-2/Tetherin Downregulation. PLoS Pathog 7: e1001265.
31. Stenmark H, (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513-525.
32. Zerial M, McBride H, (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117.
33. Pfeffer S, (2005) A model for Rab GTPase localization. Biochem Soc Trans 33: 627-630.
34. Cai H, Reinisch K, Ferro-Novick S, (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12: 671-682.
35. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M, (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62: 317-329.
36. Press B, Feng Y, Hoflack B, Wandinger-Ness A, (1998) Mutant Rab7 causes the accumulation of cathepsin D and cation- independent mannose 6-phosphate receptor in an early endocytic compartment. J Cell Biol 140: 1075-1089.
37. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B, (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11: 467-480.
38. Vitelli R, Santillo M, Lattero D, Chiariello M, Bifulco M, et al. (1997) Role of the small GTPase Rab7 in the late endocytic pathway. J Biol Chem 272: 4391-4397.
39. Feng Y, Press B, Wandinger-Ness A, (1995) Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131: 1435-1452.
40. Lebrand C, Corti M, Goodson H, Cosson P, Cavalli V, et al. (2002) Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J 21: 1289-1300.
41. Ceresa BP, Bahr SJ, (2006) rab7 activity affects epidermal growth factor:epidermal growth factor receptor degradation by regulating endocytic trafficking from the late endosome. J Biol Chem 281: 1099-1106.
42. Wang T, Ming Z, Xiaochun W, Hong W, (2011) Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal 23: 516-521.
43. Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S, (2003) Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 23: 6494-6506.
44. Vieira OV, Bucci C, Harrison RE, Trimble WS, Lanzetti L, et al. (2003) Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol Cell Biol 23: 2501-2514.
45. Gutierrez MG, Munafo DB, Beron W, Colombo MI, (2004) Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117: 2687-2697.
46. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, et al. (2004) Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 117: 4837-4848.
47. Johansson M, Rocha N, Zwart W, Jordens I, Janssen L, et al. (2007) Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J Cell Biol 176: 459-471.
48. Murray JL, Mavrakis M, McDonald NJ, Yilla M, Sheng J, et al. (2005) Rab9 GTPase is required for replication of human immunodeficiency virus type 1, filoviruses, and measles virus. J Virol 79: 11742-11751.
49. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, et al. (2008) Identification of host proteins required for HIV infection through a functional genomic screen. Science 319: 921-926.
50. Molle D, Segura-Morales C, Camus G, Berlioz-Torrent C, Kjems J, et al. (2009) Endosomal Trafficking of HIV-1 Gag and Genomic RNAs Regulates Viral Egress. J Biol Chem 284: 19727-19743.
51. Lehmann M, Milev MP, Abrahamyan L, Yao XJ, Pante N, et al. (2009) Intracellular transport of human immunodeficiency virus type 1 genomic RNA and viral production are dependent on dynein motor function and late endosome positioning. J Biol Chem 284: 14572-14585.
52. Goffinet C, Allespach I, Homann S, Tervo HM, Habermann A, et al. (2009) HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 5: 285-297.
53. Mangeat B, Gers-Huber G, Lehmann M, Zufferey M, Luban J, et al. (2009) HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog 5: e1000574.
54. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, et al. (2009) Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog 5: e1000450.
55. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, et al. (2009) Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139: 499-511.
56. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Fruh K, et al. (2009) Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a {beta}TrCP-dependent mechanism. J Virol 83: 7931-7947.
57. Neil SJ, Sandrin V, Sundquist WI, Bieniasz PD, (2007) An interferon-alpha-induced tethering mechanism inhibits HIV-1 and Ebola virus particle release but is counteracted by the HIV-1 Vpu protein. Cell Host Microbe 2: 193-203.
58. Bishop N, Horman A, Woodman P, (2002) Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J Cell Biol 157: 91-101.
59. Raiborg C, Malerod L, Pedersen NM, Stenmark H, (2008) Differential functions of Hrs and ESCRT proteins in endocytic membrane trafficking. Exp Cell Res 314: 801-813.
60. Vanlandingham PA, Ceresa BP, (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284: 12110-12124.
61. Bolte S, Cordelieres FP, (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232.
62. Iwabu Y, Fujita H, Kinomoto M, Kaneko K, Ishizaka Y, et al. (2009) HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin through transmembrane interactions leading to lysosomes. J Biol Chem 284: 35060-35072.
63. Vidricaire G, Tremblay MJ, (2005) Rab5 and Rab7, but not ARF6, govern the early events of HIV-1 infection in polarized human placental cells. J Immunol 175: 6517-6530.
64. Hallenberger S, Bosch V, Angliker H, Shaw E, Klenk HD, et al. (1992) Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360: 358-361.
65. Moulard M, Decroly E, (2000) Maturation of HIV envelope glycoprotein precursors by cellular endoproteases. Biochim Biophys Acta 1469: 121-132.
66. Rollason R, Korolchuk V, Hamilton C, Schu P, Banting G, (2007) Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. J Cell Sci 120: 3850-3858.
67. Schmidt S, Fritz JV, Bitzegeio J, Fackler OT, Keppler OT, (2011) HIV-1 Vpu Blocks Recycling and Biosynthetic Transport of the Intrinsic Immunity Factor CD317/Tetherin To Overcome the Virion Release Restriction. MBio 2: e00036-11.
68. Tokarev AA, Munguia J, Guatelli JC, (2011) Serine-threonine ubiquitination mediates downregulation of BST-2/tetherin and relief of restricted virion release by HIV-1 Vpu. J Virol 85: 51-63.
69. Pardieu C, Vigan R, Wilson SJ, Calvi A, Zang T, et al. (2010) The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLoS Pathog 6: e1000843.
70. Silva E, Au-Yeung HW, Van Goethem E, Burden J, Franc NC, (2007) Requirement for a Drosophila E3-ubiquitin ligase in phagocytosis of apoptotic cells. Immunity 27: 585-596.
71. Miyakawa K, Ryo A, Murakami T, Ohba K, Yamaoka S, et al. (2009) BCA2/Rabring7 promotes tetherin-dependent HIV-1 restriction. PLoS Pathog 5: e1000700.
72. Mizuno K, Kitamura A, Sasaki T, (2003) Rabring7, a novel Rab7 target protein with a RING finger motif. Mol Biol Cell 14: 3741-3752.
73. Sakane A, Hatakeyama S, Sasaki T, (2007) Involvement of Rabring7 in EGF receptor degradation as an E3 ligase. Biochem Biophys Res Commun 357: 1058-1064.
74. Vonderheit A, Helenius A, (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3: e233.
75. Harbison CE, Lyi SM, Weichert WS, Parrish CR, (2009) Early steps in cell infection by parvoviruses: host-specific differences in cell receptor binding but similar endosomal trafficking. J Virol 83: 10504-10514.
76. van der Schaar HM, Rust MJ, Chen C, van der Ende-Metselaar H, Wilschut J, et al. (2008) Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 4: e1000244.
77. Krishnan MN, Sukumaran B, Pal U, Agaisse H, Murray JL, et al. (2007) Rab 5 is required for the cellular entry of dengue and West Nile viruses. J Virol 81: 4881-4885.
78. Klimkait T, Strebel K, Hoggan MD, Martin MA, Orenstein JM, (1990) The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J Virol 64: 621-629.
79. Brussel A, Sonigo P, (2004) Evidence for gene expression by unintegrated human immunodeficiency virus type 1 DNA species. J Virol 78: 11263-11271.
80. Bache KG, Brech A, Mehlum A, Stenmark H, (2003) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 162: 435-442.
81. Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M, (2007) In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J Cell Biol 177: 329-341.
82. Slot JW, Geuze HJ, (2007) Cryosectioning and immunolabeling. Nat Protoc 2: 2480-2491.