The effect of experimentally-induced diabetes on rat hippocampus and the potential neuroprotective effect of Cerebrolysin combined with insulin. A histological and immunohistochemical study

References

• Rashedinia M, Alimohammadi M, Shalfroushan N, et al. Neuroprotective effect of syringic acid by modulation of oxidative stress and mitochondrial mass in diabetic rats. Bio Med Res Int. 2020;2020:8297984.
   Google Scholar
• Elgayar S. Protective effect of vitamin B complex in diabetic peripheral neuropathy - Histopathological study. Eur J Anat. 2017;21(3):173–187.
   Google Scholar
• Chandrakala BS, Kate NN, Kamalakannan V, et al. Effect of hormones on cognitive abilities and skills. National J Physiol Pharm Pharmacol. 2019;9(8):788.
   Google Scholar
• Karvani M, Simos P, Stavrakaki S, et al. Neurocognitive impairment in type 2 diabetes mellitus. Hormones. 2019;18(4):523–534. DOI:10.1007/s42000-019-00128-2
   PubMedGoogle Scholar
• Cherubini E, Miles R. The CA3 Region of the Hippocampus: how is it? What is it for? How does it do it? Front Cell Neurosci. 2015;9:4–6.
   PubMed Web of Science ®Google Scholar
• Schröder H, Moser N, Huggenberger S. The mouse Hippocampus. Neuroanatomy of the mouse: an introduction. Cham, Sprielgay: Springer International Publishing; 2020. pp. 267–288.
   Google Scholar
• Abbott LC, Nigussie FJ. Adult neurogenesis in the mammalian dentate gyrus. Anat Histol Embryol. 2020;49(1):3–16.
   PubMed Web of Science ®Google Scholar
• Abdel-Aziz H, Ahmed SM, Mohammed MZ, et al. Efficacy of cerebrolysin on dentate gyrus of hippocampus after experimentally induced acute ischemic stroke in adult albino rats (Histological, immunohistochemical and biochemical study). Egypt J Histol. 2019;42(1):229–244. DOI:10.21608/EJH.2018.4314.1013
   Google Scholar
• Yu L-Y, Pei YJ. Insulin neuroprotection and the mechanisms. Chinese Med J. 2015;128(7):976–981.
   PubMed Web of Science ®Google Scholar
• Gabbouj S, Ryhänen S, Marttinen M, et al. Altered insulin signaling in Alzheimer’s disease brain–special emphasis on PI3K-Akt pathway. Front Neurosci. 2019;13:629.
   PubMed Web of Science ®Google Scholar
• Ren Z, Zhong H, Song C, et al. Insulin promotes mitochondrial respiration and survival through PI3K/AKT/GSK3 pathway in human embryonic stem cells. Stem Cell Rep. 2020;15(6):1362–1376. DOI:10.1016/j.stemcr.2020.10.008
   PubMed Web of Science ®Google Scholar
• Bliźniewska-Kowalska K, Łukasik M, Gałecki P. Cerebrolysin–mechanism of action and application in psychiatry and neurology. Pharmacother Psychiatr Neurol. 2019;35(1):9–23.
   Google Scholar
• Azad A, Sulaiman W. Antidiabetic effects of P. macrocarpa ethanolic fruit extract in streptozotocin-induced diabetic rats. Future J Pharm Sci. 2020;6:1–12.
   Web of Science ®Google Scholar
• Jarrar YB, Al-Essa L, Kilani A, et al. Alterations in the gene expression of drug and arachidonic acid-metabolizing Cyp450 in the livers of controlled and uncontrolled insulin-dependent diabetic mice. Diabetes Metab Syndr Obesity. 2018;11:483–492.
   PubMed Web of Science ®Google Scholar
• Dong HY, Jiang XM, Niu CB, et al. Cerebrolysin improves sciatic nerve dysfunction in a mouse model of diabetic peripheral neuropathy. Neural Regen Res. 2016;11(1):156–162.
   PubMed Web of Science ®Google Scholar
• Bancroft JD, Layton C The hematoxylins and eosin. Bancroft’s theory and practice of histological techniques e-book. 8th ed. Suvarna KS, Layton C, Bancroft JD. China: Elsevier Health Sciences. 2018; 126–138
   Google Scholar
• Sanderson T, Wild G, Cull A, et al. Immunohistochemical and immunofluorescent techniques. Bancroft’s theory and practice of histological techniques e-book. 8th. Suvarna K, Layton C, and Bancroft J. China: Elsevier Health Sciences. 2018; pp. 337–394
   Google Scholar
• Khushman M, Bhardwaj A, Patel GK, et al. Exosomal Markers (CD63 and CD9) expression pattern using immunohistochemistry in resected malignant and non-malignant pancreatic specimens. Pancreas. 2017;46(6):782–788.
   PubMed Web of Science ®Google Scholar
• Bathina S, Das UN. Dysregulation of PI3K-Akt-mTOR pathway in brain of streptozotocin-induced type 2 diabetes mellitus in Wistar rats. Lipids Health Dis. 2018;17(1):1–11.
   PubMedGoogle Scholar
• Akinlade OM, Owoyele BV, Soladoye AO. Streptozotocin-induced type 1 and 2 diabetes in rodents: a model for studying diabetic cardiac autonomic neuropathy. Afr Health Sci. 2021;21(2):719–727.
   PubMed Web of Science ®Google Scholar
• Soleymaninejad M, Joursaraei SG, Feizi F, et al. The effects of lycopene and insulin on histological changes and the expression level of Bcl-2 family genes in the hippocampus of streptozotocin-induced diabetic rats. J Diabetes Res. 2017;2017:1–9.
   Web of Science ®Google Scholar
• Wang Y, Sun H, Zhang J, et al. Streptozotocin-induced diabetic cardiomyopathy in rats: ameliorative effect of PIPERINE via Bcl2, Bax/Bcl2, and caspase-3 pathways. Biosci Biotechnol Biochem. 2020;84(12):2533–2544. DOI:10.1080/09168451.2020.1815170
   PubMed Web of Science ®Google Scholar
• Ali AA, Essawy EA, Hamed HS, et al. The ameliorative role of Physalis pubescens L. against neurological impairment associated with streptozotocin induced diabetes in rats. Metab Brain Dis. 2021;36(6):1191–1200.
   PubMed Web of Science ®Google Scholar
• Furman BL. Streptozotocin‐induced diabetic models in mice and rats. Curr Protoc Pharmacol. 2021;1(4):e78.
   Google Scholar
• Ruegsegger GN, Creo AL, Cortes TM, et al. Altered mitochondrial function in insulin-deficient and insulin-resistant states. J Clin Invest. 2018;128(9):3671–3681.
   PubMed Web of Science ®Google Scholar
• Gavrilova SI, Alvarez AJ. Cerebrolysin in the therapy of mild cognitive impairment and dementia due to Alzheimer’s disease: 30 years of clinical use. Med Res Rev. 2021;41(5):2775–2803.
   PubMed Web of Science ®Google Scholar
• Farshid AA, Tamaddonfard E, Moradi-Arzeloo M, et al. The effects of crocin, insulin and their co-administration on the heart function and pathology in streptozotocin-induced diabetic rats. Avicenna J Phytomed. 2016;6(6):658. DOI:10.22038/ajp.2016.6775
   PubMed Web of Science ®Google Scholar
• Tomkin GH, Owens D. Diabetes and dyslipidemia: characterizing lipoprotein metabolism. Diabetes Metab Syndr Obesity. 2017;10:333–343.
   PubMed Web of Science ®Google Scholar
• Brown A, Guess N, Dornhorst A, et al. Insulin‐associated weight gain in obese type 2 diabetes mellitus patients: what can be done? Diabetes Obesity Metab. 2017;19(12):1655–1668. DOI:10.1111/dom.13009
   PubMed Web of Science ®Google Scholar
• Mesinovic J, Zengin A, De Courten B, et al. Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship. Diabetes Metab Syndr Obesity. 2019;12:1057–1072.
   PubMed Web of Science ®Google Scholar
• Georgy GS, Nassar NN, Mansour HA, et al. Cerebrolysin ameliorates cognitive deficits in type III diabetic rats. PLoS ONE. 2013;8(6):e64847. DOI:10.1371/journal.pone.0064847
   PubMed Web of Science ®Google Scholar
• Keshvari M, Rahmati M, Mirnasouri R, et al. Effects of endurance exercise and Urtica dioica on the functional, histological and molecular aspects of the hippocampus in STZ-Induced diabetic rats. J Ethnopharmacol. 2020;256:112801.
   PubMed Web of Science ®Google Scholar
• Woelfle S, Boeckers TM. Layer-specific vesicular glutamate transporter 1 immunofluorescence levels delineate all layers of the human hippocampus including the Stratum lucidum. Front Cell Neurosci. 2021;15:789903.
   PubMed Web of Science ®Google Scholar
• Sinha JK, Aziz A, Ghosh S. Dentate Gyrus. In: Encyclopedia of animal cognition and behavior. Vonk J, and Shackelford T. New York: Cham, Springer International Publishing. 2019; pp. 1–5
   Google Scholar
• Ghosh HS. Adult neurogenesis and the promise of adult neural stem cells. J Exp Neurosci. 2019;13:1–12.
   Web of Science ®Google Scholar
• Ahmadpour S, Foghi K. The Possible Neurodegeneration of the CA3 and CA1 of Hippocampus in STZ-Induced diabetes mellitus type1 on male wistar rats. J Med Histol. 2021;5(1):41–47.
   Google Scholar
• Yassa HD, Gergis SW, Hassan DM, et al. Therapeutic role of bone marrow mesenchymal stem cells in diabetic neuronal alternations of rat hippocampus. Folia Morphol (Warsz). 2020;79(2):211–218.
   PubMed Web of Science ®Google Scholar
• Shalaby AM, Aboregela AM, Alabiad MA, et al. The effect of induced diabetes mellitus on the cerebellar cortex of adult male rat and the possible protective role of oxymatrine: a histological, immunohistochemical and biochemical study. Ultrastruct Pathol. 2021;45(3):182–196.
   PubMed Web of Science ®Google Scholar
• Sun P, Ortega G, Tan Y, et al. Streptozotocin impairs proliferation and differentiation of adult hippocampal neural stem cells in vitro-correlation with alterations in the expression of proteins associated with the insulin system. Front Aging Neurosci. 2018;10:145.
   PubMed Web of Science ®Google Scholar
• Chen Y, Guo Z, Mao Y-F, et al. Intranasal insulin ameliorates cerebral hypometabolism, neuronal loss, and astrogliosis in streptozotocin-induced Alzheimer’s rat model. Neurotox Res. 2018;33(4):716–724. DOI:10.1007/s12640-017-9809-7
   PubMed Web of Science ®Google Scholar
• Farbood Y, Ghaderi S, Rashno M, et al. Sesamin: a promising protective agent against diabetes-associated cognitive decline in rats. Life Sci. 2019;230:169–177.
   PubMed Web of Science ®Google Scholar
• Luo H, Xiang Y, Qu X, et al. Apelin-13 suppresses neuroinflammation against cognitive deficit in a streptozotocin-induced rat model of Alzheimer’s disease through activation of BDNF-TrkB signaling pathway. Front Pharmacol. 2019;10:395.
   PubMed Web of Science ®Google Scholar
• Akash MS, Rehman K, Liaqat A. Tumor necrosis factor‐alpha: role in development of insulin resistance and pathogenesis of type 2 diabetes mellitus. J Cell Biochem. 2018;119(1):105–110.
   PubMed Web of Science ®Google Scholar
• Wang Q, Hu J, Liu Y, et al. Aerobic exercise improves synaptic-related proteins of diabetic rats by inhibiting FOXO1/NF-κB/NLRP3 inflammatory signaling pathway and ameliorating PI3K/Akt insulin signaling pathway. J Mol Neurosci. 2019;69(1):28–38. DOI:10.1007/s12031-019-01302-2
   PubMed Web of Science ®Google Scholar
• Xu T, Liu J, Li X-R, et al. The mTOR/NF-κB pathway mediates neuroinflammation and synaptic plasticity in diabetic encephalopathy. Mol Neurobiol. 2021;58(8):3848–3862. DOI:10.1007/s12035-021-02390-1
   PubMed Web of Science ®Google Scholar
• Bylicky MA, Mueller GP, Day RM. Mechanisms of endogenous neuroprotective effects of astrocytes in brain injury. Oxid Med Cell Longevity. 2018;2018:6501031.
   PubMed Web of Science ®Google Scholar
• Amin SN, Younan SM, Youssef MF, et al. A histological and functional study on hippocampal formation of normal and diabetic rats. F1000res. 2013;2:151.
   PubMedGoogle Scholar
• Sanchez‐vega L, Juárez I, De Jesus Gomez‐villalobos M, et al. Cerebrolysin reverses hippocampal neural atrophy in a mice model of diabetes mellitus type 1. Synapse. 2015;69(6):326–335. DOI:10.1002/syn.21819
   PubMed Web of Science ®Google Scholar
• Blázquez E, Velázquez E, Hurtado-Carneiro V, et al. Insulin in the brain: its pathophysiological implications for States related with central insulin resistance, type 2 diabetes and Alzheimer’s disease. Front Endocrinol (Lausanne). 2014;5:161.
   PubMed Web of Science ®Google Scholar
• Almulathanon AA, Mohammad JA, Allwash TA. Evaluation the effects of insulin on oxidant/antioxidant status in type 1 diabetic patients. Pharmacia. 2021;68:699.
   Web of Science ®Google Scholar
• Dandona P, Ghanim HJ. Diabetes, obesity, COVID-19, insulin, and other antidiabetes drugs. Diabetes Care. 2021;44(9):1929–1933.
   PubMed Web of Science ®Google Scholar
• Chang Y-W, Hung L-C, Chen Y-C, et al. Insulin reduces inflammation by regulating the activation of the NLRP3 inflammasome. Front Immunol. 2021;11:3856.
   Web of Science ®Google Scholar
• Gralle M. The neuronal insulin receptor in its environment. J Neurochem. 2017;140(3):359–367.
   PubMed Web of Science ®Google Scholar
• Hayes CA, Ashmore BG, Vijayasankar A, et al. Insulin-like growth factor-1 differentially modulates glutamate-induced toxicity and stress in cells of the neurogliovascular unit. Front Aging Neurosci. 2021;13:751304.
   PubMed Web of Science ®Google Scholar
• Kang DH, Choi BY, Lee SH, et al. Effects of cerebrolysin on hippocampal neuronal death after pilocarpine-induced seizure. Front Neurosci. 2020;14:568813.
   PubMed Web of Science ®Google Scholar
• Guan X, Wang Y, Kai G, et al. Cerebrolysin ameliorates focal cerebral ischemia injury through neuroinflammatory inhibition via CREB/PGC-1α pathway. Front Pharmacol. 2019;10:1245.
   PubMed Web of Science ®Google Scholar
• Fiani B, Covarrubias C, Wong A, et al. Cerebrolysin for stroke, neurodegeneration, and traumatic brain injury: review of the literature and outcomes. Neurol Sci. 2021;42(4):1345–1353. DOI:10.1007/s10072-021-05089-2
   PubMed Web of Science ®Google Scholar
• Attia TM. Assessment of the role of Cerebrolysin in treatment of idiopathic facial nerve paralysis. Menoufia Med J. 2019;32(2):712.
   Google Scholar
• Khavinson V, Ilina I, Kraskovskaya N, et al. Neuroprotective effects of tripeptides—epigenetic regulators in mouse model of Alzheimer’s disease. Pharmaceuticals. 2021;14(6):515.
   Web of Science ®Google Scholar
• Catalin B, Rogoveanu O-C, Pirici I, et al. Cerebrolysin and aquaporin 4 inhibition improve pathological and motor recovery after ischemic stroke. CNS & Neurol Disord. 2018;17(4):299–308.
   PubMed Web of Science ®Google Scholar
• Liu H, Qiu K, He Q, et al. Mechanisms of blood-brain barrier disruption in herpes simplex encephalitis. J Neuroimmune Pharmacol. 2019;14(2):157–172. DOI:10.1007/s11481-018-9821-6
   PubMed Web of Science ®Google Scholar