The HIV-1 transactivator factor (Tat) induces enterocyte apoptosis through a Redox-Mediated mechanism

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Buccigrossi, Vittoria ^a   Laudiero, Gabriella ^a   Nicastro, Emanuele ^a   Miele, Erasmo ^a   Esposito, Franca ^a   Guarino, Alfredo ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ACETYLCYSTEINE; CASPASE 3; CATALASE; CYTOCHROME C; GLUTATHIONE; NEUTRALIZING ANTIBODY; REACTIVE OXYGEN METABOLITE; TRANSACTIVATOR PROTEIN;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL STRAIN CACO 2; CELL STRAIN HT29; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOSOL; ENTEROPATHY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; EX VIVO STUDY; FEMALE; HIV ASSOCIATED INTESTINE DISEASE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; INTESTINE CELL; INTESTINE MUCOSA; JEJUNUM; MALE; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; SCHOOL CHILD; CELL LINE; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ACETYLCYSTEINE; APOPTOSIS; CELL LINE; ENTEROCYTES; GENE PRODUCTS, TAT; HIV-1; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84455192447     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029436     Document Type: Article

References (55)

1. Shattock RJ, Haynes BF, Pulendran B, Flores J, Esparza J, et al. (2008) Improving defences at the portal of HIV entry: mucosal and innate immunity. PLoS Med 5: e81.
2. Brenchley JM, Douek DC, (2008) HIV infection and the gastrointestinal immune system. Mucosal Immunol 1: 23-30.
3. Epple HJ, Allers K, Tröger H, Kühl A, Erben U, et al. (2010) Acute HIV infection induces mucosal infiltration with CD4+ and CD8+ T cells, epithelial apoptosis, and a mucosal barrier defect. Gastroenterology 139: 1289-300.
4. Epple HJ, Schneider T, Troeger H, Kunkel D, Allers K, et al. (2009) Impairment of the intestinal barrier is evident in untreated but absent in suppressively treated HIV-infected patients. Gut 58: 220-227.
5. Lim SG, Menzies IS, Lee CA, Johnson MA, Pounder RE, (1993) Intestinal permeability and function in patients infected with human immunodeficiency virus. A comparison with coeliac disease. Scand J Gastroenterol 28: 573-580.
6. Keating J, Bjarnason I, Somasundaram S, Macpherson A, Francis N, et al. (1995) Intestinal absorptive capacity, intestinal permeability and jejunal histology in HIV and their relation to diarrhoea. Gut 37: 623-629.
7. Sharpstone D, Neild P, Crane R, Taylor C, Hodgson C, et al. (1999) Small intestinal transit, absorption, and permeability in patients with AIDS with and without diarrhoea. Gut 45: 70-76.
8. Stockmann M, Schmitz H, Fromm M, Schmidt W, Pauli G, et al. (2000) Mechanisms of epithelial barrier impairment in HIV infection. Ann N Y Acad Sci 915: 293-303.
9. Stockmann M, Fromm M, Schmitz H, Schmidt W, Riecken EO, et al. (1998) Duodenal biopsies of HIV-infected patients with diarrhoea exhibit epithelial barrier defects but no active secretion. Aids 12: 43-51.
10. Papadia C, Kelly P, Caini S, Corazza GR, Shawa T, et al. (2010) Plasma citrulline as a quantitative biomarker of HIV-associated villous atrophy in a tropical enteropathy population. Clin Nutr 29: 795-800.
11. Kamat A, Ancuta P, Blumberg RS, Gabuzda D, (2010) Serological markers for inflammatory bowel disease in AIDS patients with evidence of microbial translocation. PLoS One 5: e15533.
12. Cello JP, Day LW, (2003) Idiopathic AIDS enteropathy and treatment of gastrointestinal opportunistic pathogens. Gastroenterology 136: 1952-1965.
13. Belmonte L, Olmos M, Fanin A, Parodi C, Baré P, et al. (2007) The intestinal mucosa as a reservoir of HIV-1 infection after successful HAART. AIDS 21: 2106-2188.
14. Kotler DP, Reka S, Borcich A, Cronin WJ, (1991) Detection, localization, and quantitation of HIV-associated antigens in intestinal biopsies from patients with HIV. Am J Pathol 139: 823-30.
15. 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.
16. Berni Canani R, 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.
17. Brailoiu E, Brailoiu GC, Mameli G, Dolei A, Sawaya BE, et al. (2006) Acute exposure to ethanol potentiates human immunodeficiency virus type 1 Tat-induced Ca(2+) overload and neuronal death in cultured rat cortical neurons. J Neurovirol 12: 17-24.
18. Agrawal L, Louboutin JP, Strayer DS, (2007) Preventing HIV-1 Tat-induced neuronal apoptosis using antioxidant enzymes: mechanistic and therapeutic implications. Virology 363: 462-472.
19. Fraternale A, Paoletti MF, Casabianca A, Orlandi C, Schiavano GF, et al. (2008) Inhibition of murine AIDS by pro-glutathione (GSH) molecules. Antiviral Res 77: 120-127.
20. Fraternale A, Paoletti MF, Casabianca A, Nencioni L, Garaci E, et al. (2009) GSH and analogs in antiviral therapy. Mol Aspects Med 30: 99-110.
21. Kline ER, Sutliff RL, (2008) The roles of HIV-1 proteins and antiretroviral drug therapy in HIV-1-associated endothelial dysfunction. J Investig Med 56: 752-769.
22. Stehbens WE, (2004) Oxidative stress in viral hepatitis and AIDS. Exp Mol Pathol 77: 121-132.
23. Banerjee A, Zhang X, Manda KR, Banks WA, Ercal N, (2010) HIV proteins (gp120 and Tat) and methamphetamine in oxidative stress-induced damage in the brain: potential role of the thiol antioxidant N-acetylcysteine amide. Free Radic Biol Med 48: 1388-1398.
24. Wanchu A, Rana SV, Pallikkuth S, Sachdeva RK, (2009) Short communication: oxidative stress in HIV-infected individuals: a cross-sectional study. AIDS Res Hum Retroviruses 25: 1307-1311.
25. Circu ML, Stringer S, Rhoads CA, Moyer MP, Aw TY, (2009) The role of GSH efflux in staurosporine-induced apoptosis in colonic epithelial cells. Biochem Pharmacol 77: 76-85.
26. Townsend DM, Tew KD, Tapiero H, (2003) The importance of glutathione in human disease. Biomed Pharmacother 57: 145-155.
27. Tsunada S, Iwakiri R, Noda T, Fujimoto K, Fuseler J, et al. (2003) Chronic exposure to subtoxic levels of peroxidized lipids suppresses mucosal cell turnover in rat small intestine and reversal by glutathione. Dig Dis Sci 48: 210-222.
28. Sbrana E, Paladini A, Bramanti E, Spinetti MC, Raspi G, (2004) Quantitation of reduced glutathione and cysteine in human immunodeficiency virus-infected patients. Electrophoresis 25: 1522-1529.
29. Sundaram M, Saghayam S, Priya B, Venkatesh KK, Balakrishnan P, et al. (2008) Changes in antioxidant profile among HIV-infected individuals on generic highly active antiretroviral therapy in southern India. Int J Infect Dis 12: e61-e66.
30. Price TO, Uras F, Banks WA, Ercal N, (2006) A novel antioxidant N-acetylcysteine amide prevents gp120- and Tat-induced oxidative stress in brain endothelial cells. Exp Neurol 201: 193-202.
31. Circu ML, Moyer MP, Harrison L, Aw TY, (2009) Contribution of glutathione status to oxidant-induced mitochondrial DNA damage in colonic epithelial cells. Free Radic Biol Med 47: 1190-8.
32. Berni Canani R, Cirillo P, Bruzzese E, Graf M, Terrin G, et al. (2002) Nitric oxide production in rectal dialysate is a marker of disease activity and location in children with inflammatory bowel disease. Am J Gastroenterol 97: 1574-6.
33. Bruzzese E, Raia V, Gaudiello G, Polito G, Buccigrossi V, et al. (2004) Intestinal inflammation is a frequent feature of cystic fibrosis and is reduced by probiotic administration. Aliment Pharmacol Ther 20: 813-9.
34. Valavanidis A, Vlachogianni T, Fiotakis C, (2009) 8-hydroxy-2′-deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27: 120-39.
35. Kroemer G, Galluzzi L, Brenner C, (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163.
36. Taha R, Seidman E, Mailhot G, Boudreau F, Gendron FP, et al. (2010) Oxidative stress and mitochondrial functions in the intestinal Caco-2/15 cell line. PLoS One 5: e11817.
37. Westendorp MO, Frank R, Ochsenbauer C, Stricker K, Dhein J, et al. (1995) Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375: 497-500.
38. Li Q, Estes JD, Duan L, Jessurun J, Pambuccian S, et al. (2008) Simian immunodeficiency virus-induced intestinal cell apoptosis is the underlying mechanism of the regenerative enteropathy of early infection. J Infect Dis 197: 420-9.
39. Pierleoni R, Menotta M, Antonelli A, Sfara C, Serafini G, et al. (2010) Effect of the redox state on HIV-1 tat protein multimerization and cell internalization and trafficking. Mol Cell Biochem 345: 105-18.
40. Gil L, Tarinas A, Hernández D, Riverón BV, Pérez D, et al. (2010) Altered oxidative stress indexes related to disease progression marker in human immunodeficiency virus infected patients with antiretroviral therapy. Biomed Pharmacother In press.
41. McCloskey TW, Oyaizu N, Kaplan M, Pahwa S, (1995) Expression of the Fas antigen in patients infected with human immunodeficiency virus. Cytometry 22: 111-4.
42. Berni Canani R, 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.
43. Chen D, Wang M, Zhou S, Zhou Q, (2002) HIV-1 Tat targets microtubules to induce apoptosis, a process promoted by the pro-apoptotic Bcl-2 relative Bim. EMBO J 21: 6801-10.
44. Huo L, Li D, Sun L, Liu M, Shi X, et al. (2011) Tat acetylation regulates its actions on microtubule dynamics and apoptosis in T lymphocytes. J Pathol 223: 28-36.
45. Attene-Ramos MS, Kitiphongspattana K, Ishii-Schrade K, Gaskins HR, (2005) Temporal changes of multiple redox couples from proliferation to growth arrest in IEC-6 intestinal epithelial cells. Am J Physiol Cell Physiol 289: C1220-C1228.
46. Gotoh Y, Noda T, Iwakiri R, Fujimoto K, Rhoads CA, et al. (2002) Lipid peroxide-induced redox imbalance differentially mediates Caco-2 cell proliferation and growth arrest. Cell Prolif 35: 221-235.
47. Herring TA, Cuppett SL, Zempleni J, (2007) Genomic implication of H2O2 for cell proliferation and growth of Caco-2 cells. Dig Dis Sci 52: 3005-3015.
48. Srinivas A, Dias BF, (2008) Antioxidants in HIV positive children. Indian J Pediatr 75: 347-50.
49. Stephensen CB, Marquis GS, Douglas SD, Kruzich LA, Wilson CM, (2007) Glutathione, glutathione peroxidase, and selenium status in HIV-positive and HIV-negative adolescents and young adults. Am J Clin Nutr 85: 173-81.
50. Chun TW, Nickle DC, Justement JS, Meyers JH, Roby G, et al. (2008) Persistence of HIV in gut-associated lymphoid tissue despite long-term antiretroviral therapy. J Infect Dis 197: 714-720.
51. Critchfield JW, Young DH, Hayes TL, Braun JV, Garcia JC, et al. (2008) Magnitude and complexity of rectal mucosa HIV-1-specific CD8+ T-cell responses during chronic infection reflect clinical status. PLoS One 3: e3577.
52. Lafeuillade A, Cheret A, Hittinger G, Bernardini D, Cuquemelle C, et al. (2009) Rectal cell-associated HIV-1 RNA: a new marker ready for the clinic. HIV Clin Trials 10: 324-7.
53. Ledda M, De Lazzari C, Lisi A, Fresiello L, Grimaldi S, et al. (2011) The role of extracellular conditions during CaCo-2 cells growth: a preliminary study for numerical model validation. Eur Rev Med Pharmacol Sci 15: 61-70.
54. Allen S, Shea JM, Felmet T, Gadra J, Dehn PF, (2000) A kinetic microassay for glutathione in cells plated on 96-well microtiter plates. Methods Cell Sci 22: 305-312.
55. Rupinder SK, Gurpreet AK, Manjeet S, (2007) Cell suicide and caspases. Vascul Pharmacol 46: 383-393.