Activity-Dependent Neuroprotective Protein Snippet NAP Reduces Tau Hyperphosphorylation and Enhances Learning in a Novel Transgenic Mouse Model
Abstract
Activity-dependent neuroprotective protein (ADNP) differentially interacts with chromatin to regulate essential genes. Because complete ADNP deficiency is embryonic lethal, the outcome of partial ADNP deficiency was examined. ADNP(+/-) mice exhibited cognitive deficits, significant increases in phosphorylated tau, tangle-like structures, and neurodegeneration compared with ADNP(+/+) mice. Increased tau hyperphosphorylation is known to cause memory impairments in neurodegenerative diseases associated with tauopathies, including the most prevalent Alzheimer's disease. The current results suggest that ADNP is an essential protein for brain function and plays a role in normal cognitive performance. ADNP-deficient mice offer an ideal paradigm for evaluation of cognitive enhancers. NAP (NAPVSIPQ) is a peptide derived from ADNP that interacts with microtubules and provides potent neuroprotection. NAP treatment partially ameliorated cognitive deficits and reduced tau hyperphosphorylation in the ADNP(+/-) mice. NAP is currently in phase II clinical trials assessing effects on mild cognitive impairment.
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ADNP+/- mice show tauopathy, neuronal cell death and abnormalities in social behaviour and cognitive functioning.
“while ADNP+/- mice show tauopathy, neuronal cell death and abnormalities in social behaviour and cognitive functioning18,34.”
From A SWI/SNF-related autism syndrome caused by de novo mutations in ADNP (2014) · cites this paper as [18]
Among genes reported as differentially expressed in Adnp-/- and Adnp+/- mice, only PLAGL2 was differentially regulated in the patients.
“Of the other genes reported as differentially expressed in Adnp-/-23 and Adnp+/-18 mice (down: CCNC, TMPO, PLAGL2; up: ABCF3), only PLAGL2 was found to be differentially regulated in our patients (Supplementary Fig. 3e).”
From A SWI/SNF-related autism syndrome caused by de novo mutations in ADNP (2014) · cites this paper as [18]
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“This is consistent with observations that NAP administration to ADNP heterozygous mice, a model of tauopathy, for two weeks resulted in reduced tau phosphorylation in the cortex 6 weeks after the cessation of NAP treatment (Vulih-Shultzman et al., 2007).”
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“…been shown to reduce tau hyperphosphorylation and Aβ accumulation in both in vitro and in vivo AD models, and also benefit cognitive test performance in some of these models (Gozes & Divinski, 2004; Matsuoka et al., 2007; Matsuoka et al., 2008; Shiryaev et al., 2009; Vulih-Shultzman et al., 2007).”
BackgroundNew approaches to the treatment of frontotemporal lobar degeneration
Vossel, K. A., & Miller, B. L. (2008) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328318444d · Cited by 66 · see citing works
Jarskog, L. F., Dong, Z., Kangarlu, A., Colibazzi, T., Girgis, R. R., Kegeles, L. S., Barch, D. M., Buchanan, R. W., Csernansky, J. G., GOFF, D. C., et al. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.23 · Cited by 67 · see citing works
“Animal studies suggest a potential therapeutic role for davunetide through its ability to stabilize microtubules and rescue cognitive deficits in several models of neurodegeneration (Merenlender- Wagner et al, 2010; Vulih-Shultzman et al, 2007).”
BackgroundDresner, E., Agam, G., & Gozes, I. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2010.06.004 · Cited by 65 · see citing works
“In this respect, antipsychotic drug treatment may cause tauopathy (Gong et al., 1996) and partial ADNP knockout resulted in tauopathy paralleled by cognitive and social deficiencies (Vulih-Shultzman et al., 2007), suggesting a possible feedback mechanism in the ADNP/ ADNP2 mRNA levels homeostasis.”
BackgroundInfluentialSelf-citationThe autism/neuroprotection-linked ADNP/NAP regulate the excitatory glutamatergic synapse
Sragovich, S., Malishkevich, A., Piontkewitz, Y., Giladi, E., Touloumi, O., Lagoudaki, R., Grigoriadis, N., & Gozes, I. (2019) · Translational Psychiatry · doi:10.1038/s41398-018-0357-6 · Cited by 60 · see citing works
Self-citationIntroducing ADNP and SIRT1 as new partners regulating microtubules and histone methylation
Hadar, A., Kapitansky, O., Ganaiem, M., Sragovich, S., Lobyntseva, A., Giladi, E., Yeheskel, A., Avitan, A. K., Vatine, G. D., Gurwitz, D., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01143-9 · Cited by 62 · see citing works
“for the ADNP syndrome [11, 12], were previously described [1, 16, 49].”
MethodSelf-citationADNP Plays a Key Role in Autophagy: From Autism to Schizophrenia and Alzheimer's Disease
Sragovich, S., Wagner, A. M., & Gozes, I. (2017) · BioEssays · doi:10.1002/bies.201700054 · Cited by 62 · see citing works
Self-citationTau-targeting therapy in Alzheimer’s disease: Critical advances and future opportunities
Guo, Y., Li, S., Zeng, L.-H., & Tan, J. (2022) · Ageing and Neurodegenerative Diseases · doi:10.20517/and.2022.16 · Cited by 61 · see citing works
What we can learn from a genetic rodent model about autism
Möhrle, D., Fernández, M. C., Peñagarikano, O., Frick, A., Allman, B. L., & Schmid, S. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.015 · Cited by 59 · see citing works
Malishkevich, A., Marshall, G. A., Schultz, A. P., Sperling, R. A., Aharon‐Peretz, J., & Gozes, I. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-150799 · Cited by 58 · see citing works
“Furthermore, ADNP haploinsufficient mice exhibit aging-related tauopathy neurodegeneration, and cognitive deficits [15].”
Self-citationIvashko‐Pachima, Y., Ganaiem, M., Ben-Horin-Hazak, I., Lobyntseva, A., Bellaiche, N., Fischer, I., Levy, G., Sragovich, S., Karmon, G., Giladi, E., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01603-w · Cited by 58 · see citing works
“NAP treatment protected against these adverse features, while inhibiting Tau hyperphosphorylation [21].”
BackgroundSelf-citationWagner, A. M., Pikman, R., Giladi, E., Andrieux, A., & Gozes, I. (2010) · Peptides · doi:10.1016/j.peptides.2010.04.011 · Cited by 58 · see citing works
Self-citationPharmacotherapeutic targets in Alzheimer's disease
Biran, Y., Masters, C. L., Barnham, K. J., Bush, A. I., & Adlard, P. A. (2008) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2008.00595.x · Cited by 56 · see citing works
“Studies in transgenic mice suggest that AL-108 interacts with microtubules, reduces -hyperphosphorylation and increases soluble levels leading to an improvement in cognition [76, 77].”
BackgroundSchirer, Y., Malishkevich, A., Ophir, Y., Lewis, J. M., Giladi, E., & Gozes, I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087383 · Cited by 57 · see citing works
“ADNP deficiency can be ameliorated in part by compensatory treatment with the ADNP fragment, the drug candidate davuentide (NAP), that stabilizes microtubules and inhibits tau pathology while protecting cognitive [12] as well as motor functions [53], by protecting microtubule-dependent axonal transport [48,53].”
BackgroundMethodInfluentialSelf-citationEpisignatures Stratifying Helsmoortel-Van Der Aa Syndrome Show Modest Correlation with Phenotype
Breen, M. S., Garg, P., Tang, L., Mendonca, D., Levy, T., Barbosa, M., Arnett, A. B., Kurtz‐Nelson, E. C., Agolini, E., Battaglia, A., et al. (2020) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2020.07.003 · Cited by 57 · see citing works
Mencer, S., Kartawy, M., Lendenfeld, F. V., Soluh, H., Tripathi, M. K., Халиулин, И. Г., & Amal, H. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01578-2 · Cited by 55 · see citing works
“Meanwhile, ADNP deficiency has been reported to promote tauopathy in AD patients [23, 26, 27].”
BackgroundMagen, I., & Gozes, I. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.011 · Cited by 52 · see citing works
Self-citationPharmacologists and Alzheimer disease therapy: to boldly go where no scientist has gone before
Mancuso, C., Siciliano, R., Barone, E., Butterfield, D. A., & Preziosi, P. (2011) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2011.601740 · Cited by 52 · see citing works
“Several preclinical studies demonstrated a neuroprotective role for davunetide due to a significant reduction in both hyperphosphorylated and insoluble tau [158,159].”
BackgroundThe autism-mutated ADNP plays a key role in stress response
Sragovich, S., Ziv, Y., Vaisvaser, S., Shomron, N., Hendler, T., & Gozes, I. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0569-4 · Cited by 51 · see citing works
Self-citationGozes, I., Patterson, M. C., Dijck, A. V., Kooy, R. F., Peeden, J., Eichenberger, J. A., Zawacki-Downing, A., & Bedrosian‐Sermone, S. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00107 · Cited by 50 · see citing works
“These findings mark ADNP as one of the most frequent ASD-associated genes known to date.”
BackgroundInfluentialSelf-citationDresner, E., Malishkevich, A., Arviv, C., Leibman Barak, S., Alon, S., Ofir, R., Gothilf, Y., & Gozes, I. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.387027 · Cited by 47 · see citing works
Self-citationTau-directed approaches for the treatment of Alzheimer’s disease: focus on leuco-methylthioninium
Seripa, D., Solfrizzi, V., Imbimbo, B. P., Daniele, A., Santamato, A., Lozupone, M., Zuliani, G., Greco, A., Logroscino, G., & Panza, F. (2016) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2016.1140039 · Cited by 50 · see citing works
D’Incal, C. P., Rossem, K. E. V., Man, K. D., Konings, A., Dijck, A. V., Rizzuti, L., Vitriolo, A., Testa, G., Gozes, I., Berghe, W. V., et al. (2023) · Clinical Epigenetics · doi:10.1186/s13148-023-01450-8 · Cited by 51 · see citing works
“No obvious phenotypic abnormalities were mentioned [13], be it that in follow-up studies a small reduction in body size of the mutant animals was measured [122].”
BackgroundMethodResultInfluentialSelf-citationDavunetide: Peptide Therapeutic in Neurological Disorders
Magen, I., & Gozes, I. (2014) · Current Medicinal Chemistry · doi:10.2174/0929867321666140217124945 · Cited by 45 · see citing works
“In this respect, ADNP heterozygous mice develop Alzheimer's-like tau pathology, cognitive deficits and neuronal cell death [26] and ADNP expression is modulated in a mouse model of Alzheimer's disease [27].”
BackgroundSelf-citationBose, M., Quipildor, G. F., Ehrlich, M. E., & Salton, S. R. (2022) · Cells · doi:10.3390/cells11223629 · Cited by 44 · see citing works
Ballatore, C., Brunden, K. R., Trojanowski, J. Q., Lee, V. M. Y., Smith, A. B., & Huryn, D. M. (2010) · Current Topics in Medicinal Chemistry · doi:10.2174/156802611794072605 · Cited by 44 · see citing works
“Furthermore, davunetide was found to reduce tau-hyperphosphorylation both in vitro [101] as well as in ADNP+/− mice [103].”
BackgroundMagen, I., Ostritsky, R., Richter, F., Zhu, C., Fleming, S. M., Lemesre, V., Stewart, A. J., Morimoto, B. H., Gozes, I., & Chesselet, M. (2014) · Pharmacology Research & Perspectives · doi:10.1002/prp2.65 · Cited by 43 · see citing works
“The intermittent regimen was chosen for long-term drug administration because it was previously shown to be beneficial in a mouse model of AD and frontotemporal dementia (Matsuoka et al. 2007, 2008; Vulih-Shultzman et al. 2007; Shiryaev et al. 2009; Jouroukhin et al. 2012, 2013).”
BackgroundSelf-citationPescosolido, M. F., Schwede, M., Harrison, A. J., Schmidt, M., Uzun, E. D. G., Chen, W. S., Donahue, J. P., Shur, N. E., Jerskey, B. A., Phornphutkul, C., et al. (2014) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2014-102444 · Cited by 43 · see citing works
Tau and Caspase 3 as Targets for Neuroprotection
Idan-Feldman, A., Ostritsky, R., & Gozes, I. (2012) · International Journal of Alzheimer s Disease · doi:10.1155/2012/493670 · Cited by 42 · see citing works
Self-citationThe Compassionate Side of Neuroscience: Tony Sermone’s Undiagnosed Genetic Journey—ADNP Mutation
Gozes, I., Helsmoortel, C., Vandeweyer, G., der Aa, N. V., Kooy, R. F., & Bedrosian‐Sermone, S. (2015) · Journal of Molecular Neuroscience · doi:10.1007/s12031-015-0586-6 · Cited by 41 · see citing works
“Taking advantage of mouse genetics, we have shown that ADNP is crucial for brain formation (Pinhasov et al. 2003) and learning and memory (Vulih-Shultzman et al. 2007), in a sex-dependent manner (Malishkevich et al. 2015; Kleiman et al. 2015).”
Self-citationIvashko‐Pachima, Y., Maor-Nof, M., & Gozes, I. (2019) · PLoS ONE · doi:10.1371/journal.pone.0213666 · Cited by 40 · see citing works
Self-citationCritical appraisal of the role of davunetide in the treatment of progressive supranuclear palsy
Gozes, I., Gold, Lorenzl, Stewart, A. J., Morimoto, B. H., & Williams (2012) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s12518 · Cited by 39 · see citing works
“In vivo confirmation comes from several animal models in which davunetide reduces the level of phosphorylated tau in models of AD,(47,48) tauopathy(33,49) and ADNP deficiency.(50) A link between davunetide’s effects on microtubules and cell survival pathways is suggested by studies involving neuroprotection against to…”
Self-citationThe ADNP Syndrome and CP201 (NAP) Potential and Hope
Gozes, I. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.608444 · Cited by 39 · see citing works
“The protective effect of CP201 was demonstrated by affecting animal traits that are equivalent to clinical symptoms in human patients with ADNP syndrome (20, 22).”
BackgroundInfluentialSelf-citationCho, H., Yoo, T., Moon, H., Kang, H., Yang, Y., Kang, M., Yang, E., Lee, D., Hwang, D., Kim, H., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02129-5 · Cited by 36 · see citing works
“These Adnp mouse phenotypes are rescued by the NAP peptide, which corresponds to eight aa residues of ADNP (NAPVSIPQ; also known as davunetide or CP201) [13, 16, 23] and is known to act through microtubule end-binding proteins [14].”
BackgroundBennison, S. A., Blazejewski, S. M., Liu, X., Hacohen-Kleiman, G., Sragovich, S., Zoidou, S., Touloumi, O., Grigoriadis, N., Gozes, I., & Toyo-oka, K. (2023) · Molecular Psychiatry · doi:10.1038/s41380-022-01939-3 · Cited by 42 · see citing works
“Treatment of cells in culture with NAP has been shown to promote or rescue neurite outgrowth [31, 32], enhance microtubule dynamics and Tau-microtubule association [29, 33, 34], and interact with microtubule end binding protein (EB3) to enhance dendritic spine formation [35, 36].”
BackgroundMethodInfluentialSelf-citationDavunetide (NAP) Protects the Retina Against Early Diabetic Injury by Reducing Apoptotic Death
Scuderi, S., D’Amico, A. G., Castorina, A., Federico, C., Marrazzo, G., Drago, F., Bucolo, C., & D’Agata, V. (2014) · Journal of Molecular Neuroscience · doi:10.1007/s12031-014-0244-4 · Cited by 35 · see citing works
Pharmacological approaches for Alzheimer’s disease: neurotransmitter as drug targets
Prakash, A. K., Kalra, J., Mani, V., Ramasamy, K., & Majeed, A. B. A. (2014) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2015.988709 · Cited by 35 · see citing works
“Neuroprotective effect of ADNF is mimicked by NAP via its interaction with tubulin, increasing assembly of microtubules, resulting in improved neuronal outgrowth [174–176].”
BackgroundEvidence of a Cardiovascular Function for Microtubule-Associated Protein Tau
Betrie, A. H., Ayton, S., Bush, A. I., Angus, J. A., Lei, P., & Wright, C. E. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161093 · Cited by 35 · see citing works
Hacohen-Kleiman, G., Barnea, O. Y., Touloumi, O., Lagoudaki, R., Avraham, K. B., Grigoriadis, N., & Gozes, I. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02723-6 · Cited by 35 · see citing works
Self-citationMolecular causes of sex‐specific deficits in rodent models of neurodevelopmental disorders
Mossa, A., & Manzini, M. C. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24577 · Cited by 36 · see citing works
“Two small peptide molecules have been widely studied: NAP, a neuroprotective ADNP-derived snippet peptide (also known as NAPVSIPQ, CP201, or davunetide) (Hacohen-Kleiman et al., 2018; Vulih-Shultzman et al., 2007) and SKIP, a four-amino-acid peptide (Amram et al., 2016).”
BackgroundCellular and animal models of skin alterations in the autism-related ADNP syndrome
Mollinedo, P., Kapitansky, O., González‐Lamuño, D., Zaslavsky, A., Real, P. J., Gozes, I., Gandarillas, A., & Fernández-Luna, J. L. (2019) · Scientific Reports · doi:10.1038/s41598-018-36859-2 · Cited by 34 · see citing works
Self-citationGanaiem, M., Karmon, G., Ivashko‐Pachima, Y., & Gozes, I. (2022) · Cells · doi:10.3390/cells11192994 · Cited by 33 · see citing works
“Conversely, ADNP deficiencies and ADNP gene mutations in transgenic mice led to dramatic alterations in mRNA/protein expression profiles as well as slower microtubule-dependent axonal transport, aberrant dendritic spine formation and tauopathy, which could be partially repaired by NAP treatment [7,8,12,13].”
BackgroundSelf-citationGozes, I., Yeheskel, A., & Pasmanik‐Chor, M. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-142490 · Cited by 33 · see citing works
“In ADNP haploinsufficient mice [5], a set of genes related to autism was deregulated including a solute carrier (SLC) transcript, involved in intracellular signaling cascade, transforming growth factor, involved in angiogenesis and Pax6 [20], involved in neuronal migration and axogenesis, which are either mutated or a…”
BackgroundResultInfluentialSelf-citationCosgrave, A. S., McKay, J. S., Bubb, V. J., Morris, R., Quinn, J. P., & Thippeswamy, T. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.02.005 · Cited by 33 · see citing works
“Importantly, a recent study by Vulih-Shultzman et al. (2007) demonstrated thatADNP+/−mice have cognitive deficits and increased phosphorylated tau, the hallmark of neurodegenerative diseases.”
BackgroundADNP Is a Therapeutically Inducible Repressor of WNT Signaling in Colorectal Cancer
Blaj, C., Bringmann, A., Schmidt, E. M., Urbischek, M., Lamprecht, S., Fröhlich, T., Arnold, G. J., Krebs, S., Blum, H., Hermeking, H., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-1604 · Cited by 33 · see citing works
“It also assumes protective roles against cognitive defects in neurodegenerative disease (12).”
BackgroundYang, M., Chen, S.-C., Lin, Y., Lee, Y., Huang, M., Chen, K., Wu, H., Lin, P., Gozes, I., & Tyan, Y. (2019) · Journal of Food and Drug Analysis · doi:10.1016/j.jfda.2018.11.009 · Cited by 33 · see citing works
“neuroprotection, central nervous system (CNS) development and immunoregulation for the brain damage [17,18,24,25,28].”
BackgroundSelf-citationNAP protects against cytochrome c release: Inhibition of the initiation of apoptosis
Zemlyak, I., Sapolsky, R. M., & Gozes, I. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.07.013 · Cited by 32 · see citing works
“, 2004); 2] ADNP deficiency in vivo has been associated with the microtubule-associated protein tau hyperphosphorylation and neurofibrillary-tangle like structure formation (Vulih-Shultzman et al., 2007); 3] in neuronal-like cells ADNP deficiency resulted in reduction in microtubule-associated protein 2 staining and l…”
BackgroundInfluentialSelf-citationConvergence of spectrums: neuronal gene network states in autism spectrum disorder
Sullivan, J. M., Rubeis, S. D., & Schaefer, A. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.04.011 · Cited by 30 · see citing works
Ganaiem, M., Gildor, N. D., Shazman, S., Karmon, G., Ivashko‐Pachima, Y., & Gozes, I. (2023) · Cells · doi:10.3390/cells12182251 · Cited by 30 · see citing works
Self-citationIntranasal delivery of a Fas-blocking peptide attenuates Fas-mediated apoptosis in brain ischemia
Ullah, I., Chung, K., Oh, J., Beloor, J., Bae, S., Lee, S. C., Lee, M., Kumar, P., & Lee, S. (2018) · Scientific Reports · doi:10.1038/s41598-018-33296-z · Cited by 30 · see citing works
Experimental Models to Study Autism Spectrum Disorders: hiPSCs, Rodents and Zebrafish
Pensado‐López, A., Veiga-Rúa, S., Carracedo, Á., Allegue, C., & Sanchez, L. E. (2020) · Genes · doi:10.3390/genes11111376 · Cited by 31 · see citing works
Mythili, Y., LaPointe, N. E., Lopus, M., Cox, C., Jordan, M. A., Feinstein, S. C., & Wilson, L. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-1335 · Cited by 30 · see citing works
“Recently NAP has been reported to reduce tau hyper-phosphorylation in animal models of Alzheimer’s disease [4], frontotemporal dementia [3], and ADNP (its parent protein)-deficiency [29].”
Brown, B. P., Kang, S., Gawelek, K., Zacharias, R. A., Anderson, S. R., Turner, C. P., & Morris, J. K. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2014.12.076 · Cited by 29 · see citing works
Sokołowska, P., Passemard, S., Mok, A., Schwendimann, L., Gozes, I., & Gressèns, P. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.074 · Cited by 29 · see citing works
Self-citationNAP Alpha-Aminoisobutyric Acid (IsoNAP)
Gozes, I., Schirer, Y., Idan-Feldman, A., David, M. P., & Furman-Assaf, S. (2013) · Journal of Molecular Neuroscience · doi:10.1007/s12031-013-0103-8 · Cited by 28 · see citing works
“The procedure used to generate ADNP heterozygous mice was previously described (Vulih-Shultzman et al. 2007).”
BackgroundMethodResultInfluentialSelf-citationReciprocal control of translation and transcription in autism spectrum disorder
Longo, F., & Klann, E. (2021) · EMBO Reports · doi:10.15252/embr.202052110 · Cited by 27 · see citing works
“Haploinsufficient ADNP ( Adnp + /- ) mice mimic human HVDAS in terms of altered gene expression patterns and synapse density, as well as compromised developmental, motor, and cognitive ability (Vulih-Shultzman et al, 2007; Amram et al, 2016).”
A convergent mechanism of high risk factors ADNP and POGZ in neurodevelopmental disorders
Conrow‐Graham, M., Williams, J. B., Martin, J. A., Zhong, P., Cao, Q., Rein, B. A., & Yan, Z. (2022) · Brain · doi:10.1093/brain/awac152 · Cited by 28 · see citing works
Greggio, S., de Paula, S., de Oliveira, I. M., Trindade, C., Rosa, R. M., Henriques, J. A. P., & DaCosta, J. C. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.06.018 · Cited by 28 · see citing works
“, 2006) and ADNPdeficient mice (Vulih-Shultzman et al., 2007), fetal alcohol syndrome (Brenneman et al.”
BackgroundGardiner, J. C. (2012) · Plant Signaling & Behavior · doi:10.4161/psb.21325 · Cited by 28 · see citing works
“NAP treatment partially ameliorates cognitive deficit and Tau hyperphosphorylation in ADNP(+/-) mice.(14) MAP2 targets PKA to microtubules.”
BackgroundGozes, I., Iram, T., Maryanovsky, E., Arviv, C., Rozenberg, L., Schirer, Y., Giladi, E., & Furman-Assaf, S. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-131664 · Cited by 27 · see citing works
“in part against ADNP deficiency [33, 85], and it is of”
Self-citation
- Authors
- Vulih-Shultzman, I., Pinhasov, A., Mandel, S., Grigoriadis, N., Touloumi, O., Pittel, Z., & Gozes, I.
- Venue
- The Journal of Pharmacology and Experimental Therapeutics
- Publisher
- Elsevier BV
- Published
- 2007-11
- Volume
- 323
- Issue
- 2
- Pages
- 438-449
- ISSN
- 0022-3565 (ISSN-L)
- OpenAlex
- W2136172091
- Cited by
- 219
- References
- 40
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 12 · 2023: 9 · 2022: 14 · 2021: 9 · 2020: 19 · 2019: 18 · 2018: 7 · 2017: 11 · 2016: 15 · 2015: 13 · 2014: 14 · 2013: 11 · 2012: 13
- FWCI
- 5.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Pharmacology and Experimental Therapeutics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- ADNP, NAP peptide, tau hyperphosphorylation, cognitive impairment, learning, neurodegeneration, tauopathy, Alzheimer's disease, mild cognitive impairment, neuroprotection, microtubule binding
- MeSH terms
- Animals, Astrocytes, Cognition Disorders, Female, Learning, Male, Mice, Inbred ICR, Mice, Transgenic, Nerve Tissue Proteins, Oligopeptides, Phosphorylation, tau Proteins, Homeodomain Proteins, Mice
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