Reactivation of simian immunodeficiency virus reservoirs in the brain of virally suppressed macaques

AIDS

Volumn 31, Issue 1, 2017, Pages 5-14

  Gama, Lucio ^a   Abreu, Celina M ^a,b   Shirk, Erin N ^a   Price, Sarah L ^a   Li, Ming ^a   Laird, Greg M ^a   Metcalf Pate, Kelly A ^a   Wietgrefe, Stephen W ^c   O'Connor, Shelby L ^d   Pianowski, Luiz ^e   Haase, Ashley T ^c   Van Lint, Carine ^f   Siliciano, Robert F ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e Kyolab Rua Isaura Ap Oliviera Barbosa Terini   (Brazil)

^f UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Brain; Central nervous system; HIV 1; Ingenol B; Latency; Latency reversing agents; Simian immunodeficiency virus; Viral reservoir; Vorinostat

Indexed keywords

CD68 ANTIGEN; DARUNAVIR; INGENOL B; INTEGRASE INHIBITOR; L 870812; PROTEIN KINASE C ACTIVATOR; RITONAVIR; TENOFOVIR; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VORINOSTAT; ANTIRETROVIRUS AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIRETROVIRAL THERAPY; ARTICLE; CONTROLLED STUDY; DISORDERS OF HIGHER CEREBRAL FUNCTION; DRUG DOSE INCREASE; ENZYME LINKED IMMUNOSORBENT ASSAY; IN SITU HYBRIDIZATION; MACACA NEMESTRINA; MACROPHAGE; NONHUMAN; OCCIPITAL CORTEX; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS LATENCY; VIRUS LOAD; VIRUS REACTIVATION; VIRUS TRANSCRIPTION; ANIMAL; BRAIN; CEREBROSPINAL FLUID; COMPLICATION; DISEASE MODEL; DNA SEQUENCE; GENETICS; GENOTYPING TECHNIQUE; MACACA; PHYLOGENY; PHYSIOLOGY; PLASMA; VIROLOGY; VIRUS ACTIVATION;

ANIMALS; ANTI-RETROVIRAL AGENTS; BRAIN; CEREBROSPINAL FLUID; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE PRODUCTS, ENV; GENOTYPING TECHNIQUES; IN SITU HYBRIDIZATION; MACACA; NEUROCOGNITIVE DISORDERS; PHYLOGENY; PLASMA; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84988603501     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000001267     Document Type: Article

References (41)

1. Epstein LG, Sharer LR, Cho ES, Myenhofer M, Navia B, Price RW. HTLV-III/LAV-like retrovirus particles in the brains of patients with AIDS encephalopathy. AIDS Res 1984; 1:447-454.
2. Gyorkey F, Melnick JL, Sinkovics JG, Gyorkey P. Retrovirus resembling HTLV in macrophages of patients with AIDS. Lancet 1985; 1:106.
3. Ances BM, Clifford DB. HIV-associated neurocognitive disorders and the impact of combination antiretroviral therapies. Curr Neurol Neurosci Rep 2008; 8:455-461.
4. Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, Vaida F, et al. HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 2010; 75:2087-2096.
5. Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, et al. HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 2011; 17:3-16.
6. Eden A, Fuchs D, Hagberg L, Nilsson S, Spudich S, Svennerholm B, et al. HIV-1 viral escape in cerebrospinal fluid of subjects on suppressive antiretroviral treatment. J Infect Dis 2010; 202:1819-1825.
7. Yilmaz A, Yiannoutsos CT, Fuchs D, Price RW, Crozier K, Hagberg L, et al. Cerebrospinal fluid neopterin decay characteristics after initiation of antiretroviral therapy. J Neuroinflammation 2013; 10:62.
8. Spudich S, Gonzalez-Scarano F. HIV-1-related central nervous system disease: current issues in pathogenesis, diagnosis, and treatment. Cold Spring Harb Perspect Med 2012; 2:a007120.
9. Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, Pierson T, et al. Latent infection of CD4R T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med 1999; 5: 512-517.
10. 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.
11. Bullen CK, Laird GM, Durand CM, Siliciano JD, Siliciano RF. New ex vivo approaches distinguish effective and ineffective single agents for reversing HIV-1 latency in vivo. Nat Med 2014; 20:425-429.
12. Siliciano JD, Siliciano RF. Recent developments in the search for a cure for HIV-1 infection: targeting the latent reservoir for HIV-1. J Allergy Clin Immunol 2014; 134:12-19.
13. Honeycutt JB, Wahl A, Baker C, Spagnuolo RA, Foster J, Zakharova O, et al. Macrophages sustain HIV replication in vivo independently of T cells. J Clin Invest 2016; 126:1353-1366.
14. Henrich TJ, Hu Z, Li JZ, Sciaranghella G, Busch MP, Keating SM, et al. Long-term reduction in peripheral blood HIV type 1 reservoirs following reduced-intensity conditioning allogeneic stem cell transplantation. J Infect Dis 2013; 207:1694-1702.
15. Lorenzo-Redondo R, Fryer HR, Bedford T, Kim EY, Archer J, Kosakovsky Pond SL, et al. Persistent HIV-1 replicationmaintains the tissue reservoir during therapy. Nature 2016; 530:51-56.
16. Clements JE, Mankowski JL, Gama L, Zink MC. The accelerated simian immunodeficiency virus macaque model of human immunodeficiency virus-associated neurological disease: from mechanism to treatment. J Neurovirol 2008; 14:309-317.
17. Dinoso JB, Rabi SA, Blankson JN, Gama L, Mankowski JL, Siliciano RF, et al. A simian immunodeficiency virus-infected macaque model to study viral reservoirs that persist during highly active antiretroviral therapy. J Virol 2009; 83:9247-9257.
18. Laird GM, Bullen CK, Rosenbloom Di, Martin AR, Hill AL, Durand CM, et al. Ex vivo analysis identifies effective HIV-1 latency-reversing drug combinations. J Clin Invest 2015; 125:1901-1912.
19. Bouchat S, Gatot JS, Kabeya K, Cardona C, Colin L, Herbein G, et al. Histone methyltransferase inhibitors induce HIV-1 recovery in resting CD4(R) T cells from HIV-1-infected HAARTtreated patients. AIDS 2012; 26:1473-1482.
20. Reuse S, Calao M, Kabeya K, Guiguen A, Gatot JS, Quivy V, et al. Synergistic activation of HIV-1 expression by deacetylase inhibitors and prostratin: implications for treatment of latent infection. PLoS One 2009; 4:e6093.
21. Avettand-Fenoel V, Chaix ML, Blanche S, Burgard M, Floch C, Toure K, et al. LTR real-time PCR for HIV-1 DNA quantitation in blood cells for early diagnosis in infants born to seropositive mothers treated in HAART area (ANRS CO 01). J Med Virol 2009; 81:217-223.
22. Zink MC, Brice AK, Kelly KM, Queen SE, Gama L, Li M, et al. Simian immunodeficiency virus-infected macaques treated with highly active antiretroviral therapy have reduced central nervous system viral replication and inflammation but persistence of viral DNA. J Infect Dis 2010; 202:161-170.
23. Strain MC, Lada SM, Luong T, Rought SE, Gianella S, Terry VH, et al. Highly precise measurement of HIV DNA by droplet digital PCR. PLoS One 2013; 8:e55943.
24. Zeng M, Smith AJ, Wietgrefe SW, Southern PJ, Schacker TW, Reilly CS, et al. Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J Clin Invest 2011; 121:998-1008.
25. Babas T, Vieler E, Hauer DA, Adams RJ, Tarwater PM, Fox K, et al. Pathogenesis of SIV pneumonia: selective replication of viral genotypes in the lung. Virology 2001; 287:371-381.
26. Clements JE, Gama L, Graham DR, Mankowski JL, Zink MC. A simian immunodeficiency virus macaque model of highly active antiretroviral treatment: viral latency in the periphery and the central nervous system. Curr Opin HIV AIDS 2011; 6:37-42.
27. Letendre S, Marquie-Beck J, Capparelli E, Best B, Clifford D, Collier AC, et al. Validation of the CNS penetration-effectiveness rank for quantifying antiretroviral penetration into the central nervous system. Arch Neurol 2008; 65:65-70.
28. Shang HT, Ding JW, Yu SY, Wu T, Zhang QL, Liang FJ. Progress and challenges in the use of latent HIV-1 reactivating agents. Acta Pharmacol Sin 2015; 36:908-916.
29. White CH, Johnston HE, Moesker B, Manousopoulou A, Margolis DM, Richman DD, et al. Mixed effects of suberoylanilide hydroxamic acid (SAHA) on the host transcriptome and proteome and their implications for HIV reactivation from latency. Antiviral Res 2015; 123:78-85.
30. Badia R, Grau J, Riveira-Munoz E, Ballana E, Giannini G, Este JA. The thioacetate-omega(gamma-lactam carboxamide) HDAC inhibitor ST7612AA1 as HIV-1 latency reactivation agent. Antiviral Res 2015; 123:62-69.
31. Miana GA, Riaz M, Shahzad-Ul-Hussan S, Paracha RZ, Paracha UZ. Prostratin: an overview. Mini Rev Med Chem 2015; 15:1122-1130.
32. Abreu CM, Price SL, Shirk EN, Cunha RD, Pianowski LF, Clements JE, et al. Dual role of novel ingenol derivatives from Euphorbia tirucalli in HIV replication: inhibition of de novo infection and activation of viral LTR. PLoS One 2014; 9:e97257.
33. Pandelo Jose D, Bartholomeeusen K, da Cunha RD, Abreu CM, Glinski J, da Costa TB, et al. Reactivation of latent HIV-1 by new semi-synthetic ingenol esters. Virology 2014; 462-463:328-339.
34. Jiang G, Mendes EA, Kaiser P, Sankaran-Walters S, Tang Y, Weber MG, et al. Reactivation of HIV latency by a newly modified ingenol derivative via protein kinase Cdelta-NFkappaB signaling. AIDS 2014; 28:1555-1566.
35. Blankson JN, Finzi D, Pierson TC, Sabundayo BP, Chadwick K, Margolick JB, et al. Biphasic decay of latently infected CD4R T cells in acute human immunodeficiency virus type 1 infection. J Infect Dis 2000; 182:1636-1642.
36. Zink MC, Clements JE. A novel simian immunodeficiency virus model that provides insight into mechanisms of human immunodeficiency virus central nervous system disease. J Neurovirol 2002; 8 (Suppl 2):42-48.
37. Ling B, Piatak M Jr, Rogers L, Johnson AM, Russell-Lodrigue K, Hazuda DJ, et al. Effects of treatment with suppressive combination antiretroviral drug therapy and the histone deacetylase inhibitor suberoylanilide hydroxamic acid; (SAHA) on SIVinfected Chinese rhesus macaques. PLoS One 2014; 9:e102795.
38. Beck SE, Queen SE, Witwer KW, Metcalf Pate KA, Mangus LM, Gama L, et al. Paving the path to HIV neurotherapy: predicting SIV CNS disease. Eur J Pharmacol 2015; 759:303-312.
39. Grant I, Atkinson JH, Hesselink JR, Kennedy CJ, Richman DD, Spector SA, et al. Evidence for early central nervous system involvement in the acquired immunodeficiency syndrome (AIDS) and other human immunodeficiency virus (HIV) infections. Studies with neuropsychologic testing and magnetic resonance imaging. Ann Intern Med 1987; 107:828-836.
40. Ellis RJ, Moore DJ, Childers ME, Letendre S, McCutchan JA, Wolfson T, et al. Progression to neuropsychological impairment in human immunodeficiency virus infection predicted by elevated cerebrospinal fluid levels of human immunodeficiency virus RNA. Arch Neurol 2002; 59:923-928.
41. Perreau M, Savoye AL, De Crignis E, Corpataux JM, Cubas R, Haddad EK, et al. Follicular helper T cells serve as the major CD4 T cell compartment for HIV-1 infection, replication, and production. J Exp Med 2013; 210:143-156.