HIV-1 Tat inhibits phagocytosis by preventing the recruitment of Cdc42 to the phagocytic cup

Nature Communications

Volumn 6, Issue , 2015, Pages

  Debaisieux, Solène ^a   Lachambre, Simon ^a   Gross, Antoine ^a   Mettling, Clément ^b   Besteiro, Sébastien ^c   Yezid, Hocine ^a   Henaff, Daniel ^a   Chopard, Christophe ^a   Mesnard, Jean Michel ^a   Beaumelle, Bruno ^a  

^a University of Montpellier I and II   (France)

^b INSTITUTE OF HUMAN GENETICS   (France)

^c UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MANNOSE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN CDC42; TRANSACTIVATOR PROTEIN; VIRULENCE FACTOR; CELL SURFACE RECEPTOR; FC RECEPTOR; FCGR1A PROTEIN, HUMAN; LECTIN; MANNOSE BINDING LECTIN; MANNOSE RECEPTOR; RECOMBINANT PROTEIN;

BACTERIOPHAGE; BLOOD; HUMAN IMMUNODEFICIENCY VIRUS; INFECTIVITY; INHIBITION; PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; MACROPHAGE; MONOCYTE; MYCOBACTERIUM AVIUM; NEUTROPHIL; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; TOXOPLASMA GONDII; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BYSTANDER EFFECT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; PSEUDOPODIUM; SIGNAL TRANSDUCTION; TOXOPLASMA; ULTRASTRUCTURE;

HUMAN IMMUNODEFICIENCY VIRUS 1; MYCOBACTERIUM AVIUM; TOXOPLASMA GONDII;

BYSTANDER EFFECT; CDC42 GTP-BINDING PROTEIN; GENE EXPRESSION REGULATION; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; LECTINS, C-TYPE; MACROPHAGES; MANNOSE-BINDING LECTINS; MONOCYTES; MYCOBACTERIUM AVIUM; NEUTROPHILS; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; PSEUDOPODIA; RECEPTORS, CELL SURFACE; RECEPTORS, IGG; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TOXOPLASMA;

EID: 84929694872     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7211     Document Type: Article

References (61)

1. Flannagan, R. S., Jaumouille, V. & Grinstein, S. The cell biology of phagocytosis. Annu. Rev. Pathol. 7, 61-98 (2012).
2. Tzircotis, G., Braga, V. M. M. & Caron, E. RhoG is required for both FcgammaR-and CR3-mediated phagocytosis. J. Cell Sci. 124, 2897-2902 (2011).
3. Zhang, J. et al. Cdc42 and RhoB activation are required for mannose receptor-mediated phagocytosis by human alveolar macrophages. Mol. Biol. Cell 16, 824-834 (2005).
4. Frantz, C. et al. Cofilin is a pH sensor for actin free barbed end formation: role of phosphoinositide binding. J. Cell Biol. 183, 865-879 (2008).
5. Raucher, D. et al. Phosphatidylinositol 4, 5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228 (2000).
6. Heo, W. D. et al. PI(3, 4, 5)P3 and PI(4, 5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461 (2006).
7. Orenstein, J. M., Fox, C. & Wahl, S. M. Macrophages as a source of HIV during opportunistic infections. Science 276, 1857-1861 (1997).
8. Collini, P., Noursadeghi, M., Sabroe, I., Miller, R. F. & Dockrell, D. H. Monocyte and macrophage dysfunction as a cause of HIV-1 induced dysfunction of innate immunity. Curr. Mol. Med. 10, 727-740 (2010).
9. Sandler, N. G. & Douek, D. C. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat. Rev. Microbiol. 10, 655-666 (2012).
10. Alexaki, A., Liu, Y. & Wigdahl, B. Cellular reservoirs of HIV-1 and their role in viral persistence. Curr. HIV Res. 6, 388-400 (2008).
11. Hrecka, K. et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474, 658-661 (2011).
12. Kedzierska, K. et al. Defective phagocytosis by human monocyte/macrophages following HIV-1 infection: underlying mechanisms and modulation by adjunctive cytokine therapy. J. Clin. Virol. 26, 247-263 (2003).
13. Mastroianni, C. M. et al. Improvement in neutrophil and monocyte function during highly active antiretroviral treatment of HIV-1-infected patients. AIDS 13, 883-890 (1999).
14. Rayne, F. et al. Phosphatidylinositol-(4, 5)-bisphosphate enables efficient secretion of HIV-1 Tat by infected T-cells. EMBO J. 29, 1348-1362 (2010).
15. Westendorp, M. O. et al. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375, 497-500 (1995).
16. Xiao, H. et al. Selective CXCR4 antagonism by tat: implications for in vivo expansion of coreceptor use by HIV-1. Proc. Natl Acad. Sci. USA 97, 11466-11471 (2000).
17. Debaisieux, S., Rayne, F., Yezid, H. & Beaumelle, B. The ins and outs of HIV-1 Tat. Traffic 13, 355-363 (2012).
18. Yezid, H., Konate, K., Debaisieux, S., Bonhoure, A. & Beaumelle, B. Mechanism for HIV-1 Tat insertion into the endosome membrane. J. Biol. Chem. 284, 22736-22746 (2009).
19. Vendeville, A. et al. HIV-1 Tat enters T cells using coated pits before translocating from acidified endosomes and eliciting biological responses. Mol. Biol. Cell 15, 2347-2360 (2004).
20. Chow, C. W., Downey, G. P. & Grinstein, S. Measurements of phagocytosis and phagosomal maturation. Curr. Protoc. Cell Biol. Chapter 15, Unit 15 17 (2004).
21. Perelson, A. S., Neumann, A. U., Markowitz, M., Leonard, J. M. & Ho, D. D. HIV-1 dynamics in vivo: virion clearance rate, infected cell life span, and viral generation time. Science 271, 1582-1586 (1996).
22. Speert, D. P. & Silverstein, S. C. Phagocytosis of unopsonized zymosan by human monocyte-derived macrophages: maturation and inhibition by mannan. J. Leukoc. Biol. 38, 655-658 (1985).
23. Caldwell, R. L., Egan, B. S. & Shepherd, V. L. HIV-1 Tat represses transcription from the mannose receptor promoter. J. Immunol. 165, 7035-7041 (2000).
24. Leeansyah, E., Wines, B. D., Crowe, S. M. & Jaworowski, A. The mechanism underlying defective Fcgamma receptor-mediated phagocytosis by HIV-1-infected human monocyte-derived macrophages. J. Immunol. 178, 1096-1104 (2007).
25. Pontow, S. E., Kery, V. & Stahl, P. D. Mannose receptor. Int. Rev. Cytol. 137B, 221-244 (1992).
26. Karakousis, P. C., Moore, R. D. & Chaisson, R. E. Mycobacterium avium complex in patients with HIV infection in the era of highly active antiretroviral therapy. Lancet Infect. Dis. 4, 557-565 (2004).
27. Kudo, K. et al. Pulmonary collectins enhance phagocytosis of Mycobacterium avium through increased activity of mannose receptor. J. Immunol. 172, 7592-7602 (2004).
28. Kedzierska, K. et al. Granulocyte-macrophage colony-stimulating factor augments phagocytosis of Mycobacterium avium complex by human immunodeficiency virus type 1-infected monocytes/macrophages in vitro and in vivo. J. Infect. Dis. 181, 390-394 (2000).
29. Abgrall, S., Rabaud, C. & Costagliola, D. Incidence and risk factors for toxoplasmic encephalitis in human immunodeficiency virus-infected patients before and during the highly active antiretroviral therapy era. Clin. Infect. Dis. 33, 1747-1755 (2001).
30. Mamidi, A., DeSimone, J. A. & Pomerantz, R. J. Central nervous system infections in individuals with HIV-1 infection. J. Neurovirol. 8, 158-167 (2002).
31. Biggs, B. A., Hewish, M., Kent, S., Hayes, K. & Crowe, S. M. HIV-1 infection of human macrophages impairs phagocytosis and killing of Toxoplasma gondii. J. Immunol. 154, 6132-6139 (1995).
32. Garber, M. E. et al. The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes Dev. 12, 3512-3527 (1998).
33. Botelho, R. J. et al. Localized biphasic changes in phosphatidylinositol-4, 5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368 (2000).
34. Yeung, T. et al. Contribution of phosphatidylserine to membrane surface charge and protein targeting during phagosome maturation. J. Cell Biol. 185, 917-928 (2009).
35. Lewkowicz, E. et al. The microtubule-binding protein CLIP-170 coordinates mDia1 and actin reorganization during CR3-mediated phagocytosis. J. Cell Biol. 183, 1287-1298 (2008).
36. Kisseleva, M. et al. The LIM protein Ajuba regulates phosphatidylinositol 4, 5-bisphosphate levels in migrating cells through an interaction with and activation of PIPKI alpha. Mol. Cell. Biol. 25, 3956-3966 (2005).
37. Johnson, J. L., Erickson, J. W. & Cerione, R. A. C-terminal di-arginine motif of Cdc42 protein is essential for binding to phosphatidylinositol 4, 5-bisphosphatecontaining membranes and inducing cellular transformation. J. Biol. Chem. 287, 5764-5774 (2012).
38. Massol, P., Montcourrier, P., Guillemot, J. C. & Chavrier, P. Fc receptormediated phagocytosis requires CDC42 and Rac1. EMBO J. 17, 6219-6229 (1998).
39. Caron, E. & Hall, A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282, 1717-1721 (1998).
40. Cox, D. et al. Requirements for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes. J. Exp. Med. 186, 1487-1494 (1997).
41. Schmidt, A. & Hall, A. Guanine nucleotide exchange factors for Rho GTPases: Turning on the switch. Genes Dev. 16, 1587-1609 (2002).
42. Ory, S., Munari-Silem, Y., Fort, P. & Jurdic, P. Rho and Rac exert antagonistic functions on spreading of macrophage-derived multinucleated cells and are not required for actin fiber formation. J. Cell Sci. 113, 1177-1188 (2000).
43. Aoki, K. & Matsuda, M. Visualization of small GTPase activity with fluorescence resonance energy transfer-based biosensors. Nat. Protoc. 4, 1623-1631 (2009).
44. Hoppe, A. D. & Swanson, J. A. Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol. Biol. Cell 15, 3509-3519 (2004).
45. Hong, L. et al. Characterization of a Cdc42 protein inhibitor and its use as a molecular probe. J. Biol. Chem. 288, 8531-8543 (2013).
46. Koziel, H. et al. Reduced binding and phagocytosis of Pneumocystis carinii by alveolar macrophages from persons infected with HIV-1 correlates with mannose receptor downregulation. J. Clin. Invest. 102, 1332-1344 (1998).
47. Azzam, R. et al. Impaired complement-mediated phagocytosis by HIV type-1-infected human monocyte-derived macrophages involves a cAMP-dependent mechanism. AIDS Res. Hum. Retroviruses 22, 619-629 (2006).
48. Tardei, G. et al. Phagocytic function of monocytes in children with human immunodeficiency virus type 1 infection. Clin. Diagn. Lab. Immunol. 7, 296-297 (2000).
49. Ensoli, B., Barillari, G., Salahuddin, S. Z., Gallo, R. C. & Wong-Staal, F. Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 345, 84-86 (1990).
50. Mediouni, S. et al. Antiretroviral therapy does not block the secretion of the human immunodeficiency virus tat protein. Infect. Disord. Drug Targets 12, 81-86 (2012).
51. Zagury, J. F. et al. Antibodies to the HIV-1 Tat protein correlated with nonprogression to AIDS: A rationale for the use of Tat toxoid as an HIV-1 vaccine. J. Hum. Virol. 1, 282-292 (1998).
52. Botelho, R. J. & Grinstein, S. Phagocytosis. Curr. Biol. 21, R533-R538 (2011).
53. Lemichez, E. & Aktories, K. Hijacking of Rho GTPases during bacterial infection. Exp. Cell Res. 319, 2329-2336 (2013).
54. Tryoen-Toth, P. et al. HIV-1 Tat protein inhibits neurosecretion by binding to phosphatidylinositol (4, 5) bisphosphate. J. Cell Sci. 126, 454-463 (2013).
55. Mazzolini, J. et al. Inhibition of phagocytosis in HIV-1-infected macrophages relies on Nef-dependent alteration of focal delivery of recycling compartments. Blood 115, 4226-4236 (2010).
56. Besteiro, S., Brooks, C. F., Striepen, B. & Dubremetz, J. F. Autophagy protein Atg3 is essential for maintaining mitochondrial integrity and for normal intracellular development of Toxoplasma gondii tachyzoites. PLoS Pathog. 7, e1002416 (2011).
57. Borregaard, N., Heiple, J. M., Simons, E. R. & Clark, R. A. Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: Translocation during activation. J. Cell Biol. 97, 52-61 (1983).
58. N'Diaye, E. N. et al. Fusion of azurophil granules with phagosomes and activation of the tyrosine kinase Hck are specifically inhibited during phagocytosis of mycobacteria by human neutrophils. J. Immunol. 161, 4983-4991 (1998).
59. Stein, M., Keshav, S., Harris, N. & Gordon, S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: A marker of alternative immunologic macrophage activation. J. Exp. Med. 176, 287-292 (1992).
60. Hammond, G. R. V. et al. Elimination of plasma membrane phosphatidylinositol (4, 5)-bisphosphate is required for exocytosis from mast cells. J. Cell Sci. 119, 2084-2094 (2006).
61. Fujinaga, K., Taube, R., Wimmer, J., Cujec, T. P. & Peterlin, B. M. Interactions between human cyclin T, Tat, and the transactivation response element (TAR) are disrupted by a cysteine to tyrosine substitution found in mouse cyclin T. Proc. Natl Acad. Sci. USA 96, 1285-1290 (1999).