A candidate anti-HIV reservoir compound, auranofin, exerts a selective 'anti-memory' effect by exploiting the baseline oxidative status of lymphocytes

Cell Death and Disease

Volumn 4, Issue 12, 2013, Pages

  Chirullo, B ^a   Sgarbanti, R ^b   Limongi, D ^b   Shytaj, I L ^a   Alvarez, D ^c   Das, B ^c   Boe, A ^a   DaFonseca, S ^d   Chomont, N ^d   Liotta, L ^e   Petricoin III, E ^e   Norelli, S ^a   Pelosi, E ^a   Garaci, E ^f   Savarino, A ^a   Palamara, A T ^g,h  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b SECTION OF MATHEMATICS   (Italy)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Vaccine and Gene Therapy Institute of Florida   (United States)

^e GEORGE MASON UNIVERSITY   (United States)

^f UNIVERSITY OF ROME TOR VERGATA   (Italy)

^g SAPIENZA UNIVERSITY OF ROME   (Italy)

^h IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

apoptosis; auranofin; differentiation effect; HIV cure; memory compartment; oxidative stress

Indexed keywords

AURANOFIN; CD27 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE P38; PYRUVIC ACID;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANTIGEN EXPRESSION; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG SELECTIVITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL;

APOPTOSIS; AURANOFIN; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CELLS, CULTURED; GLUTATHIONE; HUMANS; LYMPHOCYTES; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SULFHYDRYL COMPOUNDS;

EID: 84891751192     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.473     Document Type: Article

References (49)

1. Badley AD, Sainski A, Wightman F, Lewin SR. Altering cell death pathways as an approach to cure HIV infection. Cell Death Dis 2013; 4: 718
2. Lafeuillade A. Eliminating the HIV reservoir. Curr HIV/AIDS Rep 2012; 9: 121-131
3. Remoli AL, Marsili G, Battistini A, Sgarbanti M. The development of immune-modulating compounds to disrupt HIV latency. Cytokine Growth Factor Rev 2012; 23: 159-172
4. Monforte AD, Svicher V, Nozza S, Lazzarin A, Marchetti G, Perno CF. Highlights on HIV eradication in 2013. AIDS 2013 [Epub ahead of print]
5. Savarino A, Garaci E. Therapeutic imprinting of the immune system: Towards a remission of AIDS in primates? Retrovirology 2012; 9: 75
6. Palmer S, Josefsson L, Coffin JM. HIV reservoirs and the possibility of a cure for HIV infection. J Intern Med 2011; 270: 550-560
7. Lewis MG, Dafonseca S, Chomont N, Palamara AT, Tardugno M, Mai A et al. Gold drug auranofin restricts the viral reservoir in the monkey AIDS model and induces containment of viral load following ART suspension. AIDS 2011; 25: 1347-1356
8. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B et al. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med 2009; 15: 893-900
9. Chomont N, DaFonseca S, Vandergeeten C, Ancuta P, Sé kaly RP. Maintenance of CD4+ T-cell memory and HIV persistence: Keeping memory, keeping HIV. Curr Opin HIV AIDS 2011; 6: 30-36
10. Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, Pierson T et al. 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; 5: 512-517
11. Shytaj IL, Norelli S, Chirullo B, Della Corte A, Collins M, Yalley-Ogunro J et al. A highly intensified ART regimen induces long-Term viral suppression and restriction of the viral reservoir in a simian AIDS model. PLoS Pathog 2012; 8: E1002774
12. Shytaj IL, Chirullo B, Wagner W, Ferrari MG, Sgarbanti R, Corte AD et al. Investigational treatment suspension and enhanced cell-mediated immunity at rebound followed by drugfree remission of simian AIDS. Retrovirology 2013; 10: 71
13. Eisler R. Chrysotherapy: A synoptic review. Inflamm Res 2003; 52: 487-501
14. Friker SP. Medical uses of gold compounds: Past, present and future. Gold Bull 1996; 29: 53-59
15. Sutton BM. Gold compound for rheumatoid arthritis. Gold Bull 1986; 19: 15-16
16. Kean WF, Hart L, Buchanan WW. Auranofin. Br J Rheumatol 1997; 36: 560-572
17. Hashimoto K, Whitehurst CE, Lipsky PE. Synergistic inhibition of T cell proliferation by gold sodium thiomalate and auranofin. J Rheumatol 1994; 21: 1020-1026
18. Han S, Kim K, Kim H, Kwon J, Lee YH, Lee CK et al. Auranofin inhibits overproduction of pro-inflammatory cytokines, cyclooxygenase expression and PGE2 production in macrophages. Arch Pharm Res 2008; 31: 67-74
19. Kim TS, Kang BY, Lee MH, Choe YK, Hwang SY. Inhibition of interleukin-12 production by auranofin, an anti-rheumatic gold compound, deviates CD4(R) T cells from the Th1 to the Th2 pathway. Br J Pharmacol 2001; 134: 571-578
20. Gromer S, Wissing J, Behne D, Ashman K, Schirmer RH, Flohé L et al. A hypothesis on the catalytic mechanism of the selenoenzyme thioredoxin reductase. Biochem J 1998; 332: 591-592
21. Rigobello MP, Scutari G, Boscolo R, Bindoli A. Induction of mitochondrial permeability transition by auranofin, a gold(I)-phosphine derivative. Br J Pharmacol 2002; 136: 1162-1168
22. Rigobello MP, Folda A, Dani B, Menabo R, Scutari G, Bindoli A. Gold(I) complexes determine apoptosis with limited oxidative stress in Jurkat T cells. Eur J Pharmacol 2008; 582: 26-34
23. Cox AG, Brown KK, Arner ES, Hampton MB. The thioredoxin reductase inhibitor auranofin triggers apoptosis through a Bax/Bak-dependent process that involves peroxiredoxin 3 oxidation. Biochem Pharmacol 2008; 76: 1097-1109
24. López M, Soriano V, Peris-Pertusa A, Rallón N, Restrepo C, Benito JM. Elite controllers display higher activation on central memory CD8 T cells than HIV patients successfully on HAART. AIDS Res Hum Retroviruses 2011; 27: 157-165
25. Hazenberg MD, Otto SA, van Benthem BH, Roos MT, Coutinho RA, Lange JM et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 2003; 17: 1881-1888
26. Liu C, Liu Z, Li M, Li X, Wong YS, Ngai SM et al. Enhancement of auranofin-induced apoptosis in MCF-7 human breast cells by selenocystine, a synergistic inhibitor of thioredoxin reductase. PLoS One 2013; 8: E53945
27. Sies H. Glutathione and its role in cellular functions. Free Radic Biol Med 1999; 27: 916-921
28. Lin S, Del Razo LM, Styblo M, Wang C, Cullen WR, Thomas DJ. Arsenicals inhibit thioredoxin reductase in cultured rat hepatocytes. Chem Res Toxicol 2001; 14: 305-311
29. McCubrey JA, Lahair MM, Franklin RA. Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 2006; 8: 1775-1789
30. Cobb MH. MAP kinase pathways. Prog Biophys Mol Biol 1999; 71: 479-500
31. Sugawara T, Moriguchi T, Nishida E, Takahama Y. Differential roles of ERK and p38 MAP kinase pathways in positive and negative selection of T lymphocytes. Immunity 1998; 9: 565-574
32. Nordberg J, Arné r ES. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 2001; 31: 1287-1312
33. Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: Progress, pitfalls, and prospects. Free Radic Biol Med 2007; 43: 995-1022
34. Filomeni G, Piccirillo S, Rotilio G, Ciriolo MR. p38 MAPK and ERK1/2 dictate cell death/ survival response to different pro-oxidant stimuli via p53 and Nrf2 in neuroblastoma cells SH-SY5Y. Biochem Pharmacol 2012; 83: 1349-1357
35. Fenton HJH. Oxidation of tartaric acid in presence of iron. J Chem Soc 1894; 65: 899-910
36. Cobb MH, Goldsmith EJ. How MAP kinases are regulated. J Biol Chem 1995; 270: 14843-14846
37. Karin M. The regulation of AP-1 activity by mitogen-Activated protein kinases. J Biol Chem 1995; 270: 16483-16486
38. Ohno K, Han J. The p38 signal transduction pathway activation and function. Cell Signal 2000; 12: 1-13
39. Filomeni G, Ciriolo MR. Redox control of apoptosis: An update. Antioxid Redox Signal 2006; 8: 2187-2192
40. Chang KC, Hsu CC, Liu SH, Su CC, Yen CC, Lee MJ et al. Cadmium induces apoptosis in pancreatic b-cells through a mitochondria-dependent pathway: The role of oxidative stress-mediated c-Jun N-Terminal kinase activation. PLoS One 2013; 8: E54374
41. Zhao WX, Tang SS, Jin X, Zhang CM, Zhang T, Wang CC et al. Olaquindox-induced apoptosis is suppressed through p38 MAPK and ROS-mediated JNK pathways in HepG2 cells. Cell Biol Toxicol 2013; 29: 229-238
42. Kim IS, Jin JY, Lee IH, Park SJ. Auranofin induces apoptosis and when combined with retinoic acid enhances differentiation of acute promyelocytic leukaemia cells in vitro. Br J Pharmacol 2004; 142: 749-755
43. Buettner GR. Superoxide dismutase in redox biology: The roles of superoxide and hydrogen peroxide. Anticancer Agents Med Chem 2011; 11: 341-346
44. Takahashi A, Hanson MG, Norell HR, Havelka AM, Kono K, Malmberg KJ et al. Preferential cell death of CD8+ effector memory (CCR7-CD45RA-) T cells by hydrogen peroxideinduced oxidative stress. J Immunol 2005; 174: 6080-6087
45. De Chiara G, Marcocci ME, Torcia M, Lucibello M, Rosini P, Bonini P. Bcl-2 Phosphorylation by p38 MAPK: Identification of target sites and biologic consequences. J Biol Chem 2006; 281: 21353-21361
46. Farley N, Pedraza-Alva G, Serrano-Gomez D, Nagaleekar V, Aronshtam A, Krahl T. p38 mitogen-Activated protein kinase mediates the Fas-induced mitochondrial death pathway in CD8+ T cells. Mol Cell Biol 2006; 26: 2118-2129
47. Weiss A, Littman DR. Signal transduction by lymphocyte antigen receptors. Cell 1994; 76: 263-274
48. Marjuki H, Alam MI, Ehrhardt C, Wagner R, Planz O, Klenk HD et al. Membrane accumulation of influenza A virus hemagglutinin triggers nuclear export of the viral genome via protein kinase Calpha-mediated activation of ERK signaling. J Biol Chem 2006; 281: 16707-16715
49. Espina V, Edmiston KH, Heiby M, Pierobon M, Sciro M, Merritt B et al. A portrait of tissue phosphoprotein stability in the clinical tissue procurement process. Mol Cell Proteomics 2008; 7: 1998-2018