Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Effect of Lactobacillus Fermentation on the Anti-Inflammatory Potential of Turmeric

  • Received : 2019.06.14
  • Accepted : 2019.08.10
  • Published : 2019.10.28
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Abstract

Curcumin, the major bioactive constituent of turmeric, has been reported to have a wide range of pharmacological benefits; however, the low solubility in water has restricted its systemic bioavailability and therapeutic potential. Therefore, in the current study, we aimed to investigate the effect of turmeric fermentation on its curcumin content and anti-inflammatory activity by using several lactic acid bacteria. Fermentation with Lactobacillus fermentum significantly increased the curcumin content by 9.76% while showing no cytotoxicity in RAW 246.7 cells, as compared to the unfermented turmeric, regardless of the concentration of L. fermentum-fermented turmeric. The L. fermentum-fermented turmeric also promoted cell survival; a significantly higher number of viable cells in lipopolysaccharide (LPS)-induced RAW 264.7 cells were observed as compared to those treated with unfermented turmeric. It also displayed promising DPPH scavenging ($7.88{\pm}3.36%$) and anti-inflammatory activities by significantly reducing the nitrite level and suppressing the expression of the pro-apoptotic tumor necrosis factor-alpha and Toll-like receptor-4 in LPS-induced RAW 264.7 cells. Western blot analysis further revealed that the anti-inflammatory activity of the fermented turmeric was exerted through suppression of the c-Jun N-terminal kinase signal pathway, but not in unfermented turmeric. Taken together, the results suggested that fermentation with lactic acid bacteria increases the curcumin content of turmeric without increasing its cytotoxicity, while strengthening the specific pharmacological activity, thus, highlighting its potential application as a functional food ingredient.

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References

  1. Ammon HP, Wahl MA. 1991. Pharmacology of Curcuma longa. Planta Med. 57: 1-7. https://doi.org/10.1055/s-2006-960004
  2. Hatcher H, Planalp R, Cho J, Torti F, Torti S. 2008. Curcumin: from ancient medicine to current clinical trials. Cell. Mol. Life Sci. 65: 1631-1652. https://doi.org/10.1007/s00018-008-7452-4
  3. Ishrat T, Hoda MN, Khan MB, Yousuf S, Ahmad M, Khan MM, et al. 2009. Amelioration of cognitive deficits and neurodegeneration b y curcumin in r at m odel o f sporadic dementia of Alzheimer's type (SDAT). Eur. Neuropsychopharmacol. 19: 636-647. https://doi.org/10.1016/j.euroneuro.2009.02.002
  4. Ma Q-L, Yang F, Rosario ER, Ubeda OJ, Beech W, Gant DJ, et al. 2009. $\beta$-amyloid oligomers induce phosphorylation of tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling: suppression by omega-3 fatty acids and curcumin. J. Neurosci. 29: 9078-9089. https://doi.org/10.1523/JNEUROSCI.1071-09.2009
  5. Arafa HM. 2005. Curcumin attenuates diet-induced hypercholesterolemia in rats. Med. Sci. Monit. 11: BR228-BR234.
  6. Jin S, Hong J-H, Jung S-H, Cho K-H. 2011. Turmeric and laurel aqueous extracts exhibit in vitro anti-atherosclerotic activity and in vivo hypolipidemic effects in a zebrafish model. J. Med. Food. 14: 247-256. https://doi.org/10.1089/jmf.2009.1389
  7. Polasa K, Raghuram T, Krishna TP, Krishnaswamy K. 1992. Effect of turmeric on urinary mutagens in smokers. Mutagenesis 7: 107-109. https://doi.org/10.1093/mutage/7.2.107
  8. Lampe V, Milobedzka J. 1913. Studien uber curcumin. Ber. Dtsch. Chem. Ges. 46: 2235-2240. https://doi.org/10.1002/cber.191304602149
  9. Chan MM-Y. 1995. Inhibition of tumor necrosis factor by curcumin, a phytochemical. Biochem. Pharmacol. 49: 1551-1556. https://doi.org/10.1016/0006-2952(95)00171-U
  10. Chan MM-Y, Huang H-I, Fenton MR, Fong D. 1998. In vivo inhibition of nitric oxide synthase gene expression by curcumin, a cancer preventive natural product with antiinflammatory properties. Biochem. Pharmacol. 55: 1955-1962. https://doi.org/10.1016/S0006-2952(98)00114-2
  11. Ireson C, Orr S, Jones DJ, Verschoyle R, Lim C-K, Luo J-L, et al. 2001. Characterization of metabolites of the chemopreventive agent curcumin in human and rat hepatocytes and in the rat in vivo, and evaluation of their ability to inhibit phorbol ester-induced prostaglandin E2 production. Cancer Res. 61: 1058-1064.
  12. Gupta S, Abu-Ghannam N. 2012. Probiotic fermentation of plant based products: possibilities and opportunities. Crit. Rev. Food Sci. Nutr. 52: 183-199. https://doi.org/10.1080/10408398.2010.499779
  13. Ho JN, Park SJ, Choue R, Lee J. 2013. Standardized ethanol extract of Curcuma longa L. fermented by Aspergillus oryzae promotes lipolysis via activation of cAMP-dependent PKA in 3T3-L1 adipocytes. J. Food Biochem. 37: 595-603. https://doi.org/10.1111/jfbc.12011
  14. Kim JH, Kim O-K, Yoon H-G, Park J, You Y, Kim K, et al. 2016. Anti-obesity effect of extract from fermented Curcuma longa L. through regulation of adipogenesis and lipolysis pathway in high-fat diet-induced obese rats. Food Nutr. Res. 60: 30428. https://doi.org/10.3402/fnr.v60.30428
  15. Kim SW, Ha KC, Choi EK, Jung SY, Kim MG, Kwon DY, et al. 2013. The effectiveness of fermented turmeric powder in subjects with elevated alanine transaminase levels: a randomised controlled study. BMC Complement. Altern. Med. 13: 58. https://doi.org/10.1186/1472-6882-13-58
  16. Pianpumepong P, Anal AK, Doungchawee G, Noomhorm A. 2012. Study on enhanced absorption of phenolic compounds of Lactobacillus-fermented turmeric (Curcuma longa Linn.) beverages in rats. Int. J. Food Sci. Technol. 47: 2380-2387. https://doi.org/10.1111/j.1365-2621.2012.03113.x
  17. Kim SB, Kang BH, Kwon HS, Kang JH. 2011. Antiinflammatory and antiallergic activity of fermented turmeric by Lactobacillus johnsonii IDCC 9203. Microbiol. Biotechnol. Lett. 39: 266-273.
  18. Tonnesen HH, Karlsen J. 1983. High-performance liquid chromatography of curcumin and related compounds. J. Chromatogr. A. 259: 367-371. https://doi.org/10.1016/S0021-9673(01)88022-5
  19. Liu CF, Tseng KC, Chiang SS, Lee BH, Hsu WH, Pan TM. 2011. Immunomodulatory and antioxidant potential of Lactobacillus exopolysaccharides. J. Sci. Food Agric. 91: 2284-2291. https://doi.org/10.1002/jsfa.4456
  20. Ak T, Gulcin I. 2008. Antioxidant and radical scavenging properties of curcumin. Chem.Biol. Interact. 174: 27-37. https://doi.org/10.1016/j.cbi.2008.05.003
  21. Merrell JG, McLaughlin SW, Tie L, Laurencin CT, Chen AF, Nair LS. 2009. Curcumin-loaded poly ($\varepsilon$-caprolactone) nanofibres: diabetic wound dressing with anti-oxidant and anti-inflammatory properties. Clin. Exp. Pharmacol. Physiol. 36: 1149-1156. https://doi.org/10.1111/j.1440-1681.2009.05216.x
  22. Reddy BV, Sundari JS, Balamurugan E, Menon VP. 2009. Prevention of nicotine and streptozotocin treatment induced circulatory oxidative stress by bis-1, 7-(2-hydroxyphenyl)-hepta-1, 6-diene-3, 5-dione in diabetic rats. Mol. Cell. Biochem. 331: 127-133. https://doi.org/10.1007/s11010-009-0150-1
  23. Aggarwal BB, Sundaram C, Malani N, Ichikawa H. 2007. Curcumin: the Indian solid gold, pp. 1-75. In Aggarwal BB, Surh Y-J, Shishodia S (eds.), The molecular targets and therapeutic uses of curcumin in health and disease, Springer, Massachusetts, USA.
  24. Atsumi T, Fujisawa S, Tonosaki K. 2005. Relationship between intracellular ROS production and membrane mobility in curcumin-and tetrahydrocurcumin-treated human gingival fibroblasts and human submandibular gland carcinoma cells. Oral Dis. 11: 236-242. https://doi.org/10.1111/j.1601-0825.2005.01067.x
  25. Garden OJ, Wigmore SJ. 2007. Curcumin induces heme oxygenase 1 through generation of reactive oxygen species, p38 activation and phosphatase inhibition. Int. J. Mol. Med. 19: 165-172.
  26. Bisht K, Choi WH, Park SY, Chung MK, Koh WS. 2009. Curcumin enhances non-inflammatory phagocytic activity of RAW264.7 cells. Biochem. Biophys. Res. Commun. 379: 632-636. https://doi.org/10.1016/j.bbrc.2008.12.135
  27. Fang W, Bi D, Zheng R, Cai N, Xu H, Zhou R, et al. 2017. Identification and activation of TLR4-mediated signalling pathways by alginate-derived guluronate oligosaccharide in RAW264. 7 macrophages. Sci. Rep. 7: 1663. https://doi.org/10.1038/s41598-017-01868-0
  28. Kanzler H, Barrat FJ, Hessel EM, Coffman RL. 2007. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat. Med. 13: 552-559. https://doi.org/10.1038/nm1589
  29. Vaure C, Liu Y. 2014. A comparative review of toll-like receptor 4 expression and functionality in different animal species. Front. Immunol. 5: 316.
  30. Akdis M, Burgler S, Crameri R, Eiwegger T, Fujita H, Gomez E, et al. 2011. Interleukins, from 1 to 37, and interferon-$\gamma$: receptors, functions, and roles in diseases. J. Allergy Clin. Immunol. 127: 701-721. e770. https://doi.org/10.1016/j.jaci.2010.11.050
  31. Brown K L, C osseau C, Gardy JL, H ancock RE. 2007. Complexities of targeting innate immunity to treat infection. Trends Immunol. 28: 260-266. https://doi.org/10.1016/j.it.2007.04.005
  32. Halliwell B. 1996. Antioxidants in human health and disease. Annu. Rev. Nutr. 16: 33-50. https://doi.org/10.1146/annurev.nu.16.070196.000341
  33. Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, et al. 2002. Two antioxidative lactobacilli strains as promising probiotics. Int. J. Food Microbiol. 72: 215-224. https://doi.org/10.1016/S0168-1605(01)00674-2
  34. Lee HY, Park JH, Seok SH, Baek MW, Kim DJ, Lee KE, et al. 2006. Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show antiobesity effects in diet-induced obese mice. BBA-Mol. Cell Biol. L 1761: 736-744. https://doi.org/10.1016/j.bbalip.2006.05.007
  35. Barclay LRC, Vinqvist MR, Mukai K, Goto H, Hashimoto Y, Tokunaga A, et al. 2000. On the antioxidant mechanism of curcumin: classical methods are needed to determine antioxidant mechanism and activity. Org. Lett. 2: 2841-2843. https://doi.org/10.1021/ol000173t
  36. Hur SJ, Lee SY, Kim YC, Choi I, Kim GB. 2014. Effect of fermentation on the antioxidant activity in plant-based foods. Food Chem. 160: 346-356. https://doi.org/10.1016/j.foodchem.2014.03.112
  37. Albina JE, Cui S, Mateo RB, Reichner JS. 1993. Nitric oxidemediated apoptosis in murine peritoneal macrophages. J. Immunol. 150: 5080-5085.
  38. Allione A, Bernabei P, Bosticardo M, Ariotti S, Forni G, Novelli F. 1999. Nitric oxide suppresses human T lymphocyte proliferation through IFN-$\gamma$-dependent and IFN-$\gamma$-independent induction of apoptosis. J. Immunol. 163: 4182-4191.
  39. Jun CD, Choi BM, Kim HM, Chung HT. 1995. Involvement of protein kinase C during taxol-induced activation of murine peritoneal macrophages. J. Immunol. 154: 6541-6547.
  40. Deng Y, Ren X, Yang L, Lin Y, Wu X. 2003. A JNKdependent pathway is required for $TNF{\alpha}$-induced apoptosis. Cell 115: 61-70. https://doi.org/10.1016/S0092-8674(03)00757-8
  41. Yang X, Khosravi-Far R, Chang HY, Baltimore D. 1997. Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell 89: 1067-1076. https://doi.org/10.1016/S0092-8674(00)80294-9
  42. Seminara AR, Ruvolo PP, Murad F. 2007. LPS/IFN-$\gamma$-induced RAW 264.7 apoptosis is regulated by both nitric oxide-dependent and-independent pathways involving JNK and the Bcl-2 family. Cell Cycle 6: 1772-1778. https://doi.org/10.4161/cc.6.14.4438
  43. Wang Y, Xie J, Wang N, Li Y, Sun X, Zhang Y, et al. 2013. Lactobacillus casei Zhang modulate cytokine and toll-like receptor expression and beneficially regulate poly I: C-induced immune responses in RAW264.7 macrophages. Microbiol. Immunol. 57: 54-62. https://doi.org/10.1111/j.1348-0421.516.x

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