Organization and regulation of intracellular plasma membrane-connected HIV-1 assembly compartments in macrophages

BMC Biology

Volumn 11, Issue , 2013, Pages

  Mlcochova, Petra ^a   Pelchen Matthews, Annegret ^a   Marsh, Mark ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Actin cytoskeleton; Compartment; HIV 1; IPMC; MDM

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

ACTIN; COLORING AGENT; FUSED HETEROCYCLIC RINGS; GREEN FLUORESCENT PROTEIN; LATRUNCULIN A; LIPID; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; POLYPHOSPHOINOSITIDE; THIAZOLIDINE DERIVATIVE;

ACTIN FILAMENT; ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECT; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMAGE PROCESSING; INTRACELLULAR MEMBRANE; MACROPHAGE; METABOLISM; MONOCYTE; PATHOLOGY; PHYSIOLOGY; POLYMERIZATION; ULTRASTRUCTURE; VIROLOGY; VIRUS ASSEMBLY;

ACTIN CYTOSKELETON; ACTINS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL COMPARTMENTATION; CELL MEMBRANE; CELL SURVIVAL; COLORING AGENTS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; HIV INFECTIONS; HIV-1; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INTRACELLULAR MEMBRANES; LIPIDS; MACROPHAGES; MONOCYTES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLINOSITOL PHOSPHATES; POLYMERIZATION; THIAZOLIDINES; VIRUS ASSEMBLY;

EID: 84881145334     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-11-89     Document Type: Article

References (35)

1. Meltzer MS, Skillman DR, Gomatos PJ, Kalter DC, Gendelman HE. Role of mononuclear phagocytes in the pathogenesis of human immunodeficiency virus infection. Annu Rev Immunol 1990, 8:169-194. 10.1146/annurev.iy.08.040190.001125, 2188662.
2. Sharova N, Swingler C, Sharkey M, Stevenson M. Macrophages archive HIV-1 virions for dissemination in trans. EMBO J 2005, 24:2481-2489. 10.1038/sj.emboj.7600707, 1173148, 15920469.
3. Gonzalez-Scarano F, Martin-Garcia J. The neuropathogenesis of AIDS. Nat Rev Immunol 2005, 5:69-81. 10.1038/nri1527, 15630430.
4. Muratori C, Sistigu A, Ruggiero E, Falchi M, Bacigalupo I, Palladino C, Toschi E, Federico M. Macrophages transmit human immunodeficiency virus type 1 products to CD4-negative cells: involvement of matrix metalloproteinase 9. J Virol 2007, 81:9078-9087. 10.1128/JVI.00675-07, 1951421, 17581988.
5. Nguyen DG, Hildreth JE. Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages. Eur J Immunol 2003, 33:483-493. 10.1002/immu.200310024, 12645947.
6. Orenstein JM, Meltzer MS, Phipps T, Gendelman HE. Cytoplasmic assembly and accumulation of human immunodeficiency virus types 1 and 2 in recombinant human colony-stimulating factor-1-treated human monocytes: an ultrastructural study. J Virol 1988, 62:2578-2586. 253687, 3260631.
7. Jouve M, Sol-Foulon N, Watson S, Schwartz O, Benaroch P. HIV-1 buds and accumulates in "nonacidic" endosomes of macrophages. Cell Host Microbe 2007, 2:85-95. 10.1016/j.chom.2007.06.011, 18005723.
8. Pelchen-Matthews A, Kramer B, Marsh M. Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol 2003, 162:443-455. 10.1083/jcb.200304008, 2172706, 12885763.
9. 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. 10.1034/j.1600-0854.2002.31004.x, 12230470.
10. Bennett AE, Narayan K, Shi D, Hartnell LM, Gousset K, He H, Lowekamp BC, Yoo TS, Bliss D, Freed EO, Subramaniam S. Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages. PLoS Pathog 2009, 5:e1000591. 10.1371/journal.ppat.1000591, 2743285, 19779568.
11. Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M. In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J Cell Biol 2007, 177:329-341. 10.1083/jcb.200609050, 2064140, 17438075.
12. Jouvenet N, Neil SJ, Bess C, Johnson MC, Virgen CA, Simon SM, Bieniasz PD. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol 2006, 4:e435. 10.1371/journal.pbio.0040435, 1750931, 17147474.
13. Koppensteiner H, Banning C, Schneider C, Hohenberg H, Schindler M. Macrophage internal HIV-1 is protected from neutralizing antibodies. J Virol 2012, 86:2826-2836. 10.1128/JVI.05915-11, 3302290, 22205742.
14. Pelchen-Matthews A, Giese S, Mlcochova P, Turner J, Marsh M. β2 integrin adhesion complexes maintain the integrity of HIV-1 assembly compartments in primary macrophages. Traffic 2012, 13:273-291. 10.1111/j.1600-0854.2011.01306.x, 22017400.
15. Welsch S, Groot F, Krausslich HG, Keppler OT, Sattentau QJ. Architecture and regulation of the HIV-1 assembly and holding compartment in macrophages. J Virol 2011, 85:7922-7927. 10.1128/JVI.00834-11, 3147899, 21613397.
16. Welsch S, Keppler OT, Habermann A, Allespach I, Krijnse-Locker J, Krausslich HG. HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog 2007, 3:e36. 10.1371/journal.ppat.0030036, 1829407, 17381240.
17. Joshi A, Ablan SD, Soheilian F, Nagashima K, Freed EO. Evidence that productive human immunodeficiency virus type 1 assembly can occur in an intracellular compartment. J Virol 2009, 83:5375-5387. 10.1128/JVI.00109-09, 2681934, 19297499.
18. Betz WJ, Mao F, Bewick GS. Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 1992, 12:363-375.
19. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 2001, 70:535-602. 10.1146/annurev.biochem.70.1.535, 11395417.
20. 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 U S A 2004, 101:14889-14894. 10.1073/pnas.0405596101, 522033, 15465916.
21. Saad JS, Miller J, Tai J, Kim A, Ghanam RH, Summers MF. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc Natl Acad Sci U S A 2006, 103:11364-11369. 10.1073/pnas.0602818103, 1544092, 16840558.
22. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 2000, 19:4577-4588. 10.1093/emboj/19.17.4577, 302054, 10970851.
23. Hammond GR, Dove SK, Nicol A, Pinxteren JA, Zicha D, Schiavo G. Elimination of plasma membrane phosphatidylinositol (4,5)-bisphosphate is required for exocytosis from mast cells. J Cell Sci 2006, 119:2084-2094. 10.1242/jcs.02912, 16687737.
24. Thomas CL, Steel J, Prestwich GD, Schiavo G. Generation of phosphatidylinositol-specific antibodies and their characterization. Biochem Soc Trans 1999, 27:648-652.
25. Pendleton A, Pope B, Weeds A, Koffer A. Latrunculin B or ATP depletion induces cofilin-dependent translocation of actin into nuclei of mast cells. J Biol Chem 2003, 278:14394-14400. 10.1074/jbc.M206393200, 12566455.
26. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R. Lifeact: a versatile marker to visualize F-actin. Nat Methods 2008, 5:605-607. 10.1038/nmeth.1220, 2814344, 18536722.
27. Gaudin R, de Alencar BC, Jouve M, Berre S, Le Bouder E, Schindler M, Varthaman A, Gobert FX, Benaroch P. Critical role for the kinesin KIF3A in the HIV life cycle in primary human macrophages. J Cell Biol 2012, 199:467-479. 10.1083/jcb.201201144, 3483138, 23091068.
28. Chu H, Wang JJ, Qi M, Yoon JJ, Wen X, Chen X, Ding L, Spearman P. The intracellular virus-containing compartments in primary human macrophages are largely inaccessible to antibodies and small molecules. PLoS One 2012, 7:e35297. 10.1371/journal.pone.0035297, 3342280, 22567100.
29. Chukkapalli V, Hogue IB, Boyko V, Hu WS, Ono A. Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient gag membrane binding. J Virol 2008, 82:2405-2417. 10.1128/JVI.01614-07, 2258911, 18094158.
30. Gousset K, Ablan SD, Coren LV, Ono A, Soheilian F, Nagashima K, Ott DE, Freed EO. Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLoS Pathog 2008, 4:e1000015. 10.1371/journal.ppat.1000015, 2267008, 18369466.
31. Yu HJ, Reuter MA, McDonald D. HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog 2008, 4:e1000134. 10.1371/journal.ppat.1000134, 2515344, 18725936.
32. Chen BK. T cell virological synapses and HIV-1 pathogenesis. Immunol Res 2012, 54:133-139. 10.1007/s12026-012-8320-8, 22477441.
33. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, Blot G, Leuba F, Escola JM, Demaurex N, Marsh M, Piguet V. HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 2005, 6:488-501. 10.1111/j.1600-0854.2005.00293.x, 15882445.
34. Ruiz-Mateos E, Pelchen-Matthews A, Deneka M, Marsh M. CD63 is not required for production of infectious human immunodeficiency virus type 1 in human macrophages. J Virol 2008, 82:4751-4761. 10.1128/JVI.02320-07, 2346747, 18321974.
35. Meissner EG, Duus KM, Gao F, Yu XF, Su L. Characterization of a thymus-tropic HIV-1 isolate from a rapid progressor: role of the envelope. Virology 2004, 328:74-88. 10.1016/j.virol.2004.07.019, 15380360.