Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Protective effect of Macleaya cordata isoquinoline alkaloids on lipopolysaccharide-induced liver injury in broilers

  • Jiaxin Chen (Department of Animal Science, Qingdao Agricultural University) ;
  • Weiren Yang (Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science and Veterinary Medicine, Shandong Agricultural University) ;
  • Hua Liu (College of Animal Science and Technology, Hunan Agriculture University) ;
  • Jiaxing Niu (Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science and Veterinary Medicine, Shandong Agricultural University) ;
  • Yang Liu (Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science and Veterinary Medicine, Shandong Agricultural University) ;
  • Qun Cheng (Department of Animal Science, Qingdao Agricultural University)
  • Received : 2023.07.14
  • Accepted : 2023.09.18
  • Published : 2024.01.01
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Abstract

Objective: This experiment aimed to explore the protective action of dietary supplementation with isoquinoline alkaloids (IA) from Macleaya cordata on lipopolysaccharide (LPS)-induced liver injury in broilers. Methods: Total 216 healthy broilers were selected in a 21-d trial and assigned randomly to the following 3 treatments: control (CON) group, LPS group, and LPS+IA group. The CON and LPS groups were provided with a basal diet, whereas the LPS+IA group received the basal diet supplemented with 0.6 mg/kg Macleaya cordata IA. Broilers in LPS and LPS+IA groups were intraperitoneally injected with LPS (1 mg/kg body weight) at 17, 19, and 21 days of age, while those in CON group were injected with equivalent amount of saline solution. Results: Results showed LPS injection caused systemic and liver inflammation in broilers, inhibited immune function, and ultimately lead to liver injury. By contrast, supplementation of IA ameliorated LPS-induced adverse change in serum parameters, boosted immunity in LPS+IA group. Furthermore, IA suppressed the elevation of hepatic inflammatory cytokines and caspases levels induced by LPS, as well as the expressions of genes related to the toll-like receptor 4 (TLR4)/myeloid differentiation primary response 88 (MyD88)/nuclear factor-kappa B (NF-κB) pathway. Conclusion: Dietary inclusion of 0.6 mg/kg Macleaya cordata IA could enhance immune function of body and inhibit liver damage via inactivating TLR4/MyD88/NF-κB signaling pathway in broilers.

Keywords

Acknowledgement

This research was funded by Qingdao Agricultural University Doctoral Start-Up Fund (grant number XJ2023000401) and Shandong Province Poultry Industry and Technology System (grant number SDAIT-11-14).

References

  1. Racanelli V, Rehermann B. The liver as an immunological organ. Hepatology 2006;43:S54-62. https://doi.org/10.1002/hep.21060 
  2. Wang Q, Niu J, Liu Y, et al. Supplementation of paraformic acid as a substitute for antibiotics in the diet improves growth performance and liver health in broiler chickens. Animals (Basel) 2022;12:2825. https://doi.org/10.3390/ani12202825 
  3. Almazroo OA, Miah MK, Venkataramanan R. Drug metabolism in the liver. Clin Liver Dis 2017;21:1-20. https://doi.org/10.1016/j.cld.2016.08.001 
  4. Mei W, Hao Y, Xie H, Ni Y, Zhao R. Hepatic Inflammatory response to exogenous LPS challenge is exacerbated in broilers with fatty liver disease. Animals (Basel) 2020;10:514. https://doi.org/10.3390/ani10030514 
  5. Adachi Y, Moore LE, Bradford BU, Gao W, Thurman RG. Antibiotics prevent liver injury in rats following long-term exposure to ethanol. Gastroenterology 1995;108:218-24. https://doi.org/10.1016/0016-5085(95)90027-6 
  6. Singer RS, Finch R, Wegener HC, Bywater R, Walters J, Lipsitch M. Antibiotic resistance-the interplay between antibiotic use in animals and human beings. Lancet Infect Dis 2003;3:47-51. https://doi.org/10.1016/S1473-3099(03)00490-0 
  7. Liu Y, Li Y, Niu J, et al. Effects of dietary Macleaya cordata extract containing isoquinoline alkaloids supplementation as an alternative to antibiotics in the diets on growth performance and liver health of broiler chickens. Front Vet Sci 2022;9:950174. https://doi.org/10.3389/fvets.2022.950174 
  8. Kosina P, Gregorova J, Gruz J, et al. Phytochemical and antimicrobial characterization of Macleaya cordata herb. Fitoterapia 2010;81:1006-12. https://doi.org/10.1016/j.fitote.2010.06.020 
  9. Ni H, Martinez Y, Guan G, et al. Analysis of the impact of isoquinoline alkaloids, derived from Macleaya cordata extract, on the development and innate immune response in swine and poultry. Biomed Res Int 2016;2016:1352146. https://doi.org/10.1155/2016/1352146 
  10. Kantas D, Papatsiros VG, Tassis PD, Athanasiou LV, Tzika ED. The effect of a natural feed additive (Macleaya cordata), containing sanguinarine, on the performance and health status of weaning pigs. Anim Sci J 2015;86:92-8. https://doi.org/10.1111/asj.12240 
  11. Guo S, Lei J, Liu L, et al. Effects of Macleaya cordata extract on laying performance, egg quality, and serum indices in Xuefeng black-bone chicken. Poult Sci 2021;100:101031. https://doi.org/10.1016/j.psj.2021.101031 
  12. Liu H, Lin Q, Liu X, et al. Effects of dietary Bopu powder supplementation on serum antioxidant capacity, egg quality, and intestinal microbiota of laying hens. Front Physiol 2022;13:902784. https://doi.org/10.3389/fphys.2022.902784 
  13. Liu Y, Wang Q, Liu H, et al. Effects of dietary Bopu powder supplementation on intestinal development and microbiota in broiler chickens. Front Microbiol 2022;13:1019130. https://doi.org/10.3389/fmicb.2022.1019130 
  14. Li Y, Zhao X, Jiang X, et al. Effects of dietary supplementation with exogenous catalase on growth performance, oxidative stress, and hepatic apoptosis in weaned piglets challenged with lipopolysaccharide. J Anim Sci 2020;98:skaa067. https://doi.org/10.1093/jas/skaa067 
  15. Qu J, Wang W, Zhang Q, Li S. Inhibition of Lipopolysaccharide-induced inflammation of chicken liver tissue by selenomethionine via TLR4-NF-κB-NLRP3 signaling pathway. Biol Trace Elem Res 2020;195:205-14. https://doi.org/10.1007/s12011-019-01841-0 
  16. Huang XY, Ansari AR, Huang HB, et al. Lipopolysaccharide mediates immuno-pathological alterations in young chicken liver through TLR4 signaling. BMC Immunol 2017;18:12. https://doi.org/10.1186/s12865-017-0199-7 
  17. Jiang J, Qi L, Lv Z, Jin S, Wei X, Shi F. Dietary stevioside supplementation alleviates lipopolysaccharide-induced intestinal mucosal damage through anti-inflammatory and antioxidant effects in broiler chickens. Antioxidants (Basel) 2019;8:575. https://doi.org/10.3390/antiox8120575 
  18. Takahashi K, Takimoto T, Sato K, Akiba Y. Effect of dietary supplementation of astaxanthin from Phaffia rhodozyma on lipopolysaccharide-induced early inflammatory responses in male broiler chickens (Gallus gallus) fed a corn-enriched diet. Anim Sci J 2011;82:753-8. https://doi.org/10.1111/j.1740-0929.2011.00898.x 
  19. Chen J, Li F, Yang W, Jiang S, Li Y. Comparison of gut microbiota and metabolic status of sows with different litter sizes during pregnancy. Front Vet Sci 2021;8:793174. https://doi.org/10.3389/fvets.2021.793174 
  20. Chen J, Li F, Yang W, Jiang S, Li Y. Supplementation with exogenous catalase from Penicillium notatum in the diet ameliorates Lipopolysaccharide-induced intestinal oxidative damage through affecting intestinal antioxidant capacity and microbiota in weaned pigs. Microbiol Spectr 2021;9:e00654-21. https://doi.org/10.1128/Spectrum.00654-21 
  21. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008;3:1101-8. https://doi.org/10.1038/nprot.2008.73 
  22. Kim WR, Flamm SL, Di Bisceglie AM, Bodenheimer HC. Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology 2008;47:1363-70. https://doi.org/10.1002/hep.22109 
  23. Senior JR. Alanine aminotransferase: a clinical and regulatory tool for detecting liver injury-past, present, and future. Clin Pharmacol Ther 2012;92:332-9. https://doi.org/10.1038/clpt.2012.108 
  24. Delanghe JR, Speeckaert R, Speeckaert MM. Complement C3 and its polymorphism: biological and clinical consequences. Pathology 2014;46:1-10. https://doi.org/10.1097/PAT.0000000000000042 
  25. Qin X, Gao B. The complement system in liver diseases. Cell Mol Immunol 2006;3:333-40. 
  26. Thorgersen EB, Barratt-Due A, Haugaa H, et al. The role of complement in liver injury, regeneration, and transplantation. Hepatology 2019;70:725-36. https://doi.org/10.1002/hep.30508 
  27. Zhang QY, Guo J, Xu L, et al. Salvianolic acid A alleviates lipopolysaccharide-induced disseminated intravascular coagulation by inhibiting complement activation. BMC Complement Med Ther 2022;22:245. https://doi.org/10.1186/s12906-022-03720-z 
  28. Li MF, Zhang HQ. An overview of complement systems in teleosts. Dev Comp Immunol 2022;137:104520. https://doi.org/10.1016/j.dci.2022.104520 
  29. Lin C, Lei B, Dong C, et al. Complement inhibition alleviates donor brain death-induced liver injury and posttransplant cascade injury by regulating phosphoinositide 3-kinase signaling. Am J Transplant 2023;23:484-97. https://doi.org/10.1016/j.ajt.2023.01.019 
  30. Bell CC, Hendriks DFG, Moro SML, et al. Characterization of primary human hepatocyte spheroids as a model system for drug-induced liver injury, liver function and disease. Sci Rep 2016;6:25187. https://doi.org/10.1038/srep25187 
  31. Korhonen H, Marnila P, Gill HS. Milk immunoglobulins and complement factors. Br J Nutr 2000;84 (Suppl 1):S75-80. https://doi.org/10.1017/S0007114500002282 
  32. Liu J, Wang Y, Xiong E, et al. Role of the IgM Fc receptor in immunity and tolerance. Front Immunol 2019;10:529. https://doi.org/10.3389/fimmu.2019.00529 
  33. Aschermann S, Lux A, Baerenwaldt A, Biburger M, Nimmerjahn F. The other side of immunoglobulin G: suppressor of inflammation. Clin Exp Immunol 2010;160:161-7. https://doi.org/10.1111/j.1365-2249.2009.04081.x 
  34. Isho B, Florescu A, Wang AA, Gommerman JL. Fantastic IgA plasma cells and where to find them. Immunol Rev 2021;303:119-37. https://doi.org/10.1111/imr.12980 
  35. Umaya SR, Vijayalakshmi YC, Sejian V. Exploration of plant products and phytochemicals against aflatoxin toxicity in broiler chicken production: Present status. Toxicon 2021;200:55-68. https://doi.org/10.1016/j.toxicon.2021.06.017 
  36. Barter P, Gotto AM, LaRosa JC, et al. HDL cholesterol, very low levels of LDL cholesterol, and cardiovascular events. N Engl J Med 2007;357:1301-10. https://doi.org/10.1056/NEJMoa064278 
  37. Wolf D, Ley K. Immunity and inflammation in atherosclerosis. Circ Res 2019;124:315-27. https://doi.org/101161/circresaha118313591  101161/circresaha118313591
  38. Lopez-Castejon G, Brough D. Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev 2011;22:189-95. https://doi.org/10.1016/j.cytogfr.2011.10.001 
  39. King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol 2008;79:1527-34. https://doi.org/101902/jop2008080246  101902/jop2008080246
  40. Ding WX, Yin XM. Dissection of the multiple mechanisms of TNF-alpha-induced apoptosis in liver injury. J Cell Mol Med 2004;8:445-54. https://doi.org/10.1111/j.1582-4934.2004.tb00469.x 
  41. Esmailbeig M, Ghaderi A. Interleukin-18: a regulator of cancer and autoimmune diseases. Eur Cytokine Netw 2017;28:127-40. https://doi.org/10.1684/ecn.2018.0401 
  42. Wallenius V, Wallenius K, Hisaoka M, et al. Retarded liver growth in interleukin-6-deficient and tumor necrosis factor receptor-1-deficient mice. Endocrinology 2001;142:2953-60. https://doi.org/10.1210/endo.142.7.8270 
  43. Liu X, Pan Z, Su D, et al. Remifentanil ameliorates liver ischemia-reperfusion injury through inhibition of interleukin-18 signaling. Transplantation 2015;99:2109-17. https://doi.org/10.1097/TP.0000000000000737 
  44. Kumar R, Ng S, Engwerda C. The role of IL-10 in malaria: a double edged sword. Front Immunol 2019;10:229. https://doi.org/10.3389/fimmu.2019.00229 
  45. Treffkorn L, Scheibe R, Maruyama T, Dieter P. PGE2 exerts its effect on the LPS-induced release of TNF-alpha, ET-1, IL-1alpha, IL-6 and IL-10 via the EP2 and EP4 receptor in rat liver macrophages. Prostaglandins Other Lipid Mediat 2004;74:113-23. https://doi.org/10.1016/j.prostaglandins.2004.07.005 
  46. Jndoyan ZT, Bablumyan AY, Ginosyan KV, Shekoyan SV. Correlations between indicators of interleukin-10 and interleukin-6 in patients with periodic disease. Ter Arkh 2018;90:38-41. https://doi.org/10.26442/terarkh201890338-41 
  47. Kuzmich NN, Sivak KV, Chubarev VN, Porozov YB, Savateeva-Lyubimova TN, Peri F. TLR4 signaling pathway modulators as potential therapeutics in inflammation and sepsis. Vaccines (Basel) 2017;5:34. https://doi.org/10.3390/vaccines5040034 
  48. Kong F, Ye B, Lin L, Cai X, Huang W, Huang Z. Atorvastatin suppresses NLRP3 inflammasome activation via TLR4/MyD88/NF-κB signaling in PMA-stimulated THP-1 monocytes. Biomed Pharmacother 2016;82:167-72. https://doi.org/10.1016/j.biopha.2016.04.043 
  49. Blevins HM, Xu Y, Biby S, Zhang S. The NLRP3 inflammasome pathway: A review of mechanisms and inhibitors for the treatment of inflammatory diseases. Front Aging Neurosci 2022;14:879021. https://doi.org/10.3389/fnagi.2022.879021 
  50. Bai B, Yang Y, Wang Q, et al. NLRP3 inflammasome in endothelial dysfunction. Cell Death Dis 2020;11:776. https://doi.org/10.1038/s41419-020-02985-x 
  51. Lalier L, Cartron PF, Juin P, et al. Bax activation and mitochondrial insertion during apoptosis. Apoptosis 2007;12:887-96. https://doi.org/101007/s10495-007-0749-1  101007/s10495-007-0749-1
  52. Tsujimoto Y. Role of Bcl-2 family proteins in apoptosis: apoptosomes or mitochondria? Genes Cells 1998;3:697-707. https://doi.org/10.1046/j.1365-2443.1998.00223.x 
  53. Wu M, Liu X, Chen H, et al. Activation of pyroptosis by membrane-anchoring AIE photosensitizer design: New prospect for photodynamic cancer cell ablation. Angew Chem Int Ed 2021;60:9093-8. https://doi.org/10.1002/anie.202016399 
  54. Lei Q, Huang X, Zheng L, et al. Biosensors for Caspase-3: From chemical methodologies to biomedical applications. Talanta 2022;240:123198. https://doi.org/10.1016/j.talanta.2021.123198