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Published in: Journal of NeuroVirology 5/2013

01-10-2013

YWHAE/14-3-3ε: a potential novel genetic risk factor and CSF biomarker for HIV neurocognitive impairment

Authors: Diana Morales, Rosa Hechavarria, Valerie Wojna, Summer F. Acevedo

Published in: Journal of NeuroVirology | Issue 5/2013

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Abstract

YWHAE (14-3-3ε) protein levels are considered to be a reliable biomarker for neurodegeneration. The YWHAE protein interacts both directly and indirectly with human immunodeficiency virus (HIV) accessory proteins, leading to cell death. The purpose of this study was to examine the relationship between YWHAE polymorphisms and HIV-associated neurocognitive disorder (HAND) and the relationship between YWHAE protein levels and HAND. A cross-sectional study using random samples of HIV-seropositive (n = 20) and HIV-seronegative (controls) (n = 16) women from the Hispanic-Latino Longitudinal Cohort of Women was conducted. Individuals who are HIV-seropositive and heterozygous at the rs4790084/rs1204828 loci in the YWHAE gene were 3× more likely to display reduced cognitive functioning, to have received a HAND diagnosis, and to have less YHWAE protein expressed than homozygotes. Western blots from cerebral spinal fluid indicate that the HIV-seropositive women with HAND expressed 4.5× less YWHAE compared to HIV-seropositive cognitively normal women (94 % sensitivity, 84 % specificity; HIV-seropositive vs. controls). Therefore, polymorphism in YWHAE may be a genetic risk factor for HAND and levels of YWHAE protein are a likely biomarker for neurocognitive status in HIV-seropositive women.
Literature
go back to reference Aitken A, Jones D, Soneji Y, Howell S (1995) 14-3-3 proteins: biological function and domain structure. Biochem Soc Trans 23:605–611PubMed Aitken A, Jones D, Soneji Y, Howell S (1995) 14-3-3 proteins: biological function and domain structure. Biochem Soc Trans 23:605–611PubMed
go back to reference American Academy of Neurology AIDS Task Force (1991) Nomenclature and research case definitions for neurologic manifestations of human immunodeficiency virus-type 1 (HIV-1) infection. Report of a Working Group of the American Academy of Neurology AIDS Task Force. Neurology 41:778–785CrossRef American Academy of Neurology AIDS Task Force (1991) Nomenclature and research case definitions for neurologic manifestations of human immunodeficiency virus-type 1 (HIV-1) infection. Report of a Working Group of the American Academy of Neurology AIDS Task Force. Neurology 41:778–785CrossRef
go back to reference American Academy of Neurology AIDS Task Force (1996) 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 47:1247–1253CrossRef American Academy of Neurology AIDS Task Force (1996) 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 47:1247–1253CrossRef
go back to reference Berg D, Holzmann C, Riess O (2003) 14-3-3 proteins in the nervous system. Nat Rev Neurosci 4:752–762PubMedCrossRef Berg D, Holzmann C, Riess O (2003) 14-3-3 proteins in the nervous system. Nat Rev Neurosci 4:752–762PubMedCrossRef
go back to reference Boesenberg-Grosse C, Schulz-Schaeffer WJ, Bodemer M, Ciesielczyk B, Meissner B, Krasnianski A, Bartl M, Heinemann U, Varges D, Eigenbrod S, Kretzschmar HA, Green A, Zerr I (2006) Brain-derived proteins in the CSF: do they correlate with brain pathology in CJD? BMC Neurol 6:35PubMedCrossRef Boesenberg-Grosse C, Schulz-Schaeffer WJ, Bodemer M, Ciesielczyk B, Meissner B, Krasnianski A, Bartl M, Heinemann U, Varges D, Eigenbrod S, Kretzschmar HA, Green A, Zerr I (2006) Brain-derived proteins in the CSF: do they correlate with brain pathology in CJD? BMC Neurol 6:35PubMedCrossRef
go back to reference Bolton DL, Barnitz RA, Sakai K, Lenardo MJ (2008) 14-3-3 theta binding to cell cycle regulatory factors is enhanced by HIV-1 Vpr. Biol Direct 3:17PubMedCrossRef Bolton DL, Barnitz RA, Sakai K, Lenardo MJ (2008) 14-3-3 theta binding to cell cycle regulatory factors is enhanced by HIV-1 Vpr. Biol Direct 3:17PubMedCrossRef
go back to reference Che XH, Chen H, Xu ZM, Shang C, Sun KL, Fu WN (2010) 14-3-3epsilon contributes to tumour suppression in laryngeal carcinoma by affecting apoptosis and invasion. BMC Cancer 10:306PubMedCrossRef Che XH, Chen H, Xu ZM, Shang C, Sun KL, Fu WN (2010) 14-3-3epsilon contributes to tumour suppression in laryngeal carcinoma by affecting apoptosis and invasion. BMC Cancer 10:306PubMedCrossRef
go back to reference Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, Hillsdale, NJ Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, Hillsdale, NJ
go back to reference Cohen EA, Terwilliger EF, Jalinoos Y, Proulx J, Sodroski JG, Haseltine WA (1990) Identification of HIV-1 vpr product and function. J Acquir Immune Defic Syndr 3:11–18PubMed Cohen EA, Terwilliger EF, Jalinoos Y, Proulx J, Sodroski JG, Haseltine WA (1990) Identification of HIV-1 vpr product and function. J Acquir Immune Defic Syndr 3:11–18PubMed
go back to reference Collins SJ, Sanchez-Juan P, Masters CL, Klug GM, van Duijn C, Poleggi A, Pocchiari M, Almonti S, Cuadrado-Corrales N, de Pedro-Cuesta J, Budka H, Gelpi E, Glatzel M, Tolnay M, Hewer E, Zerr I, Heinemann U, Kretszchmar HA, Jansen GH, Olsen E, Mitrova E, Alperovitch A, Brandel JP, Mackenzie J, Murray K, Will RG (2006) Determinants of diagnostic investigation sensitivities across the clinical spectrum of sporadic Creutzfeldt–Jakob disease. Brain 129:2278–2287PubMedCrossRef Collins SJ, Sanchez-Juan P, Masters CL, Klug GM, van Duijn C, Poleggi A, Pocchiari M, Almonti S, Cuadrado-Corrales N, de Pedro-Cuesta J, Budka H, Gelpi E, Glatzel M, Tolnay M, Hewer E, Zerr I, Heinemann U, Kretszchmar HA, Jansen GH, Olsen E, Mitrova E, Alperovitch A, Brandel JP, Mackenzie J, Murray K, Will RG (2006) Determinants of diagnostic investigation sensitivities across the clinical spectrum of sporadic Creutzfeldt–Jakob disease. Brain 129:2278–2287PubMedCrossRef
go back to reference Gardino AK, Yaffe MB (2011) 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin Cell Dev Biol 22:688–695PubMedCrossRef Gardino AK, Yaffe MB (2011) 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin Cell Dev Biol 22:688–695PubMedCrossRef
go back to reference Gelman BB, Nguyen TP (2010) Synaptic proteins linked to HIV-1 infection and immunoproteasome induction: proteomic analysis of human synaptosomes. J Neuroimmune Pharmacol 5:92–102PubMedCrossRef Gelman BB, Nguyen TP (2010) Synaptic proteins linked to HIV-1 infection and immunoproteasome induction: proteomic analysis of human synaptosomes. J Neuroimmune Pharmacol 5:92–102PubMedCrossRef
go back to reference Geschwind MD, Martindale J, Miller D, DeArmond SJ, Uyehara-Lock J, Gaskin D, Kramer JH, Barbaro NM, Miller BL (2003) Challenging the clinical utility of the 14-3-3 protein for the diagnosis of sporadic Creutzfeldt–Jakob disease. Arch Neurol 60:813–816PubMedCrossRef Geschwind MD, Martindale J, Miller D, DeArmond SJ, Uyehara-Lock J, Gaskin D, Kramer JH, Barbaro NM, Miller BL (2003) Challenging the clinical utility of the 14-3-3 protein for the diagnosis of sporadic Creutzfeldt–Jakob disease. Arch Neurol 60:813–816PubMedCrossRef
go back to reference He J, Choe S, Walker R, Di Marzio P, Morgan DO, Landau NR (1995) Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J Virol 69:6705–6711PubMed He J, Choe S, Walker R, Di Marzio P, Morgan DO, Landau NR (1995) Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J Virol 69:6705–6711PubMed
go back to reference Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER study. Neurology 75:2087–2096PubMedCrossRef Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER study. Neurology 75:2087–2096PubMedCrossRef
go back to reference Hsich G, Kenney K, Gibbs CJ, Lee KH, Harrington MG (1996) The 14-3-3 brain protein in cerebrospinal fluid as a marker for transmissible spongiform encephalopathies. N Engl J Med 335:924–930PubMedCrossRef Hsich G, Kenney K, Gibbs CJ, Lee KH, Harrington MG (1996) The 14-3-3 brain protein in cerebrospinal fluid as a marker for transmissible spongiform encephalopathies. N Engl J Med 335:924–930PubMedCrossRef
go back to reference Ikeda M, Hikita T, Taya S, Uraguchi-Asaki J, Toyo-oka K, Wynshaw-Boris A, Ujike H, Inada T, Takao K, Miyakawa T, Ozaki N, Kaibuchi K, Iwata N (2008) Identification of YWHAE, a gene encoding 14-3-3epsilon, as a possible susceptibility gene for schizophrenia. Hum Mol Genet 17:3212–3222PubMedCrossRef Ikeda M, Hikita T, Taya S, Uraguchi-Asaki J, Toyo-oka K, Wynshaw-Boris A, Ujike H, Inada T, Takao K, Miyakawa T, Ozaki N, Kaibuchi K, Iwata N (2008) Identification of YWHAE, a gene encoding 14-3-3epsilon, as a possible susceptibility gene for schizophrenia. Hum Mol Genet 17:3212–3222PubMedCrossRef
go back to reference Iskander S, Walsh KA, Hammond RR (2004) Human CNS cultures exposed to HIV-1 gp120 reproduce dendritic injuries of HIV-1-associated dementia. J Neuroinflammation 1:7PubMedCrossRef Iskander S, Walsh KA, Hammond RR (2004) Human CNS cultures exposed to HIV-1 gp120 reproduce dendritic injuries of HIV-1-associated dementia. J Neuroinflammation 1:7PubMedCrossRef
go back to reference Kapasi AA, Fan S, Singhal PC (2001) Role of 14-3-3epsilon, c-Myc/Max, and Akt phosphorylation in HIV-1 gp 120-induced mesangial cell proliferation. Am J Physiol Renal Physiol 280:F333–F342PubMed Kapasi AA, Fan S, Singhal PC (2001) Role of 14-3-3epsilon, c-Myc/Max, and Akt phosphorylation in HIV-1 gp 120-induced mesangial cell proliferation. Am J Physiol Renal Physiol 280:F333–F342PubMed
go back to reference Kino T, Pavlakis GN (2004) Partner molecules of accessory protein Vpr of the human immunodeficiency virus type 1. DNA Cell Biol 23:193–205PubMedCrossRef Kino T, Pavlakis GN (2004) Partner molecules of accessory protein Vpr of the human immunodeficiency virus type 1. DNA Cell Biol 23:193–205PubMedCrossRef
go back to reference Kino T, De Martino MU, Charmandari E, Ichijo T, Outas T, Chrousos GP (2005a) HIV-1 accessory protein Vpr inhibits the effect of insulin on the Foxo subfamily of forkhead transcription factors by interfering with their binding to 14-3-3 proteins: potential clinical implications regarding the insulin resistance of HIV-1-infected patients. Diabetes 54:23–31PubMedCrossRef Kino T, De Martino MU, Charmandari E, Ichijo T, Outas T, Chrousos GP (2005a) HIV-1 accessory protein Vpr inhibits the effect of insulin on the Foxo subfamily of forkhead transcription factors by interfering with their binding to 14-3-3 proteins: potential clinical implications regarding the insulin resistance of HIV-1-infected patients. Diabetes 54:23–31PubMedCrossRef
go back to reference Kino T, Gragerov A, Valentin A, Tsopanomihalou M, Ilyina-Gragerova G, Erwin-Cohen R, Chrousos GP, Pavlakis GN (2005b) Vpr protein of human immunodeficiency virus type 1 binds to 14-3-3 proteins and facilitates complex formation with Cdc25C: implications for cell cycle arrest. J Virol 79:2780–2787PubMedCrossRef Kino T, Gragerov A, Valentin A, Tsopanomihalou M, Ilyina-Gragerova G, Erwin-Cohen R, Chrousos GP, Pavlakis GN (2005b) Vpr protein of human immunodeficiency virus type 1 binds to 14-3-3 proteins and facilitates complex formation with Cdc25C: implications for cell cycle arrest. J Virol 79:2780–2787PubMedCrossRef
go back to reference Kogan M, Rappaport J (2011) HIV-1 accessory protein Vpr: relevance in the pathogenesis of HIV and potential for therapeutic intervention. Retrovirology 8:25PubMedCrossRef Kogan M, Rappaport J (2011) HIV-1 accessory protein Vpr: relevance in the pathogenesis of HIV and potential for therapeutic intervention. Retrovirology 8:25PubMedCrossRef
go back to reference Lipton SA (1992) Requirement for macrophages in neuronal injury induced by HIV envelope protein gp120. Neuroreport 3:913–915PubMedCrossRef Lipton SA (1992) Requirement for macrophages in neuronal injury induced by HIV envelope protein gp120. Neuroreport 3:913–915PubMedCrossRef
go back to reference Luo X, Carlson KA, Wojna V, Mayo R, Biskup TM, Stoner J, Anderson J, Gendelman HE, Melendez LM (2003) Macrophage proteomic fingerprinting predicts HIV-1-associated cognitive impairment. Neurology 60:1931–1937PubMedCrossRef Luo X, Carlson KA, Wojna V, Mayo R, Biskup TM, Stoner J, Anderson J, Gendelman HE, Melendez LM (2003) Macrophage proteomic fingerprinting predicts HIV-1-associated cognitive impairment. Neurology 60:1931–1937PubMedCrossRef
go back to reference Lyons JL, Uno H, Ancuta P, Kamat A, Moore DJ, Singer EJ, Morgello S, Gabuzda D (2011) Plasma sCD14 is a biomarker associated with impaired neurocognitive test performance in attention and learning domains in HIV infection. J Acquir Immune Defic Syndr 57:371–379PubMedCrossRef Lyons JL, Uno H, Ancuta P, Kamat A, Moore DJ, Singer EJ, Morgello S, Gabuzda D (2011) Plasma sCD14 is a biomarker associated with impaired neurocognitive test performance in attention and learning domains in HIV infection. J Acquir Immune Defic Syndr 57:371–379PubMedCrossRef
go back to reference Matsuda N, Tanaka H, Yamazaki S, Suzuki J, Tanaka K, Yamada T, Masuda M (2006) HIV-1 Vpr induces G2 cell cycle arrest in fission yeast associated with Rad24/14-3-3-dependent, Chk1/Cds1-independent Wee1 upregulation. Microbes Infect 8:2736–2744PubMedCrossRef Matsuda N, Tanaka H, Yamazaki S, Suzuki J, Tanaka K, Yamada T, Masuda M (2006) HIV-1 Vpr induces G2 cell cycle arrest in fission yeast associated with Rad24/14-3-3-dependent, Chk1/Cds1-independent Wee1 upregulation. Microbes Infect 8:2736–2744PubMedCrossRef
go back to reference Mhawech-Fauceglia P, Herrmann FR, Andrews C, South S, Beck A, Lele S, Odunsi K (2009) 14-3-3sigma expression and prognostic value in patients with epithelial ovarian carcinoma: a high throughput tissue microarray analysis. Eur J Surg Oncol 35:763–767PubMedCrossRef Mhawech-Fauceglia P, Herrmann FR, Andrews C, South S, Beck A, Lele S, Odunsi K (2009) 14-3-3sigma expression and prognostic value in patients with epithelial ovarian carcinoma: a high throughput tissue microarray analysis. Eur J Surg Oncol 35:763–767PubMedCrossRef
go back to reference Mignon-Ravix C, Cacciagli P, El-Waly B, Moncla A, Milh M, Girard N, Chabrol B, Philip N, Villard L (2010) Deletion of YWHAE in a patient with periventricular heterotopias and pronounced corpus callosum hypoplasia. J Med Genet 47:132–136PubMedCrossRef Mignon-Ravix C, Cacciagli P, El-Waly B, Moncla A, Milh M, Girard N, Chabrol B, Philip N, Villard L (2010) Deletion of YWHAE in a patient with periventricular heterotopias and pronounced corpus callosum hypoplasia. J Med Genet 47:132–136PubMedCrossRef
go back to reference Morales D, Acevedo SF, Skolasky RL, Hechavarria R, Santiago S, De La Torre T, Maldonado E, Wojna V (2012a) Translational spatial task and its relationship to HIV-associated neurocognitive disorders and apolipoprotein E in HIV-seropositive women. J Neurovirol 18:488–502PubMedCrossRef Morales D, Acevedo SF, Skolasky RL, Hechavarria R, Santiago S, De La Torre T, Maldonado E, Wojna V (2012a) Translational spatial task and its relationship to HIV-associated neurocognitive disorders and apolipoprotein E in HIV-seropositive women. J Neurovirol 18:488–502PubMedCrossRef
go back to reference Morales D, Skoulakis EC, Acevedo SF (2012b) 14-3-3s are potential biomarkers for HIV-related neurodegeneration. J Neurovirol 18:341–353PubMedCrossRef Morales D, Skoulakis EC, Acevedo SF (2012b) 14-3-3s are potential biomarkers for HIV-related neurodegeneration. J Neurovirol 18:341–353PubMedCrossRef
go back to reference Rackstraw S (2011) HIV-related neurocognitive impairment—a review. Psychol Health Med 16:548–563PubMedCrossRef Rackstraw S (2011) HIV-related neurocognitive impairment—a review. Psychol Health Med 16:548–563PubMedCrossRef
go back to reference Shiga Y, Wakabayashi H, Miyazawa K, Kido H, Itoyama Y (2006) 14-3-3 protein levels and isoform patterns in the cerebrospinal fluid of Creutzfeldt–Jakob disease patients in the progressive and terminal stages. J Clin Neurosci 13:661–665PubMedCrossRef Shiga Y, Wakabayashi H, Miyazawa K, Kido H, Itoyama Y (2006) 14-3-3 protein levels and isoform patterns in the cerebrospinal fluid of Creutzfeldt–Jakob disease patients in the progressive and terminal stages. J Clin Neurosci 13:661–665PubMedCrossRef
go back to reference Torres M, Cartier L, Matamala JM, Hernandez N, Woehlbier U, Hetz C (2012) Altered Prion protein expression pattern in CSF as a biomarker for Creutzfeldt–Jakob disease. PLoS One 7:e36159PubMedCrossRef Torres M, Cartier L, Matamala JM, Hernandez N, Woehlbier U, Hetz C (2012) Altered Prion protein expression pattern in CSF as a biomarker for Creutzfeldt–Jakob disease. PLoS One 7:e36159PubMedCrossRef
go back to reference Ushijima H, Nishio O, Klocking R, Perovic S, Muller WE (1995) Exposure to gp120 of HIV-1 induces an increased release of arachidonic acid in rat primary neuronal cell culture followed by NMDA receptor-mediated neurotoxicity. Eur J Neurosci 7:1353–1359PubMedCrossRef Ushijima H, Nishio O, Klocking R, Perovic S, Muller WE (1995) Exposure to gp120 of HIV-1 induces an increased release of arachidonic acid in rat primary neuronal cell culture followed by NMDA receptor-mediated neurotoxicity. Eur J Neurosci 7:1353–1359PubMedCrossRef
go back to reference Vodicka MA, Koepp DM, Silver PA, Emerman M (1998) HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection. Genes Dev 12:175–185PubMedCrossRef Vodicka MA, Koepp DM, Silver PA, Emerman M (1998) HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection. Genes Dev 12:175–185PubMedCrossRef
go back to reference Wakabayashi H, Yano M, Tachikawa N, Oka S, Maeda M, Kido H (2001) Increased concentrations of 14-3-3 epsilon, gamma and zeta isoforms in cerebrospinal fluid of AIDS patients with neuronal destruction. Clin Chim Acta 312:97–105PubMedCrossRef Wakabayashi H, Yano M, Tachikawa N, Oka S, Maeda M, Kido H (2001) Increased concentrations of 14-3-3 epsilon, gamma and zeta isoforms in cerebrospinal fluid of AIDS patients with neuronal destruction. Clin Chim Acta 312:97–105PubMedCrossRef
go back to reference Wojna V, Skolasky RL, Hechavarria R, Mayo R, Selnes O, McArthur JC, Melendez LM, Maldonado E, Zorrilla CD, Garcia H, Kraiselburd E, Nath A (2006) Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment. J Neurovirol 12:356–364PubMedCrossRef Wojna V, Skolasky RL, Hechavarria R, Mayo R, Selnes O, McArthur JC, Melendez LM, Maldonado E, Zorrilla CD, Garcia H, Kraiselburd E, Nath A (2006) Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment. J Neurovirol 12:356–364PubMedCrossRef
go back to reference Wojna V, Robles L, Skolasky RL, Mayo R, Selnes O, de la Torre T, Maldonado E, Nath A, Melendez LM, Lasalde-Dominicci J (2007) Associations of cigarette smoking with viral immune and cognitive function in human immunodeficiency virus-seropositive women. J Neurovirol 13:561–568PubMedCrossRef Wojna V, Robles L, Skolasky RL, Mayo R, Selnes O, de la Torre T, Maldonado E, Nath A, Melendez LM, Lasalde-Dominicci J (2007) Associations of cigarette smoking with viral immune and cognitive function in human immunodeficiency virus-seropositive women. J Neurovirol 13:561–568PubMedCrossRef
go back to reference Xiao T, Ying W, Li L, Hu Z, Ma Y, Jiao L, Ma J, Cai Y, Lin D, Guo S, Han N, Di X, Li M, Zhang D, Su K, Yuan J, Zheng H, Gao M, He J, Shi S, Li W, Xu N, Zhang H, Liu Y, Zhang K, Gao Y, Qian X, Cheng S (2005) An approach to studying lung cancer-related proteins in human blood. Mol Cell Proteomics 4:1480–1486PubMedCrossRef Xiao T, Ying W, Li L, Hu Z, Ma Y, Jiao L, Ma J, Cai Y, Lin D, Guo S, Han N, Di X, Li M, Zhang D, Su K, Yuan J, Zheng H, Gao M, He J, Shi S, Li W, Xu N, Zhang H, Liu Y, Zhang K, Gao Y, Qian X, Cheng S (2005) An approach to studying lung cancer-related proteins in human blood. Mol Cell Proteomics 4:1480–1486PubMedCrossRef
go back to reference Zhao LJ, Mukherjee S, Narayan O (1994a) Biochemical mechanism of HIV-I Vpr function. Specific interaction with a cellular protein. J Biol Chem 269:15577–15582PubMed Zhao LJ, Mukherjee S, Narayan O (1994a) Biochemical mechanism of HIV-I Vpr function. Specific interaction with a cellular protein. J Biol Chem 269:15577–15582PubMed
go back to reference Zhao LJ, Wang L, Mukherjee S, Narayan O (1994b) Biochemical mechanism of HIV-1 Vpr function. Oligomerization mediated by the N-terminal domain. J Biol Chem 269:32131–32137PubMed Zhao LJ, Wang L, Mukherjee S, Narayan O (1994b) Biochemical mechanism of HIV-1 Vpr function. Oligomerization mediated by the N-terminal domain. J Biol Chem 269:32131–32137PubMed
Metadata
Title
YWHAE/14-3-3ε: a potential novel genetic risk factor and CSF biomarker for HIV neurocognitive impairment
Authors
Diana Morales
Rosa Hechavarria
Valerie Wojna
Summer F. Acevedo
Publication date
01-10-2013
Publisher
Springer US
Published in
Journal of NeuroVirology / Issue 5/2013
Print ISSN: 1355-0284
Electronic ISSN: 1538-2443
DOI
https://doi.org/10.1007/s13365-013-0200-z

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