Humanized mouse models for HIV-1 infection of the CNS

Journal of NeuroVirology

Volumn 21, Issue 3, 2015, Pages 301-309

  Honeycutt, Jenna B ^a   Sheridan, Patricia A ^b   Matsushima, Glenn K ^a   Garcia, J Victor ^a  

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

^b University of North Carolina   (United States)

Author keywords

BLT mice; CNS; HIV; Humanized mice; Neuropathology

Indexed keywords

ANIMAL; DISEASE MODEL; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MOUSE;

AIDS DEMENTIA COMPLEX; ANIMALS; DISEASE MODELS, ANIMAL; HIV-1; HUMANS; MICE;

EID: 84939971082     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-014-0299-6     Document Type: Article

References (73)

1. Albright AV, Soldan SS, Gonzalez-Scarano F (2003) Pathogenesis of human immunodeficiency virus-induced neurological disease. J Neurovirol 9(2):222–227
2. Annamalai L, Bhaskar V, Pauley DR, Knight H, Williams K, Lentz M, Ratai E, Westmoreland SV, Gonzalez RG, O’Neil SP (2010) Impact of short-term combined antiretroviral therapy on brain virus burden in simian immunodeficiency virus-infected and CD8+ lymphocyte-depleted rhesus macaques. Am J Pathol 177(2):777–791
3. Anthony IC, Bell JE (2008) The Neuropathology of HIV/AIDS. Int Rev Psychiatry 20(1):15–24
4. Asheuer M, Pflumio F, Benhamida S, Dubart-Kupperschmitt A, Fouquet F, Imai Y, Aubourg P, Cartier N (2004) Human CD34+ cells differentiate into microglia and express recombinant therapeutic protein. Proc Natl Acad Sci U S A 101(10):3557–3562
5. Atchison RE, Gosling J, Monteclaro FS, Franci C, Digilio L, Charo IF, Goldsmith MA (1996) Multiple extracellular elements of CCR5 and HIV-1 entry: dissociation from response to chemokines. Science 274(5294):1924–1926
6. Chen MF, AJ Gill and D. L. Kolson (2014) “Neuropathogenesis of HIV-associated neurocognitive disorders: roles for immune activation, HIV blipping and viral tropism.” Curr Opin HIV AIDS
7. Clements JE, Gama L, Graham DR, Mankowski JL, Zink MC (2011) 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 6(1):37–42
8. Clifford DB, Ances BM (2013) HIV-associated neurocognitive disorder. Lancet Infect Dis 13(11):976–986
9. Cook-Easterwood J, Middaugh LD, Griffin WC 3rd, Khan I, Tyor WR (2007) Highly active antiretroviral therapy of cognitive dysfunction and neuronal abnormalities in SCID mice with HIV encephalitis. Exp Neurol 205(2):506–512
10. Dash PK, Gorantla S, Gendelman HE, Knibbe J, Casale GP, Makarov E, Epstein AA, Gelbard HA, Boska MD, Poluektova LY (2011) Loss of neuronal integrity during progressive HIV-1 infection of humanized mice. J Neurosci 31(9):3148–3157
11. Dash PK, Gendelman HE, Roy U, Balkundi S, Alnouti Y, Mosley RL, Gelbard HA, McMillan J, Gorantla S, Poluektova LY (2012) Long-acting nanoformulated antiretroviral therapy elicits potent antiretroviral and neuroprotective responses in HIV-1-infected humanized mice. AIDS 26(17):2135–2144
12. Denton PW, Estes JD, Sun Z, Othieno FA, Wei BL, Wege AK, Powell DA, Payne D, Haase AT, Garcia JV (2008) Antiretroviral pre-exposure prophylaxis prevents vaginal transmission of HIV-1 in humanized BLT mice. PLoS Med 5(1):e16
13. Denton PW, Garcia JV (2011) Humanized mouse models of HIV infection. AIDS Rev 13(3):135–148
14. Denton PW, Krisko JF, Powell DA, Mathias M, Kwak YT, Martinez-Torres F, Zou W, Payne DA, Estes JD, Garcia JV (2010) Systemic administration of antiretrovirals prior to exposure prevents rectal and intravenous HIV-1 transmission in humanized BLT mice. PLoS One 5(1):e8829
15. Denton PW, Olesen R, Choudhary SK, Archin NM, Wahl A, Swanson MD, Chateau M, Nochi T, Krisko JF, Spagnuolo RA, Margolis DM, Garcia JV (2012) Generation of HIV latency in humanized BLT mice. J Virol 86(1):630–634
16. Denton PW, Long JM, Wietgrefe SW, Sykes C, Spagnuolo RA, Snyder OD, Perkey K, Archin NM, Choudhary SK, Yang K, Hudgens MG, Pastan I, Haase AT, Kashuba AD, Berger EA, Margolis DM, Garcia JV (2014) Targeted cytotoxic therapy kills persisting HIV infected cells during ART. PLoS Pathog 10(1):e1003872
17. Desplats P, Dumaop W, Smith D, Adame A, Everall I, Letendre S, Ellis R, Cherner M, Grant I, Masliah E (2013) Molecular and pathologic insights from latent HIV-1 infection in the human brain. Neurology 80(15):1415–1423
18. Gerson T, Makarov E, Senanayake TH, Gorantla S, Poluektova LY, Vinogradov SV (2014) Nano-NRTIs demonstrate low neurotoxicity and high antiviral activity against HIV infection in the brain. Nanomedicine 10(1):177–185
19. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330(6005):841–845
20. Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5(1):69–81
21. Gorantla S, Makarov E, Finke-Dwyer J, Castanedo A, Holguin A, Gebhart CL, Gendelman HE, Poluektova L (2010a) Links between progressive HIV-1 infection of humanized mice and viral neuropathogenesis. Am J Pathol 177(6):2938–2949
22. Gorantla S, Makarov E, Finke-Dwyer J, Gebhart CL, Domm W, Dewhurst S, Gendelman HE, Poluektova LY (2010b) CD8+ cell depletion accelerates HIV-1 immunopathology in humanized mice. J Immunol 184(12):7082–7091
23. Gorantla S, Gendelman HE, Poluektova LY (2012a) Can humanized mice reflect the complex pathobiology of HIV-associated neurocognitive disorders? J Neuroimmune Pharmacol 7(2):352–362
24. Gorantla S, Poluektova L, Gendelman HE (2012b) Rodent models for HIV-associated neurocognitive disorders. Trends Neurosci 35(3):197–208
25. Graham DR, Gama L, Queen SE, Li M, Brice AK, Kelly KM, Mankowski JL, Clements JE, Zink MC (2011) Initiation of HAART during acute simian immunodeficiency virus infection rapidly controls virus replication in the CNS by enhancing immune activity and preserving protective immune responses. J Neurovirol 17(1):120–130
26. Gras G, Kaul M (2010) Molecular mechanisms of neuroinvasion by monocytes-macrophages in HIV-1 infection. Retrovirology 7:30
27. Harbison C, Zhuang K, Gettie A, Blanchard J, Knight H, Didier P, Cheng-Mayer C, Westmoreland S (2014) Giant cell encephalitis and microglial infection with mucosally transmitted simian-human immunodeficiency virus SHIVSF162P3N in rhesus macaques. J Neurovirol 20(1):62–72
28. Honeycutt JB, Wahl A, Archin N, Choudhary S, Margolis D, Garcia JV (2013) HIV-1 infection, response to treatment and establishment of viral latency in a novel humanized T cell-only mouse (TOM) model. Retrovirology 10:121
29. Kapadia F, Cook JA, Cohen MH, Sohler N, Kovacs A, Greenblatt RM, Choudhary I, Vlahov D (2005) The relationship between non-injection drug use behaviors on progression to AIDS and death in a cohort of HIV seropositive women in the era of highly active antiretroviral therapy use. Addiction 100(7):990–1002
30. Kim EY, Veazey RS, Zahn R, McEvers KJ, Baumeister SH, Foster GJ, Rett MD, Newberg MH, Kuroda MJ, Rieber EP, Piatak M Jr, Lifson JD, Letvin NL, Wolinsky SM, Schmitz JE (2008) Contribution of CD8+ T cells to containment of viral replication and emergence of mutations in Mamu-A*01-restricted epitopes in Simian immunodeficiency virus-infected rhesus monkeys. J Virol 82(11):5631–5635
31. Koneru R, Olive MF, Tyor WR (2014) Combined antiretroviral therapy reduces brain viral load and pathological features of HIV encephalitis in a mouse model. J Neurovirol 20(1):9–17
32. Koyanagi Y, Tanaka Y, Tanaka R, Misawa N, Kawano Y, Tanaka T, Miyasaka M, Ito M, Ueyama Y, Yamamoto N (1997) High levels of viremia in hu-PBL-NOD-scid mice with HIV-1 infection. Leukemia 11(Suppl 3):109–112
33. Kranick S M and A Nath (2012) “Neurologic complications of HIV-1 infection and its treatment in the era of antiretroviral therapy.” Continuum (Minneap Minn) 18(6 Infectious Disease): 1319–1337
34. Langford D, Marquie-Beck J, de Almeida S, Lazzaretto D, Letendre S, Grant I, McCutchan JA, Masliah E, Ellis RJ (2006) Relationship of antiretroviral treatment to postmortem brain tissue viral load in human immunodeficiency virus-infected patients. J Neurovirol 12(2):100–107
35. Letendre SL, McCutchan JA, Childers ME, Woods SP, Lazzaretto D, Heaton RK, Grant I, Ellis RJ (2004) Enhancing antiretroviral therapy for human immunodeficiency virus cognitive disorders. Ann Neurol 56(3):416–423
36. Lim RW, Halpain S (2000) Regulated association of microtubule-associated protein 2 (MAP2) with Src and Grb2: evidence for MAP2 as a scaffolding protein. J Biol Chem 275(27):20578–20587
37. Marcondes MC, Burudi EM, Huitron-Resendiz S, Sanchez-Alavez M, Watry D, Zandonatti M, Henriksen SJ, Fox HS (2001) Highly activated CD8(+) T cells in the brain correlate with early central nervous system dysfunction in simian immunodeficiency virus infection. J Immunol 167(9):5429–5438
38. Masters MC, Ances BM (2014) Role of neuroimaging in HIV-associated neurocognitive disorders. Semin Neurol 34(1):89–102
39. Matsuda K, Brown CR, Foley B, Goeken R, Whitted S, Dang Q, Wu F, Plishka R, Buckler-White A, Hirsch VM (2013) Laser capture microdissection assessment of virus compartmentalization in the central nervous systems of macaques infected with neurovirulent simian immunodeficiency virus. J Virol 87(16):8896–8908
40. Maung R, Medders KE, Sejbuk NE, Desai MK, Russo R, Kaul M (2012) Genetic knockouts suggest a critical role for HIV co-receptors in models of HIV gp120-induced brain injury. J Neuroimmune Pharmacol 7(2):306–318
41. McPhail ME, Robertson KR (2011) Neurocognitive impact of antiretroviral treatment: thinking long-term. Curr HIV/AIDS Rep 8(4):249–256
42. Medders KE, Sejbuk NE, Maung R, Desai MK, Kaul M (2010) Activation of p38 MAPK is required in monocytic and neuronal cells for HIV glycoprotein 120-induced neurotoxicity. J Immunol 185(8):4883–4895
43. Melkus MW, Estes JD, Padgett-Thomas A, Gatlin J, Denton PW, Othieno FA, Wege AK, Haase AT, Garcia JV (2006) Humanized mice mount specific adaptive and innate immune responses to EBV and TSST-1. Nat Med 12(11):1316–22
44. Milush JM, Chen HL, Atteberry G, Sodora DL (2013) Early detection of simian immunodeficiency virus in the central nervous system following oral administration to rhesus macaques. Front Immunol 4:236
45. Miura Y, Misawa N, Kawano Y, Okada H, Inagaki Y, Yamamoto N, Ito M, Yagita H, Okumura K, Mizusawa H, Koyanagi Y (2003) Tumor necrosis factor-related apoptosis-inducing ligand induces neuronal death in a murine model of HIV central nervous system infection. Proc Natl Acad Sci U S A 100(5):2777–2782
46. Mosier DE, Gulizia RJ, Baird SM, Wilson DB, Spector DH, Spector SA (1991) Human immunodeficiency virus infection of human-PBL-SCID mice. Science 251(4995):791–794
47. Ousman SS, Kubes P (2012) Immune surveillance in the central nervous system. Nat Neurosci 15(8):1096–1101
48. Palmer BE, Neff CP, Lecureux J, Ehler A, Dsouza M, Remling-Mulder L, Korman AJ, Fontenot AP, Akkina R (2013) In vivo blockade of the PD-1 receptor suppresses HIV-1 viral loads and improves CD4+ T cell levels in humanized mice. J Immunol 190(1):211–219
49. Parolin C, Borsetti A, Choe H, Farzan M, Kolchinsky P, Heesen M, Ma Q, Gerard C, Palu G, Dorf ME, Springer T, Sodroski J (1998) Use of murine CXCR-4 as a second receptor by some T-cell-tropic human immunodeficiency viruses. J Virol 72(2):1652–1656
50. Patel K, Ming X, Williams PL, Robertson KR, Oleske JM, Seage GR 3rd (2009) Impact of HAART and CNS-penetrating antiretroviral regimens on HIV encephalopathy among perinatally infected children and adolescents. AIDS 23(14):1893–1901
51. Persidsky Y, Limoges J, McComb R, Bock P, Baldwin T, Tyor W, Patil A, Nottet HS, Epstein L, Gelbard H, Flanagan E, Reinhard J, Pirruccello SJ, Gendelman HE (1996) Human immunodeficiency virus encephalitis in SCID mice. Am J Pathol 149(3):1027–1053
52. Persidsky Y, Buttini M, Limoges J, Bock P, Gendelman HE (1997) An analysis of HIV-1-associated inflammatory products in brain tissue of humans and SCID mice with HIV-1 encephalitis. J Neurovirol 3(6):401–416
53. Persidsky Y, Ghorpade A, Rasmussen J, Limoges J, Liu XJ, Stins M, Fiala M, Way D, Kim KS, Witte MH, Weinand M, Carhart L, Gendelman HE (1999) Microglial and astrocyte chemokines regulate monocyte migration through the blood–brain barrier in human immunodeficiency virus-1 encephalitis. Am J Pathol 155(5):1599–1611
54. Pistell PJ, Gupta S, Knight AG, Domingue M, Uranga RM, Ingram DK, Kheterpal I, Ruiz C, Keller JN, Bruce-Keller AJ (2010) Metabolic and neurologic consequences of chronic lopinavir/ritonavir administration to C57BL/6 mice. Antiviral Res 88(3):334–342
55. Poluektova LY, Munn DH, Persidsky Y, Gendelman HE (2002) Generation of cytotoxic T cells against virus-infected human brain macrophages in a murine model of HIV-1 encephalitis. J Immunol 168(8):3941–3949
56. Poluektova L, Gorantla S, Faraci J, Birusingh K, Dou H, Gendelman HE (2004) Neuroregulatory events follow adaptive immune-mediated elimination of HIV-1-infected macrophages: studies in a murine model of viral encephalitis. J Immunol 172(12):7610–7617
57. Rao VR, Sas AR, Eugenin EA, Siddappa NB, Bimonte-Nelson H, Berman JW, Ranga U, Tyor WR, Prasad VR (2008) HIV-1 clade-specific differences in the induction of neuropathogenesis. J Neurosci 28(40):10010–10016
58. Romao PR, Lemos JC, Moreira J, de Chaves G, Moretti M, Castro AA, Andrade VM, Boeck CR, Quevedo J, Gavioli EC (2011) Anti-HIV drugs nevirapine and efavirenz affect anxiety-related behavior and cognitive performance in mice. Neurotox Res 19(1):73–80
59. Salgado M, Swanson MD, Pohlmeyer CW, Buckheit RW 3rd, Wu J, Archin NM, Williams TM, Margolis DM, Siliciano RF, Garcia JV, Blankson JN (2014) HLA-B*57 elite suppressor and chronic progressor HIV-1 isolates replicate vigorously and cause CD4+ T cell depletion in humanized BLT mice. J Virol 88(6):3340–3352
60. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336(6077):86–90
61. Siliciano RF, Greene WC (2011) HIV latency. Cold Spring Harb Perspect Med 1(1):a007096
62. Smurzynski M, Wu K, Letendre S, Robertson K, Bosch RJ, Clifford DB, Evans S, Collier AC, Taylor M, Ellis R (2011) Effects of central nervous system antiretroviral penetration on cognitive functioning in the ALLRT cohort. AIDS 25(3):357–365
63. Sopper S, Koutsilieri E, Scheller C, Czub S, Riederer P, ter Meulen V (2002) Macaque animal model for HIV-induced neurological disease. J Neural Transm 109(5–6):747–766
64. 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
65. 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
66. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367(6459):188–193
67. Tyor WR, Power C, Gendelman HE, Markham RB (1993) A model of human immunodeficiency virus encephalitis in scid mice. Proc Natl Acad Sci U S A 90(18):8658–8662
68. Veazey RS, Acierno PM, McEvers KJ, Baumeister SH, Foster GJ, Rett MD, Newberg MH, Kuroda MJ, Williams K, Kim EY, Wolinsky SM, Rieber EP, Piatak M Jr, Lifson JD, Montefiori DC, Brown CR, Hirsch VM, Schmitz JE (2008) Increased loss of CCR5+ CD45RA- CD4+ T cells in CD8+ lymphocyte-depleted Simian immunodeficiency virus-infected rhesus monkeys. J Virol 82(11):5618–5630
69. von Herrath M, Oldstone MB, Fox HS (1995) Simian immunodeficiency virus (SIV)-specific CTL in cerebrospinal fluid and brains of SIV-infected rhesus macaques. J Immunol 154(10):5582–5589
70. Wahl A, Swanson MD, Nochi T, Olesen R, Denton PW, Chateau M, Garcia JV (2012) Human breast milk and antiretrovirals dramatically reduce oral HIV-1 transmission in BLT humanized mice. PLoS Pathog 8(6):e1002732
71. Watkins RL, Zou W, Denton PW, Krisko JF, Foster JL, Garcia JV (2013) In vivo analysis of highly conserved Nef activities in HIV-1 replication and pathogenesis. Retrovirology 10:125
72. Wiley CA, Baldwin M, Achim CL (1996) Expression of HIV regulatory and structural mRNA in the central nervous system. AIDS 10(8):843–847
73. Wiley CA, Soontornniyomkij V, Radhakrishnan L, Masliah E, Mellors J, Hermann SA, Dailey P, Achim CL (1998) Distribution of brain HIV load in AIDS. Brain Pathol 8(2):277–284