GV1001 modulates neuroinflammation and improves memory and behavior through the activation of gonadotropin-releasing hormone receptors in a triple transgenic Alzheimer’s disease mouse model

Brain, Behavior, and Immunity - Tập 115 - Trang 295-307 - 2024
Hyunhee Park1, Hyuk Sung Kwon1, Kyu-Yong Lee1, Ye Eun Kim1, Jeong-Woo Son1, Na-Young Choi1, Eun Ji Lee1, Myung-Hoon Han2, Dong Woo Park3, Sangjae Kim4, Seong-Ho Koh1,5
1Department of Neurology, Hanyang University Guri Hospital, Hanyang University College of Medicine, 153, Gyeongchun-ro, Guri-si, Gyeonggi-do 11923, South Korea
2Department of Neurosurgery, Hanyang University Guri Hospital, Hanyang University College of Medicine, 153, Gyeongchun-ro, Guri-si, Gyeonggi-do 11923, South Korea
3Department of Radiology, Hanyang University Guri Hospital, Hanyang University College of Medicine, 153, Gyeongchun-ro, Guri-si, Gyeonggi-do 11923, South Korea
4Teloid Inc., 3580 Wilshire Boulevard, Suite 900-31, Los Angeles, CA 90010, USA
5Department of Translational Medicine, Hanyang University Graduate School of Biomedical Science & Engineering, Seoul 04763, South Korea

Tài liệu tham khảo

Alhadidi, 2018, Cofilin mediates LPS-induced microglial cell activation and associated neurotoxicity through activation of NF-κB and JAK-STAT pathway, Mol. Neurobiol., 55, 1676, 10.1007/s12035-017-0432-7 Anderson, 2017, Why do so many clinical trials of therapies for Alzheimer's disease fail?, Lancet, 390, 2327, 10.1016/S0140-6736(17)32399-1 Asai, 2015, Depletion of microglia and inhibition of exosome synthesis halt tau propagation, Nat Neurosci, 18, 1584, 10.1038/nn.4132 Bartus, 1982, The cholinergic hypothesis of geriatric memory dysfunction, Science, 217, 408, 10.1126/science.7046051 Baruch-Eliyahu, 2019, Telomerase increasing compound protects hippocampal neurons from amyloid beta toxicity by enhancing the expression of neurotrophins and plasticity related genes, Sci. Rep., 9, 18118, 10.1038/s41598-019-54741-7 Bellaver, 2023, Astrocyte reactivity influences amyloid-β effects on tau pathology in preclinical Alzheimer's disease, Nat. Med., 29, 1775, 10.1038/s41591-023-02380-x Brosseron, 2014, Body fluid cytokine levels in mild cognitive impairment and Alzheimer's disease: a comparative overview, Mol. Neurobiol., 50, 534, 10.1007/s12035-014-8657-1 Butterfield, 2009, Multifunctional roles of enolase in Alzheimer's disease brain: beyond altered glucose metabolism, J. Neurochem., 111, 915, 10.1111/j.1471-4159.2009.06397.x Carter, 2019, Astrocyte biomarkers in Alzheimer's disease, Trends Mol. Med., 25, 77, 10.1016/j.molmed.2018.11.006 Choi, 2015, The anti-inflammatory effect of GV1001 mediated by the downregulation of ENO1-induced pro-inflammatory cytokine production, Immune Network, 15, 291, 10.4110/in.2015.15.6.291 Cnops, 2022, Test, rinse, repeat: A review of carryover effects in rodent behavioral assays, Neurosci. Biobehav. Rev., 135, 10.1016/j.neubiorev.2022.104560 Cummings, 2022, Alzheimer's disease drug development pipeline: 2022, Alzheimers Dement. (N. Y.), 8 D'Amico, 2010, Luteinizing-hormone releasing hormone therapy and the risk of death from Alzheimer disease, Alzheimer Dis. Assoc. Disord., 24, 85, 10.1097/WAD.0b013e31819cb8f4 Dennison, 2021, Sexual dimorphism in the 3xTg-AD mouse model and its impact on pre-clinical research, J. Alzheimers Dis., 80, 41, 10.3233/JAD-201014 D'Hooge, 2001, Applications of the Morris water maze in the study of learning and memory, Brain Res. Brain Res. Rev., 36, 60, 10.1016/S0165-0173(01)00067-4 Di, 2015, Strategic approaches to optimizing peptide ADME properties, AAPS J., 17, 134, 10.1208/s12248-014-9687-3 Frozza, 2018, Challenges for Alzheimer's disease therapy: insights from novel mechanisms beyond memory defects, Front. Neurosci., 12, 37, 10.3389/fnins.2018.00037 Ghosh, 2016, Cyclic AMP is a key regulator of M1 to M2a phenotypic conversion of microglia in the presence of Th2 cytokines, J. Neuroinflamm., 13, 9, 10.1186/s12974-015-0463-9 Goldberg, J., Currais, A., Prior, M., Fischer, W., Chiruta, C., Ratliff, E., Daugherty, D., Dargusch, R., Finley, K., Esparza-Moltó, P.B., Cuezva, J.M., Maher, P., Petrascheck, M., Schubert, D., 2018. The mitochondrial ATP synthase is a shared drug target for aging and dementia. Aging Cell 17. Grigorova, 2006, Effects of treatment with leuprolide acetate depot on working memory and executive functions in young premenopausal women, Psychoneuroendocrinology, 31, 935, 10.1016/j.psyneuen.2006.05.004 Grundtman, 2011, Heat shock protein 60 and immune inflammatory responses in atherosclerosis, Arterioscler. Thromb. Vasc. Biol., 31, 960, 10.1161/ATVBAHA.110.217877 Hadas, 2012, Complement receptor-3 negatively regulates the phagocytosis of degenerated myelin through tyrosine kinase Syk and cofilin, J. Neuroinflamm., 9, 166, 10.1186/1742-2094-9-166 Haghani, A., Cacciottolo, M., Doty, K.R., D'Agostino, C., Thorwald, M., Safi, N., Levine, M.E., Sioutas, C., Town, T.C., Forman, H.J., Zhang, H., Morgan, T.E., Finch, C.E., 2020. Mouse brain transcriptome responses to inhaled nanoparticulate matter differed by sex and APOE in Nrf2-Nfkb interactions. eLife 9. He, 2018, Amyloid-β plaques enhance Alzheimer's brain tau-seeded pathologies by facilitating neuritic plaque tau aggregation, Nat. Med., 24, 29, 10.1038/nm.4443 Hughes, 2004, The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory, Neurosci. Biobehav. Rev., 28, 497, 10.1016/j.neubiorev.2004.06.006 Jang, 2021, Prevalence and incidence of dementia in South Korea: a nationwide analysis of the national health insurance service senior cohort, J. Clin. Neurol. (Seoul, Korea), 17, 249, 10.3988/jcn.2021.17.2.249 Javonillo, 2021, Systematic phenotyping and characterization of the 3xTg-AD mouse model of Alzheimer's disease, Front. Neurosci., 15 Kim, 2019, Phosphatidylethanolamine-binding protein 1 ameliorates ischemia-induced inflammation and neuronal damage in the rabbit spinal cord, Cells, 8, 10.3390/cells8111370 Kim, 2019, Anti-cancer effect of GV1001 for prostate cancer: function as a ligand of GnRHR, Endocr. Relat. Cancer, 26, 147, 10.1530/ERC-18-0454 Kim, 2021, Anti-metastatic effect of GV1001 on prostate cancer cells; roles of GnRHR-mediated Gαs-cAMP pathway and AR-YAP1 axis, Cell Biosci., 11, 191, 10.1186/s13578-021-00704-3 Ko, Y.J., Kwon, K.Y., Kum, K.Y., Lee, W.C., Baek, S.H., Kang, M.K., Shon, W.J., 2015. The anti-inflammatory effect of human telomerase-derived peptide on P. gingivalis lipopolysaccharide-induced inflammatory cytokine production and its mechanism in human dental pulp cells. Mediat. Inflamm. 2015, 385127. Koh, 2021, Efficacy and safety of GV1001 in patients with moderate-to-severe Alzheimer's disease already receiving donepezil: a phase 2 randomized, double-blind, placebo-controlled, multicenter clinical trial, Alzheimers Res. Ther., 13, 66, 10.1186/s13195-021-00803-w Kraeuter, 2019, The Y-maze for assessment of spatial working and reference memory in mice, Methods Mol. Biol., 1916, 105, 10.1007/978-1-4939-8994-2_10 Kwon, 2020, Neuroinflammation in neurodegenerative disorders: the roles of microglia and astrocytes, Transl. Neurodegener., 9, 42, 10.1186/s40035-020-00221-2 Larkin, 2023, Lecanemab gains FDA approval for early Alzheimer disease, JAMA, 329, 363, 10.1001/jama.2022.24494 Lau, 2018, Therapeutic peptides: Historical perspectives, current development trends, and future directions, Bioorg. Med. Chem., 26, 2700, 10.1016/j.bmc.2017.06.052 Liu, 2021, Can we learn lessons from the FDA's approval of aducanumab? Nature reviews, Neurology, 17, 715 Maeng, 2017, Acute gonadotropin-releasing hormone agonist treatment enhances extinction memory in male rats, Psychoneuroendocrinology, 82, 164, 10.1016/j.psyneuen.2017.05.015 Marbouti, 2020, GnRH protective effects against amyloid β-induced cognitive decline: A potential role of the 17β-estradiol, Mol. Cell. Endocrinol., 518, 10.1016/j.mce.2020.110985 Misrani, 2021, Mitochondrial deficits with neural and social damage in early-stage Alzheimer's disease model mice, Front. Aging Neurosci., 13, 10.3389/fnagi.2021.748388 Morris, 1982, Place navigation impaired in rats with hippocampal lesions, Nature, 297, 681, 10.1038/297681a0 Nazem, 2015, Rodent models of neuroinflammation for Alzheimer's disease, J. Neuroinflammation, 12, 74, 10.1186/s12974-015-0291-y Oakley, 2006, Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation, J. Neurosci., 26, 10129, 10.1523/JNEUROSCI.1202-06.2006 Oksanen, 2019, Astrocyte alterations in neurodegenerative pathologies and their modeling in human induced pluripotent stem cell platforms, Cell. Mol. Life Sci., 76, 2739, 10.1007/s00018-019-03111-7 Olfert, 1998, The CCAC guidelines on: choosing an appropriate endpoint in experiments using animals for research, Teaching and Testing Canadian Council on Animal Care guideline, 1, 1 Pardridge, 2020, Treatment of Alzheimer's disease and blood-brain barrier drug delivery, Pharmaceuticals (Basel, Switzerland), 13 Paris, 2011, Selective antihypertensive dihydropyridines lower Aβ accumulation by targeting both the production and the clearance of Aβ across the blood-brain barrier, Mol. Med. (Cambridge, Mass.), 17, 149 Park, 2014, Novel vaccine peptide GV1001 effectively blocks β-amyloid toxicity by mimicking the extra-telomeric functions of human telomerase reverse transcriptase, Neurobiol. Aging, 35, 1255, 10.1016/j.neurobiolaging.2013.12.015 Park, 2016, Neural stem cells injured by oxidative stress can be rejuvenated by GV1001, a novel peptide, through scavenging free radicals and enhancing survival signals, Neurotoxicology, 55, 131, 10.1016/j.neuro.2016.05.022 Park, 2018, Tracking and protection of transplanted stem cells using a ferrocenecarboxylic acid-conjugated peptide that mimics hTERT, Biomaterials, 155, 80, 10.1016/j.biomaterials.2017.11.009 Prange-Kiel, 2008, Gonadotropin-releasing hormone regulates spine density via its regulatory role in hippocampal estrogen synthesis, J. Cell Biol., 180, 417, 10.1083/jcb.200707043 Prince, 2013, The global prevalence of dementia: a systematic review and metaanalysis, Alzheimers Dement., 9, 63, 10.1016/j.jalz.2012.11.007 Quintanar, 2008, Neurotrophic effects of GnRH on neurite outgrowth and neurofilament protein expression in cultured cerebral cortical neurons of rat embryos, Neurochem. Res., 33, 1051, 10.1007/s11064-007-9549-9 Relitti, 2020, Telomerase-based cancer therapeutics: a review on their clinical trials, Curr. Top. Med. Chem., 20, 433, 10.2174/1568026620666200102104930 Schott, 2019, Unsuccessful trials of therapies for Alzheimer's disease, Lancet, 393, 29, 10.1016/S0140-6736(18)31896-8 Skinner, 1995, Luteinizing hormone (LH)-releasing hormone in third ventricular cerebrospinal fluid of the ewe: correlation with LH pulses and the LH surge, Endocrinology, 136, 3230, 10.1210/endo.136.8.7628356 Takata, 2010, Galantamine-induced amyloid-{beta} clearance mediated via stimulation of microglial nicotinic acetylcholine receptors, J. Biol. Chem., 285, 40180, 10.1074/jbc.M110.142356 Tang, 2016, Differential roles of M1 and M2 microglia in neurodegenerative diseases, Mol. Neurobiol., 53, 1181, 10.1007/s12035-014-9070-5 Ullman-Cullere, 1999, Body condition scoring: a rapid and accurate method for assessing health status in mice, Lab Anim Sci, 49, 319 Wang, F., Zhang, Z., Han, J., Zheng, J., Wang, X., Wang, Z., 2023. Discovery of microglia gonadotropin‑releasing hormone receptor and its potential role in polycystic ovarian syndrome. Mol. Med. Reports 27. Wang, 2020, Role of cofilin in Alzheimer's disease, Front. Cell Dev. Biol., 8, 10.3389/fcell.2020.584898 Xu, 2023, Systemic treatment with GnRH agonist produces antidepressant-like effects in LPS induced depression male mouse model, Neuropharmacology, 233, 10.1016/j.neuropharm.2023.109560 Zhang, 2013, Hypothalamic programming of systemic ageing involving IKK-β, NF-κB and GnRH, Nature, 497, 211, 10.1038/nature12143