Home LiteratureArticle Details
PMID: 16505369 Published · ppublish English Journal Article

R5 and X4 HIV envelopes induce distinct gene expression profiles in primary peripheral blood mononuclear cells.

Cicala C, Arthos J, Martinelli E, Censoplano N, Cruz CC, Chung E, Selig SM, Van Ryk D, Yang J, Jagannatha S, Chun TW, Ren P, Lempicki RA, Fauci AS

Abstract

HIV envelope binds to and signals through its primary cellular receptor, CD4, and through a coreceptor, either CC chemokine receptor 5 (CCR5) or CXC chemokine receptor 4 (CXCR4). Here, we evaluate the response of peripheral blood mononuclear cells to a panel of genetically diverse R5 and X4 envelope proteins. Modulation of gene expression was evaluated by using oligonucleotide microarrays. Activation of transcription factors was evaluated by using an array of oligonucleotides encoding transcription factor binding sites. Responses were strongly influenced by coreceptor specificity. Treatment of cells from CCR5delta32 homozygous donors with glycoprotein (gp)120 derived from an R5 virus demonstrated that the majority of responses elicited by R5 envelopes required engagement of CCR5. R5 envelopes, to a greater extent than X4 envelopes, induced the expression of genes belonging to mitogen-activated protein kinase signal transduction pathways and genes regulating the cell cycle. A number of genes induced by R5, but not X4, envelopes were also up-regulated in the resting CD4+ T cell population of HIV-infected individuals. These results suggest that R5 envelope facilitates replication of HIV in the pool of resting CD4+ T cells. Additionally, signaling by R5 gp120 may facilitate the transmission of R5 viruses by inducing a permissive environment for HIV replication.

MeSH Terms
CD4-Positive T-Lymphocytes/immunology,metabolism,pathology,virology Cell Cycle/genetics Cell Proliferation Gene Expression Profiling HIV Envelope Protein gp120/immunology HIV Infections/genetics,immunology,pathology,virology HIV-1/immunology,pathogenicity,physiology Humans In Vitro Techniques Leukocytes, Mononuclear/immunology,metabolism,pathology,virology Receptors, CCR5/metabolism Receptors, CXCR4/metabolism Signal Transduction Transcription Factors/genetics Virus Replication
Chemicals
HIV Envelope Protein gp120 Receptors, CCR5 Receptors, CXCR4 Transcription Factors
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Cicala Claudia
Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA. ccicala@niaid.nih.gov
Arthos James
Martinelli Elena
Censoplano Nina
Cruz Catherine C
Chung Eva
Selig Sara M
Van Ryk Donald
Yang Jun
Jagannatha Shyla
Chun Tae Wook
Ren Ping
Lempicki Richard A
Fauci Anthony S
References (41)
41 references, click to expand
  1. Inhibition of CD3/CD28-mediated activation of the MEK/ERK signaling pathway represses replication of X4 but not R5 human immunodeficiency virus type 1 in peripheral blood CD4(+) T lymphocytes.
    J Virol. 2000 Mar;74(6):2558-66 PMID: 10684270
  2. Identifying biological themes within lists of genes with EASE.
    Genome Biol. 2003;4(10):R70 PMID: 14519205
  3. Reciprocal regulation of the nuclear factor of activated T cells and HIV-1.
    Genes Immun. 2004 May;5(3):158-67 PMID: 14762397
  4. Reservoirs for HIV-1.
    Curr Infect Dis Rep. 1999 Aug;1(3):298-304 PMID: 11095802
  5. HIV envelope induces a cascade of cell signals in non-proliferating target cells that favor virus replication.
    Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9380-5 PMID: 12089333
  6. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5.
    Nature. 1996 Jun 20;381(6584):667-73 PMID: 8649512
  7. Gene expression and viral prodution in latently infected, resting CD4+ T cells in viremic versus aviremic HIV-infected individuals.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1908-13 PMID: 12552096
  8. NFAT1 enhances HIV-1 gene expression in primary human CD4 T cells.
    Clin Immunol. 2000 Mar;94(3):179-91 PMID: 10692237
  9. Binding of human immunodeficiency virus type 1 to CD4 and CXCR4 receptors differentially regulates expression of inflammatory genes and activates the MEK/ERK signaling pathway.
    J Virol. 1998 Aug;72(8):6406-13 PMID: 9658081
  10. Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy.
    Nat Med. 1999 May;5(5):512-7 PMID: 10229227
  11. Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis.
    J Exp Med. 1992 Oct 1;176(4):1099-106 PMID: 1402655
  12. The role of the CD4 receptor versus HIV coreceptors in envelope-mediated apoptosis in peripheral blood mononuclear cells.
    Virology. 2002 Jan 5;292(1):98-106 PMID: 11878912
  13. Effect of human immunodeficiency virus gp120 glycoprotein on the association of the protein tyrosine kinase p56lck with CD4 in human T lymphocytes.
    J Biol Chem. 1991 Jun 15;266(17):11176-83 PMID: 2040625
  14. Human immunodeficiency virus type-1 and chemokines: beyond competition for common cellular receptors.
    Cytokine Growth Factor Rev. 2001 Jun-Sep;12(2-3):219-43 PMID: 11325604
  15. Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences.
    J Virol. 2003 Dec;77(24):13376-88 PMID: 14645592
  16. Identification of a major co-receptor for primary isolates of HIV-1.
    Nature. 1996 Jun 20;381(6584):661-6 PMID: 8649511
  17. Genotypic and phenotypic characterization of HIV-1 patients with primary infection.
    Science. 1993 Aug 27;261(5125):1179-81 PMID: 8356453
  18. Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor.
    Nature. 1997 Oct 30;389(6654):981-5 PMID: 9353123
  19. Latent reservoirs of HIV: obstacles to the eradication of virus.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):10958-61 PMID: 10500107
  20. HIV envelope induces virus expression from resting CD4+ T cells isolated from HIV-infected individuals in the absence of markers of cellular activation or apoptosis.
    J Immunol. 2003 Mar 1;170(5):2449-55 PMID: 12594269
  21. HIV-1 gp120 induces NFAT nuclear translocation in resting CD4+ T-cells.
    Virology. 2006 Feb 5;345(1):105-14 PMID: 16260021
  22. V3: HIV's switch-hitter.
    AIDS Res Hum Retroviruses. 2005 Feb;21(2):171-89 PMID: 15725757
  23. Perils at mucosal front lines for HIV and SIV and their hosts.
    Nat Rev Immunol. 2005 Oct;5(10):783-92 PMID: 16200081
  24. Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5.
    J Exp Med. 1997 Nov 17;186(10):1793-8 PMID: 9362541
  25. Role of p38 mitogen-activated protein kinase in HIV type 1 production in vitro.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7422-6 PMID: 9636165
  26. Cell type-specific fusion cofactors determine human immunodeficiency virus type 1 tropism for T-cell lines versus primary macrophages.
    J Virol. 1996 Aug;70(8):5487-94 PMID: 8764060
  27. HIV-1 coreceptor usage, transmission, and disease progression.
    Curr HIV Res. 2003 Apr;1(2):217-27 PMID: 15043204
  28. MAP kinases in the immune response.
    Annu Rev Immunol. 2002;20:55-72 PMID: 11861597
  29. Mechanisms of CD4+ T lymphocyte cell death in human immunodeficiency virus infection and AIDS.
    J Gen Virol. 2003 Jul;84(Pt 7):1649-61 PMID: 12810858
  30. Human T cell transcription factor GATA-3 stimulates HIV-1 expression.
    Nucleic Acids Res. 1993 Jun 25;21(12):2831-6 PMID: 8332492
  31. Macrophage activation through CCR5- and CXCR4-mediated gp120-elicited signaling pathways.
    J Leukoc Biol. 2003 Nov;74(5):676-82 PMID: 12960231
  32. T cell dynamics in HIV-1 infection.
    Annu Rev Immunol. 2003;21:265-304 PMID: 12524385
  33. Host control of HIV-1 parasitism in T cells by the nuclear factor of activated T cells.
    Cell. 1998 Nov 25;95(5):595-604 PMID: 9845362
  34. Suppression of HIV-1 viral replication and cellular pathogenesis by a novel p38/JNK kinase inhibitor.
    AIDS. 2004 Mar 26;18(5):739-48 PMID: 15075508
  35. HIV-1 gp120 chemokine receptor-mediated signaling in human macrophages.
    Immunol Res. 2003;27(2-3):261-76 PMID: 12857973
  36. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor.
    Science. 1996 May 10;272(5263):872-7 PMID: 8629022
  37. The CCR5 and CXCR4 coreceptors--central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection.
    AIDS Res Hum Retroviruses. 2004 Jan;20(1):111-26 PMID: 15000703
  38. Cellular gene expression upon human immunodeficiency virus type 1 infection of CD4(+)-T-cell lines.
    J Virol. 2003 Jan;77(2):1392-402 PMID: 12502855
  39. Protection against lethal simian immunodeficiency virus SIVsmmPBj14 disease by a recombinant Semliki Forest virus gp160 vaccine and by a gp120 subunit vaccine.
    J Virol. 1996 Mar;70(3):1953-60 PMID: 8627721
  40. Issues in T-helper 1 development--resolved and unresolved.
    Immunol Rev. 2004 Dec;202:157-74 PMID: 15546392
  41. Induction of phosphorylation and intracellular association of CC chemokine receptor 5 and focal adhesion kinase in primary human CD4+ T cells by macrophage-tropic HIV envelope.
    J Immunol. 1999 Jul 1;163(1):420-6 PMID: 10384144
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2006-03-07
Epub
2006-00-27
Pages
3746-51
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1533779
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