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Clathrin-nanoparticles deliver BDNF to hippocampus and enhance neurogenesis, synaptogenesis and cognition in HIV/neuroAIDS mouse model

  • Illum, L. Nasal drug delivery—recent developments and future prospects. J. Control Release 161, 254–263 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Gomez, D., Martinez, J. A., Hanson, L. R., Frey, W. H. 2nd & Toth, C. C. Intranasal treatment of neurodegenerative diseases and stroke. Front. Biosci. 4, 74–89 (2012).

    Google Scholar 

  • Zhu, J., Jiang, Y., Xu, G. & Liu, X. Intranasal administration: a potential solution for cross-BBB delivering neurotrophic factors. Histol. Histopathol. 27, 537–548 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Vitaliano, G. D., Vitaliano, F., Rios, J. D., Renshaw, P. F. & Teicher, M. H. New clathrin-based nanoplatforms for magnetic resonance imaging. PLoS ONE 7, e35821 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Brodsky, F. M. Diversity of clathrin function: new tricks for an old protein. Annu. Rev. Cell Dev. Biol. 28, 309–336 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Kirchhausen, T., Owen, D. & Harrison, S. C. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb. Perspect. Biol. 6, a016725 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Preston, J. E., Joan Abbott, N. & Begley, D. J. Transcytosis of macromolecules at the blood-brain barrier. Adv. Pharmacol. 71, 147–163 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Granseth, B., Odermatt, B., Royle, S. J. & Lagnado, L. Clathrin-mediated endocytosis: the physiological mechanism of vesicle retrieval at hippocampal synapses. J. Physiol. 585, 681–686 (2007).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mills, I. G. The interplay between clathrin-coated vesicles and cell signalling. Semin. Cell Dev. Biol. 18, 459–470 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Royle, S. J. The cellular functions of clathrin. Cell. Mol. Life Sci. 63, 1823–1832 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baba, T. et al. Clathrin-dependent and clathrin-independent endocytosis are differentially sensitive to insertion of poly (ethylene glycol)-derivatized cholesterol in the plasma membrane. Traffic 2, 501–512 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Schmid, S. L., Matsumoto, A. K. & Rothman, J. E. A domain of clathrin that forms coats. Proc. Natl Acad. Sci. USA 79, 91–95 (1982).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bartus, R. T. & Johnson, E. M., Jr. Clinical tests of neurotrophic factors for human neurodegenerative diseases, part 1: Where have we been and what have we learned? Neurobiol. Dis. 97, 156–168 (2017).

  • Lu, B., Nagappan, G., Guan, X., Nathan, P. J. & Wren, P. BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nat. Rev. Neurosci. 14, 401–416 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Ghosh, A., Carnahan, J. & Greenberg, M. E. Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263, 1618–1623 (1994).

    CAS 
    PubMed 

    Google Scholar 

  • Horch, H. W. & Katz, L. C. BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat. Neurosci. 5, 1177–1184 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Zagrebelsky, M. & Korte, M. Form follows function: BDNF and its involvement in sculpting the function and structure of synapses. Neuropharmacology 76, 628–638 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Mattson, M. P., Maudsley, S. & Martin, B. BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 27, 589–594 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • Leal, G., Afonso, P. M., Salazar, I. L. & Duarte, C. B. Regulation of hippocampal synaptic plasticity by BDNF. Brain Res. 1621, 82–101 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Song, M., Martinowich, K. & Lee, F. S. BDNF at the synapse: why location matters. Mol. Psychiatry 22, 1370–1375 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yamada, K., Mizuno, M. & Nabeshima, T. Role for brain-derived neurotrophic factor in learning and memory. Life Sci. 70, 735–744 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Cunha, C., Brambilla, R. & Thomas, K. L. A simple role for BDNF in learning and memory? Front. Mol. Neurosci. 3, 1 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bekinschtein, P., Cammarota, M. & Medina, J. H. BDNF and memory processing. Neuropharmacology 76, 677–683 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Andero, R., Choi, D. C. & Ressler, K. J. BDNF-TrkB receptor regulation of distributed adult neural plasticity, memory formation, and psychiatric disorders. Prog. Mol. Biol. Transl. Sci. 122, 169–192 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Nagahara, A. H. et al. Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer’s disease. Nat. Med. 15, 331–337 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nagahara, A. H. & Tuszynski, M. H. Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat. Rev. Drug Discov. 10, 209–219 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • Poduslo, J. F. & Curran, G. L. Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF. Brain Res. Mol. Brain Res. 36, 280–286 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • Pardridge, W. M., Kang, Y. S. & Buciak, J. L. Transport of human recombinant brain-derived neurotrophic factor (BDNF) through the rat blood-brain barrier in vivo using vector-mediated peptide drug delivery. Pharm. Res. 11, 738–746 (1994).

    CAS 
    PubMed 

    Google Scholar 

  • Alcala-Barraza, S. R. et al. Intranasal delivery of neurotrophic factors BDNF, CNTF, EPO, and NT-4 to the CNS. J. Drug Target. 18, 179–190 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Scharfman, H. et al. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192, 348–356 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Bekinschtein, P. et al. BDNF is essential to promote persistence of long-term memory storage. Proc. Natl Acad. Sci. USA 105, 2711–2716 (2008).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kuipers, S. D. et al. BDNF-induced LTP is associated with rapid Arc/Arg3.1-dependent enhancement in adult hippocampal neurogenesis. Sci. Rep. 6, 21222 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Blurton-Jones, M. et al. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc. Natl Acad. Sci. USA 106, 13594–13599 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, W. et al. Neural stem cell transplants improve cognitive function without altering amyloid pathology in an APP/PS1 double transgenic model of Alzheimer’s disease. Mol. Neurobiol. 50, 423–437 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Ando, S. et al. Animal model of dementia induced by entorhinal synaptic damage and partial restoration of cognitive deficits by BDNF and carnitine. J. Neurosci. Res. 70, 519–527 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Quesseveur, G. et al. BDNF overexpression in mouse hippocampal astrocytes promotes local neurogenesis and elicits anxiolytic-like activities. Transl. Psychiatry 3, e253 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sirianni, R. W., Olausson, P., Chiu, A. S., Taylor, J. R. & Saltzman, W. M. The behavioral and biochemical effects of BDNF containing polymers implanted in the hippocampus of rats. Brain Res. 1321, 40–50 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Angelov, B. et al. Multicompartment lipid cubic nanoparticles with high protein upload: millisecond dynamics of formation. ACS Nano 8, 5216–5226 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Chen, H. et al. Focused ultrasound-enhanced intranasal brain delivery of brain-derived neurotrophic factor. Sci. Rep. 6, 28599 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Geral, C., Angelova, A. & Lesieur, S. From molecular to nanotechnology strategies for delivery of neurotrophins: emphasis on brain-derived neurotrophic factor (BDNF). Pharmaceutics 5, 127–167 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, Y. & Pardridge, W. M. Blood-brain barrier targeting of BDNF improves motor function in rats with middle cerebral artery occlusion. Brain Res. 1111, 227–229 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Khalin, I. et al. Brain-derived neurotrophic factor delivered to the brain using poly (lactide-co-glycolide) nanoparticles improves neurological and cognitive outcome in mice with traumatic brain injury. Drug Deliv. 23, 3520–3528 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Jiang, Y. et al. Nanoformulation of brain-derived neurotrophic factor with target receptor-triggered-release in the central nervous system. Adv. Funct. Mater. 28, 1703982 (2018).

  • Ma, X. C. et al. Intranasal delivery of recombinant AAV containing BDNF fused with HA2TAT: a potential promising therapy strategy for major depressive disorder. Sci. Rep. 6, 22404 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kim, B. O. et al. 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, 1693–1707 (2003).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Langford, D. et al. Doxycycline-inducible and astrocyte-specific HIV-1 Tat transgenic mice (iTat) as an HIV/neuroAIDS model. J. Neurovirol. 24, 168–179 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • Mocchetti, I., Bachis, A., Campbell, L. A. & Avdoshina, V. Implementing neuronal plasticity in NeuroAIDS: the experience of brain-derived neurotrophic factor and other neurotrophic factors. J. NeuroImmune Pharmacol. 9, 80–91 (2014).

    PubMed 

    Google Scholar 

  • Bachis, A., Avdoshina, V., Zecca, L., Parsadanian, M. & Mocchetti, I. Human immunodeficiency virus type 1 alters brain-derived neurotrophic factor processing in neurons. J. Neurosci. 32, 9477–9484 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Albrecht, D. et al. Trophic factors in cerebrospinal fluid and spinal cord of patients with tropical spastic paraparesis, HIV, and Creutzfeldt-Jakob disease. AIDS Res. Hum. Retroviruses 22, 248–254 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Meeker, R. B., Poulton, W., Markovic-Plese, S., Hall, C. & Robertson, K. Protein changes in CSF of HIV-infected patients: evidence for loss of neuroprotection. J. Neurovirol. 17, 258–273 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fields, J. et al. HIV-1 Tat alters neuronal autophagy by modulating autophagosome fusion to the lysosome: implications for HIV-associated neurocognitive disorders. J. Neurosci. 35, 1921–1938 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • King, J. E., Eugenin, E. A., Buckner, C. M. & Berman, J. W. HIV tat and neurotoxicity. Microbes Infect. 8, 1347–1357 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Hudson, L. et al. Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J. Neurovirol. 6, 145–155 (2000).

    CAS 
    PubMed 

    Google Scholar 

  • Henderson, L. J. et al. Presence of Tat and transactivation response element in spinal fluid despite antiretroviral therapy. Aids 33, S145–S157 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Jones, M., Olafson, K., Del Bigio, M. R., Peeling, J. & Nath, A. Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J. Neuropathol. Exp. Neurol. 57, 563–570 (1998).

    CAS 
    PubMed 

    Google Scholar 

  • McLaughlin, J. P. et al. Conditional human immunodeficiency virus transactivator of transcription protein expression induces depression-like effects and oxidative stress. Biol. Psychiatry Cogn Neurosci Neuroimaging 2, 599–609 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Carey, A. N. et al. Conditional Tat protein expression in the GT-tg bigenic mouse brain induces gray matter density reductions. Prog. Neuro-Psychopharmacol. 43, 49–54 (2013).

    CAS 

    Google Scholar 

  • Rahimian, P. & He, J. J. HIV-1 Tat-shortened neurite outgrowth through regulation of microRNA-132 and its target gene expression. J. Neuroinflamm. 13, 247 (2016).

    Google Scholar 

  • Carey, A. N., Sypek, E. I., Singh, H. D., Kaufman, M. J. & McLaughlin, J. P. Expression of HIV-Tat protein is associated with learning and memory deficits in the mouse. Behav. Brain Res. 229, 48–56 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Marks, W. D. et al. HIV-1 Tat causes cognitive deficits and selective loss of parvalbumin, somatostatin, and neuronal nitric oxide synthase expressing hippocampal CA1 interneuron subpopulations. J. Neurovirol. 22, 747–762 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fitting, S. et al. Synaptic dysfunction in the hippocampus accompanies learning and memory deficits in human immunodeficiency virus type-1 Tat transgenic mice. Biol. Psychiatry 73, 443–453 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Ramirez, S. H. et al. Neurotrophins prevent HIV Tat-induced neuronal apoptosis via a nuclear factor-kappaB (NF-kappaB)-dependent mechanism. J. Neurochem. 78, 874–889 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Fujimura, R. K. et al. HIV-1 proviral DNA load across neuroanatomic regions of individuals with evidence for HIV-1-associated dementia. JAIDS 16, 146–152 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Wiley, C. A. et al. Distribution of brain HIV load in AIDS. Brain Pathol. 8, 277–284 (1998).

    CAS 
    PubMed 

    Google Scholar 

  • Anthony, I. C., Ramage, S. N., Carnie, F. W., Simmonds, P. & Bell, J. E. Influence of HAART on HIV-related CNS disease and neuroinflammation. J. Neuropathol. Exp. Neurol. 64, 529–536 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Nir, T. M. et al. Association of immunosuppression and viral load with subcortical brain volume in an International sample of people living With HIV. JAMA Netw. Open 4, e2031190 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Ferguson, M. L. et al. Conformation of a clathrin triskelion in solution. Biochemistry 45, 5916–5922 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Kocsis, E., Trus, B. L., Steer, C. J., Bisher, M. E. & Steven, A. C. Image averaging of flexible fibrous macromolecules: the clathrin triskelion has an elastic proximal segment. J. Struct. Biol. 107, 6–14 (1991).

    CAS 
    PubMed 

    Google Scholar 

  • Kirchhausen, T., Harrison, S. C. & Heuser, J. Configuration of clathrin trimers: evidence from electron microscopy. J. Ultrastruct. Mol. Struct. Res. 94, 199–208 (1986).

    CAS 
    PubMed 

    Google Scholar 

  • Kotova, S. et al. AFM visualization of clathrin triskelia under fluid and in air. FEBS Lett. 584, 44–48 (2010).

  • Fitting, S. 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. 177, 1397–1410 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lee, R., Kermani, P., Teng, K. K. & Hempstead, B. L. Regulation of cell survival by secreted proneurotrophins. Science 294, 1945–1948 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Yasuda, M. et al. Robust stimulation of TrkB induces delayed increases in BDNF and Arc mRNA expressions in cultured rat cortical neurons via distinct mechanisms. J. Neurochem. 103, 626–636 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Yang, J. et al. proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus. Cell Rep. 7, 796–806 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Guo, W., Nagappan, G. & Lu, B. Differential effects of transient and sustained activation of BDNF-TrkB signaling. Dev. Neurobiol. 78, 647–659 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • Panja, D. & Bramham, C. R. BDNF mechanisms in late LTP formation: a synthesis and breakdown. Neuropharmacology 76, 664–676 (2014). Pt C.

    CAS 
    PubMed 

    Google Scholar 

  • Patterson, S. L. et al. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 1137–1145 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • Kang, H. & Schuman, E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658–1662 (1995).

    CAS 
    PubMed 

    Google Scholar 

  • Rossi, C. et al. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 24, 1850–1856 (2006).

    PubMed 

    Google Scholar 

  • Woo, N. H. et al. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat. Neurosci. 8, 1069–1077 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Teng, H. K. et al. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J. Neurosci. 25, 5455–5463 (2005).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Barnes, P. & Thomas, K. L. Proteolysis of proBDNF is a key regulator in the formation of memory. PLoS ONE 3, e3248 (2008).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Qiao, H., An, S. C., Xu, C. & Ma, X. M. Role of proBDNF and BDNF in dendritic spine plasticity and depressive-like behaviors induced by an animal model of depression. Brain Res. 1663, 29–37 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Numakawa, T. et al. BDNF function and intracellular signaling in neurons. Histol. Histopathol. 25, 237–258 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Brunet, A., Datta, S. R. & Greenberg, M. E. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11, 297–305 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Yang, J. W. et al. BDNF promotes the growth of human neurons through crosstalk with the Wnt/beta-catenin signaling pathway via GSK-3beta. Neuropeptides 54, 35–46 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Green, M. V. & Thayer, S. A. NMDARs adapt to neurotoxic HIV protein Tat downstream of a GluN2A-ubiquitin ligase signaling pathway. J. Neurosci. 36, 12640–12649 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fassnacht, M. et al. AKT is highly phosphorylated in pheochromocytomas but not in benign adrenocortical tumors. J. Clin. Endocrinol. Metab. 90, 4366–4370 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Yan, Q. et al. Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 78, 431–448 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Barde, Y. A., Edgar, D. & Thoenen, H. Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1, 549–553 (1982).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lindholm, D., Carroll, P., Tzimagiorgis, G. & Thoenen, H. Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT-3 and NT-4. Eur. J. Neurosci. 8, 1452–1460 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • Johnson-Farley, N. N., Travkina, T. & Cowen, D. S. Cumulative activation of akt and consequent inhibition of glycogen synthase kinase-3 by brain-derived neurotrophic factor and insulin-like growth factor-1 in cultured hippocampal neurons. J. Pharmacol. Exp. Ther. 316, 1062–1069 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Vaka, S. R., Murthy, S. N., Balaji, A. & Repka, M. A. Delivery of brain-derived neurotrophic factor via nose-to-brain pathway. Pharm. Res. 29, 441–447 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Zheng, F., Soellner, D., Nunez, J. & Wang, H. The basal level of intracellular calcium gates the activation of phosphoinositide 3-kinase-Akt signaling by brain-derived neurotrophic factor in cortical neurons. J. Neurochem. 106, 1259–1274 (2008).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Numakawa, T., Odaka, H. & Adachi, N. Actions of brain-derived neurotrophin factor in the neurogenesis and neuronal function, and its involvement in the pathophysiology of brain diseases. Int. J. Mol. Sci. 19, 3650 (2018).

  • Lian, D. et al. Exogenous BDNF increases neurogenesis in the hippocampus in experimental Streptococcus pneumoniae meningitis. J. Neuroimmunol. 294, 46–55 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Fatima, M. et al. Tripartite containing motif 32 modulates proliferation of human neural precursor cells in HIV-1 neurodegeneration. Cell Death Differ. 23, 776–786 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Mishra, M., Taneja, M., Malik, S., Khalique, H. & Seth, P. Human immunodeficiency virus type 1 Tat modulates proliferation and differentiation of human neural precursor cells: implication in NeuroAIDS. J. Neurovirol. 16, 355–367 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Fan, Y., Gao, X., Chen, J., Liu, Y. & He, J. J. HIV Tat impairs neurogenesis through functioning as a notch ligand and activation of notch signaling pathway. J. Neurosci. 36, 11362–11373 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hill, J. D., Zuluaga-Ramirez, V., Gajghate, S., Winfield, M. & Persidsky, Y. Chronic intrahippocampal infusion of HIV-1 neurotoxic proteins: a novel mouse model of HIV-1 associated inflammation and neural stem cell dysfunction. J. NeuroImmune Pharmacol. 14, 375–382 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Coffey, E. T., Akerman, K. E. & Courtney, M. J. Brain derived neurotrophic factor induces a rapid upregulation of synaptophysin and tau proteins via the neurotrophin receptor TrkB in rat cerebellar granule cells. Neurosci. Lett. 227, 177–180 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Bamji, S. X., Rico, B., Kimes, N. & Reichardt, L. F. BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions. J. Cell Biol. 174, 289–299 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fukumitsu, H., Ohashi, A., Nitta, A., Nomoto, H. & Furukawa, S. BDNF and NT-3 modulate expression and threonine phosphorylation of microtubule-associated protein 2 analogues, and alter their distribution in the developing rat cerebral cortex. Neurosci. Lett. 238, 107–110 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Melo, C. V. et al. Spatiotemporal resolution of BDNF neuroprotection against glutamate excitotoxicity in cultured hippocampal neurons. Neuroscience 237, 66–86 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Levine, A. J. et al. Multilevel analysis of neuropathogenesis of neurocognitive impairment in HIV. J. Neurovirol. 22, 431–441 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Shin, A. H. & Thayer, S. A. Human immunodeficiency virus-1 protein Tat induces excitotoxic loss of presynaptic terminals in hippocampal cultures. Mol. Cell. Neurosci. 54, 22–29 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Butler, T. R., Smith, K. J., Self, R. L., Braden, B. B. & Prendergast, M. A. Neurodegenerative effects of recombinant HIV-1 Tat(1–86) are associated with inhibition of microtubule formation and oxidative stress-related reductions in microtubule-associated protein-2(a,b). Neurochem. Res. 36, 819–828 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Aprea, S. et al. Tubulin-mediated binding of human immunodeficiency virus-1 Tat to the cytoskeleton causes proteasomal-dependent degradation of microtubule-associated protein 2 and neuronal damage. J. Neurosci. 26, 4054–4062 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Maragos, W. F. et al. Neuronal injury in hippocampus with human immunodeficiency virus transactivating protein, Tat. Neuroscience 117, 43–53 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • LaBel, C. P. & Foss, J. Use of a rodent neurotoxicity screening battery in the preclinical safety assessment of recombinant-methionyl human brain-derived neurotrophic factor. Neurotoxicology 17, 851–864 (1996).

  • Zhang, L. et al. Brain-derived neurotrophic factor ameliorates learning deficits in a rat model of Alzheimer’s disease induced by abeta1–42. PLoS ONE 10, e0122415 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Mizuno, M. et al. Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol. Psychiatry 8, 217–224 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • Schmitt, U., Tanimoto, N., Seeliger, M., Schaeffel, F. & Leube, R. E. Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 162, 234–243 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • Khuchua, Z. et al. Deletion of the N-terminus of murine map2 by gene targeting disrupts hippocampal ca1 neuron architecture and alters contextual memory. Neuroscience 119, 101–111 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • Dickens, A. M. et al. Chronic low-level expression of HIV-1 Tat promotes a neurodegenerative phenotype with aging. Sci. Rep. 7, 7748 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Jaeger, L. B. & Nath, A. Modeling HIV-associated neurocognitive disorders in mice: new approaches in the changing face of HIV neuropathogenesis. Dis. Models Mech. 5, 313–322 (2012).

    CAS 

    Google Scholar 

  • Paterson, R. W. et al. The emerging spectrum of COVID-19 neurology: clinical, radiological and laboratory findings. Brain 143, 3104–3120 (2020).

  • Zhu, Y., Drake, M. T. & Kornfeld, S. Adaptor protein 1-dependent clathrin coat assembly on synthetic liposomes and Golgi membranes. Methods Enzymol. 329, 379–387 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Soderquist, R. G. et al. PEGylation of brain-derived neurotrophic factor for preserved biological activity and enhanced spinal cord distribution. J. Biomed. Mater. Res. Part A 91, 719–729 (2009).

    Google Scholar 

  • Sakane, T. & Pardridge, W. M. Carboxyl-directed pegylation of brain-derived neurotrophic factor markedly reduces systemic clearance with minimal loss of biologic activity. Pharm. Res. 14, 1085–1091 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Hahn, Y. K. 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 Struct. Funct. 220, 605–623 (2013).

  • Boado, R. J., Zhang, Y., Zhang, Y. & Pardridge, W. M. Genetic engineering, expression, and activity of a fusion protein of a human neurotrophin and a molecular Trojan horse for delivery across the human blood-brain barrier. Biotechnol. Bioeng. 97, 1376–1386 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Kummer, U. Tritium radiolabeling of antibodies to high specific activity with N-succinimidyl [2,3-3H]propionate: use in detecting and analyzing monoclonal antibodies. Methods Enzymol. 121, 670–678 (1986).

    CAS 
    PubMed 

    Google Scholar 

  • Chartoff, E. H., Mague, S. D., Barhight, M. F., Smith, A. M. & Carlezon, W. A. Jr. Behavioral and molecular effects of dopamine D1 receptor stimulation during naloxone-precipitated morphine withdrawal. J. Neurosci. 26, 6450–6457 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dingwall, C. et al. Human immunodeficiency virus 1 tat protein binds trans-activation-responsive region (TAR) RNA in vitro. Proc. Natl Acad. Sci. USA 86, 6925–6929 (1989).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Snyder, J. S. et al. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J. Neurosci.29, 14484–14495 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wojtowicz, J. M. & Kee, N. BrdU assay for neurogenesis in rodents. Nat. Protoc. 1, 1399–1405 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Scholzen, T. & Gerdes, J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182, 311–322 (2000).

    CAS 
    PubMed 

    Google Scholar 

  • Couillard-Despres, S. et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21, 1–14 (2005).

    PubMed 

    Google Scholar 

  • Knaus, P., Betz, H. & Rehm, H. Expression of synaptophysin during postnatal development of the mouse brain. J. Neurochem. 47, 1302–1304 (1986).

    CAS 
    PubMed 

    Google Scholar 

  • Caceres, A., Banker, G. A. & Binder, L. Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J. Neurosci. 6, 714–722 (1986).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Antunes, M. & Biala, G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn. Process. 13, 93–110 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Akaike, H., Parzen, E., Tanabe, K. & Kitagawa, G. Selected Papers of Hirotugu Akaike, (Springer, 1998).

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