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Anti-inflammatory and anti-apoptotic effects of naringin on bacterial endotoxin-induced small intestine damage in rats

Year 2022, Volume: 47 Issue: 3, 1137 - 1146, 30.09.2022

Ali Tuğrul Akin Mohamed Lemine El Bechir Emin Kaymak Tayfun Ceylan Meryem Sayan Necla Değer Derya Karabulut Ayşe Toluk

https://doi.org/10.17826/cumj.1124641
Cited By: 1

Abstract

Purpose: The aim of this study is to investigate the anti-inflammatory and anti-apoptotic effects of naringin (NRG), which has many biological properties, on bacterial endotoxin-induced small intestine damage in rats.
Materials and Methods: For this purpose, 40 female Wistar albino rats were divided into 4 groups as Control (group given no treatment), LPS (group given 10 mg/kg/i.p lipopolysaccharide), NRG (group given 100 mg/kg/i.p naringin for 14 days) and LPS + NRG (group given 100 mg/kg/i.p naringin for 14 days before 10 mg/kg/i.p lipopolysaccharide injection). After experimental procedure, small intestine tissues of animals were extracted and prepared according to tissue processing protocol. Hematoxylin and Eosin staining were performed to evaluate the histopathological changes and histological damage scoring was applied to compare experimental groups in terms of histopathological changes. Moreover, TNF- and Caspase-3 expression levels were detected by immunohistochemical staining and the density of immunoreactivity were scored to determine the difference in the expression levels of TNF- and Caspase-3 expressions among groups.
Results: Epithelial and Brunner’s gland damage, mononuclear cell infiltration, hemorrhage, and TNF- and Caspase-3 expressions significantly increased in the LPS group. However, NRG administrations exerted a strong protective effect on the small intestine tissues in terms of these parameters in LPS+NRG group.
Conclusion: This study demonstrated that 100 mg/kg NRG injection can be regarded as a protective agent against negative effects of endotoxin-induced infection on the intestinal mucosa and that it should not be disregarded in further clinical trials.

Keywords

Endotoxin Small intestine damage lipopolysaccharide naringin

Thanks

Erciyes University

References

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  • Bektas, A., S.H. Schurman, R. Sen, and L. Ferrucci, Aging, inflammation and the environment. Exp Gerontol, 2018. 105: p. 10-18. doi: 10.1016/j.exger.2017.12.015
  • Ciesielska, A., M. Matyjek, and K. Kwiatkowska, TLR4 and CD14 trafficking and its influence on LPS-induced pro-inflammatory signaling. Cell Mol Life Sci, 2021. 78(4): p. 1233-1261. doi: 10.1007/s00018-020-03656-y
  • Fritsche, K.L., The science of fatty acids and inflammation. Adv Nutr, 2015. 6(3): p. 293s-301s. doi: 10.3945/an.114.006940
  • Płóciennikowska, A., A. Hromada-Judycka, K. Borzęcka, and K. Kwiatkowska, Co-operation of TLR4 and raft proteins in LPS-induced pro-inflammatory signaling. Cell Mol Life Sci, 2015. 72(3): p. 557-581. doi: 10.1007/s00018-014-1762-5
  • Kuzmich, N.N., K.V. Sivak, V.N. Chubarev, Y.B. Porozov, T.N. Savateeva-Lyubimova, and F. Peri, TLR4 Signaling Pathway Modulators as Potential Therapeutics in Inflammation and Sepsis. Vaccines (Basel), 2017. 5(4). doi: 10.3390/vaccines5040034
  • Anderson, S.T., S. Commins, P.N. Moynagh, and A.N. Coogan, Lipopolysaccharide-induced sepsis induces long-lasting affective changes in the mouse. Brain Behav Immun, 2015. 43: p. 98-109. doi: 10.1016/j.bbi.2014.07.007
  • Bae, J.Y., D.S. Lee, Y.K. Cho, J.Y. Lee, J.H. Park, and S.H. Lee, Daphne jejudoensis Attenuates LPS-Induced Inflammation by Inhibiting TNF-α, IL-1β, IL-6, iNOS, and COX-2 Expression in Periodontal Ligament Cells. Pharmaceuticals (Basel), 2022. 15(4). doi: 10.3390/ph15040387
  • Kuypers, F.A., Hyperinflammation, apoptosis, and organ damage. Experimental Biology and Medicine. 0(0): p. 15353702221090454. doi: 10.1177/15353702221090454
  • AKIN, A.T., E. KAYMAK, E. ÖZTÜRK, T. CEYLAN, B. YALÇIN, K.E. BAŞARAN, et al., Mitigative effects of chloroquine treatment against hypoxia-induced intestinal injury: A histological and immunohistochemical study. Turk Hij Den Biyol Derg, 2022. 79(1): p. 59-70. doi: 10.5505/TurkHijyen.2022.78476
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  • Khodayar, M.J., H. Kalantari, M. Mahdavinia, L. Khorsandi, S. Alboghobeish, A. Samimi, et al., Protective effect of naringin against BPA-induced cardiotoxicity through prevention of oxidative stress in male Wistar rats. Drug and Chemical Toxicology, 2020. 43(1): p. 85-95. doi: 10.1080/01480545.2018.1504958
  • Caglayan, C., Y. Temel, F.M. Kandemir, S. Yildirim, and S. Kucukler, Naringin protects against cyclophosphamide-induced hepatotoxicity and nephrotoxicity through modulation of oxidative stress, inflammation, apoptosis, autophagy, and DNA damage. Environmental Science and Pollution Research, 2018. 25(21): p. 20968-20984. doi: 10.1007/s11356-018-2242-5
  • Cerkezkayabekir, A., F. Sanal, E. Bakar, E. Ulucam, and M. Inan, Naringin protects viscera from ischemia/reperfusion injury by regulating the nitric oxide level in a rat model. Biotechnic & Histochemistry, 2017. 92(4): p. 252-263. doi: 10.1080/10520295.2017.1305499
  • Yilmaz, D., O. Teksoy, R. Bilaloglu, and N. Çinkilic, Anti-genotoxic effect of naringin against bleomycin-induced genomic damage in human lymphocytes in vitro. Drug Chem Toxicol, 2016. 39(2): p. 119-23. doi: 10.3109/01480545.2015.1039647
  • Kim, H.J., H.I. Yong, S. Park, K. Kim, T.H. Kim, W. Choe, et al., Effect of atmospheric pressure dielectric barrier discharge plasma on the biological activity of naringin. Food Chem, 2014. 160: p. 241-5. doi: 10.1016/j.foodchem.2014.03.101
  • Cheng, P.Y., Y.M. Lee, Y.S. Wu, T.W. Chang, J.S. Jin, and M.H. Yen, Protective effect of baicalein against endotoxic shock in rats in vivo and in vitro. Biochem Pharmacol, 2007. 73(6): p. 793-804. doi: 10.1016/j.bcp.2006.11.025
  • Koroglu, O.F., M. Gunata, N. Vardi, A. Yildiz, B. Ates, C. Colak, et al., Protective effects of naringin on valproic acid-induced hepatotoxicity in rats. Tissue Cell, 2021. 72: p. 101526. doi: 10.1016/j.tice.2021.101526
  • Karabulut, D., A.T. Akin, M. Unsal, A. Lekesizcan, T.M. Ozyazgan, D.B. Keti, et al., L-Carnitine ameliorates the liver by regulating alpha-SMA, iNOS, HSP90, HIF-1alpha, and RIP1 expressions of CCL4-toxic rats. Iranian journal of basic medical sciences, 2021. 24(2): p. 184-190. doi: 10.22038/IJBMS.2020.47711.10990
  • Kaymak, E., A.T. Akin, E. Tufan, K.E. Başaran, S. Taheri, S. Özdamar, et al., The effect of chloroquine on the TRPC1, TRPC6, and CaSR in the pulmonary artery smooth muscle cells in hypoxia-induced experimental pulmonary artery hypertension. J Biochem Mol Toxicol, 2021. 35(2): p. e22636. doi: 10.1002/jbt.22636
  • Sönmez, M.F., Ş. Ozdemir, M. Guzel, and E. Kaymak, The ameliorative effects of vinpocetine on apoptosis and HSP-70 expression in testicular torsion in rats. Biotech Histochem, 2017. 92(2): p. 92-99. doi: 10.1080/10520295.2016.1259499
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Naringinin ratlarda bakteriyel endotoksin kaynaklı ince bağırsak hasarı üzerindeki anti-inflamatuvar ve anti-apoptotik etkileri

Year 2022, Volume: 47 Issue: 3, 1137 - 1146, 30.09.2022

Ali Tuğrul Akin Mohamed Lemine El Bechir Emin Kaymak Tayfun Ceylan Meryem Sayan Necla Değer Derya Karabulut Ayşe Toluk

https://doi.org/10.17826/cumj.1124641
Cited By: 1

Abstract

Amaç. Bu çalışmanın amacı, birçok biyolojik özelliği bulunan naringinin (NRG) ratlarda bakteriyel endotoksin kaynaklı ince bağırsak hasarı üzerine anti-inflamatuar ve antiapoptotik etkilerinin araştırılmasıdır.
Gereç ve Yöntem: Bu amaçla, 40 adet dişi Wistar albino ırkı rat 4 gruba ayrılmıştır: Kontrol (hiçbir uygulama yapılmayan grup), LPS (10 mg/kg/ip lipopolisakkarit uygulanan grup), NRG (14 gün boyunca 100 mg/kg/ip naringin uygulanan grup) ve LPS+NRG (10 mg/kg/ip lipopolisakkarit uygulamasından önce 14 gün boyunca naringin uygulanan grup). Deneysel prosedürün uygulanmasından sonra, deney hayvanlarının ince barsak dokuları çıkarıldı ve doku takibi protokolüne göre hazırlandı. Barsak dokusundaki histopatolojik değişiklikleri değerlendirmek amacıyla Hematoksilen-Eozin boyaması gerçekleştirildi ve histopatolojik değişiklikler açısından deney gruplarının karşılaştırılması amacıyla hasar skorlaması yapıldı. Ayrıca, immunohistokimyasal boyamalar ile TNF- ve Kaspaz-3 ekspresyon seviyeleri belirlendi ve gruplar arasında bu proteinlerin ekspresyon seviyelerindeki değişikliklerin belirlenmesi için immunohistokimyasal boyanma yoğunluğu skorlandı.
Bulgular: LPS grubunda epitel ve Brunner bezlerinde hasar, mononüklear hücre infiltrasyonu, hemorajik alanlar belirlendi. Ayrıca TNF- ve Kaspaz-3 ekspresyonları bu grupta anlamlı bir şekilde arttı. Ancak, NRG uygulamaları bu parametreler açısından LPS+NRG grubundaki deney hayvanlarının ince barsak dokusunda güçlü bir koruyucu etki gösterdi.
Sonuç: Bu çalışma, 100 mg/kg NRG enjeksiyonunun endotoksin kaynaklı enfeksiyonun bağırsak mukozası üzerindeki olumsuz etkilerine karşı koruyucu bir ajan olarak kabul edilebileceğini ve daha ileri klinik çalışmalarda göz ardı edilmemesi gerektiğini göstermiştir.

Keywords

Endotoksin İnce Bağırsak Hasarı Lipopolisakkarit naringin

References

  • Zhang, X., X. Meng, Y. Chen, S.X. Leng, and H. Zhang, The Biology of Aging and Cancer: Frailty, Inflammation, and Immunity. Cancer J, 2017. 23(4): p. 201-205. doi: 10.1097/ppo.0000000000000270
  • Bektas, A., S.H. Schurman, R. Sen, and L. Ferrucci, Aging, inflammation and the environment. Exp Gerontol, 2018. 105: p. 10-18. doi: 10.1016/j.exger.2017.12.015
  • Ciesielska, A., M. Matyjek, and K. Kwiatkowska, TLR4 and CD14 trafficking and its influence on LPS-induced pro-inflammatory signaling. Cell Mol Life Sci, 2021. 78(4): p. 1233-1261. doi: 10.1007/s00018-020-03656-y
  • Fritsche, K.L., The science of fatty acids and inflammation. Adv Nutr, 2015. 6(3): p. 293s-301s. doi: 10.3945/an.114.006940
  • Płóciennikowska, A., A. Hromada-Judycka, K. Borzęcka, and K. Kwiatkowska, Co-operation of TLR4 and raft proteins in LPS-induced pro-inflammatory signaling. Cell Mol Life Sci, 2015. 72(3): p. 557-581. doi: 10.1007/s00018-014-1762-5
  • Kuzmich, N.N., K.V. Sivak, V.N. Chubarev, Y.B. Porozov, T.N. Savateeva-Lyubimova, and F. Peri, TLR4 Signaling Pathway Modulators as Potential Therapeutics in Inflammation and Sepsis. Vaccines (Basel), 2017. 5(4). doi: 10.3390/vaccines5040034
  • Anderson, S.T., S. Commins, P.N. Moynagh, and A.N. Coogan, Lipopolysaccharide-induced sepsis induces long-lasting affective changes in the mouse. Brain Behav Immun, 2015. 43: p. 98-109. doi: 10.1016/j.bbi.2014.07.007
  • Bae, J.Y., D.S. Lee, Y.K. Cho, J.Y. Lee, J.H. Park, and S.H. Lee, Daphne jejudoensis Attenuates LPS-Induced Inflammation by Inhibiting TNF-α, IL-1β, IL-6, iNOS, and COX-2 Expression in Periodontal Ligament Cells. Pharmaceuticals (Basel), 2022. 15(4). doi: 10.3390/ph15040387
  • Kuypers, F.A., Hyperinflammation, apoptosis, and organ damage. Experimental Biology and Medicine. 0(0): p. 15353702221090454. doi: 10.1177/15353702221090454
  • AKIN, A.T., E. KAYMAK, E. ÖZTÜRK, T. CEYLAN, B. YALÇIN, K.E. BAŞARAN, et al., Mitigative effects of chloroquine treatment against hypoxia-induced intestinal injury: A histological and immunohistochemical study. Turk Hij Den Biyol Derg, 2022. 79(1): p. 59-70. doi: 10.5505/TurkHijyen.2022.78476
  • Shen, L., Functional morphology of the gastrointestinal tract. Curr Top Microbiol Immunol, 2009. 337: p. 1-35. doi: 10.1007/978-3-642-01846-6_1
  • Tsukita, S., M. Furuse, and M. Itoh, Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol, 2001. 2(4): p. 285-93. doi: 10.1038/35067088
  • Xavier, R.J. and D.K. Podolsky, Unravelling the pathogenesis of inflammatory bowel disease. Nature, 2007. 448(7152): p. 427-34. doi: 10.1038/nature06005
  • Li, L., G. Wan, B. Han, and Z. Zhang, Echinacoside alleviated LPS-induced cell apoptosis and inflammation in rat intestine epithelial cells by inhibiting the mTOR/STAT3 pathway. Biomed Pharmacother, 2018. 104: p. 622-628. doi: 10.1016/j.biopha.2018.05.072
  • Van Deventer, S.J., Tumour necrosis factor and Crohn's disease. Gut, 1997. 40(4): p. 443-448. doi: 10.1136/gut.40.4.443
  • Chen, R., Q.-L. Qi, M.-T. Wang, and Q.-Y. Li, Therapeutic potential of naringin: an overview. Pharmaceutical Biology, 2016. 54(12): p. 3203-3210. doi: 10.1080/13880209.2016.1216131
  • Khodayar, M.J., H. Kalantari, M. Mahdavinia, L. Khorsandi, S. Alboghobeish, A. Samimi, et al., Protective effect of naringin against BPA-induced cardiotoxicity through prevention of oxidative stress in male Wistar rats. Drug and Chemical Toxicology, 2020. 43(1): p. 85-95. doi: 10.1080/01480545.2018.1504958
  • Caglayan, C., Y. Temel, F.M. Kandemir, S. Yildirim, and S. Kucukler, Naringin protects against cyclophosphamide-induced hepatotoxicity and nephrotoxicity through modulation of oxidative stress, inflammation, apoptosis, autophagy, and DNA damage. Environmental Science and Pollution Research, 2018. 25(21): p. 20968-20984. doi: 10.1007/s11356-018-2242-5
  • Cerkezkayabekir, A., F. Sanal, E. Bakar, E. Ulucam, and M. Inan, Naringin protects viscera from ischemia/reperfusion injury by regulating the nitric oxide level in a rat model. Biotechnic & Histochemistry, 2017. 92(4): p. 252-263. doi: 10.1080/10520295.2017.1305499
  • Yilmaz, D., O. Teksoy, R. Bilaloglu, and N. Çinkilic, Anti-genotoxic effect of naringin against bleomycin-induced genomic damage in human lymphocytes in vitro. Drug Chem Toxicol, 2016. 39(2): p. 119-23. doi: 10.3109/01480545.2015.1039647
  • Kim, H.J., H.I. Yong, S. Park, K. Kim, T.H. Kim, W. Choe, et al., Effect of atmospheric pressure dielectric barrier discharge plasma on the biological activity of naringin. Food Chem, 2014. 160: p. 241-5. doi: 10.1016/j.foodchem.2014.03.101
  • Cheng, P.Y., Y.M. Lee, Y.S. Wu, T.W. Chang, J.S. Jin, and M.H. Yen, Protective effect of baicalein against endotoxic shock in rats in vivo and in vitro. Biochem Pharmacol, 2007. 73(6): p. 793-804. doi: 10.1016/j.bcp.2006.11.025
  • Koroglu, O.F., M. Gunata, N. Vardi, A. Yildiz, B. Ates, C. Colak, et al., Protective effects of naringin on valproic acid-induced hepatotoxicity in rats. Tissue Cell, 2021. 72: p. 101526. doi: 10.1016/j.tice.2021.101526
  • Karabulut, D., A.T. Akin, M. Unsal, A. Lekesizcan, T.M. Ozyazgan, D.B. Keti, et al., L-Carnitine ameliorates the liver by regulating alpha-SMA, iNOS, HSP90, HIF-1alpha, and RIP1 expressions of CCL4-toxic rats. Iranian journal of basic medical sciences, 2021. 24(2): p. 184-190. doi: 10.22038/IJBMS.2020.47711.10990
  • Kaymak, E., A.T. Akin, E. Tufan, K.E. Başaran, S. Taheri, S. Özdamar, et al., The effect of chloroquine on the TRPC1, TRPC6, and CaSR in the pulmonary artery smooth muscle cells in hypoxia-induced experimental pulmonary artery hypertension. J Biochem Mol Toxicol, 2021. 35(2): p. e22636. doi: 10.1002/jbt.22636
  • Sönmez, M.F., Ş. Ozdemir, M. Guzel, and E. Kaymak, The ameliorative effects of vinpocetine on apoptosis and HSP-70 expression in testicular torsion in rats. Biotech Histochem, 2017. 92(2): p. 92-99. doi: 10.1080/10520295.2016.1259499
  • Bone, R.C., R.A. Balk, F.B. Cerra, R.P. Dellinger, A.M. Fein, W.A. Knaus, et al., Definitions for Sepsis and Organ Failure and Guidelines for the Use of Innovative Therapies in Sepsis. Chest, 1992. 101(6): p. 1644-1655. doi: https://doi.org/10.1378/chest.101.6.1644
  • Dellinger, R.P., M.M. Levy, A. Rhodes, D. Annane, H. Gerlach, S.M. Opal, et al., Surviving Sepsis Campaign: International Guidelines for Management of Severe Sepsis and Septic Shock, 2012. Intensive Care Medicine, 2013. 39(2): p. 165-228. doi: 10.1007/s00134-012-2769-8
  • Zanello, M., M. Vincenzi, L. Di Mauro, and S. Gualdani, Gut and sepsis: Victim of circumstance or prime mover. Trends in Anaesthesia and Critical Care, 2013. 3(3): p. 130-134. doi: https://doi.org/10.1016/j.tacc.2013.03.002
  • Deitch, E.A., Gut-origin sepsis: Evolution of a concept. The Surgeon, 2012. 10(6): p. 350-356. doi: https://doi.org/10.1016/j.surge.2012.03.003
  • Gao, X., S. Hao, H. Yan, W. Ding, K. Li, and J. Li, Neutrophil extracellular traps contribute to the intestine damage in endotoxemic rats. J Surg Res, 2015. 195(1): p. 211-8. doi: 10.1016/j.jss.2014.12.019
  • Deng, B., J. Wu, X. Li, X. Men, and Z. Xu, Probiotics and Probiotic Metabolic Product Improved Intestinal Function and Ameliorated LPS-Induced Injury in Rats. Curr Microbiol, 2017. 74(11): p. 1306-1315. doi: 10.1007/s00284-017-1318-7
  • Stephens, M. and P.Y. von der Weid, Lipopolysaccharides modulate intestinal epithelial permeability and inflammation in a species-specific manner. Gut Microbes, 2020. 11(3): p. 421-432. doi: 10.1080/19490976.2019.1629235
  • Zhou, M., W. Xu, J. Wang, J. Yan, Y. Shi, C. Zhang, et al., Boosting mTOR-dependent autophagy via upstream TLR4-MyD88-MAPK signalling and downstream NF-κB pathway quenches intestinal inflammation and oxidative stress injury. EBioMedicine, 2018. 35: p. 345-360. doi: 10.1016/j.ebiom.2018.08.035
  • Shen, L., Y. Zhou, X. Wu, Y. Sun, T. Xiao, Y. Gao, et al., TREM1 Blockade Ameliorates Lipopolysaccharide-Induced Acute Intestinal Dysfunction through Inhibiting Intestinal Apoptosis and Inflammation Response. Biomed Res Int, 2021. 2021: p. 6635452. doi: 10.1155/2021/6635452
  • Liu, Y., F. Meng, S. Wang, S. Xia, and R. Wang, Vitamin D(3) mitigates lipopolysaccharide-induced oxidative stress, tight junction damage and intestinal inflammatory response in yellow catfish, Pelteobagrus fulvidraco. Comp Biochem Physiol C Toxicol Pharmacol, 2021. 243: p. 108982. doi: 10.1016/j.cbpc.2021.108982
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There are 40 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Research
Authors

Ali Tuğrul Akin 0000-0002-1408-8571

Mohamed Lemine El Bechir 0000-0002-0550-780X

Emin Kaymak 0000-0002-3818-2693

Tayfun Ceylan 0000-0002-0917-0378

Meryem Sayan 0000-0002-9068-1094

Necla Değer 0000-0001-7239-3331

Derya Karabulut 0000-0003-2067-6174

Ayşe Toluk 0000-0003-1787-505X

Publication Date September 30, 2022
Acceptance Date August 3, 2022
Published in Issue Year 2022 Volume: 47 Issue: 3

Cite

MLA Akin, Ali Tuğrul et al. “Anti-Inflammatory and Anti-Apoptotic Effects of Naringin on Bacterial Endotoxin-Induced Small Intestine Damage in Rats”. Cukurova Medical Journal, vol. 47, no. 3, 2022, pp. 1137-46, doi:10.17826/cumj.1124641.

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