Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2019

Open Access 01-12-2019 | Cytokines | Research article

Anti-inflammatory and nephroprotective activity of Juglans mollis against renal ischemia–reperfusion damage in a Wistar rat model

Authors: Jonathan Perez-Meseguer, Liliana Torres-González, Jorge Aurelio Gutiérrez-González, Gabriela Alarcón-Galván, Homero Zapata-Chavira, Noemi Waksman-de Torres, Diana Patricia Moreno-Peña, Linda Elsa Muñoz-Espinosa, Paula Cordero-Pérez

Published in: BMC Complementary Medicine and Therapies | Issue 1/2019

Login to get access

Abstract

Background

Oxidative stress and the inflammatory process are involved in ischemia–reperfusion (I/R) injury. Juglans mollis has been reported as having antioxidant activity, which could attenuate the damage caused by I/R. We evaluated whether a methanolic extract of Juglans mollis (JM) exhibits nephroprotective activity in a Wistar rat model of I/R injury.

Methods

Four groups of six rats were used: Sham, I/R, JM, and JM + I/R. Two groups were dosed with JM (300 mg/kg) for 7 days before I/R. I/R injury was induced by clamping the renal hilums for 45 min and then reperfusing the kidneys for 15 h. Blood samples were taken to evaluate the levels of alanine aminotransferase (ALT), blood urea nitrogen, creatinine, superoxide dismutase (SOD), malondialdehyde (MDA), interleukin 1β (IL-1β), IL-6, and tumor necrosis factor α (TNF-α).

Results

The levels of creatinine, ALT, MDA, IL-1β, IL-6, and TNF-α were lower in JM + I/R than in I/R rats, whereas SOD level only was higher in JM + I/R than in Sham rats. No biochemical or histological damage was observed in JM rats compared with Sham rats; however, less histological damage was observed in JM + I/R rats compared with I/R rats.

Conclusions

To our knowledge, this is the first report of nephroprotective activity of J. mollis against damage induced by I/R. This activity may be related to decreased levels of proinflammatory cytokines (IL-1β, IL-6, and TNF-α) and modulation of oxidative stress markers (SOD and MDA) observed in the present study.
Literature
1.
go back to reference Zahran MH, Hussein AM, Barakat N, Awadalla A, Khater S, Harraz A, et al. Sildenafil activates antioxidant and antiapoptotic genes and inhibits proinflammatory cytokine genes in a rat model of renal ischemia/reperfusion injury. Int Urol Nephrol. 2015;47:1907–15.CrossRef Zahran MH, Hussein AM, Barakat N, Awadalla A, Khater S, Harraz A, et al. Sildenafil activates antioxidant and antiapoptotic genes and inhibits proinflammatory cytokine genes in a rat model of renal ischemia/reperfusion injury. Int Urol Nephrol. 2015;47:1907–15.CrossRef
3.
go back to reference Montagna G, Hofer CG, Torres AM. Impairment of cellular redox status and membrane protein activities in kidneys from rats with ischemic acute renal failure. Biochim Biophys Acta. 1998;1407:99–108.CrossRef Montagna G, Hofer CG, Torres AM. Impairment of cellular redox status and membrane protein activities in kidneys from rats with ischemic acute renal failure. Biochim Biophys Acta. 1998;1407:99–108.CrossRef
4.
go back to reference Hussein AA, Shokeir AA, Sarhan ME, El-Menabawy FR, Abd-Elmoneim HA, El-Nashar EM, et al. Effects of combined erythropoietin and epidermal growth factor on renal ischaemia/reperfusion injury: a randomized experimental controlled study. BJU Int. 2011 Jan;107(2):323–8.CrossRef Hussein AA, Shokeir AA, Sarhan ME, El-Menabawy FR, Abd-Elmoneim HA, El-Nashar EM, et al. Effects of combined erythropoietin and epidermal growth factor on renal ischaemia/reperfusion injury: a randomized experimental controlled study. BJU Int. 2011 Jan;107(2):323–8.CrossRef
5.
go back to reference Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol. 2006;17:1503–20.CrossRef Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol. 2006;17:1503–20.CrossRef
6.
go back to reference McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med. 1985;312:159–63.CrossRef McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med. 1985;312:159–63.CrossRef
7.
go back to reference Cho EJ, Yokozawa T, Rhee SH, Park KY. The role of Coptidis Rhizoma extract in a renal ischemia-reperfusion model. Phytomedicine. 2004;11:576–84.CrossRef Cho EJ, Yokozawa T, Rhee SH, Park KY. The role of Coptidis Rhizoma extract in a renal ischemia-reperfusion model. Phytomedicine. 2004;11:576–84.CrossRef
8.
go back to reference Hosseinzadeh H, Sadeghnia HR, Ziaee T, Danaee A. Protective effect of aqueous extract saffron (Crocus sativus L.) and crocin, its active constituent, on renal ischemia-reperfusion injury-induced oxidative damage in rats. J Pharm Sci. 2005;8:387–93. Hosseinzadeh H, Sadeghnia HR, Ziaee T, Danaee A. Protective effect of aqueous extract saffron (Crocus sativus L.) and crocin, its active constituent, on renal ischemia-reperfusion injury-induced oxidative damage in rats. J Pharm Sci. 2005;8:387–93.
9.
go back to reference Panth N, Paudel KR, Karki R. Phytochemical profile and biological activity of Juglans regia. J Integr Med. 2016;14:359–73.CrossRef Panth N, Paudel KR, Karki R. Phytochemical profile and biological activity of Juglans regia. J Integr Med. 2016;14:359–73.CrossRef
10.
go back to reference Erdemoglu N, Küpeli E, Yeşilada E. Anti-inflammatory and antinociceptive activity assessment of plants used as remedy in Turkish folk medicine. J Ethnopharmacol. 2003;89:123–9.CrossRef Erdemoglu N, Küpeli E, Yeşilada E. Anti-inflammatory and antinociceptive activity assessment of plants used as remedy in Turkish folk medicine. J Ethnopharmacol. 2003;89:123–9.CrossRef
11.
go back to reference Taha NA, Al-wadaan MA. Utility and importance of walnut, Juglans regia Linn: a review. Afr J Microbiol Res. 2011;5:5796–805. Taha NA, Al-wadaan MA. Utility and importance of walnut, Juglans regia Linn: a review. Afr J Microbiol Res. 2011;5:5796–805.
12.
go back to reference Jaradat NA, Zaid AN, Al-Ramahi R, Alqub MA, Hussein F, Hamdan Z, et al. Ethnopharmacological survey of medicinal plants practiced by traditional healers and herbalists for treatment of some urological diseases in the West Bank/Palestine. BMC Complement Altern Med. 2017;17:255.CrossRef Jaradat NA, Zaid AN, Al-Ramahi R, Alqub MA, Hussein F, Hamdan Z, et al. Ethnopharmacological survey of medicinal plants practiced by traditional healers and herbalists for treatment of some urological diseases in the West Bank/Palestine. BMC Complement Altern Med. 2017;17:255.CrossRef
13.
go back to reference Yao GD, Cheng ZY, Shang XY, Gao PY, Huang XX, Song SJ. Coumarins from the bark of Juglans mandshurica exhibited anti-hepatoma inducing apoptosis via activities. Asian Nat Prod Res J. 2017;19:1–9.CrossRef Yao GD, Cheng ZY, Shang XY, Gao PY, Huang XX, Song SJ. Coumarins from the bark of Juglans mandshurica exhibited anti-hepatoma inducing apoptosis via activities. Asian Nat Prod Res J. 2017;19:1–9.CrossRef
14.
go back to reference Joukar S, Ebrahimi S, Khazaei M, Bashiri A, Shakibi MR, Naderi V, et al. Co-administration of walnut (Juglans regia) prevents systemic hypertension induced by long-term use of dexamethasone: a promising strategy for steroid consumers. Pharm Biol. 2017;55:184–9.CrossRef Joukar S, Ebrahimi S, Khazaei M, Bashiri A, Shakibi MR, Naderi V, et al. Co-administration of walnut (Juglans regia) prevents systemic hypertension induced by long-term use of dexamethasone: a promising strategy for steroid consumers. Pharm Biol. 2017;55:184–9.CrossRef
15.
go back to reference Fuentealba C, Hernández I, Saa S, Toledo L, Burdiles P, Chirinos R, et al. Colour and in vitro quality attributes of walnuts from different growing conditions correlate with key precursors of primary and secondary metabolism. Food Chem. 2017 Oct;232:664–72.CrossRef Fuentealba C, Hernández I, Saa S, Toledo L, Burdiles P, Chirinos R, et al. Colour and in vitro quality attributes of walnuts from different growing conditions correlate with key precursors of primary and secondary metabolism. Food Chem. 2017 Oct;232:664–72.CrossRef
16.
go back to reference Calcabrini C, De Bellis R, Mancini U, Cucchiarini L, Stocchi V, Potenza L. Protective effect of Juglans regia L. walnut extract against oxidative DNA damage. Plant Foods Hum Nutr. 2017;72:192–7.CrossRef Calcabrini C, De Bellis R, Mancini U, Cucchiarini L, Stocchi V, Potenza L. Protective effect of Juglans regia L. walnut extract against oxidative DNA damage. Plant Foods Hum Nutr. 2017;72:192–7.CrossRef
17.
go back to reference Xu Z, Zhao Y, Ge Y, Peng J, Dong M, Yang G. Characterization of a vacuolar H+-ATPase G subunit gene from Juglans regia (JrVHAG1) involved in mannitol-induced osmotic stress tolerance. Plant Cell Rep. 2017;36:407–18.CrossRef Xu Z, Zhao Y, Ge Y, Peng J, Dong M, Yang G. Characterization of a vacuolar H+-ATPase G subunit gene from Juglans regia (JrVHAG1) involved in mannitol-induced osmotic stress tolerance. Plant Cell Rep. 2017;36:407–18.CrossRef
18.
go back to reference Park S, Kim N, Yoo G, Kim SN, Kwon HJ, Jung K, et al. Phenolics and neolignans isolated from the fruits of Juglans mandshurica Maxim and their effects on lipolysis in adipocytes. Phytochemistry. 2017;137:87–93.CrossRef Park S, Kim N, Yoo G, Kim SN, Kwon HJ, Jung K, et al. Phenolics and neolignans isolated from the fruits of Juglans mandshurica Maxim and their effects on lipolysis in adipocytes. Phytochemistry. 2017;137:87–93.CrossRef
19.
go back to reference Mollica A, Zengin G, Locatelli F, Stefanucci A, Macedonio G, Bellagamba G, Onaolapo O, Onaolapo A, Azeez F, Ayileka A, Novellino E. An assessment of the nutraceutical potential of Juglans regia L. leaf powder in diabetic rats. Food Chem Toxicol. 2017;107(PtB):554–64.CrossRef Mollica A, Zengin G, Locatelli F, Stefanucci A, Macedonio G, Bellagamba G, Onaolapo O, Onaolapo A, Azeez F, Ayileka A, Novellino E. An assessment of the nutraceutical potential of Juglans regia L. leaf powder in diabetic rats. Food Chem Toxicol. 2017;107(PtB):554–64.CrossRef
20.
go back to reference Singh V, Sherpa M. Neuronal differentiation of murine-like mesenchymal stem cell line: stimulation by Juglans regia L. oil. Appl Biochem Biotechnol. 2017;183:385–95.CrossRef Singh V, Sherpa M. Neuronal differentiation of murine-like mesenchymal stem cell line: stimulation by Juglans regia L. oil. Appl Biochem Biotechnol. 2017;183:385–95.CrossRef
21.
go back to reference Pavan V, Ribaudo G, Zorzan M, Redaelli M, Pezzani R, Mucignat-Caretta C, et al. Antiproliferative activity of Juglone derivatives on rat glioma. Nat Prod Res. 2017;31:632–8.CrossRef Pavan V, Ribaudo G, Zorzan M, Redaelli M, Pezzani R, Mucignat-Caretta C, et al. Antiproliferative activity of Juglone derivatives on rat glioma. Nat Prod Res. 2017;31:632–8.CrossRef
22.
go back to reference Salazar R, Pozos ME, Cordero P, Perez J, Salinas MC, Waksman N. Determination of the antioxidant activity of plants from Northeast Mexico. Pharm Biol. 2008;46:166–70.CrossRef Salazar R, Pozos ME, Cordero P, Perez J, Salinas MC, Waksman N. Determination of the antioxidant activity of plants from Northeast Mexico. Pharm Biol. 2008;46:166–70.CrossRef
23.
go back to reference Cruz-Vega DE, Verde-Star MJ, Salinas-González N, Rosales-Hernández B, Estrada-García I, Mendez-Aragón P, et al. Antimycobacterial activity of Juglans regia, Juglans mollis, Carya illinoensis and Bocconia frutescens. Phytother Res. 2008;22:557–9.CrossRef Cruz-Vega DE, Verde-Star MJ, Salinas-González N, Rosales-Hernández B, Estrada-García I, Mendez-Aragón P, et al. Antimycobacterial activity of Juglans regia, Juglans mollis, Carya illinoensis and Bocconia frutescens. Phytother Res. 2008;22:557–9.CrossRef
24.
go back to reference Muñoz-Espinosa LT-GLE, Rivas-Estilla AM, Trujillo-Murillo K, Salazar-Aranda R, De Torres NW, Cordero-Pérez P. Protective effect of four Mexican plants against CCl4-induced damage on the Huh7 human hepatoma cell line. Ann Hepatol. 2011;10:73–9.CrossRef Muñoz-Espinosa LT-GLE, Rivas-Estilla AM, Trujillo-Murillo K, Salazar-Aranda R, De Torres NW, Cordero-Pérez P. Protective effect of four Mexican plants against CCl4-induced damage on the Huh7 human hepatoma cell line. Ann Hepatol. 2011;10:73–9.CrossRef
25.
go back to reference Verde MJ, García S, Rivas C. Metodología científica para el estudio de plantas medicinales. Rivas-Morales, C., Oranday-Cardenas, MA and Verde- Star MJ (Eds.). Investigación en plantas de importancia médica. Barcelona España Omnia Science, 16: 26-34. DOI. 2016. https://doi.org/10.3926/oms.313.CrossRef Verde MJ, García S, Rivas C. Metodología científica para el estudio de plantas medicinales. Rivas-Morales, C., Oranday-Cardenas, MA and Verde- Star MJ (Eds.). Investigación en plantas de importancia médica. Barcelona España Omnia Science, 16: 26-34. DOI. 2016. https://​doi.​org/​10.​3926/​oms.​313.CrossRef
26.
go back to reference Zapata-Chavira H, Hernández-Guedea M, Jiménez-Pérez JC, Pérez-Rodríguez E, Muñoz-Espinosa L, Muñoz-Maldonado G, Cordero-Pérez P. Modulation of remote ischemic preconditioning by Proinflammatory cytokines in renal transplant recipients. J Investig Surg. 2017;30:1–9.CrossRef Zapata-Chavira H, Hernández-Guedea M, Jiménez-Pérez JC, Pérez-Rodríguez E, Muñoz-Espinosa L, Muñoz-Maldonado G, Cordero-Pérez P. Modulation of remote ischemic preconditioning by Proinflammatory cytokines in renal transplant recipients. J Investig Surg. 2017;30:1–9.CrossRef
27.
go back to reference Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;186:421–31.CrossRef Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;186:421–31.CrossRef
28.
go back to reference Kobuchi S, Shintani T, Sugiura T, Tanaka R, Suzuki R, Tsutsui H, et al. Renoprotective effects of gamma-aminobutyric acid on ischemia/reperfusion-induced renal injury in rats. Eur J Pharmacol. 2009;623(1–3):113–8.CrossRef Kobuchi S, Shintani T, Sugiura T, Tanaka R, Suzuki R, Tsutsui H, et al. Renoprotective effects of gamma-aminobutyric acid on ischemia/reperfusion-induced renal injury in rats. Eur J Pharmacol. 2009;623(1–3):113–8.CrossRef
29.
go back to reference Moosavi SM, Bayat G, Owji SM, Panjehshahin MR. Early renal post-ischaemic tissue damage and dysfunction with contribution of A1-adenosine receptor activation in rat. Nephrology (Carlton) 2009; 14(2):179:88.CrossRef Moosavi SM, Bayat G, Owji SM, Panjehshahin MR. Early renal post-ischaemic tissue damage and dysfunction with contribution of A1-adenosine receptor activation in rat. Nephrology (Carlton) 2009; 14(2):179:88.CrossRef
30.
go back to reference Mohamadi Yarijani Z, Najafi H, Shackebaeir D, Madani SH, Modarresi M, Jassemi SV. Amelioration of renal and hepatic function, oxidative stress, inflammation and histopathologic damages by Malva sylvestris extract in gentamicin induced renal toxicity. Biomed Pharmacother. 2019;112:108635.CrossRef Mohamadi Yarijani Z, Najafi H, Shackebaeir D, Madani SH, Modarresi M, Jassemi SV. Amelioration of renal and hepatic function, oxidative stress, inflammation and histopathologic damages by Malva sylvestris extract in gentamicin induced renal toxicity. Biomed Pharmacother. 2019;112:108635.CrossRef
31.
go back to reference Minutoli L, Puzzolo D, Rinaldi M, Irrera N, Marini H, Arcoraci V, et al. ROS-mediated NLRP3 inflammasome activation in brain, heart, kidney, and testis ischemia/reperfusion injury. Oxidative Med Cell Longev. 2016;2016:2183026.CrossRef Minutoli L, Puzzolo D, Rinaldi M, Irrera N, Marini H, Arcoraci V, et al. ROS-mediated NLRP3 inflammasome activation in brain, heart, kidney, and testis ischemia/reperfusion injury. Oxidative Med Cell Longev. 2016;2016:2183026.CrossRef
32.
go back to reference Limón-Pacheco J, Gonsebatt ME. The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutat Res. 2009;674:137–47.CrossRef Limón-Pacheco J, Gonsebatt ME. The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutat Res. 2009;674:137–47.CrossRef
33.
go back to reference Kasote DM, Katyare SS, Hegde MV, Bae H. Significance of antioxidant potential of plants and its relevance to therapeutic applications. Int J Biol Sci. 2015;11:982–91.CrossRef Kasote DM, Katyare SS, Hegde MV, Bae H. Significance of antioxidant potential of plants and its relevance to therapeutic applications. Int J Biol Sci. 2015;11:982–91.CrossRef
34.
go back to reference Fukuda T, Ito H, Yoshida T. Antioxidative polyphenols from walnuts (Juglans regia L.). Phytochemistry. 2003;63:795–801.CrossRef Fukuda T, Ito H, Yoshida T. Antioxidative polyphenols from walnuts (Juglans regia L.). Phytochemistry. 2003;63:795–801.CrossRef
35.
go back to reference Haque R, Bin-Hafeez B, Parvez S, Pandey S, Sayeed I, Ali M, et al. Aqueous extract of walnut (Juglans regia L.) protects mice against cyclophosphamide-induced biochemical toxicity. Hum Exp Toxicol. 2003;22:473–80.CrossRef Haque R, Bin-Hafeez B, Parvez S, Pandey S, Sayeed I, Ali M, et al. Aqueous extract of walnut (Juglans regia L.) protects mice against cyclophosphamide-induced biochemical toxicity. Hum Exp Toxicol. 2003;22:473–80.CrossRef
36.
go back to reference Zhao P, Qi C, Wang G, Dai X, Hou X. Enrichment and purification of total flavonoids from cortex Juglandis Mandshuricae extracts and their suppressive effect on carbon tetrachloride-induced hepatic injury in mice. J Chromatogr B Analyt Technol Biomed Life Sci. 2015;1007:8–17.CrossRef Zhao P, Qi C, Wang G, Dai X, Hou X. Enrichment and purification of total flavonoids from cortex Juglandis Mandshuricae extracts and their suppressive effect on carbon tetrachloride-induced hepatic injury in mice. J Chromatogr B Analyt Technol Biomed Life Sci. 2015;1007:8–17.CrossRef
37.
go back to reference Hodges DM, DeLong JM, Forney CF, Prange RK. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta. 1999;207:604–11.CrossRef Hodges DM, DeLong JM, Forney CF, Prange RK. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta. 1999;207:604–11.CrossRef
38.
go back to reference Wei H, Chen X, Zong X, Shu H, Gao D, Liu Q. Comparative transcriptome analysis of genes involved in anthocyanin biosynthesis in the red and yellow fruits of sweet cherry (Prunus avium L.). PLoS One. 2015;10(3):e0121164.CrossRef Wei H, Chen X, Zong X, Shu H, Gao D, Liu Q. Comparative transcriptome analysis of genes involved in anthocyanin biosynthesis in the red and yellow fruits of sweet cherry (Prunus avium L.). PLoS One. 2015;10(3):e0121164.CrossRef
39.
go back to reference Landi, M. Commentary to:“Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds” by Hodges et al.. Planta (1999) 207: 604–611. 2017 Planta; 245:1067–1067. Landi, M. Commentary to:“Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds” by Hodges et al.. Planta (1999) 207: 604–611. 2017 Planta; 245:1067–1067.
40.
go back to reference Hosseinzadeh H, Zarei H, Taghiabadi E. Antinociceptive, anti-inflammatory and acute toxicity effects of juglans regia L. leaves in mice. Iran Red Crescent Med J. 2011;13:27–33.PubMedPubMedCentral Hosseinzadeh H, Zarei H, Taghiabadi E. Antinociceptive, anti-inflammatory and acute toxicity effects of juglans regia L. leaves in mice. Iran Red Crescent Med J. 2011;13:27–33.PubMedPubMedCentral
41.
go back to reference Shen XD, Ke B, Zhai Y, Gao F, Anselmo D, Lassman CR, et al. Stat4 and Stat6 signaling in hepatic ischemia/reperfusion injury in mice: HO-1 dependence of Stat4 disruption-mediated cytoprotection. Hepatology. 2003;37:296–303.CrossRef Shen XD, Ke B, Zhai Y, Gao F, Anselmo D, Lassman CR, et al. Stat4 and Stat6 signaling in hepatic ischemia/reperfusion injury in mice: HO-1 dependence of Stat4 disruption-mediated cytoprotection. Hepatology. 2003;37:296–303.CrossRef
42.
go back to reference Xu H, Manivannan A, Jiang HR, Liversidge J, Sharp PF, Forrester JV, et al. Recruitment of IFN-γ-producing (Th1-like) cells into the inflamed retina in vivo is preferentially regulated by P-selectin glycoprotein ligand 1:P/E-selectin interactions. J Immunol. 2004;172:3215–24.CrossRef Xu H, Manivannan A, Jiang HR, Liversidge J, Sharp PF, Forrester JV, et al. Recruitment of IFN-γ-producing (Th1-like) cells into the inflamed retina in vivo is preferentially regulated by P-selectin glycoprotein ligand 1:P/E-selectin interactions. J Immunol. 2004;172:3215–24.CrossRef
43.
go back to reference Yokota N, Burne-Taney M, Racusen L, Rabb H. Contrasting roles for STAT4 and STAT6 signal transduction pathways in murine renal ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2003;285:F319–25.CrossRef Yokota N, Burne-Taney M, Racusen L, Rabb H. Contrasting roles for STAT4 and STAT6 signal transduction pathways in murine renal ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2003;285:F319–25.CrossRef
44.
go back to reference Saat TC, Susa D, Roest HP, Kok NF, van den Engel S, Ijzermans JN, et al. A comparison of inflammatory, cytoprotective and injury gene expression profiles in kidneys from brain death and cardiac death donors. Transplantation. 2014;98:15–21.CrossRef Saat TC, Susa D, Roest HP, Kok NF, van den Engel S, Ijzermans JN, et al. A comparison of inflammatory, cytoprotective and injury gene expression profiles in kidneys from brain death and cardiac death donors. Transplantation. 2014;98:15–21.CrossRef
45.
go back to reference Farmacopea Herbolaria de los Estados Unidos Mexicanos (FHEUM). 2nd ed. Distrito Federal, Mexico: Secretaria de Salud; 2013. Farmacopea Herbolaria de los Estados Unidos Mexicanos (FHEUM). 2nd ed. Distrito Federal, Mexico: Secretaria de Salud; 2013.
46.
go back to reference Nunez-Melendez E. Plantas Medicinales de Puerto Rico: Folklore y Fundamentos Científicos. San Juan, Puerto Rico: Editorial de la Universidad de Puerto Rico; 1982. Nunez-Melendez E. Plantas Medicinales de Puerto Rico: Folklore y Fundamentos Científicos. San Juan, Puerto Rico: Editorial de la Universidad de Puerto Rico; 1982.
47.
go back to reference Ruijun W, Shi W, Yijun X, Mengwuliji T, Lijuan Z, Yumin W. Antitumor effects and immune regulation activities of a purified polysaccharide extracted from Juglan regia. Int J Biol Macromol. 2015;72:771–5.CrossRef Ruijun W, Shi W, Yijun X, Mengwuliji T, Lijuan Z, Yumin W. Antitumor effects and immune regulation activities of a purified polysaccharide extracted from Juglan regia. Int J Biol Macromol. 2015;72:771–5.CrossRef
48.
go back to reference Alonso-Castro AJ, Juárez-Vázquez MC, Campos-Xolalpa N. Medicinal plants from Mexico, Central America, and the Caribbean used as Immunostimulants. Evid Based Complement Alternat Med. 2016;2016:4017676.CrossRef Alonso-Castro AJ, Juárez-Vázquez MC, Campos-Xolalpa N. Medicinal plants from Mexico, Central America, and the Caribbean used as Immunostimulants. Evid Based Complement Alternat Med. 2016;2016:4017676.CrossRef
49.
go back to reference Peirce A. The American pharmaceutical association practical guide to natural medicines. New York: Morrow; 1999. Peirce A. The American pharmaceutical association practical guide to natural medicines. New York: Morrow; 1999.
50.
go back to reference Qadan F, Thewaini AJ, Ali DA, Afifi R, Elkhawad A, Matalka KZ. The antimicrobial activities of Psidium guajava and Juglans regia leaf extracts to acne-developing organisms. Am J Chin Med. 2005;33(2):197–204.CrossRef Qadan F, Thewaini AJ, Ali DA, Afifi R, Elkhawad A, Matalka KZ. The antimicrobial activities of Psidium guajava and Juglans regia leaf extracts to acne-developing organisms. Am J Chin Med. 2005;33(2):197–204.CrossRef
51.
go back to reference Hajimahmoodi M, Shams-Ardakani M, Saniee P, Siavoshi F, Mehrabani M, Hosseinzadeh H, et al. In vitro antibacterial activity of some Iranian medicinal plant extracts against helicobacter pylori. Nat Prod Res. 2011;25:1059–66.CrossRef Hajimahmoodi M, Shams-Ardakani M, Saniee P, Siavoshi F, Mehrabani M, Hosseinzadeh H, et al. In vitro antibacterial activity of some Iranian medicinal plant extracts against helicobacter pylori. Nat Prod Res. 2011;25:1059–66.CrossRef
52.
go back to reference Hosseini S, Huseini HF, Larijani B, Mohammad K, Najmizadeh A, Nourijelyani K, et al. The hypoglycemic effect of Juglans regia leaves aqueous extract in diabetic patients: a first human trial. Daru. 2014;22:19–23.CrossRef Hosseini S, Huseini HF, Larijani B, Mohammad K, Najmizadeh A, Nourijelyani K, et al. The hypoglycemic effect of Juglans regia leaves aqueous extract in diabetic patients: a first human trial. Daru. 2014;22:19–23.CrossRef
53.
go back to reference Gushiken LF, Beserra FP, Rozza AL, Bérgamo PL, Bérgamo DA, Pellizzon CH. Chemical and biological aspects of extracts from medicinal plants with antidiabetic effects. Rev Diabet Stud. 2016;13:96–112.CrossRef Gushiken LF, Beserra FP, Rozza AL, Bérgamo PL, Bérgamo DA, Pellizzon CH. Chemical and biological aspects of extracts from medicinal plants with antidiabetic effects. Rev Diabet Stud. 2016;13:96–112.CrossRef
54.
go back to reference Orlando RA, Gonzales AM, Hunsaker LA, Franco CR, Royer RE, Vander Jagt DL, et al. Inhibition of nuclear factor kappaB activation and cyclooxygenase-2 expression by aqueous extracts of Hispanic medicinal herbs. J Med Food. 2010;13:888–95.CrossRef Orlando RA, Gonzales AM, Hunsaker LA, Franco CR, Royer RE, Vander Jagt DL, et al. Inhibition of nuclear factor kappaB activation and cyclooxygenase-2 expression by aqueous extracts of Hispanic medicinal herbs. J Med Food. 2010;13:888–95.CrossRef
55.
go back to reference Blumenthal M, Goldberg A, Brinckann J. Herbal medicine: expanded commission E monographs. USA: Newton American Botanical Council; 2000. p. 401–3. Blumenthal M, Goldberg A, Brinckann J. Herbal medicine: expanded commission E monographs. USA: Newton American Botanical Council; 2000. p. 401–3.
56.
go back to reference Jiménez-Gómez Y, López-Miranda J, Blanco-Colio LM, Marín C, Pérez-Martínez P, Ruano J, et al. Olive oil and walnut breakfasts reduce the postprandial inflammatory response in mononuclear cells compared with a butter breakfast in healthy men. Atherosclerosis. 2009;204:e70–6.CrossRef Jiménez-Gómez Y, López-Miranda J, Blanco-Colio LM, Marín C, Pérez-Martínez P, Ruano J, et al. Olive oil and walnut breakfasts reduce the postprandial inflammatory response in mononuclear cells compared with a butter breakfast in healthy men. Atherosclerosis. 2009;204:e70–6.CrossRef
Metadata
Title
Anti-inflammatory and nephroprotective activity of Juglans mollis against renal ischemia–reperfusion damage in a Wistar rat model
Authors
Jonathan Perez-Meseguer
Liliana Torres-González
Jorge Aurelio Gutiérrez-González
Gabriela Alarcón-Galván
Homero Zapata-Chavira
Noemi Waksman-de Torres
Diana Patricia Moreno-Peña
Linda Elsa Muñoz-Espinosa
Paula Cordero-Pérez
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Cytokines
Published in
BMC Complementary Medicine and Therapies / Issue 1/2019
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-019-2604-7

Other articles of this Issue 1/2019

BMC Complementary Medicine and Therapies 1/2019 Go to the issue