Login Register Cart 0
Generic placeholder image

The Natural Products Journal

Editor-in-Chief

ISSN (Print): 2210-3155
ISSN (Online): 2210-3163

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Neuroprotective Effect of Nano Emulsion Containing Salvia on CA1 Region of Hippocampus Following Transient Global Ischemia/Reperfusion in Rat

Author(s): Mahsa Abdolrahimkhan, Negar Motakef Kazemi, Shabnam Movassaghi, Nazanin Gharehkhani, Hamid Zaferani Arani and Zahra Nadia Sharifi*

Volume 12, Issue 5, 2022

Published on: 11 January, 2022

Article ID: e011021196945 Pages: 10

DOI: 10.2174/2210315511666211001141515

Price: $65

Abstract

Background: Ischemia/reperfusion (I/R) injury is one of the major causes of mortality. I/R injury leads to apoptosis in the brain, especially in the hippocampus and induces cognitive impairments. On the other hand, Salvia officinalis L. is perennial, evergreen subshrub that is widely used in traditional medicine. The antiapoptosis and antioxidant effects of Salvia officinalis L. have also been reported.

Objective: In this study, we aimed to investigate the effect of Salvia officinalis L. on the expression of genes involved in apoptosis and percentage of viable neurons in the CA1 hippocampal region of rats following transient global I/R.

Methods: The expression of Bcl-2, Bax, and Caspase 3 was evaluated using Real time PCR. Nissl staining was used to measure the number of viable neurons. The percentage of cell viability was also evaluated using MTT assay and flow cytometry. Salvia officinalis L. was injected intraperitoneal at the doses of 50, 75, and 100 mg/kg at both aqueous-alcoholic and aqueous extracts.

Results: The expression of Bax and Caspase 3 was increased and the expression of Bcl-2 was decreased following transient global I/R in the CA1 region. The injection of Salvia officinalis L. at most doses reversed the effect of transient global I/R on genes expression. The number of viable neurons in the CA1 region was also decreased following transient global I/R and injection of Salvia officinalis L. at all doses reversed this effect.

Conclusion: Transient global I/R significantly promotes apoptosis and cell death, and Salvia officinalis L. may induce neuroprotective and anti-apoptosis effects.

Keywords: Neuroprotective, nano emulsion, salvia, hippocampus, ischemia, reperfusion, anti-apoptosis.

Graphical Abstract

[1]
Zhang, M.; Yan, H.; Li, S.; Yang, J. Rosmarinic acid protects rat hippocampal neurons from cerebral ischemia/reperfusion injury via the Akt/JNK3/caspase-3 signaling pathway. Brain Res., 2017, 1657, 9-15.
[http://dx.doi.org/10.1016/j.brainres.2016.11.032] [PMID: 27923634]
[2]
Lozano, R.; Naghavi, M.; Foreman, K.; Lim, S.; Shibuya, K.; Aboyans, V.; Abraham, J.; Adair, T.; Aggarwal, R.; Ahn, S.Y.; Alvarado, M.; Anderson, H.R.; Anderson, L.M.; Andrews, K.G.; Atkinson, C.; Baddour, L.M.; Barker-Collo, S.; Bartels, D.H.; Bell, M.L.; Benjamin, E.J.; Bennett, D.; Bhalla, K.; Bikbov, B.; Bin Abdulhak, A.; Birbeck, G.; Blyth, F.; Bolliger, I.; Boufous, S.; Bucello, C.; Burch, M.; Burney, P.; Carapetis, J.; Chen, H.; Chou, D.; Chugh, S.S.; Coffeng, L.E.; Colan, S.D.; Colquhoun, S.; Colson, K.E.; Condon, J.; Connor, M.D.; Cooper, L.T.; Corriere, M.; Cortinovis, M.; de Vaccaro, K.C.; Couser, W.; Cowie, B.C.; Criqui, M.H.; Cross, M.; Dabhadkar, K.C.; Dahodwala, N.; De Leo, D.; Degenhardt, L.; Delossantos, A.; Denenberg, J.; Des Jarlais, D.C.; Dharmaratne, S.D.; Dorsey, E.R.; Driscoll, T.; Duber, H.; Ebel, B.; Erwin, P.J.; Espindola, P.; Ezzati, M.; Feigin, V.; Flaxman, A.D.; Forouzanfar, M.H.; Fowkes, F.G.; Franklin, R.; Fransen, M.; Freeman, M.K.; Gabriel, S.E.; Gakidou, E.; Gaspari, F.; Gillum, R.F.; Gonzalez-Medina, D.; Halasa, Y.A.; Haring, D.; Harrison, J.E.; Havmoeller, R.; Hay, R.J.; Hoen, B.; Hotez, P.J.; Hoy, D.; Jacobsen, K.H.; James, S.L.; Jasrasaria, R.; Jayaraman, S.; Johns, N.; Karthikeyan, G.; Kassebaum, N.; Keren, A.; Khoo, J.P.; Knowlton, L.M.; Kobusingye, O.; Koranteng, A.; Krishnamurthi, R.; Lipnick, M.; Lipshultz, S.E.; Ohno, S.L.; Mabweijano, J.; MacIntyre, M.F.; Mallinger, L.; March, L.; Marks, G.B.; Marks, R.; Matsumori, A.; Matzopoulos, R.; Mayosi, B.M.; McAnulty, J.H.; McDermott, M.M.; McGrath, J.; Mensah, G.A.; Merriman, T.R.; Michaud, C.; Miller, M.; Miller, T.R.; Mock, C.; Mocumbi, A.O.; Mokdad, A.A.; Moran, A.; Mulholland, K.; Nair, M.N.; Naldi, L.; Narayan, K.M.; Nasseri, K.; Norman, P.; O’Donnell, M.; Omer, S.B.; Ortblad, K.; Osborne, R.; Ozgediz, D.; Pahari, B.; Pandian, J.D.; Rivero, A.P.; Padilla, R.P.; Perez-Ruiz, F.; Perico, N.; Phillips, D.; Pierce, K.; Pope, C.A., III; Porrini, E.; Pourmalek, F.; Raju, M.; Ranganathan, D.; Rehm, J.T.; Rein, D.B.; Remuzzi, G.; Rivara, F.P.; Roberts, T.; De León, F.R.; Rosenfeld, L.C.; Rushton, L.; Sacco, R.L.; Salomon, J.A.; Sampson, U.; Sanman, E.; Schwebel, D.C.; Segui-Gomez, M.; Shepard, D.S.; Singh, D.; Singleton, J.; Sliwa, K.; Smith, E.; Steer, A.; Taylor, J.A.; Thomas, B.; Tleyjeh, I.M.; Towbin, J.A.; Truelsen, T.; Undurraga, E.A.; Venketasubramanian, N.; Vijayakumar, L.; Vos, T.; Wagner, G.R.; Wang, M.; Wang, W.; Watt, K.; Weinstock, M.A.; Weintraub, R.; Wilkinson, J.D.; Woolf, A.D.; Wulf, S.; Yeh, P.H.; Yip, P.; Zabetian, A.; Zheng, Z.J.; Lopez, A.D.; Murray, C.J.; AlMazroa, M.A.; Memish, Z.A. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: A systematic analysis for the Global Burden of Disease Study 2010. Lancet, 2012, 380(9859), 2095-2128.
[http://dx.doi.org/10.1016/S0140-6736(12)61728-0] [PMID: 23245604]
[3]
Hankey, G.J. Potential new risk factors for ischemic stroke: What is their potential? Stroke, 2006, 37(8), 2181-2188.
[http://dx.doi.org/10.1161/01.STR.0000229883.72010.e4] [PMID: 16809576]
[4]
Ritzel, R.M.; Pan, S.J.; Verma, R.; Wizeman, J.; Crapser, J.; Patel, A.R.; Lieberman, R.; Mohan, R.; McCullough, L.D. Early retinal inflammatory biomarkers in the middle cerebral artery occlusion model of ischemic stroke. Mol. Vis., 2016, 22, 575-588.
[PMID: 27293375]
[5]
Lavenex, P.; Banta Lavenex, P.; Amaral, D.G. Postnatal development of the primate hippocampal formation. Dev. Neurosci., 2007, 29(1-2), 179-192.
[http://dx.doi.org/10.1159/000096222] [PMID: 17148960]
[6]
Pu, F.; Motohashi, K.; Kaneko, T.; Tanaka, Y.; Manome, N.; Irie, K.; Takata, J.; Egashira, N.; Oishi, R.; Okamoto, T.; Sei, Y.; Yokozawa, T.; Mishima, K.; Iwasaki, K.; Fujiwara, M. Neuroprotective effects of Kangen-karyu on spatial memory impairment in an 8-arm radial maze and neuronal death in the hippocampal CA1 region induced by repeated cerebral ischemia in rats. J. Pharmacol. Sci., 2009, 109(3), 424-430.
[http://dx.doi.org/10.1254/jphs.08245FP] [PMID: 19276616]
[7]
Smith, P.F.; Darlington, C.L.; Zhen, Y. The effects of complete vestibular deafferentation on spatial memory and the hippocampus in the rat: The dunedin experience. Multisens. Res., 2015, 28(5-6), 461-485.
[http://dx.doi.org/10.1163/22134808-00002469] [PMID: 26595952]
[8]
Javad-Moosavi, B.Z.; Nasehi, M.; Vaseghi, S.; Jamaldini, S.H.; Zarrindast, M.R. Activation and inactivation of nicotinic receptnors in the dorsal hippocampal region restored negative effects of total (TSD) and REM sleep deprivation (RSD) on memory acquisition, locomotor activity and pain perception. Neuroscience, 2020, 433, 200-211.
[http://dx.doi.org/10.1016/j.neuroscience.2020.03.006] [PMID: 32200080]
[9]
Rezaie, M.; Nasehi, M.; Vaseghi, S.; Alimohammadzadeh, K.; Islami Vaghar, M.; Mohammadi-Mahdiabadi-Hasani, M.H.; Zarrindast, M.R. The interaction effect of sleep deprivation and cannabinoid type 1 receptor in the CA1 hippocampal region on passive avoidance memory, depressive-like behavior and locomotor activity in rats. Behav. Brain Res., 2021, 396, 112901.
[http://dx.doi.org/10.1016/j.bbr.2020.112901] [PMID: 32920013]
[10]
Mirarab, E.; Hojati, V.; Vaezi, G.; Shiravi, A.; Khaksari, M. Obestatin inhibits apoptosis and astrogliosis of hippocampal neurons following global cerebral ischemia reperfusion via antioxidant and anti-inflammatory mechanisms. Iran. J. Basic Med. Sci., 2019, 22(6), 617-622.
[PMID: 31231488]
[11]
Erfani, S.; Khaksari, M.; Oryan, S.; Shamsaei, N.; Aboutaleb, N.; Nikbakht, F.; Jamali-Raeufy, N.; Gorjipour, F. Visfatin reduces hippocampal CA1 cells death and improves learning and memory deficits after transient global ischemia/reperfusion. Neuropeptides, 2015, 49, 63-68.
[http://dx.doi.org/10.1016/j.npep.2014.12.004] [PMID: 25617953]
[12]
Shamsaei, N.; Khaksari, M.; Erfani, S.; Rajabi, H.; Aboutaleb, N. Exercise preconditioning exhibits neuroprotective effects on hippocampal CA1 neuronal damage after cerebral ischemia. Neural Regen. Res., 2015, 10(8), 1245-1250.
[http://dx.doi.org/10.4103/1673-5374.162756] [PMID: 26487851]
[13]
Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516.
[http://dx.doi.org/10.1080/01926230701320337] [PMID: 17562483]
[14]
Chen, Y.F.; Wu, K.J.; Huang, W.S.; Hsieh, Y.W.; Wang, Y.W.; Tsai, H.Y.; Lee, M.M. Neuroprotection of Gueichih-Fuling-Wan on cerebral ischemia/ reperfusion injury in streptozotocin-induced hyperglycemic rats via the inhibition of the cellular apoptosis pathway and neuroinflammation. Biomedicine (Taipei), 2016, 6(4), 21.
[http://dx.doi.org/10.7603/s40681-016-0021-5] [PMID: 27854047]
[15]
Nasehi, M.; Torabinejad, S.; Hashemi, M.; Vaseghi, S.; Zarrindast, M.R. Effect of cholestasis and NeuroAid treatment on the expression of Bax, Bcl-2, Pgc-1α and Tfam genes involved in apoptosis and mitochondrial biogenesis in the striatum of male rats. Metab. Brain Dis., 2020, 35(1), 183-192.
[http://dx.doi.org/10.1007/s11011-019-00508-y] [PMID: 31773435]
[16]
Doyle, K.P.; Simon, R.P.; Stenzel-Poore, M.P. Mechanisms of ischemic brain damage. Neuropharmacology, 2008, 55(3), 310-318.
[http://dx.doi.org/10.1016/j.neuropharm.2008.01.005] [PMID: 18308346]
[17]
Azmand, M.J.; Rajaei, Z. Effects of crocin on spatial or aversive learning and memory impairments induced by lipopolysaccharide in rats. Avicenna J. Phytomed., 2021, 11(1), 79-90.
[PMID: 33628722]
[18]
Sun, X.J.; Zhao, X.; Xie, J.N.; Wan, H. Crocin alleviates schizophrenia-like symptoms in rats by upregulating silent information regulator-1 and brain derived neurotrophic factor. Compr. Psychiatry, 2020, 103, 152209.
[http://dx.doi.org/10.1016/j.comppsych.2020.152209] [PMID: 33045669]
[19]
Azami, S.; Shahriari, Z.; Asgharzade, S.; Farkhondeh, T.; Sadeghi, M.; Ahmadi, F.; Vahedi, M.M.; Forouzanfar, F. Therapeutic potential of saffron (Crocus sativus L.) in ischemia stroke. Evid. Based Complement. Alternat. Med., 2021, 2021, 6643950.
[http://dx.doi.org/10.1155/2021/6643950] [PMID: 33747107]
[20]
Malboosi, N.; Nasehi, M.; Hashemi, M.; Vaseghi, S.; Zarrindast, M.R. The neuroprotective effect of NeuroAid on morphine-induced amnesia with respect to the expression of TFAM, PGC-1α, ΔfosB and CART genes in the hippocampus of male Wistar rats. Gene, 2020, 742, 144601.
[http://dx.doi.org/10.1016/j.gene.2020.144601] [PMID: 32198124]
[21]
Nasehi, M.; Zadeh-Tehrani, S.N.; Khakpai, F.; Zarrindast, M.R. A possible neuroprotective property of ethanol and/or NeuroAiD on the modulation of cognitive function. Neurotoxicol. Teratol., 2020, 82, 106927.
[http://dx.doi.org/10.1016/j.ntt.2020.106927] [PMID: 32861843]
[22]
Brindisi, M.; Bouzidi, C.; Frattaruolo, L.; Loizzo, M.R.; Cappello, M.S.; Dugay, A.; Deguin, B.; Lauria, G.; Cappello, A.R.; Tundis, R. New I\insights into the antioxidant and anti-inflammatory effects of italian salvia officinalis leaf and flower extracts in lipopolysaccharide and tumor-mediated inflammation models. Antioxidants, 2021, 10(2), 311.
[http://dx.doi.org/10.3390/antiox10020311] [PMID: 33669555]
[23]
Ghorbani, A.; Esmaeilizadeh, M. Pharmacological properties of Salvia officinalis and its components. J. Tradit. Complement. Med., 2017, 7(4), 433-440.
[http://dx.doi.org/10.1016/j.jtcme.2016.12.014] [PMID: 29034191]
[24]
Jakovljević, M.; Jokić, S.; Molnar, M.; Jašić, M.; Babić, J.; Jukić, H.; Banjari, I. Bioactive profile of various Salvia officinalis L. preparations. Plants, 2019, 8(3), E55.
[http://dx.doi.org/10.3390/plants8030055] [PMID: 30845696]
[25]
Cortese, K.; Daga, A.; Monticone, M.; Tavella, S.; Stefanelli, A.; Aiello, C.; Bisio, A.; Bellese, G.; Castagnola, P. Carnosic acid induces proteasomal degradation of Cyclin B1, RB and SOX2 along with cell growth arrest and apoptosis in GBM cells. Phytomedicine, 2016, 23(7), 679-685.
[http://dx.doi.org/10.1016/j.phymed.2016.03.007] [PMID: 27235706]
[26]
AlMotwaa, S.M.; Alkhatib, M.H.; Alkreathy, H.M. Incorporating ifosfamide into salvia oil-based nanoemulsion diminishes its nephrotoxicity in mice inoculated with tumor. Bioimpacts, 2020, 10(1), 9-16.
[http://dx.doi.org/10.15171/bi.2020.02] [PMID: 31988852]
[27]
Huang, J.; Shen, C.; Ye, R.; Shi, Y.; Li, W. The effect of early maternal separation combined with adolescent chronic unpredictable mild stress on behavior and synaptic plasticity in adult female rats. Front. Psychiatry, 2021, 12, 539299.
[http://dx.doi.org/10.3389/fpsyt.2021.539299] [PMID: 33746787]
[28]
Kumar, P.; Nagarajan, A.; Uchil, P.D. Analysis of cell viability by the MTT assay. Cold Spring Harb. Protoc., 2018, 2018(6)
[http://dx.doi.org/10.1101/pdb.prot095505] [PMID: 29858338]
[29]
Aubry, J.P.; Blaecke, A.; Lecoanet-Henchoz, S.; Jeannin, P.; Herbault, N.; Caron, G.; Moine, V.; Bonnefoy, J.Y. Annexin V used for measuring apoptosis in the early events of cellular cytotoxicity. Cytometry, 1999, 37(3), 197-204.
[http://dx.doi.org/10.1002/(SICI)1097-0320(19991101)37:3<197::AID-CYTO6>3.0.CO;2-L] [PMID: 10520200]
[30]
Wan, K.; Mao, F.; Li, Q.; Wang, L.; Wei, Z.; Wang, P.; Liao, X.; Xu, M.; Huang, J.; Pan, Z.; Wang, C.; Luo, J.; Gao, R.; Gan, S. Neuritin-overexpressing transgenic mice demonstrate enhanced neuroregeneration capacity and improved spatial learning and memory recovery after ischemia-reperfusion injury. Aging (Albany NY), 2020, 13(2), 2681-2699.
[http://dx.doi.org/10.18632/aging.202318] [PMID: 33323541]
[31]
Petito, C.K.; Feldmann, E.; Pulsinelli, W.A.; Plum, F. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology, 1987, 37(8), 1281-1286.
[http://dx.doi.org/10.1212/WNL.37.8.1281] [PMID: 3614648]
[32]
Pulsinelli, W.A.; Brierley, J.B.; Plum, F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol., 1982, 11(5), 491-498.
[http://dx.doi.org/10.1002/ana.410110509] [PMID: 7103425]
[33]
Langdon, K.D.; Granter-Button, S.; Corbett, D. Persistent behavioral impairments and neuroinflammation following global ischemia in the rat. Eur. J. Neurosci., 2008, 28(11), 2310-2318.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06513.x] [PMID: 19019197]
[34]
Bonato, J.M.; Meyer, E.; de Mendonça, P.S.B.; Milani, H.; Prickaerts, J.; Weffort de Oliveira, R.M. Roflumilast protects against spatial memory impairments and exerts anti-inflammatory effects after transient global cerebral ischemia. Eur. J. Neurosci., 2021, 53(4), 1171-1188.
[http://dx.doi.org/10.1111/ejn.15089] [PMID: 33340424]
[35]
Lee, N.T.; Selan, C.; Chia, J.S.J.; Sturgeon, S.A.; Wright, D.K.; Zamani, A.; Pereira, M.; Nandurkar, H.H.; Sashindranath, M. Characterization of a novel model of global forebrain ischaemia-reperfusion injury in mice and comparison with focal ischaemic and haemorrhagic stroke. Sci. Rep., 2020, 10(1), 18170.
[http://dx.doi.org/10.1038/s41598-020-75034-4] [PMID: 33097782]
[36]
Wahul, A.B.; Joshi, P.C.; Kumar, A.; Chakravarty, S. Transient global cerebral ischemia differentially affects cortex, striatum and hippocampus in Bilateral Common Carotid Arterial occlusion (BCCAo) mouse model. J. Chem. Neuroanat., 2018, 92, 1-15.
[http://dx.doi.org/10.1016/j.jchemneu.2018.04.006] [PMID: 29702163]
[37]
Milanlioglu, A.; Aslan, M.; Ozkol, H.; Çilingir, V.; Nuri Aydın, M.; Karadas, S. Serum antioxidant enzymes activities and oxidative stress levels in patients with acute ischemic stroke: influence on neurological status and outcome. Wien. Klin. Wochenschr., 2016, 128(5-6), 169-174.
[http://dx.doi.org/10.1007/s00508-015-0742-6] [PMID: 25854910]
[38]
Jangholi, E.; Sharifi, Z.N.; Hoseinian, M.; Zarrindast, M.R.; Rahimi, H.R.; Mowla, A.; Aryan, H.; Javidi, M.A.; Parsa, Y.; Ghaffarpasand, F.; Yadollah-Damavandi, S.; Arani, H.Z.; Shahi, F.; Movassaghi, S. Verapamil inhibits mitochondria-induced reactive oxygen species and dependent apoptosis pathways in cerebral transient global ischemia/reperfusion. Oxid. Med. Cell. Longev., 2020, 2020, 5872645.
[http://dx.doi.org/10.1155/2020/5872645] [PMID: 33133347]
[39]
Tu, Q.; Wang, R.; Ding, B.; Zhong, W.; Cao, H. Protective and antioxidant effect of Danshen polysaccharides on cerebral ischemia/reperfusion injury in rats. Int. J. Biol. Macromol., 2013, 60, 268-271.
[http://dx.doi.org/10.1016/j.ijbiomac.2013.05.035] [PMID: 23748011]
[40]
Ghowsi, M.; Yousofvand, N.; Moradi, S. Effects of Salvia officinalis L. (common sage) leaves tea on insulin resistance, lipid profile, and oxidative stress in rats with polycystic ovary: An experimental study. Avicenna J. Phytomed., 2020, 10(3), 263-272.
[PMID: 32523881]
[41]
Taheri, R.; Hadipour, E.; Tayarani-Najaran, Z. Crocin protects against beta-amyloid peptide-induced apoptosis in PC12 cells via PI3 K pathway. Curr. Mol. Pharmacol., 2021, 14(4), 627-634.
[http://dx.doi.org/10.2174/1874467213666201012160401] [PMID: 33045973]
[42]
Looti Bashiyan, M.; Nasehi, M.; Vaseghi, S.; Khalifeh, S. Investigating the effect of crocin on memory deficits induced by total sleep deprivation (TSD) with respect to the BDNF, TrkB and ERK levels in the hippocampus of male Wistar rats. J. Psychopharmacol., 2021, 35(6), 744-754.
[http://dx.doi.org/10.1177/02698811211000762] [PMID: 33899577]
[43]
Hadizadeh-Bazaz, M.; Vaezi, G.; Khaksari, M.; Hojati, V. Curcumin attenuates spatial memory impairment by anti-oxidative, anti-apoptosis, and anti-inflammatory mechanism against methamphetamine neurotoxicity in male Wistar rats: Histological and biochemical changes. Neurotoxicology, 2021, 84, 208-217.
[http://dx.doi.org/10.1016/j.neuro.2021.03.011] [PMID: 33819551]
[44]
Zheng, Y.; Zhang, J.; Zhao, Y.; Zhang, Y.; Zhang, X.; Guan, J.; Liu, Y.; Fu, J. Curcumin protects against cognitive impairments in a rat model of chronic cerebral hypoperfusion combined with diabetes mellitus by suppressing neuroinflammation, apoptosis, and pyroptosis. Int. Immunopharmacol., 2021, 93, 107422.
[http://dx.doi.org/10.1016/j.intimp.2021.107422] [PMID: 33548579]
[45]
Hamidpour, M.; Hamidpour, R.; Hamidpour, S.; Shahlari, M. Chemistry, pharmacology, and medicinal property of sage (Salvia) to prevent and cure illnesses such as obesity, diabetes, depression, dementia, lupus, autism, heart disease, and cancer. J. Tradit. Complement. Med., 2014, 4(2), 82-88.
[http://dx.doi.org/10.4103/2225-4110.130373] [PMID: 24860730]
[46]
Lima, C.F.; Andrade, P.B.; Seabra, R.M.; Fernandes-Ferreira, M.; Pereira-Wilson, C. The drinking of a Salvia officinalis infusion improves liver antioxidant status in mice and rats. J. Ethnopharmacol., 2005, 97(2), 383-389.
[http://dx.doi.org/10.1016/j.jep.2004.11.029] [PMID: 15707779]
[47]
Qnais, E.Y.; Abu-Dieyeh, M.; Abdulla, F.A.; Abdalla, S.S. The antinociceptive and anti-inflammatory effects of Salvia officinalis leaf aqueous and butanol extracts. Pharm. Biol., 2010, 48(10), 1149-1156.
[http://dx.doi.org/10.3109/13880200903530763] [PMID: 20860437]
[48]
Xavier, C.P.; Lima, C.F.; Fernandes-Ferreira, M.; Pereira-Wilson, C. Salvia fruticosa, Salvia officinalis, and rosmarinic acid induce apoptosis and inhibit proliferation of human colorectal cell lines: the role in MAPK/ERK pathway. Nutr. Cancer, 2009, 61(4), 564-571.
[http://dx.doi.org/10.1080/01635580802710733] [PMID: 19838929]
[49]
Zhong, J.; Zhou, J.; Sun, H.; Wu, Y.; Wu, Y.; Li, M. Effects of Salvia miltiorrhiza injection on apoptosis of Schwann cells induced by hydrogen peroxide. Ann. Palliat. Med., 2021, 10(1), 625-632.
[http://dx.doi.org/10.21037/apm-20-2580] [PMID: 33545791]
[50]
Kempuraj, D.; Madhappan, B.; Christodoulou, S.; Boucher, W.; Cao, J.; Papadopoulou, N.; Cetrulo, C.L.; Theoharides, T.C. Flavonols inhibit proinflammatory mediator release, intracellular calcium ion levels and protein kinase C theta phosphorylation in human mast cells. Br. J. Pharmacol., 2005, 145(7), 934-944.
[http://dx.doi.org/10.1038/sj.bjp.0706246] [PMID: 15912140]
[51]
Kitagawa, K. CREB and cAMP response element-mediated gene expression in the ischemic brain. FEBS J., 2007, 274(13), 3210-3217.
[http://dx.doi.org/10.1111/j.1742-4658.2007.05890.x] [PMID: 17565598]
[52]
Bollen, E.; Puzzo, D.; Rutten, K.; Privitera, L.; De Vry, J.; Vanmierlo, T.; Kenis, G.; Palmeri, A.; D’Hooge, R.; Balschun, D.; Steinbusch, H.M.; Blokland, A.; Prickaerts, J. Improved long-term memory via enhancing cGMP-PKG signaling requires cAMP-PKA signaling. Neuropsychopharmacology, 2014, 39(11), 2497-2505.
[http://dx.doi.org/10.1038/npp.2014.106] [PMID: 24813825]
[53]
Salminen, A.; Liu, P.K.; Hsu, C.Y. Alteration of transcription factor binding activities in the ischemic rat brain. Biochem. Biophys. Res. Commun., 1995, 212(3), 939-944.
[http://dx.doi.org/10.1006/bbrc.1995.2060] [PMID: 7626134]
[54]
Khodagholi, F.; Ashabi, G. Dietary supplementation with Salvia sahendica attenuates memory deficits, modulates CREB and its down-stream molecules and decreases apoptosis in amyloid beta-injected rats. Behav. Brain Res., 2013, 241, 62-69.
[http://dx.doi.org/10.1016/j.bbr.2012.11.026] [PMID: 23201360]
[55]
Sun, L.; Zhao, R.; Zhang, L.; Zhang, W.; He, G.; Yang, S.; Song, J.; Du, G. Prevention of vascular smooth muscle cell proliferation and injury-induced neointimal hyperplasia by CREB-mediated p21 induction: An insight from a plant polyphenol. Biochem. Pharmacol., 2016, 103, 40-52.
[http://dx.doi.org/10.1016/j.bcp.2016.01.015] [PMID: 26807478]

Rights & Permissions Print Cite
Article Metrics
11
1
© 2024 Bentham Science Publishers | Privacy Policy