Generic placeholder image

Current Radiopharmaceuticals

Editor-in-Chief

ISSN (Print): 1874-4710
ISSN (Online): 1874-4729

Research Article

Radioprotective Effect of Piperine, as a Major Component of Black Pepper, Against Radiation-induced Colon Injury: Biochemical and Histological Studies

Author(s): Asal Safarbalou, Fatemeh Ebrahimi, Fereshteh Talebpour Amiri and Seyed Jalal Hosseinimehr*

Volume 17, Issue 1, 2024

Published on: 01 August, 2023

Page: [38 - 45] Pages: 8

DOI: 10.2174/1874471016666230725112319

Price: $65

Abstract

Background: Patients undergoing radiotherapy are prone to radiation-induced gastrointestinal injury. Piperine is an alkaloid component in black pepper with a unique chemopreventive activity against oxidative stress-related damage in healthy tissues. The purpose of this study was to investigate the effects of piperine on intestinal damage.

Methods: In this study, mice were divided into eight groups: including the control, piperine (10, 25, and 50 mg/kg), radiation (6 Gy), and piperine+radiation (10, 25 and 50 mg/kg + 6 Gy) groups. The radioprotective effects of piperine were evaluated by biochemical (MDA, GSH, and PC) and histopathological assessments in colon tissues.

Results: The 10 mg/kg dose of piperine significantly reduced the levels of oxidative stress biomarkers compared to the group that received only radiation. In addition, pre-treatment with 10 mg/kg piperine diminished the histopathological changes like vascular congestion in the submucosa, while the dose of 50 mg/kg led to the infiltration of inflammatory cells.

Conclusion: Based on this study, it is concluded that piperine, at low dose, with its antioxidant properties, could reduce the colon damage caused by radiation.

Keywords: Ionizing radiation, piperine, radiation, colon injury, oxidative stress, radioprotective.

[1]
Dennert, G.; Horneber, M. Selenium for alleviating the side effects of chemotherapy, radiotherapy and surgery in cancer patients. Cochrane Libr., 2006, 2017(3), CD005037.
[http://dx.doi.org/10.1002/14651858.CD005037.pub2] [PMID: 16856073]
[2]
Brook, I. Late side effects of radiation treatment for head and neck cancer. Radiat. Oncol. J., 2020, 38(2), 84-92.
[http://dx.doi.org/10.3857/roj.2020.00213] [PMID: 33012151]
[3]
Xie, L.W.; Cai, S.; Zhao, T.S.; Li, M.; Tian, Y. Green tea derivative (−)-epigallocatechin-3-gallate (EGCG) confers protection against ionizing radiation-induced intestinal epithelial cell death both in vitro and in vivo. Free Radic. Biol. Med., 2020, 161, 175-186.
[http://dx.doi.org/10.1016/j.freeradbiomed.2020.10.012] [PMID: 33069855]
[4]
Hosseinimehr, S.J. Trends in the development of radioprotective agents. Drug Discov. Today, 2007, 12(19-20), 794-805.
[http://dx.doi.org/10.1016/j.drudis.2007.07.017] [PMID: 17933679]
[5]
Rahmanian, N.; Hosseinimehr, S.J.; Khalaj, A. The paradox role of caspase cascade in ionizing radiation therapy. J. Biomed. Sci., 2016, 23(1), 88.
[http://dx.doi.org/10.1186/s12929-016-0306-8] [PMID: 27923354]
[6]
Nuszkiewicz, J.; Woźniak, A.; Szewczyk-Golec, K. Ionizing radiation as a source of oxidative stress-the protective role of melatonin and vitamin D. Int. J. Mol. Sci., 2020, 21(16), 5804.
[http://dx.doi.org/10.3390/ijms21165804] [PMID: 32823530]
[7]
Lu, L.; Li, W.; Chen, L.; Su, Q.; Wang, Y.; Guo, Z.; Lu, Y.; Liu, B.; Qin, S. Radiation-induced intestinal damage: latest molecular and clinical developments. Future Oncol., 2019, 15(35), 4105-4118.
[http://dx.doi.org/10.2217/fon-2019-0416] [PMID: 31746639]
[8]
Thomsen, M.; Vitetta, L. Adjunctive treatments for the prevention of chemotherapy and radiotherapy-induced mucositis. Integr. Cancer Ther., 2018, 17(4), 1027-1047.
[http://dx.doi.org/10.1177/1534735418794885] [PMID: 30136590]
[9]
Zhu, N.; Liu, R.; He, L.X.; Mao, R.X.; Liu, X.R.; Zhang, T.; Hao, Y.T.; Fan, R.; Xu, M.H.; Li, Y. Radioprotective effect of walnut oligopeptides against gamma radiation-induced splenocyte apoptosis and intestinal injury in mice. Molecules, 2019, 24(8), 1582.
[http://dx.doi.org/10.3390/molecules24081582] [PMID: 31013611]
[10]
Aras, S.; Efendioğlu, M.; Wulamujiang, A.; Ozkanli, S.S.; Keleş, M.S.; Tanzer, İ.O. Radioprotective effect of melatonin against radiotherapy-induced cerebral cortex and cerebellum damage in rat. Int. J. Radiat. Biol., 2021, 97(3), 348-355.
[http://dx.doi.org/10.1080/09553002.2021.1864047] [PMID: 33320758]
[11]
Hosseinimehr, S.J.; Ahmadi, A.; Beiki, D.; Habibi, E.; Mahmoudzadeh, A. Protective effects of hesperidin against genotoxicity induced by 99mTc-MIBI in human cultured lymphocyte cells. Nucl. Med. Biol., 2009, 36(7), 863-867.
[http://dx.doi.org/10.1016/j.nucmedbio.2009.06.002] [PMID: 19720298]
[12]
Hosseinimehr, S.J. The protective effects of trace elements against side effects induced by ionizing radiation. Radiat. Oncol. J., 2015, 33(2), 66-74.
[http://dx.doi.org/10.3857/roj.2015.33.2.66] [PMID: 26157675]
[13]
Derosa, G.; Maffioli, P.; Sahebkar, A. Piperine and Its Role in Chronic Diseases. Adv. Exp. Med. Biol., 2016, 928, 173-184.
[http://dx.doi.org/10.1007/978-3-319-41334-1_8] [PMID: 27671817]
[14]
Banerjee, S.; Katiyar, P.; Kumar, V.; Saini, S.S.; Varshney, R.; Krishnan, V.; Sircar, D.; Roy, P. Black pepper and piperine induce anticancer effects on leukemia cell line. Toxicol. Res. (Camb.), 2021, 10(2), 169-182.
[http://dx.doi.org/10.1093/toxres/tfab001] [PMID: 33884168]
[15]
Pawar, K.S.; Mastud, R.N.; Pawar, S.K.; Pawar, S.S.; Bhoite, R.R.; Bhoite, R.R.; Kulkarni, M.V.; Deshpande, A.R. Oral curcumin with piperine as adjuvant therapy for the treatment of COVID-19: A randomized clinical trial. Front. Pharmacol., 2021, 12, 669362.
[http://dx.doi.org/10.3389/fphar.2021.669362] [PMID: 34122090]
[16]
Baspinar, Y.; Üstündas, M.; Bayraktar, O.; Sezgin, C. Curcumin and piperine loaded zein-chitosan nanoparticles: Development and in-vitro characterisation. Saudi Pharm. J., 2018, 26(3), 323-334.
[http://dx.doi.org/10.1016/j.jsps.2018.01.010] [PMID: 29556123]
[17]
Haq, I.U.; Imran, M.; Nadeem, M.; Tufail, T.; Gondal, T.A.; Mubarak, M.S. Piperine: A review of its biological effects. Phytother. Res., 2021, 35(2), 680-700.
[http://dx.doi.org/10.1002/ptr.6855] [PMID: 32929825]
[18]
Selvendiran, K.; Senthilnathan, P.; Magesh, V.; Sakthisekaran, D. Modulatory effect of Piperine on mitochondrial antioxidant system in Benzo(a)pyrene-induced experimental lung carcinogenesis. Phytomedicine, 2004, 11(1), 85-89.
[http://dx.doi.org/10.1078/0944-7113-00355] [PMID: 14971727]
[19]
Verma, N.; Bal, S.; Gupta, R.; Aggarwal, N.; Yadav, A. Antioxidative effects of piperine against cadmium-induced oxidative stress in cultured human peripheral blood lymphocytes. J. Diet. Suppl., 2020, 17(1), 41-52.
[http://dx.doi.org/10.1080/19390211.2018.1481485] [PMID: 30299203]
[20]
Manayi, A.; Nabavi, S.M.; Setzer, W.N.; Jafari, S. Piperine as a potential anti-cancer agent: A review on preclinical studies. Curr. Med. Chem., 2019, 25(37), 4918-4928.
[http://dx.doi.org/10.2174/0929867324666170523120656] [PMID: 28545378]
[21]
Quijia, C.R.; Chorilli, M. Characteristics, biological properties and analytical methods of piperine: A review. Crit. Rev. Anal. Chem., 2020, 50(1), 62-77.
[http://dx.doi.org/10.1080/10408347.2019.1573656] [PMID: 30810335]
[22]
de Almeida, G.C.; Oliveira, L.F.S.; Predes, D.; Fokoue, H.H.; Kuster, R.M.; Oliveira, F.L.; Mendes, F.A.; Abreu, J.G. Piperine suppresses the Wnt/β-catenin pathway and has anti-cancer effects on colorectal cancer cells. Sci. Rep., 2020, 10(1), 11681.
[http://dx.doi.org/10.1038/s41598-020-68574-2] [PMID: 32669593]
[23]
Ghelishli, N.; Ghasemi, A.; Hosseinimehr, S.J. The influence of piperine on the radioprotective effect of curcumin in irradiated human lymphocytes turk. J. Pharm. Sci., 2019, 16(3), 366-370.
[24]
EL-Ghazaly. M.A.; Fadel, N.A.; Rashed, E.R.; Kenawy S.A. Anti-inflammatory and anti-nociceptive effects of piperine in gamma-irradiated rats. EJRSA, 2016, 29(1), 1-16.
[http://dx.doi.org/10.21608/ejrsa.2016.1575]
[25]
Chen, T.; Wang, L.; Chen, K.; Qiu, S.; Cen, X.; Li, H.; Hu, C. Evaluation of gamma ray-induced gastrointestinal tract morphological and proliferative activity changes in rhesus monkeys. Hum. Exp. Toxicol., 2016, 35(10), 1133-1144.
[http://dx.doi.org/10.1177/0960327115622259] [PMID: 26699188]
[26]
Johnston, C.J.; Manning, C.; Hernady, E.; Reed, C.; Thurston, S.W.; Finkelstein, J.N.; Williams, J.P. Effect of total body irradiation on late lung effects: Hidden dangers. Int. J. Radiat. Biol., 2011, 87(8), 902-913.
[http://dx.doi.org/10.3109/09553002.2011.573439] [PMID: 21574903]
[27]
Hosseinpour, S.; Nejad Moghaddam, A.E.; Talebpour Amir, F.; Hosseinimehr, S.J.; Zargari, M.; Karimpour Malekshah, A.; Ghasemi, A. Radioprotective effect of hesperidin against ovarian toxicity induced by Ionizing radiation through inhibiting oxidative stress in mice. Int. J. Radiat. Res, 2022, 20(2), 417-423.
[http://dx.doi.org/10.52547/ijrr.20.2.24]
[28]
Farzipour, S.; Amiri, F.T.; Mihandoust, E.; Shaki, F.; Noaparast, Z.; Ghasemi, A.; Hosseinimehr, S.J. Radioprotective effect of diethylcarbamazine on radiation-induced acute lung injury and oxidative stress in mice. J. Bioenerg. Biomembr., 2020, 52(1), 39-46.
[http://dx.doi.org/10.1007/s10863-019-09820-9] [PMID: 31853753]
[29]
Talebpour Amiri, F.; Hamzeh, M.; Naeimi, R.A.; Ghasemi, A.; Hosseinimehr, S.J. Radioprotective effect of atorvastatin against ionizing radiation-induced nephrotoxicity in mice. Int. J. Radiat. Biol., 2018, 94(2), 106-113.
[http://dx.doi.org/10.1080/09553002.2018.1420926] [PMID: 29268056]
[30]
Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 1976, 72(1-2), 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[31]
Buege, J.A.; Aust, S.D. Microsomal lipid peroxidation. Methods Enzymol., 1978, 52, 302-310.
[http://dx.doi.org/10.1016/S0076-6879(78)52032-6] [PMID: 672633]
[32]
Colombo, G.; Clerici, M.; Garavaglia, M.E.; Giustarini, D.; Rossi, R.; Milzani, A.; Dalle-Donne, I. A step-by-step protocol for assaying protein carbonylation in biological samples. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2016, 1019, 178-190.
[http://dx.doi.org/10.1016/j.jchromb.2015.11.052] [PMID: 26706659]
[33]
Ansari, M.N.; Rehman, N.U.; Karim, A.; Soliman, G.A.; Ganaie, M.A.; Raish, M.; Hamad, A.M. Role of Oxidative Stress and Inflammatory Cytokines (TNF-α and IL-6) in Acetic Acid-Induced Ulcerative Colitis in Rats: Ameliorated by Otostegia fruticosa. Life (Basel), 2021, 11(3), 195.
[http://dx.doi.org/10.3390/life11030195] [PMID: 33802553]
[34]
Elsawi, S.A.; Radwan, R.R.; Elbatanony, M.M.; El-Feky, A.M.; Sherif, N.H. Prophylactic effect of opuntia ficus indica fruit peel extract against irradiation-induced colon injury in rats. Planta Med., 2020, 86(1), 61-69.
[http://dx.doi.org/10.1055/a-1019-9801] [PMID: 31627218]
[35]
France, H.G., Jr; Jirtle, R.L.; Mansbach, C.M. II Intracolonic WR 2721 protection of the rat colon from acute radiation injury. Gastroenterology, 1986, 91(3), 644-650.
[http://dx.doi.org/10.1016/0016-5085(86)90634-7] [PMID: 3015711]
[36]
Cagin, Y.F.; Parlakpinar, H.; Polat, A.; Vardi, N.; Atayan, Y.; Erdogan, M.A.; Ekici, K.; Yildiz, A.; Sarihan, M.E.; Aladag, H. The protective effects of apocynin on ionizing radiation-induced intestinal damage in rats. Drug Dev. Ind. Pharm., 2016, 42(2), 317-324.
[http://dx.doi.org/10.3109/03639045.2015.1052080] [PMID: 26072994]
[37]
Sezen, O.; Erdemci, B.; Calik, M.; Koc, M. The role of melatonin in preventing radiation-induced intestinal injury. J. BUON, 2021, 26(2), 626-633.
[PMID: 34077015]
[38]
Jothy, S.L.; Saito, T.; Kanwar, J.R.; Chen, Y.; Aziz, A.; Yin-Hui, L.; Sasidharan, S. Radioprotective activity of Polyalthia longifolia standardized extract against X-ray radiation injury in mice. Phys. Med., 2016, 32(1), 150-161.
[http://dx.doi.org/10.1016/j.ejmp.2015.10.090] [PMID: 26526749]
[39]
Li, S.; Nguyen, T.T.; Ung, T.T.; Sah, D.K.; Park, S.Y.; Lakshmanan, V.K.; Jung, Y.D. Piperine attenuates lithocholic acid-stimulated interleukin-8 by suppressing Src/EGFR and reactive oxygen species in human colorectal cancer cells. Antioxidants, 2022, 11(3), 530.
[40]
Abdel-Daim, M.M.; Sayed, A.A.; Abdeen, A.; Aleya, L.; Ali, D.; Alkahtane, A.A.; Alarifi, S.; Alkahtani, S. Piperine enhances the antioxidant and anti-inflammatory activities of thymoquinone against microcystin-LR-induced hepatotoxicity and neurotoxicity in mice. Oxid. Med. Cell. Longev., 2019, 2019, 1-10.
[http://dx.doi.org/10.1155/2019/1309175] [PMID: 31178949]
[41]
Tripathi, A.K.; Ray, A.K.; Mishra, S.K. Molecular and pharmacological aspects of piperine as a potential molecule for disease prevention and management: evidence from clinical trials. Beni. Suef Univ. J. Basic Appl. Sci., 2022, 11(1), 16.
[http://dx.doi.org/10.1186/s43088-022-00196-1] [PMID: 35127957]
[42]
Dalle-Donne, I.; Rossi, R.; Giustarini, D.; Milzani, A.; Colombo, R. Protein carbonyl groups as biomarkers of oxidative stress. Clin. Chim. Acta, 2003, 329(1-2), 23-38.
[http://dx.doi.org/10.1016/S0009-8981(03)00003-2] [PMID: 12589963]
[43]
Abou-Zeid, S.M. EL-bialy, B.E.; EL-borai, N.B.; AbuBakr, H.O.; Elhadary, A.M.A. Radioprotective effect of Date syrup on radiation- induced damage in Rats. Sci. Rep., 2018, 8(1), 7423.
[http://dx.doi.org/10.1038/s41598-018-25586-3] [PMID: 29743497]
[44]
Rehman, M.U.; Rashid, S.; Arafah, A.; Qamar, W.; Alsaffar, R.M.; Ahmad, A.; Almatroudi, N.M.; Alqahtani, S.M.A.; Rashid, S.M.; Ahmad, S.B. Piperine regulates Nrf-2/Keap-1 signalling and exhibits anticancer effect in experimental colon carcinogenesis in wistar rats. Biology (Basel), 2020, 9(9), 302.
[http://dx.doi.org/10.3390/biology9090302] [PMID: 32967203]
[45]
Nabil, H.M.; Hassan, B.N.; Tohamy, A.A.; Waaer, H.F.; Abdel Moneim, A.E. Radioprotection of 1,2-dimethylhydrazine-initiated colon cancer in rats using low-dose γ rays by modulating multidrug resistance-1, cytokeratin 20, and β-catenin expression. Hum. Exp. Toxicol., 2016, 35(3), 282-292.
[http://dx.doi.org/10.1177/0960327115584687] [PMID: 25926526]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy