Neuropeptide W alleviates cognitive impairment and anxiety-like behaviors in rats with chronic stress
Year 2023,
Volume: 6 Issue: 3, 334 - 339, 21.10.2023
Sevil Arabacı Tamer
,
Emine Karahan
Abstract
Objective: NPW plays a regulatory role in the neuroendocrine response to stress and the activation of the HPA axis. The current study aimed to investigate the effects of peripherally administered NPW on the cognitive functions and anxiety-like behavior of rats under chronic stress conditions.
Methods: Wistar albino (250-290 gr) male rats were randomly divided as control, chronic stress group, and chronic stress exposed NPW-treated (0.1 µg/kg, subcutaneously) group. Chronic stress was induced by exposing the animals to water avoidance stress (WAS) for 1 h/day for ten consecutive days. At the end of the experimental stress procedure, an object recognition test was used to evaluate cognitive functions, and a hole-board test was used to assess anxiety levels. After the experiments, blood samples were collected to measure corticosterone levels.
Results: WAS significant increases in the level of corticosterone when compared with control rats (p<0.05), showing the activation of HPA axis. Application of WAS also caused anxiety and diminished cognitive functions. In NPW-treated rats with WAS, the corticosterone level was not different from the control group. The number of rearing up and head-dips by WAS-induced rats increased after NPW application. (p<0.05-0.01) and also decreased the immobilization time (p<0.01). Moreover, the difference score in the object recognition test was increased by the NPW application in WAS group (p< 0.05).
Conclusion: Our results showed for the first time that NPW pretreatment exerted an anxiolytic effect and attenuated cognitive function in rats subjected to water aversion stress.
Supporting Institution
The Scientific and Technological Research Council of Turkey (TUBITAK)
Project Number
program code: 2209, project no: 1919B012204884
References
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- Choobdar S, Vafaei AA, Sedaghat K. Protective role of vitamin-D on chronic stress induced-learning and memory deficits in rats. Koomesh. 2019;21(4): 708-715.
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- Zhang H, Wei M, Sun Q, et al. Lycopene ameliorates chronic stress-induced hippocampal injury and subsequent learning and memory dysfunction through inhibiting ROS/JNK signaling pathway in rats. Food Chem Toxicol. 2020;145:111688. doi:10.1016/j.fct.2020.111688
- Algamal M, Pearson AJ, Hahn-Townsend C, et al. Repeated unpredictable stress and social isolation induce chronic HPA axis dysfunction and persistent abnormal fear memory. Prog Neuropsychopharmacol Biol Psychiatry. 2021;104:110035. doi:10.1016/j.pnpbp.2020.110035
- Leistner C, Menke A. Hypothalamic-pituitary-adrenal axis and stress. Handb Clin Neurol. 2020;175:55-64.
doi:10.1016/B978-0-444-64123-6.00004-7
- Juszczyk G, Mikulska J, Kasperek K, Pietrzak D, Mrozek W, Herbet M. Chronic Stress and Oxidative Stress as Common Factors of the Pathogenesis of Depression and Alzheimer's Disease: The Role of Antioxidants in Prevention and Treatment. Antioxidants (Basel). 2021;10(9):1439. Published 2021 Sep 9. doi:10.3390/antiox10091439
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- Fujii R, Yoshida H, Fukusumi S, et al. Identification of a neuropeptide modified with bromine as an endogenous ligand for GPR7. J Biol Chem. 2002;277(37):34010-34016. doi:10.1074/jbc.M205883200
- Niimi M, Murao K. Neuropeptide W as a stress mediator in the hypothalamus. Endocrine. 2005;27(1):51-54. doi:10.1385/ENDO:27:1:051
- Koyuncuoglu T, Ipek BE, Dertsiz EK, Akakin D, Yuksel M, Yegen BC. The neuroprotective effects of neuropeptide W in newborn rats with cerebral palsy. In Acta Physiologica. 2019;227:87-87.
- Arabacı Tamer S, Akbulut S, Peker Eyüboğlu İ, et al. Peripheral administration of Neuropeptide-W protects against stress-induced gastric injury in rats. Life Sci. 2022;310:121087. doi:10.1016/j.lfs.2022.121087
- Arabacı Tamer S, Üçem S, Büke B, et al. Regular moderate exercise alleviates gastric oxidative damage in rats via the contribution of oxytocin receptors. J Physiol. 2020;598(12):2355-2370. doi:10.1113/JP279577
- Koyuncuoğlu T, Sevim H, Çetrez N, et al. High intensity interval training protects from Post Traumatic Stress Disorder induced cognitive impairment. Behav Brain Res. 2021;397:112923. doi:10.1016/j.bbr.2020.112923
- Agorastos A, Chrousos GP. The neuroendocrinology of stress: the stress-related continuum of chronic disease development. Mol Psychiatry. 2022;27(1):502-513.
doi:10.1038/s41380-021-01224-9
- Chen P, Li X, Yu Y, et al. Administration Time and Dietary Patterns Modified the Effect of Inulin on CUMS-Induced Anxiety and Depression. Mol Nutr Food Res. 2023;67(8):e2200566. doi:10.1002/mnfr.202200566
- Liu C, Shi R, Liu Y, et al. Low-frequency transcranial magnetic stimulation protects cognition in mice with chronic unpredictable mild stress through autophagy regulation. Behav Brain Res. 2023;444:114366. doi:10.1016/j.bbr.2023.114366
- Mello AF, Mello MF, Carpenter LL, Price LH. Update on stress and depression: the role of the hypothalamic-pituitary-adrenal (HPA) axis. Braz J Psychiatry. 2003;25(4):231-238. doi:10.1590/s1516-44462003000400010
- Mizoguchi K, Shoji H, Ikeda R, Tanaka Y, Tabira T. Persistent depressive state after chronic stress in rats is accompanied by HPA axis dysregulation and reduced prefrontal dopaminergic neurotransmission. Pharmacol Biochem Behav. 2008;91(1):170-175. doi:10.1016/j.pbb.2008.07.002
- Lim DW, Han D, Lee C. Pedicularis resupinata Extract Prevents Depressive-like Behavior in Repeated Corticosterone-Induced Depression in Mice: A Preliminary Study. Molecules. 2022;27(11):3434. Published 2022 May 26. doi:10.3390/molecules27113434
- Vinkers CH, Kuzminskaite E, Lamers F, Giltay EJ, Penninx BWJH. An integrated approach to understand biological stress system dysregulation across depressive and anxiety disorders. J Affect Disord. 2021;283:139-146. doi:10.1016/j.jad.2021.01.051
- Eliwa H, Brizard B, Le Guisquet AM, Hen R, Belzung C, Surget A. Adult neurogenesis augmentation attenuates anhedonia and HPA axis dysregulation in a mouse model of chronic stress and depression. Psychoneuroendocrinology. 2021;124:105097. doi:10.1016/j.psyneuen.2020.105097
- Gao K, Farzi A, Ke X, et al. Oral administration of Lactococcus lactis WHH2078 alleviates depressive and anxiety symptoms in mice with induced chronic stress. Food Funct. 2022;13(2):957-969. Published 2022 Jan 24. doi:10.1039/d1fo03723d
- West EG, McDermott C, Chess-Williams R, Sellers DJ. Partial recovery of voiding function in female mice following repeated psychological stress exposure. PLoS One. 2022;17(4):e0266458. Published 2022 Apr 21. doi:10.1371/journal.pone.0266458
- Atici AE, Arabacı Tamer S, Levent HN, et al. Neuropeptide W Attenuates Oxidative Multi-Organ Injury in Rats Induced with Intra-Abdominal Sepsis. Inflammation. 2022;45(1):279-296. doi:10.1007/s10753-021-01545-5
- Mazzocchi G, Rebuffat P, Ziolkowska A, Rossi GP, Malendowicz LK, Nussdorfer GG. G protein receptors 7 and 8 are expressed in human adrenocortical cells, and their endogenous ligands neuropeptides B and w enhance cortisol secretion by activating adenylate cyclase- and phospholipase C-dependent signaling cascades. J Clin Endocrinol Metab. 2005;90(6):3466-3471. doi:10.1210/jc.2004-2132
- Hochol A, Belloni AS, Rucinski M, et al. Expression of neuropeptides B and W and their receptors in endocrine glands of the rat. Int J Mol Med. 2006;18(6):1101-1106.
- Zareie M, Johnson-Henry K, Jury J, et al. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut. 2006;55(11):1553-1560. doi:10.1136/gut.2005.080739
- Bozorgi H, Rashidy-Pour A, Moradikor N, et al. Reversal of chronic restraint stress-induced memory impairment by Japanese sake yeast supplement in mice: Role of adenosine A1 and A2A receptors. J Psychiatr Res. 2023;161:123-131. doi:10.1016/j.jpsychires.2023.02.033
- Ahmed Z, Tokhi A, Arif M, et al. Fraxetin attenuates disrupted behavioral and central neurochemical activity in a model of chronic unpredictable stress. Front Pharmacol. 2023;14:1135497. Published 2023 Mar 23. doi:10.3389/fphar.2023.1135497
- Kageyama K, Iwasaki Y, Daimon M. Hypothalamic Regulation of Corticotropin-Releasing Factor under Stress and Stress Resilience. Int J Mol Sci. 2021;22(22):12242. Published 2021 Nov 12. doi:10.3390/ijms222212242
- Welcome MO. Cellular mechanisms and molecular signaling pathways in stress-induced anxiety, depression, and blood-brain barrier inflammation and leakage. Inflammopharmacology. 2020;28(3):643-665. doi:10.1007/s10787-020-00712-8.
- Qin D, Wang J, Le A, Wang TJ, Chen X, Wang J. Traumatic Brain Injury: Ultrastructural Features in Neuronal Ferroptosis, Glial Cell Activation and Polarization, and Blood-Brain Barrier Breakdown. Cells. 2021;10(5):1009. Published 2021 Apr 24. doi:10.3390/cells10051009
- Yan Y, Xu X, Chen R, et al. Down-regulation of MST1 in hippocampus protects against stress-induced depression-like behaviours and synaptic plasticity impairments. Brain Behav Immun. 2021;94:196-209. doi:10.1016/j.bbi.2021.02.007
- Lei H, Zhang Y, Huang L, et al. L-3-n-Butylphthalide Regulates Proliferation, Migration, and Differentiation of Neural Stem Cell In Vitro and Promotes Neurogenesis in APP/PS1 Mouse Model by Regulating BDNF/TrkB/CREB/Akt Pathway. Neurotox Res. 2018;34(3):477-488. doi:10.1007/s12640-018-9905-3
- Choi GY, Kim HB, Cho JM, et al. Umbelliferone Ameliorates Memory Impairment and Enhances Hippocampal Synaptic Plasticity in Scopolamine-Induced Rat Model. Nutrients. 2023;15(10):2351. Published 2023 May 17. doi:10.3390/nu15102351
- Wang R, Yan F, Liao R, Wan P, Little PJ, Zheng W. Role of brain-derived neurotrophic factor and nerve growth factor in the regulation of Neuropeptide W in vitro and in vivo. Mol Cell Endocrinol. 2017;447:71-78. doi:10.1016/j.mce.2017.02.040
- Taylor MM, Yuill EA, Baker JR, et al. Actions of neuropeptide W in paraventricular hypothalamus: implications for the control of stress hormone secretion. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R270-R275. doi:10.1152/ajpregu.00396.2004
- Yogo K, Oki Y, Iino K, et al. Neuropeptide W stimulates adrenocorticotrophic hormone release via corticotrophin-releasing factor but not via arginine vasopressin. Endocr J. 2012;59(7):547-554. doi:10.1507/endocrj.ej11-0221
- Hu Y, Li H, Zhang J, et al. Periodontitis Induced by P. gingivalis-LPS Is Associated With Neuroinflammation and Learning and Memory Impairment in Sprague-Dawley Rats. Front Neurosci. 2020;14:658. Published 2020 Jul 2. doi:10.3389/fnins.2020.00658
- Michelucci A, Heurtaux T, Grandbarbe L, Morga E, Heuschling P. Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: Effects of oligomeric and fibrillar amyloid-beta. J Neuroimmunol. 2009;210(1-2):3-12. doi:10.1016/j.jneuroim.2009.02.003
Nöropeptid W, kronik stresli sıçanlarda bilişsel bozukluğu ve kaygı benzeri davranışları hafifletir
Year 2023,
Volume: 6 Issue: 3, 334 - 339, 21.10.2023
Sevil Arabacı Tamer
,
Emine Karahan
Abstract
Amaç: NPW, strese karşı nöroendokrin yanıtta ve HPA ekseninin aktivasyonunda düzenleyici bir rol oynar. Bu çalışmanın amacı, kronik stres koşullarında periferik olarak uygulanan NPW'nin sıçanların bilişsel işlevler ve kaygı benzeri davranışlar üzerindeki etkilerini araştırmaktır.
Yöntem: Wistar albino (250-290 gr) erkek sıçanlar kontrol, kronik stres grubu ve kronik strese maruz kalan ve NPW ile tedavi edilen (0.1 µg/kg, subkutan) grup olarak rastgele ayrıldı. Kronik stres indüksiyonu hayvanlara art arda on gün boyunca günde 1 saat sudan kaçınma stresi (WAS) uygulanarak yapıldı. Deneysel stres işleminin sonunda bilişsel işlevleri değerlendirmek için obje tanıma testi, kaygı düzeylerini değerlendirmek için delikli tahta testi kullanıldı. Deneylerden sonra, kortikosteron seviyelerini ölçmek için kan örnekleri alındı.
Bulgular: Kontrol sıçanları ile karşılaştırıldığında WAS grubunda kortikosteron seviyesinde anlamlı artış görüldü (p<0.05), bu da HPA ekseninin aktivasyonunu göstermektedir. WAS uygulanması ayrıca kaygıya ve bilişsel işlevlerin azalmasına neden oldu. WAS uygulanıp NPW ile tedavi edilen sıçanlarda, kortikosteron seviyesi kontrol grubundan farklı değildi. NPW tedavisi, WAS ile indüklenen sıçanlarda şaha kalkma ve burun sokma sayılarını artırdı (p<0.05-0.01) ve immobilizasyon süresini azalttı (p<0.01). Ayrıca WAS grubunda NPW uygulaması ile obje tanıma testinde fark skoru arttı(p< 0.05).
Sonuç: Sonuçlarımız ilk kez NPW ön tedavisinin sudan kaçınma stresi uygulanan sıçanlarda anksiyolitik etki gösterdiğini ve bilişsel işlevi hafiflettiğini gösterdi.
Project Number
program code: 2209, project no: 1919B012204884
References
- Bustamante-Sánchez Á, Tornero-Aguilera JF, Fernández-Elías VE, Hormeño-Holgado AJ, Dalamitros AA, Clemente-Suárez VJ. Effect of Stress on Autonomic and Cardiovascular Systems in Military Population: A Systematic Review. Cardiol Res Pract. 2020;2020:7986249.
- Karin O, Raz M, Tendler A, et al. A new model for the HPA axis explains dysregulation of stress hormones on the timescale of weeks. Mol Syst Biol. 2020;16(7):e9510.
- Choobdar S, Vafaei AA, Sedaghat K. Protective role of vitamin-D on chronic stress induced-learning and memory deficits in rats. Koomesh. 2019;21(4): 708-715.
- Kasimay Cakir O, Ellek N, Salehin N, et al. Protective effect of low dose caffeine on psychological stress and cognitive function. Physiol Behav. 2017;168:1-10. doi:10.1016/j.physbeh.2016.10.010.
- Zhang H, Wei M, Sun Q, et al. Lycopene ameliorates chronic stress-induced hippocampal injury and subsequent learning and memory dysfunction through inhibiting ROS/JNK signaling pathway in rats. Food Chem Toxicol. 2020;145:111688. doi:10.1016/j.fct.2020.111688
- Algamal M, Pearson AJ, Hahn-Townsend C, et al. Repeated unpredictable stress and social isolation induce chronic HPA axis dysfunction and persistent abnormal fear memory. Prog Neuropsychopharmacol Biol Psychiatry. 2021;104:110035. doi:10.1016/j.pnpbp.2020.110035
- Leistner C, Menke A. Hypothalamic-pituitary-adrenal axis and stress. Handb Clin Neurol. 2020;175:55-64.
doi:10.1016/B978-0-444-64123-6.00004-7
- Juszczyk G, Mikulska J, Kasperek K, Pietrzak D, Mrozek W, Herbet M. Chronic Stress and Oxidative Stress as Common Factors of the Pathogenesis of Depression and Alzheimer's Disease: The Role of Antioxidants in Prevention and Treatment. Antioxidants (Basel). 2021;10(9):1439. Published 2021 Sep 9. doi:10.3390/antiox10091439
- Shimomura Y, Harada M, Goto M, et al. Identification of neuropeptide W as the endogenous ligand for orphan G-protein-coupled receptors GPR7 and GPR8. J Biol Chem. 2002;277(39):35826-35832. doi:10.1074/jbc.M205337200
- Fujii R, Yoshida H, Fukusumi S, et al. Identification of a neuropeptide modified with bromine as an endogenous ligand for GPR7. J Biol Chem. 2002;277(37):34010-34016. doi:10.1074/jbc.M205883200
- Niimi M, Murao K. Neuropeptide W as a stress mediator in the hypothalamus. Endocrine. 2005;27(1):51-54. doi:10.1385/ENDO:27:1:051
- Koyuncuoglu T, Ipek BE, Dertsiz EK, Akakin D, Yuksel M, Yegen BC. The neuroprotective effects of neuropeptide W in newborn rats with cerebral palsy. In Acta Physiologica. 2019;227:87-87.
- Arabacı Tamer S, Akbulut S, Peker Eyüboğlu İ, et al. Peripheral administration of Neuropeptide-W protects against stress-induced gastric injury in rats. Life Sci. 2022;310:121087. doi:10.1016/j.lfs.2022.121087
- Arabacı Tamer S, Üçem S, Büke B, et al. Regular moderate exercise alleviates gastric oxidative damage in rats via the contribution of oxytocin receptors. J Physiol. 2020;598(12):2355-2370. doi:10.1113/JP279577
- Koyuncuoğlu T, Sevim H, Çetrez N, et al. High intensity interval training protects from Post Traumatic Stress Disorder induced cognitive impairment. Behav Brain Res. 2021;397:112923. doi:10.1016/j.bbr.2020.112923
- Agorastos A, Chrousos GP. The neuroendocrinology of stress: the stress-related continuum of chronic disease development. Mol Psychiatry. 2022;27(1):502-513.
doi:10.1038/s41380-021-01224-9
- Chen P, Li X, Yu Y, et al. Administration Time and Dietary Patterns Modified the Effect of Inulin on CUMS-Induced Anxiety and Depression. Mol Nutr Food Res. 2023;67(8):e2200566. doi:10.1002/mnfr.202200566
- Liu C, Shi R, Liu Y, et al. Low-frequency transcranial magnetic stimulation protects cognition in mice with chronic unpredictable mild stress through autophagy regulation. Behav Brain Res. 2023;444:114366. doi:10.1016/j.bbr.2023.114366
- Mello AF, Mello MF, Carpenter LL, Price LH. Update on stress and depression: the role of the hypothalamic-pituitary-adrenal (HPA) axis. Braz J Psychiatry. 2003;25(4):231-238. doi:10.1590/s1516-44462003000400010
- Mizoguchi K, Shoji H, Ikeda R, Tanaka Y, Tabira T. Persistent depressive state after chronic stress in rats is accompanied by HPA axis dysregulation and reduced prefrontal dopaminergic neurotransmission. Pharmacol Biochem Behav. 2008;91(1):170-175. doi:10.1016/j.pbb.2008.07.002
- Lim DW, Han D, Lee C. Pedicularis resupinata Extract Prevents Depressive-like Behavior in Repeated Corticosterone-Induced Depression in Mice: A Preliminary Study. Molecules. 2022;27(11):3434. Published 2022 May 26. doi:10.3390/molecules27113434
- Vinkers CH, Kuzminskaite E, Lamers F, Giltay EJ, Penninx BWJH. An integrated approach to understand biological stress system dysregulation across depressive and anxiety disorders. J Affect Disord. 2021;283:139-146. doi:10.1016/j.jad.2021.01.051
- Eliwa H, Brizard B, Le Guisquet AM, Hen R, Belzung C, Surget A. Adult neurogenesis augmentation attenuates anhedonia and HPA axis dysregulation in a mouse model of chronic stress and depression. Psychoneuroendocrinology. 2021;124:105097. doi:10.1016/j.psyneuen.2020.105097
- Gao K, Farzi A, Ke X, et al. Oral administration of Lactococcus lactis WHH2078 alleviates depressive and anxiety symptoms in mice with induced chronic stress. Food Funct. 2022;13(2):957-969. Published 2022 Jan 24. doi:10.1039/d1fo03723d
- West EG, McDermott C, Chess-Williams R, Sellers DJ. Partial recovery of voiding function in female mice following repeated psychological stress exposure. PLoS One. 2022;17(4):e0266458. Published 2022 Apr 21. doi:10.1371/journal.pone.0266458
- Atici AE, Arabacı Tamer S, Levent HN, et al. Neuropeptide W Attenuates Oxidative Multi-Organ Injury in Rats Induced with Intra-Abdominal Sepsis. Inflammation. 2022;45(1):279-296. doi:10.1007/s10753-021-01545-5
- Mazzocchi G, Rebuffat P, Ziolkowska A, Rossi GP, Malendowicz LK, Nussdorfer GG. G protein receptors 7 and 8 are expressed in human adrenocortical cells, and their endogenous ligands neuropeptides B and w enhance cortisol secretion by activating adenylate cyclase- and phospholipase C-dependent signaling cascades. J Clin Endocrinol Metab. 2005;90(6):3466-3471. doi:10.1210/jc.2004-2132
- Hochol A, Belloni AS, Rucinski M, et al. Expression of neuropeptides B and W and their receptors in endocrine glands of the rat. Int J Mol Med. 2006;18(6):1101-1106.
- Zareie M, Johnson-Henry K, Jury J, et al. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut. 2006;55(11):1553-1560. doi:10.1136/gut.2005.080739
- Bozorgi H, Rashidy-Pour A, Moradikor N, et al. Reversal of chronic restraint stress-induced memory impairment by Japanese sake yeast supplement in mice: Role of adenosine A1 and A2A receptors. J Psychiatr Res. 2023;161:123-131. doi:10.1016/j.jpsychires.2023.02.033
- Ahmed Z, Tokhi A, Arif M, et al. Fraxetin attenuates disrupted behavioral and central neurochemical activity in a model of chronic unpredictable stress. Front Pharmacol. 2023;14:1135497. Published 2023 Mar 23. doi:10.3389/fphar.2023.1135497
- Kageyama K, Iwasaki Y, Daimon M. Hypothalamic Regulation of Corticotropin-Releasing Factor under Stress and Stress Resilience. Int J Mol Sci. 2021;22(22):12242. Published 2021 Nov 12. doi:10.3390/ijms222212242
- Welcome MO. Cellular mechanisms and molecular signaling pathways in stress-induced anxiety, depression, and blood-brain barrier inflammation and leakage. Inflammopharmacology. 2020;28(3):643-665. doi:10.1007/s10787-020-00712-8.
- Qin D, Wang J, Le A, Wang TJ, Chen X, Wang J. Traumatic Brain Injury: Ultrastructural Features in Neuronal Ferroptosis, Glial Cell Activation and Polarization, and Blood-Brain Barrier Breakdown. Cells. 2021;10(5):1009. Published 2021 Apr 24. doi:10.3390/cells10051009
- Yan Y, Xu X, Chen R, et al. Down-regulation of MST1 in hippocampus protects against stress-induced depression-like behaviours and synaptic plasticity impairments. Brain Behav Immun. 2021;94:196-209. doi:10.1016/j.bbi.2021.02.007
- Lei H, Zhang Y, Huang L, et al. L-3-n-Butylphthalide Regulates Proliferation, Migration, and Differentiation of Neural Stem Cell In Vitro and Promotes Neurogenesis in APP/PS1 Mouse Model by Regulating BDNF/TrkB/CREB/Akt Pathway. Neurotox Res. 2018;34(3):477-488. doi:10.1007/s12640-018-9905-3
- Choi GY, Kim HB, Cho JM, et al. Umbelliferone Ameliorates Memory Impairment and Enhances Hippocampal Synaptic Plasticity in Scopolamine-Induced Rat Model. Nutrients. 2023;15(10):2351. Published 2023 May 17. doi:10.3390/nu15102351
- Wang R, Yan F, Liao R, Wan P, Little PJ, Zheng W. Role of brain-derived neurotrophic factor and nerve growth factor in the regulation of Neuropeptide W in vitro and in vivo. Mol Cell Endocrinol. 2017;447:71-78. doi:10.1016/j.mce.2017.02.040
- Taylor MM, Yuill EA, Baker JR, et al. Actions of neuropeptide W in paraventricular hypothalamus: implications for the control of stress hormone secretion. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R270-R275. doi:10.1152/ajpregu.00396.2004
- Yogo K, Oki Y, Iino K, et al. Neuropeptide W stimulates adrenocorticotrophic hormone release via corticotrophin-releasing factor but not via arginine vasopressin. Endocr J. 2012;59(7):547-554. doi:10.1507/endocrj.ej11-0221
- Hu Y, Li H, Zhang J, et al. Periodontitis Induced by P. gingivalis-LPS Is Associated With Neuroinflammation and Learning and Memory Impairment in Sprague-Dawley Rats. Front Neurosci. 2020;14:658. Published 2020 Jul 2. doi:10.3389/fnins.2020.00658
- Michelucci A, Heurtaux T, Grandbarbe L, Morga E, Heuschling P. Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: Effects of oligomeric and fibrillar amyloid-beta. J Neuroimmunol. 2009;210(1-2):3-12. doi:10.1016/j.jneuroim.2009.02.003