Abstract
Diabetes mellitus is a chronic disease involving persistent hyperglycemia, which causes an imbalance between reactive oxygen species and antioxidant enzymes and results in damage to various tissues, including the brain. Many societies have traditionally employed medicinal plants to control the hyperglycemia. Pouteria ramiflora, a species occurring in the savanna biome of the Cerrado (Brazil) has been studied because of its possible ability to inhibit carbohydrate digestion. Rats with streptozotocin-induced diabetes treated with an alcoholic extract of Pouteria ramiflora show an improved glycemic level, increased glutathione peroxidase activity, decreased superoxide dismutase activity, and reduced lipid peroxidation and antioxidant status. The extract also restored myosin-Va expression and the nuclear diameters of pyramidal neurons of the CA3 subregion and that of the polymorphic cells of the hilus. We conclude that Pouteria ramiflora extract exerts a neuroprotective effect against oxidative damage and myosin-Va expression and is able to prevent hippocampal neuronal loss in the CA3 and hilus subfields of diabetic rats. However, future studies are needed to understand the mechanism of action of Pouteria ramiflora extract in acute and chronic diabetes.
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References
Alfonso JE, Ariza ID (2008) New therapies for diabetes: beyond injectable insulin and oral antidiabetics. Rev Assoc Med Bras 54:447–454
Apostolidis E, Kwon Y-I, Shetty K (2007) Inhibitory potential of herb, fruit, and fungal-enriched cheese against key enzymes linked to type 2 diabetes and hypertension. Inn Food Sci Emerg Technol 8:46–54
Aragno M, Mastrocola R, Catalano MG, Brignardello E, Danni O, Boccuzzi G (2004) Oxidative stress impairs skeletal muscle repair in diabetic rats. Diabetes 53:1082–1088
Baynes JW (1991) Role of oxidative stress in development of complications in diabetes. Diabetes 40:405–412
Bhor VM, Raghuram N, Sivakami S (2004) Oxidative damage and altered antioxidant enzyme activities in the small intestine of streptozotocin-induced diabetic rats. Int J Biochem Cell Biol 36:89–97
Biessels GJ, Kappelle AC, Bravenboer B, Erkelens DW, Gispen WH (1994) Cerebral function in diabetes mellitus. Diabetologia 37:643–650
Biessels GJ, Kamal A, Ramakers GM, Urban IJ, Spruijt BM, Erkelens DW, Gispen WH (1996) Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 45:1259–1266
Bose A, Guilherme A, Robida SI, Nicoloro SM, Zhou QL, Jiang ZY, Pomerleau DP, Czech MP (2002) Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420:821–824
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brinn LS, Pereira Leite J, Larson RE, Martins AR (2010) Differential patterns of myosin Va expression during the ontogenesis of the rat hippocampus. Braz J Med Biol Res 43:890–898
Calabria LK, da Cruz GC, Nascimento R, Carvalho WJ, de Gouveia NM, Alves FV, Furtado FB, Ishikawa-Ankerhold HC, de Sousa MV, Goulart LR, Espindola FS (2011) Overexpression of myosin-IIB in the brain of a rat model of streptozotocin-induced diabetes. J Neurol Sci 303:43–49
Ceriello A, Bortolotti N, Falleti E, Taboga C, Tonutti L, Crescentini A, Motz E, Lizzio S, Russo A, Bartoli E (1997) Total radical-trapping antioxidant parameter in NIDDM patients. Diabetes Care 20:194–197
Ceriello A, Motz E (2004) Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 24:816–823
Coirault C, Guellich A, Barbry T, Samuel JL, Riou B, Lecarpentier Y (2007) Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 292:H1009–H1017
da Costa AV, Calabria LK, Nascimento R, Carvalho WJ, Goulart LR, Espindola FS (2011) The streptozotocin-induced rat model of diabetes mellitus evidences significant reduction of myosin-Va expression in the brain. Metab Brain Dis 26:247–251
Deconte SR, Oliveira RJ, Calabria LK, Oliveira VN, Gouveia NM, Moraes Ada S, Espindola FS (2011) Alterations of antioxidant biomarkers and type I collagen deposition in the parotid gland of streptozotocin-induced diabetic rats. Arch Oral Biol 56:744–751
Eliza J, Daisy P, Ignacimuthu S (2010) Antioxidant activity of costunolide and eremanthin isolated from Costus speciosus (Koen ex. Retz) Sm. Chem Biol Interact 188:467–472
Espindola FS, Suter DM, Partata LB, Cao T, Wolenski JS, Cheney RE, King SM, Mooseker MS (2000) The light chain composition of chicken brain myosin-Va: calmodulin, myosin-II essential light chains, and 8-kDa dynein light chain/PIN. Cell Motil Cytoskeleton 47:269–281
Espindola FS, Banzi SR, Calabria LK, Custodio RJ, Oliveira RA, Procopio LD, Lima AB, Cunha-Junior JP, Coelho MV, Guedes IM, Pellizzon CH, Larson RE, Espreafico EM (2008) Localization of myosin-Va in subpopulations of cells in rat endocrine organs. Cell Tissue Res 333:263–279
Fazeli SA, Gharravi AM, Jahanshahi M, Ghafari S, Behnampour N, Golalipour MJ (2009) Resistance of CA1 pyramidal cells to STZ-induced diabetes in young rats. Int J Morphol 27:997–1001
Funke I, Melzig MF (2006) Traditionally used plants in diabetes therapy - phytotherapeutics as inhibitors of a-amylase activity. Rev Bras Farmacogn 16:1–5
Godin DV, Wohaieb SA, Garnett ME, Goumeniouk AD (1988) Antioxidant enzyme alterations in experimental and clinical diabetes. Mol Cell Biochem 84:223–231
Goke B, Herrmann-Rinke C (1998) The evolving role of alpha-glucosidase inhibitors. Diabetes Metab Rev 14(Suppl 1):S31–S38
Gutteridge JM, Halliwell B (2000) Free radicals and antioxidants in the year 2000. A historical look to the future. Ann N Y Acad Sci 899:136–147
Hamdy NM, Taha RA (2009) Effects of Nigella sativa oil and thymoquinone on oxidative stress and neuropathy in streptozotocin-induced diabetic rats. Pharmacology 84:127–134
Hasanein P, Shahidi S (2010) Effects of combined treatment with vitamins C and E on passive avoidance learning and memory in diabetic rats. Neurobiol Learn Mem 93:472–478
Jarrard LE (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60:9–26
Josephy DP (1997) Molecular Toxicology. Oxford University Press, New York
Kakkar R, Kalra J, Mantha SV, Prasad K (1995) Lipid peroxidation and activity of antioxidant enzymes in diabetic rats. Mol Cell Biochem 151:113–119
Kesavulu MM, Giri R, Kameswara Rao B, Apparao C (2000) Lipid peroxidation and antioxidant enzyme levels in type 2 diabetics with microvascular complications. Diabetes Metab 26:387–392
Kosif R, Aktas R, Oztekin A (2008) The effects of oral administration of Aloe vera [barbadensis] on rat central nervous system: an experimental preliminary study. Neuroanatomy 7:22–27
Kowluru R, Chan P (2007) Oxidative stress and diabetic retinopathy. Exp Diabetes Res 2007:43603
Kuhad A, Chopra K (2007) Curcumin attenuates diabetic encephalopathy in rats: behavioral and biochemical evidences. Eur J Pharmacol 576:34–42
Li ZG, Zhang W, Grunberger G, Sima AA (2002) Hippocampal neuronal apoptosis in type 1 diabetes. Brain Res 946:221–231
Ma J, Yang H, Basile MJ, Kennelly EJ (2004) Analysis of polyphenolic antioxidants from the fruits of three pouteria species by selected ion monitoring liquid chromatography-mass spectrometry. J Agric Food Chem 52:5873–5878
Mihm MJ, Yu F, Reiser PJ, Bauer JA (2003) Effects of peroxynitrite on isolated cardiac trabeculae: selective impact on myofibrillar energetic controllers. Biochimie 85:587–596
Mukherjee B, Mukherjee JR, Chatterjee M (1994) Lipid peroxidation, glutathione levels and changes in glutathione-related enzyme activities in streptozotocin-induced diabetic rats. Immunol Cell Biol 72:109–114
Pari L, Latha M (2004) Protective role of Scoparia dulcis plant extract on brain antioxidant status and lipidperoxidation in STZ diabetic male Wistar rats. BMC Complement Altern Med 4:16
Perfetti R, Barnett PS, Mathur R, Egan JM (1998) Novel therapeutic strategies for the treatment of type 2 diabetes. Diabetes Metab Rev 14:207–225
Qi WW, Zhong LY, Li XR, Li G, Liu ZX, Hu JF, Chen NH (2012) Hyperglycemia induces the variations of 11β-hydroxysteroid dehydrogenase type 1 and peroxisome proliferator-activated receptor-γ expression in hippocampus and hypothalamus of diabetic rats. Exp Diabetes Res 2012:107130
Rastogi M, Ojha RP, Rajamanickam GV, Agrawal A, Aggarwal A, Dubey GP (2008) Curcuminoids modulates oxidative damage and mitochondrial dysfunction in diabetic rat brain. Free Radic Res 42:999–1005
Reck-Peterson SL, Provance DW Jr, Mooseker MS, Mercer JA (2000) Class V myosins. Biochim Biophys Acta 1496:36–51
Rudolf R, Bittins CM, Gerdes HH (2011) The role of myosin V in exocytosis and synaptic plasticity. J Neurochem 116:177–191
Shanmugam KR, Mallikarjuna K, Kesireddy N, Sathyavelu Reddy K (2011) Neuroprotective effect of ginger on anti-oxidant enzymes in streptozotocin-induced diabetic rats. Food Chem Toxicol 49:893–897
Silva C, Simeoni L, Silveira D (2009) Genus pouteria: chemistry and biological activity. Braz J Pharmacogn 19:501–509
Souza PM, Sales PM, Simeoni LA, Silva EC, Silveira D, Magalhaes Pde O (2012) Inhibitory activity of alpha-amylase and alpha-glucosidase by plant extracts from the Brazilian cerrado. Planta Med 78:393–399
Taleb-Senouci D, Ghomari H, Krouf D, Bouderbala S, Prost J, Lacaille-Dubois MA, Bouchenak M (2009) Antioxidant effect of Ajuga iva aqueous extract in streptozotocin-induced diabetic rats. Phytomedicine 16:623–631
Tilelli CQ, Martins AR, Larson RE, Garcia-Cairasco N (2003) Immunohistochemical localization of myosin Va in the adult rat brain. Neuroscience 121:573–586
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76(9):4350–4354
Van de Laar FA (2008) Alpha-glucosidase inhibitors in the early treatment of type 2 diabetes. Vasc Health Risk Manag 4:1189–1195
VanGilder RL, Kelly KA, Chua MD, Ptachcinski RL, Huber JD (2009) Administration of sesamol improved blood-brain barrier function in streptozotocin-induced diabetic rats. Exp Brain Res 197:23–34
Varadi A, Tsuboi T, Rutter GA (2005) Myosin Va transports dense core secretory vesicles in pancreatic MIN6 beta-cells. Mol Biol Cell 16:2670–2680
Wadhwa S, Anand P, Bhowmick D (1999) Quantitative study of plasticity in the auditory nuclei of chick under conditions of prenatal sound attenuation and overstimulation with species specific and music sound stimuli. Int J Dev Neurosci 17:239–253
Wolff SP (1993) Diabetes mellitus and free radicals. Free radicals, transition metals and oxidative stress in the aetiology of diabetes mellitus and complications. Br Med Bull 49:642–652
Ye L, Wang F, Yang RH (2011) Diabetes impairs learning performance and affects the mitochondrial function of hippocampal pyramidal neurons. Brain Res 1411:57–64
Yoshizaki T, Imamura T, Babendure JL, Lu JC, Sonoda N, Olefsky JM (2007) Myosin 5a is an insulin-stimulated Akt2 (protein kinase Bbeta) substrate modulating GLUT4 vesicle translocation. Mol Cell Biol 27:5172–5183
Zaltzberg H, Kanter Y, Aviram M, Levy Y (1999) Increased plasma oxidizability and decreased erythrocyte and plasma antioxidative capacity in patients with NIDDM. Isr Med Assoc J 1:228–231
Zhu D, Tan KS, Zhang X, Sun AY, Sun GY, Lee JC (2005) Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J Cell Sci 118:3695–3703
Acknowledgments
The authors thank Fernanda Vieira Alves for technical support and the Laboratory of Clinical Analysis of the School of Veterinary Medicine, Federal University of Uberlândia, especially Antônio Vicente Mundim and Felipe Cesar Gonçalves, for help in processing the biochemical data. This work was supported by grants from FAPEMIG to FSE, by a CAPES fellowship to LKC, RJOS and NMG, and a FAPEMIG fellowship to FBF.
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da Costa, A.V., Calábria, L.K., Furtado, F.B. et al. Neuroprotective effects of Pouteria ramiflora (Mart.) Radlk (Sapotaceae) extract on the brains of rats with streptozotocin-induced diabetes. Metab Brain Dis 28, 411–419 (2013). https://doi.org/10.1007/s11011-013-9390-6
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DOI: https://doi.org/10.1007/s11011-013-9390-6