The Potential Radioprotective Effect of Piperine against Radiation-induced Lung Injury in Mice: Histopathological and Biochemical Evaluations


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Introduction:It has been hypothesized that piperine, the main alkaloid component of black pepper, possesses a unique radioprotective effect. This study aimed to investigate the protective effect of piperine against Radiation-Induced Lung Injury (RILI) in mice.

Methods:Firstly, eighty male mice were divided into eight groups; the control group did not receive any dosage of piperine and radiation (6 Gy), and the other groups received piperine alone at doses 10, 25, and 50 mg/kg, radiation, and radiation-piperine combination (6 Gy + 10, 25, and 50 mg/kg). Animals received piperine by gavage for 7 consecutive days. To investigate the effect of piperine pretreatment in mice that were exposed to radiation, histopathological and biochemical evaluations (markers of oxidative stress) were performed. Irradiation led to an increase in oxidative stress (increase in MDA and PC). Pretreatment of piperine in all three doses in irradiated mice was able to reduce oxidative stress compared to mice that were only exposed to radiation.

Results:Piperine at a dose of 25 mg/kg exhibited the highest protective effect as compared to other doses. Also, in the histopathological examination, it was seen that pretreatment with piperine was able to improve the infiltration of inflammatory cells and reduce the thickness of the alveolar septum and air sac damage.

Conclusion:The outcomes completely proved significant lung protection by piperine in mice through reducing oxidative stress. This natural compound could be considered a protective agent against lung injury induced by ionizing radiation.

Sobre autores

Asal Safarbalou

Department of Pharmacy,, Mazandaran University of Medical Sciences

Email: info@benthamscience.net

Fatemeh Ebrahimi

Department of Radiopharmacy, Faculty of Pharmacy,, Mazandaran University of Medical Sciences,

Email: info@benthamscience.net

Fereshteh Talebpour Amiri

Department of Anatomy, Faculty of Medicine, Molecular and Cell Biology Research Center, Mazandaran University of Medical Sciences

Email: info@benthamscience.net

Seyed Hosseinimehr

Department of Radiopharmacy, Faculty of Pharmacy,, Mazandaran University of Medical Sciences

Autor responsável pela correspondência
Email: info@benthamscience.net

Bibliografia

  1. Szumiel I. Ionizing radiation-induced oxidative stress, epigenetic changes and genomic instability: The pivotal role of mitochondria. Int J Radiat Biol 2015; 91(1): 1-12. doi: 10.3109/09553002.2014.934929 PMID: 24937368
  2. Kim HM, Kim SH, Kang BS. Radioprotective effects of delphinidin on normal human lung cells against proton beam exposure. Nutr Res Pract 2018; 12(1): 41-6. doi: 10.4162/nrp.2018.12.1.41 PMID: 29399295
  3. Johnson S, Shaikh SB, Muneesa F, Rashmi B, Bhandary YP. Radiation induced apoptosis and pulmonary fibrosis: Curcumin an effective intervention? Int J Radiat Biol 2020; 96(6): 709-17. doi: 10.1080/09553002.2020.1739773 PMID: 32149561
  4. Pan J, Su Y, Hou X, et al. Protective effect of recombinant protein SOD-TAT on radiation-induced lung injury in mice. Life Sci 2012; 91(3-4): 89-93. doi: 10.1016/j.lfs.2012.06.003 PMID: 22727792
  5. Hosseinimehr SJ. The protective effects of trace elements against side effects induced by ionizing radiation. Radiat Oncol J 2015; 33(2): 66-74. doi: 10.3857/roj.2015.33.2.66 PMID: 26157675
  6. Tian X, Wang F, Luo Y, et al. Protective role of nuclear factor-erythroid 2-related factor 2 against radiation-induced lung injury and inflammation. Front Oncol 2018; 8: 542. doi: 10.3389/fonc.2018.00542 PMID: 30533397
  7. Hou G, Li J, Liu W, Wei J, Xin Y, Jiang X. Mesenchymal stem cells in radiation-induced lung injury: From mechanisms to therapeutic potential. Front Cell Dev Biol 2022; 10: 1100305. doi: 10.3389/fcell.2022.1100305 PMID: 36578783
  8. Hillman GG, Singh-Gupta V, Lonardo F, et al. Radioprotection of lung tissue by soy isoflavones. J Thorac Oncol 2013; 8(11): 1356-64. doi: 10.1097/JTO.0b013e3182a4713e PMID: 24077456
  9. Zhu N, Liu R, He LX, et al. Radioprotective effect of walnut oligopeptides against gamma radiation-induced splenocyte apoptosis and intestinal injury in mice. Molecules 2019; 24(8): 1582. doi: 10.3390/molecules24081582 PMID: 31013611
  10. Aras S, Efendioğlu M, Wulamujiang A, Ozkanli SS, Keleş MS, Tanzer İO. Radioprotective effect of melatonin against radiotherapy-induced cerebral cortex and cerebellum damage in rat. Int J Radiat Biol 2021; 97(3): 348-55. doi: 10.1080/09553002.2021.1864047 PMID: 33320758
  11. Hosseinimehr SJ. Trends in the development of radioprotective agents. Drug Discov Today 2007; 12(19-20): 794-805. doi: 10.1016/j.drudis.2007.07.017 PMID: 17933679
  12. Talebpour Amiri F, Hamzeh M, Naeimi RA, Ghasemi A, Hosseinimehr SJ. Radioprotective effect of atorvastatin against ionizing radiation-induced nephrotoxicity in mice. Int J Radiat Biol 2018; 94(2): 106-13. doi: 10.1080/09553002.2018.1420926 PMID: 29268056
  13. Yeung KS, Hernandez M, Mao JJ, Haviland I, Gubili J. Herbal medicine for depression and anxiety: A systematic review with assessment of potential psycho-oncologic relevance. Phytother Res 2018; 32(5): 865-91. doi: 10.1002/ptr.6033 PMID: 29464801
  14. Moon C, Kim SH, Kim JC, et al. Protective effect of phlorotannin components phloroglucinol and eckol on radiation-induced intestinal injury in mice. Phytother Res 2008; 22(2): 238-42. doi: 10.1002/ptr.2298 PMID: 17886227
  15. Farzipour S, Amiri FT, Mihandoust E, et al. Radioprotective effect of diethylcarbamazine on radiation-induced acute lung injury and oxidative stress in mice. J Bioenerg Biomembr 2020; 52(1): 39-46. doi: 10.1007/s10863-019-09820-9 PMID: 31853753
  16. Fountain MD, McLellan LA, Smith NL, et al. Isoflavone-mediated radioprotection involves regulation of early endothelial cell death and inflammatory signaling in radiation-induced lung injury. Int J Radiat Biol 2020; 96(2): 245-56. doi: 10.1080/09553002.2020.1683642 PMID: 31633433
  17. Derosa G, Maffioli P, Sahebkar A. Piperine and its role in chronic diseases. Adv Exp Med Biol 2016; 928: 173-84. doi: 10.1007/978-3-319-41334-1_8 PMID: 27671817
  18. Gorgani L, Mohammadi M, Najafpour GD, Nikzad M. Piperine-the bioactive compound of black pepper: From isolation to medicinal formulations. Compr Rev Food Sci Food Saf 2017; 16(1): 124-40. doi: 10.1111/1541-4337.12246 PMID: 33371546
  19. Bano G, Amla V, Raina R, Zutshi U, Chopra C. The effect of piperine on pharmacokinetics of phenytoin in healthy volunteers. Planta Med 1987; 53(6): 568-9. doi: 10.1055/s-2006-962814 PMID: 3444866
  20. Sunila ES, Kuttan G. Immunomodulatory and antitumor activity of Piper longum Linn. and piperine. J Ethnopharmacol 2004; 90(2-3): 339-46. doi: 10.1016/j.jep.2003.10.016 PMID: 15013199
  21. Pawar KS, Mastud RN, Pawar SK, et al. Oral curcumin with piperine as adjuvant therapy for the treatment of COVID-19: A randomized clinical trial. Front Pharmacol 2021; 12: 669362. doi: 10.3389/fphar.2021.669362 PMID: 34122090
  22. 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): 323-34. doi: 10.1016/j.jsps.2018.01.010 PMID: 29556123
  23. Haq IU, Imran M, Nadeem M, Tufail T, Gondal TA, Mubarak MS. Piperine: A review of its biological effects. Phytother Res 2021; 35(2): 680-700. doi: 10.1002/ptr.6855 PMID: 32929825
  24. 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. doi: 10.1080/19390211.2018.1481485 PMID: 30299203
  25. de Souza Grinevicius VMA, Kviecinski MR, Santos Mota NSR, et al. Piper nigrum ethanolic extract rich in piperamides causes ROS overproduction, oxidative damage in DNA leading to cell cycle arrest and apoptosis in cancer cells. J Ethnopharmacol 2016; 189: 139-47. doi: 10.1016/j.jep.2016.05.020 PMID: 27178634
  26. Manayi A, Nabavi SM, Setzer WN, Jafari S. Piperine as a potential anti-cancer agent: A review on preclinical studies. Curr Med Chem 2019; 25(37): 4918-28. doi: 10.2174/0929867324666170523120656 PMID: 28545378
  27. Rehman MU, Rashid S, Arafah A, et al. Piperine regulates Nrf-2/Keap-1 signalling and exhibits anticancer effect in experimental colon carcinogenesis in wistar rats. Biology 2020; 9(9): 302. doi: 10.3390/biology9090302 PMID: 32967203
  28. Ghelishli N, Ghasemi A, Hosseinimehr SJ. The influence of piperine on the radioprotective effect of curcumin in irradiated human lymphocytes. TurkJ Pharm Sci 2019; 16(3): 366-70.
  29. Safarbalou A, Ebrahimi F, Amiri FT, Hosseinimehr SJ. Radioprotective effect of piperine, as a major component of black pepper, against radiation-induced colon injury: Biochemical and histological studies. Curr Radiopharm 2024; 17(1): 38-45. doi: 10.2174/1874471016666230725112319 PMID: 37489775
  30. El-Ghazaly MA, Fadel NA, Rashed ER, Kenawy SA. Anti-inflammatory and anti-nociceptive effects of piperine in gamma-irradiated rats. Egypt J Rad Sci Applic 2016; 29(1): 1-16. doi: 10.21608/ejrsa.2016.1575
  31. Chen T, Wang L, Chen K, et al. Evaluation of gamma ray-induced gastrointestinal tract morphological and proliferative activity changes in rhesus monkeys. Hum Exp Toxicol 2016; 35(10): 1133-44. doi: 10.1177/0960327115622259 PMID: 26699188
  32. Johnston CJ, Manning C, Hernady E, et al. Effect of total body irradiation on late lung effects: Hidden dangers. Int J Radiat Biol 2011; 87(8): 902-13. doi: 10.3109/09553002.2011.573439 PMID: 21574903
  33. Hosseinpour S, Nejad Moghaddam AE, Talebpour Amir F, et al. Radioprotective effect of hesperidin against ovarian toxicity induced by ionizing radiation through inhibiting oxidative stress in mice. Int J Rad Res 2022; 20(2): 417-23. doi: 10.52547/ijrr.20.2.24
  34. Bradford MM. 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): 248-54. doi: 10.1016/0003-2697(76)90527-3 PMID: 942051
  35. Colombo G, Clerici M, Garavaglia ME, et al. A step-by-step protocol for assaying protein carbonylation in biological samples. J Chromatogr B Analyt Technol Biomed Life Sci 2016; 1019: 178-90. doi: 10.1016/j.jchromb.2015.11.052 PMID: 26706659
  36. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978; 52: 302-10. doi: 10.1016/S0076-6879(78)52032-6 PMID: 672633
  37. Habibi E, Shokrzadeh M, Chabra A, Naghshvar F, Keshavarz-Maleki R, Ahmadi A. Protective effects of Origanum vulgare ethanol extract against cyclophosphamide-induced liver toxicity in mice. Pharm Biol 2015; 53(1): 10-5. doi: 10.3109/13880209.2014.908399 PMID: 25026348
  38. Hanania AN, Mainwaring W, Ghebre YT, Hanania NA, Ludwig M. Radiation-induced lung injury. Chest 2019; 156(1): 150-62. doi: 10.1016/j.chest.2019.03.033 PMID: 30998908
  39. Elsawi SA, Radwan RR, Elbatanony MM, El-Feky AM, Sherif NH. Prophylactic effect of Opuntia ficus indica fruit peel extract against irradiation-induced colon injury in rats. Planta Med 2020; 86(1): 61-9. doi: 10.1055/a-1019-9801 PMID: 31627218
  40. Kim W, Lee S, Seo D, et al. Cellular stress responses in radiotherapy. Cells 2019; 8(9): 1105. doi: 10.3390/cells8091105 PMID: 31540530
  41. Choochana P, Moungjaroen J, Jongkon N, Gritsanapan W, Tangyuenyongwatana P. Development of piperic acid derivatives from Piper nigrum as UV protection agents. Pharm Biol 2015; 53(4): 477-82. doi: 10.3109/13880209.2014.924020 PMID: 25471519
  42. Selvendiran K, Banu SM, Sakthisekaran D. Oral supplementation of piperine leads to altered phase II enzymes and reduced DNA damage and DNA-protein cross links in Benzo(a)pyrene induced experimental lung carcinogenesis. Mol Cell Biochem 2005; 268(1-2): 141-7. doi: 10.1007/s11010-005-3702-z PMID: 15724447
  43. Lu Y, Liu J, Li H, Gu L. Piperine ameliorates lipopolysaccharide-induced acute lung injury via modulating NF-κB signaling pathways. Inflammation 2016; 39(1): 303-8. doi: 10.1007/s10753-015-0250-x PMID: 26410851
  44. Papac-Milicevic N, Busch CJL, Binder CJ. Malondialdehyde epitopes as targets of immunity and the implications for atherosclerosis. Adv Immunol 2016; 131: 1-59. doi: 10.1016/bs.ai.2016.02.001 PMID: 27235680
  45. Heath RL, Packer L. Effect of light on lipid peroxidation in chloroplasts. Biochem Biophys Res Commun 1965; 19(6): 716-20. doi: 10.1016/0006-291X(65)90316-5 PMID: 5840698
  46. 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. doi: 10.1016/S0009-8981(03)00003-2 PMID: 12589963

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