Acremonium terricola culture plays anti-inflammatory and antioxidant roles by modulating MAPK signaling pathways in rats with lipopolysaccharide-induced mastitis

  • Yang Li College of Animal Science and Technology, Northeast Agricultural University, Harbin, China
  • Xin Jiang College of Animal Science and Technology, Northeast Agricultural University, Harbin, China
  • Hongjian Xu College of Animal Science and Technology, Northeast Agricultural University, Harbin, China
  • Jingyi Lv College of Animal Science and Technology, Northeast Agricultural University, Harbin, China
  • Guangning Zhang College of Animal Science and Technology, Northeast Agricultural University, Harbin, China
  • Xiujing Dou College of Animal Science and Technology, Northeast Agricultural University, Harbin, China
  • Yonggen Zhang College of Animal Science and Technology, Northeast Agricultural University, Harbin, China
  • Xiaoxiang Li Microbial Biological Engineering Company Limited, Hefei, China
DOI: https://doi.org/10.29219/fnr.v64.3649
Keywords: Acrermonium terricola culture; mastitis; anti-inflammation; antioxidant

Abstract

Background: As a major disease affecting dairy cow production worldwide, bovine mastitis is caused by a variety of pathogenic microorganisms that eventually cause mammary gland inflammation. Acremonium terricola culture (ATC) is a new type of affordable feed additive produced by the solid fermentation of A. terricola isolated from Cordyceps gunnii and exerted its anti-inflammatory effect.

Objectives: To evaluate the protective effects of ATC on mastitis and investigate its active mechanism, a lipopolysaccharide (LPS)-induced rat mastitis model was used in two experiments.

Design: In Experiment 1, a total of 40 female Sprague–Dawley rats were used to determine the optimal supplementary dose of ATC via gavage trial. In Experiment 2, we examined the effects of an optimal dose of ATC on LPS-induced mastitis in rats.

Results: The results of Experiment 1 showed that administration of ATC improved growth performance and antioxidant functions in the serum and the liver, as well as immunoglobulin A, G, and M levels in rat serum, and it decreased the content of alanine aminotransferase, aspartate aminotransferase, triglyceride, cholesterol, low-density lipoprotein, and serum urea nitrogen in rat serum; a dosage of 250–1,250 mg/kg/day was shown to be high enough to be effective. The results of Experiment 2 indicated that ATC can relieve the inflammatory reaction of mammary glands in rats, and the LPS-induced expression of tumor necrosis factor-α, interleukin-1β, interleukin-6, and inducible nitric oxide synthase significantly decreased after ATC treatment. Moreover, our results demonstrated that ATC markedly enhanced the activity of antioxidase in this rat mastitis model. The results of Western blot analysis revealed that ATC could suppress the expression of toll-like receptor 4, phosphorylation of extracellular signal-regulated kinase, and activity of c-Jun N-terminal kinase in the LPS-stimulated mastitis model.

Conclusion: Taken together, ATC was shown to exert its anti-inflammatory effect by blocking mitogen-activated protein kinase signaling pathways. These results demonstrate that ATC exerts anti-inflammatory and antioxidant effects in mastitis prevention.

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References


  1. Bradley A. Bovine mastitis: an evolving disease. Vet J 2002; 164(2): 116–28. doi: 10.1053/tvjl.2002.0724

  2. Halasa T, Huijps K, Østerås O, Hogeveen H. Economic effects of bovine mastitis and mastitis management: a review. Vet Quart 2007; 29(1): 18–31. doi: 10.1080/01652176.2007.9695224

  3. Song X, Zhang W, Wang T, Jiang H, Zhang Z, Fu Y, et al. Geniposide plays an anti-inflammatory role via regulating TLR4 and downstream signaling pathways in lipopolysaccharide-induced mastitis in mice. Inflammation 2014; 37(5): 1588–98. doi: 10.1007/s10753-014-9885-2

  4. Guo M, Zhang N, Li D, Liang D, Liu Z, Li F, et al. Baicalin plays an anti-inflammatory role through reducing nuclear factor-κB and p38 phosphorylation in S. aureus-induced mastitis. Int Immunopharmacol 2013; 16(2): 125–30. doi: 10.1016/j.intimp.2013.03.006

  5. Wang ZM, Peng X, Lee KLD, Tang JCO, Cheung PCK, Wu JY. Structural characterisation and immunomodulatory property of an acidic polysaccharide from mycelial culture of Cordyceps sinensis fungus Cs-HK1. J Dairy Sci 2011; 125: 637–43. doi: 10.1016/j.foodchem.2010.09.052

  6. Li Y, Sun YK, Li X, Zhang GN, Xin HS, Xu HJ, et al. Effects of Acremonium terricola culture on performance, milk composition, rumen fermentation and immune functions in dairy cows. Anim Feed Sci Tech 2018; 240: 40–51. doi: 10.1016/j.anifeedsci.2018.03.015

  7. Li Y, Wang YZ, Ding X, Zhang YG, Xue SC, Lin C, et al. Effects of Acremonium terricola culture on growth performance, antioxidant status and immune functions in weaned calves. Livestock Sci 2016; 193: 66–70. doi: 10.1016/j.livsci.2016.09.009

  8. Jinwoo J, Jin CY, Giyoung K, Jaedong L, Cheol P, Gundo K, et al. Anti-inflammatory effects of cordycepin via suppression of inflammatory mediators in BV2 microglial cells. Int Immunopharmacol 2010; 10(12): 1580–6. doi: 10.1016/j.intimp.2010.09.011

  9. Notebaert S, Meyer E. Mouse models to study the pathogenesis and control of bovine mastitis. A review. Vet Quart 2006; 28(1): 2–13. doi: 10.1080/01652176.2006.9695201

  10. Chandler RL. Experimental bacterial mastitis in the mouse. J Med Microbiol 1970; 3(2): 273–82. doi: 10.1099/00222615-3-2-273

  11. Breyne K, Vliegher SD, Visscher AD, Piepers S, Meyer E. Technical note: a pilot study using a mouse mastitis model to study differences between bovine associated coagulase-negative staphylococci. J Dairy Sci 2015; 98(2): 1090–100. doi: 10.3168/jds.2014-8699

  12. Tsukamoto H, Takeuchi S, Kubota K, Kobayashi Y, Kozakai S, Ukai I, et al. Lipopolysaccharide (LPS)-binding protein stimulates CD14-dependent toll-like receptor 4 internalization and LPS-induced TBK1–IKKϵ–IRF3 axis activation. J Biol Chem 2018; 293: 10186–201. doi: 10.1074/jbc.M117.796631

  13. Fan MZ, Huang B, Li CR, Li ZZ. A new record species of the genus Acremonium from China. Mycosystema 1999; 18: 449.

  14. Zhang GL, Jiang L, Yan Q, Liu RH, Zhang L. Anti-tumor effect of matrine combined with cisplatin on rat models of cervical cancer. Asian Pac J Trop Med 2015; 8(12): 1055–9. doi: 10.1016/j.apjtm.2015.11.005

  15. Chang CY, Lue MY, Pan TM. Determination of adenosine, cordycepin and ergosterol contents in cultivated Antrodia camphorata by HPLC method. J Food Drug Anal 2005; 13(4): 338–42. doi: 10.38212/2224-6614.2569

  16. AOAC, 2000. Official Methods of Analysis, 17th ed. Association of Official Analytical Chemist, Arlington, VA, USA.

  17. Dou XJ, Gao N, Lan J, Han JL, Yang Y, Shan AS. TLR2/EGFR are two sensors for pBD3 and pEP2C induction by sodium butyrate independent of HDAC inhibition. J Agric Food Chem 2020; 68: 512–522. doi: 10.1021/acs.jafc.9b06569

  18. Wang JG. Effects of fermentation products of on growth performance and bone mineralization of broiler chicks. J Appl Anim Res 2015; 43(2): 236–41. doi: 10.1080/09712119.2014.928630

  19. Wang CL, Chiang CJ, Chao YP, Yu B, Lee TT. Effect of Cordyceps militaris waster medium on production performance, egg traits and egg yolk cholesterol of laying hens. J Poultry Sci 2015; 52(3): 188–96. doi: 10.2141/jpsa.0140191

  20. Deng B, Wang ZP, Tao WJ, Li WF, Wang C, Wang MQ, et al. Effects of polysaccharides from mycelia of Cordyceps sinensis on growth performance, immunity and antioxidant indicators of the white shrimp Litopenaeus vannamei. Aquacult Nutr 2015; 21(2): 173–9. doi: 10.1111/anu.12147

  21. Ahn YJ, Park SJ, Lee SG, Shin SC, Choi DH. CordycepIn: selective growth inhibitor derived from liquid culture of Cordyceps militaris against Clostridium spp. J Agric Food Chem 2000; 48(7): 2744–8. doi: 10.1021/jf990862n

  22. Xiao JH, Liang ZQ, Liu AY, Chen DX, Xiao Y, Liu JW, et al. Immunosuppressive activity of polysaccharides from Cordyceps gunnii mycelia in mice in vivo/vitro. J Food Agric Environ 2004; 2(3–4): 69–73.

  23. Koh JH, Suh HJ, Ahn TS. Hot-water extract from mycelia of Cordyceps sinensis as a substitute for antibiotic growth promoters. Biotechnol Lett 2003; 25(7): 585–90. doi: 10.1023/A:1022893000418

  24. Ko WS, Hsu SL, Chyau CC, Chen KC, Peng RY. Compound Cordyceps TCM-700C exhibits potent hepatoprotective capability in animal model. Fitoterapia 2010; 81(1): 1–7. doi: 10.1016/j.fitote.2009.06.018

  25. Haneul C, Yanghee J, Minjoo K, Minjeong S, Kang BW, Yongkee J, et al. Cordyceps militaris alleviates non-alcoholic fatty liver disease in ob/ob mice. Nutr Res Pract 2014; 8(2): 172–6. doi: 10.4162/nrp.2014.8.2.172

  26. Ademuyiwa O, Ugbaja RN, Idumebor F, Adebawo O. Plasma lipid profiles and risk of cardiovascular disease in occupational lead exposure in Abeokuta, Nigeria. Lipids Health Dis 2005; 4(1): 19. doi: 10.1186/1476-511X-4-19

  27. Kiho T, Yamane A, Hui J, Usui S, Ukai S. Polysaccharides in fungi. XXXVI. Hypoglycemic activity of a polysaccharide (CS-F30) from the cultural mycelium of Cordyceps sinensis and its effect on glucose metabolism in mouse liver. Biol Pharmaceut Bull 1996; 19(2): 294–6. doi: 10.1248/bpb.19.294

  28. Park JH, Park NS, Sang ML, Park E. Effect of Dongchunghacho rice on blood glucose level, lipid profile, and antioxidant metabolism in streptozotocin-induced diabetic rats. Food Sci Biotechnol 2011; 20(4): 933–40. doi: 10.1007/s10068-011-0129-z

  29. Kalkan Y, Kapakin KA, Kara A, Atabay T, Karadeniz A, Simsek N, et al. Protective effect of Panax ginseng against serum biochemical changes and apoptosis in kidney of rats treated with gentamicin sulphate. J Mol Histol 2012; 43(5): 603–13. doi: 10.1007/s10735-012-9412-4

  30. Li Y, Xue WJ, Tian PX, Ding XM, Yan H, Pan XM, et al. Clinical application of Cordyceps sinensis on immunosuppressive therapy in renal transplantation. Transplant P 2009; 41(5): 1565–9. doi: 10.1016/j.transproceed.2009.02.085

  31. Chae SW, Mitsunaga F, Jung SJ, Ha KC, Sin HS, Jang SH, et al. Nutrigenomic study on immunomodulatory function of mycelium extract (Paecilomyces hepiali) in mitomycin C-treated mice. Food Nutr Sci 2014; 5(22): 2217–24. doi: 10.4236/fns.2014.522235

  32. Liu JY, Feng CP, Li X, Chang MC, Meng JL, Xu LJ. Immunomodulatory and antioxidative activity of Cordyceps militaris polysaccharides in mice. Int J Biol Macromol 2016; 86: 594–8. doi: 10.1016/j.ijbiomac.2016.02.009

  33. Wu Y, Sun H, Qin F, Pan Y, Sun C. Effect of various extracts and a polysaccharide from the edible mycelia of Cordyceps sinensis on cellular and humoral immune response against ovalbumin in mice. Phytother Res 2006; 20(8): 646–52. doi: 10.1002/ptr.1921

  34. Yamaguchi Y, Kagota S, Nakamura K, Shinozuka K, Kunitomo M. Antioxidant activity of the extracts from fruiting bodies of cultured Cordyceps sinensis. Phytother Res 2015; 14(8): 647–9. doi: 10.1002/1099-1573(200012)14:8%3C647::AID-PTR670%3E3.0.CO;2-W

  35. Wang M, Meng XY, Yang RL, Qin T, Wang XY, Zhang KY, et al. Cordyceps militaris polysaccharides can enhance the immunity and antioxidation activity in immunosuppressed mice. Carbohyd Polym 2012; 89(2): 461–6. doi: 10.1016/j.carbpol.2012.03.029

  36. Cha JY, Ahn HY, Cho YS, Je JY. Protective effect of cordycepin-enriched Cordyceps militaris on alcoholic hepatotoxicity in Sprague-Dawley rats. Food Chem Toxicol 2013; 60(10): 52–7. doi: 10.1016/j.fct.2013.07.033

  37. Wu R, Gao JP, Wang HL, Gao Y, Wu Q, Cui XH. Effects of fermented Cordyceps sinensis on oxidative stress in doxorubicin treated rats. Pharmacogn Mag 2015; 11(44): 724–31. doi: 10.4103/0973-1296.165562

  38. Yuan P, Qian C, Tao Y, Tao Y, Xiong L, Liu C. Cultured mycelium Cordyceps sinensis protects liver sinusoidal endothelial cells in acute liver injured mice. Mol Biol Rep 2014; 41(3): 1815–27. doi: 10.1007/s11033-014-3031-y

  39. Chiu CH, Chyau CC, Chen CC, Lin CH, Cheng CH, Mong MC. Polysaccharide extract of Cordyceps sobolifera attenuates renal injury in endotoxemic rats. Food Chem Toxicol Int J 2014; 69: 281–8. doi: 10.1016/j.fct.2014.04.009

  40. Zhang J, Yu Y, Zhang Z, Ding Y, Dai X, Li Y. Effect of polysaccharide from cultured Cordyceps sinensis on immune function and anti-oxidation activity of mice exposed to 60Co. Int Immunopharmacol 2011; 11(12): 2251–7. doi: 10.1016/j.intimp.2011.09.019

  41. Rainard P, Riollet C. Innate immunity of the bovine mammary gland. Vet Res 2015; 37(3): 369–400. doi: 10.1051/vetres:2006007

  42. Moore EE, Presnell S, Garrigues U, Guilbot A, Leguern E, Smith D, et al. Expression of IL-17B in neurons and evaluation of its possible role in the chromosome 5q-linked form of Charcot-Marie-Tooth disease. Neuromuscular Disord 2002; 12(2): 141–50. doi: 10.1016/S0960-8966(01)00250-4

  43. Liu WF, Huang S, Li YL, Zhang K, Zheng X. Suppressive effect of glycyrrhizic acid against lipopolysaccharide-induced neuroinflammation and cognitive impairment in C57 mice via toll-like receptor 4 signaling pathway. Food Nutr Res 2019; 63: 1516. doi: 10.29219/fnr.v63.1516

  44. Triantafilou M, Triantafilou K. The dynamics of LPS recognition: complex orchestration of multiple receptors. J Endotoxin Res 2005; 11(1): 5–11. doi: 10.1179/096805105225006641

  45. Zhong W, Chi G, Jiang L, Soromou LW, Chen N, Huo M, et al. p-Cymene modulates in vitro and in vivo cytokine production by inhibiting MAPK and NF-κB activation. Inflammation 2013; 36(3): 529–37. doi: 10.1007/s10753-012-9574-y

Published
2020-11-13
How to Cite
Li Y., Jiang X., Xu H., Lv J., Zhang G., Dou X., Zhang Y., & Li X. (2020). <em>Acremonium terricola</em&gt; culture plays anti-inflammatory and antioxidant roles by modulating MAPK signaling pathways in rats with lipopolysaccharide-induced mastitis. Food & Nutrition Research, 64. https://doi.org/10.29219/fnr.v64.3649
Issue
Vol 64 (2020)
Section
Original Articles

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