HIV-1 Tat-induced microgliosis and synaptic damage via interactions between peripheral and central myeloid cells

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Lu, Shao Ming ^a   Tremblay, Marie Ève ^b   King, Irah L ^c   Qi, Jin ^d   Reynolds, Holly M ^e   Marker, Daniel F ^a   Varrone, John J P ^a   Majewska, Ania K ^a   Dewhurst, Stephen ^a   Gelbard, Harris A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

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

^c TRUDEAU INSTITUTE   (United States)

^d NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^e Diffinity Genomics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; MYELOPEROXIDASE; TRANSACTIVATOR PROTEIN; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL INFILTRATION; CELL INTERACTION; CELL LINEAGE; CONTROLLED STUDY; DENDRITE; GLIOSIS; GRANULOCYTE; HIPPOCAMPUS; HIV ASSOCIATED DEMENTIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOCOMPETENT CELL; LEUKOCYTE; MICROGLIOSIS; MOUSE; NERVOUS SYSTEM INFLAMMATION; NERVOUS SYSTEM INJURY; NEUROIMMUNOLOGY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; SYNAPTIC INJURY; VIRUS REPLICATION; WILD TYPE; ANIMAL; CELL COMMUNICATION; CYTOLOGY; DRUG EFFECT; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; INFLAMMATION; INJECTION; METABOLISM; MICROGLIA; NERVE CELL; PATHOLOGY; PHYSIOLOGY; SYNAPSE; TIME; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MUS;

ANIMALS; CELL COMMUNICATION; GRANULOCYTES; HIV-1; INFLAMMATION; INJECTIONS; MICE; MICROGLIA; MYELOID CELLS; NEURONS; NEUTROPHIL INFILTRATION; RECEPTORS, CHEMOKINE; SYNAPSES; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TIME FACTORS;

EID: 80052425327     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023915     Document Type: Article

References (71)

1. Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, et al. (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 75 (23): 2087-96.
2. Clifford DB, (2008) HIV-associated neurocognitive disease continues in the antiretroviral era. Top HIV Med 16 (2): 94-8.
3. Ernst T, Yakupov R, Nakama H, Crocket G, Cole M, et al. (2009) Declined neural efficiency in cognitively stable human immunodeficiency virus patients. Ann Neurol 65 (3): 316-25.
4. Sharer LR, (1992) Pathology of HIV-1 infection of the central nervous system. A review. J Neuropathol Exp Neurol 51 (1): 3-11.
5. Everall IP, Glass JD, McArthur J, Spargo E, Lantos P, (1994) Neuronal density in the superior frontal and temporal gyri does not correlate with the degree of human immunodeficiency virus-associated dementia. Acta Neuropathol (Berl) 88 (6): 538-44.
6. Everall IP, Heaton RK, Marcotte TD, Ellis RJ, McCutchan JA, et al. (1999) Cortical synaptic density is reduced in mild to moderate human immunodeficiency virus neurocognitive disorder. HNRC Group. HIV Neurobehavioral Research Center. Brain Pathol 9 (2): 209-17.
7. Glass JD, Fedor H, Wesselingh SL, McArthur JC, (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38 (5): 755-62.
8. Masliah E, Heaton RK, Marcotte TD, Ellis RJ, Wiley CA, et al. (1997) Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. HNRC Group. The HIV Neurobehavioral Research Center. Ann Neurol 42 (6): 963-72.
9. Jones M, Olafson K, Del Bigio MR, Peeling J, Nath A, (1998) Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J Neuropathol Exp Neurol 57 (6): 563-70.
10. Norman JP, Perry SW, Reynolds HM, Kiebala M, De Mesy Bentley KL, et al. (2008) HIV-1 Tat activates neuronal ryanodine receptors with rapid induction of the unfolded protein response and mitochondrial hyperpolarization. PLoS One 3 (11): e3731.
11. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, et al. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8 (6): 752-8.
12. Hanisch UK, Kettenmann H, (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10 (11): 1387-94.
13. Neumann J, Sauerzweig S, Ronicke R, Gunzer F, Dinkel K, et al. (2008) Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: a new mechanism of CNS immune privilege. J Neurosci 28 (23): 5965-75.
14. Nimmerjahn A, Kirchhoff F, Helmchen F, (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308 (5726): 1314-8.
15. Simioni S, Cavassini M, Annoni JM, Rimbault Abraham A, Bourquin I, et al. (2010) Cognitive dysfunction in HIV patients despite long-standing suppression of viremia. Aids 24 (9): 1243-50.
16. Cowley D, Gray LR, Wesselingh SL, Gorry PR, Churchill MJ, (2011) Genetic and functional heterogeneity of CNS-derived tat alleles from patients with HIV-associated dementia. J Neurovirol 17 (1): 70-81.
17. Dash PK, Gorantla S, Gendelman HE, Knibbe J, Casale GP, et al. (2011) Loss of Neuronal Integrity during Progressive HIV-1 Infection of Humanized Mice. J Neurosci 31 (9): 3148-57.
18. Barks JD, Sun R, Malinak C, Silverstein FS, (1995) gp120, an HIV-1 protein, increases susceptibility to hypoglycemic and ischemic brain injury in perinatal rats. Exp Neurol 132 (1): 123-33.
19. Burudi EM, Fox HS, (2001) Simian immunodeficiency virus model of HIV-induced central nervous system dysfunction. Adv Virus Res 56: 435-68.
20. Kim BO, Liu Y, Ruan Y, Xu ZC, Schantz L, et al. (2003) Neuropathologies in transgenic mice expressing human immunodeficiency virus type 1 Tat protein under the regulation of the astrocyte-specific glial fibrillary acidic protein promoter and doxycycline. Am J Pathol 162 (5): 1693-707.
21. Orandle MS, MacLean AG, Sasseville VG, Alvarez X, Lackner AA, (2002) Enhanced expression of proinflammatory cytokines in the central nervous system is associated with neuroinvasion by simian immunodeficiency virus and the development of encephalitis. J Virol 76 (11): 5797-802.
22. Persidsky Y, Limoges J, McComb R, Bock P, Baldwin T, et al. (1996) Human immunodeficiency virus encephalitis in SCID mice. Am J Pathol 149 (3): 1027-53.
23. Potash MJ, Chao W, Bentsman G, Paris N, Saini M, et al. (2005) A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc Natl Acad Sci U S A 102 (10): 3760-5.
24. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, et al. (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367 (6459): 188-93.
25. Fitting S, Booze RM, Hasselrot U, Mactutus CF, (2010) Dose-dependent long-term effects of Tat in the rat hippocampal formation: a design-based stereological study. Hippocampus 20 (4): 469-80.
26. Fitting S, Booze RM, Mactutus CF, (2008) Neonatal intrahippocampal injection of the HIV-1 proteins gp120 and Tat: differential effects on behavior and the relationship to stereological hippocampal measures. Brain Res 1232: 139-54.
27. Keblesh JP, Dou H, Gendelman HE, Xiong H, (2009) 4-Aminopyridine improves spatial memory in a murine model of HIV-1 encephalitis. J Neuroimmune Pharmacol 4 (3): 317-27.
28. Kim HJ, Martemyanov KA, Thayer SA, (2008) Human immunodeficiency virus protein Tat induces synapse loss via a reversible process that is distinct from cell death. J Neurosci 28 (48): 12604-13.
29. Okamoto S, Kang YJ, Brechtel CW, Siviglia E, Russo R, et al. (2007) HIV/gp120 decreases adult neural progenitor cell proliferation via checkpoint kinase-mediated cell-cycle withdrawal and G1 arrest. Cell Stem Cell 1 (2): 230-6.
30. Toborek M, Lee YW, Pu H, Malecki A, Flora G, et al. (2003) HIV-Tat protein induces oxidative and inflammatory pathways in brain endothelium. J Neurochem 84 (1): 169-79.
31. Solovjov DA, Pluskota E, Plow EF, (2005) Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J Biol Chem 280 (2): 1336-45.
32. Shapiro LA, Perez ZD, Foresti ML, Arisi GM, Ribak CE, (2009) Morphological and ultrastructural features of Iba1-immunolabeled microglial cells in the hippocampal dentate gyrus. Brain Res 1266: 29-36.
33. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, et al. (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20 (11): 4106-14.
34. Onoe K, Yasumizu R, Oh-Ishi T, Kakinuma M, Good RA, et al. (1981) Restricted antibody formation to sheep erythrocytes of allogeneic bone marrow chimeras histoincompatible at the K end of the H-2 complex. J Exp Med 153 (4): 1009-14.
35. Geissmann F, Jung S, Littman DR, (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19 (1): 71-82.
36. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, et al. (2007) Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317 (5838): 666-70.
37. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM, (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10 (12): 1538-43.
38. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, et al. (2007) Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10 (12): 1544-53.
39. Ransohoff RM, (2007) Microgliosis: the questions shape the answers. Nat Neurosci 10 (12): 1507-9.
40. Rausch PG, Pryzwansky KB, Spitznagel JK, Herion JC, (1978) Immunocytochemical identification of abnormal polymorphonuclear neutrophils in patients with leukemia. Blood Cells 4 (3): 369-82.
41. Cervantes-Sandoval I, Serrano-Luna Jde J, Garcia-Latorre E, Tsutsumi V, Shibayama M, (2008) Characterization of brain inflammation during primary amoebic meningoencephalitis. Parasitol Int 57 (3): 307-13.
42. Hudson L, Liu J, Nath A, Jones M, Raghavan R, et al. (2000) Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J Neurovirol 6 (2): 145-55.
43. Abraham S, Sawaya BE, Safak M, Batuman O, Khalili K, et al. (2003) Regulation of MCP-1 gene transcription by Smads and HIV-1 Tat in human glial cells. Virology 309 (2): 196-202.
44. Abraham S, Sweet T, Sawaya BE, Rappaport J, Khalili K, et al. (2005) Cooperative interaction of C/EBP beta and Tat modulates MCP-1 gene transcription in astrocytes. J Neuroimmunol 160 (1-2): 219-27.
45. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, et al. (1998) Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci U S A 95 (6): 3117-21.
46. Khiati A, Chaloin O, Muller S, Tardieu M, Horellou P, (2010) Induction of monocyte chemoattractant protein-1 (MCP-1/CCL2) gene expression by human immunodeficiency virus-1 Tat in human astrocytes is CDK9 dependent. J Neurovirol 16 (2): 150-67.
47. Pu H, Tian J, Flora G, Lee YW, Nath A, et al. (2003) HIV-1 Tat protein upregulates inflammatory mediators and induces monocyte invasion into the brain. Mol Cell Neurosci 24 (1): 224-37.
48. Weiss JM, Nath A, Major EO, Berman JW, (1999) HIV-1 Tat induces monocyte chemoattractant protein-1-mediated monocyte transmigration across a model of the human blood-brain barrier and up-regulates CCR5 expression on human monocytes. J Immunol 163 (5): 2953-9.
49. Arese M, Ferrandi C, Primo L, Camussi G, Bussolino F, (2001) HIV-1 Tat protein stimulates in vivo vascular permeability and lymphomononuclear cell recruitment. J Immunol 166 (2): 1380-8.
50. Del Sorbo L, Arese M, Giraudo E, Tizzani M, Biancone L, et al. (2001) Tat-induced platelet-activating factor synthesis contributes to the angiogenic effect of HIV-1 Tat. Eur J Immunol 31 (2): 376-83.
51. New DR, Maggirwar SB, Epstein LG, Dewhurst S, Gelbard HA, (1998) HIV-1 Tat induces neuronal death via tumor necrosis factor-alpha and activation of non-N-methyl-D-aspartate receptors by a NFkappaB-independent mechanism. J Biol Chem 273 (28): 17852-8.
52. Perry SW, Hamilton JA, Tjoelker LW, Dbaibo G, Dzenko KA, et al. (1998) Platelet-activating factor receptor activation. An initiator step in HIV-1 neuropathogenesis. J Biol Chem 273 (28): 17660-4.
53. Satoh S, Kobayashi T, Hitomi A, Ikegaki I, Suzuki Y, et al. (1999) Inhibition of neutrophil migration by a protein kinase inhibitor for the treatment of ischemic brain infarction. Jpn J Pharmacol 80 (1): 41-8.
54. Anderson E, Zink W, Xiong H, Gendelman HE, (2002) HIV-1-associated dementia: a metabolic encephalopathy perpetrated by virus-infected and immune-competent mononuclear phagocytes. J Acquir Immune Defic Syndr 31 (Suppl 2): S43-54.
55. Marcondes MC, Burdo TH, Sopper S, Huitron-Resendiz S, Lanigan C, et al. (2007) Enrichment and persistence of virus-specific CTL in the brain of simian immunodeficiency virus-infected monkeys is associated with a unique cytokine environment. J Immunol 178 (9): 5812-9.
56. Tremblay ME, Lowery RL, Majewska AK, (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol 8 (11): e1000527.
57. Yao H, Bethel-Brown C, Li CZ, Buch SJ, (2010) HIV neuropathogenesis: a tight rope walk of innate immunity. J Neuroimmune Pharmacol 5 (4): 489-95.
58. Avgeropoulos NG, Burris GW, Ohlandt GW, Wesselingh SL, Markham RB, et al. (1998) Potential relationships between the presence of HIV, macrophages, and astrogliosis in SCID mice with HIV encephalitis. J NeuroAIDS 2 (1): 1-20.
59. Lelekov-Boissard T, Chapuisat G, Boissel JP, Grenier E, Dronne MA, (2009) Exploration of beneficial and deleterious effects of inflammation in stroke: dynamics of inflammation cells. Philos Transact A Math Phys Eng Sci 367 (1908): 4699-716.
60. Ma Q, Manaenko A, Khatibi NH, Chen W, Zhang JH, et al. (2011) Vascular adhesion protein-1 inhibition provides antiinflammatory protection after an intracerebral hemorrhagic stroke in mice. J Cereb Blood Flow Metab.
61. McColl BW, Rothwell NJ, Allan SM, (2007) Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J Neurosci 27 (16): 4403-12.
62. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, et al. (2010) Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 467 (7317): 863-7.
63. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, et al. (2009) Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461 (7261): 282-6.
64. Deshpande P, King IL, Segal BM, (2007) Cutting edge: CNS CD11c+ cells from mice with encephalomyelitis polarize Th17 cells and support CD25+CD4+ T cell-mediated immunosuppression, suggesting dual roles in the disease process. J Immunol 178 (11): 6695-9.
65. McLean IW, Nakane PK, (1974) Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem 22 (12): 1077-83.
66. Tremblay ME, Riad M, Majewska A, (2010) Preparation of mouse brain tissue for immunoelectron microscopy. J Vis Exp (41).
67. Oster-Granite ML, McPhie DL, Greenan J, Neve RL, (1996) Age-dependent neuronal and synaptic degeneration in mice transgenic for the C terminus of the amyloid precursor protein. J Neurosci 16 (21): 6732-41.
68. Peters A, Sethares C, (2004) Oligodendrocytes, their progenitors and other neuroglial cells in the aging primate cerebral cortex. Cereb Cortex 14 (9): 995-1007.
69. Peters A, Palay SL, Webster H, (1991) The fine structure of the nervous system: the neurons and supporting cells Philadelphia W.B. Saunders.
70. Turmaine M, Raza A, Mahal A, Mangiarini L, Bates GP, et al. (2000) Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc Natl Acad Sci U S A 97 (14): 8093-7.
71. Yang DS, Kumar A, Stavrides P, Peterson J, Peterhoff CM, et al. (2008) Neuronal apoptosis and autophagy cross talk in aging PS/APP mice, a model of Alzheimer's disease. Am J Pathol 173 (3): 665-81.