HIV eradication symposium: will the brain be left behind?

Journal of NeuroVirology

Volumn 21, Issue 3, 2015, Pages 322-334

  Brew, B J ^a   Robertson, K ^b   Wright, E J ^c   Churchill, M ^e   Crowe, S M ^c   Cysique, L A ^a,d   Deeks, S ^f   Garcia, J V ^b   Gelman, B ^g   Gray, L R ^e   Johnson, T ^h   Joseph, J ⁱ   Margolis, D M ^b   Mankowski, J L ^j   Spencer, B ^k  

^a ST VINCENT S HOSPITAL   (Australia)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c ALFRED HOSPITAL   (Australia)

^d School of Medical Science   (Australia)

^e BURNET INSTITUTE   (Australia)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^h NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

ⁱ NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

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

^k UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

Acquired immunodeficiency syndrome; Brain; Eradication; HIV associated neurocognitive disorders; Human immunodeficiency virus type 1

Indexed keywords

BRAIN; DISEASE CARRIER; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; VIROLOGY;

BRAIN; DISEASE RESERVOIRS; HIV INFECTIONS; HUMANS;

EID: 84939970909     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-015-0322-6     Document Type: Article

References (72)

1. An SF, Groves M, Giometto B, Beckett AA, Scaravilli F (1999) Detection and localisation of HIV-1 DNA and RNA in fixed adult AIDS brain by polymerase chain reaction/in situ hybridisation technique. Acta Neuropathol 98(5):481–487
2. Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE (2005) Influence of HAART on HIV-related CNS disease and neuroinflammation. J Neuropathol Exp Neurol 64(6):529–536
3. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM et al (2012a) Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487(7408):482–485
4. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM, Parker DC, Anderson EM, Kearney MF, Strain MC, Richman DD, Hudgens MG, Bosch RJ, Coffin JM, Eron JJ, Hazuda DJ, Margolis DM (2012b) Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487(7408):482–485, Erratum in: Nature 2012 Sep 20;489(7416):460
5. Archin NM, Sung JM, Garrido C, Soriano-Sarabia N, Margolis DM (2014) Eradicating HIV-1 infection: seeking to clear a persistent pathogen. Nat Rev Microbiol 12(11):750–764
6. Barouch DH, Deeks SG (2014) Immunologic strategies for HIV-1 remission and eradication. Science 345(6193):169–174
7. Brew BJ, Gray L, Lewin SR, Churchill M (2013) Is specific HIV eradication from the brain possible or needed? Exp Opin Biol Ther 13(3):403–409
8. Bullen CK, Laird GM, Durand CM, Siliciano JD, Siliciano RF (2014) New ex vivo approaches distinguish effective and ineffective single agents for reversing HIV-1 latency in vivo. Nat Med 20(4):425–429
9. Butler KM, Gavin P, Coughlan S, Rochford A, Donagh SM, Cunningham O, Poulsom H, Watters S, Klein N (2014) Rapid Viral Rebound after 4 Years of Suppressive Therapy in a Seronegative HIV-1 Infected Infant Treated from Birth. Pediatr Infect Dis J. [Epub ahead of print]
10. Buzon MJ, Massanella M, Llibre JM, Esteve A, Dahl V, Puertas MC et al (2010) HIV-1 replication and immune dynamics are affected by raltegravir intensification of HAART-suppressed subjects. Nat Med 16(4):460–465
11. Caniglia EC, Cain LE, Justice A, Tate J, Logan R, Sabin C, Winston A, van Sighem A, Miro JM, Podzamczer D, Olson A, Arribas JR, Moreno S, Meyer L, del Romero J, Dabis F, Bucher HC, Wandeler G, Vourli G, Skoutelis A, Lanoy E, Gasnault J, Costagliola D, Hernán MA, HIV-CAUSAL Collaboration (2014) Antiretroviral penetration into the CNS and incidence of AIDS-defining neurologic conditions. Neurology 83(2):134–141
12. Chiu YL, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, Greene WC (2005) Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 435(7038):108–114
13. Chun TW, Davey RT Jr, Ostrowski M, Shawn Justement J, Engel D, Mullins JI et al (2000) Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat Med 6(7):757–761
14. Churchill MJ, Gorry PR, Cowley D, Lal L, Sonza S, Purcell DF, Thompson KA, Gabuzda D, McArthur JC, Pardo CA, Wesselingh SL (2006) Use of laser capture microdissection to detect integrated HIV-1 DNA in macrophages and astrocytes from autopsy brain tissues. J Neurovirol 12(2):146–152
15. Churchill MJ, Wesselingh SL, Cowley D, Pardo CA, McArthur JC, Brew BJ, Gorry PR (2009) Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 66(2):253–258
16. Clarke JN, Lake JA, Burrell CJ, Wesselingh SL, Gorry PR, Li P (2006) Novel pathway of human immunodeficiency virus type 1 uptake and release in astrocytes. Virology 348(1):141–155
17. Cockerham LR, Siliciano JD, Sinclair E, O'Doherty U, Palmer S, Yukl SA et al (2014) CD4+ and CD8+ T cell activation are associated with HIV DNA in resting CD4+ T cells. PLoS One 9(10):e110731
18. Dahl V, Lee E, Peterson J, Spudich SS, Leppla I, Sinclair E et al (2011) Raltegravir treatment intensification does not alter cerebrospinal fluid HIV-1 infection or immunoactivation in subjects on suppressive therapy. J Infect Dis 204(12):1936–1945
19. Dahl V, Gisslen M, Hagberg L, Peterson J, Shao W, Spudich S et al (2014a) An example of genetically distinct HIV type 1 variants in cerebrospinal fluid and plasma during suppressive therapy. J Infect Dis 209(10):1618–1622
20. Dahl V, Peterson J, Fuchs D, Gisslen M, Palmer S, Price RW (2014b) Low levels of HIV-1 RNA detected in the cerebrospinal fluid after up to 10 years of suppressive therapy are associated with local immune activation. AIDS 28(15):2251–2258
21. Deiva K, Khiati A, Hery C, Salim H, Leclerc P, Horellou P, Tardieu M (2006) CCR5-, DC-SIGN-dependent endocytosis and delayed reverse transcription after human immunodeficiency virus type 1 infection in human astrocytes. AIDS Res Hum Retrovir 22(11):1152–1161
22. Denton PW, Olesen R, Choudhary SK, Archin NM, Wahl A, Swanson MD et al (2012) Generation of HIV latency in humanized BLT mice. J Virol 86(1):630–634
23. Desplats P, Dumaop W, Smith D, Adame A, Everall I, Letendre S et al (2013) Molecular and pathologic insights from latent HIV-1 infection in the human brain. Neurology 80(15):1415–1423
24. Dinoso JB, Rabi SA, Blankson JN, Gama L, Mankowski JL, Siliciano RF et al (2009) A simian immunodeficiency virus-infected macaque model to study viral reservoirs that persist during highly active antiretroviral therapy. J Virol 83(18):9247–9257
25. Dou H, Grotepas CB, McMillan JM, Destache CJ, Chaubal M, Werling J et al (2009) Macrophage delivery of nanoformulated antiretroviral drug to the brain in a murine model of neuroAIDS. J Immunol 183(1):661–669
26. Eden A, Fuchs D, Hagberg L, Nilsson S, Spudich S, Svennerholm B et al (2010) HIV-1 viral escape in cerebrospinal fluid of subjects on suppressive antiretroviral treatment. J Infect Dis 202(12):1819–1825
27. Ellery PJ, Tippett E, Chiu YL, Paukovics G, Cameron PU, Solomon A et al (2007) The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J Immunol 178(10):6581–6589
28. Fischer-Smith T, Croul S, Sverstiuk AE, Capini C, L'Heureux D, Regulier EG et al (2001) CNS invasion by CD14+/CD16+ peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J Neurovirol 7(6):528–541
29. Gandhi RT, Coombs RW, Chan ES, Bosch RJ, Zheng L, Margolis DM et al (2012) No effect of raltegravir intensification on viral replication markers in the blood of HIV-1-infected patients receiving antiretroviral therapy. J Acquir Immune Defic Syndr 59(3):229–235
30. Garvey LJ, Pavese N, Politis M, Ramlackhansingh A, Brooks DJ, Taylor-Robinson SD et al (2014) Increased microglia activation in neurologically asymptomatic HIV-infected patients receiving effective ART. AIDS 28(1):67–72
31. Gelman BB, Chen T, Lisinicchia JG, Soukup VM, Carmical JR, Starkey JM, Masliah E, Commins DL, Brandt D, Grant I, Singer EJ, Levine AJ, Miller J, Winkler JM, Fox HS, Luxon BA, Morgello S (2012a) National NeuroAIDS Tissue Consortium. The National NeuroAIDS Tissue Consortium brain gene array: two types of HIV-associated neurocognitive impairment. PLoS One 7(9):e46178
32. Gelman BB, Lisinicchia JG, Chen T, Johnson KM, Jennings K, Freeman DH Jr, Soukup VM (2012b) Prefrontal dopaminergic and enkephalinergic synaptic accommodation in HIV-associated neurocognitive disorders and encephalitis. J Neuroimmune Pharm 7(3):686–700
33. Gelman BB, Lisinicchia JG, Morgello S, Masliah E, Commins D, Achim CL, Fox HS, Kolson DL, Grant I, Singer E, Yiannoutsos CT, Sherman S, Gensler G, Moore DJ, Chen T, Soukup VM (2013) Neurovirological correlation with HIV-associated neurocognitive disorders and encephalitis in a HAART-era cohort. J Acquir Immune Defic Syndr 62(5):487–495
34. Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5(1):69–81
35. Gray LR, Tachedjian G, Ellett AM, Roche MJ, Cheng W-J, Guillemin G, Brew BJ, Turville SG, Wesselingh SL, Gorry PR, Churchill MJ (2013) The NRTIs lamivudine, stavudine and zidovudine have reduced HIV-1 inhibitory activity in astrocytes. PLoS One 8(4):e62196
36. Gray LR, Turville SG, Hitchen TL, Cheng WJ, Ellett AM, Salimi H, Roche MJ, Wesselingh SL, Gorry PR, Churchill MJ (2014) HIV-1 entry and trans-infection of astrocytes involves CD81 vesicles. PLoS One 9(2):e90620
37. Hatano H, Strain MC, Scherzer R, Bacchetti P, Wentworth D, Hoh R et al (2013) Increase in 2-long terminal repeat circles and decrease in D-dimer after raltegravir intensification in patients with treated HIV infection: a randomized, placebo-controlled trial. J Infect Dis 208(9):1436–1442
38. Henrich TJ, Hanhauser E, Marty FM, Sirignano MN, Keating S, Lee TH et al (2014) Antiretroviral-free HIV-1 remission and viral rebound after allogeneic stem cell transplantation: report of 2 cases. Ann Intern Med 161(5):319–327
39. Ho YC, Shan L, Hosmane NN, Wang J, Laskey SB, Rosenbloom DI et al (2013) Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure. Cell 155(3):540–551
40. Honeycutt JB, Sheridan PA, Matsushima GK, Garcia JV (2014) Humanized mouse models for HIV-1 infection of the CNS. J Neurovirol
41. Hutter G, Nowak D, Mossner M, Ganepola S, Mussig A, Allers K et al (2009) Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 360(7):692–698
42. Johnson TP, Patel K, Johnson KR, Maric D, Calabresi PA, Hasbun R, Nath A (2013) Induction of IL-17 and nonclassical T-cell activation by HIV-Tat protein. Proc Natl Acad Sci U S A 110(33):13588–13593
43. Kelly KM, Beck SE, Metcalf Pate KA, Queen SE, Dorsey JL, Adams RJ, Avery LB, Hubbard W, Tarwater PM, Mankowski JL (2013) Neuroprotective maraviroc monotherapy in simian immunodeficiency virus-infected macaques: reduced replicating and latent SIV in the brain. AIDS 27(18):F21–F28
44. Letendre S (2011) Central nervous system complications in HIV disease: HIV-associated neurocognitive disorder. Top Antivir Med 19(4):137–142
45. Letendre SL, Ellis RJ, Ances BM, McCutchan JA (2010) Neurologic complications of HIV disease and their treatment. Top HIV Med Publ Int AIDS Soc USA 18(2):45–55
46. Liu Y, Liu H, Kim BO, Gattone VH, Li J, Nath A, Blum J, He JJ (2004) CD4-independent infection of astrocytes by human immunodeficiency virus type 1: requirement for the human mannose receptor. Journal Virology 2004;78(8):4120–33. Erratum in. J Virol 78(13):7288–7289
47. Llibre JM, Buzon MJ, Massanella M, Esteve A, Dahl V, Puertas MC et al (2012) Treatment intensification with raltegravir in subjects with sustained HIV-1 viraemia suppression: a randomized 48-week study. Antivir Ther 17(2):355–364
48. Marra CM, Zhao Y, Clifford DB, Letendre S, Evans S, Henry K, Ellis RJ, Rodriguez B, Coombs RW, Schifitto G, McArthur JC, Robertson K, AIDS Clinical Trials Group 736 Study Team (2009) Impact of combination antiretroviral therapy on cerebrospinal fluid HIV RNA and neurocognitive performance. AIDS 23(11):1359–1366
49. McElrath MJ, Steinman RM, Cohn ZA (1991) Latent HIV-1 infection in enriched populations of blood monocytes and T cells from seropositive patients. J Clin Investig 87(1):27–30
50. Mikovits JA, Lohrey NC, Schulof R, Courtless J, Ruscetti FW (1992) Activation of infectious virus from latent human immunodeficiency virus infection of monocytes in vivo. J Clin Invest 90(4):1486–1491
51. Nath A, Hartloper V, Furer M, Fowke KR (1995) Infection of human fetal astrocytes with HIV-1: viral tropism and the role of cell to cell contact in viral transmission. J Neuropathol Exp Neurol 54(3):320–330
52. Patrick C, Crews L, Desplats P, Dumaop W, Rockenstein E, Achim CL et al (2011) Increased CDK5 expression in HIV encephalitis contributes to neurodegeneration via tau phosphorylation and is reversed with Roscovitine. Am J Pathol 178(4):1646–1661
53. Prinz M, Priller J (2014) Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci 15(5):300–312
54. Robertson K, Liner J, Meeker RB (2012a) Antiretroviral neurotoxicity. J Neurovirol 18(5):388–399
55. Robertson K, Jiang H, Kumwenda J, Supparatpinyo K, Evans S, Campbell TB, Price R, Tripathy S, Kumarasamy N, La Rosa A, Santos B, 5199 study team, Silva MT, Montano S, Kanyama C, Faesen S, Murphy R, Hall C, Marra CM, Marcus C, Berzins B, Allen R, Housseinipour M, Amod F, Sanne I, Hakim J, Walawander A, Nair A, AIDS Clinical Trials Group (2012b) Improved neuropsychological and neurological functioning across three antiretroviral regimens in diverse resource-limited settings: AIDS Clinical Trials Group study a5199, the International Neurological Study. Clin Infect Dis 55(6):868–76
56. Schnell G, Price RW, Swanstrom R, Spudich S (2010) Compartmentalization and clonal amplification of HIV-1 variants in the cerebrospinal fluid during primary infection. J Virol 84(5):2395–2407
57. Schnell G, Joseph S, Spudich S, Price RW, Swanstrom R (2011) HIV-1 replication in the central nervous system occurs in two distinct cell types. PLoS Pathog 7(10):e1002286
58. Sharer LR, Saito Y, Da Cunha A, Ung PC, Gelbard HA, Epstein LG, Blumberg BM (1996) In situ amplification and detection of HIV-1 DNA in fixed pediatric AIDS brain tissue. Hum Pathol 27(6):614–617
59. Sonza S, Maerz A, Deacon N, Meanger J, Mills J, Crowe S (1996) Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes. J Virol 70(6):3863–3869
60. Sonza S, Mutimer HP, Oelrichs R, Jardine D, Harvey K, Dunne A et al (2001) Monocytes harbour replication-competent, non-latent HIV-1 in patients on highly active antiretroviral therapy. AIDS 15(1):17–22
61. Spudich S, Gisslen M, Hagberg L, Lee E, Liegler T, Brew B, Fuchs D, Tambussi G, Cinque P, Hecht FM, Price RW (2011) Central nervous system immune activation characterizes primary human immunodeficiency virus 1 infection even in participants with minimal cerebrospinal fluid viral burden. J Infect Dis 204(5):753–760
62. Sturdevant CB, Schnell G, Price RW, Spudich S, Swanstrom R (2014) Replication of HIV-1 in the Central Nervous System of Adults Early After Infection. Oral abstract #32 CROI
63. Takahashi K, Wesselingh SL, Griffin DE, McArthur JC, Johnson RT, Glass JD (1996) Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunocytochemistry. Ann Neurol 39(6):705–711
64. Teo I, Veryard C, Barnes H, An SF, Jones M, Lantos PL et al (1997) Circular forms of unintegrated human immunodeficiency virus type 1 DNA and high levels of viral protein expression: association with dementia and multinucleated giant cells in the brains of patients with AIDS. J Virol 71(4):2928–2933
65. Thompson KA, Churchill MJ, Gorry PR, Sterjovski J, Oelrichs RB, Wesselingh SL, McLean CA (2004) Astrocyte specific viral strains in HIV dementia. Ann Neurol 56(6):873–877
66. Thompson KA, Cherry CL, Bell JE, McLean CA (2011) Brain cell reservoirs of latent virus in presymptomatic HIV-infected individuals. Am J Pathol 179(4):1623–1629
67. Valcour V, Chalermchai T, Sailasuta N, Marovich M, Lerdlum S, Suttichom D, Suwanwela NC, Jagodzinski L, Michael N, Spudich S, van Griensven F, de Souza M, Kim J, Ananworanich J, RV254/SEARCH 010 Study Group (2012) Central nervous system viral invasion and inflammation during acute HIV infection. J Infect Dis 206(2):275–282
68. Wege AK, Melkus MW, Denton PW, Estes JD, Garcia JV (2008) Functional and phenotypic characterization of the humanized BLT mouse model. Curr Top Microbiol Immunol 324:149–165
69. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C et al (2001) Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J Exp Med 193(8):905–915
70. Yukl SA, Shergill AK, Ho T, Killian M, Girling V, Epling L et al (2013) The distribution of HIV DNA and RNA in cell subsets differs in gut and blood of HIV-positive patients on ART: implications for viral persistence. J Infect Dis 208(8):1212–1220
71. Zhang LJ, Vogel WK, Liu X, Topark-Ngarm A, Arbogast BL, Maier CS et al (2012) Coordinated regulation of transcription factor Bcl11b activity in thymocytes by the mitogen-activated protein kinase (MAPK) pathways and protein sumoylation. J Biol Chem 287(32):26971–26988
72. Zhu T, Muthui D, Holte S, Nickle D, Feng F, Brodie S et al (2002) Evidence for human immunodeficiency virus type 1 replication in vivo in CD14(+) monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy. J Virol 76(2):707–716