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Effect of Persian sage (Salvia Rhytidia) extract on histomorphometric changes of cerebellum following ischemia reperfusion injuries in rat

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Abstract

In the present study, the role of Salvia Rhytidia (SR) extract in ameliorating cerebellar ischemia reperfusion (IR) injuries is evaluated. This is an experimental in vivo study of 35 healthy male Wistar rats between 250 and 300 g. Animals were randomly divided into seven groups of five rats. In ischemic groups, under general anesthesia, the left common carotid and vertebral arteries were approached from ventral midline cervical incision and occluded for 10 min by Rumel tourniquet. Group A received (3.2 mg/kg) S. Rhytidia extract 72, 48, 24, and 0 h before operation, whereas group C received (50 mg/kg) silymarin 72, 48, 24, and 0 h before operation. Sham group (G) received normal saline (NS) 72, 48, 24, and 0 h before surgery. Control group (E) received nothing, and only the ischemic group (F) created IR injury. Group B received (3.2 mg/kg) SR extract 2 h after operation but group D received (50 mg/kg) silymarin 2 h after surgery. All procedures were achieved in groups A–D. After 24 h, the cerebellum in all the groups was removed for histomorphometrical studies. IR resulted in a significant decrease of the thickness of granular layer and size of Purkinje cells (P < 0/05). The antioxidant effect of SR extract had an influence on prevention of ischemia reperfusion injury of rat cerebellum and can reduce the harmful ischemia injury. The thickness of granular layer and size of Purkinje cells in groups A and C compared to those in groups B, D, and F were significantly increased (P > 0/05), whereas there was no significant increase (P > 0/05) in thickness in groups B and D compared to group F. This study showed that SR extract can protect the forebrain from IR injuries due to anti-oxidative effect of drug which is similar to silymarin.

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References

  • Aliabadi A, Yousefi A, Mahjoor A, Farahmand M (2011) Evaluation of wound healing activity of silymarin (Silybum marianum) in streptozotocin induced experimental diabetes in rats. J Anim Vet Adv 10:3287–3292

    CAS  Google Scholar 

  • Asadi S, Ahmadiani A, Esmaeili MA et al (2010) In vitro antioxidant activities and an investigation of neuroprotection by six Salvia species from Iran: a comparative study. Food Chem Toxicol 48:1341–1349

    Article  CAS  PubMed  Google Scholar 

  • Baser KHC, Kurkcuoglu M, Aytac Z (1998) Composition of the essential oil of Salvia euphratica Montbret et Aucher ex Bentham var. Euphratica from turkey. Flavour Fragr J 13:63–64

    Article  CAS  Google Scholar 

  • Bolaños JP, Almeida A (1999) Role of nitric oxide in brain hypoxia-ischemia. Biochim Biophys Acta 1411:415–436

    Article  PubMed  Google Scholar 

  • Bors W, Heller W, Michel C, Saran M (1990) Flavonoids as antioxidants: determinations of radical-scavenging efficiencies. Methods Enzymol 186:343–355

    Article  CAS  PubMed  Google Scholar 

  • Cao G, Sofic E, Prior RL (1997) Antioxidant and prooxidant behavior of flavonoids: structure–activity relationships. Free Radic Biol Med 22:749–760

    Article  CAS  PubMed  Google Scholar 

  • Cassina A, Radi R (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328:309–316

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Lesnefsky EJ (2006) Depletion of cardiolipin and cytochrome c during ischemia increases hydrogen peroxide production from the electron transport chain. Free Radic Biol Med 15:976–982

    Article  Google Scholar 

  • Chen GY, Nuñez G (2010) Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 10:826–837

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cohen JJ (1993) Overview: mechanisms of apoptosis. Immunol Today 14:126–130

    Article  CAS  PubMed  Google Scholar 

  • Cotelle N, Bernier JL, Catteau JP, Pommery J, Wallet JC, Gaydou EM (1996) Antioxidant properties of hydroxy-flavones. Free Radic Biol Med 20:35–43

    Article  CAS  PubMed  Google Scholar 

  • Cushman M, Nagaratham D, Burg DL, Geahlen RL (1991) Synthesis and protein-tyrosine kinase inhibitory activities of flavonoid analogues. J Med Chem 34:798–806

    Article  CAS  PubMed  Google Scholar 

  • Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391–397

    Article  CAS  PubMed  Google Scholar 

  • Duranteau J, Chandel NS, Kulisz A, Shao Z, Schumacker PT (1998) Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J B iol Chem 8:11619–11624

    Article  Google Scholar 

  • Durrani NK, Yavuzer R, Mittal V et al (2006) The effect of gradually increased blood flow on ischemia-reperfusion injury in rat kidney. Am J Surg 191:334–337

    Article  PubMed  Google Scholar 

  • Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M et al (2009) Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461:282–286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Esmaeili MA, Sonboli A (2010) Antioxidant, free radical scavenging activities of Salvia brachyantha and its protective effect against oxidative cardiac cell injury. Food Chem Toxicol 48:846–853

    Article  CAS  PubMed  Google Scholar 

  • Ghannadi A, Samsam-Shariat SH, Moattar F (1999) Volatile constituents of the flower of Salvia hydrangea DC. ex Benth. Daru 7:23–25

    CAS  Google Scholar 

  • Gil B, Sanz MJ, Terencio MC, Ferrandiz ML, Bustos G, Payà M et al (1994) Effects of flavonoids on Naja naja and human recombinant synovial phospholipase A2 and inflammatory responses in mice. Life Sci 54:333–338

    Article  Google Scholar 

  • Giulivi C, Boveris A, Cadenas E (1995) Hydroxyl radical generation during mitochondrial electron transfer and the formation of 8-hydroxydesoxyguanosine in mitochondrial DNA. Arch Biochem Biophys 316:909–916

    Article  CAS  PubMed  Google Scholar 

  • Gross GJ, Auchampach JA (2007) Reperfusion injury: does it exist? J Mol Cell Cardiol 42:12–18

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gurel A, Armutcu F, Sahin S et al (2004) Protective role of [alpha]-tocopherol and caffeic acid phenethyl ester on ischemia-reperfusion injury via nitric oxide and myeloperoxidase in rat kidneys. Clin Chim Acta 339:33–41

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Han J-Y, Fan J-Y, Horie Y et al (2008) Ameliorating effects of compounds derived from Salvia miltiorrhiza root extract on microcirculatory disturbance and target organ injury by ischemia and reperfusion. Pharmacol Ther 117:280–295

    Article  CAS  PubMed  Google Scholar 

  • Hashemnia1 Sh, Oloumi M, Rezayan M, Derakhshanfar A, Mostafavi A, Hojabri5 Kh, Esmailzadeh S (2009) Persian Sage (Salvia Rhytidia) Essential oil can ameliorate the renal ischemia-reperfusion injuries in rat

  • Hosseinzadeh H, Sadat Motamedshariaty V, Ziaee T (2009) Protective effects of Salvia leriifolia Benth. Root aqueous and ethanolic extracts on renal ischemia-reperfusion in uninephrectomized Wistar male rats. Pharmacologyonline 2:651–655

    Google Scholar 

  • Hou YC1, Liou KT, Chern CM, Wang YH, Liao JF, Chang S, Chou YH, Shen YC (2010).Preventive effect of silymarin in cerebral ischemia-reperfusion-induced brain injury in rats possibly through impairing NF-κB and STAT-1 activation

  • Hoult JRS, Moroney MA, Payà M (1994) Action of flavonoids and coumarins on lipoxygenase and cyclooxygenase. Methods Enzymol 234:443–455

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Agus DB, Winfree CJ, Kiss S, Mack WJ, McTaggart RA, Choudhri TF, Kim LJ, Mocco J, Pinsky DJ, Fox WD, Israel RJ, Boyd TA, Golde DW, Connolly ES Jr (2001) Dehydroascorbic acid, a blood-brain barrier transportable form of vitamin C, mediates potent cerebroprotection in experimental stroke. Proc Natl Acad Sci U S A 98:11720–11724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kietadisorn R, Juni RP, Moens AL (2012) Tackling endothelial dysfunction by modulating NOS uncoupling: new insights into its pathogenesis and therapeutic possibilities. Am J Physiol Endocrinol Metab 302:E481–E495

    Article  CAS  PubMed  Google Scholar 

  • Laughton MJ, Evans PJ, Moroney MA, Hoult JRC, Halliwell B (1991) Inhibition of mammalian 5-lipoxygenase and cyclo-oxygenase by flavonoids and phenolic dietary additives: relationship to antioxidant activity and to ion-reducing ability. Biochem Pharmacol 42:1673–1681

    Article  CAS  PubMed  Google Scholar 

  • Leist M, Nicotera P (1997) Cell death: apoptosis versus necrosis. In: Welch KMA, Caplan LR, Reis DJ et al (eds) Primer on cerebrovascular disease. Academic, Philadelphia, pp 101–104

    Google Scholar 

  • Li J, Zhang H, Zhang C (2012) Role of inflammation in the regulation of coronary blood flow in ischemia and reperfusion: mechanisms and therapeutic implications. J Mol Cell Cardiol 52:865–872

    Article  CAS  PubMed  Google Scholar 

  • Lima CF, Carvalho F, Fernandes E, Bastos ML, Santos-Gomes PC, Fernandes-Ferreira M, Pereira-Wilson C (2004) Evaluation of toxic/protective effects of the essential oil of Salvia officinalis on freshly isolated rat hepatocytes. Toxicol In Vitro 18:457–465

    Article  CAS  PubMed  Google Scholar 

  • Lima CF, Valentao PCR, Andrade PB et al (2007) Water and methanolic extracts of Salvia officinalis protect HepG2 cells from t-BHP induced oxidative damage. Chem-Biol Interact 167:107–115

    Article  CAS  PubMed  Google Scholar 

  • Lo CJ, Lin JG, Kuo JS, Chiang SY, Chen SC, Liao ET, Hsieh CL (2003) Effect of Salvia miltiorrhiza Bunge on cerebral infarct in ischemia-reperfusion injured rats. Am J Chin Med 31(2):191–200

    Article  PubMed  Google Scholar 

  • Lu Y, Foo LY (2002) Polyphenolics of Salvia—a review. Phytochemistry 59:114–140

    Google Scholar 

  • Martin LJ, Sieber FE, Traystman RJ (2000) Apoptosis and necrosis occur in separate neuronal populations in hippocampus and cerebellum after ischemia and are associated with differential alterations in metabotropic glutamate receptor signaling pathways. J Cereb Blood Flow Metab 20:153–167

    Article  CAS  PubMed  Google Scholar 

  • Matsuo Y, Kihara T, Ikeda M, Ninomiya M, Onodera H, Kogure K (1996) Role of platelet-activating factor and thromboxane A2 in radical production during ischemia and reperfusion of the rat brain. Brain Res 709:296–302

    Article  CAS  PubMed  Google Scholar 

  • Mattson MP (1998) Modification of ion homeostasis by lipid peroxidation: roles in neuronal degeneration and adaptive plasticity. Trends Neurosci 20:53–57

    Article  Google Scholar 

  • Middleton E Jr, Kandaswami C, Theoharides TC (2000) The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease and cancer. Pharmacol Rev 52:673–751

    CAS  PubMed  Google Scholar 

  • Moudgil R, Michelakis ED, Archer SL (2005) Hypoxic pulmonary vasoconstriction. J Appl Physiol 98:390–403

    Article  CAS  PubMed  Google Scholar 

  • Nijveldt RJ, van Nood E, van Hoorn DEC, Boelens PG, van Norren K, van Leeuwen PAM (2001) Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 74:418–425

    CAS  PubMed  Google Scholar 

  • Olmez I, Ozyurt H (2012) Reactive oxygen species and ischemic cerebrovascular disease. Neurochem Int 60:208–212

    Article  CAS  PubMed  Google Scholar 

  • Patel PM, Drummond JC, Sano T, Cole DJ, Kalkman CJ, Yaksh TL (1993) Effect of ibuprofen on regional eicosanoid production and neuronal injury after forebrain ischemia in rats. Brain Res 614:315–324

    Article  CAS  PubMed  Google Scholar 

  • Pederson JA (2000) Distribution and taxonomic implications of some phenolics in the family Lamiaceae determined by ESR spectroscopy. Biochem System Ecol 28:229–253

    Article  Google Scholar 

  • Peters O, Back T, Lindauer U, Busch C, Megow D, Dreier J, Dirnagl U (1998) Increased formation of reactive oxygen species after permanent and reversible middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 18:196–205

    Article  CAS  PubMed  Google Scholar 

  • Radi R, Sims S, Cassina A, Turrens JF (1993) Roles of catalase and cytochrome c in hydroperoxide-dependent lipid peroxidation and chemiluminescence in rat heart and kidney mitochondria. Free Radic Biol Med 15:653–659

    Article  CAS  PubMed  Google Scholar 

  • Radi R, Rodriguez M, Castro L, Telleri R (1994) Inhibition of mitochondrial electron transport by peroxynitrite. Arch Biochem Biophys 308:89–95

    Article  CAS  PubMed  Google Scholar 

  • Rao AM, Hatcher JF, Kindy MS, Dempsey RJ (1999) Arachidonicacid and leukotriene C4: role in transient cerebral ischemia of gerbils. Neurochem Res 24:1225–1232

    Article  CAS  PubMed  Google Scholar 

  • Ratty AK, Sunamoto J, Das NP (1988) Interaction of flavonoids with 1, 1-Diphenyl -2-picryhydrazinyl free radical, liposomal membranes and soybean lipoxygenase-1. Biochem Pharmacol 37:989–995

    Article  CAS  PubMed  Google Scholar 

  • Rego AC, Santos MS, Oliveira CR (2000) Glutamatemediated inhibition of oxidative phosphorylation in cultured retinal cells. Neurochem Int 36:159–166

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez F, Bonacasa B, Fenoy FJ, Salom MG (2013) Reactive oxygen and nitrogen species in the renal ischemia/reperfusion injury. Curr Pharm Des 19:2776–2794

    Article  CAS  PubMed  Google Scholar 

  • Saito A, Hayashi T, Okuno S, Nishi T, Chan PH (2004) Modulation of the Omi/HtrA2 signaling pathway after transient focal cerebral ischemia in mouse brains that overexpress SOD1. Brain Res Mol Brain Res 127:89–95

    Article  CAS  PubMed  Google Scholar 

  • Salah N, Miller NJ, Paganga G, Tijburg L, Bolwell GP, Rice-Evans C (1995) Polyphenolic flavanols as scavengers of aqueous phase radicals and as chain-breaking antioxidants. Arch Biochem Biophys 322:339–346

    Article  CAS  PubMed  Google Scholar 

  • Schweizer M, Richter C (1994) Gliotoxin stimulates Ca2+ release from intact rat liver mitochondria. Biochemistry 33:13401–13405

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Qiu X, Jiang B, Zhang D, Xin W, Fung PCW, Zhao B (2003) Nitric oxide and oxygen radicals induced apoptosis via bcl-2 and p53 pathway in hypoxia-reoxygenated cardiomyocytes. Sci China C Life Sci 46:28–39

    Article  CAS  PubMed  Google Scholar 

  • Sivropoulou A, Nikolaou C, Papanikolaou E, Kokkini S, Lanars T, Arsenakis M (1997) Antimicrobial cytotoxic and antiviral activity of Salvia fructicosa essential oil. J Agric Food Chem 45:3197–3201

    Article  CAS  Google Scholar 

  • Springer JE, Azbill RD, Mark RJ, Begley JG, Waeg G, Mattson MP (1997) 4-Hydroxynonenal, a lipid peroxidation product, rapidly accumulates following traumatic spinal cord injury and inhibits glutamate uptake. J Neurochem 68:2469–2476

    Article  CAS  PubMed  Google Scholar 

  • Takadera T, Matsuda I, Ohyashiki T (1999) Apoptotic cell death and caspase-3 activation induced by N-methyl-D-aspartate receptor antagonists and their prevention by insulin-like growth factor I. J Neurochem 73:548–556

    Article  CAS  PubMed  Google Scholar 

  • Tel G, Öztürk M, Duru ME et al (2010) Chemical composition of the essential oil and hexane extract of Salvia chionantha and their antioxidant and anticholinesterase activities. Food Chem Toxicol 48:3189–3193

    Article  CAS  PubMed  Google Scholar 

  • Tepe B (2008) Antioxidant potentials and rosmarinic acid levels of the methanolic extracts of Salvia virgata (Jacq), Salvia staminea (Montbret & Aucher ex Bentham) and Salvia verbenaca (L.) from Turkey. Bioresource Technol 99:1584–1588

    Article  CAS  Google Scholar 

  • Tepe B, Daferera D, Sokmen A et al (2005) Antimicrobial and antioxidant activities of the essential oil and various extracts of Salvia tomentosa Miller (Lamiaceae). Food Chem 90:333–340

    Article  CAS  Google Scholar 

  • Terao J, Piskula M, Yao Q (1994) Protective effect of epicatechin, epicatechin gallate, and quercetin on lipid peroxidation in phospholipid bilayers. Arch Biochem Biophys 308:278–284

    Article  CAS  PubMed  Google Scholar 

  • Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267:1456–1462

    Article  CAS  PubMed  Google Scholar 

  • Toescu EC (2004) Hypoxia response elements. Cell Calcium 36:181–185

    Article  CAS  PubMed  Google Scholar 

  • Tsai-Hui Lin, Ching-Liang Hsieh (2010) Pharmacological effects of Salvia miltiorrhiza (Danshen) on cerebral infarction

  • Vaux L, Haecker G, Strasser A (1994) An evolutionary perspective on apoptosis. Cell 76:777–779

    Article  CAS  PubMed  Google Scholar 

  • Vitturi DA, Patel RP (2011) Current perspectives and challenges in understanding the role of nitrite as an integral player in nitric oxide biology and therapy. Free Radic Biol Med 51:805–812

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Watanabe T, Yuki S, Egawa M, Nishi H (1994) Protective effects of MCI-186 on cerebral ischemia possible involvement of free radical scavenging and antioxidant actions. J Pharmacol Exp Ther 268:1597–1604

    CAS  PubMed  Google Scholar 

  • Waypa GB, Schumacker PT (2005) Hypoxic pulmonary vasoconstriction: redox events in oxygen sensing. J Appl Physiol 98:404–414

    Article  CAS  PubMed  Google Scholar 

  • Westerberg E, Deshpande JK, Wieloch T (1987) Regional differences in arachidonic acid release in rat hippocampal CA1 and CA3 regions during cerebral ischemia. J Cereb Blood Flow Metab 7:189–192

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Marcillat O, Giulivi C, Ernster L, Davies KJ (1990) The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J Biol Chem 265:16330–16336

    CAS  PubMed  Google Scholar 

  • Zhang W, Wang J, Zhou Y, Yi Li J (2003). Gadolinium chloride and Salvia miltiorrhiza compound ameliorate reperfusion injury in hepatocellular mitochondria. 9(9):2040–2044

  • Zhao G-R, Xiang Z-J, Ye T-X et al (2006) Antioxidant activities of Salvia miltiorrhiza and Panax notoginseng. Food Chem 99:767–774

    Article  CAS  Google Scholar 

  • Zhao G-R, Zhang H-M, Ye T-X et al (2008) Characterization of the radical scavenging and antioxidant activities of danshensu and salvianolic acid B. Food Chem Toxicol 46:73–81

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Town JR, Yang A et al (2010) A novel ELR-CXC cemokine antagonist reduces intestinal ischemia reperfusion-induced mortality, and local and remote organ injury. J Surg Res 162:264–273

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The author would like to thank Prof. S. Dehghani from the Department of Surgery, School of Veterinary Medicine of Shiraz University, for performing surgical procedure on rat.

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  1. Department of Basic Science, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

    Maryam Farahmand & Mina Tadjali

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  1. Maryam Farahmand
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Correspondence to Maryam Farahmand.

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Farahmand, M., Tadjali, M. Effect of Persian sage (Salvia Rhytidia) extract on histomorphometric changes of cerebellum following ischemia reperfusion injuries in rat. Comp Clin Pathol 24, 1129–1137 (2015). https://doi.org/10.1007/s00580-014-2046-z

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