Casein Kinase 2 Mediates HIV- and Opioid-Induced Pathologic Phosphorylation of TAR DNA Binding Protein 43 in the Basal Ganglia

References

• Alquezar C., Salado I. G., de la Encarnación A., Pérez D. I., Moreno F., Gil C., de Munain A. L., Martínez A., Martín-Requero Á (2016). Targeting TDP-43 phosphorylation by Casein Kinase-1δ inhibitors: A novel strategy for the treatment of frontotemporal dementia. Molecular Neurodegeneration, 11(1), 36. https://doi.org/10.1186/s13024-016-0102-7
   PubMedGoogle Scholar
• Arai T., Hasegawa M., Nonoka T., Kametani F., Yamashita M., Hosokawa M., Niizato K., Tsuchiya K., Kobayashi Z., Ikeda K., Yoshida M., Onaya M., Fujishiro H., Akiyama H. (2010). Phosphorylated and cleaved TDP-43 in ALS, FTLD and other neurodegenerative disorders and in cellular models of TDP-43 proteinopathy. Neuropathology: Official Journal of the Japanese Society of Neuropathology, 30(2), 170–181. https://doi.org/10.1111/j.1440-1789.2009.01089.x
   PubMed Web of Science ®Google Scholar
• Arai T., Mackenzie I. R. A., Hasegawa M., Nonoka T., Niizato K., Tsuchiya K., Iritani S., Onaya M., Akiyama H. (2009). Phosphorylated TDP-43 in Alzheimer’s disease and dementia with Lewy bodies. Acta Neuropathologica, 117(2), 125–136. https://doi.org/10.1007/s00401-008-0480-1
   PubMed Web of Science ®Google Scholar
• Barmada S. J., Skibinski G., Korb E., Rao E. J., Wu J. Y., Finkbeiner S. (2010). Cytoplasmic mislocalization of TDP-43 is toxic to neurons and enhanced by a mutation associated with familial amyotrophic lateral sclerosis. Journal of Neuroscience, 30(2), 639–649. https://doi.org/10.1523/JNEUROSCI.4988-09.2010
   PubMed Web of Science ®Google Scholar
• Berger J. R., Arendt G. (2000). HIV Dementia: The role of the basal ganglia and dopaminergic systems. J Psychopharmacol (Oxford), 14(3), 214–221. https://doi.org/10.1177/026988110001400304
   PubMed Web of Science ®Google Scholar
• Bhargavan B., Woollard S. M., McMillan J. E., Kanmogne G. D. (2021). CCR5 Antagonist reduces HIV-induced amyloidogenesis, tau pathology, neurodegeneration, and blood-brain barrier alterations in HIV-infected hu-PBL-NSG mice. Molecular Neurodegeneration, 16(1), 78. https://doi.org/10.1186/s13024-021-00500-0
   PubMed Web of Science ®Google Scholar
• Brady O. A., Meng P., Zheng Y., Mao Y., Hu F. (2011). Regulation of TDP-43 aggregation by phosphorylation and p62/SQSTM1. Journal of Neurochemistry, 116(2), 248–259. https://doi.org/10.1111/j.1471-4159.2010.07098.x
   PubMed Web of Science ®Google Scholar
• Brown L. A. M., Scarola J., Smith A. J., Sanberg P. R., Tan J., Giunta B. (2014). The role of tau protein in HIV-associated neurocognitive disorders. Molecular Neurodegeneration, 9(1), 40. https://doi.org/10.1186/1750-1326-9-40
   PubMedGoogle Scholar
• Bruce-Keller A. J., Turchan-Cholewo J., Smart E. J., Geurin T., Chauhan A., Reid R., Xu R., Nath A., Knapp P. E., Hauser K. F. (2008). Morphine causes rapid increases in glial activation and neuronal injury in the striatum of inducible HIV-1 Tat transgenic mice. Glia, 56(13), 1414–1427. https://doi.org/10.1002/glia.20708
   PubMed Web of Science ®Google Scholar
• Carlomagno Y., Zhang Y., Davis M., Lin W.-L., Cook C., Dunmore J., Tay W., Menkosky K., Cao X., Petrucelli L., Deture M. (2014). Casein kinase II induced polymerization of soluble TDP-43 into filaments is inhibited by heat shock proteins. PLoS One, 9(3), e90452. https://doi.org/10.1371/journal.pone.0090452
   PubMed Web of Science ®Google Scholar
• Chakrabarti S., Liu N.-J., Gintzler A. R. (2020). Phosphorylation of unique C-terminal sites of the mu-opioid receptor variants 1B2 and 1C1 influences their Gs association following chronic morphine. Journal of Neurochemistry, 152(4), 449–467. https://doi.org/10.1111/jnc.14863
   PubMed Web of Science ®Google Scholar
• Chaudhry A., Rubin R. P. (1990). Mediators of Ca2+-dependent secretion. Environmental Health Perspectives, 84, 35–39. https://doi.org/10.1289/ehp.908435
   PubMed Web of Science ®Google Scholar
• Davison S. E., Aylward E. H., McArthur J. C., Selnes O. A., Lyketsos C., Barta P. E., Pearlson G. D. (1997). A quantitative MRI study of the basal ganglia in depression in HIV seropositive men. Journal of Neuro-Aids, 1(3), 29–41. https://doi.org/10.1300/J128v01n03_02
   PubMedGoogle Scholar
• Douville R. N., Nath A. (2017). Human endogenous retrovirus-K and TDP-43 expression bridges ALS and HIV neuropathology. Frontiers in Microbiology, 8, 1986. https://doi.org/10.3389/fmicb.2017.01986
   PubMed Web of Science ®Google Scholar
• Eck R. J., Kraemer B. C., Liachko N. F. (2021). Regulation of TDP-43 phosphorylation in aging and disease. Geroscience, 43(4), 1605–1614. https://doi.org/10.1007/s11357-021-00383-5
   PubMed Web of Science ®Google Scholar
• El-Hage N., Gurwell J. A., Singh I. N., Knapp P. E., Nath A., Hauser K. F. (2005). Synergistic increases in intracellular Ca2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 Tat. Glia, 50(2), 91–106. https://doi.org/10.1002/glia.20148
   PubMed Web of Science ®Google Scholar
• Fitting S., Knapp P. E., Zou S., Marks W. D., Bowers M. S., Akbarali H. I., Hauser K. F. (2014). Interactive HIV-1 Tat and morphine-induced synaptodendritic injury is triggered through focal disruptions in Na+ influx, mitochondrial instability, and Ca2+ overload. Journal of Neuroscience, 34(38), 12850–12864. https://doi.org/10.1523/JNEUROSCI.5351-13.2014
   PubMed Web of Science ®Google Scholar
• Fitting S., McRae M., Hauser K. F. (2020). Opioid and neuroHIV comorbidity - current and future perspectives. Journal of Neuroimmune Pharmacology: The Official Journal of the Society on NeuroImmune Pharmacology, 15(4), 584–627. https://doi.org/10.1007/s11481-020-09941-8
   PubMed Web of Science ®Google Scholar
• Fitting S., Xu R., Bull C., Buch S. K., El-Hage N., Nath A., Knapp P. E., Hauser K. F. (2010). Interactive comorbidity between opioid drug abuse and HIV-1 Tat: Chronic exposure augments spine loss and sublethal dendritic pathology in striatal neurons. American Journal of Pathology, 177(3), 1397–1410. https://doi.org/10.2353/ajpath.2010.090945
   PubMed Web of Science ®Google Scholar
• Goossens J., Vanmechelen E., Trojanowski J. Q., Lee V. M. Y., Van Broeckhoven C., van der Zee J., Engelborghs S. (2015). TDP-43 as a possible biomarker for frontotemporal lobar degeneration: A systematic review of existing antibodies. Acta Neuropathologica Communications, 3(1), 15. https://doi.org/10.1186/s40478-015-0195-1
   PubMedGoogle Scholar
• Guerrero E. N., Mitra J., Wang H., Rangaswamy S., Hegde P. M., Basu P., Rao K. S., Hegde M. L. ( 2019a). Amyotrophic lateral sclerosis-associated TDP-43 mutation Q331K prevents nuclear translocation of XRCC4-DNA ligase 4 complex and is linked to genome damage-mediated neuronal apoptosis. Human Molecular Genetics, 28(15), 2459–2476. https://doi.org/10.1093/hmg/ddz062
   PubMed Web of Science ®Google Scholar
• Guerrero E. N., Mitra J., Wang H., Rangaswamy S., Hegde P. M., Basu P., Rao K. S., Hegde M. L. ( 2019b). Amyotrophic lateral sclerosis-associated TDP-43 mutation Q331K prevents nuclear translocation of XRCC4-DNA ligase 4 complex and is linked to genome damage-mediated neuronal apoptosis. Human Molecular Genetics, 28(18), 3161–3162. https://doi.org/10.1093/hmg/ddz141
   PubMed Web of Science ®Google Scholar
• Hasegawa M., Arai T., Nonaka T., Kametani F., Yoshida M., Hashizume Y., Beach T. G., Buratti E., Baralle F., Morita M., Nakano I., Oda T., Tsuchiya K., Akiyama H. (2008). Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Annals of Neurology, 64(1), 60–70. https://doi.org/10.1002/ana.21425
   PubMed Web of Science ®Google Scholar
• Hauser K. F., El-Hage N., Buch S., Nath A., Tyor W. R., Bruce-Keller A. J., Knapp P. E. (2006). Impact of opiate-HIV-1 interactions on neurotoxic signaling. Journal of Neuroimmune Pharmacology: The Official Journal of the Society on NeuroImmune Pharmacology, 1(1), 98–105. https://doi.org/10.1007/s11481-005-9000-4
   PubMed Web of Science ®Google Scholar
• Hauser K. F., Hahn Y. K., Adjan V. V., Zou S., Buch S. K., Nath A., Bruce-Keller A. J., Knapp P. E. (2009). HIV-1 Tat and morphine have interactive effects on oligodendrocyte survival and morphology. Glia, 57(2), 194–206. https://doi.org/10.1002/glia.20746
   PubMed Web of Science ®Google Scholar
• Hauser K. F., Stiene-Martin A., Mattson M. P., Elde R. P., Ryan S. E., Godleske C. C. (1996). μ-Opioid receptor-induced Ca2+ mobilization and astroglial development: Morphine inhibits DNA synthesis and stimulates cellular hypertrophy through a Ca2+-dependent mechanism. Brain Research, 720(1-2), 191–203. https://doi.org/10.1016/0006-8993(96)00103-5
   PubMed Web of Science ®Google Scholar
• Henderson L. J., Johnson T. P., Smith B. R., Reoma L. B., Santamaria U. A., Bachani M., Demarino C., Barclay R. A., Snow J., Sacktor N., Mcarthur J., Letendre S., Steiner J., Kashanchi F., Nath A. (2019). Presence of Tat and transactivation response element in spinal fluid despite antiretroviral therapy. AIDS (London, England), 33(Suppl 2), S145–S157. https://doi.org/10.1097/QAD.0000000000002268
   PubMedGoogle Scholar
• Huang W., Zhou Y., Tu L., Ba Z., Huang J., Huang N., Luo Y. (2020). TDP-43: From Alzheimer’s disease to limbic-predominant age-related TDP-43 encephalopathy. Frontiers in Molecular Neuroscience, 13, 26. https://doi.org/10.3389/fnmol.2020.00026
   PubMed Web of Science ®Google Scholar
• Jang S. W., Hwang S. S., Kim H. S., Lee K. O., Kim M. K., Lee W., Kim K., Lee G. R. (2017). Casein kinase 2 is a critical determinant of the balance of Th17 and Treg cell differentiation. Experimental and Molecular Medicine, 49(9), e375. https://doi.org/10.1038/emm.2017.132
   PubMed Web of Science ®Google Scholar
• Jiang L.-L., Xue W., Hong J.-Y., Zhang J.-T., Li M.-J., Yu S.-N., He J.-H., Hu H.-Y. (2017). The N-terminal dimerization is required for TDP-43 splicing activity. Scientific Reports, 7(1), 6196. https://doi.org/10.1038/s41598-017-06263-3
   PubMedGoogle Scholar
• Jiang L.-L., Zhao J., Yin X.-F., He W.-T., Yang H., Che M.-X., Hu H.-Y. (2016). Two mutations G335D and Q343R within the amyloidogenic core region of TDP-43 influence its aggregation and inclusion formation. Scientific Reports, 6(1), 23928. https://doi.org/10.1038/srep23928
   PubMedGoogle Scholar
• Jo M., Lee S., Jeon Y.-M., Kim S., Kwon Y., Kim H.-J. (2020). The role of TDP-43 propagation in neurodegenerative diseases: Integrating insights from clinical and experimental studies. Experimental and Molecular Medicine, 52(10), 1652–1662. https://doi.org/10.1038/s12276-020-00513-7
   PubMed Web of Science ®Google Scholar
• Johnson T. P., Patel K., Johnson K. R., Maric D., Calabresi P. A., Hasbun R., Nath A. (2013). Induction of IL-17 and nonclassical T-cell activation by HIV-Tat protein. Proceedings of the National Academy of Sciences of the USA, 110(33), 13588–13593. https://doi.org/10.1073/pnas.1308673110
   PubMed Web of Science ®Google Scholar
• Josephs K. A., Whitwell J. L., Weigand S. D., Murray M. E., Tosakulwong N., Liesinger A. M., Petrucelli L., Senjem M. L., Knopman D. S., Boeve B. F., Ivnik R. J., Smith G. E., Jack C. R., Parisi J. E., Petersen R. C., Dickson D. W. (2014). TDP-43 is a key player in the clinical features associated with Alzheimer’s disease. Acta Neuropathologica, 127(6), 811–824. https://doi.org/10.1007/s00401-014-1269-z
   PubMed Web of Science ®Google Scholar
• Jucker M., Walker L. C. (2018). Propagation and spread of pathogenic protein assemblies in neurodegenerative diseases. Nature Neuroscience, 21(10), 1341–1349. https://doi.org/10.1038/s41593-018-0238-6
   PubMed Web of Science ®Google Scholar
• Jung E. B., Kim Y. J., Lee C. S. (2014). Casein kinase 2 inhibition attenuates cholesterol oxidation product-induced apoptosis by suppressing the activation of the mitochondrial pathway and the caspase-8- and bid-dependent pathways. Neurochemistry International, 65, 30–39. https://doi.org/10.1016/j.neuint.2013.12.010
   PubMed Web of Science ®Google Scholar
• Kadri F., Pacifici M., Wilk A., Parker-Struckhoff A., Del Valle L., Hauser K. F., Knapp P. E., Parsons C., Jeansonne D., Lassak A., Peruzzi F. (2015). HIV-1-Tat protein inhibits SC35-mediated Tau Exon 10 inclusion through up-regulation of DYRK1A kinase. Journal of Biological Chemistry, 290(52), 30931–30946. https://doi.org/10.1074/jbc.M115.675751
   PubMed Web of Science ®Google Scholar
• Latimer C. S., Liachko N. F. (2021). Tau and TDP-43 synergy: A novel therapeutic target for sporadic late-onset Alzheimer’s disease. Geroscience, 43(3), 1627–1634. https://doi.org/10.1007/s11357-021-00407-0
   PubMedGoogle Scholar
• Latimer C. S., Stair J. G., Hincks J. C., Currey H. N., Bird T. D., Keene C. D., Kraemer B. C., Liachko N. F. (2022). TDP-43 promotes tau accumulation and selective neurotoxicity in bigenic Caenorhabditis elegans. Disease Models & Mechanisms, 15(4), dmm049323. https://doi.org/10.1242/dmm.049323
   PubMed Web of Science ®Google Scholar
• Lee H. R., Shin H. K., Park S. Y., Kim H. Y., Lee W. S., Rhim B. Y., Hong K. W., Kim C. D. (2014). Attenuation of β-amyloid-induced tauopathy via activation of CK2α/SIRT1: Targeting for cilostazol. Journal of Neuroscience Research, 92(2), 206–217. https://doi.org/10.1002/jnr.23310
   PubMed Web of Science ®Google Scholar
• Montalbano M., McAllen S., Cascio F. L., Sengupta U., Garcia S., Bhatt N., Ellsworth A., Heidelman E. A., Johnson O. D., Doskocil S., Kayed R. (2020). TDP-43 and Tau oligomers in Alzheimer’s disease, amyotrophic lateral sclerosis, and frontotemporal dementia. Neurobiology of Disease, 146, 105130. https://doi.org/10.1016/j.nbd.2020.105130
   PubMed Web of Science ®Google Scholar
• Morrison W. J., Shukla S. D. (1988). Desensitization of receptor-coupled activation of phosphoinositide-specific phospholipase C in platelets: Evidence for distinct mechanisms for platelet-activating factor and thrombin. Molecular Pharmacology, 33(1), 58–63.
   PubMed Web of Science ®Google Scholar
• Murphy A., Barbaro J., Martínez-Aguado P., Chilunda V., Jaureguiberry-Bravo M., Berman J. W. (2019). The effects of opioids on HIV neuropathogenesis. Frontiers in Immunology, 10, 2445. https://doi.org/10.3389/fimmu.2019.02445
   PubMed Web of Science ®Google Scholar
• Nass S. R., Lark A. R. S., Hahn Y. K., McLane V. D., Ihrig T. M., Contois L., Napier T. C., Knapp P. E., Hauser K. F. (2021). HIV-1 Tat and morphine decrease murine inter-male social interactions and associated oxytocin levels in the prefrontal cortex, amygdala, and hypothalamic paraventricular nucleus. Hormones and Behavior, 133, 105008. https://doi.org/10.1016/j.yhbeh.2021.105008
   PubMed Web of Science ®Google Scholar
• Nass S. R., Ohene-Nyako M., Hahn Y. K., Knapp P. E., Hauser K. F. (2022). Neurodegeneration within the amygdala is differentially induced by opioid and HIV-1 Tat exposure. Frontiers in Neuroscience, 16, 804774. https://doi.org/10.3389/fnins.2022.804774
   PubMed Web of Science ®Google Scholar
• Nelson P. T., et al. (2019). Limbic-predominant age-related TDP-43 encephalopathy (LATE): Consensus working group report. Brain, 142(6), 1503–1527. https://doi.org/10.1093/brain/awz099
   PubMed Web of Science ®Google Scholar
• Neumann M., Kwong L. K., Truax A. C., Vanmassenhove B., Kretzschmar H. A., Van Deerlin V. M., Clark C. M., Grossman M., Miller B. L., Trojanowski J. Q., Lee V. M.-Y. (2007). TDP-43-positive white matter pathology in frontotemporal lobar degeneration with ubiquitin-positive inclusions. Journal of Neuropathology & Experimental Neurology, 66(3), 177–183. https://doi.org/10.1097/01.jnen.0000248554.45456.58
   PubMed Web of Science ®Google Scholar
• Newsome S. D., Johnson E., Pardo C., McArthur J. C., Nath A. (2011). Fulminant encephalopathy with basal ganglia hyperintensities in HIV-infected drug users. Neurology, 76(9), 787–794. https://doi.org/10.1212/WNL.0b013e31820e7b4e
   PubMed Web of Science ®Google Scholar
• Nonaka T., Suzuki G., Tanaka Y., Kametani F., Hirai S., Okado H., Miyashita T., Saitoe M., Akiyama H., Masai H., Hasegawa M. (2016). Phosphorylation of TAR DNA-binding protein of 43 kDa (TDP-43) by truncated casein kinase 1δ triggers mislocalization and accumulation of TDP-43. Journal of Biological Chemistry, 291(11), 5473–5483. https://doi.org/10.1074/jbc.M115.695379
   PubMed Web of Science ®Google Scholar
• Ohene-Nyako M., Nass S. R., Hahn Y. K., Knapp P. E., Hauser K. F. (2021). Morphine and HIV-1 Tat interact to cause region-specific hyperphosphorylation of tau in transgenic mice. Neuroscience Letters, 741, 135502. https://doi.org/10.1016/j.neulet.2020.135502
   PubMed Web of Science ®Google Scholar
• Oinuma I., Ito Y., Katoh H., Negishi M. (2010). Semaphorin 4D/Plexin-B1 stimulates PTEN activity through R-Ras GTPase-activating protein activity, inducing growth cone collapse in hippocampal neurons. Journal of Biological Chemistry, 285(36), 28200–28209. https://doi.org/10.1074/jbc.M110.147546
   PubMed Web of Science ®Google Scholar
• Ou S. H., Wu F., Harrich D., García-Martínez L. F., Gaynor R. B. (1995). Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. Journal of Virology, 69(6), 3584–3596. https://doi.org/10.1128/jvi.69.6.3584-3596.1995
   PubMed Web of Science ®Google Scholar
• Peng C., Trojanowski J. Q., Lee V. M.-Y. (2020). Protein transmission in neurodegenerative disease. Nature Reviews. Neurology, 16(4), 199–212. https://doi.org/10.1038/s41582-020-0333-7
   PubMed Web of Science ®Google Scholar
• Pinna L. A. (2002). Protein kinase CK2: A challenge to canons. Journal of Cell Science, 115(Pt 20), 3873–3878. https://doi.org/10.1242/jcs.00074
   PubMed Web of Science ®Google Scholar
• Rayaprolu S., Fujioka S., Traynor S., Soto-Ortolaza A. I., Petrucelli L., Dickson D. W., Rademakers R., Boylan K. B., Graff-Radford N. R., Uitti R. J., Wszolek Z. K., Ross O. A. (2013). TARDBP Mutations in Parkinson’s disease. Parkinsonism & Related Disorders, 19(3), 312–315. https://doi.org/10.1016/j.parkreldis.2012.11.003
   PubMed Web of Science ®Google Scholar
• Ren Y., Li S., Chen S., Sun X., Yang F., Wang H., Li M., Cui F., Huang X. (2021). TDP-43 and phosphorylated TDP-43 levels in paired plasma and CSF samples in amyotrophic lateral sclerosis. Frontiers in Neurology, 12, 663637. https://doi.org/10.3389/fneur.2021.663637
   PubMed Web of Science ®Google Scholar
• Sanna P. P., Fu Y., Masliah E., Lefebvre C., Repunte-Canonigo V. (2021). Central nervous system (CNS) transcriptomic correlates of human immunodeficiency virus (HIV) brain RNA load in HIV-infected individuals. Scientific Reports, 11(1), 12176. https://doi.org/10.1038/s41598-021-88052-7
   PubMed Web of Science ®Google Scholar
• Solyakov L., Cain K., Tracey B. M., Jukes R., Riley A. M., Potter B. V. L., Tobin A. B. (2004). Regulation of casein kinase-2 (CK2) activity by inositol phosphates. Journal of Biological Chemistry, 279(42), 43403–43410. https://doi.org/10.1074/jbc.M403239200
   PubMed Web of Science ®Google Scholar
• Steinacker P., Barschke P., Otto M. (2019). Biomarkers for diseases with TDP-43 pathology. Molecular and Cellular Neuroscience, 97, 43–59. https://doi.org/10.1016/j.mcn.2018.10.003
   PubMed Web of Science ®Google Scholar
• Tomé S. O., Vandenberghe R., Ospitalieri S., Van Schoor E., Tousseyn T., Otto M., von Arnim C. A. F., Thal D. R. (2020). Distinct molecular patterns of TDP-43 pathology in Alzheimer’s disease: Relationship with clinical phenotypes. Acta Neuropathologica Communications, 8(1), 61. https://doi.org/10.1186/s40478-020-00934-5
   PubMed Web of Science ®Google Scholar
• Tremblay C., St-Amour I., Schneider J., Bennett D. A., Calon F. (2011). Accumulation of transactive response DNA binding protein 43 in mild cognitive impairment and Alzheimer disease. Journal of Neuropathology & Experimental Neurology, 70(9), 788–798. https://doi.org/10.1097/NEN.0b013e31822c62cf
   PubMed Web of Science ®Google Scholar
• Tsoi P. S., Choi K.-J., Leonard P. G., Sizovs A., Moosa M. M., MacKenzie K. R., Ferreon J. C., Ferreon A. C. M. (2017). The N-terminal domain of ALS-linked TDP-43 assembles without misfolding. Angewandte Chemie International Edition, 56(41), 12590–12593. https://doi.org/10.1002/anie.201706769
   PubMed Web of Science ®Google Scholar
• Uhlen M., Bandrowski A., Carr S., Edwards A., Ellenberg J., Lundberg E., Rimm D. L., Rodriguez H., Hiltke T., Snyder M., Yamamoto T. (2016). A proposal for validation of antibodies. Nature Methods, 13(10), 823–827. https://doi.org/10.1038/nmeth.3995
   PubMed Web of Science ®Google Scholar
• von Giesen H. J., Wittsack H. J., Wenserski F., Köller H., Hefter H., Arendt G. (2001). Basal ganglia metabolite abnormalities in minor motor disorders associated with human immunodeficiency virus type 1. Archives of Neurology, 58(8), 1281–1286. https://doi.org/10.1001/archneur.58.8.1281
   PubMedGoogle Scholar
• Wager T. T., et al. (2014). Casein kinase 1δ/ε inhibitor PF-5006739 attenuates opioid drug-seeking behavior. ACS Chemical Neuroscience, 5(12), 1253–1265. https://doi.org/10.1021/cn500201x
   PubMed Web of Science ®Google Scholar
• Wang W., Arakawa H., Wang L., Okolo O., Siedlak S. L., Jiang Y., Gao J., Xie F., Petersen R. B., Wang X. (2017). Motor-Coordinative and cognitive dysfunction caused by mutant TDP-43 could be reversed by inhibiting its mitochondrial localization. Molecular Therapy, 25(1), 127–139. https://doi.org/10.1016/j.ymthe.2016.10.013
   PubMed Web of Science ®Google Scholar
• Wang W., Wang L., Lu J., Siedlak S. L., Fujioka H., Liang J., Jiang S., Ma X., Jiang Z., da Rocha E. L., Sheng M., Choi H., Lerou P. H., Li H., Wang X. (2016). The inhibition of TDP-43 mitochondrial localization blocks its neuronal toxicity. Nature Medicine, 22(8), 869–878. https://doi.org/10.1038/nm.4130
   PubMed Web of Science ®Google Scholar
• Wen B. G., Pletcher M. T., Warashina M., Choe S. H., Ziaee N., Wiltshire T., Sauer K., Cooke M. P. (2004). Inositol (1,4,5) trisphosphate 3 kinase B controls positive selection of T cells and modulates Erk activity. Proceedings of the National Academy of Sciences of the USA, 101(15), 5604–5609. https://doi.org/10.1073/pnas.0306907101
   PubMed Web of Science ®Google Scholar
• Wu C.-C., Jin L.-W., Wang I.-F., Wei W.-Y., Ho P.-C., Liu Y.-C., Tsai K.-J. (2020). HDAC1 Dysregulation induces aberrant cell cycle and DNA damage in progress of TDP-43 proteinopathies. EMBO Molecular Medicine, 12(6), e10622. https://doi.org/10.15252/emmm.201910622
   PubMed Web of Science ®Google Scholar
• Zou S., Fitting S., Hahn Y.-K., Welch S. P., El-Hage N., Hauser K. F., Knapp P. E. (2011). Morphine potentiates neurodegenerative effects of HIV-1 Tat through actions at μ-opioid receptor-expressing glia. Brain, 134(Pt 12), 3616–3631. https://doi.org/10.1093/brain/awr281
   PubMedGoogle Scholar