CCR5 signaling through phospholipase D involves p44/42 MAP-kinases and promotes HIV-1 LTR-directed gene expression

FASEB Journal

Volumn 21, Issue 14, 2007, Pages 4038-4046

  Paruch, Sylvain ^a,b   Heinis, Mylène ^a,b   Lemay, Julie ^a,b   Hoeffel, Guillaume ^a,b   Marañón, Concepción ^a,b   Hosmalin, Anne ^a,b   Périanin, Axel ^a,b  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

Author keywords

HIV 1 coreceptors; Infection; Signal transducers

Indexed keywords

CHEMOKINE RECEPTOR CCR5; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOLIPASE D;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERMINAL REPEAT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

CHOLINE; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHOLIPASE D; RECEPTORS, CCR5; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 36849032786     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7325com     Document Type: Article

References (53)

1. Alkhatib, G., Combadiere, C., Broder, C. C., Feng, Y., Kennedy, P. E., Murphy, P. M., and Berger, E. A. (1996) CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272, 1955-1958
2. Arthos, J., Rubbert, A., Rabin, R. L., Cicala, C., Machado, E., Wildt, K., Hanbach, M., Steenbeke, T. D., Swofford, R., Farber, J. M., and Fauci, A. S. (2000) CCR5 signal transduction in macrophages by human immunodeficiency virus and simian immunodeficiency virus envelopes. J. Virol. 74, 6418-6424
3. Zack, J. A., Arrigo, S. J., Weitsman, S. R., Go, A. S., Haislip, A., and Chen, I. S. (1990) HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61, 213-222
4. Bukrinskaya, A., Brichacek, B., Mann, A., and Stevenson, M. (1998) Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 188, 2113-2125
5. Zagury, D., Bernard, J., Leonard, R., Cheynier, R., Feldman, M., Sarin, P. S., and Gallo, R. C. (1986) Long-term cultures of HTLV-III-infected T cells: a model of cytopathology of T-cell depletion in AIDS. Science 231, 850-853
6. McCune, J. M. (1995) Viral latency in HIV disease. Cell 82, 183-188
7. Dayton, A. I., Sodroski, J. G., Rosen, C. A., Goh, W. C., and Haseltine, W. A. (1986) The trans-activator gene of the human T cell lymphotropic virus type III is required for replication. Cell 44, 941-947
8. Fisher, A. G., Feinberg, M. B., Josephs, S. F., Harper, M. E., Marselle, L. M., Reyes, G., Gonda, M. A., Aldovini, A., Debouk, C., Gallo, R. C., et al. (1986) The trans-activator gene of HTLV-III is essential for virus replication. Nature 320, 367-371
9. Gaynor, R. (1992) Cellular transcription factors involved in the regulation of HIV-1 gene expression. AIDS 6, 347-363
10. Rohr, O., Marban, C., Aunis, D., and Schaeffer, E. (2003) Regulation of HIV-1 gene transcription: from lymphocytes to microglial cells. J. Leukoc. Biol. 74, 736-749
11. Kreisberg, J. F., Yonemoto, W., and Greene, W. C. (2006) Endogenous factors enhance HIV infection of tissue naive CD4 T cells by stimulating high molecular mass APOBEC3G complex formation. J. Exp. Med. 203, 865-870
12. Harada, S., Koyanagi, Y., Nakashima, H., Kobayashi, N., and Yamamoto, N. (1986) Tumor promoter, TPA, enhances replication of HTLV-III/LAV. Virology 154, 249-258
13. Jakobovits, A., Rosenthal, A., and Capon, D. J. (1990) Transactivation of HIV-1 LTR-directed gene expression by tat requires protein kinase C. EMBO J. 9, 1165-1170
14. Klebanoff, S. J., and Headley, C. M. (1999) Activation of the human immunodeficiency virus-1 long terminal repeat by respiratory burst oxidants of neutrophils. Blood 93, 350-356
15. Lin, Y. L., Mettling, C., Portales, P., Reynes, J., Clot, J., and Corbeau, P. (2002) Cell surface CCR5 density determines the postentry efficiency of R5 HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 99, 15590-15595
16. Lin, Y. L., Mettling, C., Portales, P., Reant, B., Robert-Hebmann, V., Reynes, J., Clot, J., and Corbeau, P. (2006) The efficiency of R5 HIV-1 infection is determined by CD4 T-cell surface CCR5 density through G alpha i-protein signalling. AIDS 20, 1369-1377
17. Rizzi, C., Crippa, M. P., Jeeninga, R. E., Berkhout, B., Blasi, F., Poli, G., and Alfano, M. (2006) Pertussis toxin B-oligomer suppresses IL-6 induced HIV-1 and chemokine expression in chronically infected U1 cells via inhibition of activator protein 1. J. Immunol. 176, 999-1006
18. Francois, F., and Klotman, M. E. (2003) Phosphatidylinositol 3-kinase regulates human immunodeficiency virus type 1 replication following viral entry in primary CD4(+) T lymphocytes and macrophages. J. Virol. 77, 2539-2549
19. West, M. J., Lowe, A. D., and Karn, J. (2001) Activation of human immunodeficiency virus transcription in T cells revisited: NF-kappaB p65 stimulates transcriptional elongation. J. Virol. 75, 8524-8537
20. Yang, X., Chen, Y., and Gabuzda, D. (1999) ERK MAP kinase links cytokine signals to activation of latent HIV-1 infection by stimulating a cooperative interaction of AP-1 and NF-kappaB. J. Biol. Chem. 274, 27981-27988
21. Billah, M. M., Eckel, S., Mullmann, T. J., Egan, R. W., and Siegel, M. I. (1989) Phosphatidylcholine hydrolysis by phospholipase D determines phosphatidate and diglyceride levels in chemotactic peptide-stimulated human neutrophils. Involvement of phosphatidate phosphohydrolase in signal transduction. J. Biol. Chem. 264, 17069-17077
22. Liscovitch, M., Ben-Av, P., Danin, M., Faiman, G., Eldar, H., and Livneh, E. (1993) Phospholipase D-mediated hydrolysis of phosphatidylcholine: role in cell signalling. J. Lipid. Mediat. 8, 177-182
23. Exton, J. H. (2002) Phospholipase D - structure, regulation and function. Rev. Physiol. Biochem. Pharmacol. 144, 1-94
24. Gutkind, J. (2000) Regulation of mitogen-activated protein kinase signalling networks by G-protein-coupled receptors. Sci. STKE 2000, RE1
25. Hammond, S. M., Altshuller, Y. M., Sung, T. C., Rudge, S. A., Rose, K., Engebrecht, J., Morris, A. J., and Frohman, M. A. (1995) Human ADP-ribosylation factor-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J. Biol. Chem. 270, 29640-29643
26. Paruch, S., El-Benna, J., Djerdjouri, B., Marullo, S., and Perianin, A. (2006) A role of p44/42 mitogen-activated protein kinases in formyl-peptide receptor-mediated phospholipase D activity and oxidant production. F ASEB J. 20, 142-144
27. Su, S. B., Gong, W. H., Gao, J. L., Shen, W. P., Grimm, M. C., Deng, X., Murphy, P. M., Oppenheim, J. J., and Wang, J. M. (1999) T20/DP178, an ectodomain peptide of human immunodeficiency virus type 1 gp41, is an activator of human phagocyte N-formyl peptide receptor. Blood 93, 3885-3892
28. Fang, Y., Park, I. H., Wu, A. L., Du, G., Huang, P., Frohman, M. A., Walker, S. J., Brown, H. A., and Chen, J. (2003) PLD1 regulates mTOR signaling and mediates Cdc42 activation of S6K1. Curr. Biol. 13, 2037-2044
29. Powner, D. J., Payne, R. M., Pettitt, T. R., Giudici, M. L., Irvine, R. F., and Wakelam, M. J. (2005) Phospholipase D2 stimulates integrin-mediated adhesion via phosphatidylinositol 4-phosphate 5-kinase Igamma b. J. Cell Sci. 118, 2975-2986
30. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498
31. Sung, T. C., Roper, R. L., Zhang, Y., Rudge, S. A., Temel, R., Hammond, S. M., Morris, A. J., Moss, B., Engebrecht, J., and Frohman, M. A. (1997) Mutagenesis of phospholipase D defines a superfamily including a trans-Golgi viral protein required for poxvirus pathogenicity. EMBO J. 16, 4519-4530
32. Brunet, A., Pages, G., and Pouyssegur, J. (1994) Constitutively active mutants of MAP kinase kinase (MEK1) induce growth factor-relaxation and oncogenicity when expressed in fibroblasts. Oncogene 9, 3379-3387
33. Bar, S., and Alizon, M. (2004) Role of the ectodomain of the gp41 transmembrane envelope protein of human immunodeficiency virus type 1 in late steps of the membrane fusion process. J. Virol. 78, 811-820
34. Chackerian, B., Long, E. M., Luciw, P. A., and Overbaugh, J. (1997) Human immunodeficiency virus type 1 coreceptors participate in postentry stages in the virus replication cycle and function in simian immunodeficiency virus infection. J. Virol. 71, 3932-3939
35. Deng, H., Liu, R., Ellmeier, W., Choe, S., Unutmaz, D., Burkhart, M., Di Marzio, P., Marmon, S., Sutton, R. E., Hill, C. M., et al. (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature 381, 661-666
36. Kwan, W. H., Helt, A. M., Maranon, C., Barbaroux, J. B., Hosmalin, A., Harris, E., Fridman, W. H., and Mueller, C. G. (2005) Dendritic cell precursors are permissive to dengue virus and human immunodeficiency virus infection. J. Virol. 79, 7291-7299
37. Pedruzzi, E., Hakim, J., Giroud, J. P., and Perianin, A. (1998) Analysis of choline and phosphorylcholine content in human neutrophils stimulated by f-Met-Leu-Phe and phorbol myristate acetate: contribution of phospholipase D and C. Cell. Signal. 10, 481-489
38. Pirounaki, M., Heyden, N. A., Arens, M., and Ratner, L. (2000) Rapid phenotypic drug susceptibility assay for HIV-1 with a CCR5 expressing indicator cell line. J. Virol. Methods 85, 151-161
39. Kutsch, O., Benveniste, E. N., Shaw, G. M., and Levy, D. N. (2002) Direct and quantitative single-cell analysis of human immunodeficiency virus type 1 reactivation from latency. J. Virol. 76, 8776-8786
40. Oppermann, M. (2004) Chemokine receptor CCR5: insights into structure, function, and regulation. Cell. Signal. 16, 1201-1210
41. Dang, P. M., Rais, S., Hakim, J., and Perianin, A. (1995) Redistribution of protein kinase C isoforms in human neutrophils stimulated by formyl peptides and phorbol myristate acetate. Biochem. Biophys. Res. Commun. 212, 664-672
42. Muthalif, M. M., Parmentier, J. H., Benter, I. F., Karzoun, N., Ahmed, A., Khandekar, Z., Adl, M. Z., Bourgoin, S., and Malik, K. U. (2000) Ras/mitogen-activated protein kinase mediates norepinephrine-induced phospholipase D activation in rabbit aortic smooth muscle cells by a phosphorylation-dependent mechanism. J. Pharmacol. Exp. Ther. 293, 268-274
43. Luttrell, L. M., Roudabush, F. L., Choy, E. W., Miller, W. E., Field, M. E., Pierce, K. L., and Lefkowitz, R. J. (2001) Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds. Proc. Natl. Acad. Sci. U. S. A. 98, 2449-2454
44. Gosling, J., Monteclaro, F. S., Atchison, R. E., Arai, H., Tsou, C. L., Goldsmith, M. A., and Charo, I. F. (1997) Molecular uncoupling of C-C chemokine receptor 5-induced chemotaxis and signal transduction from HIV-1 coreceptor activity. Proc. Natl. Acad. Sci. U. S. A. 94, 5061-5066
45. Arai, H., and Charo, I. F. (1996) Differential regulation of G-protein-mediated signaling by chemokine receptors. J. Biol. Chem. 271, 21814-21819
46. Mueller, A., and Strange, P. G. (2004) CCL3, acting via the chemokine receptor CCR5, leads to independent activation of Janus kinase 2 (JAK2) and Gi proteins. FEBS Lett. 570, 126-132
47. Leung, D. W., Peterson, P. K., Weeks, R., Gekker, G., Chao, C. C., Kaplan, A. H., Balantac, N., Tompkins, C., Underiner, G. E., Bursten, S., et al. (1995) CT-2576, an inhibitor of phospholipid signaling, suppresses constitutive and induced expression of human immunodeficiency virus. Proc. Natl. Acad. Sci. U. S. A. 92, 4813-4817
48. Benelli, R., Barbero, A., Ferrini, S., Scapini, P., Cassatella, M., Bussolino, F., Tacchetti, C., Noonan, D. M., and Albini, A. (2000) Human immunodeficiency virus transactivator protein (Tat) stimulates chemotaxis, calcium mobilization, and activation of human polymorphonuclear leukocytes: implications for Tat-mediated pathogenesis. J. Infect. Dis. 182, 1643-1651
49. Treisman, R. (1996) Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8, 205-215
50. Pereira, L. A., Bentley, K., Peeters, A., Churchill, M. J., and Deacon, N. J. (2000) A compilation of cellular transcription factor interactions with the HIV-1 LTR promoter. Nucleic Acids Res. 28, 663-668
51. Hu, Q., Natarajan, V., and Ziegelstein, R. C. (2002) Phospholipase D regulates calcium oscillation frequency and nuclear factor-kappaB activity in histamine-stimulated human endothelial cells. Biochem. Biophys. Res. Commun. 292, 325-332
52. Kwun, H. J., Lee, J. H., Min do, S., and Jang, K. L. (2003) Transcriptional repression of cyclin-dependent kinase inhibitor p21 gene by phospholipase D1 and D2. FEBS Lett. 544, 38-44
53. Djerdjouri, B., Lenoir, M., Giroud, J. P., and Perianin, A. (1999) Contribution of mitogen-activated protein kinase to stimulation of phospholipase D by the chemotactic peptide fMet-leu-Phe in human neutrophils. Biochem. Biophys. Res. Commun. 264, 371-375