Effect of Γ-aminobutyric acid on kidney injury induced by renal ischemia-reperfusion in male and female rats: Gender-related difference
Marzieh Vafapour1, Mehdi Nematbakhsh2, Ramesh Monajemi3, Safoora Mazaheri4, Ardeshir Talebi5, Nahid Talebi1, Soheyla Shirdavani4
1 Water and Electrolytes Research Center, Isfahan University of Medical Sciences; Department of Biology, Falavarjan Branch, Islamic Azad University, Isfahan, Iran
2 Water and Electrolytes Research Center; Department of Physiology, Isfahan University of Medical Sciences; Isfahan-MN Institute of Basic and Applied Sciences Research, Isfahan, Iran
3 Department of Biology, Falavarjan Branch, Islamic Azad University, Isfahan, Iran
4 Water and Electrolytes Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
5 Water and Electrolytes Research Center; Department of Clinical Pathology, Isfahan University of Medical Sciences, Isfahan, Iran
|Date of Submission||10-Nov-2014|
|Date of Acceptance||17-Jan-2015|
|Date of Web Publication||27-Jul-2015|
Department of Physiology, Water and Electrolytes Research Center, Kidney Diseases Research Center, Isfahan University of Medical Sciences, Isfahan
Source of Support: None, Conflict of Interest: None
Background: The most important cause of kidney injury is renal ischemia/reperfusion injury (IRI), which is gender-related. This study was designed to investigate the protective role of Γ-aminobutyric acid (GABA (against IRI in male and female rats.
Materials and Methods: Thirty-six female and male wistar rats were assigned to six experimental groups. The IRI was induced by clamping renal vessels for 45 min then was performed reperfusion for 24 h. The group sex posed to IRI were pretreated with GABA and were compared with the control groups.
Results: Serum levels of creatinine and blood urea nitrogen, kidney weight, and kidney tissue damage score increased in the IRI alone groups, (P < 0.05), while GABA decreased these parameters in female significantly (P < 0.05), but not in male rats. Uterus weight decreased significantly in female rats treated with GABA. Testis weight did not alter in male rats. Serum level of nitrite and kidney level of malondialdehyde (MDA) had no significant change in both female and male rats. Kidney level of nitrite increased significantly in female rats experienced IRI and serum level of MDA increased significantly in males that were exposed to IRI (P < 0.05).
Conclusion: GABA could ameliorate kidney injury induced by renal IRI in a gender dependent manner.
Keywords: Γ-aminobutyric acid, gender, rat, renal ischemia-reperfusion
|How to cite this article:|
Vafapour M, Nematbakhsh M, Monajemi R, Mazaheri S, Talebi A, Talebi N, Shirdavani S. Effect of Γ-aminobutyric acid on kidney injury induced by renal ischemia-reperfusion in male and female rats: Gender-related difference. Adv Biomed Res 2015;4:158
|How to cite this URL:|
Vafapour M, Nematbakhsh M, Monajemi R, Mazaheri S, Talebi A, Talebi N, Shirdavani S. Effect of Γ-aminobutyric acid on kidney injury induced by renal ischemia-reperfusion in male and female rats: Gender-related difference. Adv Biomed Res [serial online] 2015 [cited 2023 Jun 6];4:158. Available from: https://www.advbiores.net/text.asp?2015/4/1/158/161585
| Introduction|| |
Acute kidney injury (AKI) is a clinical syndrome with high morbidity and mortality. , Kidney ischemia/reperfusion injury (IRI) is one of the most common cause of AKI,  by which complex events related to kidney damage and cell death occur. ,
Several causal factors contribute to the pathogenesis of this renal damage. , However, the mechanisms underlying IRI are not fully understood,  but sex hormones have been reported to play an important role in kidney injuries induced by inflammatory processes.
In this regard, the incidence of acute renal failure in surgical patients is significantly higher in men than women.  Males exhibit rapid progression of nondiabetic kidney diseases.  In this regard, male sex hormone, testosterone, increases the susceptibility to ischemic renal injury when compared with estrogen depletion or absence of male sex hormones, which induce a reduction in the levels of markers of postischemic oxidative stress in the kidney. ,,
Γ-aminobutyric acid (GABA) is a major neurotransmitter that is largely found in the central nervous system. ,, The peripheral GABAergic system is one of the major inhibitory neurotransmitters in the brain. , The peripheral organs including the kidneys are known to possess various subtypes of GABAA receptors.  Moreover, it is reported that GABA has neuroprotective effects in the brain ischemic injury, which is one of the serious complications of atherosclerosis. 
Although, some reports indicated that GABA provides a powerful protective mechanism against ischemic injury in a variety of organ systems including kidneys,  and on conditions including acute renal failure,  endocrine disorders,  hypertension,  and IRIs;  still its effect on IRI between males and females has not been compared.
Studies have shown that GABA has renoprotective effects against glycerol-induced AKI and administration of GABA ameliorates renal dysfunction, and a longer administration period of GABA increases its protective effect.  The results also indicate that GABA may play a protective role against chronic renal failure through improvement of the serum lipid profile.  Therefore, we hypothesized that GABA may affect renal ischemia in a gender-related manner.
| Materials and methods|| |
Eighteen adult female (weight: 191 ± 4 g) and 18 adult male (weight: 216 ± 5 g) wistar rats were used in this study. The rats were housed at a temperature of 23-25°C with a 12-h light/12-h dark cycle and the experimental procedures were in advance approved by the Isfahan University of Medical Sciences Ethics Committee.
Γ-aminobutyric acid (code A2129-10G) was provided from Sigma (St. Louis, MO, USA).
The animals were randomly divided into six experimental groups as follows:
- Group 1 (n = 7, named MG), male rats exposed to surgery without IRI and 15 min before ischemia received GABA (50 μmol/kg; intravenously)
- Group 2 (n = 5, named MI), male rats treated as Group 1 except saline instead of GABA
- Group 3 (n = 6, named MIG), male rats exposed to IRI and treated with GABA 15 min before the surgery
- Groups 4 (n = 7), 5 (n = 6), and 6 (n = 6) named as FG, FI, and FIG, female rats treated as Groups 1-3, respectively.
To induce the IRI model, the animals in Groups 2, 3, 5, and 6 were anesthetized by chlorohydrate (450 mg/kg). Two small incisions were made on the skin to expose kidneys and vessels. Both the renal artery and vein were clamped simultaneously in each kidney for 45 min. then, the clamps were removed to initiate reperfusion. The skin was sutured, and the animals were returned back to the cages under direct observation.
After 24 h, the animals were anesthetized again, blood samples were taken via heart puncture and the animals were sacrificed. The samples were centrifuged to obtain serum sample for measuring the serum level of blood urea nitrogen (BUN), creatinine (Cr), nitrite, and malondialdehyde (MDA). The kidneys were also removed. The right kidney was homogenized and centrifuged at 15,000 g for 2 min, and the supernatant was used for MDA and nitrite measurements. The left kidney was fixed in formalin for histopathological investigation.
Serum levels of Cr and BUN were measured using quantitative kits (Pars Azmoon, Iran). Serum and kidney levels of nitrite (stable metabolite of nitric oxide [NO]) were measured using a colorimetric kit (Promega Corporation, USA) that involved the Griess reaction. Assessment of MDA levels in the serum and kidney was performed by the manual method. ,
The removed kidneys were fixed in 10% formalin solution, embedded in paraffin for histopathological staining. Hematoxylin and eosin staining was applied to examine the tubular injury. The intensity of tubular lesions was scored by a pathologist who was blind to the study protocol. The score was considered from 1 to 4, while score zero was assigned to normal tissue.
Statistical data were presented as mean ± standard error of the mean. The quantitative data between the groups were compared by the one-way analysis of variance, followed by the least significant difference. The Mann-Whitney or Kruskal-Wallis tests were used to compare the pathological damage score among groups. P < 0.05 were considered statistically significant.
| Results|| |
Effect of ischemia/reperfusion injury on serum levels of blood urea nitrogen and creatinine
The serum levels of Cr and BUN increased significantly in male and female rats exposed to IRI (P < 0.05). Administration of GABA ameliorated the increased levels of BUN and Cr induced by IRI in female (P < 0.05), but not in male rats [Figure 1].
|Figure 1: Serum levels of blood urea nitrogen (BUN) and creatinine (Cr); kidney weight (KW); body weight change (BW), kidney tissue damage score (KTDS), uterus weight (UW) or testis weight (TW) in female and male rats, respectively. The *, #, and @ indicate significant difference from the MG, FI, and FG groups, respectively|
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Effect of ischemia/reperfusion injury on kidney tissue damage score
Ischemia/reperfusion injury increased kidney tissue damage score (KTDS) significantly in male and female rats (P < 0.05) [Figure 2]; however, GABA could attenuate KTDS in female rats underwent IRI.
|Figure 2: Images (magnification × 400) of kidney tissue. MG = Male + Ã-aminobutyric acid (GABA), MI = Male + Ischemia, MIG = Male + Ischemia + GABA, FG = Female + GABA, FI = Female + Ischemia, FIG = Female + Ischemia + GABA. Higher damage scores were observed in the FI and MI groups|
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Effect of ischemia/reperfusion injury on bodyweight and kidney weight changes
Total kidney weight/100 g body weight (KW) increased significantly in male groups exposed to IRI (P < 0.05) and decreased significantly in the female groups exposed to IRI pretreated with GABA (P < 0.05).
In male rats, BW in the group exposed to IRI decreased significantly compared to other groups (P < 0.05). However, this was not the case in female rats [Figure 1].
Effect of ischemia/reperfusion injury on uterus weight and testis weight
The uterus weight in rats exposed to IRI and treated with GABA decreased significantly (P < 0.05) [Figure 1], while no significant differences in testis weight were detected between the groups.
Effect of ischemia/reperfusion injury on kidney and serum nitrite and malondialdehyde levels
Kidney nitrite level in female rats exposed to IRI increased significantly when compared with the FG group (P < 0.05) [Table 1], while MDA level in the MG group was greater than that in the MI group (P < 0.05) [Table 1].
|Table 1: Level of nitrite and MDA in serum and kidney in all experimental groups|
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| Discussion|| |
Our objective was to determine the effects of GABA on IRI in male and female rats. The findings indicate that GABA has protective effects on renal IRI, although it is more efficient in female rats. Different reports have described that renal IRI affects serum biochemical factors such as Cr, BUN, nitrite, and MDA levels; as well as weight and histology of the kidney. ,,,,, We found that the functional markers of kidney, BUN and Cr, increased significantly after renal IR in the female and male rats while GABA reduced these parameters in male and female rats with renal IRI. The ischemia-reperfusion causes increase in some serum parameters and markers of oxidative stress and histopathological changes in renal tissues. , It appears that reduction of BUN and Cr levels in the current study and other studies is probably associated with alteration of glomerular filtration rate, , since obstruction and destruction of tubules together with a renal artery stenosis lead to changes in glomerular filtration rate. 
Body weight loss and KTDS increase were observed after renal IRI. , BW loss in rodents after kidney IRI is most likely due to the inability of the kidney to retain salt and water, and this effect causes polyuria. 
Γ-aminobutyric acid did not significantly ameliorate kidney damage, but its improvement in female rats was clear. Renal sympathetic nerve activity plays an important role in IRI.  GABA inhibits the development of ischemia by suppressing sympathetic nerve activity in excessive norepinephrine secretion from sympathetic nerve endings of the kidney.  The recovery may be related to the inhibitory effect of GABA on sympathetic nerve activity and its suppression.  The sex difference in ischemic injury of likely may be related to sex hormones  and pretreatment with the antioxidants abolished sex differences.  In addition, the sex hormone status may be important for initiation of the inflammatory response following renal IRI. 
Malondialdehyde, as the final product of lipid peroxidation, is one of the biomarkers of oxidative stress.  Several studies have reported that IRI increases the MDA level. , In the present study, the serum and tissue levels of MDA increased insignificantly after renal IR, but GABA did not decrease the MDA levels except the serum MDA level in female rats. This may be related to the female sex hormones because estrogen has antioxidant properties and reduction of free radicals will decrease the MDA level.  Although administration of GABA improved renal dysfunction through regulation of blood pressure and improved oxidative stress induced by nephrectomy, this effect is probably due to the increased activity of superoxide dismutase or other antioxidant enzymes. , According to the scavenging effects of GABA on protecting against renal failure progression  and it the antioxidant properties,  possibly administration of GABA with estrogen in the female have a positive effect on sex difference in renal ischemia.
The serum and tissue levels of nitrite were increased by IRI. GABA did not decrease the nitrite levels in the male rats. NO is produced by endothelial NO synthase and inducible NO synthase increased after renal IRI in response to the oxidative stress.  The vasodilator action of NO on vascular smooth muscle cells is well known.  The major new finding of this study was that GABA improved postischemic structural recovery in kidney in both female and male rats, but this recovery was more significant in females. Sex difference in the IRIs has been studied in diverse organs and in most organs such as brain, heart, and gastrointestinal system, females are more resistant to the injuries.  Individual published reports have presented conflicting result.  Gasbarrini et al. reported that the liver is more vulnerable to IRI in females.  Mόller et al. revealed that IRI in the kidney is less severe in female than male rats.  It has been shown that progression of renal diseases in males is much rapider than that in females. Furthermore, in chronic renal diseases, the outcome is worse in males. ,,, This might be due to the differences in kidney structure, glomerular hemodynamic responses to stress, and the direct cellular effects of sex hormones. , The difference is due to the activity of the sympathetic nervous system, leading to increase in norepinephrine level after reperfusion and is significantly higher in male rats than in female rats.  This decline may be related to the estrogen hormone system. 
In the present study, GABA administration ameliorated renal functional loss in the treatment group. According to the results obtained, there was no significant difference between male and female groups in the kidney function tests. However, we found that IRIs were less in males and also the protective effects of GABA were more pronounced in females.
| Conclusion|| |
Although GABA improved IRI in male and female rats, its improvement was more pronounced in females.
| Acknowledgments|| |
This research was supported by Isfahan University of Medical Sciences.
| References|| |
Sharfuddin AA, Molitoris BA. Pathophysiology of ischemic acute kidney injury. Nat Rev Nephrol 2011;7:189-200.
Tanaka R, Takayama J, Takaoka M, Sugino Y, Ohkita M, Matsumura Y. Oligomycin, an F1Fo-ATPase inhibitor, protects against ischemic acute kidney injury in male but not in female rats. J Pharmacol Sci 2013;123:227-34.
del Moral RM, Gómez-Morales M, Hernández-Cortés P, Aguilar D, Caballero T, Aneiros-Fernández J, et al.
PARP inhibition attenuates histopathological lesion in ischemia/reperfusion renal mouse model after cold prolonged ischemia. ScientificWorldJournal 2013;2013:486574.
Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol 2006;17:1503-20.
Hutchens MP, Dunlap J, Hurn PD, Jarnberg PO. Renal ischemia: Does sex matter? Anesth Analg 2008;107:239-49.
Lien YH, Lai LW, Silva AL. Pathogenesis of renal ischemia/reperfusion injury: Lessons from knockout mice. Life Sci 2003;74:543-52.
Edelstein CL, Ling H, Schrier RW. The nature of renal cell injury. Kidney Int 1997;51:1341-51.
Rodríguez F, Nieto-Cerón S, Fenoy FJ, López B, Hernández I, Martinez RR, et al.
Sex differences in nitrosative stress during renal ischemia. Am J Physiol Regul Integr Comp Physiol 2010;299:R1387-95.
Neugarten J, Acharya A, Silbiger SR. Effect of gender on the progression of nondiabetic renal disease: A meta-analysis. J Am Soc Nephrol 2000;11:319-29.
Soljancic A, Ruiz AL, Chandrashekar K, Maranon R, Liu R, Reckelhoff JF, et al.
Protective role of testosterone in ischemia-reperfusion-induced acute kidney injury. Am J Physiol Regul Integr Comp Physiol 2013;304:R951-8.
Kim J, Kil IS, Seok YM, Yang ES, Kim DK, Lim DG, et al.
Orchiectomy attenuates post-ischemic oxidative stress and ischemia/reperfusion injury in mice. A role for manganese superoxide dismutase. J Biol Chem 2006;281:20349-56.
Park KM, Kim JI, Ahn Y, Bonventre AJ, Bonventre JV. Testosterone is responsible for enhanced susceptibility of males to ischemic renal injury. J Biol Chem 2004;279:52282-92.
Li DP, Pan HL. Role of gamma-aminobutyric acid (GABA) A and GABAB receptors in paraventricular nucleus in control of sympathetic vasomotor tone in hypertension. J Pharmacol Exp Ther 2007;320:615-26.
Kobuchi S, Tanaka R, Shintani T, Suzuki R, Tsutsui H, Ohkita M, et al.
Mechanisms underlying the renoprotective effect of GABA against ischemia/reperfusion-induced renal injury in rats. J Pharmacol Exp Ther 2011;338:767-74.
Gajcy K, Lochynski S, Librowski T. A role of GABA analogues in the treatment of neurological diseases. Curr Med Chem 2010;17:2338-47.
Gladkevich A, Korf J, Hakobyan VP, Melkonyan KV. The peripheral GABAergic system as a target in endocrine disorders. Auton Neurosci 2006;124:1-8.
Watanabe M, Maemura K, Kanbara K, Tamayama T, Hayasaki H. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 2002;213:1-47.
Párducz A, Dobó E, Wolff JR, Petrusz P, Erdö SL. GABA-immunoreactive structures in rat kidney. J Histochem Cytochem 1992;40:675-80.
Yang Y, Luo H, Cheng LX, Liu K. Inhibitory role for GABA in atherosclerosis. Med Hypotheses 2013;81:803-4.
Kim HY, Yokozawa T, Nakagawa T, Sasaki S. Protective effect of gamma-aminobutyric acid against glycerol-induced acute renal failure in rats. Food Chem Toxicol 2004;42:2009-14.
Brar R, Singh JP, Kaur T, Arora S, Singh AP. Role of GABAergic activity of sodium valproate against ischemia-reperfusion-induced acute kidney injury in rats. Naunyn Schmiedebergs Arch Pharmacol 2014;387:143-51.
Sasaki S, Yokozawa T, Cho EJ, Oowada S, Kim M. Protective role of gamma-aminobutyric acid against chronic renal failure in rats. J Pharm Pharmacol 2006;58:1515-25.
Azarkish F, Nematbakhsh M, Fazilati M, Talebi A, Pilehvarian AA, Pezeshki Z, et al.
N-acetylcysteine prevents kidney and lung disturbances in renal ischemia/reperfusion Injury in rat. Int J Prev Med 2013;4:1139-46.
Moeini M, Nematbakhsh M, Fazilati M, Talebi A, Pilehvarian AA, Azarkish F, et al.
Protective role of recombinant human erythropoietin in kidney and lung injury following renal bilateral ischemia-reperfusion in rat model. Int J Prev Med 2013;4:648-55.
Nitescu N, Ricksten SE, Marcussen N, Haraldsson B, Nilsson U, Basu S, et al.
N-acetylcysteine attenuates kidney injury in rats subjected to renal ischaemia-reperfusion. Nephrol Dial Transplant 2006;21:1240-7.
Hammad FT, Al-Salam S, Lubbad L. Curcumin provides incomplete protection of the kidney in ischemia reperfusion injury. Physiol Res 2012;61:503-11.
Hassoun HT, Grigoryev DN, Lie ML, Liu M, Cheadle C, Tuder RM, et al.
Ischemic acute kidney injury induces a distant organ functional and genomic response distinguishable from bilateral nephrectomy. Am J Physiol Renal Physiol 2007;293:F30-40.
Choi DE, Jeong JY, Lim BJ, Chung S, Chang YK, Lee SJ, et al.
Pretreatment of sildenafil attenuates ischemia-reperfusion renal injury in rats. Am J Physiol Renal Physiol 2009;297:F362-70.
Nath KA, Norby SM. Reactive oxygen species and acute renal failure. Am J Med 2000;109:665-78.
Pflueger A, Abramowitz D, Calvin AD. Role of oxidative stress in contrast-induced acute kidney injury in diabetes mellitus. Med Sci Monit 2009;15:RA125-36.
Lameire N, Van Biesen W, Hoste E, Vanholder R. The prevention of acute kidney injury an in-depth narrative review. Part 2: Drugs in the prevention of acute kidney injury. NDT Plus 2009;2:1-10.
Klahr S, Morrissey J. Obstructive nephropathy and renal fibrosis. Am J Physiol Renal Physiol 2002;283:F861-75.
Rabb H, Wang Z, Nemoto T, Hotchkiss J, Yokota N, Soleimani M. Acute renal failure leads to dysregulation of lung salt and water channels. Kidney Int 2003;63:600-6.
Ohno T, Kato S, Wakatsuki M, Noda SE, Murakami C, Nakamura M, et al.
Incidence and temporal pattern of anorexia, diarrhea, weight loss, and leukopenia in patients with cervical cancer treated with concurrent radiation therapy and weekly cisplatin: Comparison with radiation therapy alone. Gynecol Oncol 2006;103:94-9.
Sasaki S, Tohda C, Kim M, Yokozawa T. Gamma-aminobutyric acid specifically inhibits progression of tubular fibrosis and atrophy in nephrectomized rats. Biol Pharm Bull 2007;30:687-91.
Kang KP, Lee JE, Lee AS, Jung YJ, Kim D, Lee S, et al.
Effect of gender differences on the regulation of renal ischemia-reperfusion-induced inflammation in mice. Mol Med Rep 2014;9:2061-8.
Nielsen F, Mikkelsen BB, Nielsen JB, Andersen HR, Grandjean P. Plasma malondialdehyde as biomarker for oxidative stress: Reference interval and effects of life-style factors. Clin Chem 1997;43:1209-14.
Singh D, Chander V, Chopra K. Protective effect of catechin on ischemia-reperfusion-induced renal injury in rats. Pharmacol Rep 2005;57:70-6.
Paoletti F, Mocali A. Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Methods Enzymol 1990;186:209-20.
Deng Y, Xu L, Zeng X, Li Z, Qin B, He N. New perspective of GABA as an inhibitor of formation of advanced lipoxidation end-products: It's interaction with malondiadehyde. J Biomed Nanotechnol 2010;6:318-24.
Burger D, Lei M, Geoghegan-Morphet N, Lu X, Xenocostas A, Feng Q. Erythropoietin protects cardiomyocytes from apoptosis via up-regulation of endothelial nitric oxide synthase. Cardiovasc Res 2006;72:51-9.
Hale SL, Birnbaum Y, Kloner RA. beta-Estradiol, but not alpha-estradiol, reduced myocardial necrosis in rabbits after ischemia and reperfusion. Am Heart J 1996;132:258-62.
Silbiger SR, Neugarten J. The impact of gender on the progression of chronic renal disease. Am J Kidney Dis 1995;25:515-33.
Gasbarrini A, Addolorato G, Di Campli C, Simoncini M, Montemagno S, Castagneto M, et al.
Gender affects reperfusion injury in rat liver. Dig Dis Sci 2001;46:1305-12.
Müller V, Losonczy G, Heemann U, Vannay A, Fekete A, Reusz G, et al.
Sexual dimorphism in renal ischemia-reperfusion injury in rats: Possible role of endothelin. Kidney Int 2002;62:1364-71.
Silbiger SR, Neugarten J. The role of gender in the progression of renal disease. Adv Ren Replace Ther 2003;10:3-14.
Tanaka R, Tsutsui H, Ohkita M, Takaoka M, Yukimura T, Matsumura Y. Sex differences in ischemia/reperfusion-induced acute kidney injury are dependent on the renal sympathetic nervous system. Eur J Pharmacol 2013;714:397-404.
Torras J, Herrero-Fresneda I, Lloberas N, Riera M, Ma Cruzado J, Ma Grinyó J. Promising effects of ischemic preconditioning in renal transplantation. Kidney Int 2002;61:2218-27.
[Figure 1], [Figure 2]
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