DOI QR코드

DOI QR Code

Water Extract of Ecklonia cava Protects against Fine Dust (PM2.5)-Induced Health Damage by Regulating Gut Health

  • Park, Seon Kyeong (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Kang, Jin Yong (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Kim, Jong Min (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Kim, Min Ji (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Lee, Hyo Lim (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Moon, Jong Hyun (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Jeong, Hye Rin (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Kim, Hyun-Jin (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Heo, Ho Jin (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University)
  • Received : 2022.03.11
  • Accepted : 2022.06.02
  • Published : 2022.07.28

Abstract

To confirm the therapeutic effect of the water extract from Ecklonia cava (WEE) against PM2.5 induced systemic health damage, we evaluated gut health with a focus on the microbiota and metabolites. Systemic damage in mice was induced through PM2.5 exposure for 12 weeks in a whole-body chamber. After exposure for 12 weeks, body weight and food intake decreased, and WEE at 200 mg/kg body weight (mpk) alleviated these metabolic efficiency changes. In addition, PM2.5 induced changes in the length of the colon and fecal water content. The administration of the WEE at 200 mpk oral dose effectively reduced changes in the colon caused by PM2.5 exposure. We also attempted to confirm whether the effect of the WEE is mediated via regulation of the microbiota-gut-brain axis in mice with PM2.5 induced systemic damage. We examined changes in the fecal microbiota and gut metabolites such as short-chain fatty acids (SCFAs) and kynurenine metabolites. In the PM2.5 exposed group, a decrease in the abundance of Lactobacillus (Family: Lactobacillaceae) and an increase in the abundance of Alistipes (Family: Rikenellaceae) were observed, and the administration of the WEE showed a beneficial effect on the gut microbiota. In addition, the WEE effectively increased the levels of SCFAs (acetate, propionate, and butyrate). Furthermore, kynurenic acid (KYNA), which is a critical neuroprotective metabolite in the gut-brain axis, was increased by the administration of the WEE. Our findings suggest that the WEE could be used as a potential therapeutic against PM2.5 induced health damage by regulating gut function.

Keywords

Acknowledgement

This study was supported by the Basic Science Research Program through the National Research Foundation (NRF) of Korea (NRF 2018R1D1A3B07043398) funded by the Ministry of Education and Korean Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (2017029713), Republic of Korea. Seon Kyeong Park, Jin Yong Kang, Jong Min Kim, Min Ji Kim, Hyo Lim Lee, Jong Hyun Moon, Hye Rin Jeong were supported by the BK21 program, Ministry of Education, Republic of Korea.

References

  1. Zhang J, Zeng X, Du X, Pan K, Song L, Song W, et al. 2019. Parental PM2.5 exposure-promoted development of metabolic syndrome in offspring is associated with the changes of immune microenvironment. Toxicol. Sci. 170: 415-426. https://doi.org/10.1093/toxsci/kfz109
  2. Choi JH, Kim JS, Kim YC, Kim YS, Chung NH, Cho MH. 2004. Comparative study of PM2.5- and PM10-induced oxidative stress in rat lung epithelial cells. J. Vet. Sci. 5: 11-18. https://doi.org/10.4142/jvs.2004.5.1.11
  3. Shou Y, Huang Y, Zhu X, Liu C, Hu Y, Wang H. 2019. A review of the possible associations between ambient PM2.5 exposures and the development of Alzheimer's disease. Ecotoxicol. Environ. Safety 174: 344-352. https://doi.org/10.1016/j.ecoenv.2019.02.086
  4. Fu P, Guo X, Cheung FMH, Yung KKL. 2019. The association between PM2.5 exposure and neurological disorders: a systematic review and meta-analysis. Sci. Total Environ. 655: 1240-1248. https://doi.org/10.1016/j.scitotenv.2018.11.218
  5. Salim SY, Kaplan GG, Madsen KL. 2014. Air pollution effects on the gut microbiota: a link between exposure and inflammatory disease. Gut Microbes 5: 215-219. https://doi.org/10.4161/gmic.27251
  6. Wang W, Zhou J, Chen M, Huang X, Xie X, Li W, et al. 2018. Exposure to concentrated ambient PM2.5 alters the composition of gut microbiota in a murine model. Part. Fibre Toxicol. 15: 17.
  7. Mutlu EA, Comba IY, Cho T, Engen PA, Yazici C, Soberanes S, et al. 2018. Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome. Environ. Pollut. 240: 817-830. https://doi.org/10.1016/j.envpol.2018.04.130
  8. Wiedlocha M, Marcinowicz P, Janoska-Jazdzik M, Szulc A. 2021. Gut microbiota, kynurenine pathway and mental disorders-Review. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 106: 110145.
  9. Kennedy PJ, Cryan JF, Dinan TG, Clarke G. 2017. Kynurenine pathway metabolism and the microbiota-gut-brain axis. Neuropharmacology 112: 399-412. https://doi.org/10.1016/j.neuropharm.2016.07.002
  10. Dinan TG, Cryan JF. 2017. The microbiome-gut-brain axis in health and disease. Gastroenterol. Clin. North Am. 46: 77-89. https://doi.org/10.1016/j.gtc.2016.09.007
  11. van der Meulen TA, Harmsen HJ, Bootsma H, Spijkervet FK, Kroese FG, Vissink A. 2016. The microbiome-systemic diseases connection. Oral Dis. 22: 719-734. https://doi.org/10.1111/odi.12472
  12. Chen Y, Guillemin GJ. 2009. Kynurenine pathway metabolites in humans: disease and healthy states. Int. J. Tryptophan Res. 2: IJTR. S2097.
  13. Liang Y, Xie S, He Y, Xu M, Qiao X, Zhu Y, et al. 2022. Kynurenine pathway metabolites as biomarkers in Alzheimer's disease. Dis. Markers. 2022: 9484217.
  14. Choi DM, Ko YW, Kang R-S, Kim JH. 2015. Morphological and genetic variability among Ecklonia cava (Laminariales, Phaeophyceae) populations in Korea. Algae 30: 89-101. https://doi.org/10.4490/algae.2015.30.2.089
  15. Wijesekara I, Yoon NY, Kim SK. 2010. Phlorotannins from Ecklonia cava (Phaeophyceae): Biological activities and potential health benefits. Biofactors 36: 408-414. https://doi.org/10.1002/biof.114
  16. Wijesinghe W, Jeon Y-J. 2012. Exploiting biological activities of brown seaweed Ecklonia cava for potential industrial applications: a review. Int. J. Food Sci. Nutr. 63: 225-235. https://doi.org/10.3109/09637486.2011.619965
  17. Park SK, Kang JY, Kim JM, Kim H-J, Heo HJ. 2021. Ecklonia cava attenuates PM2.5-induced cognitive decline through mitochondrial activation and anti-inflammatory effect. Mar. Drugs 19: 131.
  18. Lee S, Youn K, Kim DH, Ahn M-R, Yoon E, Kim O-Y, et al. 2018. Anti-neuroinflammatory property of phlorotannins from Ecklonia cava on Aβ25-35-induced damage in PC12 cells. Mar. Drugs 17: 7.
  19. Han M, Hur Y, Hwang J, Park J. 2017. Biological effects of blood-brain barrier disruption using a focused ultrasound. Biomed. Eng. Lett. 7: 115-120. https://doi.org/10.1007/s13534-017-0025-4
  20. Liu X, Cao S, Zhang X. 2015. Modulation of gut microbiota-brain axis by probiotics, prebiotics, and diet. J. Agric. Food Chem. 63: 7885-7895. https://doi.org/10.1021/acs.jafc.5b02404
  21. Kang JE, Park SK, Kang JY, Kim JM, Kwon BS, Park SH, et al. 2021. Actinidia arguta sprout as a natural antioxidant: Ameliorating effect on lipopolysaccharide-induced cognitive impairment. J. Microbiol. Biotechnol. 31: 51-62. https://doi.org/10.4014/jmb.2009.09012
  22. Virag D, Kiraly M, Drahos L, Edes AE, Gecse K, Bagdy G, et al. 2020. Development, validation and application of LC-MS/MS method for quantification of amino acids, kynurenine and serotonin in human plasma. J. Pharm. Biomed. Anal. 180: 113018.
  23. Wang L-S, Zhang M-D, Tao X, Zhou Y-F, Liu X-M, Pan R-L, et al. 2019. LC-MS/MS-based quantification of tryptophan metabolites and neurotransmitters in the serum and brain of mice. J. Chromatography B. Analyt. Biomed. Life Sci. 1112: 24-32. https://doi.org/10.1016/j.jchromb.2019.02.021
  24. Peters R, Ee N, Peters J, Booth A, Mudway I, Anstey KJ. 2019. Air pollution and dementia: a systematic review. J. Alzheimer's Dis. 70: S145-S163. https://doi.org/10.3233/JAD-180631
  25. Konturek S, Konturek J, Pawlik T, Brzozowski T. 2004. Brain-gut axis and its role in the control of food intake. J. Physiol. Pharmacol. 55: 137-154.
  26. Sun L-J, Li J-N, Nie Y-Z. 2020. Gut hormones in microbiota-gut-brain cross-talk. Chin. Med. J. 133: 826-833. https://doi.org/10.1097/CM9.0000000000000706
  27. Yang M, Jia W, Wang D, Han F, Niu W, Zhang H, et al. 2019. Effects and mechanism of constitutive TL1A expression on intestinal mucosal barrier in DSS-induced colitis. Dig. Dis. Sci. 64: 1844-1856. https://doi.org/10.1007/s10620-019-05580-z
  28. Wu L-H, Xu Z-L, Dong D, He S-A, Yu H. 2011. Protective effect of anthocyanins extract from blueberry on TNBS-induced IBD model of mice. Evid. Based Complement. Alternat. Med. 2011: 525462.
  29. Akbari P, Braber S, Alizadeh A, Verheijden KA, Schoterman MH, Kraneveld AD, et al. 2015. Galacto-oligosaccharides protect the intestinal barrier by maintaining the tight junction network and modulating the inflammatory responses after a challenge with the mycotoxin deoxynivalenol in human Caco-2 cell monolayers and B6C3F1 mice. J. Nutr. 145: 1604-1613. https://doi.org/10.3945/jn.114.209486
  30. Xue M, Ji X, Liang H, Liu Y, Wang B, Sun L, et al. 2018. The effect of fucoidan on intestinal flora and intestinal barrier function in rats with breast cancer. Food Funct. 9: 1214-1223. https://doi.org/10.1039/C7FO01677H
  31. Sun T, Liang H, Xue M, Liu Y, Gong A, Jiang Y, et al. 2020. Protective effect and mechanism of fucoidan on intestinal mucosal barrier function in NOD mice. Food Agric. Immunol. 31: 939-953. https://doi.org/10.1080/09540105.2020.1789071
  32. Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. 2015. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 26: 26191.
  33. Liu Y, Wang T, Si B, Du H, Liu Y, Waqas A, et al. 2021. Intratracheally instillated diesel PM2.5 significantly altered the structure and composition of indigenous murine gut microbiota. Ecotoxicol. Environ. Safety 210: 111903.
  34. Isolauri E, Sutas Y, Kankaanpaa P, Arvilommi H, Salminen S. 2001. Probiotics: effects on immunity. Am. Clin. Nutr. 73: 444s-450s. https://doi.org/10.1093/ajcn/73.2.444s
  35. Kong Y, Olejar KJ, On SL, Chelikani V. 2020. The potential of Lactobacillus spp. for modulating oxidative stress in the gastrointestinal tract. Antioxidants 9: 610.
  36. Kelley N, Jeltema D, Duan Y, He Y. 2019. The NLRP3 inflammasome: an overview of mechanisms of activation and regulation. Int. J. Mol. Sci. 20: 3328.
  37. Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, et al. 2011. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141: 599-609. e593. https://doi.org/10.1053/j.gastro.2011.04.052
  38. Xu M, Mo X, Huang H, Chen X, Liu H, Peng Z, et al. 2020. Yeast β-glucan alleviates cognitive deficit by regulating gut microbiota and metabolites in Aβ1-42-induced AD-like mice. Int. J. Biol. Macromol. 161: 258-270. https://doi.org/10.1016/j.ijbiomac.2020.05.180
  39. Zheng L-X, Chen X-Q, Cheong K-L. 2020. Current trends in marine algae polysaccharides: the digestive tract, microbial catabolism, and prebiotic potential. Int. J. Biol. Macromol. 151: 344-354. https://doi.org/10.1016/j.ijbiomac.2020.02.168
  40. Martin-Gallausiaux C, Larraufie P, Jarry A, Beguet-Crespel F, Marinelli L, Ledue F, et al. 2018. Butyrate produced by commensal bacteria down-regulates indolamine 2, 3-dioxygenase 1 (IDO-1) expression via a dual mechanism in human intestinal epithelial cells. Front. Immunol. 9: 2838.
  41. Allison DJ, Ditor DS. 2014. The common inflammatory etiology of depression and cognitive impairment: a therapeutic target. J. Neuroinflamm. 11: 1-12. https://doi.org/10.1186/1742-2094-11-1
  42. Charoensiddhi S, Conlon MA, Vuaran MS, Franco CM, Zhang W. 2016. Impact of extraction processes on prebiotic potential of the brown seaweed Ecklonia radiata by in vitro human gut bacteria fermentation. J. Funct. Foods 24: 221-230. https://doi.org/10.1016/j.jff.2016.04.016
  43. Mudry JM, Alm PS, Erhardt S, Goiny M, Fritz T, Caidahl K, et al. 2016. Direct effects of exercise on kynurenine metabolism in people with normal glucose tolerance or type 2 diabetes. Diabetes Metab. Res. Rev. 32: 754-761. https://doi.org/10.1002/dmrr.2798
  44. Guidetti P, Okuno E, Schwarcz R. 1997. Characterization of rat brain kynurenine aminotransferases I and II. J. Neurosci. Res. 50: 457-465. https://doi.org/10.1002/(SICI)1097-4547(19971101)50:3<457::AID-JNR12>3.0.CO;2-3
  45. Cervenka I, Agudelo LZ, Ruas JL. 2017. Kynurenines: Tryptophan's metabolites in exercise, inflammation, and mental health. Science 357: eaaf9794.
  46. Mandi Y, Vecsei L. 2012. The kynurenine system and immunoregulation. J. Neural Transm. 119: 197-209. https://doi.org/10.1007/s00702-011-0681-y
  47. Muller N, Myint A-M, Schwarz MJ. 2009. The impact of neuroimmune dysregulation on neuroprotection and neurotoxicity in psychiatric disorders-relation to drug treatment. Dialogues Clin. Neurosci. 11: 319-332. https://doi.org/10.31887/DCNS.2009.11.3/nmueller
  48. Guillemin GJ, Williams KR, Smith DG, Smythe GA, Croitoru-Lamoury J, Brew BJ. 2003. Quinolinic acid in the pathogenesis of Alzheimer's disease, pp. 167-176. Developments in Tryptophan and Serotonin Metabolism, Ed. Springer
  49. Singh S, Kumar P. 2016. Neuroprotective activity of curcumin in combination with piperine against quinolinic acid induced neurodegeneration in rats. Pharmacology 97: 151-160. https://doi.org/10.1159/000443896
  50. Stone TW. 2000. Development and therapeutic potential of kynurenic acid and kynurenine derivatives for neuroprotection. Trends Pharmacol. Sci. 21: 149-154. https://doi.org/10.1016/S0165-6147(00)01451-6
  51. Foster AC, Vezzani A, French ED, Schwarcz R. 1984. Kynurenic acid blocks neurotoxicity and seizures induced in rats by the related brain metabolite quinolinic acid. Neurosci. Lett. 48: 273-278. https://doi.org/10.1016/0304-3940(84)90050-8
  52. Morales-Martinez A, Sanchez-Mendoza A, Martinez-Lazcano JC, Pineda-Farias JB, Montes S, El-Hafidi M, et al. 2017. Essential fatty acid-rich diets protect against striatal oxidative damage induced by quinolinic acid in rats. Nutr. Neurosci. 20: 388-395. https://doi.org/10.1080/1028415X.2016.1147683
  53. Parasram K. 2018. Phytochemical treatments target kynurenine pathway induced oxidative stress. Redox Rep. 23: 25-28. https://doi.org/10.1080/13510002.2017.1343223
  54. Savitz J. 2020. The kynurenine pathway: a finger in every pie. Mol. Psychiatry. 25: 131-147. https://doi.org/10.1038/s41380-019-0414-4
  55. Connor TJ, Starr N, O'Sullivan JB, Harkin A. 2008. Induction of indolamine 2, 3-dioxygenase and kynurenine 3-monooxygenase in rat brain following a systemic inflammatory challenge: a role for IFN-γ? Neurosci. Lett. 441: 29-34. https://doi.org/10.1016/j.neulet.2008.06.007
  56. Molteni R, Macchi F, Zecchillo C, Dell'Agli M, Colombo E, Calabrese F, et al. 2013. Modulation of the inflammatory response in rats chronically treated with the antidepressant agomelatine. Eur. Neuropsychopharmacol. 23: 1645-1655. https://doi.org/10.1016/j.euroneuro.2013.03.008