Grape seed extract effects on hippocampal neurogenesis, synaptogenesis and dark neurons production in old mice. Can this extract improve learning and memory in aged animals?

References

• Khoshdel-Sarkarizi H, Hami J, Mohammadipour A, Sadr-Nabavi A, Mahmoudi M, Kheradmand H, et al. Developmental regulation and lateralization of GABA receptors in the rat hippocampus. Int J Dev Neurosci. 2019;76:86–94. doi:10.1016/j.ijdevneu.2019.07.006.
   PubMed Web of Science ®Google Scholar
• Rastegar-Moghaddam SHR, Mohammadipour A, Hosseini M, Bargi R, Ebrahimzadeh-Bideskan A. Maternal exposure to atrazine induces the hippocampal cell apoptosis in mice offspring and impairs their learning and spatial memory. Toxin Reviews. 2019;38(4):298–306. doi:10.1080/15569543.2018.1466804.
   Web of Science ®Google Scholar
• Baghishani F, Mohammadipour A, Hosseinzadeh H, Hosseini M, Ebrahimzadeh-Bideskan A. The effects of tramadol administration on hippocampal cell apoptosis, learning and memory in adult rats and neuroprotective effects of crocin. Metab Brain Dis. 2018;33(3):907–916. doi:10.1007/s11011-018-0194-6.
   PubMed Web of Science ®Google Scholar
• Baradaran R, Khoshdel-Sarkarizi H, Kargozar S, Hami J, Mohammadipour A, Sadr-Nabavi A, et al. Developmental regulation and lateralisation of the α7 and α4 subunits of nicotinic acetylcholine receptors in developing rat hippocampus. Int J Dev Neurosci. 2020;80(4):303–318. doi:10.1002/jdn.10026.
   PubMed Web of Science ®Google Scholar
• Ebrahimzadeh Bideskan A, Mohammadipour A, Fazel A, Haghir H, Rafatpanah H, Hosseini M, et al. Maternal exposure to titanium dioxide nanoparticles during pregnancy and lactation alters offspring hippocampal mRNA BAX and Bcl-2 levels, induces apoptosis and decreases neurogenesis. Exp Toxicol Pathol. 2017;69(6):329–337. doi:10.1016/j.etp.2017.02.006.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Loh HH, Law PY. Effect of Opioid on Adult Hippocampal Neurogenesis. Scientific World Journal. 2016;2016:2601264. doi:10.1155/2016/2601264.
   Google Scholar
• Anacker C, Hen R. Adult hippocampal neurogenesis and cognitive flexibility - linking memory and mood. Nat Rev Neurosci. 2017;18(6):335–346. doi:10.1038/nrn.2017.45.
   PubMed Web of Science ®Google Scholar
• Katsimpardi L, Lledo PM. Regulation of neurogenesis in the adult and aging brain. Curr Opin Neurobiol. 2018;53:131–138. doi:10.1016/j.conb.2018.07.006.
   PubMed Web of Science ®Google Scholar
• Gebara E, Sultan S, Kocher-Braissant J, Toni N. Adult hippocampal neurogenesis inversely correlates with microglia in conditions of voluntary running and aging. Front Neurosci. 2013;7:145. doi:10.3389/fnins.2013.00145.
   PubMed Web of Science ®Google Scholar
• Shen K, Cowan CW. Guidance molecules in synapse formation and plasticity. Cold Spring Harb Perspect Biol. 2010;2(4):a001842. doi:10.1101/cshperspect.a001842.
   PubMed Web of Science ®Google Scholar
• Tolias KF, Duman JG, Um K. Control of synapse development and plasticity by Rho GTPase regulatory proteins. Prog Neurobiol. 2011;94(2):133–48. doi:10.1016/j.pneurobio.2011.04.011.
   PubMed Web of Science ®Google Scholar
• Rothman SM, Mattson MP. Adverse stress, hippocampal networks, and Alzheimer's disease. Neuromolecular Med. 2010;12(1):56–70. doi:10.1007/s12017-009-8107-9.
   PubMed Web of Science ®Google Scholar
• Ho N, Sommers MS, Lucki I. Effects of diabetes on hippocampal neurogenesis: links to cognition and depression. Neurosci Biobehav Rev. 2013;37(8):1346–62. doi:10.1016/j.neubiorev.2013.03.010.
   PubMed Web of Science ®Google Scholar
• Song C, Wang H. Cytokines mediated inflammation and decreased neurogenesis in animal models of depression. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35(3):760–8. doi:10.1016/j.pnpbp.2010.06.020.
   PubMed Web of Science ®Google Scholar
• Kopustinskiene DM, Jakstas V, Savickas A, Bernatoniene J. Flavonoids as Anticancer Agents. Nutrients. 2020;12(2):457. doi:10.3390/nu12020457.
   PubMed Web of Science ®Google Scholar
• Xu L, Long J, Su Z, Xu B, Lin M, Chen Y, et al. Restored presynaptic synaptophysin and cholinergic inputs contribute to the protective effects of physical running on spatial memory in aged mice. Neurobiol Dis. 2019;132:104586. doi:10.1016/j.nbd.2019.104586.
   PubMed Web of Science ®Google Scholar
• Cichon N, Saluk-Bijak J, Gorniak L, Przyslo L, Bijak M. Flavonoids as a Natural Enhancer of Neuroplasticity-an Overview of the Mechanism of Neurorestorative Action. Antioxidants Basel. 2020;9(11):1035. doi:10.3390/antiox9111035.
   Web of Science ®Google Scholar
• Godos J, Caraci F, Castellano S, Currenti W, Galvano F, Ferri R, et al. Association Between Dietary Flavonoids Intake and Cognitive Function in an Italian Cohort. Biomolecules. 2020;10(9G):1300. doi:10.3390/biom10091300.
   Google Scholar
• Dias GP, Cavegn N, Nix A, et al. The role of dietary polyphenols on adult hippocampal neurogenesis: molecular mechanisms and behavioural effects on depression and anxiety. Oxid Med Cell Longev. 2012;2012:541971. doi:10.1155/2012/541971.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang Y, Shen W, Wang Y, Cao Y, Nuerbulati N, et al. Grape seed Polyphenols Ameliorated Dextran Sulfate Sodium-induced Colitis via Suppression of Inflammation and Apoptosis. Pharmacology. 2020;105(1-2):9–18. doi:10.1159/000501897.
   PubMed Web of Science ®Google Scholar
• Barbe A, Ramé C, Mellouk N, Estienne A, Bongrani A, Brossaud A, et al. Effects of Grape Seed Extract and Proanthocyanidin B2 on in Vitro Proliferation, Viability, Steroidogenesis, Oxidative Stress, and Cell Signaling in Human Granulosa Cells. Int J Mol Sci. 2019;20(17):4215. doi:10.3390/ijms20174215.
   PubMed Web of Science ®Google Scholar
• Irak K, Yıldırım S, Mert H, Mert N. Grape seed extract effects on serum amylase levels and immunohistochemical alterations in Streptozotocin-induced diabetic rats. Cell Mol Biol (Noisy-le-Grand). 2018;64(4):92–97. PMID: 29631689.
   PubMed Web of Science ®Google Scholar
• Nassiri-Asl M, Hosseinzadeh H. Review of the pharmacological effects of Vitis vinifera (Grape) and its bioactive compounds. Phytother Res. 2009;23(9):1197–1204. doi:10.1002/ptr.2761.
   PubMed Web of Science ®Google Scholar
• Yilmaz Y, Toledo RT. Major flavonoids in grape seeds and skins: antioxidant capacity of catechin, epicatechin, and gallic acid. J Agric Food Chem. 2004;52(2):255–260. doi:10.1021/jf030117h.
   PubMed Web of Science ®Google Scholar
• Georgiev V, Ananga A, Tsolova V. Recent advances and uses of grape flavonoids as nutraceuticals. Nutrients. 2014;6(1):391–415. doi:10.3390/nu6010391.
   PubMed Web of Science ®Google Scholar
• Facino R M, Carini M, Aldini G, Bombardelli E, Morazzoni P, Morelli R. Free radicals scavenging action and anti-enzyme activities of procyanidines from Vitis vinifera. A mechanism for their capillary protective action. Arzneimittelforschung. 1994;44(5):592–601.
   PubMed Web of Science ®Google Scholar
• Abhijit S, Tripathi SJ, Bhagya V, Shankaranarayana Rao BS, Subramanyam MV, Asha Devi S. Antioxidant action of grape seed polyphenols and aerobic exercise in improving neuronal number in the hippocampus is associated with decrease in lipid peroxidation and hydrogen peroxide in adult and middle-aged rats. Exp Gerontol. 2018;101:101–112. doi:10.1016/j.exger.2017.11.012.
   PubMed Web of Science ®Google Scholar
• Karimooy FN, Bideskan AE, Pour AM, Hoseini SM. Neurotoxic Effects of Stanozolol on Male Rats’ Hippocampi: Does Stanozolol Cause Apoptosis? Biomol Concepts. 2019;10(1):73–81. doi:10.1515/bmc-2019-0009.
   PubMedGoogle Scholar
• Heidari Z, Mohammadipour A, Haeri P, Ebrahimzadeh-Bideskan A. The effect of titanium dioxide nanoparticles on mice midbrain substantia nigra. Iran J Basic Med Sci. 2019;22(7):745–751. doi:10.22038/ijbms.2019.33611.8018.
   PubMed Web of Science ®Google Scholar
• Darweesh RS, El-Elimat T, Zayed A, Khamis TN, Babaresh WM, Arafat T, et al. The effect of grape seed and green tea extracts on the pharmacokinetics of imatinib and its main metabolite, N-desmethyl imatinib, in rats. BMC Pharmacol Toxicol. 2020;21(1):77. doi:10.1186/s40360-020-00456-9.
   PubMed Web of Science ®Google Scholar
• Satyam SM, Bairy LK, Pirasanthan R, Vaishnav RL. Grape Seed Extract and Zinc containing nutritional food supplement delays onset and progression of streptozocin-induced diabetic cataract in Wistar rats. J Food Sci Technol. 2015;52(5):2824–32. doi:10.1007/s13197-014-1305-y.
   PubMed Web of Science ®Google Scholar
• Charradi K, Elkahoui S, Karkouch I, Limam F, Hamdaoui G, Ben Hassine F, et al. Grape seed and skin extract alleviates high-fat diet-induced renal lipotoxicity and prevents copper depletion in rat. Appl Physiol Nutr Metab. 2013;38(3):259–67. doi:10.1139/apnm-2012-0416.
   PubMed Web of Science ®Google Scholar
• Abdou HM, Wahby MM. Neuroprotection of Grape Seed Extract and Pyridoxine Against Triton-induced Neurotoxicity. Oxid Med Cell Longev. 2016;2016:8679506. doi:10.1155/2016/8679506.
   PubMed Web of Science ®Google Scholar
• Mohammadipour A, Hosseini M, Fazel A, Haghir H, Rafatpanah H, Pourganji M, et al. The effects of exposure to titanium dioxide nanoparticles during lactation period on learning and memory of rat offspring. Toxicol Ind Health. 2016;32(2):221–8. doi:10.1177/0748233713498440.
   PubMed Web of Science ®Google Scholar
• Haeri P, Mohammadipour A, Heidari Z, Ebrahimzadeh-Bideskan A. Neuroprotective effect of crocin on substantia nigra in MPTP-induced Parkinson's disease model of mice. Anat Sci Int. 2019;94(1):119–127. doi:10.1007/s12565-018-0457-7.
   PubMed Web of Science ®Google Scholar
• Fani M, Mohammadipour A, Ebrahimzadeh-Bideskan A. The effect of crocin on testicular tissue and sperm parameters of mice offspring from mothers exposed to atrazine during pregnancy and lactation periods: An experimental study. Int J Reprod Biomed. 2018;16(8):519–528. PMCID: PMC6163052.
   PubMed Web of Science ®Google Scholar
• Lieberwirth C, Pan Y, Liu Y, Zhang Z, Wang Z. Hippocampal adult neurogenesis: Its regulation and potential role in spatial learning and memory. Brain Res. 2016;1644:127–40. doi:10.1016/j.brainres.2016.05.015.
   PubMed Web of Science ®Google Scholar
• Oomen CA, Bekinschtein P, Kent BA, Saksida LM, Bussey TJ. Adult hippocampal neurogenesis and its role in cognition. Wiley Interdiscip Rev Cogn Sci. 2014;5(5):573–587. doi:10.1002/wcs.1304.
   PubMed Web of Science ®Google Scholar
• Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci. 2005;21(1):1–14. doi:10.1111/j.1460-9568.2004.03813.x.
   PubMed Web of Science ®Google Scholar
• Kuhn HG, Toda T, Gage FH. Adult hippocampal neurogenesis: A Coming-of-age Story. J Neurosci. 2018;38(49):10401–10410. doi:10.1523/JNEUROSCI.2144-18.2018.
   PubMed Web of Science ®Google Scholar
• Kase Y, Otsu K, Shimazaki T, Okano H. Involvement of p38 in Age-Related Decline in Adult Neurogenesis via Modulation of Wnt Signaling. Stem Cell Reports. 2019;12(6):1313–1328. doi:10.1016/j.stemcr.2019.04.010.
   PubMed Web of Science ®Google Scholar
• Shruster A, Melamed E, Offen D. Neurogenesis in the aged and neurodegenerative brain. Apoptosis. 2010;15(11):1415–1421. doi:10.1007/s10495-010-0491-y.
   PubMed Web of Science ®Google Scholar
• Kempermann G, Song H, Gage FH. Neurogenesis in the Adult Hippocampus. Cold Spring Harb Perspect Biol. 2015;7(9):a018812. doi:10.1101/cshperspect.a018812.
   PubMed Web of Science ®Google Scholar
• Ferreira FF, Ribeiro FF, Rodrigues RS, Sebastião AM, Xapelli S. Brain-Derived Neurotrophic Factor (BDNF) Role in Cannabinoid-Mediated Neurogenesis. Front Cell Neurosci. 2018;12:441. doi:10.3389/fncel.2018.00441.
   PubMed Web of Science ®Google Scholar
• Liu PZ, Nusslock R. Exercise-Mediated Neurogenesis in the Hippocampus via BDNF. Front Neurosci. 2018;12:52. doi:10.3389/fnins.2018.00052.
   PubMed Web of Science ®Google Scholar
• Reyes-Izquierdo T, Nemzer B, Shu C, et al. Modulatory effect of coffee fruit extract on plasma levels of brain-derived neurotrophic factor in healthy subjects. Br J Nutr. 2013;110(3):420–425. doi:10.1017/S0007114512005338.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Liu Y, Zhu C, Ma X, Ma L, Zhou L, et al. Minocycline enhances hippocampal memory, neuroplasticity and synapse-associated proteins in aged C57 BL/6 mice. Neurobiol Learn Mem. 2015;121:20–29. doi:10.1016/j.nlm.2015.03.003.
   PubMed Web of Science ®Google Scholar
• Nemes AD, Ayasoufi K, Ying Z, Zhou QG, Suh H, Najm IM. Growth Associated Protein 43 (GAP-43) as a Novel Target for the Diagnosis, Treatment and Prevention of Epileptogenesis. Sci Rep. 2017;7(1):17702. doi:10.1038/s41598-017-17377-z.
   PubMedGoogle Scholar
• Björkholm C, Monteggia LM. BDNF - a key transducer of antidepressant effects. Neuropharmacology. 2016;102:72–9. doi:10.1016/j.neuropharm.2015.10.034.
   PubMed Web of Science ®Google Scholar
• Mohammadipour A, Fazel A, Haghir H, Motejaded F, Rafatpanah H, Zabihi H, et al. Maternal exposure to titanium dioxide nanoparticles during pregnancy; impaired memory and decreased hippocampal cell proliferation in rat offspring. Environ Toxicol Pharmacol. 2014;37(2):617–25. doi:10.1016/j.etap.2014.01.014.
   PubMed Web of Science ®Google Scholar
• Tönnies E, Trushina E. Oxidative Stress, Synaptic Dysfunction, and Alzheimer's Disease. J Alzheimers Dis. 2017;57(4):1105–1121. doi:10.3233/JAD-161088.
   PubMed Web of Science ®Google Scholar
• Singh AK, Singh SK, Nandi MK, Mishra G, Maurya A, Rai A, et al. Berberine: a Plant-Derived Alkaloid with Therapeutic Potential to Combat Alzheimer's Disease. Cent Nerv Syst Agents Med Chem. 2019;19(3):154–170. doi:10.2174/1871524919666190820160053.
   PubMedGoogle Scholar
• Bobadilla M, García-Sanmartín J, Martínez A. Natural food Supplements Reduce Oxidative Stress in Primary Neurons and in the Mouse Brain, Suggesting applications in the prevention of neurodegenerative diseases. Antioxidants (Basel). 2021;10(1):46. doi:10.3390/antiox10010046.
   Google Scholar
• Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol. 2009;7(1):65–74. doi:10.2174/157015909787602823.
   PubMed Web of Science ®Google Scholar
• Ben Youssef S, Brisson G, Doucet-Beaupré H, Castonguay AM, Gora C, Amri M, et al. Neuroprotective benefits of grape seed and skin extract in a mouse model of Parkinson's disease [published online ahead of print, 2019 May 25]. Nutr Neurosci. 2019: 1–15. doi:10.1080/1028415X.2019.1616435.
   Web of Science ®Google Scholar
• Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA. 2003;100(23):13632–13637. doi:10.1073/pnas.2234031100.
   PubMed Web of Science ®Google Scholar
• Wang YJ, Thomas P, Zhong JH, Bi FF, Kosaraju S, Pollard A, et al. Consumption of grape seed extract prevents amyloid-beta deposition and attenuates inflammation in brain of an Alzheimer's disease mouse. Neurotox Res. 2009;15(1):3–14. doi:10.1007/s12640-009-9000-x.
   PubMed Web of Science ®Google Scholar