Human immunodeficiency virus type 1 endocytic trafficking through macrophage bridging conduits facilitates spread of infection

Journal of Neuroimmune Pharmacology

Volumn 6, Issue 4, 2011, Pages 658-675

  Kadiu, Irena ^a   Gendelman, Howard E ^a  

^a NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Bridging conduits; Early endosomes; Endocytic sorting; HIV 1; Intercellular viral spread; Lysosomes; Macrophage; Motor proteins; Multivesicular bodies; Recycling endosomes; Tubulin; Tunneling nanotubes; Viral trafficking

Indexed keywords

BLEBBISTATIN; CLATHRIN; CYTOCHALASIN D; MYOSIN II; RAB11 PROTEIN;

ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL SELECTION; CONTROLLED STUDY; DISEASE TRANSMISSION; ENDOPLASMIC RETICULUM; ENDOSOME; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; VIRUS ENTRY;

CELL COMMUNICATION; ENDOCYTOSIS; ENDOSOMES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; MACROPHAGES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON;

EID: 81355138720     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-011-9298-z     Document Type: Article

References (57)

1. M Babst DJ Katzmann EJ Estepa-Sabal T Meerloo SD Emr 2002 Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting Dev Cell 3 271 282 12194857 10.1016/S1534-5807(02)00220-4 1:CAS:528: DC%2BD38Xmtl2it7c%3D
2. E Basyuk T Galli M Mougel JM Blanchard M Sitbon E Bertrand 2003 Retroviral genomic RNAs are transported to the plasma membrane by endosomal vesicles Dev Cell 5 161 174 12852860 10.1016/S1534-5807(03)00188-6 1:CAS:528:DC%2BD3sXmt1Smsbw%3D (Pubitemid 36827350)
3. ME Beckner X Chen J An BW Day IF Pollack 2005 Proteomic characterization of harvested pseudopodia with differential gel electrophoresis and specific antibodies Lab Invest 85 316 327 15654357 10.1038/labinvest.3700239 1:CAS:528:DC%2BD2MXhtlertLs%3D (Pubitemid 40333149)
4. EJ Blott GM Griffiths 2002 Secretory lysosomes Nat Rev Mol Cell Biol 3 122 131 11836514 10.1038/nrm732 1:CAS:528:DC%2BD38XhsFSrs7w%3D
5. S Bolte FP Cordelieres 2006 A guided tour into subcellular colocalization analysis in light microscopy J Microsc 224 213 232 17210054 10.1111/j.1365-2818.2006.01706.x 1:CAS:528:DC%2BD2sXhvVWquro%3D (Pubitemid 46010930)
6. AL Brass DM Dykxhoorn Y Benita N Yan A Engelman RJ Xavier J Lieberman SJ Elledge 2008 Identification of host proteins required for HIV infection through a functional genomic screen Science 319 921 926 18187620 10.1126/science.1152725 1:CAS:528:DC%2BD1cXhslOmtL4%3D (Pubitemid 351263756)
7. NA Bright BJ Reaves BM Mullock JP Luzio 1997 Dense core lysosomes can fuse with late endosomes and are re-formed from the resultant hybrid organelles J Cell Sci 110 Pt 17 2027 2040 9378754 1:CAS:528:DyaK2sXmtlWqsLw%3D (Pubitemid 27440427)
8. K Brown SH Sacks W Wong 2008 Extensive and bidirectional transfer of major histocompatibility complex class II molecules between donor and recipient cells in vivo following solid organ transplantation FASEB J 22 3776 3784 18632850 10.1096/fj.08-107441 1:CAS:528:DC%2BD1cXhtlCgtrbN
9. C Bucci RG Parton IH Mather H Stunnenberg K Simons B Hoflack M Zerial 1992 The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway Cell 70 715 728 1516130 10.1016/0092-8674(92)90306-W 1:CAS:528:DyaK38XlvVyrt7w%3D
10. KM Callahan JF Rowell MJ Soloski CE Machamer RF Siliciano 1993 HIV-1 envelope protein is expressed on the surface of infected cells before its processing and presentation to class II-restricted T lymphocytes J Immunol 151 2928 2942 8376762 1:CAS:528:DyaK3sXms1yrtL0%3D (Pubitemid 23282606)
11. A Chauveau A Aucher P Eissmann E Vivier DM Davis 2010 Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells Proc Natl Acad Sci USA 107 5545 5550 20212116 10.1073/pnas.0910074107 1:CAS:528:DC%2BC3cXktFKhsLk%3D
12. HR Chinnery E Pearlman PG McMenamin 2008 Cutting edge: membrane nanotubes in vivo: a feature of MHC class II + cells in the mouse cornea J Immunol 180 5779 5783 18424694 1:CAS:528:DC%2BD1cXkvVequ7s%3D
13. S Christoforidis HM McBride RD Burgoyne M Zerial 1999 The Rab5 effector EEA1 is a core component of endosome docking Nature 397 621 625 10050856 10.1038/17618 1:CAS:528:DyaK1MXhtlyitb4%3D (Pubitemid 29091948)
14. P Ciborowski HE Gendelman 2006 Human immunodeficiency virus-mononuclear phagocyte interactions: emerging avenues of biomarker discovery, modes of viral persistence and disease pathogenesis Curr HIV Res 4 279 291 16842081 10.2174/157016206777709474 1:CAS:528:DC%2BD28XmvV2mtrs%3D (Pubitemid 44027718)
15. A de Gassart C Geminard D Hoekstra M Vidal 2004 Exosome secretion: the art of reutilizing nonrecycled proteins? Traffic 5 896 903 15479454 10.1111/j.1600-0854.2004.00223.x (Pubitemid 39433559)
16. M Deneka A Pelchen-Matthews R Byland E Ruiz-Mateos M Marsh 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 17438075 10.1083/jcb.200609050 1:CAS:528:DC%2BD2sXks1Kqt7o%3D (Pubitemid 46658643)
17. AS DePina GM Langford 1999 Vesicle transport: the role of actin filaments and myosin motors Microsc Res Tech 47 93 106 10523788 10.1002/(SICI)1097- 0029(19991015)47:2<93::AID-JEMT2>3.0.CO;2-P 1:STN:280:DyaK1MvlsVOltw%3D%3D (Pubitemid 29519818)
18. R Dixit V Tiwari D Shukla 2008 Herpes simplex virus type 1 induces filopodia in differentiated P19 neural cells to facilitate viral spread Neurosci Lett 440 113 118 18554796 10.1016/j.neulet.2008.05.031 1:CAS:528: DC%2BD1cXnsFClsLo%3D
19. DJ Eilbott N Peress H Burger D LaNeve J Orenstein HE Gendelman R Seidman B Weiser 1989 Human immunodeficiency virus type 1 in spinal cords of acquired immunodeficiency syndrome patients with myelopathy: expression and replication in macrophages Proc Natl Acad Sci USA 86 3337 3341 2717618 10.1073/pnas.86.9. 3337 1:STN:280:DyaL1M3ktVOhug%3D%3D (Pubitemid 19129606)
20. EA Eugenin PJ Gaskill JW Berman 2009 Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking Cell Immunol 254 142 148 18835599 10.1016/j.cellimm.2008.08.005 1:CAS:528:DC%2BD1cXhsV2gt7%2FI
21. EA Eugenin PJ Gaskill JW Berman 2009 Tunneling nanotubes (TNT): a potential mechanism for intercellular HIV trafficking Commun Integr Biol 2 243 244 19641744 10.4161/cib.2.3.8165 1:CAS:528:DC%2BD1MXht1yru7fL
22. DM Fernandes L Vidard KL Rock 2000 Characterization of MHC class II-presented peptides generated from an antigen targeted to different endocytic compartments Eur J Immunol 30 2333 2343 10940924 10.1002/1521-4141(2000)30: 8<2333::AID-IMMU2333>3.0.CO;2-F 1:CAS:528:DC%2BD3cXlvFenu7Y%3D (Pubitemid 30655769)
23. JE Garrus UK von Schwedler OW Pornillos SG Morham KH Zavitz HE Wang DA Wettstein KM Stray M Cote RL Rich DG Myszka WI Sundquist 2001 Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding Cell 107 55 65 11595185 10.1016/S0092-8674(01)00506-2 1:CAS:528:DC%2BD3MXnsFOntLo%3D (Pubitemid 32972037)
24. HE Gendelman JM Orenstein MA Martin C Ferrua R Mitra T Phipps LA Wahl HC Lane AS Fauci DS Burke, et al. 1988 Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes J Exp Med 167 1428 1441 3258626 10.1084/jem.167.4.1428 1:CAS:528:DyaL1cXit1Sitr0%3D
25. HH Gerdes NV Bukoreshtliev JF Barroso 2007 Tunneling nanotubes: a new route for the exchange of components between animal cells FEBS Lett 581 2194 2201 17433307 10.1016/j.febslet.2007.03.071 1:CAS:528:DC%2BD2sXlt1ChsLw%3D (Pubitemid 46709910)
26. DJ Gill H Teo J Sun O Perisic DB Veprintsev SD Emr RL Williams 2007 Structural insight into the ESCRT-I/-II link and its role in MVB trafficking EMBO J 26 600 612 17215868 10.1038/sj.emboj.7601501 1:CAS:528: DC%2BD2sXotFKgtw%3D%3D (Pubitemid 46160959)
27. K Gousset E Schiff C Langevin Z Marijanovic A Caputo DT Browman N Chenouard F de Chaumont A Martino J Enninga JC Olivo-Marin D Mannel C Zurzolo 2009 Prions hijack tunnelling nanotubes for intercellular spread Nat Cell Biol 11 328 336 19198598 10.1038/ncb1841 1:CAS:528:DC%2BD1MXisVOlsb4%3D
28. J Gruenberg H Stenmark 2004 The biogenesis of multivesicular endosomes Nat Rev Mol Cell Biol 5 317 323 15071556 10.1038/nrm1360 1:CAS:528: DC%2BD2cXivV2itrg%3D (Pubitemid 38480612)
29. M Jouve N Sol-Foulon S Watson O Schwartz P Benaroch 2007 HIV-1 buds and accumulates in "nonacidic" endosomes of macrophages Cell Host Microbe 2 85 95 18005723 10.1016/j.chom.2007.06.011 1:CAS:528:DC%2BD2sXpsFelt7o%3D (Pubitemid 47209523)
30. I Kadiu HE Gendelman 2011 Macrophage bridging conduit trafficking of HIV-1 through the endoplasmic reticulum and Golgi network J Proteome Res 10 7 3225 3238 21563830 10.1021/pr200262q 1:CAS:528:DC%2BC3MXntVGisrs%3D
31. I Kadiu M Ricardo-Dukelow P Ciborowski HE Gendelman 2007 Cytoskeletal protein transformation in HIV-1-infected macrophage giant cells J Immunol 178 6404 6415 17475870 1:CAS:528:DC%2BD2sXksl2nu7Y%3D (Pubitemid 46717424)
32. I Kadiu T Wang JD Schlautman L Dubrovsky P Ciborowski M Bukrinsky HE Gendelman 2009 HIV-1 transforms the monocyte plasma membrane proteome Cell Immunol 258 44 58 19358982 10.1016/j.cellimm.2009.03.012 1:CAS:528: DC%2BD1MXmtVeitrs%3D
33. EA Lundquist 2009 The finer points of filopodia PLoS Biol 7 e1000142 19564901 10.1371/journal.pbio.1000142
34. Luzio JP, Pryor PR, Gray SR, Gratian MJ, Piper RC, Bright NA (2005) Membrane traffic to and from lysosomes. Biochem Soc Symp 72:77-86 (Pubitemid 44804737)
35. N Martin Q Sattentau 2009 Cell-to-cell HIV-1 spread and its implications for immune evasion Curr Opin HIV AIDS 4 143 149 19339954 10.1097/COH. 0b013e328322f94a
36. FR Maxfield TE McGraw 2004 Endocytic recycling Nat Rev Mol Cell Biol 5 121 132 15040445 10.1038/nrm1315 1:CAS:528:DC%2BD2cXnsFOjtg%3D%3D (Pubitemid 38160255)
37. K Miyauchi Y Kim O Latinovic V Morozov GB Melikyan 2009 HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes Cell 137 433 444 19410541 10.1016/j.cell.2009.02.046 1:CAS:528:DC%2BD1MXlvFams78%3D
38. B Onfelt S Nedvetzki RK Benninger MA Purbhoo S Sowinski AN Hume MC Seabra MA Neil PM French DM Davis 2006 Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria J Immunol 177 8476 8483 17142745 (Pubitemid 44893810)
39. JM Orenstein MS Meltzer T Phipps HE Gendelman 1988 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 62 2578 2586 3260631 1:STN:280:DyaL1c3nsFShsw%3D%3D
40. DE Ott LV Coren DG Johnson BP Kane RC Sowder 2nd YD Kim RJ Fisher XZ Zhou KP Lu LE Henderson 2000 Actin-binding cellular proteins inside human immunodeficiency virus type 1 Virology 266 42 51 10612659 10.1006/viro.1999.0075 1:CAS:528:DyaK1MXotFGktrg%3D (Pubitemid 30048635)
41. A Pelchen-Matthews B Kramer M Marsh 2003 Infectious HIV-1 assembles in late endosomes in primary macrophages J Cell Biol 162 443 455 12885763 10.1083/jcb.200304008 1:CAS:528:DC%2BD3sXmt1Cru78%3D (Pubitemid 36988553)
42. EJ Platt K Wehrly SE Kuhmann B Chesebro D Kabat 1998 Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1 J Virol 72 2855 2864 9525605 1:CAS:528:DyaK1cXhvVKqu7g%3D (Pubitemid 28175522)
43. G Raposo M Moore D Innes R Leijendekker A Leigh-Brown P Benaroch H Geuze 2002 Human macrophages accumulate HIV-1 particles in MHC II compartments Traffic 3 718 729 12230470 10.1034/j.1600-0854.2002.31004.x 1:CAS:528: DC%2BD38XnsFKlsLw%3D
44. P Romagnoli C Layet J Yewdell O Bakke RN Germain 1993 Relationship between invariant chain expression and major histocompatibility complex class II transport into early and late endocytic compartments J Exp Med 177 583 596 8436902 10.1084/jem.177.3.583 1:CAS:528:DyaK3sXhsVGms74%3D (Pubitemid 23104269)
45. A Rustom R Saffrich I Markovic P Walther HH Gerdes 2004 Nanotubular highways for intercellular organelle transport Science 303 1007 1010 14963329 10.1126/science.1093133 1:CAS:528:DC%2BD2cXhtlWnu7w%3D (Pubitemid 38209703)
46. N Sharova C Swingler M Sharkey M Stevenson 2005 Macrophages archive HIV-1 virions for dissemination in trans EMBO J 24 2481 2489 15920469 10.1038/sj.emboj.7600707 1:CAS:528:DC%2BD2MXlvVWqsbk%3D (Pubitemid 41032598)
47. NM Sherer W Mothes 2008 Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis Trends Cell Biol 18 414 420 18703335 10.1016/j.tcb.2008.07.003 1:CAS:528:DC%2BD1cXhtVOhsrzP
48. NM Sherer MJ Lehmann LF Jimenez-Soto C Horensavitz M Pypaert W Mothes 2007 Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission Nat Cell Biol 9 310 315 17293854 10.1038/ncb1544 1:CAS:528:DC%2BD2sXit12rsr4%3D (Pubitemid 46344610)
49. Simons M, Raposo G (2009) Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol
50. S Sowinski C Jolly O Berninghausen MA Purbhoo A Chauveau K Kohler S Oddos P Eissmann FM Brodsky C Hopkins B Onfelt Q Sattentau DM Davis 2008 Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission Nat Cell Biol 10 211 219 18193035 10.1038/ncb1682 1:CAS:528:DC%2BD1cXhs1Kiuro%3D (Pubitemid 351194051)
51. M Trischler W Stoorvogel O Ullrich 1999 Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway J Cell Sci 112 Pt 24 4773 4783 10574724 1:CAS:528:DC%2BD3cXntlGgsA%3D%3D (Pubitemid 30034824)
52. PD Uchil W Mothes 2009 HIV entry revisited Cell 137 402 404 19410537 10.1016/j.cell.2009.04.033 1:CAS:528:DC%2BD1MXlvFamsrk%3D
53. L Vonna A Wiedemann M Aepfelbacher E Sackmann 2007 Micromechanics of filopodia mediated capture of pathogens by macrophages Eur Biophys J 36 145 151 17160406 10.1007/s00249-006-0118-y 1:STN:280:DC%2BD2s%2FkvVyrtQ%3D%3D (Pubitemid 46175653)
54. JJ Wang S Sandefur P Spearman CT Chiou PH Chiang L Ratner 2001 Tracking the assembly pathway of human immunodeficiency virus type 1 Gag deletion mutants by immunogold labeling Appl Immunohistochem Mol Morphol 9 371 379 11759066 10.1097/00022744-200112000-00014 1:CAS:528:DC%2BD3MXpt1GqtbY%3D (Pubitemid 33098149)
55. S Welsch OT Keppler A Habermann I Allespach J Krijnse-Locker HG Krausslich 2007 HIV-1 buds predominantly at the plasma membrane of primary human macrophages PLoS Pathog 3 e36 17381240 10.1371/journal.ppat.0030036 (Pubitemid 46535810)
56. W Xu PA Santini JS Sullivan B He M Shan SC Ball WB Dyer TJ Ketas A Chadburn L Cohen-Gould DM Knowles A Chiu RW Sanders K Chen A Cerutti 2009 HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits Nat Immunol 10 1008 1017 19648924 10.1038/ni.1753 1:CAS:528:DC%2BD1MXpt1Ogtr8%3D
57. M Zerial H McBride 2001 Rab proteins as membrane organizers Nat Rev Mol Cell Biol 2 107 117 11252952 10.1038/35052055 1:CAS:528:DC%2BD3MXivVSitL8%3D (Pubitemid 33674039)