Exogenous HIV-1 nef upsets the IFN-γ-induced impairment of human intestinal epithelial integrity

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Quaranta, Maria Giovanna ^a   Vincentini, Olimpia ^a   Felli, Cristina ^a   Spadaro, Francesca ^a   Silano, Marco ^a   Moricoli, Diego ^b   Giordani, Luciana ^a   Viora, Marina ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Diatheva srl ^*  (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MEMBRANE PROTEIN; RECOMBINANT NEF PROTEIN; RECOMBINANT PROTEIN; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CHEMOKINE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOKINE; DEXTRAN; DRUG DERIVATIVE; FLUORESCEIN ISOTHIOCYANATE; NEF PROTEIN; NEF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PHOSPHOPROTEIN; PROSTAGLANDIN E2; PROTEIN ZO1; PTGS2 PROTEIN, HUMAN; ZONULA OCCLUDENS-1 PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL STIMULATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DIGESTIVE SYSTEM INFLAMMATION; DOWN REGULATION; DRUG ACTIVITY; ELECTRIC RESISTANCE; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE EPITHELIUM CELL; PROTEIN EXPRESSION; UPREGULATION; CELL STRAIN CACO 2; CELL STRAIN HEK293; DOSE RESPONSE; DRUG EFFECT; EPITHELIUM CELL; GENETICS; INTESTINE MUCOSA; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL; WESTERN BLOTTING;

HUMAN IMMUNODEFICIENCY VIRUS 1;

APOPTOSIS; ARACHIDONIC ACID; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; CHEMOKINES; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOKINES; DEXTRANS; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FLUORESCEIN-5-ISOTHIOCYANATE; HEK293 CELLS; HUMANS; INTERFERON-GAMMA; INTESTINAL MUCOSA; MEMBRANE PROTEINS; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PHOSPHOPROTEINS; RECOMBINANT PROTEINS;

EID: 79961187811     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023442     Document Type: Article

References (54)

1. Shen L, Turner JR, (2006) Role of epithelial cells in initiation and propagation of intestinal inflammation. Eliminating the static: tight junction dynamics exposed. Am J Physiol Gastrointest Liver Physiol 290: G577-582.
2. Kotler DP, (2005) HIV infection and the gastrointestinal tract. AIDS 19: 107-117.
3. Janoff EN, Smith PD, (2001) Emerging concepts in gastrointestinal aspects of HIV-1 pathogenesis and management. Gastroenterology 120: 607-621.
4. Paiardini M, Frank I, Pandrea I, Apetrei C, Silvestri G, (2008) Mucosal immunedysfunction in AIDS pathogenesis. AIDS Rev 10: 36-46.
5. Delézay O, Yahi N, Tamalet C, Baghdiguian S, Boudier JA, et al. (1997) Direct effect of type 1 human immunodeficiency virus (HIV-1) on intestinal epithelial cell differentiation: relationship to HIV-1 enteropathy. Virology 238: 231-242.
6. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, et al. (2010) Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 6: e1000852.
7. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
8. Boirivant M, Viora M, Giordani L, Luzzati AL, Pronio AM, et al. (1998) HIV-1 gp120 accelerates Fas-mediated activation-induced human lamina propria T cell apoptosis. J Clin Immunol 18: 39-47.
9. Canani RB, De Marco G, Passariello A, Buccigrossi V, Ruotolo S, et al. (2006) Inhibitory effect of HIV-1 Tat protein on the sodium-D-glucose symporter of human intestinal epithelial cells. AIDS 20: 5-10.
10. Canani RB, Cirillo P, Mallardo G, Buccigrossi V, Secondo A, et al. (2003) Effects of HIV-1 Tat protein on ion secretion and on cell proliferation in human intestinal epithelial cells. Gastroenterology 124: 368-376.
11. Kirchhoff F, Schindler M, Specht A, Arhel N, Münch J, (2008) Role of Nef in primate lentiviral immunopathogenesis. Cell Mol Life Sci 65: 2621-2636.
12. Quaranta MG, Mattioli B, Giordani L, Viora M, (2009) Immunoregulatory effects of HIV-1 Nef protein. Biofactors 35: 169-174.
13. Quaranta MG, Mattioli B, Spadaro F, Straface E, Giordani L, et al. (2003) HIV-1 Nef triggers Vav-mediated signaling pathway leading to functional and morphological differentiation of dendritic cells. FASEB J 17: 2025-2036.
14. Greenway AL, Holloway G, McPhee DA, Ellis P, Cornall A, et al. (2003) HIV-1 Nef control of cell signalling molecules: multiple strategies to promote virus replication. J Biosci 28: 323-335.
15. Thoulouze MI, Sol-Foulon N, Blanchet F, Dautry-Varsat A, Schwartz O, et al. (2006) Human immunodeficiency virus type-1 infection impairs the formation of the immunological synapse. Immunity 24: 547-561.
16. Fujii Y, Otake K, Tashiro M, Adachi A, (1996) Soluble Nef antigen of HIV-1 is cytotoxic for human CD4+ T cells. FEBS Lett 393: 93-96.
17. Campbell TD, Khan M, Huang MB, Bond VC, Powell MD, (2008) HIV-1 Nef protein is secreted into vesicles that can fuse with target cells and virions. Ethn Dis 18: S2-14-19.
18. Muratori C, Cavallin LE, Krätzel K, Tinari A, De Milito A, et al. (2009) Massive secretion by T cells is caused by HIV Nef in infected cells and by Nef transfer to bystander cells. Cell Host Microbe 6: 218-230.
19. Quaranta MG, Tritarelli E, Giordani L, Viora M, (2002) HIV-1 Nef induces dendritic cell differentiation: a possible mechanism of uninfected CD4(+) T cell activation. Exp Cell Res 275: 243-254.
20. Quaranta MG, Mattioli B, Giordani L, Viora M, (2004) HIV-1 Nef equips dendritic cells to reduce survival and function of CD8+ T cells: a mechanism of immune evasion. FASEB J 18: 1459-1461.
21. Quaranta MG, Napolitano A, Sanchez M, Giordani L, Mattioli B, et al. (2007) HIV-1 Nef impairs the dynamic of DC/NK crosstalk: different outcome of CD56(dim) and CD56(bright) NK cell subsets. FASEB J 21: 2323-2334.
22. Giordani L, Giacomini E, Quaranta MG, Viora M, (2000) HIV-1 Nef protein inhibits the in vitro induction of a specific antibody response to Candida albicans by an early up-regulation of IL-15 production. Clin Exp Immunol 122: 358-363.
23. Olivetta E, Pugliese K, Bona R, D'Aloja P, Ferrantelli F, et al. (2000) cis expression of the F12 human immunodeficiency virus (HIV) Nef allele transforms the highly productive NL4-3 HIV type 1 to a replication-defective strain: involvement of both Env gp41 and CD4 intracytoplasmic tails. J Virol 74: 483-492.
24. Fackler OT, d'Aloja P, Baur AS, Federico M, Peterlin BM, (2001) Nef from human immunodeficiency virus type 1(F12) inhibits viral production and infectivity. J Virol 75: 6601-6608.
25. Alessandrini L, Santarcangelo AC, Olivetta E, Ferrantelli F, d'Aloja P, et al. (2000) T-tropic human immunodeficiency virus (HIV) type 1 Nef protein enters human monocyte-macrophages and induces resistance to HIV replication: a possible mechanism of HIV T-tropic emergence in AIDS. J Gen Virol 81: 2905-2917.
26. Peretti S, Schiavoni I, Pugliese K, Federico M, (2005) Cell death induced by the herpes simplex virus-1 thymidine kinase delivered by human immunodeficiency virus-1-based virus-like particles. Mol Ther 12: 1185-1196.
27. De Angelis I, Vincentini O, Brambilla G, Stammati A, Zucco F, (1998) Characterization of furazolidone apical relative effect to human polarized intestinal cell line. Toxicol Appl Pharmacol 152: 119-127.
28. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, et al. (2003) Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 171: 6164-6172.
29. Jumarie C, Malo C, (1991) Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro. J Cell Physio 149: 24-33.
30. Wang Q, Guo XL, Wells-Byrum D, Noel G, Pritts TA, et al. (2008) Cytokine-induced epithelial permeability changes are regulated by the activation of the p38 mitogen-activated protein kinase pathway in cultured Caco-2 cells. Shock 29: 531-537.
31. Madara JL, Stafford J, (1989) Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 83: 724-727.
32. Dhawan S, Wahl LM, Heredia A, Zhang Y, Epstein JS, et al. (1995) Interferon-gamma inhibits HIV-induced invasiveness of monocytes. J Leukoc Biol 58: 713-716.
33. Hariharan D, Douglas SD, Lee B, Lai JP, Campbell DE, et al. (1999) Interferon-gamma upregulates CCR5 expression in cord and adult blood mononuclear phagocytes. Blood 93: 1137-1144.
34. Biswas P, Poli G, Kinter AL, Justement JS, Stanley SK, et al. (1992) Interferon gamma induces the expression of human immunodeficiency virus in persistently infected promonocytic cells (U1) and redirects the production of virions to intracytoplasmic vacuoles in phorbol myristate acetate-differentiated U1 cells. J Exp Med 176: 739-750.
35. Quaranta MG, Falzano L, Vincentini O, Fiorentini C, Giordani L, et al. (2011) Effects of HIV-1 Nef on virus co-receptor expression and cytokine release in human bladder, laryngeal, and intestinal epithelial cell lines. Viral Immunol 24: 245-250.
36. Husain M, Gusella GL, Klotman ME, Gelman IH, Ross MD, et al. (2002) HIV-1 Nef induces proliferation and anchorage-independent growth in podocytes. J Am Soc Nephrol 13: 1806-1815.
37. Husain M, D'Agati VD, He JC, Klotman ME, Klotman PE, (2005) HIV-1 Nef induces dedifferentiation of podocytes in vivo: a characteristic feature of HIVAN. AIDS 19: 1975-1980.
38. Lu TC, He JC, Wang ZH, Feng X, Fukumi-Tominaga T, et al. (2008) HIV-1 Nef disrupts the podocyte actin cytoskeleton by interacting with diaphanous interacting protein. J Biol Chem 283: 8173-8182.
39. Sunamoto M, Husain M, He JC, Schwartz EJ, Klotman PE, (2003) Critical role for Nef in HIV-1-induced podocyte dedifferentiation. Kidney Int 64: 1695-1701.
40. Kuster H, Opravil M, Ott P, Schlaepfer E, Fischer M, et al. (2000) Treatment-induced decline of human immunodeficiency virus-1 p24 and HIV-1 RNA in lymphoid tissue of patients with early human immunodeficiency virus-1 infection. Am J Pathol 156: 1973-1986.
41. Ndolo T, Syvanen M, Ellison T, Dandekar S, (2005) Evolution of nef variants in gut associated lymphoid tissue of rhesus macaques during primary simian immunodeficiency virus infection. Virology 343: 1-11.
42. Sharpstone D, Gazzard B, (1996) Gastrointestinal manifestations of HIV infection. Lancet 348: 379-383.
43. Belyakov IM, Berzofsky JA, (2004) Immunobiology of mucosal HIV infection and the basis for development of a new generation of mucosal AIDS vaccines. Immunity 20: 247-253.
44. Neutra MR, Kozlowski PA, (2006) Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 6: 148-158.
45. Iliev ID, Spadoni I, Mileti E, Matteoli G, Sonzogni A, et al. (2009) Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58: 1481-1489.
46. Kaiserlian D, Cerf-Bensussan N, Hosmalin A, (2005) The mucosal immune system: from control of inflammation to protection against infections. J Leukoc Biol 78: 311-318.
47. Quaranta MG, Camponeschi B, Straface E, Malorni W, Viora M, (1999) Induction of interleukin-15 production by HIV-1 nef protein: a role in the proliferation of uninfected cells. Exp Cell Res 250: 112-121.
48. Percario Z, Olivetta E, Fiorucci G, Mangino G, Peretti S, et al. (2003) Human immunodeficiency virus type 1 (HIV-1) Nef activates STAT3 in primary human monocyte/macrophages through the release of soluble factors: involvement of Nef domains interacting with the cell endocytotic machinery. J Leukoc Biol 74: 821-832.
49. Swingler S, Mann A, Jacqué J, Brichacek B, Sasseville VG, et al. (1999) HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nat Med 5: 997-1003.
50. Rosenberg ZF, Fauci AS, (1990) Immunopathogenic mechanisms of HIV infection: cytokine induction of HIV expression. Immunol Today 11: 176-180.
51. Poli G, Fauci AS, (1992) The effect of cytokines and pharmacologic agents on chronic HIV infection. AIDS Res Hum Retroviruses 8: 191-197.
52. Martín-Venegas R, Roig-Pérez S, Ferrer R, Moreno JJ, (2006) Arachidonic acid cascade and epithelial barrier function during Caco-2 cell differentiation. J Lipid Res 47: 1416-1423.
53. Harizi H, Corcuff JB, Gualde N, (2008) Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol Med 14: 461-469.
54. Wu L, Fossum E, Joo CH, Inn KS, Shin YC, et al. (2009) Epstein-Barr virus LF2: an antagonist to type I interferon. J Virol 83: 1140-1146.