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Prophylactic effect of resveratrol and piperine on pristane-induced murine model of lupus-like disease

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Abstract

Systemic lupus erythematosus is a multisystem autoimmune disease. Apart from usual treatments, approximately 50% of lupus patients use complementary medicine. Resveratrol is a phytoalexin with various pharmacological properties. We hypothesised that prophylactic treatment with resveratrol may abrogate manifestations in pristane-induced murine model of lupus-like disease and piperine; a bio-enhancer of resveratrol may enhance these properties. The prophylactic effect of resveratrol (25 mg/kg body weight: P-Res) alone and in combination with piperine (2.5 mg/kg body weight: P-RP) were assessed. P-Res and P-RP were equally efficient in mitigating oxidative stress (enzyme activity of catalase, superoxide dismutase, glutathione peroxidase and level of reduced glutathione, lipid peroxidation, and reactive oxygen species). Inflammation is associated with an increase in inflammatory cytokines. IL-6 was decreased by 71.60% with P-Res, and TNF-α was reduced by 59.70% with P-Res and 62.66% with P-RP (p < 0.05). Prevention of renal pathologies was evident by reduction in creatinine level by P-RP (p < 0.05) and abrogation of proteinuria (P-Res and P-RP). P-RP was efficient in restoring histopathology of liver and lungs and decreased immune complexes in lungs. P-Res proved more beneficial by extenuating lipogranulomas, histopathological manifestations in kidney, liver, and lungs, and eliminating immune complexes in liver and lungs. None of the treatments could regulate auto-antibody formation. Resveratrol decreases the susceptibility of developing pathogenesis in murine model of lupus-like disease. The results also conclude that addressing the bioavailability of resveratrol using it in combination with piperine does not prove more efficacious in preventing lupus-associated pathologies than resveratrol alone.

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References

  • Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    CAS  PubMed  Google Scholar 

  • Choi J, Kim ST, Craft J (2012) The pathogenesis of systemic lupus erythematosus-an update. Curr Opin Immunol 24:651–657

    Article  CAS  Google Scholar 

  • Chowdhary VR, Grande JP, Luthra HS, David CS (2007) Characterization of haemorrhagic pulmonary capillaritis: another manifestation of Pristane-induced lupus. Rheumatology 46:1405–1410

    Article  CAS  Google Scholar 

  • Du Y, Sanam S, Kate K, Mohan C (2015) Animal models of lupus and lupus nephritis. Curr Pharm Des 21:2320–2349

    Article  CAS  Google Scholar 

  • Faghihzadeh F, Hekmatdoost A, Adibi P (2015) Resveratrol and liver: a systematic review. J Res Med Sci 20:797–810

    Article  CAS  Google Scholar 

  • Fava A, Petri M (2019) Systemic lupus erythematosus: diagnosis and clinical management. J Autoimmun 96:1–13

    Article  Google Scholar 

  • Fischer AH, Jacobson KA, Rose J, Zeller R (2008) Hematoxylin and eosin staining of tissue and cell sections. CSH Protoc. https://doi.org/10.1101/pdb.prot4986

    Article  PubMed  Google Scholar 

  • Greco CM, Nakajima C, Manzi S (2013) Updated review of complementary and alternative medicine treatments for systemic lupus erythematosus. Curr Rheumatol Rep 15:378. https://doi.org/10.1007/s11926-013-0378-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kono Y (1978) Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186:189–195

    Article  CAS  Google Scholar 

  • Lightfoot YL, Blanco LP, Kaplan MJ (2017) Metabolic abnormalities and oxidative stress in lupus. Curr Opin Rheumatol 29:442–449

    Article  CAS  Google Scholar 

  • Luck H (1954) Quantitative determination of catalase activity of biological material. Enzymologia 17:31–40

    CAS  PubMed  Google Scholar 

  • Manson JJ, Rahman A (2006) Systemic lupus erythematosus. Orphanet J Rare Dis 1:1750–1172

    Article  Google Scholar 

  • Mok CC, Lau CS (2003) Pathogenesis of systemic lupus erythematosus. J Clin Pathol 56:481–490

    Article  CAS  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(158–169):12

    Google Scholar 

  • Pannu N, Bhatnagar A (2019a) Oxidative stress and immune complexes: pathogenic mechanisms in pristane induced murine model of lupus. Immunobiology. https://doi.org/10.1016/j.imbio.2019.11.006

    Article  PubMed  Google Scholar 

  • Pannu N, Bhatnagar A (2019b) Combinatorial therapeutic effect of resveratrol and piperine on murine model of systemic lupus erythematosus. Inflammopharmacology 15:019–00662

    Google Scholar 

  • Pannu N, Bhatnagar A (2019c) Resveratrol: from enhanced biosynthesis and bioavailability to multitargeting chronic diseases. Biomed Pharmacother 109:2237–2251. https://doi.org/10.1016/j.biopha.2018.11.075

    Article  CAS  PubMed  Google Scholar 

  • Perry D, Sang A, Yin Y, Zheng YY, Morel L (2011) Murine models of systemic lupus erythematosus. J Biomed Biotechnol 271694:14

    Google Scholar 

  • Reeves WH, Lee PY, Weinstein JS, Satoh M, Lu L (2009) Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol 30:455–464

    Article  CAS  Google Scholar 

  • Salehi B et al (2018) Resveratrol: a double-edged sword in health benefits. Biomedicines 6:91

    Article  CAS  Google Scholar 

  • Sharma P, Huq AU, Singh R (2014) Cypermethrin-induced reproductive toxicity in the rat is prevented by resveratrol J Hum. Reprod Sci 7:99–106

    CAS  Google Scholar 

  • Shortman K, Williams N, Adams P (1972a) Simple procedures for the removal of cell debris. Damaged cells and erythroid cells from lymphoid cell suspensions. J Immunol Methods 1:273–287

    Article  CAS  Google Scholar 

  • Shortman K, Williams N, Adams P (1972b) The separation of different cell classes from lymphoid organs. V. Simple procedures for the removal of cell debris. Damaged cells and erythroid cells from lymphoid cell suspensions. J Immunol Methods 1:273–287

    Article  CAS  Google Scholar 

  • Skogh T, Blomhoff R, Eskild W, Berg T (1985) Hepatic uptake of circulating IgG immune complexes. Immunology 55:585–594

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith DL, Dong X, Du S, Oh M, Singh RR, Voskuhl RR (2007) A female preponderance for chemically induced lupus in SJL/J mice. Clin Immunol 122:101–107

    Article  CAS  Google Scholar 

  • Talaat RM, Mohamed SF, Bassyouni IH, Raouf AA (2015) Th1/Th2/Th17/Treg cytokine imbalance in systemic lupus erythematosus (SLE) patients: correlation with disease activity. Cytokine 72:146–153

    Article  CAS  Google Scholar 

  • Wang ZL et al (2014) Resveratrol possesses protective effects in a pristane-induced lupus mouse model. PLoS One 9:e114792

    Article  Google Scholar 

  • Zhong M, Cheng GF, Wang WJ, Guo Y, Zhu XY, Zhang JT (1999) Inhibitory effect of resveratrol on interleukin 6 release by stimulated peritoneal macrophages of mice. Phytomedicine 6:79–84

    Article  CAS  Google Scholar 

  • Zhu XD, Lei XP, Dong WB (2017) Resveratrol as a potential therapeutic drug for respiratory system diseases. Drug Des Devel Ther 11:3591–3598

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by University Grant Commission-Basic Scientific Research (UGC-BSR) [Grant number: F4-1/2006(BSR)/7–209/2009(BSR)], The Department of Science & Technology—Promotion of University Research and Scientific Excellence (DST-PURSE), and University Grants Commission- Special Assistance Programme (UGC-SAP).

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  1. Panjab University, Chandigarh, India

    Naveet Pannu & Archana Bhatnagar

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  1. Naveet Pannu
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  2. Archana Bhatnagar
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Correspondence to Archana Bhatnagar.

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Pannu, N., Bhatnagar, A. Prophylactic effect of resveratrol and piperine on pristane-induced murine model of lupus-like disease. Inflammopharmacol 28, 719–735 (2020). https://doi.org/10.1007/s10787-020-00717-3

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