Apolipoprotein E-dependent differences in innate immune responses of maturing human neuroepithelial progenitor cells exposed to HIV-1

Journal of Neuroimmune Pharmacology

Volumn 8, Issue 4, 2013, Pages 1010-1026

  Geffin, Rebeca ^a,b   Martinez, Ricardo ^a   Perez, Roberto ^a   Issac, Biju ^c   McCarthy, Micheline ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MIAMI   (United States)

Author keywords

Apolipoprotein E; HIV; Human immunodeficiency virus; Innate immune response; Neuron

Indexed keywords

2 ' 5 ' OLIGOADENYLATE SYNTHETASE 1; 2 ' 5' OLIGOADENYLATE SYNTHETASE 3; APOLIPOPROTEIN E3; BONE MARROW STROMAL CELL ANTIGEN 2; EPITHELIAL STROMAL INTERACTION 1; GUANYLATE BINDING PROTEIN 1; HECT AND RLD DOMAIN CONTAINING E3 UBIQUITIN PROTEIN LIGASE; HECT AND RLD DOMAIN CONTAINING E3 UBIQUITIN PROTEIN LIGASE 6; HLA CLASS I HISTOCOMPATIBILITY ANTIGEN ALPHA CHAIN F; HLA COMPLEX P5; INTERFERON; INTERFERON ALPHA INDUCIBLE PROTEIN 27; INTERFERON INDUCED PROTEIN 44; INTERFERON INDUCED PROTEIN 44 LIKE; INTERFERON INDUCED PROTEIN WITH TETRATRICOPEPTIDE REPEATS 1; INTERFERON INDUCED PROTEIN WITH TETRATRICOPEPTIDE REPEATS 3; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 1; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 2; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 3; INTERFERON INDUCIBLE PROTEIN 6; INTERFERON REGULATORY FACTOR 9; MAJOR HISTOCOMPATIBILITY COMPLEX 1B; POLY(ADP RIBOSE)POLYMERASE 14; POLY(ADP RIBOSE)POLYMERASE 9; PROTEASOME BETA 9; PROTEIN; SOLUTE CARRIER FAMILY 15 MEMBER 3; STAT1 PROTEIN; STERILE ALPHA MOTIF DOMAIN CONTAINING 9; UBIQUITIN LIKE MODIFIER; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CELL PROLIFERATION; CELL SURVIVAL; FETUS; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INNATE IMMUNITY; INTERFERON INDUCTION; MICROARRAY ANALYSIS; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM; PRIORITY JOURNAL; UPREGULATION;

APOLIPOPROTEINS E; CELLS, CULTURED; FETAL STEM CELLS; GENOTYPE; HIV-1; HUMANS; IMMUNITY, INNATE; NEURAL STEM CELLS; NEUROEPITHELIAL CELLS;

EID: 84882280647     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-013-9478-0     Document Type: Article

References (49)

1. Bachoo RM, Kim RS, Ligon KL, Maher EA, Brennan C, Billings N, Chan S, Li C, Rowitch DH, Wong WH, DePinho RA (2004) Molecular diversity of astrocytes with implications for neurological disorders. Proc Natl Acad Sci U S A 101:8384-8389
2. Barr SD, Smiley JR, Bushman FD (2008) The interferon response inhibits HIV particle production by induction of TRIM22. PLoS Pathog 4:e1000007
3. Borjabad A, Brooks AI, Volsky DJ (2010) Gene expression profiles of HIV-1-infected glia and brain: toward better understanding of the role of astrocytes in HIV-1-associated neurocognitive disorders. J Neuroimmune Pharmacol 5:44-62
4. Borjabad A, Morgello S, Chao W, Kim SY, Brooks AI, Murray J, Potash MJ, Volsky DJ (2011) Significant effects of antiretroviral therapy on global gene expression in brain tissues of patients with HIV-1-associated neurocognitive disorders. PLoS Pathog 7:e1002213
5. Burt TD, Agan BK, Marconi VC, He W, Kulkarni H, Mold JE, Cavrois M, Huang Y, Mahley RW, Dolan MJ, McCune JM, Ahuja SK (2008) Apolipoprotein (apo) E4 enhances HIV-1 cell entry in vitro, and the APOE epsilon4/epsilon4 genotype accelerates HIV disease progression. Proc Natl Acad Sci U S A 105:8718-8723
6. Carter DB (2005) The interaction of amyloid-beta with ApoE. Subcell Biochem 38:255-272
7. Chen J, Li Q, Wang J (2011) Topology of human apolipoprotein E3 uniquely regulates its diverse biological functions. Proc Natl Acad Sci U S A 108:14813-14818
8. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921-923
9. Corder EH, Saunders AM, Risch NJ, Strittmatter WJ, Schmechel DE, Gaskell PC Jr, Rimmler JB, Locke PA, Conneally PM, Schmader KE et al (1994) Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat Genet 7:180-184
10. Davies DL, Niesman IR, Boop FA, Phelan KD (2000) Heterogeneity of astroglia cultured from adult human temporal lobe. Int J Dev Neurosci 18:151-160
11. Dewhurst S, Bresser J, Stevenson M, Sakai K, Evinger-Hodges MJ, Volsky DJ (1987) Susceptibility of human glial cells to infection with human immunodeficiency virus (HIV). FEBS Lett 213:138-143
12. Galey D, Becker K, Haughey N, Kalehua A, Taub D, Woodward J, Mattson MP, Nath A (2003) Differential transcriptional regulation by human immunodeficiency virus type 1 and gp120 in human astrocytes. J Neurovirol 9:358-371
13. Hauser PS, Narayanaswami V, Ryan RO (2011) Apolipoprotein E: from lipid transport to neurobiology. Prog Lipid Res 50:62-74
14. Hazenberg MD, Otto SA, van Benthem BH, Roos MT, Coutinho RA, Lange JM, Hamann D, Prins M, Miedema F (2003) Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 17:1881-1888
15. Hixson JE, Vernier DT (1990) Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J Lipid Res 31:545-548
16. Johnson WE, Li C, Rabinovic A (2007) Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8:118-127
17. Kim SY, Li J, Bentsman G, Brooks AI, Volsky DJ (2004) Microarray analysis of changes in cellular gene expression induced by productive infection of primary human astrocytes: implications for HAD. J Neuroimmunol 157:17-26
18. Kuhlmann I, Minihane AM, Huebbe P, Nebel A, Rimbach G (2010) Apolipoprotein E genotype and hepatitis C, HIV and herpes simplex disease risk: a literature review. Lipids Health Dis 9:8
19. Li W, Galey D, Mattson MP, Nath A (2005) Molecular and cellular mechanisms of neuronal cell death in HIV dementia. Neurotox Res 8:119-134
20. Lu J, Pan Q, Rong L, He W, Liu SL, Liang C (2011) The IFITM proteins inhibit HIV-1 infection. J Virol 85:2126-2137
21. Maezawa I, Maeda N, Montine TJ, Montine KS (2006a) Apolipoprotein E-specific innate immune response in astrocytes from targeted replacement mice. J Neuroinflammation 3:10
22. Maezawa I, Nivison M, Montine KS, Maeda N, Montine TJ (2006b) Neurotoxicity from innate immune response is greatest with targeted replacement of E4 allele of apolipoprotein E gene and is mediated by microglial p38MAPK. FASEB J 20:797-799
23. Mahley RW (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240:622-630
24. Mahley RW, Rall SC Jr (2000) Apolipoprotein E: far more than a lipid transport protein. Annu Rev Genomics Hum Genet 1:507-537
25. Martinez R, Chunjing W, Geffin R, McCarthy M (2012) Depressed neurofilament expression associates with apolipoprotein E3/E4 genotype in maturing human fetal neurons exposed to HIV-1. J Neurovirol 18:323-330
26. Masliah E, Roberts ES, Langford D, Everall I, Crews L, Adame A, Rockenstein E, Fox HS (2004) Patterns of gene dysregulation in the frontal cortex of patients with HIV encephalitis. J Neuroimmunol 157:163-175
27. McCarthy M, He J, Wood C (1998) HIV-1 strain-associated variability in infection of primary neuroglia. J Neurovirol 4:80-89
28. McCarthy M, Vidaurre I, Geffin R (2006) Maturing neurons are selectively sensitive to human immunodeficiency virus type 1 exposure in differentiating human neuroepithelial progenitor cell cultures. J Neurovirol 12:333-348
29. Mondor I, Ugolini S, Sattentau QJ (1998) Human immunodeficiency virus type 1 attachment to HeLa CD4 cells is CD4 independent and gp120 dependent and requires cell surface heparans. J Virol 72:3623-3634
30. Nath A, Geiger J (1998) Neurobiological aspects of human immunodeficiency virus infection: neurotoxic mechanisms. Prog Neurobiol 54:19-33
31. 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 54:320-330
32. Neil SJ, Zang T, Bieniasz PD (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430
33. Okumura A, Lu G, Pitha-Rowe I, Pitha PM (2006) Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15. Proc Natl Acad Sci U S A 103:1440-1445
34. Palm K, Salin-Nordstrom T, Levesque MF, Neuman T (2000) Fetal and adult human CNS stem cells have similar molecular characteristics and developmental potential. Brain Res Mol Brain Res 78:192-195
35. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, Bieniasz PD (2009) Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139:499-511
36. Pincetic A, Kuang Z, Seo EJ, Leis J (2010) The interferon-induced gene ISG15 blocks retrovirus release from cells late in the budding process. J Virol 84:4725-4736
37. Poirier J, Davignon J, Bouthillier D, Kogan S, Bertrand P, Gauthier S (1993) Apolipoprotein E polymorphism and Alzheimer's disease. Lancet 342:697-699
38. Roberts ES, Zandonatti MA, Watry DD, Madden LJ, Henriksen SJ, Taffe MA, Fox HS (2003) Induction of pathogenic sets of genes in macrophages and neurons in NeuroAIDS. Am J Pathol 162:2041-2057
39. Roderiquez G, Oravecz T, Yanagishita M, Bou-Habib DC, Mostowski H, Norcross MA (1995) Mediation of human immunodeficiency virus type 1 binding by interaction of cell surface heparan sulfate proteoglycans with the V3 region of envelope gp120-gp41. J Virol 69:2233-2239
40. Stephens EB, Jackson M, Cui L, Pacyniak E, Choudhuri R, Liverman CS, Salomon DS, Berman NE (2006) Early dysregulation of cripto-1 and immunomodulatory genes in the cerebral cortex in a macaque model of neuroAIDS. Neurosci Lett 410:94-99
41. Su ZZ, Kang DC, Chen Y, Pekarskaya O, Chao W, Volsky DJ, Fisher PB (2002) Identification and cloning of human astrocyte genes displaying elevated expression after infection with HIV-1 or exposure to HIV-1 envelope glycoprotein by rapid subtraction hybridization, RaSH. Oncogene 21:3592-3602
42. Tornatore C, Nath A, Amemiya K, Major EO (1991) Persistent human immunodeficiency virus type 1 infection in human fetal glial cells reactivated by T-cell factor(s) or by the cytokines tumor necrosis factor alpha and interleukin-1 beta. J Virol 65:6094-6100
43. Trkola A, Ketas T, Kewalramani VN, Endorf F, Binley JM, Katinger H, Robinson J, Littman DR, Moore JP (1998) Neutralization sensitivity of human immunodeficiency virus type 1 primary isolates to antibodies and CD4-based reagents is independent of coreceptor usage. J Virol 72:1876-1885
44. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034
45. Vitek MP, Brown CM, Colton CA (2009) APOE genotype-specific differences in the innate immune response. Neurobiol Aging 30:1350-1360
46. Wang Z, Pekarskaya O, Bencheikh M, Chao W, Gelbard HA, Ghorpade A, Rothstein JD, Volsky DJ (2003) Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 312:60-73
47. Wang Z, Trillo-Pazos G, Kim SY, Canki M, Morgello S, Sharer LR, Gelbard HA, Su ZZ, Kang DC, Brooks AI, Fisher PB, Volsky DJ (2004) Effects of human immunodeficiency virus type 1 on astrocyte gene expression and function: potential role in neuropathogenesis. J Neurovirol 10(Suppl 1):25-32
48. Winkler JM, Chaudhuri AD, Fox HS (2012) Translating the brain transcriptome in neuroAIDS: from non-human primates to humans. J Neuroimmune Pharmacol 7:372-379
49. Yao H, Bethel-Brown C, Li CZ, Buch SJ (2010) HIV neuropathogenesis: a tight rope walk of innate immunity. J Neuroimmune Pharmacol 5:489-495