Home LiteratureArticle Details
PMID: 23091068 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Critical role for the kinesin KIF3A in the HIV life cycle in primary human macrophages.

The Journal of cell biology ·Vol. 199 ·No. 3 ·2012-10-29 ·Pages 467-79

Gaudin R, de Alencar BC, Jouve M, Bèrre S, Le Bouder E, Schindler M, Varthaman A, Gobert FX, Benaroch P

Abstract

Macrophages are long-lived target cells for HIV infection and are considered viral reservoirs. HIV assembly in macrophages occurs in virus-containing compartments (VCCs) in which virions accumulate and are stored. The regulation of the trafficking and release of these VCCs remains unknown. Using high resolution light and electron microscopy of HIV-1-infected primary human macrophages, we show that the spatial distribution of VCCs depended on the microtubule network and that VCC-limiting membrane was closely associated with KIF3A+ microtubules. Silencing KIF3A strongly decreased virus release from HIV-1-infected macrophages, leading to VCC accumulation intracellularly. Time-lapse microscopy further suggested that VCCs and associated KIF3A move together along microtubules. Importantly, KIF3A does not play a role in HIV release from T cells that do not possess VCCs. These results reveal that HIV-1 requires the molecular motor KIF3 to complete its cycle in primary macrophages. Targeting this step may lead to novel strategies to eliminate this viral reservoir.

MeSH Terms
Blotting, Western Cells, Cultured HIV/physiology HIV Infections/virology Humans Kinesins/genetics,metabolism Macrophages/virology Microtubules/virology Virion/physiology
Chemicals
KIF3A protein, human Kinesins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Gaudin Raphaël
Institut Curie, Centre de Recherche, Paris, F-75248 France.
de Alencar Bruna Cunha
Jouve Mabel
Bèrre Stefano
Le Bouder Emmanuel
Schindler Michael
Varthaman Aditi
Gobert François-Xavier
Benaroch Philippe
References (41)
41 references, click to expand
  1. KIF3C and KIF3A form a novel neuronal heteromeric kinesin that associates with membrane vesicles.
    Mol Biol Cell. 1998 Mar;9(3):637-52 PMID: 9487132
  2. Kaposi's sarcoma-associated herpesvirus ORF45 interacts with kinesin-2 transporting viral capsid-tegument complexes along microtubules.
    PLoS Pathog. 2009 Mar;5(3):e1000332 PMID: 19282970
  3. 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 Aug;62(8):2578-86 PMID: 3260631
  4. Stability and specificity of heterodimer formation for the coiled-coil neck regions of the motor proteins Kif3A and Kif3B: the role of unstructured oppositely charged regions.
    J Pept Res. 2005 Feb;65(2):209-20 PMID: 15705165
  5. Traffic control: regulation of kinesin motors.
    Nat Rev Mol Cell Biol. 2009 Nov;10(11):765-77 PMID: 19851335
  6. The role of unstructured highly charged regions on the stability and specificity of dimerization of two-stranded alpha-helical coiled-coils: analysis of the neck-hinge region of the kinesin-like motor protein Kif3A.
    J Struct Biol. 2002 Jan-Feb;137(1-2):206-19 PMID: 12064947
  7. Evidence for human immunodeficiency virus type 1 replication in vivo in CD14(+) monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy.
    J Virol. 2002 Jan;76(2):707-16 PMID: 11752161
  8. Human macrophages accumulate HIV-1 particles in MHC II compartments.
    Traffic. 2002 Oct;3(10):718-29 PMID: 12230470
  9. Macrophages archive HIV-1 virions for dissemination in trans.
    EMBO J. 2005 Jul 6;24(13):2481-9 PMID: 15920469
  10. Microtubule-dependent movement of late endocytic vesicles in vitro: requirements for Dynein and Kinesin.
    Mol Biol Cell. 2004 Aug;15(8):3688-97 PMID: 15181154
  11. Kinesin-2 is a motor for late endosomes and lysosomes.
    Traffic. 2005 Dec;6(12):1114-24 PMID: 16262723
  12. Infectious HIV-1 assembles in late endosomes in primary macrophages.
    J Cell Biol. 2003 Aug 4;162(3):443-55 PMID: 12885763
  13. Focusing light on infection in four dimensions.
    Cell Microbiol. 2004 Apr;6(4):333-43 PMID: 15009025
  14. Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes.
    J Exp Med. 1988 Apr 1;167(4):1428-41 PMID: 3258626
  15. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding.
    Cell. 2001 Oct 5;107(1):55-65 PMID: 11595185
  16. Sequence of human immunodeficiency virus type 1 (HIV-1) Gag localization and oligomerization monitored with live confocal imaging of a replication-competent, fluorescently tagged HIV-1.
    J Virol. 2007 Nov;81(22):12596-607 PMID: 17728233
  17. Altered dynamics and differential infection profiles of lymphoid and myeloid cell subsets during acute and chronic HIV-1 infection.
    J Leukoc Biol. 2011 May;89(5):785-95 PMID: 21310820
  18. Genome-scale RNAi screen for host factors required for HIV replication.
    Cell Host Microbe. 2008 Nov 13;4(5):495-504 PMID: 18976975
  19. Primary human immunodeficiency virus type 2 (HIV-2) isolates, like HIV-1 isolates, frequently use CCR5 but show promiscuity in coreceptor usage.
    J Virol. 1999 Mar;73(3):2343-9 PMID: 9971817
  20. Intraflagellar transport motors in cilia: moving along the cell's antenna.
    J Cell Biol. 2008 Jan 14;180(1):23-9 PMID: 18180368
  21. Cellular reservoirs of HIV-1 and their role in viral persistence.
    Curr HIV Res. 2008 Sep;6(5):388-400 PMID: 18855649
  22. Kinesin superfamily motor proteins and intracellular transport.
    Nat Rev Mol Cell Biol. 2009 Oct;10(10):682-96 PMID: 19773780
  23. HIV assembly and budding in macrophages.
    Biochem Soc Trans. 2009 Feb;37(Pt 1):185-9 PMID: 19143628
  24. HIV-1 buds and accumulates in "nonacidic" endosomes of macrophages.
    Cell Host Microbe. 2007 Aug 16;2(2):85-95 PMID: 18005723
  25. Identification of host proteins required for HIV infection through a functional genomic screen.
    Science. 2008 Feb 15;319(5865):921-6 PMID: 18187620
  26. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding.
    Cell. 2003 Sep 19;114(6):689-99 PMID: 14505569
  27. Different microtubule motors move early and late endocytic compartments.
    Traffic. 2008 Apr;9(4):492-509 PMID: 18194411
  28. Macrophage internal HIV-1 is protected from neutralizing antibodies.
    J Virol. 2012 Mar;86(5):2826-36 PMID: 22205742
  29. HIV-1 buds predominantly at the plasma membrane of primary human macrophages.
    PLoS Pathog. 2007 Mar;3(3):e36 PMID: 17381240
  30. In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53.
    J Cell Biol. 2007 Apr 23;177(2):329-41 PMID: 17438075
  31. Stirring up development with the heterotrimeric kinesin KIF3.
    Traffic. 2000 Jan;1(1):29-34 PMID: 11208056
  32. KAP, the accessory subunit of kinesin-2, binds the predicted coiled-coil stalk of the motor subunits.
    Biochemistry. 2009 Mar 17;48(10):2248-60 PMID: 19161286
  33. Single molecule imaging reveals differences in microtubule track selection between Kinesin motors.
    PLoS Biol. 2009 Oct;7(10):e1000216 PMID: 19823565
  34. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1.
    J Virol. 2007 Jun;81(11):5547-60 PMID: 17360745
  35. Tubulation of class II MHC compartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells.
    J Immunol. 2007 Jun 1;178(11):7199-210 PMID: 17513769
  36. Plasma membrane is the site of productive HIV-1 particle assembly.
    PLoS Biol. 2006 Dec;4(12):e435 PMID: 17147474
  37. Inositol pyrophosphate mediated pyrophosphorylation of AP3B1 regulates HIV-1 Gag release.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21161-6 PMID: 19934039
  38. Macrophage are the principal reservoir and sustain high virus loads in rhesus macaques after the depletion of CD4+ T cells by a highly pathogenic simian immunodeficiency virus/HIV type 1 chimera (SHIV): Implications for HIV-1 infections of humans.
    Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):658-63 PMID: 11136236
  39. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress.
    Nat Med. 2001 Dec;7(12):1313-9 PMID: 11726971
  40. A guide to super-resolution fluorescence microscopy.
    J Cell Biol. 2010 Jul 26;190(2):165-75 PMID: 20643879
  41. Kinesin assembly and movement in cells.
    Annu Rev Biophys. 2011;40:267-88 PMID: 21332353
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
Published
2012-10-29
Epub
2012-00-22
Pages
467-79
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC3483138
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com