Longitudinal in vivo positron emission tomography imaging of infected and activated brain macrophages in a macaque model of human immunodeficiency virus encephalitis correlates with central and peripheral markers of encephalitis and areas of synaptic degeneration

American Journal of Pathology

Volumn 172, Issue 6, 2008, Pages 1603-1616

  Venneti, Sriram ^a   Bonneh Barkay, Dafna ^a   Lopresti, Brian J ^a   Bissel, Stephanie J ^a   Wang, Guoji ^a   Mathis, Chester A ^a   Piatak Jr , Michael ^b   Lifson, Jeffrey D ^b   Nyaundi, Julia O ^a   Murphey Corb, Michael ^a   Wiley, Clayton A ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 11; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; RADIOLIGAND; VIRUS DNA; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTORADIOGRAPHY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MACACA; MACROPHAGE ACTIVATION; MALE; NERVE DEGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; SYNAPSE; VIRUS ENCEPHALITIS;

EID: 44849116945     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.070967     Document Type: Article

References (55)

1. McArthur JC: NeuroAIDS: diagnosis and management. Hosp Pract 1997, 32:73-84
2. Dore GJ, Correll PK, Li Y, Kaldor JM, Cooper DA, Brew BJ: Changes to AIDS dementia complex in the era of highly active antiretroviral therapy. AIDS 1999, 13:1249-1253
3. Brew BJ: AIDS dementia complex. Neurol Clin 1999, 17:861-881
4. Baskin GB, Murphey-Corb M, Roberts ED, Didier PJ, Martin LN: Correlates of SIV encephalitis in rhesus monkeys. J Med Primatol 1992, 21:59-63
5. Budka H: Neuropathology of human immunodeficiency virus infection. Brain Pathol 1991, 1:163-175
6. Lackner AA, Smith MO, Munn RJ, Martfeld DJ, Gardner MB, Marx PA, Dandekar S: Localization of simian immunodeficiency virus in the central nervous system of rhesus monkeys. Am J Pathol 1991, 139:609-621
7. Wang TH, Donaldson YK, Brettle RP, Bell JE, Simmonds P: Identification of shared populations of human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system. J Virol 2001, 75:11686-11699
8. Mankowski JL, Flaherty MT, Spelman JP, Hauer DA, Didier PJ, Amedee AM, Murphey-Corb M, Kirstein LM, Munoz A, Clements JE, Zink MC: Pathogenesis of simian immunodeficiency virus encephalitis: viral determinants of neurovirulence. J Virol 1997, 71:6055-6060
9. Reddy RT, Achim CL, Sirko DA, Tehranchi S, Kraus FG, Wong-Staal F, Wiley CA: Sequence analysis of the V3 loop in brain and spleen of patients with HIV encephalitis. AIDS Res Hum Retroviruses 1996, 12:477-482
10. Gorry PR, Bristol G, Zack JA, Ritola K, Swanstrom R, Birch CJ, Bell JE, Bannert N, Crawford K, Wang H, Schols D, De Clercq E, Kunstman K, Wolinsky SM, Gabuzda D: Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J Virol 2001, 75:10073-10089
11. Bouwman FH, Skolasky RL, Hes D, Selnes OA, Glass JD, Nance-Sproson TE, Royal W, Dal Pan GJ, McArthur JC: Variable progression of HIV-associated dementia. Neurology 1998, 50:1814-1820
12. Adamson DC, McArthur JC, Dawson TM, Dawson VL: Rate and severity of HIV-associated dementia (HAD): correlations with Gp41 and iNOS. Mol Med 1999, 5:98-109
13. Westmoreland SV, Halpern E, Lackner AA: Simian immunodeficiency virus encephalitis in rhesus macaques is associated with rapid disease progression. J Neurovirol 1998, 4:260-268
14. O'Neil SP, Suwyn C, Anderson DC, Niedziela G, Bradley J, Novembre FJ, Herndon JG, McClure HM: Correlation of acute humoral response with brain virus burden and survival time in pig-tailed macaques infected with the neurovirulent simian immunodeficiency virus SIVsmmFGb. Am J Pathol 2004, 164:1157-1172
15. Gray F, Chretien F, Vallat-Decouvelaere AV, Scaravilli F: The changing pattern of HIV neuropathology in the HAART era. J Neuropathol Exp Neurol 2003, 62:429-440
16. Cysique LA, Maruff P, Brew BJ: Variable benefit in neuropsychological function in HIV-infected HAART-treated patients. Neurology 2006, 66:1447-1450
17. Banati RB: Visualising microglial activation in vivo. Glia 2002, 40:206-217
18. Venneti S, Lopresti BJ, Wang G, Bissel SJ, Mathis CA, Meltzer CC, Boada F, Capuano S III, Kress GJ, Davis DK, Ruszkiewicz J, Reynolds IJ, Murphey-Corb M, Trichel AM, Wisniewski SR, Wiley CA: PET imaging of brain macrophages using the peripheral benzodiazepine receptor in a macaque model of neuroAIDS. J Clin Invest 2004, 113:981-989
19. + T-cell-depleted macaques that develop lentiviral encephalitis. Am J Pathol 2006, 168:1553-1569
20. Bergamini A, Faggioli E, Bolacchi F, Gessani S, Cappannoli L, Uccella I, Demin F, Capozzi M, Cicconi R, Placido R, Vendetti S, Colizzi GM, Rocchi G: Enhanced production of tumor necrosis factor-alpha and interleukin-6 due to prolonged response to lipopolysaccharide in human macrophages infected in vitro with human immunodeficiency virus type 1. J Infect Dis 1999, 179:832-842
21. Barami K, Grever WE, Diaz FG, Lyman WD: An efficient method for the culturing and generation of neurons and astrocytes from second trimester human central nervous system tissue. Neurol Res 2001, 23:321-326
22. Padmanabhan J, Clayton D, Shelanski ML: Dibutyryl cyclic AMP-induced process formation in astrocytes is associated with a decrease in tyrosine phosphorylation of focal adhesion kinase and paxillin. J Neurobiol 1999, 39:407-422
23. Shah F, Hume SP, Pike VW, Ashworth S, McDermott J: Synthesis of the enantiomers of [N-methyl-11C]PK 11195 and comparison of their behaviours as radioligands for PK binding sites in rats. Nucl Med Biol 1994, 21:573-581
24. Woods RP, Cherry SR, Mazziotta JC: Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 1992, 16:620-633
25. Cline AN, Bess JW, Piatak M Jr, Lifson JD: Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 2005, 34:303-312
26. Mummidi S, Bamshad M, Ahuja SS, Gonzalez E, Feuillet PM, Begum K, Galvis MC, Kostecki V, Valente AJ, Murthy KK, Haro L, Dolan MJ, Allan JS, Ahuja SK: Evolution of human and non-human primate CC chemokine receptor 5 gene and mRNA. Potential roles for haplotype and mRNA diversity, differential haplotype-specific transcriptional activity, and altered transcription factor binding to polymorphic nucleotides in the pathogenesis of HIV-1 and simian immunodeficiency virus. J Biol Chem 2000, 275:18946-18961
27. Bissel SJ, Wang G, Ghosh M, Reinhart TA, Capuano S III, Stefano Cole K, Murphey-Corb M, Piatak M Jr, Lifson JD, Wiley CA: Macrophages relate presynaptic and postsynaptic damage in simian immunodeficiency virus encephalitis. Am J Pathol 2002, 160:927-941
28. Seman AL, Pewen WF, Fresh LF, Martin LN, Murphey-Corb M: The replicative capacity of rhesus macaque peripheral blood mononuclear cells for simian immunodeficiency virus in vitro is predictive of the rate of progression to AIDS in vivo. J Gen Virol 2000, 81:2441-2449
29. Bissel SJ, Wang G, Trichel AM, Murphey-Corb M, Wiley CA: Longitudinal analysis of activation markers on monocyte subsets during the development of simian immunodeficiency virus encephalitis. J Neuroimmunol 2006, 177:85-98
30. Banati RB, Newcombe J, Gunn RN, Cagnin A, Turkheimer F, Heppner F, Price G, Wegner F, Giovannoni G, Miller DH, Perkin GD, Smith T, Hewson AK, Bydder G, Kreutzberg GW, Jones T, Cuzner ML, Myers R: The peripheral benzodiazepine binding site in the brain in multiple sclerosis: quantitative in vivo imaging of microglia as a measure of disease activity. Brain 2000, 123:2321-2337
31. Masliah E, Achim CL, Ge N, DeTeresa R, Terry RD, Wiley CA: Spectrum of human immunodeficiency virus-associated neocortical damage. Ann Neurol 1992, 32:321-329
32. Mankowski JL, Queen SE, Tarwater PJ, Adams RJ, Guilarte TR: Elevated peripheral benzodiazepine receptor expression in simian immunodeficiency virus encephalitis. J Neurovirol 2003, 9:94-100
33. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH: Isolation of the mitochondrial benzodiazepine receptor: association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci USA 1992, 89:3170-3174
34. Everett H, Barry M, Sun X, Lee SF, Frantz C, Berthiaume LG, McFadden G, Bleackley RC: The myxoma poxvirus protein. M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. J Exp Med 2002, 196:1127-1139
35. Johnston C, Jiang W, Chu T, Levine B: Identification of genes involved in the host response to neurovirulent alphavirus infection. J Virol 2001, 75:10431-10445
36. Aquaro S, Bagnarelli P, Guenci T, De Luca A, Clementi M, Balestra E, Calio R, Perno CF: Long-term survival and virus production in human primary macrophages infected by human immunodeficiency virus. J Med Virol 2002, 68:479-488
37. Brew BJ, Rosenblum M, Cronin K, Price RW: AIDS dementia complex and HIV-1 brain infection: clinical-virological correlations. Ann Neurol 1995, 38:563-570
38. Moore DJ, Masliah E, Rippeth JD, Gonzalez R, Carey CL, Cherner M, Ellis RJ, Achim CL, Marcotte TD, Heaton RK, Grant I: Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS 2006, 20:879-887
39. Zink MC, Suryanarayana K, Mankowski JL, Shen A, Piatak M Jr, Spelman JP, Carter DL, Adams RJ, Lifson JD, Clements JE: High viral load in the cerebrospinal fluid and brain correlates with severity of simian immunodeficiency virus encephalitis. J Virol 1999, 73:10480-10488
40. McArthur JC, McClernon DR, Cronin MF, Nance-Sproson TE, Saah AJ, St Clair M, Lanier ER: Relationship between human immunodeficiency virus-associated dementia and viral load in cerebrospinal fluid and brain. Ann Neurol 1997, 42:689-698
41. Cinque P, Vago L, Ceresa D, Mainini F, Terreni MR, Vagani A, Torri W, Bossolasco S, Lazzarin A: Cerebrospinal fluid HIV-1 RNA levels: correlation with HIV encephalitis. AIDS 1998, 12:389-394
42. Hammoud DA, Endres CJ, Chander AR, Guilarte TR, Wong DF, Sacktor NC, McArthur JC, Pomper MG: Imaging glial cell activation with [11C]-R-PK11195 in patients with AIDS. J Neurovirol 2005, 11:346-355
43. Wiley CA, Lopresti BJ, Becker JT, Boada F, Lopez OL, Mellors J, Meltzer CC, Wisniewski SR, Mathis CA: Positron emission tomography imaging of peripheral benzodiazepine receptor binding in human immunodeficiency virus-infected subjects with and without cognitive impairment. J Neurovirol 2006, 12:262-271
44. Clinical confirmation of the American Academy of Neurology algorithm for HIV-1-associated cognitive/motor disorder. The Dana Consortium on Therapy for HIV Dementia and Related Cognitive Disorders. Neurology 1996, 47:1247-1253
45. Langford TD, Letendre SL, Larrea GJ, Masliah E: Changing patterns in the neuropathogenesis of HIV during the HAART era. Brain Pathol 2003, 13:195-210
46. McArthur JC, McDermott MP, McClernon D, St Hillaire C, Conant K, Marder K, Schifitto G, Selnes OA, Sacktor N, Stern Y, Albert SM, Kieburtz K, deMarcaida JA, Cohen B, Epstein LG: Attenuated central nervous system infection in advanced HIV/AIDS with combination antiretroviral therapy. Arch Neurol 2004, 61:1687-1696
47. Valcour VG, Shikuma CM, Watters MR, Sacktor NC: Cognitive impairment in older HIV-1-seropositive individuals: prevalence and potential mechanisms. AIDS 2004, 18(Suppl 1):S79-S86
48. Geraci AP, Simpson DM: Neurological manifestations of HIV-1 infection in the HAART era. Compr Ther 2001, 27:232-241
49. Ellis R, Langford D, Masliah E: HIV and antiretroviral therapy in the brain: neuronal injury and repair. Nat Rev Neurosci 2007, 8:33-44
50. Damle NK, Doyle LV: Ability of human T lymphocytes to adhere to vascular endothelial cells and to augment endothelial permeability to macromolecules is linked to their state of post-thymic maturation. J Immunol 1990, 144:1233-1240
51. + memory T cells by human immunodeficiency virus type 1: evidence for a role in the selective T-cell functional defects observed in infected individuals. Proc Natl Acad Sci USA 1990, 87:6058-6062
52. Fauci AS, Mavilio D, Kottilil S: NK cells in HIV infection: paradigm for protection or targets for ambush. Nat Rev Immunol 2005, 5:835-843
53. Mavilio D, Lombardo G, Benjamin J, Kim D, Follman D, Marcenaro E, O'Shea MA, Kinter A, Kovacs C, Moretta A, Fauci AS: Characterization of CD56-/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc Natl Acad Sci USA 2005, 102:2886-2891
54. Shieh TM, Carter DL, Blosser RL, Mankowski JL, Zink MC, Clements JE: Functional analyses of natural killer cells in macaques infected with neurovirulent simian immunodeficiency virus. J Neurovirol 2001, 7:11-24
55. Wachtman LM, Tarwater PM, Queen SE, Adams RJ, Mankowski JL: Platelet decline: an early predictive hematological marker of simian immunodeficiency virus central nervous system disease. J Neurovirol 2006, 12:25-33