Chronic HIV-1 Tat and HIV reduce Rbfox3/NeuN: Evidence for sex- related effects

Current HIV Research

Volumn 13, Issue 1, 2015, Pages 10-20

  Hahn, Yun Kyung ^a   Masvekar, Ruturaj R ^a   Xu, Ruqiang ^a   Hauser, Kurt F ^a   Knapp, Pamela E ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Human; Male; NeuroAIDS; Neurodegeneration; Stereology; Transgenic

Indexed keywords

DOXYCYCLINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; NEURON SPECIFIC NUCLEAR PROTEIN; RNA BINDING FEMINIZING LOCUS X 3 PROTEIN; RNA BINDING PROTEIN; TATA BINDING PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; CELL NUCLEUS ANTIGEN; NERVE PROTEIN; NEUN PROTEIN, MOUSE; NUCLEAR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CELL CULTURE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LUND HUMAN MESENCEPHALIC CELL; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; NEUROLOGIC EXAMINATION; NEUROTOXICITY; NISSL STAINING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; RNA EXTRACTION; SEXUAL FUNCTION; SIGNAL TRANSDUCTION; STEREOLOGY; VIRUS REPLICATION; ALTERNATIVE RNA SPLICING; ANIMAL; BASAL GANGLION; CELL LINE; CYTOPLASM; GENETICS; HIPPOCAMPUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; NERVE CELL; PHYSIOLOGY; SEX DIFFERENCE; TRANSGENIC MOUSE;

ALTERNATIVE SPLICING; ANIMALS; ANTIGENS, NUCLEAR; BASAL GANGLIA; CELL LINE; CYTOPLASM; FEMALE; HIPPOCAMPUS; HIV INFECTIONS; HIV-1; HUMANS; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; RNA, MESSENGER; SEX FACTORS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84930972208     PISSN: 1570162X     EISSN: 18734251     Source Type: Journal    
DOI: 10.2174/1570162X13666150311163733     Document Type: Article

References (52)

1. [1] Everall IP, Bell C, Mallory M, et al. Lithium ameliorates HIVgp120-mediated neurotoxicity. Mol Cell Neurosci 2002; 21: 493-501.
2. [2] Zujovic V, Benavides J, Vige X, Carter C, Taupin V. Fractalkine modulates TNF-alpha secretion and neurotoxicity induced by microglial activation. Glia 2000; 29: 305-15.
3. [3] Dou H, Birusingh K, Faraci J, et al. Neuroprotective activities of sodium valproate in a murine model of human immunodeficiency virus-1 encephalitis. J Neurosci 2003; 23: 9162-70.
4. [4] Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992; 116: 201-11.
5. [5] Jin Y, Suzuki H, Maegawa S, et al. A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG. EMBO J 2003; 22: 905-12.
6. [6] Nakahata S, Kawamoto S. Tissue-dependent isoforms of mammalian Fox-1 homologs are associated with tissue-specific splicing activities. Nucleic Acids Res 2005;33(7):2078-89.
7. [7] Ponthier JL, Schluepen C, Chen W, et al. Fox-2 splicing factor binds to a conserved intron motif to promote inclusion of protein 4.1R alternative exon 16. J Biol Chem 2006; 281: 12468-74.
8. [8] Underwood JG, Boutz PL, Dougherty JD, Stoilov P, Black DL. Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol Cell Biol 2005; 25: 10005-16.
9. [9] Kim KK, Adelstein RS, Kawamoto S. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 2009; 284: 31052-61.
10. [10] Kim KK, Nam J, Mukouyama YS, Kawamoto S. Rbfox3-regulated alternative splicing of Numb promotes neuronal differentiation during development. J Cell Biol 2013; 200: 443-58.
11. [11] Kim KK, Yang Y, Zhu J, Adelstein RS, Kawamoto S. Rbfox3 controls the biogenesis of a subset of microRNAs. Nat Stru & Mol Biol 2014; 21: 901-10.
12. [12] Kim KK, Adelstein RS, Kawamoto S. Isoform-specific proteasomal degradation of Rbfox3 during chicken embryonic development. Biochem & Biophysi Res Commu 2014; 450: 1662-7.
13. [13] Unal-Cevik I, Kilinc M, Gursoy-Ozdemir Y, Gurer G, Dalkara T. Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res. 2004; 1015: 169-74.
14. [14] Collombet JM, Masqueliez C, Four E, et al. Early reduction of NeuN antigenicity induced by soman poisoning in mice can be used to predict delayed neuronal degeneration in the hippocampus. Neurosci Lett 2006; 398: 337-42.
15. [15] Utami KH, Hillmer AM, Aksoy I, et al. Detection of chromosomal breakpoints in patients with developmental delay and speech disorders. PLoS ONE 2014; 9: e90852.
16. [16] Lucas CH, Calvez M, Babu R, Brown A. Altered subcellular localization of the NeuN/Rbfox3 RNA splicing factor in HIVassociated neurocognitive disorders (HAND). Neurosci Lett 2014; 558: 97-102.
17. [17] Van Nassauw L, Wu M, De Jonge F, Adriaensen D, Timmermans JP. Cytoplasmic, but not nuclear, expression of the neuronal nuclei (NeuN) antibody is an exclusive feature of Dogiel type II neurons in the guinea-pig gastrointestinal tract. Histochem and Cell Biol 2005; 124: 369-77.
18. [18] Gelman BB, Chen T, Lisinicchia JG, et al. The National NeuroAIDS Tissue Consortium brain gene array: two types of HIV-associated neurocognitive impairment. PLoS ONE 2012; 7: e46178.
19. [19] Morgello S, Gelman BB, Kozlowski PB, et al. The National NeuroAIDS Tissue Consortium: a new paradigm in brain banking with an emphasis on infectious disease. Neuropath Appl Neuro 2001; 27: 326-35.
20. [20] Dever SM, Xu R, Fitting S, Knapp PE, Hauser KF. Differential expression and HIV-1 regulation of mu-opioid receptor splice variants across human central nervous system cell types. J Neurovirol 2012; 18: 181-90.
21. [21] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-8.
22. [22] Schildknecht S, Poltl D, Nagel DM, et al. Requirement of a dopaminergic neuronal phenotype for toxicity of low concentrations of 1-methyl-4-phenylpyridinium to human cells. Toxicol Appl Pharm 2009; 241: 23-35.
23. [23] Scholz D, Poltl D, Genewsky A, et al. Rapid, complete and largescale generation of post-mitotic neurons from the human LUHMES cell line. J Neurochem 2011; 119: 957-71.
24. [24] Lotharius J, Falsig J, van Beek J, et al. Progressive degeneration of human mesencephalic neuron-derived cells triggered by dopaminedependent oxidative stress is dependent on the mixed-lineage kinase pathway. J Neurosci 2005; 25: 6329-42.
25. [25] Masvekar RR, El-Hage N, Hauser KF, Knapp PE. Morphine enhances HIV-1SF162-mediated neuron death and delays recovery of injured neurites. PLoS ONE 2014; 9: e100196.
26. [26] Hahn YK, Podhaizer EM, Hauser KF, Knapp PE. HIV-1 alters neural and glial progenitor cell dynamics in the central nervous system: Coordinated response to opiates during maturation. Glia 2012; 60: 1871-87.
27. Cheng-Mayer C, Levy JA. Distinct biological and serological properties of human immunodeficiency viruses from the brain. Ann Neurol 1988; 23 Suppl:S58-61.
28. [28] Hauser KF, Hahn YK, Adjan VV, Zou S, Buch SK, Nath A, et al. HIV-1 Tat and morphine have interactive effects on oligodendrocyte survival and morphology. Glia 2009; 57: 194-206.
29. [29] Fitting S, Xu R, Bull C, et al. Interactive comorbidity between opioid drug abuse and HIV-1 Tat: chronic exposure augments spine loss and sublethal dendritic pathology in striatal neurons. Am J Pathol. 2010; 177: 1397-410.
30. [30] Bruce-Keller AJ, Turchan-Cholewo J, Smart EJ, et al. Morphine causes rapid increases in glial activation and neuronal injury in the striatum of inducible HIV-1 tat transgenic mice. Glia 2008; 56: 1414-27.
31. [31] Fitting S, Ignatowska-Jankowska BM, Bull C, et al. Synaptic Dysfunction in the Hippocampus Accompanies Learning and Memory Deficits in Human Immunodeficiency Virus Type 1 Transactivator of Transcription Transgenic Mice. Biol Psychiat 2013; 73: 443-53.
32. [32] Hahn YK, Podhaizer EM, Farris SP, et al. Effects of chronic HIV-1 Tat exposure in the CNS: heightened vulnerability of males versus females to changes in cell numbers, synaptic integrity, and behavior. Brain Struc Funct 2015; in press.
33. Davenport HA. Histological and Histochemical Techniques. 1960.
34. [34] Nielsen MS, Sorensen JC, Bjarkam CR. The substantia nigra pars compacta of the Gottingen minipig: an anatomical and stereological study. Brain Struc Funct 2009; 213: 481-8.
35. [35] Fitting S, Booze RM, Mactutus CF. Neonatal intrahippocampal injection of the HIV-1 proteins gp120 and Tat: differential effects on behavior and the relationship to stereological hippocampal measures. Brain Res 2008; 1232: 139-54.
36. [36] Fitting S, Booze RM, Hasselrot U, Mactutus CF. Dose-dependent long-term effects of Tat in the rat hippocampal formation: a designbased stereological study. Hippocampus 2010; 20: 469-80.
37. [37] Cyr M, Caron MG, Johnson GA, Laakso A. Magnetic resonance imaging at microscopic resolution reveals subtle morphological changes in a mouse model of dopaminergic hyperfunction. Neuroimage 2005; 26: 83-90.
38. [38] Sherwood CC, Stimpson CD, Raghanti MA, et al. Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci USA 2006; 103:13606-11.
39. Mouton PR. Principles and practices of unbiased stereology: an introduction for bioscientists. Baltimore: Johns Hopkins University Press; 2002. x, 214 p. p.
40. [40] Portiansky EL, Barbeito CG, Gimeno EJ, Zuccolilli GO, Goya RG. Loss of NeuN immunoreactivity in rat spinal cord neurons during aging. Exp Neurol 2006; 202: 519-21.
41. [41] Wojna V, Skolasky RL, Hechavarria R, et al. Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment. J Neurovirol 2006; 12: 356-64.
42. [42] Gupta JD, Satishchandra P, Gopukumar K, et al. Neuropsychological deficits in human immunodeficiency virus type 1 clade C-seropositive adults from South India. J Neurovirol 2007; 13: 195-202.
43. [43] Hestad KA, Menon JA, Silalukey-Ngoma M, et al. Sex differences in neuropsychological performance as an effect of human immunodeficiency virus infection: a pilot study in Zambia, Africa. J Nerv Ment Dis 2012; 200: 336-42.
44. [44] Joska JA, Westgarth-Taylor J, Myer L, et al. Characterization of HIV-Associated Neurocognitive Disorders among individuals starting antiretroviral therapy in South Africa. AIDS Behav 2011; 15: 1197-203.
45. [45] Lopes M, Olfson M, Rabkin J, et al. Gender, HIV status, and psychiatric disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. J Clin Psychiatry 2012; 73: 384-91.
46. [46] de Lau LM, Breteler MM. Epidemiology of Parkinson's disease. Lancet Neurol 2006; 5: 525-35.
47. [47] Van Den Eeden SK, Tanner CM, Bernstein AL, et al. Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am J Epidemiol 2003; 157: 1015-22.
48. [48] Coronado VG, Xu L, Basavaraju SV, et al. Surveillance for traumatic brain injury-related deaths--United States, 1997-2007. MMWR Surveill Summ 2011; 60: 1-32.
49. [49] Maxeiner S, Glassmann A, Kao HT, Schilling K. The molecular basis of the specificity and cross-reactivity of the NeuN epitope of the neuron-specific splicing regulator, Rbfox3. Histochem Cell Biol 2014; 141:43-55.
50. [50] Dredge BK, Jensen KB. NeuN/Rbfox3 nuclear and cytoplasmic isoforms differentially regulate alternative splicing and nonsensemediated decay of Rbfox2. PLoS ONE 2011; 6: e21585.
51. [51] Weyer A, Schilling K. Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 2003; 73: 400-9.
52. [52] Johnson TP, Patel K, Johnson KR, et al. Induction of IL-17 and nonclassical T-cell activation by HIV-Tat protein. Proc Natl Acad Sci USA 2013; 110: 13588-93.