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DOI QR Code

The effect of Panax notoginseng saponins on oxidative stress induced by PCV2 infection in immune cells: in vitro and in vivo studies

  • Wang, Qiu-Hua (College of Animal Science and Technology, Guangxi University) ;
  • Kuang, Na (College of Animal Science and Technology, Guangxi University) ;
  • Hu, Wen-yue (School of Life Sciences & Biotechnology, Shanghai Jiao Tong University) ;
  • Yin, Dan (College of Animal Science and Technology, Guangxi University) ;
  • Wei, Ying-Yi (College of Animal Science and Technology, Guangxi University) ;
  • Hu, Ting-Jun (College of Animal Science and Technology, Guangxi University)
  • 투고 : 2020.02.12
  • 심사 : 2020.04.27
  • 발행 : 2020.07.31

초록

Background: Panax notoginseng saponins (PNS) are bioactive substances extracted from P. notoginseng that are widely used to treat cardiovascular and cerebrovascular diseases and interstitial diseases. PNS have the functions of scavenging free radicals, anti-inflammation, improving blood supply for tissue and so on. Objectives: The aim of this study was to investigate the effects of PNS on the oxidative stress of immune cells induced by porcine circovirus 2 (PCV2) infection in vitro and in vivo. Methods: Using an oxidative stress model of PCV2 infection in a porcine lung cell line (3D4/2 cells) and mice, the levels of nitric oxide (NO), reactive oxygen species (ROS), total glutathione (T-GSH), reduced glutathione (GSH), and oxidized glutathione (GSSG) and the activities of xanthine oxidase (XOD), myeloperoxidase (MPO) and inducible nitric oxide synthetase (iNOS) were determined to evaluate the regulatory effects of PNS on oxidative stress. Results: PNS treatment significantly reduced the levels of NO and ROS, the content of GSSG and the activities of XOD, MPO, and iNOS (p < 0.05), while significantly increasing GSH and the ratio of GSH/GSSG in infected 3D4/2 cells (p < 0.05).Similarly, in the in vivo study, PNS treatment significantly decreased the level of ROS in spleen lymphocytes of infected mice (p < 0.05), increased the levels of GSH and T-GSH (p < 0.05), significantly decreased the GSSG level (p < 0.05), and decreased the activities of XOD, MPO, and iNOS. Conclusions: PNS could regulate the oxidative stress of immune cells induced by PCV2 infection in vitro and in vivo.

키워드

과제정보

We thank Dr. Huang KH in the College of Veterinary Medicine at Nanjing Agricultural University, for his kindness of providing PCV2.

참고문헌

  1. Yang J, Tan HL, Gu LY, Song ML, Wu YY, Peng JB, et al. Sophora subprosrate polysaccharide inhibited cytokine/chemokine secretion via suppression of histone acetylation modification and NF-κb activation in PCV2 infected swine alveolar macrophage. Int J Biol Macromol. 2017;104(Pt A):900-908. https://doi.org/10.1016/j.ijbiomac.2017.06.102
  2. Ouardani M, Wilson L, Jette R, Montpetit C, Dea S. Multiplex PCR for detection and typing of porcine circoviruses. J Clin Microbiol. 1999;37(12):3917-3924. https://doi.org/10.1128/JCM.37.12.3917-3924.1999
  3. Segales J. Porcine circovirus type 2 (PCV2) infections: clinical signs, pathology and laboratory diagnosis. Virus Res. 2012;164(1-2):10-19. https://doi.org/10.1016/j.virusres.2011.10.007
  4. Opriessnig T, Meng XJ, Halbur PG. Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J Vet Diagn Invest. 2007;19(6):591-615. https://doi.org/10.1177/104063870701900601
  5. Burton GJ, Jauniaux E. Oxidative stress. Best Pract Res Clin Obstet Gynaecol. 2011;25(3):287-299. https://doi.org/10.1016/j.bpobgyn.2010.10.016
  6. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7(9):405-410. https://doi.org/10.1016/S1360-1385(02)02312-9
  7. Durackova Z. Some current insights into oxidative stress. Physiol Res. 2010;59(4):459-469. https://doi.org/10.33549/physiolres.931844
  8. Peterhans E, Grob M, Burge T, Zanoni R. Virus-induced formation of reactive oxygen intermediates in phagocytic cells. Free Radic Res Commun. 1987;3(1-5):39-46. https://doi.org/10.3109/10715768709069768
  9. Schwarz KB. Oxidative stress during viral infection: a review. Free Radic Biol Med. 1996;21(5):641-649. https://doi.org/10.1016/0891-5849(96)00131-1
  10. Chen X, Ren F, Hesketh J, Shi X, Li J, Gan F, et al. Reactive oxygen species regulate the replication of porcine circovirus type 2 via NF-κB pathway. Virology. 2012;426(1):66-72. https://doi.org/10.1016/j.virol.2012.01.023
  11. Han LF, Sakah KJ, Liu LL, Kojo A, Wang T, Zhang Y. Saponins from roots of Panax notoginseng. Chin Herb Med. 2014;6(2):159-163. https://doi.org/10.1016/s1674-6384(14)60025-3
  12. Zhao GR, Xiang ZJ, Ye TX, Yuan YJ, Guo ZX. Antioxidant activities of Salvia miltiorrhiza and Panax notoginseng. Food Chem. 2006;99(4):767-774. https://doi.org/10.1016/j.foodchem.2005.09.002
  13. Zhou N, Tang Y, Keep RF, Ma X, Xiang J. Antioxidative effects of Panax notoginseng saponins in brain cells. Phytomedicine. 2014;21(10):1189-1195. https://doi.org/10.1016/j.phymed.2014.05.004
  14. Shen Q, Li J, Zhang C, Wang P, Mohammed A, Ni S, et al. Panax notoginseng saponins reduce highrisk factors for thrombosis through peroxisome proliferator-activated receptor -γ pathway. Biomed Pharmacother. 2017;96:1163-1169. https://doi.org/10.1016/j.biopha.2017.11.106
  15. Chinese Veterinary Pharmacopoeia Commission. Chinese Veterinary Pharmacopoeia. Beijing: China Medical Science and Technology Press; 2015, p 11.
  16. Su ZJ, Wei YY, Yin D, Shuai XH, Zeng Y, Hu TJ. Effect of Sophora subprosrate polysaccharide on oxidative stress induced by PCV2 infection in RAW264.7 cells. Int J Biol Macromol. 2013;62:457-464. https://doi.org/10.1016/j.ijbiomac.2013.09.026
  17. Wang X, Wang Z, Wu H, Jia W, Teng L, Song J, et al. Sarcodon imbricatus polysaccharides protect against cyclophosphamide-induced immunosuppression via regulating Nrf2-mediated oxidative stress. Int J Biol Macromol. 2018;120(Pt A):736-744. https://doi.org/10.1016/j.ijbiomac.2018.08.157
  18. Wei YY, Hu TJ, Su ZJ, Zeng Y, Wei XJ, Zhang SX. Immunomodulatory and antioxidant effects of carboxymethylpachymaran on the mice infected with PCV2. Int J Biol Macromol. 2012;50(3):713-719. https://doi.org/10.1016/j.ijbiomac.2011.12.024
  19. Chen X, Ren F, Hesketh J, Shi X, Li J, Gan F, et al. Interaction of porcine circovirus type 2 replication with intracellular redox status in vitro. Redox Rep. 2013;18(5):186-192. https://doi.org/10.1179/1351000213Y.0000000058
  20. Niki E. Do antioxidants impair signaling by reactive oxygen species and lipid oxidation products? FEBS Lett. 2012;586(21):3767-3770. https://doi.org/10.1016/j.febslet.2012.09.025
  21. Block G, Dietrich M, Norkus EP, Morrow JD, Hudes M, Caan B, et al. Factors associated with oxidative stress in human populations. Am J Epidemiol. 2002;156(3):274-285. https://doi.org/10.1093/aje/kwf029
  22. Casola A, Burger N, Liu T, Jamaluddin M, Brasier AR, Garofalo RP. Oxidant tone regulates RANTES gene expression in airway epithelial cells infected with respiratory syncytial virus. Role in viral-induced interferon regulatory factor activation. J Biol Chem. 2001;276(23):19715-19722. https://doi.org/10.1074/jbc.M101526200
  23. Jamaluddin M, Tian B, Boldogh I, Garofalo RP, Brasier AR. Respiratory syncytial virus infection induces a reactive oxygen species-MSK1-phospho-Ser-276 RelA pathway required for cytokine expression. J Virol. 2009;83(20):10605-10615. https://doi.org/10.1128/JVI.01090-09
  24. Korenaga M, Wang T, Li Y, Showalter LA, Chan T, Sun J, et al. Hepatitis C virus core protein inhibits mitochondrial electron transport and increases reactive oxygen species (ROS) production. J Biol Chem. 2005;280(45):37481-37488. https://doi.org/10.1074/jbc.M506412200
  25. Waris G, Turkson J, Hassanein T, Siddiqui A. Hepatitis C virus (HCV) constitutively activates STAT-3 via oxidative stress: role of STAT-3 in HCV replication. J Virol. 2005;79(3):1569-1580. https://doi.org/10.1128/JVI.79.3.1569-1580.2005
  26. Zhai N, Wang H, Chen Y, Li H, Viktor K, Huang K, et al. Taurine attenuates OTA-promoted PCV2 replication through blocking ROS-dependent autophagy via inhibiting AMPK/mTOR signaling pathway. Chem Biol Interact. 2018;296:220-228. https://doi.org/10.1016/j.cbi.2018.10.005
  27. Liu D, Xu J, Qian G, Hamid M, Gan F, Chen X, et al. Selenizing astragalus polysaccharide attenuates PCV2 replication promotion caused by oxidative stress through autophagy inhibition via PI3K/AKT activation. Int J Biol Macromol. 2018;108:350-359. https://doi.org/10.1016/j.ijbiomac.2017.12.010
  28. Xue H, Gan F, Zhang Z, Hu J, Chen X, Huang K. Astragalus polysaccharides inhibits PCV2 replication by inhibiting oxidative stress and blocking NF-κB pathway. Int J Biol Macromol. 2015;81:22-30. https://doi.org/10.1016/j.ijbiomac.2015.07.050
  29. Kobayashi S, Hamashima S, Homma T, Sato M, Kusumi R, Bannai S, et al. Cystine/glutamate transporter, system Xc-, is involved in nitric oxide production in mouse peritoneal macrophages. Nitric Oxide. 2018;78:32-40. https://doi.org/10.1016/j.niox.2018.05.005
  30. Kawakami T, Koike A, Amano F. Sodium bicarbonate regulates nitric oxide production in mouse macrophage cell lines stimulated with lipopolysaccharide and interferon γ. Nitric Oxide. 2018;79:45-50. https://doi.org/10.1016/j.niox.2018.07.008
  31. Uetani K, Der SD, Zamanian-Daryoush M, de La Motte C, Lieberman BY, Williams BR, et al. Central role of double-stranded RNA-activated protein kinase in microbial induction of nitric oxide synthase. J Immunol. 2000;165(2):988-996. https://doi.org/10.4049/jimmunol.165.2.988
  32. Stark JM, Khan AM, Chiappetta CL, Xue H, Alcorn JL, Colasurdo GN. Immune and functional role of nitric oxide in a mouse model of respiratory syncytial virus infection. J Infect Dis. 2005;191(3):387-395. https://doi.org/10.1086/427241
  33. Lalle E, Bordi L, Castilletti C, Meschi S, Selleri M, Carletti F, et al. Design and clinical application of a molecular method for detection and typing of the influenza A/H1N1pdm virus. J Virol Methods. 2010;163(2):486-488. https://doi.org/10.1016/j.jviromet.2009.10.004
  34. Jones DP. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol. 2002;348:93-112. https://doi.org/10.1016/S0076-6879(02)48630-2
  35. Biswas SK, Newby DE, Rahman I, Megson IL. Depressed glutathione synthesis precedes oxidative stress and atherogenesis in Apo-E(-/-) mice. Biochem Biophys Res Commun. 2005;338(3):1368-1373. https://doi.org/10.1016/j.bbrc.2005.10.098
  36. Hosakote YM, Liu T, Castro SM, Garofalo RP, Casola A. Respiratory syncytial virus induces oxidative stress by modulating antioxidant enzymes. Am J Respir Cell Mol Biol. 2009;41(3):348-357. https://doi.org/10.1165/rcmb.2008-0330OC
  37. Nakamura H, Masutani H, Yodoi J. Redox imbalance and its control in HIV infection. Antioxid Redox Signal. 2002;4(3):455-464. https://doi.org/10.1089/15230860260196245
  38. Aratani Y. Myeloperoxidase: its role for host defense, inflammation, and neutrophil function. Arch Biochem Biophys. 2018;640:47-52. https://doi.org/10.1016/j.abb.2018.01.004
  39. Guilpain P, Servettaz A, Batteux F, Guillevin L, Mouthon L. Natural and disease associated antimyeloperoxidase (MPO) autoantibodies. Autoimmun Rev. 2008;7(6):421-425. https://doi.org/10.1016/j.autrev.2008.03.009
  40. Strzepa A, Pritchard KA, Dittel BN. Myeloperoxidase: a new player in autoimmunity. Cell Immunol. 2017;317:1-8. https://doi.org/10.1016/j.cellimm.2017.05.002
  41. Wan Y, Zou B, Zeng H, Zhang L, Chen M, Fu G. Inhibitory effect of verbascoside on xanthine oxidase activity. Int J Biol Macromol. 2016;93(Pt A):609-614. https://doi.org/10.1016/j.ijbiomac.2016.09.022