Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Research Article

Impact of Vitamin D3 on Carbonyl-Oxidative Stress and Matrix Metalloproteinases after Acute Intracerebral Hemorrhage in Rats with Type 2 Diabetes Mellitus

Author(s): Anton Lievykh*, Volodymyr Zhyliuk, Galyna Ushakova, Victoriia Tkachenko, Yuliia Kovalchuk, Olena Dovban, Yuliia Kharchenko and Alla Shevtsova

Volume 23, Issue 10, 2023

Published on: 23 May, 2023

Page: [1326 - 1339] Pages: 14

DOI: 10.2174/1871530323666230321100534

Price: $65

Abstract

Introduction: Diabetes mellitus is associated with the development of carbonyl-oxidative stress (COS) and an increased risk of a cerebral hemorrhage. Vitamin D3 is considered an additional drug to have an impact on COS and proteolysis in the extracellular matrix.

Objective: The study aimed to evaluate the impact of D3 on the COS-markers and matrix metalloproteinases MMP2/MMP9 activity after acute intracerebral hemorrhage (ICH) in rats with experimental type 2 diabetes mellitus (Т2DM) compared to metformin (Met).

Methods: T2DM was induced in rats via the intraperitoneal injection of streptozotocin (STZ) and nicotinamide (NA), ICH – by microinjection of bacterial collagenase into the striatum. Rats were randomized into five groups: 1 – intact animals (n = 8), 2 – T2DM (n = 9); 3 – T2DM+ICH (n = 7); 4 – T2DM+ICH+Met (n = 7); 5 – T2DM+ICH+D3 (n = 7). Blood glucose, glycated hemoglobin, and oral glucose tolerance test (OGTT) were assessed using commercial kits. Advanced oxidation protein products (AOPP), protein carbonyls (PC370/430), and ischemia-modified albumin (IMA) were measured by spectrophotometry, advanced glycation end products (AGEs) by quantitative fluorescence, and matrix metalloproteinases MMP2/9 by gelatin zymography.

Results: D3 does not significantly affect the glucose level and OGTT in rats with T2DM+ICH. However, it reduces AOPP, PC, and AGEs, thus reducing the COS index. In contrast, the activity of proMMP9 increases after D3 administration. These effects of D3 have been reported to be stronger and sometimes opposite to those of metformin.

Conclusion: D3 supplementation may decrease the negative consequences of a cerebral hemorrhage in T2DM by reducing COS and preventing the accumulation of COS-modified proteins in the brain by regulating the expression and activity of MMP9.

Graphical Abstract

[1]
Lau, L.H.; Lew, J.; Borschmann, K.; Thijs, V.; Ekinci, E.I. Prevalence of diabetes and its effects on stroke outcomes: A meta‐analysis and literature review. J. Diabetes Investig., 2019, 10(3), 780-792.
[http://dx.doi.org/10.1111/jdi.12932] [PMID: 30220102]
[2]
Zahra, F.; Kidwai, S.S.; Siddiqi, S.A.; Khan, R.M. Frequency of newly diagnosed diabetes mellitus in acute ischaemic stroke patients. J. Coll. Physicians Surg. Pak., 2012, 22(4), 226-229.
[PMID: 22482378]
[3]
Piernik-Yoder, B.; Ketchum, N.; Siddiqi, S.A.; Khan, R.M. Rehabilitation outcomes of stroke patients with and without diabetes. Arch. Phys. Med. Rehabil., 2013, 94(8), 1508-1512.
[http://dx.doi.org/10.1016/j.apmr.2013.04.014] [PMID: 23639547]
[4]
Eriksson, M.; Carlberg, B.; Eliasson, M. The disparity in long-term survival after a first stroke in patients with and without diabetes persists: the Northern Sweden MONICA study. Cerebrovasc. Dis., 2012, 34(2), 153-160.
[http://dx.doi.org/10.1159/000339763] [PMID: 22907276]
[5]
Saliba, W.; Barnett-Griness, O.; Gronich, N.; Molad, J.; Naftali, J.; Rennert, G.; Auriel, E. Association of diabetes and glycated hemoglobin with the risk of intracerebral hemorrhage: A population-based cohort study. Diabetes Care, 2019, 42(4), 682-688.
[http://dx.doi.org/10.2337/dc18-2472] [PMID: 30728223]
[6]
Issa, C.M.; Lucas, R.M.; Allen-Hall, A.; Fleury, N.; Feelisch, M. Vitamin D and type 2 diabetes mellitus, ultraviolet light in human health. Diseasest Environ., 2017, 996, 193-205.
[7]
Mirhosseini, N.; Vatanparast, H.; Mazidi, M.; Kimball, S.M. Vitamin D supplementation, glycemic control, and insulin resistance in prediabetics: A meta-analysis. J. Endocr. Soc., 2018, 2(7), 687-709.
[http://dx.doi.org/10.1210/js.2017-00472] [PMID: 29951596]
[8]
Maddaloni, E.; Cavallari, I.; Napoli, N.; Conte, C. Vitamin D and diabetes mellitus. Front. Horm. Res., 2018, 50, 161-176.
[http://dx.doi.org/10.1159/000486083] [PMID: 29597238]
[9]
Seida, J.C.; Mitri, J.; Colmers, I.N.; Majumdar, S.R.; Davidson, M.B.; Edwards, A.L.; Hanley, D.A.; Pittas, A.G.; Tjosvold, L.; Johnson, J.A. Clinical review: Effect of vitamin D3 supplementation on improving glucose homeostasis and preventing diabetes: a systematic review and meta-analysis. J. Clin. Endocrinol. Metab., 2014, 99(10), 3551-3560.
[http://dx.doi.org/10.1210/jc.2014-2136] [PMID: 25062463]
[10]
Wexler, D.J. D2d - no defense against diabetes. N. Engl. J. Med., 2019, 381(6), 581-582.
[http://dx.doi.org/10.1056/NEJMe1906815] [PMID: 31173678]
[11]
Karonova, T.; Stepanova, A.; Bystrova, A.; Jude, E.B. High-dose vitamin D supplementation improves microcirculation and reduces inflammation in diabetic neuropathy patients. Nutrients, 2020, 12(9), 2518.
[http://dx.doi.org/10.3390/nu12092518] [PMID: 32825324]
[12]
Ghadiri-Anari, A.; Mozafari, Z.; Gholami, S.; Khodaei, S.A.; Aboutorabi-Zarchi, M.; Sepehri, F.; Nadjarzade, A.; Rahmanian, M.; Namiranian, N. Dose vitamin D supplementations improve peripheral diabetic neuropathy? A before-after clinical trial. Diabetes Metab. Syndr., 2019, 13(1), 890-893.
[13]
Pittas, A.G.; Dawson-Hughes, B.; Sheehan, P.; Ware, J.H.; Knowler, W.C.; Aroda, V.R.; Brodsky, I.; Ceglia, L.; Chadha, C.; Chatterjee, R.; Desouza, C.; Dolor, R.; Foreyt, J.; Fuss, P.; Ghazi, A.; Hsia, D.S.; Johnson, K.C.; Kashyap, S.R.; Kim, S.; LeBlanc, E.S.; Lewis, M.R.; Liao, E.; Neff, L.M.; Nelson, J.; O’Neil, P.; Park, J.; Peters, A.; Phillips, L.S.; Pratley, R.; Raskin, P.; Rasouli, N.; Robbins, D.; Rosen, C.; Vickery, E.M.; Staten, M. D2d research group. vitamin D supplementation and prevention of type 2 diabetes. N. Engl. J. Med., 2019, 381(6), 520-530.
[http://dx.doi.org/10.1056/NEJMoa1900906] [PMID: 31173679]
[14]
Makk-Merczel, K.; Szarka, A. The role of carbonyl stress in the development of diabetic complications. Orv. Hetil., 2019, 160(40), 1567-1573.
[http://dx.doi.org/10.1556/650.2019.31519] [PMID: 31565977]
[15]
Alouffi, S.; Khan, M.W.A. Dicarbonyls generation, toxicities, detoxifications and potential roles in diabetes complications. Curr. Protein Pept. Sci., 2020, 21(9), 890-898.
[http://dx.doi.org/10.2174/1389203720666191010155145] [PMID: 31660813]
[16]
Babizhayev, M.A.; Strokov, I.A.; Nosikov, V.V.; Savel’yeva, E.L.; Sitnikov, V.F.; Lankin, V.Z.; Lankin, V.Z.; Yegorov, Y.E. The role of oxidative stress in diabetic neuropathy: generation of free radical species in the glycation reaction and gene polymorphisms encoding antioxidant enzymes to genetic susceptibility to diabetic neuropathy in population of type I diabetic patients. Cell Biochem. Biophys., 2015, 71(3), 1425-1443.
[http://dx.doi.org/10.1007/s12013-014-0365-y] [PMID: 25427889]
[17]
Menon, B.; Ramalingam, K.; Krishna, V. Study of ischemia modified albumin as a biomarker in acute ischaemic stroke. Ann. Neurosci., 2018, 25(4), 187-190.
[http://dx.doi.org/10.1159/000488188] [PMID: 31000956]
[18]
Kumar, P.A.; Subramanian, K. The role of ischemia modified albumin as a biomarker in patients with chronic liver disease. J. Clin. Diagn. Res., 2016, 10, 09-12.
[http://dx.doi.org/10.7860/JCDR/2016/17168.7399]
[19]
Ma, S.G.; Wei, C.L.; Hong, B.; Yu, W.N.; Yu, W.N. Ischemia-modified albumin in type 2 diabetic patients with and without peripheral arterial disease. Clinics, 2011, 66(10), 1677-1680.
[PMID: 22012037]
[20]
Elgebaly, M.M.; Prakash, R.; Li, W.; Ogbi, S.; Johnson, M.H.; Mezzetti, E.M.; Fagan, S.C.; Ergul, A. Vascular protection in diabetic stroke: Role of matrix metalloprotease-dependent vascular remodeling. J. Cereb. Blood Flow Metab., 2010, 30(12), 1928-1938.
[http://dx.doi.org/10.1038/jcbfm.2010.120] [PMID: 20664613]
[21]
Wang, X.; Khalil, R.A. Matrix metalloproteinases, vascular remodeling, and vascular disease. Adv. Pharmacol., 2018, 81, 241-330.
[http://dx.doi.org/10.1016/bs.apha.2017.08.002] [PMID: 29310800]
[22]
Zhong, C.; Yang, J.; Xu, T.; Xu, T.; Peng, Y.; Wang, A.; Wang, J.; Peng, H.; Li, Q.; Ju, Z.; Geng, D.; Zhang, Y.; He, J. CATIS Investigators. Serum matrix metalloproteinase-9 levels and prognosis of acute ischemic stroke. Neurology, 2017, 89(8), 805-812.
[http://dx.doi.org/10.1212/WNL.0000000000004257] [PMID: 28747453]
[23]
Hawkins, B.T.; Lundeen, T.F.; Norwood, K.M.; Brooks, H.L.; Egleton, R.D. Increased blood–brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases. Diabetologia, 2006, 50(1), 202-211.
[http://dx.doi.org/10.1007/s00125-006-0485-z] [PMID: 17143608]
[24]
Kostov, K.; Blazhev, A. Use of glycated hemoglobin (A1c) as a biomarker for vascular risk in type 2 diabetes: its relationship with matrix metalloproteinases-2, -9 and the metabolism of collagen IV and elastin. Medicina, 2020, 56(5), 231.
[http://dx.doi.org/10.3390/medicina56050231] [PMID: 32403389]
[25]
Aggarwal, A.; Khera, A.; Singh, I.; Sandhir, R. S -nitrosoglutathione prevents blood-brain barrier disruption associated with increased matrix metalloproteinase-9 activity in experimental diabetes. J. Neurochem., 2015, 132(5), 595-608.
[http://dx.doi.org/10.1111/jnc.12939] [PMID: 25187090]
[26]
Dallak, M.; Haidara, M.A.; Bin-Jaliah, I.; Eid, R.A.; Amin, S.N.; Abdel Latif, N.S.; Al-Ani, B. Metformin suppresses aortic ultrastrucural damage and hypertension induced by diabetes: A potential role of advanced glycation end products. Ultrastruct. Pathol., 2019, 43(4-5), 190-198.
[http://dx.doi.org/10.1080/01913123.2019.1666952] [PMID: 31522593]
[27]
Ren, H.; Shao, Y.; Wu, C.; Ma, X.; Lv, C.; Wang, Q. Metformin alleviates oxidative stress and enhances autophagy in diabetic kidney disease via AMPK/SIRT1-FoxO1 pathway. Mol. Cell. Endocrinol., 2020, 500, 110628.
[http://dx.doi.org/10.1016/j.mce.2019.110628] [PMID: 31647955]
[28]
Potârniche, A.V. Dreancă, A.I.; Sarpataki, O.; Sevastre, B.; Marcus, I. Experimental model of streptozotocin-nicotinamide induced diabetes mellitus type II in sprague-dawley rats: step by step protocol and the encountered issues. Rev. Rom. Med. Vet., 2018, 28(2), 22-26.
[29]
Ghasemi, A.; Khalifi, S.; Jedi, S. Streptozotocin-nicotinamide-induced rat model of type 2 diabetes. Acta Physiol. Hung., 2014, 101(4), 408-420.
[http://dx.doi.org/10.1556/APhysiol.101.2014.4.2] [PMID: 25532953]
[30]
Tyurenkov, I.N.; Kurkin, D.V.; Bakulin, D.A.; Volotova, E.V.; Chafeev, M.A.; Smirnov, A.V.; Morkovin, E.I. ZB-16, a novel GPR119 agonist, relieves the severity of streptozotocin-nicotinamide-induced diabetes in rats. Front. Endocrinol., 2017, 8, 152.
[http://dx.doi.org/10.3389/fendo.2017.00152] [PMID: 28736546]
[31]
Chen, J.; Xu, Z.C.; Xu, X.M.; Zhang, J.H. Animal Models of Acute Neurological Injury, 2nd ed.; Springer, 2nd ed., 2019, 2, p. 544.
[32]
MacLellan, C.L.; Silasi, G.; Poon, C.C.; Edmundson, C.L.; Buist, R.; Peeling, J.; Colbourne, F. Intracerebral hemorrhage models in rat: Comparing collagenase to blood infusion. J. Cereb. Blood Flow Metab., 2008, 28(3), 516-525.
[http://dx.doi.org/10.1038/sj.jcbfm.9600548] [PMID: 17726491]
[33]
Monneret, D.; Corlouer, C.; Bigot, J.; Atlan, G.; Alkouri, R.; Mestari, F.; Dever, S.; Imbert-Bismut, F.; Bonnefont-Rousselot, D. Comparison of a 10- vs. 15-min centrifugation time for chemical and immunochemical assays and impact on turnaround time in a hospital laboratory. Clin. Chem. Laboratory Med. (CCLM), 2016, 54(4), e117-e121.
[http://dx.doi.org/10.1515/cclm-2015-0664] [PMID: 26479346]
[34]
Tang, D.; Liu, L.; Ajiakber, D.; Ye, J.; Xu, J.; Xin, X.; Aisa, H.A. Anti-diabetic effect of punica granatum flower polyphenols extract in type 2 diabetic rats: activation of Akt/GSK-3β and Inhibition of IRE1α-XBP1 Pathways. Front. Endocrinol., 2018, 9, 586.
[http://dx.doi.org/10.3389/fendo.2018.00586] [PMID: 30374328]
[35]
Gabbay, K.H.; Sosenko, J.M.; Banuchi, G.A.; Mininsohn, M.J.; Flückiger, R. Glycosylated hemoglobins: increased glycosylation of hemoglobin A in diabetic patients. Diabetes, 1979, 28(4), 337-340.
[http://dx.doi.org/10.2337/diab.28.4.337] [PMID: 437373]
[36]
Koroliuk, M.A.; Ivanova, L.I. Maĭorova, I.G.; Tokarev, V.E. A method of determining catalase activity. Lab. Delo, 1988, 1(1), 16-19.
[PMID: 2451064]
[37]
Kostyuk, V.A.; Potapovich, A.I.; Afanasyev, I.B. The method of determining the activity of superoxide dismutase. Laboratory Work, 1987, 1, 4-9.
[38]
Ohkawa, H.; Ohishi, N.; Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem., 1979, 95(2), 351-358.
[http://dx.doi.org/10.1016/0003-2697(79)90738-3]
[39]
Katsuki, H.; Kawano, C.; Yoshida, T.; Kanayuki, H.; Tanaka, S. The determination of pyruvic acid by 2,4-dinitrophenylhydrazine method. Anal. Biochem., 1961, 2, 433-440.
[http://dx.doi.org/10.1016/0003-2697(61)90047-1] [PMID: 14454340]
[40]
Witko-Sarsat, V.; Friedlander, M.; Capeillère-Blandin, C.; Nguyen-Khoa, T.; Nguyen, A.T.; Zingraff, J.; Jungers, P.; Descamps-Latscha, B. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int., 1996, 49(5), 1304-1313.
[http://dx.doi.org/10.1038/ki.1996.186] [PMID: 8731095]
[41]
Taylor, E.L.; Armstrong, K.R.; Perrett, D.; Hattersley, A.T.; Winyard, P.G. Optimisation of an advanced oxidation protein products assay: Its application to studies of oxidative stress in diabetes mellitus. Oxid. Med. Cell. Longev., 2015, 2015, 496271.
[http://dx.doi.org/10.1155/2015/496271] [PMID: 26113954]
[42]
Levine, R.L.; Garland, D.; Oliver, C.N.; Amici, A.; Climent, I.; Lenz, A.G.; Ahn, B.W.; Shaltiel, S.; Stadtman, E.R. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol., 1990, 186, 464-478.
[http://dx.doi.org/10.1016/0076-6879(90)86141-H] [PMID: 1978225]
[43]
Soglia, F.; Petracci, M.; Ertbjerg, P. Novel DNPH-based method for determination of protein carbonylation in muscle and meat. Food Chem., 2016, 197(Pt A), 670-675.
[http://dx.doi.org/10.1016/j.foodchem.2015.11.038] [PMID: 26617002]
[44]
Dzydzan, O.; Brodyak, I. Sokół-Łętowska, A.; Kucharska, A.Z.; Sybirna, N. Loganic acid, an iridoid glycoside extracted from cornus mas l. fruits, reduces of carbonyl/oxidative stress biomarkers in plasma and restores antioxidant balance in Leukocytes of rats with streptozotocin-induced. Life, 2020, 10(12), 349.
[http://dx.doi.org/10.3390/life10120349] [PMID: 33333730]
[45]
Münch, G.; Keis, R.; Weßels, A.; Riederer, P.; Bahner, U.; Heidland, A.; Niwa, T.; Lemke, H.D.; Schinzel, R. Determination of advanced glycation end products in serum by fluorescence spectroscopy and competitive ELISA. Clin. Chem. Lab. Med., 1997, 35(9), 669-677.
[http://dx.doi.org/10.1515/cclm.1997.35.9.669] [PMID: 9352229]
[46]
Tkachenko, V.; Kovalchuk, Y.; Bondarenko, N.; Bondarenko, O.; Ushakova, G.; Shevtsova, A. The cardio-and neuroprotective effects of corvitin and 2-oxoglutarate in rats with pituitrin-isoproterenol-induced myocardial damage. Biochem. Res. Int., 2018, 2018, 9302414.
[47]
Bar-Or, D.; Lau, E.; Winkler, J.V. A novel assay for cobalt-albumin binding and its potential as a marker for myocardial ischemia—a preliminary report. J. Emerg. Med., 2000, 19(4), 311-315.
[http://dx.doi.org/10.1016/S0736-4679(00)00255-9] [PMID: 11074321]
[48]
Collinson, P.O.; Gaze, D.C. Ischaemia-modified albumin: Clinical utility and pitfalls in measurement. J. Clin. Pathol., 2008, 61(9), 1025-1028.
[http://dx.doi.org/10.1136/jcp.2007.053363] [PMID: 18755726]
[49]
Toth, M.; Sohail, A.; Fridman, R. Assessment of gelatinases (MMP-2 and MMP-9) by gelatin zymography. Methods Mol. Biol., 2012, 878, 121-135.
[http://dx.doi.org/10.1007/978-1-61779-854-2_8] [PMID: 22674130]
[50]
Muriach, M.; Flores-Bellver, M.; Romero, F.J.; Barcia, J.M. Diabetes and the brain: oxidative stress, inflammation, and autophagy. Oxid. Med. Cell. Longev., 2014, 2014, 1-9.
[http://dx.doi.org/10.1155/2014/102158] [PMID: 25215171]
[51]
Shou, J.; Zhou, L.; Zhu, S.; Zhang, X. Diabetes is an independent risk factor for stroke recurrence in stroke patients: a meta-analysis. J. Stroke Cerebrovasc. Dis., 2015, 24(9), 1961-1968.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.04.004] [PMID: 26166420]
[52]
Hagg, S.; Thorn, L.; Forsblom, C.; Gordin, D.; Saraheimo, M.; Tolonen, N.; Wadén, J.; Liebkind, R.; Putaala, J.; Tatlisumak, T. Per-Henrik Groop, FinnDiane Study Group. Different risk factor profiles for ischaemic and haemorrhagic stroke in type 1 diabetes mellitus. Stroke, 2014, 45, 2558-2562.
[http://dx.doi.org/10.1161/STROKEAHA.114.005724] [PMID: 25061078]
[53]
Velayutham, P.K.; Adhikary, S.D.; Babu, S.K.; Vedantam, R.; Korula, G.; Ramachandran, A. Oxidative stress–associated hypertension in surgically induced brain injury patients: Effects of β-blocker and angiotensin-converting enzyme inhibitor. J. Surg. Res., 2013, 179(1), 125-131.
[http://dx.doi.org/10.1016/j.jss.2012.09.005] [PMID: 23020955]
[54]
Esteghamati, A.; Eskandari, D.; Mirmiranpour, H.; Noshad, S.; Mousavizadeh, M.; Hedayati, M.; Nakhjavani, M. Effects of metformin on markers of oxidative stress and antioxidant reserve in patients with newly diagnosed type 2 diabetes: A randomized clinical trial. Clin. Nutr., 2013, 32(2), 179-185.
[http://dx.doi.org/10.1016/j.clnu.2012.08.006] [PMID: 22963881]
[55]
Ding, C.Y.; Peng, L.; Lin, Y.X.; Yu, L.H.; Wang, D.L.; Kang, D.Z. Elevated lactate dehydrogenase level predicts postoperative pneumonia in patients with aneurysmal subarachnoid hemorrhage. World Neurosurg., 2019, 129, e821-e830.
[http://dx.doi.org/10.1016/j.wneu.2019.06.041] [PMID: 31203058]
[56]
Chu, H.; Huang, C.; Dong, J.; Yang, X.; Xiang, J.; Dong, Q.; Tang, Y. Lactate dehydrogenase predicts early hematoma expansion and poor outcomes in intracerebral hemorrhage patients. Transl. Stroke Res., 2019, 10(6), 620-629.
[http://dx.doi.org/10.1007/s12975-019-0686-7] [PMID: 30706410]
[57]
Heidari, F.; Rabizadeh, S.; Mansournia, M.A.; Mirmiranpoor, H.; Salehi, S.S.; Akhavan, S.; Esteghamati, A.; Nakhjavani, M. Inflammatory, oxidative stress and anti-oxidative markers in patients with endometrial carcinoma and diabetes. Cytokine, 2019, 120, 186-190.
[http://dx.doi.org/10.1016/j.cyto.2019.05.007] [PMID: 31100682]
[58]
Dayanand, C.D.; Vegi, P.K.; Lakshmaiah, V.; Kutty, A.V.M. Association of ischemia modified albumin in terms of hypoxic risk with carbonylated protein, glycosylated hemoglobin and plasma insulin in type 2 diabetes mellitus. Int. J. Biotechnol. Biochem., 2013, 9(3), 275-284.
[http://dx.doi.org/10.26611/10211214]
[59]
Sushith, S.; Krishnamurthy, H.N.; Reshma, S.; Janice, D.S.; Madan, G.; Ashok, K.J.; Prathima, M.B.; Kalal, B.S. Serum ischemia-modified albumin, fibrinogen, high sensitivity C- reactive proteins in type-2 diabetes mellitus without hypertension and diabetes mellitus with hypertension: A case-control study. Rep. Biochem. Mol. Biol., 2020, 9(2), 241-249.
[http://dx.doi.org/10.29252/rbmb.9.2.241] [PMID: 33178875]
[60]
Gunduz, A.; Turedi, S.; Mentese, A.; Altunayoglu, V.; Turan, I.; Karahan, S.C.; Topbas, M.; Aydin, M.; Eraydin, I.; Akcan, B. Ischemia-modified albumin levels in cerebrovascular accidents. Am. J. Emerg. Med., 2008, 26(8), 874-878.
[http://dx.doi.org/10.1016/j.ajem.2007.11.023] [PMID: 18926343]
[61]
Ahn, J.H.; Choi, S.C.; Lee, W.G.; Jung, Y.S. The usefulness of albumin-adjusted ischemia-modified albumin index as early detecting marker for ischemic stroke. Neurol. Sci., 2011, 32(1), 133-138.
[http://dx.doi.org/10.1007/s10072-010-0457-4] [PMID: 21153598]
[62]
Türedi, S. Şahin, A.; Akça, M.; Demir, S.; Reis Köse, G.D.; Çekiç, A.B.; Yıldırım, M.; Yuluğ, E.; Menteşe, A.; Türkmen, S.; Acar, S. Ischemia-modified albumin and the IMA/albumin ratio in the diagnosis and staging of hemorrhagic shock: A randomized controlled experimental study. Ulus. Travma Acil Cerrahi Derg., 2020, 26(2), 153-162.
[PMID: 32185760]
[63]
Tan, H.; Yang, W.; Wu, C.; Liu, B.; Lu, H.; Wang, H.; Yan, H. Assessment of the role of intracranial hypertension and stress on hippocampal cell apoptosis and hypothalamic-pituitary dysfunction after TBI. Sci. Rep., 2017, 7(1), 3805.
[http://dx.doi.org/10.1038/s41598-017-04008-w] [PMID: 28630478]
[64]
Chen, T.; Zhu, J.; Wang, Y.H.; Hang, C.H. ROS-mediated mitochondrial dysfunction and ER stress contribute to compression-induced neuronal injury. Neuroscience, 2019, 416, 268-280.
[http://dx.doi.org/10.1016/j.neuroscience.2019.08.007] [PMID: 31425734]
[65]
Kara, I.; Pampal, H.K.; Yildirim, F.; Dilekoz, E.; Emmez, G. U, F.P.; Kocabiyik, M.; Demirel, C.B. Role of ischemic modified albumin in the early diagnosis of increased intracranial pressure and brain death. Bratisl. Med. J., 2017, 118(2), 112-117.
[http://dx.doi.org/10.4149/BLL_2017_023] [PMID: 28814093]
[66]
Bar-Or, D.; Winkler, J.V.; VanBenthuysen, K.; Harris, L.; Lau, E.; Hetzel, F.W. Reduced albumin-cobalt binding with transient myocardial ischemia after elective percutaneous transluminal coronary angioplasty: A preliminary comparison to creatine kinase-MB, myoglobin, and troponin I. Am. Heart J., 2001, 141(6), 985-991.
[http://dx.doi.org/10.1067/mhj.2001.114800] [PMID: 11376314]
[67]
Gaze, D.C. Biomarkers of Cardiac Ischemia; [Internet]. ; Ischemic Heart Disease. InTech, 2013, pp. 91-122.
[http://dx.doi.org/10.5772/55250]
[68]
Sinha, M.K.; Vazquez, J.M.; Calvino, R.; Gaze, D.C.; Collinson, P.O.; Kaski, J.C. Effects of balloon occlusion during percutaneous coronary intervention on circulating Ischemia Modified Albumin and transmyocardial lactate extraction. Heart, 2006, 92(12), 1852-1853.
[http://dx.doi.org/10.1136/hrt.2005.078089] [PMID: 17105887]
[69]
Venna, V.R.; Li, J.; Hammond, M.D.; Mancini, N.S.; McCullough, L.D. Chronic metformin treatment improves post-stroke angiogenesis and recovery after experimental stroke. Eur. J. Neurosci., 2014, 39(12), 2129-2138.
[http://dx.doi.org/10.1111/ejn.12556] [PMID: 24649970]
[70]
Deng, T.; Zheng, Y.R.; Hou, W.W.; Yuan, Y.; Shen, Z.; Wu, X.L.; Chen, Y.; Zhang, L.S.; Hu, W.W.; Chen, Z.; Zhang, X.N. Pre-stroke metformin treatment is neuroprotective involving AMPK reduction. Neurochem. Res., 2016, 41(10), 2719-2727.
[http://dx.doi.org/10.1007/s11064-016-1988-8] [PMID: 27350579]
[71]
Liang, Y.; Yu, H.; Ke, X.; Eyles, D.; Sun, R.; Wang, Z.; Huang, S.; Lin, L.; McGrath, J.J.; Lu, J.; Guo, X.; Yao, P. Vitamin D deficiency worsens maternal diabetes induced neurodevelopmental disorder by potentiating hyperglycemia‐mediated epigenetic changes. Ann. N. Y. Acad. Sci., 2021, 1491(1), 74-88.
[http://dx.doi.org/10.1111/nyas.14535] [PMID: 33305416]
[72]
Lee, T.W.; Kao, Y.H.; Chen, Y.J.; Chao, T.F.; Lee, T.I. Therapeutic potential of vitamin D in AGE/RAGE-related cardiovascular diseases. Cell. Mol. Life Sci., 2019, 76(20), 4103-4115.
[http://dx.doi.org/10.1007/s00018-019-03204-3] [PMID: 31250032]
[73]
Omidian, M.; Djalali, M.; Javanbakht, M.H.; Eshraghian, M.R.; Abshirini, M.; Omidian, P.; Alvandi, E.; Mahmoudi, M. Effects of vitamin D supplementation on advanced glycation end products signaling pathway in T2DM patients: a randomized, placebo-controlled, double blind clinical trial. Diabetol. Metab. Syndr., 2019, 11(1), 86.
[http://dx.doi.org/10.1186/s13098-019-0479-x] [PMID: 31673295]
[74]
Colombo, G.; Clerici, M.; Garavaglia, M.E.; Giustarini, D.; Rossi, R.; Milzani, A.; Dalle-Donne, I. A step-by-step protocol for assaying protein carbonylation in biological samples. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2016, 1019, 178-190.
[http://dx.doi.org/10.1016/j.jchromb.2015.11.052] [PMID: 26706659]
[75]
Wang, G.S.; Hoyte, C. Review of Biguanide (Metformin) Toxicity. J. Intensive Care Med., 2019, 34(11-12), 863-876.
[http://dx.doi.org/10.1177/0885066618793385] [PMID: 30126348]
[76]
Hamden, K.; Carreau, S.; Jamoussi, K.; Miladi, S.; Lajmi, S.; Aloulou, D.; Ayadi, F.; Elfeki, A. 1Alpha,25 dihydroxyvitamin D3: Therapeutic and preventive effects against oxidative stress, hepatic, pancreatic and renal injury in alloxan-induced diabetes in rats. J. Nutr. Sci. Vitaminol., 2009, 55(3), 215-222.
[http://dx.doi.org/10.3177/jnsv.55.215] [PMID: 19602829]
[77]
Tavakoli, H.; Rostami, H.; Avan, A.; Bagherniya, M.; Ferns, G.A.; Khayyatzadeh, S.S.; Ghayour-Mobarhan, M. High dose vitamin D supplementation is associated with an improvement in serum markers of liver function. Biofactors, 2019, 45(3), 335-342.
[http://dx.doi.org/10.1002/biof.1496] [PMID: 30761636]
[78]
Tombulturk, F.K.; Todurga-Seven, Z.G.; Huseyinbas, O.; Ozyazgan, S.; Ulutin, T.; Kanigur-Sultuybek, G. Topical application of metformin accelerates cutaneous wound healing in streptozotocin-induced diabetic rats. Mol. Biol. Rep., 2022, 49(1), 73-83.
[http://dx.doi.org/10.1007/s11033-021-06843-7] [PMID: 34718940]
[79]
Takata, F.; Dohgu, S.; Matsumoto, J.; Machida, T.; Kaneshima, S.; Matsuo, M.; Sakaguchi, S.; Takeshige, Y.; Yamauchi, A.; Kataoka, Y. Metformin induces up-regulation of blood–brain barrier functions by activating AMP-activated protein kinase in rat brain microvascular endothelial cells. Biochem. Biophys. Res. Commun., 2013, 433(4), 586-590.
[http://dx.doi.org/10.1016/j.bbrc.2013.03.036] [PMID: 23523792]
[80]
López-López, N.; González-Curiel, I.; Treviño-Santa Cruz, M.B.; Rivas-Santiago, B.; Trujillo-Paez, V.; Enciso-Moreno, J.A.; Serrano, C.J. Expression and vitamin D-mediated regulation of matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs) in healthy skin and in diabetic foot ulcers. Arch. Dermatol. Res., 2014, 306(9), 809-821.
[http://dx.doi.org/10.1007/s00403-014-1494-2] [PMID: 25168880]
[81]
Velimirović, M.; Jevtić Dožudić, G.; Selaković, V.; Stojković, T.; Puškaš, N.; Zaletel, I.; Živković, M.; Dragutinović, V.; Nikolić, T.; Jelenković, A.; Djorović, D.; Mirčić, A.; Petronijević, N.D. Effects of Vitamin D3 on the NADPH oxidase and matrix metalloproteinase 9 in an animal model of global cerebral ischemia. Oxid. Med. Cell. Longev., 2018, 2018, 3273654.
[http://dx.doi.org/10.1155/2018/3273654] [PMID: 29849881]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy