Role of the immune system in HIV-associated neuroinflammation and neurocognitive implications

Brain, Behavior, and Immunity

Volumn 45, Issue , 2015, Pages 1-12

  Hong, Suzi ^a   Banks, William A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Blood brain barrier; Cognition; HIV; Inflammation; Microglia; NeuroAIDS; Neuroinflammation; Virus

Indexed keywords

EXCITATORY AMINO ACID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR NECROSIS FACTOR; VIRUS PROTEIN; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CYTOKINE;

ANTIVIRAL THERAPY; ASTROCYTE; BEHAVIOR CHANGE; BLOOD BRAIN BARRIER; CAPILLARY ENDOTHELIAL CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; COGNITION; COGNITIVE DEFECT; CYTOKINE RELEASE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE COURSE; EXECUTIVE FUNCTION; HIV ASSOCIATED DEMENTIA; HIV ASSOCIATED NEUROINFLAMMATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; INNATE IMMUNITY; LEUKOCYTE MIGRATION; MICROGLIA; MIXED INFECTION; MONOCYTE; MOOD DISORDER; MOUSE; NERVE CONDUCTION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYMPTOMATOLOGY; T LYMPHOCYTE; VIRAL TROPISM; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS LOAD; VIRUS PATHOGENESIS; VIRUS REPLICATION; AGE; AIDS DEMENTIA COMPLEX; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOLOGY; INFLAMMATION; METABOLISM; PSYCHOLOGY;

AGE FACTORS; AIDS DEMENTIA COMPLEX; ANTI-HIV AGENTS; ASTROCYTES; BLOOD-BRAIN BARRIER; COINFECTION; CYTOKINES; CYTOMEGALOVIRUS INFECTIONS; HIV; HIV INFECTIONS; HUMANS; INFLAMMATION; MICROGLIA; MONOCYTES; T-LYMPHOCYTES; VIRAL LOAD;

EID: 84924048096     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.10.008     Document Type: Review

References (170)

1. Alonso K., Pontiggia P., Medenica R., Rizzo R. Cytokine patterns in adults with AIDS. Immunol. Invest. 1997, 26:341-350.
2. Ances B.M., Ellis R.J. Dementia and neurocognitive disorders due to HIV-1 infection. Semin. Neurol. 2007, 27:86-92.
3. Ancuta P., Kamat A., Kunstman K.J., Kim E.Y., Autissier P., Wurcel A., Zaman T., Stone D., Mefford M., Morgello S., Singer E.J., Wolinsky S.M., Gabuzda D. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS ONE 2008, 3:e2516.
4. Andras I.E., Toborek M. Amyloid beta accumulation in HIV-1-infected brain: the role of the blood brain barrier. IUBMB Life 2013, 65:43-49.
5. Anthony I.C., Bell J.E. The neuropathology of HIV/AIDS. Int. Rev. Psychiatry 2008, 20:15-24.
6. Antinori A., Arendt G., Becker J.T., Brew B.J., Byrd D.A., Cherner M., et al. Updated research nosology for HIV-associated neurocognitive disorders. Neurology 2007, 69(18):1789-1799.
7. Antonelli L.R., Mahnke Y., Hodge J.N., Porter B.O., Barber D.L., DerSimonian R., Greenwald J.H., Roby G., Mican J., Sher A., Roederer M., Sereti I. Elevated frequencies of highly activated CD4+ T cells in HIV+ patients developing immune reconstitution inflammatory syndrome. Blood 2010, 116:3818-3827.
8. Appay V., Fastenackels S., Katlama C., Ait-Mohand H., Schneider L., Guihot A., Keller M., Grubeck-Loebenstein B., Simon A., Lambotte O., Hunt P.W., Deeks S.G., Costagliola D., Autran B., Sauce D. Old age and anti-cytomegalovirus immunity are associated with altered T-cell reconstitution in HIV-1-infected patients. AIDS 2011, 25(15):1813-1822.
9. Aubert R.D., Kamphorst A.O., Sarkar S., Vezys V., Ha S.J., et al. Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:21182-21187.
10. Bagasra O., Lavi E., Bobroski L., Khalili K., Pestaner J.P., Tawadros R., Pomerantz R.J. Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: identification by the combination of in situ polymerase chain reaction and immunohistochemistry. AIDS 1996, 10:573-585.
11. Balashov K.E., Rottman J.B., Weiner H.L., Hancock W.W. CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(12):6873-6878.
12. Banks W.A., Broadwell R.D. Blood to brain and brain to blood passage of native horseradish peroxidase, wheat germ agglutinin and albumin: pharmacokinetic and morphological assessments. J. Neurochem. 1994, 62:2404-2419.
13. Banks W.A., Freed E.O., Wolf K.M., Robinson S.M., Franko M., Kumar V.B. Transport of human immunodeficiency virus type 1 pseudoviruses across the blood-brain barrier: role of envelope proteins and adsorptive endocytosis. J. Virol. 2001, 75:4681-4691.
14. Banks W.A., Kastin A.J., Brennan J.M., Vallance K.L. Adsorptive endocytosis of HIV-1 gp120 by blood-brain barrier is enhanced by lipopolysaccharide. Exp. Neurol. 1999, 156:165-171.
15. Barrett L., Walmsley S. CMV retinopathy in the antiretroviral therapy era: prevention, diagnosis, and management. Curr. Infect. Dis. Rep. 2012, 14:435-444.
16. Barre-Sinoussi F., Chermann J.C., Rey F., Nugeyre M.T., Chamaret S., Gruest J., Dauguet C., xler-Blin C., Vezinet-Brun F., Rouzioux C., Rozenbaum W., Montagnier L. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 1983, 220:868-871.
17. Baruch K., Schwartz M. CNS-specific T cells shape brain function via the choroid plexus. Brain Behav. Immun. 2013, 34:11-16.
18. Begley D.J. ABC transporters and the blood-brain barrier. Curr. Pharm. Des. 2004, 10:1295-1312.
19. Bezzi P., Domercq M., Brambilla L., Galli R., Schols D., De Clercq E., Vescovi A., Bagetta G., Kollias G., Meldolesi J., Volterra A. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 2001, 4:702-710.
20. ++ monocytes are a major source of TNF. J. Immunol. 2002, 168:3536-3542.
21. Bobardt M.D., Salmon P., Wang L., Esko J.D., Gabuzda D., Fiala M., Trono D., Van der Schueren B., David G., Gallay P.A. Contribution of proteoglycans to human immunodeficiency virus type 1 brain invasion. J. Virol. 2004, 78:6567-6584.
22. Brabers N.A., Nottet H.S. Role of the pro-inflammatory cytokines TNF-alpha and IL-1beta in HIV-associated dementia. Eur. J. Clin. Invest. 2006, 36:447-458.
23. Brenchley J.M., Price D.A., Schacker T.W., Asher T.E., Silvestri G., Rao S., Kazzaz Z., Bornstein E., Lambotte O., Altmann D., Blazar B.R., Rodriguez B., Teixeira-Johnson L., Landay A., Martin J.N., Hecht F.M., Picker L.J., Lederman M.M., Deeks S.G., Douek D.C. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 2006, 12(12):1365-1371.
24. Buckner C.M., Calderon T.M., Willams D.W., Belbin T.J., Berman J.W. Characterization of monocyte maturation/differentiation that facilitates their transmigration across the blood-brain barrier and infection by HIV: implications for NeuroAIDS. Cell. Immunol. 2011, 267:109-123.
25. Budka H., Wiley C.A., Kleihues P., Artigas J., Asbury A.K., Cho E.S., Cornblath D.R., Dal Canto M.C., DeGirolami U., Dickson D. HIV-associated disease of the nervous system: review of nomenclature and proposal for neuropathology-based terminology. Brain Pathol. 1991, 1:143-152.
26. Burdo T.H., Weiffenbach A., Woods S., Letendre S., Ellis R.J., Williams K.C. Elevated sCD163 in plasma but not cerebrospinal fluid is a marker of neurocognitive impairment in HIV infection. AIDS. 2013, 27(9):1387-1395.
27. Cha L., Berry C.M., Nolan D., Castley A., Fernandez S., French M.A. Interferon-alpha, immune activation and immune dysfunction in treated HIV infection. Clin. Trans. Immunol. 2014, 2014. (ePub ahead of print).
28. Chang J.R., Mukerjee R., Bagashev A., Del Valle L., Chabrashvili T., Hawkins B.J., He J.J., Sawaya B.E. HIV-1 Tat protein promotes neuronal dysfunction through disruption of microRNAs. J. Biol. Chem. 2011, 286(47):41125-41134.
29. Chang L., Holt J.L., Yakupov R., Jiang C.S., Ernst T. Lower cognitive reserve in the aging human immunodeficiency virus-infected brain. Neurobiol. Aging 2008, 34(4):1240-1253.
30. Chaudhuri A., Yang B., Gendelman H.E., Persidsky Y., Kanmogne G.D. STAT1 signaling modulates HIV-1-induced inflammatory responses and leukocyte transmigration across the blood-brain barrier. Blood 2008, 111:2062-2072.
31. Cheeran M.C., Hu S., Yager S.L., Gekker G., Peterson P.K., Lokensgard J.R. Cytomegalovirus induces cytokine and chemokine production differentially in microglia and astrocytes: antiviral implications. J. Neurovirol. 2001, 7:135-147.
32. Chompre G., Cruz E., Maldonado L., Rivera-Amill V., Porter J.T., Noel R.J. Astrocytic expression of HIV-1 Nef impairs spatial and recognition memory. Neurobiol. Dis. 2013, 49:128-136.
33. Cioni C., Annunziata P. Circulating gp120 alters the blood-brain barrier permeability in HIV-1 gp120 transgenic mice. Neurosci. Lett. 2002, 330(3):299-301.
34. Clifford D.B., Ances B.M. HIV-associated neurocognitive disorder. Lancet Infect. Dis. 2013, 13:976-986.
35. Corral I., Quereda C., Moreno A., Perez-Elias M.J., Dronda F., Casado J.L., Muriel A., Masjuan J., onso-de-Lecinana M., Moreno S. Cerebrovascular ischemic events in HIV-1-infected patients receiving highly active antiretroviral therapy: incidence and risk factors. Cerebrovasc. Dis. 2009, 27:559-563.
36. Cusini A., Vernazza P.L., Yerly S., et al. Higher CNS penetration effectiveness of long-term combination antiretroviral therapy is associated with better HIV-1 viral suppression in cerebrospinal fluid. J. Acquir. Immune Defic. Syndr. 2013, 62:28-35.
37. Cysique L.A., Franklin D., Abramson I., Ellis R.J., Letendre S., Collier A., Clifford D., Gelman B., McArthur J., Morgello S., Simpson D., McCutchan J.A., Grant I., Heaton R.K. Normative data and validation of a regression based summary score for assessing meaningful neuropsychological change. J. Clin. Exp. Neuropsychol. 2011, 33(5):505-522. CHARTER Group, HNRC GroupHNRC Group.
38. Cysique L.A., Vaida F., Letendre S., Gibson S., Cherner M., Woods S.P., McCutchan J.A., Heaton R.K., Ellis R.J. Dynamics of cognitive change in impaired HIV-positive patients initiating antiretroviral therapy. Neurology 2009, 73:342-348.
39. Dahl V., Peterson J., Spudich S., Lee E., Shacklett B.L., Price R.W., Palmer S. Single-copy assay quantification of HIV-1 RNA in paired cerebrospinal fluid and plasma samples from elite controllers. AIDS 2013, 27(7):1145-1149.
40. Dimitrov S., Shaikh F., Pruitt C., Green M., Wilson K., Beg N., Hong S. Differential TNF production by monocyte subsets under physical stress: blunted mobilization of proinflammatory monocytes in prehypertensive individuals. Brain Behav. Immun. 2013, 27(1):101-108.
41. Dobbs M.R., Berger J.R. Stroke in HIV infection and AIDS. Expert Rev. Cardiovasc. Ther. 2009, 7:1263-1271.
42. Dohgu S., Banks W.A. Lipopolysaccharide-enhanced transcellular transport of HIV-1 across the blood-brain barrier is mediated by the p38 mitogen-activated protein kinase pathway. Exp. Neurol. 2008, 210:740-749.
43. Dohgu S., Banks W.A. Brain pericytes increase the lipopolysaccharide-enhanced transcytosis of HIV-1 free virus across the in vitro blood-brain barrier: evidence for cytokine-mediated pericyte-endothelial cell cross talk. Fluids Barriers CNS 2013, 10:23.
44. Dohgu S., Fleegal-DeMotta M.A., Banks W.A. Lipopolysaccharide-enhanced transcellular transport of HIV-1 across the blood-brain barrier is mediated by luminal microvessel IL-6 and GM-CSF. J. Neuroinflamm. 2011, 8:167.
45. Dohgu S., Ryerse J.S., Robinson S.M., Banks W.A. Human immunodeficiency virus-1 uses the mannos-6-phosphate receptor to cross the blood-brain barrier. PLoS ONE 2012, 7:e41623.
46. Eletto D., Russo G., Passiatore G., Del V.L., Giordano A., Khalili K., Gualco E., Peruzzi F. Inhibition of SNAP25 expression by HIV-1 Tat involves the activity of mir-128a. J. Cell. Physiol. 2008, 216:764-770.
47. Ellery P.J., Crowe S.M. Phenotypic characterization of blood monocytes from HIV-infected individuals. Methods Mol. Biol. 2005, 304:343-353.
48. Ellis R.J., Badiee J., Vaida F., Letendre S., Heaton R.K., et al. CD4 nadir is a predictor of HIV neurocognitive impairment in the era of combination antiretroviral therapy. AIDS 2011, 25:1747-1751.
49. Ellis R.J., Badiee J., Vaida F., Letendre S., Heaton R.K., Clifford D., Collier A.C., Gelman B., McArthur J., Morgello S., McCutchan J.A., Grant I. CD4 nadir is a predictor of HIV neurocognitive impairment in the era of combination antiretroviral therapy. AIDS 2011, 25:1747-1751.
50. Ellis R.J., Croteau D., Hong S. Nervous system infections. The Textbook of Geriatric Neurology 2014, Wiley & Sons Inc, Upper Saddle River, NJ. A.K. Nair, M. Sabbagh (Eds.).
51. Ellis R.J., Hsia K., Spector S.A., Nelson J.A., Heaton R.K., Wallace M.R., Abramson I., Atkinson J.H., Grant I., McCutchan J.A. Cerebrospinal fluid human immunodeficiency virus type 1 RNA levels are elevated in neurocognitively impaired individuals with acquired immunodeficiency syndrome. HIV neurobehavioral research center group. Ann. Neurol. 1997, 42:679-688.
52. Ellis R.J., Deutsch R., Heaton R.K., Marcotte T.D., McCutchan J.A., Nelson J.A., Abramson I., Thal L.J., Atkinson J.H., Wallace M.R., Grant I. Neurocognitive impairment is an independent risk factor for death in HIV infection. San Diego HIV neurobehavioral research center group. Arch. Neurol. 1997, 54:416-424.
53. Esiri M.M., Biddolph S.C., Morris C.S. Prevalence of Alzheimer plaques in AIDS. J. Neurol. Neurosurg. Psychiatry 1998, 65:29-33.
54. Everall I., Vaida F., Khanlou N., Lazzaretto D., Achim C., Letendre S., Moore D., Ellis R., Cherner M., Gelman B., Morgello S., Singer E., Grant I., Masliah E. Cliniconeuropathologic correlates of human immunodeficiency virus in the era of antiretroviral therapy. J. Neurovirol. 2009, 15:360-370.
55. Everall I., Luthert P., Lantos P. A review of neuronal damage in human immunodeficiency virus infection: its assessment, possible mechanism and relationship to dementia. J. Neuropathol. Exp. Neurol. 1993, 52:561-566.
56. Fauci A.S. 25 years of HIV. Nature 2008, 453:289-290.
57. Feuth T., Arends J.E., Fransen J.H., Nanlohy N.M., van Erpecum K.J., Siersema P.D., Hoepelman A.I., van B.D. Complementary role of HCV and HIV in T-cell activation and exhaustion in HIV/HCV coinfection. PLoS ONE 2013, 8:e59302.
58. Fiala M., Looney D.J., Stins M., Way D.D., Zhang L., Gan X., Chiappelli F., Schweitzer E.S., Shapshak P., Weinand M., Graves M.C., Witte M., Kim K.S. TNF-alpha opens a paracellular route for HIV-1 invasion across the blood-brain barrier. Mol. Med. 1997, 3:553-564.
59. Fischer-Smith T., Croul S., Sverstiuk A.E., Capini C., L'Heureux D., Regulier E.G., Richardson M.W., Amini S., Morgello S., Khalili K., Rappaport J. CNS invasion by CD14/CD16 peripheral blood derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J. Neurovirol. 2001, 7:528-541.
60. Garden G.A. Microglia in human immunodeficiency virus-associated neurodegeneration. Glia. 2002, 40(2):240-251.
61. Glass J.D., Fedor H., Wesselingh S.L., McArthur J.C. Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann. Neurol. 1995, 38(5):755-762.
62. Gray F., Lescure F.X., Adle-Biassette H., Polivka M., Gallien S., Pialoux G., Moulignier A. Encephalitis with infiltration by CD8+ lymphocytes in HIV patients receiving combination antiretroviral treatment. Brain Pathol. 2013, 23(5):525-533.
63. Guillemin G.J., Kerr S.J., Brew B.J. Involvement of quinolinic acid in AIDS dementia complex. Neurotox. Res. 2005, 7:103-123.
64. Giulian D., Vaca K., Noonan C.A. Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 1990, 250(4987):1593-1596.
65. Giunti D., Borsellino G., Benelli R., Marchese M., Capello E., Valle M.T., Pedemonte E., Noonan D., Albini A., Bernardi G., Mancardi G.L., Battistini L., Uccelli A. Phenotypic and functional analysis of T cells homing into the CSF of subjects with inflammatory diseases of the CNS. J. Leukoc. Biol. 2003, 73:584-590.
66. Grant I., Heaton R.K., Atkinson J.H., Wiley C.A., Kirson D., Velin R., Chandler J., McCutchan J.A. HIV-1 associated neurocognitive disorder. The HNRC group. Clin. Neuropharmacol. 1992, 15(Suppl. 1 Pt A):364A-365A.
67. Hambleton S. Chickenpox. Curr. Opin. Infect. Dis. 2005, 18:235-240.
68. Haraguchi S., Ho S.K., Morrow M., Goodenow M.M., Sleasman J.W. Developmental regulation of P-glycoprotein activity within thymocytes results in increased protease inhibitor activity. J. Leukoc. Biol. 2011, 90(4):653-660.
69. Hayashi K., Pu H., Andras I.E., Eum S.Y., Yamauchi A., Henning B., Toborek M. HIV-TAT protein upregulates expression of multidrug resistance protein 1 in the blood-brain barrier. J. Cereb. Blood Flow Metab. 2006, 26:1052-1065.
70. Heaton R.K., Clifford D.B., Franklin D.R., Woods S.P., Ake C., Vaida F., Ellis R.J., Letendre S.L., Marcotte T.D., Atkinson J.H., Rivera-Mindt M., Vigil O.R., Taylor M.J., Collier A.C., Marra C.M., Gelman B.B., McArthur J.C., Morgello S., Simpson D.M., McCutchan J.A., Abramson I., Gamst A., Fennema-Notestine C., Jernigan T.L., Wong J., Grant I. HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER study. Neurology 2010, 75:2087-2096.
71. Heaton R.K., Franklin D.R., Ellis R.J., McCutchan J.A., Letendre S.L., Leblanc S., Corkran S.H., Duarte N.A., Clifford D.B., Woods S.P., Collier A.C., Marra C.M., Morgello S., Mindt M.R., Taylor M.J., Marcotte T.D., Atkinson J.H., Wolfson T., Gelman B.B., McArthur J.C., Simpson D.M., Abramson I., Gamst A., Fennema-Notestine C., Jernigan T.L., Wong J., Grant I. 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.
72. Hoare J., Fouche J.P., Spottiswoode B., Joska J.A., Schoeman R., Stein D.J., Carey P.D. White matter correlates of apathy in HIV-positive subjects: a diffusion tensor imaging study. J. Neuropsychiatry Clin. Neurosci. 2010, 22:313-320.
73. Hong S., Schrier R.D., Kao Y., Vaida F., Cherner M., Crescini M., Ellis R., Letendre S. Does migration of immune cells into the CNS play a role in HIV-associated neurocognitive impairment during antiretroviral therapy?. Brain Behav. Immun. 2013, 32(Suppl. 1):e40-e41. (Meeting Abstract).
74. Hornik A., Rodriguez-Porcel F., Wallery S., Flaster M., Lee J.M., Biller J. Late onset CNS immune reconstitution inflammatory syndrome in an immunocompetent patient. Front. Neurol. 2013, 4:12.
75. Hsue P.Y., Lo J.C., Franklin A., Bolger A.F., Martin J.N., Deeks S.G., Waters D.D. Progression of atherosclerosis as assessed by carotid intima-media thickness in patients with HIV infection. Circulation 2004, 109:1603-1608.
76. Huang Y., Zhao L., Jia B., Wu L., Li Y., Curthoys N., Zheng J.C. Glutaminase dysregulation in HIV-1-infected human microglia mediates neurotoxicity: relevant to HIV-1-associated neurocognitive disorders. J. Neurosci. 2011, 31(42):15195-15204.
77. Heine G.H., Ortiz A., Massy Z.A., Lindholm B., Wiecek A., Martinez-Castelao A., Covic A., Goldsmith D., Suleymanlar G., London G.M., Parati G., Sicari R., Zoccali C., Fliser D. Monocyte subpopulations and cardiovascular risk in chronic kidney disease. Nat. Rev. Nephrol. 2012, 8(6):362-369.
78. Hong S., Mills P.J. Effects of an exercise challenge on mobilization and surface marker expression of monocyte subsets in individuals with normal vs. elevated blood pressure. Brain Behav. Immun. 2008, 22:590-599.
79. Hunt P.W. HIV and aging: emerging research issues. Curr. Opin. HIV AIDS 2014, 9(4):302-308.
80. Iskander S., Walsh K.A., Hammond R.R. Human CNS cultures exposed to HIV-1 gp120 reproduce dendritic injuries of HIV-1-associated dementia. J. Neuroinflamm. 2004, 1:7.
81. Jana A., Pahan K. Human immunodeficiency virus type 1 gp120 induces apoptosis in human primary neurons through redox-regulated activation of neutral sphingomyelinase. J. Neurosci. 2004, 24:9531-9540.
82. Joska J.A., Gouse H., Paul R.H., Stein D.J., Flisher A.J. Does highly active antiretroviral therapy improve neurocognitive function? a systematic review. J. Neurovirol. 2010, 16:101-114.
83. Karris M.A., Smith D.M. Tissue-specific HIV-1 infection: why it matters. Future Virol. 2011, 6(7):869-882.
84. Kaul M., Garden G.A., Lipton S.A. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature. 2001, 410(6831):988-994.
85. Kaul M. HIV-1 associated dementia: update on pathological mechanisms and therapeutic approaches. Curr. Opin. Neurol. 2009, 22:315-320.
86. Kamat A., Lyons J.L., Misra V., Uno H., Morgello S., Singer E.J., Gabuzda D. Monocyte activation markers in cerebrospinal fluid associated with impaired neurocognitive testing in advanced HIV infection. J. Acquir. Immune Defic. Syndr. 2012, 60(3):234-243.
87. Kanmogne G.D., Schall K., Leibhart J., Knipe B., Gendelman H.E., Persidsky Y. HIV-1 gp120 compromises blood-brain barrier integrity and enhances monocyte migration across blood-brain barrier: implication for viral neuropathogenesis. J. Cereb. Blood Flow Metab. 2007, 27(1):123-134.
88. Kereveur A., McIlroy D., Samri A., Oksenhendler E., Clauvel J.P., Autran B. Up-regulation of adhesion and MHC molecules on splenic monocyte/macrophages in adult hemophagocytic syndrome. Br. J. Haematol. 1999, 104:871-877.
89. Khanlou N., Moore D.J., Chana G., Cherner M., Lazzaretto D., Dawes S., Grant I., Masliah E., Everall I.P. Increased frequency of alpha-synuclein in the substantia nigra in human immunodeficiency virus infection. J. Neurovirol. 2009, 15:131-138.
90. Khoury M.N., Tan C.S., Peaslee M., Koralnik I.J. CSF viral escape in a patient with HIV-associated neurocognitive disorder. J. Neurovirol. 2013, 19(4):402-405.
91. Kim R.B., Fromm M.F., Wandel C., Leake B., Wood A.J.J., Roden D.M., Wilkinson G.R. The drug transporter p-glycoprotein limits oral absorption and brain entry of HIV-1 protease inhibitors. J. Clin. Invest. 1998, 101:289-294.
92. Kipnis J., Derecki N.C., Yang C., Scrable H. Immunity and cognition: what do age-related dementia, HIV-dementia and 'chemo-brain' have in common?. Trends Immunol. 2008, 29:455-463.
93. Kumar A.M., Borodowsky I., Fernandez B., Gonzalez L., Kumar M. Human immunodeficiency virus type 1 RNA Levels in different regions of human brain: quantification using real-time reverse transcriptase-polymerase chain reaction. J. Neurovirol. 2007, 13:210-224.
94. Laskus T., Radkowski M., Adair D.M., Wilkinson J., Scheck A.C., Rakela J. Emerging evidence of hepatitis C virus neuroinvasion. AIDS 2005, 19(Suppl. 3):S140-S144.
95. Lanoy E., Guiguet M., Bentata M., Rouveix E., Dhiver C., Poizot-Martin I., Costagliola D., Gasnault J. Survival after neuroAIDS: association with antiretroviral CNS Penetration-Effectiveness score. Neurology 2011, 76(7):644-651. FHDH-ANRS CO4.
96. Letendre S., Marquie-Beck J., Capparelli E., et al. Validation of the CNS Penetration-Effectiveness rank for quantifying antiretroviral penetration into the central nervous system. Arch. Neurol. 2008, 65(1):65-70.
97. Letendre S.L., Lanier E.R., McCutchan J.A. Cerebrospinal fluid beta chemokine concentrations in neurocognitively impaired individuals infected with human immunodeficiency virus type 1. J. Infect. Dis. 1999, 180:310-319.
98. Letendre S., Paulino A.D., Rockenstein E., Adame A., Crews L., Cherner M., Heaton R., Ellis R., Everall I.P., Grant I., Masliah E. Pathogenesis of hepatitis C virus coinfection in the brains of patients infected with HIV. J. Infect. Dis. 2007, 196:361-370.
99. Letendre S.L., Cherner M., Ellis R.J., Marquie-Beck J., Gragg B., Marcotte T., Heaton R.K., McCutchan J.A., Grant I. The effects of hepatitis C, HIV, and methamphetamine dependence on neuropsychological performance: biological correlates of disease. AIDS 2005, 19(Suppl. 3):S72-S78.
100. Letendre S.L., McCutchan J.A., Childers M.E., Woods S.P., Lazzaretto D., Heaton R.K., Grant I., Ellis R.J. Enhancing antiretroviral therapy for human immunodeficiency virus cognitive disorders. Ann. Neurol. 2004, 56:416-423.
101. Li J., Wang Y., Wang X., Ye L., Zhou Y., Persidsky Y., ho W. Immune activation of human brain microvascular endothelial cells inhibits HIV replication in macrophages. Blood 2013, 121:2934-2942.
102. Lipton S.A. Requirement for macrophages in neuronal injury induced by HIV envelope protein gp120. NeuroReport 1992, 3(10):913-915.
103. Lyons J.L., Uno H., Ancuta P., Kamat A., Moore D.J., Singer E.J., Morgello S., Gabuzda D. Plasma sCD14 is a biomarker associated with impaired neurocognitive test performance in attention and learning domains in HIV infection. J. Acquir. Immune Defic. Syndr. 2011, 57(5):371-379.
104. Marcotte T.D., Deutsch R., McCutchan J.A., Moore D.J., Letendre S., et al. Prediction of incident neurocognitive impairment by plasma HIV RNA and CD4 levels early after HIV seroconversion. Arch. Neurol. 2003, 60:1406-1412.
105. Marra C.M., Zhao Y., Clifford D.B., Letendre S., Evans S., Henry K., Ellis R.J., Rodriguez B., Coombs R.W., Schifitto G., McArthur J.C., Robertson K. Impact of combination antiretroviral therapy on cerebrospinal fluid HIV RNA and neurocognitive performance. AIDS 2009, 23(11):1359-1366. AIDS Clinical Trials Group 736 Study Team.
106. Marsh M. The entry of enveloped viruses into cells by endocytosis. Biochem. J. 1984, 218:1-10.
107. McCutchan J.A. Cytomegalovirus infections of the nervous system in patients with AIDS. Clin. Infect. Dis. 1995, 20(4):747-754.
108. McManus H., Li P.C., Nolan D., Bloch M., Kiertiburanakul S., Choi J.Y., Mulhall B., Petoumenos K., Zhou J., Law M., Brew B.J., Wright E. Does use of antiretroviral therapy regimens with high central nervous system penetration improve survival in HIV-infected adults?. HIV Med. 2011, 12(10):610-619.
109. Mehla R., Bivalkar-Mehla S., Nagarkatti M., Chauhan A. Programming of neurotoxic cofactor CXCL-10 in HIV-1-associated dementia: abrogation of CXCL-10-induced neuro-glial toxicity in vitro by PKC activator. J. Neuroinflamm. 2012, 9:239. 10.1186/1742-2094-9-239, 239.
110. Meucci O., Fatatis A., Simen A.A., Miller R.J. Expression of CX3CR1 chemokine receptors on neurons and their role in neuronal survival. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8075-8080.
111. Michael N.L., Moore J.P., Miller R.F., Isaacson P.G., Hall-Craggs M., Lucas S., Gray F., et al. Cerebral CD8+ lymphocytosis in HIV-1 infected patients with immune restoration induced by HAART. Acta. Neuropathol. 2004, 108:17-23.
112. Miller R.F., Isaacson P.G., Hall-Craggs M., Lucas S., Gray F., Scaravilli F., An S.F. Cerebral CD8+ lymphocytosis in HIV-1 infected patients with immune restoration induced by HAART. Acta. Neuropathol. 2004, 108(1):17-23.
113. Mukerjee R., Deshmane S.L., Fan S., Del V.L., White M.K., Khalili K., Amini S., Sawaya B.E. Involvement of the p53 and p73 transcription factors in neuroAIDS. Cell Cycle 2008, 7:2682-2690.
114. Muratori C., Mangino G., Affabris E., Federico M. Astrocytes contacting HIV-1-infected macrophages increase the release of CCL2 in response to the HIV-1-dependent enhancement of membrane-associated TNFalpha in macrophages. Glia 2010, 58:1893-1904.
115. Naeger D.M., Martin J.N., Sinclair E., Hunt P.W., Bangsberg D.R., Hecht F., Hsue P., McCune J.M., Deeks S.G. Cytomegalovirus-specific T cells persist at very high levels during long-term antiretroviral treatment of HIV disease. PLoS ONE 2010, 5:e8886.
116. Nakagawa S., Castro V., Toborek M. Infection of human pericytes by HIV-1 disrupts the integrity of the blood-brain barrier. J. Cell Mol. Med. 2012, 16:2950-2957.
117. Nath A., Schiess N., Venkatesan A., Rumbaugh J., Sacktor N., McArthur J. Evolution of HIV dementia with HIV infection. Int. Rev. Psychiatry 2008, 20:25-31.
118. Neuenburg J.K., Brodt H.R., Herndier B.G., Bickel M., Bacchetti P., Price R.W., Grant R.M., Schlote W. HIV-related neuropathology, 1985-1999: rising prevalence of HIV encephalopathy in the era of highly active antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 2002, 31:171-177.
119. Nottet H.S., Persidsky Y., Sasseville V.G., Nukuna A.N., Bock P., Zhai Q.H., Sharer L.R., McComb R.D., Swindells S., Soderland C., Gendelman H.E. Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J. Immunol. 1996, 156:1284-1295.
120. Nottet H.S. Interactions between macrophages and brain microvascular endothelial cells: role in pathogenesis of HIV-1 infection and blood-brain barrier function. J. Neurovirol. 1999, 5:659-669.
121. Ovbiagele B., Nath A. Increasing incidence of ischemic stroke in patients with HIV infection. Neurology 2011, 76:444-450.
122. Parrinello C.M., Landay A.L., Hodis H.N., Gange S.J., Norris P.J., Young M., Anastos K., Tien P.C., Xue X., Lazar J., Benning L., Tracy R.P., Kaplan R.C. Association of subclinical atherosclerosis with lipid levels amongst antiretroviral-treated and untreated HIV-infected women in the Women's Interagency HIV study. Atherosclerosis. 2012, 225(2):408-411.
123. Pawelec G., Derhovanessian E., Larbi A., Strindhall J., Wikby A. Cytomegalovirus and human immunosenescence. Rev. Med. Virol. 2009, 19(1):47-56.
124. Pereyra F., Palmer S., Miura T., Block B.L., Wiegand A., Rothchild A.C., Baker B., Rosenberg R., Cutrell E., Seaman M.S., Coffin J.M., Walker B.D. Persistent low-level viremia in HIV-1 elite controllers and relationship to immunologic parameters. J. Infect. Dis. 2009, 200(6):984-990.
125. Perrella O., Carreiri P.B., Perrella A., Sbreglia C., Gorga F., Guarnaccia D., Tarantino G. Transforming growth factor beta-1 and interferon-alpha in the AIDS dementia complex (ADC): possible relationship with cerebral viral load?. Eur. Cytokine Netw. 2001, 12(1):51-55.
126. Persidsky Y., Stins M., Way D., Witte M.H., Weinand M., Kim K.S., Bock P., Gendelman H.E., Fiala M. A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. J. Immunol. 1997, 158:3499-3510.
127. Persidsky Y., Ghorpade A., Rasmussen J., Limoges J., Liu X.J., Stins M., Fiala M., Way D., Kim K.S., Witte M.H., Weinand M., Carhart L., Gendelman H.E. Microglial and astrocyte chemokines regulate monocyte migration through the blood-brain barrier in human immunodeficiency virus-1 encephalitis. Am. J. Pathol. 1999, 155:1599-1611.
128. Popovic M., Sarngadharan M.G., Read E., Gallo R.C. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science 1984, 224:497-500.
129. Probasco J.C., Deeks S.G., Lee E., Hoh R., Hunt P.W., Liegler T., Price R.W., Spudich S.S. Cerebrospinal fluid in HIV-1 systemic viral controllers: absence of HIV-1 RNA and intrathecal inflammation. AIDS 2010, 24(7):1001-1005.
130. Pulliam L. Cognitive consequences of a sustained monocyte type 1 IFN response in HIV-1 infection. Curr. HIV Res. 2014, 12(2):77-84.
131. Pulliam L., Gascon R., Stubblebine M., McGuire D., McGrath M.S. Unique monocyte subset in patients with AIDS dementia. Lancet 1997, 349(9053):692-695.
132. Pulliam L., Sun B., Rempel H. Invasive chronic inflammatory monocyte phenotype in subjects with high HIV-1 viral load. J. Neuroimmunol. 2004, 157(1-2):93-98.
133. Rempel H., Sun B., Calosing C., Abadjian L., Monto A., Pulliam L. Monocyte activation in HIV/HCV coinfection correlates with cognitive impairment. PLoS ONE 2013, 8:e55776.
134. Resnick L., Berger J., Shapshak P., Tourtellotte W.W. Early penetration of the blood-brain-barrier by HIV. Neurology 1988, 38:9-14.
135. Rho M.B., Wesselingh S., Glass J.D., McArthur J.C., Choi S., Griffin J., Tyor W.R. A potential role for interferon-alpha in the pathogenesis of HIV-associated dementia. Brain Behav. Immun. 1995, 9(4):366-377.
136. Robertson K.R., Smurzynski M., Parsons T.D., Wu K., Bosch R.J., Wu J., McArthur J.C., Collier A.C., Evans S.R., Ellis R.J. The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 2007, 21:1915-1921.
137. Ronaldson P.T., Bendayan R. HIV-1 viral envelope glycoprotein gp120 triggers an inflammatory response in cultured rat astrocytes and regulates the functional expression of P-glycoprotein. Mol. Pharm. 2006, 70:1087-1098.
138. Rosca E.C., Rosca O., Simu M., Chirileanu R.D. HIV-associated neurocognitive disorders: a historical review. Neurologist 2012, 18:64-67.
139. Rosenberg E.S., Billingsley J.M., Caliendo A.M., Boswell S.L., Sax P.E., Kalams S.A., Walker B.D. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science. 1997, 278(5342):1447-1450.
140. Sandler N.G., Bosinger S.E., Estes J.D., Zhu R.T., Tharp G.K., Boritz E., Levin D., Wijeyesinghe S., Makamdop K.N., del Prete G.Q., Hill B.J., Timmer J.K., Reiss E., Yarden G., Darko S., Contijoch E., Todd J.P., Silvestri G., Nason M., Norgren R.B., Keele B.F., Rao S., Langer J.A., Lifson J.D., Schreiber G., Douek D.C. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 2014, 511(7511):601-605.
141. Sas A.R., Bimonte-Nelson H., Smothers C.T., Woodward J., Tyor W.R. Interferon-alpha causes neuronal dysfunction in encephalitis. J. Neurosci. 2009, 29(12):3948-3955.
142. Schrier, R., Hong, S., Crescini, M., Ellis R, Santiago, J.P., Letendre, S. for the HNRC Group. CD8+ T-cells that express interferon-γ contribute to HIV associated neurocogntive disorder (HAND). submitted for publication.
143. Schwartz M., Shechter R. Protective autoimmunity functions by intracranial immunosurveillance to support the mind: the missing link between health and disease. Mol. Psychiatry 2010, 15:342-354.
144. Schweighardt B., Atwood W.J. Virus receptors in the human central nervous system. J. Neurovirol. 2001, 7:187-195.
145. Seilhean D., Dzia-Lepfoundzou A., Sazdovitch V., Cannella B., Raine C.S., Katlama C., Bricaire F., Duyckaerts C., Hauw J.J. Astrocytic adhesion molecules are increased in HIV-1-associated cognitive/motor complex. Neuropathol. Appl. Neurobiol. 1997, 23:83-92.
146. Shacklett B.L., Cox C.A., Wilkens D.T., Karl K.R., Nilsson A., Nixon D.F., Price R.W. Increased adhesion molecule and chemokine receptor expression on CD8+ T cells trafficking to cerebrospinal fluid in HIV-1 infection. J. Infect. Dis. 2004, 189:2202-2212.
147. Shan L., Deng K., Shroff N.S., Durand C.M., Rabi S.A., et al. Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 2012, 36:491-501.
148. Simioni S., Cavassini M., Annoni J.M., Rimbault A.A., Bourquin I., Schiffer V., Calmy A., Chave J.P., Giacobini E., Hirschel B., Du Pasquier R.A. Cognitive dysfunction in HIV patients despite long-standing suppression of viremia. AIDS 2010, 24:1243-1250.
149. Smurzynski M., Wu K., Letendre S., Robertson K., Bosch R.J., Clifford D.B., Evans S., Collier A.C., Taylor M., Ellis R. Effects of central nervous system antiretroviral penetration on cognitive functioning in the ALLRT cohort. AIDS 2011, 25(3):357-365.
150. Tarter K.D., Simanek A.M., Dowd J.B., Aiello A.E. Persistent viral pathogens and cognitive impairment across the life course in the third national health and nutrition examination survey. J. Infect. Dis. 2013, 209(6):837-844.
151. Toggas S.M., Masliah E., Rockenstein E.M., Rall G.F., Abraham C.R., Mucke L. Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature. 1994, 367(6459):188-193.
152. Toneatto S., Finco O., van der Putten H., Abrignani S., Annunziata P. Evidence of blood-brain barrier alteration and activation in HIV-1 gp120 transgenic mice. AIDS 1999, 13:2343-2348.
153. Torres-Munoz J., Stockton P., Tacoronte N., Roberts B., Maronpot R.R., Petito C.K. Detection of HIV-1 gene sequences in hippocampal neurons isolated from postmortem AIDS brains by laser capture microdissection. J. Neuropathol. Exp. Neurol. 2001, 60:885-892.
154. Tozzi V., Balestra P., Salvatori M.F., Vlassi C., Liuzzi G., Giancola M.L., Giulianelli M., Narciso P., Antinori A. Changes in cognition during antiretroviral therapy: comparison of 2 different ranking systems to measure antiretroviral drug efficacy on HIV-associated neurocognitive disorders. J. Acquir. Immune Defic. Syndr. 2009, 52(1):56-63.
155. Udina M., Castellvi P., Moreno-Espana J., Navines R., Valdes M., Forns X., Langohr K., Sola R., Vieta E., Martin-Santos R. Interferon-induced depression in chronic hepatitis C: a systematic review and meta-analysis. J. Clin. Psychiatry 2012, 73:1128-1138.
156. Valcour V., Sithinamsuwan P., Letendre S., Ances B. Pathogenesis of HIV in the central nervous system. Curr. HIV/AIDS Rep. 2011, 8:54-61.
157. Valcour V.G., Shikuma C.M., Watters M.R., Sacktor N.C. Cognitive impairment in older HIV-1-seropositive individuals prevalence and potential mechanisms. AIDS 2004, 18(Suppl. 1):S79-S86.
158. van Marle G., Henry S., Todoruk T., Sullivan A., Silva C., Rourke S.B., Holden J., McArthur J.C., Gill M.J., Power C. Human immunodeficiency virus type 1 Nef protein mediates neural cell death: a neurotoxic role for IP-10. Virology. 2004, 329(2):302-318.
159. Venkataramana A., Pardo C.A., McArthur J.C., Kerr D.A., Irani D.N., Griffin J.W., Burger P., Reich D.S., Calabresi P.A., Nath A. Immune reconstitution inflammatory syndrome in the CNS of HIV-infected patients. Neurology 2006, 67:383-388.
160. Verma R., Anand K.S. HIV presenting as young-onset dementia. J. Int. Assoc. Provid. AIDS Care 2014, 13(2):110-112.
161. Walsh J.G., Reinke S.N., Mamik M.K., McKenzie B.A., Maingat F., Branton W.G., Broadhurst D.I., Power C.1. Rapid inflammasome activation in microglia contributes to brain disease in HIV/AIDS. Retrovirology 2014, 13(11):35.
162. Wendelken L.A., Valcour V. Impact of HIV and aging on neuropsychological function. J. Neurovirol. 2012, 18(4):256-263.
163. Wesselingh S.L., Takahashi K., Glass J.D., McArthur J.C., Griffin J.W., Griffin D.E. Cellular localization of tumor necrosis factor mRNA in neurological tissue from HIV-infected patients by combined reverse transcriptase/polymerase chain reaction in situ hybridization and immunohistochemistry. J. Neuroimmunol. 1997, 74:1-8.
164. Weber C., Belge K.U., von Hundelshausen P., Draude G., Steppich B., Mack M., Frankenberger M., Weber K.S., Ziegler-Heitbrock H.W. Differential chemokine receptor expression and function in human monocyte subpopulations. J. Leukoc. Biol. 2000, 67(5):699-704.
165. Westhorpe C.L., Zhou J., Webster N.L., Kalionis B., Lewin S.R., Jaworowski A., Muller W.A., Crowe S.M. Effects of HIV-1 infection in vitro on transendothelial migration by monocytes and monocyte-derived macrophages. J. Leukoc. Biol. 2009, 85(6):1027-1035.
166. Wiley C.A., Achim C.L., Christopherson C., Kidane Y., Kwok S., Masliah E., Mellors J., Radhakrishnan L., Wang G., Soontornniyomkij V. HIV mediates a productive infection of the brain. AIDS 1999, 13:2055-2059.
167. Williams R., Dhillon N.K., Hegde S.T., Yao H., Peng F., Callen S., Chebloune Y., Davis R.L., Buch S.J. Proinflammatory cytokines and HIV-1 synergistically enhance CXCL10 expression in human astrocytes. Glia 2009, 57:734-743.
168. Williams D.W., Eugenin E.A., Calderon T.M., Berman J.W. Monocyte maturation, HIV susceptibility, and transmigration across the blood brain barrier are critical in HIV neuropathogenesis. J. Leukoc. Biol. 2012, 91(3):401-415.
169. Ziegler-Heitbrock L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 2007, 81:584-592.
170. Ziegler-Heitbrock L., Ancuta P., Crowe S., Dalod M., Grau V., Hart D.N., Leenen P.J., Liu Y.J., MacPherson G., Randolph G.J., Scherberich J., Schmitz J., Shortman K., Sozzani S., Strobl H., Zembala M., Austyn J.M., Lutz M.B. Nomenclature of monocytes and dendritic cells in blood. Blood 2010, 116:e74-e80.