Minocycline attenuates HIV-1 infection and suppresses chronic immune activation in humanized NOD/LtsZ-scidIL-2Rγnull mice

Immunology

Volumn 142, Issue 4, 2014, Pages 562-572

  Singh, Maneesh ^a   Singh, Pratibha ^a   Vaira, Dolores ^a   Amand, Mathieu ^a   Rahmouni, Souad ^a   Moutschen, Michel ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

HIV; Immune activation; Minocycline

Indexed keywords

CD14 ANTIGEN; CD38 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; HLA DR ANTIGEN; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MINOCYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL THERAPY; ARTICLE; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPHOCYTE COUNT; MOUSE; NOD SCID GAMMA MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; UMBILICAL CORD BLOOD; UPREGULATION; VIRUS ACTIVATION; VIRUS ATTENUATION; VIRUS LOAD; VIRUS REPLICATION;

HIV; HUMANIZED NOD/LTSZ-SCIDIL-2RΓNULL MICE; IMMUNE ACTIVATION; MINOCYCLINE;

ANIMALS; ANTI-BACTERIAL AGENTS; HIV INFECTIONS; HIV-1; HUMANS; INTERLEUKIN-10; MICE; MICE, INBRED NOD; MICE, SCID; MINOCYCLINE; VIRUS REPLICATION;

EID: 84899657924     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12246     Document Type: Article

References (57)

1. d'Ettorre G, Paiardini M, Ceccarelli G, Silvestri G, Vullo V. HIV-associated immune activation: from bench to bedside. AIDS Res Hum Retroviruses 2011; 27:355-64.
2. Douek D. HIV disease progression: immune activation, microbes, and a leaky gut. Top HIV Med 2007; 15:114-17.
3. Douek DC, Roederer M, Koup RA. Emerging concepts in the immunopathogenesis of AIDS. Annu Rev Med 2009; 60:471-84.
4. Corbeau P, Reynes J. Immune reconstitution under antiretroviral therapy: the new challenge in HIV-1 infection. Blood 2011; 117:5582-90.
5. + T-cells despite suppression of HIV replication under HAART. AIDS Rev 2006; 8:88-97.
6. Lichtfuss GF, Hoy J, Rajasuriar R, Kramski M, Crowe SM, Lewin SR. Biomarkers of immune dysfunction following combination antiretroviral therapy for HIV infection. Biomark Med 2011; 5:171-86.
7. Grossman Z, Meier-Schellersheim M, Paul WE, Picker LJ. Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nat Med 2006; 12:289-95.
8. Liovat AS, Jacquelin B, Ploquin MJ, Barre-Sinoussi F, Muller-Trutwin MC. African non human primates infected by SIV - why don't they get sick? Lessons from studies on the early phase of non-pathogenic SIV infection. Curr HIV Res 2009; 7:39-50.
9. Chahroudi A, Bosinger SE, Vanderford TH, Paiardini M, Silvestri G. Natural SIV hosts: showing AIDS the door. Science 2012; 335:1188-93.
10. Long BR, Stoddart CA. Alpha interferon and HIV infection cause activation of human T cells in NSG-BLT mice. J Virol 2012; 86:3327-36.
11. Singh M, Singh P, Gaudray G et al. An improved protocol for efficient engraftment in NOD/LTSZ-SCIDIL-2Rγnull mice allows HIV replication and development of anti-HIV immune responses. PLoS ONE 2012; 7:e38491.
12. Brainard DM, Seung E, Frahm N et al. Induction of robust cellular and humoral virus-specific adaptive immune responses in human immunodeficiency virus-infected humanized BLT mice. J Virol 2009; 83:7305-21.
13. Copeland KF, Brooks JI. A novel use for an old drug: the potential for minocycline as anti-HIV adjuvant therapy. J Infect Dis 2010; 201:1115-17.
14. + T cells. J Infect Dis 2010; 201:1132-40.
15. Campbell JH, Burdo TH, Autissier P et al. Minocycline inhibition of monocyte activation correlates with neuronal protection in SIV neuroAIDS. PLoS ONE 2011; 6:e18688.
16. Follstaedt SC, Barber SA, Zink MC. Mechanisms of minocycline-induced suppression of simian immunodeficiency virus encephalitis: inhibition of apoptosis signal-regulating kinase 1. J Neurovirol 2008; 14:376-88.
17. Zink MC, Uhrlaub J, DeWitt J et al. Neuroprotective and anti-human immunodeficiency virus activity of minocycline. JAMA 2005; 293:2003-11.
18. Ratai EM, Bombardier JP, Joo CG et al. Proton magnetic resonance spectroscopy reveals neuroprotection by oral minocycline in a nonhuman primate model of accelerated NeuroAIDS. PLoS ONE 2010; 5:e10523.
19. Jenwitheesuk E, Samudrala R. Identification of potential HIV-1 targets of minocycline. Bioinformatics 2007; 23:2797-9.
20. Sacktor N, Miyahara S, Deng L et al. Minocycline treatment for HIV-associated cognitive impairment: results from a randomized trial. Neurology 2011; 77:1135-42.
21. Ho EL, Spudich SS, Lee E, Fuchs D, Sinclair E, Price RW. Minocycline fails to modulate cerebrospinal fluid HIV infection or immune activation in chronic untreated HIV-1 infection: results of a pilot study. AIDS Res Ther 2011; 8:17.
22. Benito JM, Lopez M, Lozano S, Martinez P, Gonzalez-Lahoz J, Soriano V. CD38 expression on CD8 T lymphocytes as a marker of residual virus replication in chronically HIV-infected patients receiving antiretroviral therapy. AIDS Res Hum Retroviruses 2004; 20:227-33.
23. + cell levels. The Multicenter AIDS Cohort Study Group. J Infect Dis 1994; 170:775-81.
24. Giorgi JV, Hultin LE, McKeating JA et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 1999; 179:859-70.
25. Day CL, Kaufmann DE, Kiepiela P et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006; 443:350-4.
26. + T cells correlates with disease progression and defines a reversible immune dysfunction. Nat Immunol 2007; 8:1246-54.
27. Kaufmann DE, Walker BD. PD-1 and CTLA-4 inhibitory cosignaling pathways in HIV infection and the potential for therapeutic intervention. J Immunol 2009; 182:5891-7.
28. Brenchley JM, Price DA, Schacker TW et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12:1365-71.
29. Sandler NG, Wand H, Roque A et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 2011; 203:780-90.
30. + T-cell changes independent of viral load. Blood 2004; 104:942-7.
31. -/- (NSG) BLT mice. Virology 2011; 417:154-60.
32. Garrido-Mesa N, Zarzuelo A, Galvez J. What is behind the non-antibiotic properties of minocycline? Pharmacol Res 2013; 67:18-30.
33. Kloppenburg M, Brinkman BM, de Rooij-Dijk HH, Miltenburg AM, Daha MR, Breedveld FC, Dijkmans BA, Verweij C The tetracycline derivative minocycline differentially affects cytokine production by monocytes and T lymphocytes. Antimicrob Agents Chemother 1996; 40:934-40.
34. Giuliani F, Hader W, Yong VW. Minocycline attenuates T cell and microglia activity to impair cytokine production in T cell-microglia interaction. J Leukoc Biol 2005; 78:135-43.
35. Kloppenburg M, Verweij CL, Miltenburg AM, Verhoeven AJ, Daha MR, Dijkmans BA, Breedveld FC. The influence of tetracyclines on T cell activation. Clin Exp Immunol 1995; 102:635-41.
36. Li L, Ben Y, Zhu Z, Li W, Xu J, Zhang X. Minocycline down-regulates topical mucosal inflammation during the application of microbicide candidates. PLoS ONE 2012; 7:e43211.
37. + T cells. J Biol Chem 2011; 286:11275-82.
38. Lawn SD, Butera ST, Folks TM. Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin Microbiol Rev 2001; 14:753-77, table of contents.
39. Si Q, Cosenza M, Kim MO, Zhao ML, Brownlee M, Goldstein H, Lee S. A novel action of minocycline: inhibition of human immunodeficiency virus type 1 infection in microglia. J Neurovirol 2004; 10:284-92.
40. Liegler TJ, Yonemoto W, Elbeik T, Vittinghoff E, Buchbinder SP, Greene WC. Diminished spontaneous apoptosis in lymphocytes from human immunodeficiency virus-infected long-term nonprogressors. J Infect Dis 1998; 178:669-79.
41. Katsikis PD, Garcia-Ojeda ME, Torres-Roca JF, Tijoe IM, Smith CA, Herzenberg LA, Herzenberg LA. Interleukin-1β converting enzyme-like protease involvement in Fas-induced and activation-induced peripheral blood T cell apoptosis in HIV infection. TNF-related apoptosis-inducing ligand can mediate activation-induced T cell death in HIV infection. J Exp Med 1997; 186:1365-72.
42. Chen M, Ona VO, Li M et al. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 2000; 6:797-801.
43. Wang X, Zhu S, Drozda M et al. Minocycline inhibits caspase-independent and -dependent mitochondrial cell death pathways in models of Huntington's disease. Proc Natl Acad Sci USA 2003; 100:10483-7.
44. Pi R, Li W, Lee NT et al. Minocycline prevents glutamate-induced apoptosis of cerebellar granule neurons by differential regulation of p38 and Akt pathways. J Neurochem 2004; 91:1219-30.
45. Sandler NG, Douek DC. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 2012; 10:655-66.
46. + T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 2008; 197:126-33.
47. Jiang W, Lederman MM, Hunt P et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis 2009; 199:1177-85.
48. Hofer U, Schlaepfer E, Baenziger S et al. Inadequate clearance of translocated bacterial products in HIV-infected humanized mice. PLoS Pathog 2010; 6:e1000867.
49. Cunha BA, Comer JB, Jonas M. The tetracyclines. Med Clin North Am 1982; 66:293-302.
50. Ejim L, Farha MA, Falconer SB, Wildenhain J, Coombes BK, Tyers M, Brown ED, Wright GD. Combinations of antibiotics and nonantibiotic drugs enhance antimicrobial efficacy. Nat Chem Biol 2011; 7:348-50.
51. Huang TY, Chu HC, Lin YL, Lin CK, Hsieh TY, Chang WK, Chao YC, Liao CL. Minocycline attenuates experimental colitis in mice by blocking expression of inducible nitric oxide synthase and matrix metalloproteinases. Toxicol Appl Pharmacol 2009; 237:69-82.
52. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 1999; 96:13496-500.
53. Tikka TM, Koistinaho JE. Minocycline provides neuroprotection against N-methyl-d-aspartate neurotoxicity by inhibiting microglia. J Immunol 2001; 166:7527-33.
54. Tikka TM, Vartiainen NE, Goldsteins G, Oja SS, Andersen PM, Marklund SL, Koistinaho J. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain 2002; 125:722-31.
55. Zhou B, Cron RQ, Wu B, Genin A, Wang Z, Liu S, Robson P, Baldwin HS. Regulation of the murine Nfatc1 gene by NFATc2. J Biol Chem 2002; 277:10704-11.
56. Oestreich KJ, Yoon H, Ahmed R, Boss JM. NFATc1 regulates PD-1 expression upon T cell activation. J Immunol 2008; 181:4832-9.
57. Gibson HM, Hedgcock CJ, Aufiero BM, Wilson AJ, Hafner MS, Tsokos GC, Wong HK. Induction of the CTLA-4 gene in human lymphocytes is dependent on NFAT binding the proximal promoter. J Immunol 2007; 179:3831-40.