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Spirulina Protects against Hepatic Inflammation in Aging: An Effect Related to the Modulation of the Gut Microbiota?

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Neyrinck, Audrey M. [UCL] Taminiau, Bernard Walgrave, Hannah [UCL] Daube, Georges Cani, Patrice D. [UCL] Bindels, Laure B. [UCL] Delzenne, Nathalie M. [UCL]

Aging predisposes to hepatic dysfunction and inflammation that can contribute to the development of non-alcoholic fatty liver disease. Spirulina, a cyanobacterium used as a food additive or food supplement, has been shown to impact immune function. We have tested the potential hepatoprotective effect of a Spirulina in aged mice and to determine whether these effects can be related to a modulation of the gut microbiota. Old mice have been fed a standard diet supplemented with or without 5% Spirulina for six weeks. Among several changes of gut microbiota composition, an increase in Roseburia and Lactobacillus proportions occurs upon Spirulina treatment. Interestingly, parameters related to the innate immunity are upregulated in the small intestine of Spirulina-treated mice. Furthermore, the supplementation with Spirulina reduces several hepatic inflammatory and oxidative stress markers that are upregulated in old mice versus young mice. We conclude that the oral administration of a Spirulina is able to modulate the gut microbiota and to activate the immune system in the gut, a mechanism that may be involved in the improvement of the hepatic inflammation in aged mice. Those data open the way to new therapeutic tools in the management of immune alterations in aging, based on gut microbe-host interactions.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2017
Language Anglais
Journal information "Nutrients" - Vol. 9, no.6, p. 633 [1-13] (2017)
Peer reviewed yes
Publisher MDPI Publishing ((Switzerland ) Basel)
e-issn 2072-6643
Publication status Publié
Affiliation UCL - SSS/LDRI - Louvain Drug Research Institute
Keywords Spirulina ; Aging ; Gut-liver axis ; Inflammaging ; Microbiota
Links
  1. Nikoletopoulou Vassiliki, Kyriakakis Emmanouil, Tavernarakis Nektarios, Cellular and molecular longevity pathways: the old and the new, 10.1016/j.tem.2013.12.003
  2. Sheedfar Fareeba, Biase Stefano Di, Koonen Debby, Vinciguerra Manlio, Liver diseases and aging: friends or foes?, 10.1111/acel.12128
  3. Fontana Luis, Zhao Enpeng, Amir Muhammad, Dong Hanqing, Tanaka Kathryn, Czaja Mark J., Aging promotes the development of diet-induced murine steatohepatitis but not steatosis, 10.1002/hep.26099
  4. Lyons Claire, Kennedy Elaine, Roche Helen, Metabolic Inflammation-Differential Modulation by Dietary Constituents, 10.3390/nu8050247
  5. Deng Ruitang, Chow Te-Jin, Hypolipidemic, Antioxidant, and Antiinflammatory Activities of Microalgae Spirulina : Hypolipidemic, Antioxidant, and Antiinflammatory Activities of Microalgae Spirulina, 10.1111/j.1755-5922.2010.00200.x
  6. Serban Maria-Corina, Sahebkar Amirhossein, Dragan Simona, Stoichescu-Hogea Gheorghe, Ursoniu Sorin, Andrica Florina, Banach Maciej, A systematic review and meta-analysis of the impact of Spirulina supplementation on plasma lipid concentrations, 10.1016/j.clnu.2015.09.007
  7. Ku Chai Siah, Yang Yue, Park Youngki, Lee Jiyoung, Health Benefits of Blue-Green Algae: Prevention of Cardiovascular Disease and Nonalcoholic Fatty Liver Disease, 10.1089/jmf.2012.2468
  8. Biagi Elena, Nylund Lotta, Candela Marco, Ostan Rita, Bucci Laura, Pini Elisa, Nikkïla Janne, Monti Daniela, Satokari Reetta, Franceschi Claudio, Brigidi Patrizia, De Vos Willem, Correction: Through Ageing, and Beyond: Gut Microbiota and Inflammatory Status in Seniors and Centenarians, 10.1371/annotation/df45912f-d15c-44ab-8312-e7ec0607604d
  9. Neyrinck Audrey M., Etxeberria Usune, Taminiau Bernard, Daube Georges, Van Hul Matthias, Everard Amandine, Cani Patrice D., Bindels Laure B., Delzenne Nathalie M., Rhubarb extract prevents hepatic inflammation induced by acute alcohol intake, an effect related to the modulation of the gut microbiota, 10.1002/mnfr.201500899
  10. Neyrinck Audrey M., Possemiers Sam, Verstraete Willy, De Backer Fabienne, Cani Patrice D., Delzenne Nathalie M., Dietary modulation of clostridial cluster XIVa gut bacteria (Roseburia spp.) by chitin–glucan fiber improves host metabolic alterations induced by high-fat diet in mice, 10.1016/j.jnutbio.2010.10.008
  11. Folch, J. Biol. Chem., 226, 497 (1957)
  12. Mukherjee Sohini, Hooper Lora V., Antimicrobial Defense of the Intestine, 10.1016/j.immuni.2014.12.028
  13. Everard Amandine, Lazarevic Vladimir, Gaïa Nadia, Johansson Maria, Ståhlman Marcus, Backhed Fredrik, Delzenne Nathalie M, Schrenzel Jacques, François Patrice, Cani Patrice D, Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity, 10.1038/ismej.2014.45
  14. Claesson Marcus J., Jeffery Ian B., Conde Susana, Power Susan E., O’Connor Eibhlís M., Cusack Siobhán, Harris Hugh M. B., Coakley Mairead, Lakshminarayanan Bhuvaneswari, O’Sullivan Orla, Fitzgerald Gerald F., Deane Jennifer, O’Connor Michael, Harnedy Norma, O’Connor Kieran, O’Mahony Denis, van Sinderen Douwe, Wallace Martina, Brennan Lorraine, Stanton Catherine, Marchesi Julian R., Fitzgerald Anthony P., Shanahan Fergus, Hill Colin, Ross R. Paul, O’Toole Paul W., Gut microbiota composition correlates with diet and health in the elderly, 10.1038/nature11319
  15. Sze Marc A., Schloss Patrick D., Looking for a Signal in the Noise: Revisiting Obesity and the Microbiome, 10.1128/mbio.01018-16
  16. Biagi Elena, Candela Marco, Fairweather-Tait Susan, Franceschi Claudio, Brigidi Patrizia, Ageing of the human metaorganism: the microbial counterpart, 10.1007/s11357-011-9217-5
  17. Xiao Shuiming, Fei Na, Pang Xiaoyan, Shen Jian, Wang Linghua, Zhang Baorang, Zhang Menghui, Zhang Xiaojun, Zhang Chenhong, Li Min, Sun Lifeng, Xue Zhengsheng, Wang Jingjing, Feng Jie, Yan Feiyan, Zhao Naisi, Liu Jiaqi, Long Wenmin, Zhao Liping, A gut microbiota-targeted dietary intervention for amelioration of chronic inflammation underlying metabolic syndrome, 10.1111/1574-6941.12228
  18. Neyrinck Audrey M., Schüppel Valentina L., Lockett Trevor, Haller Dirk, Delzenne Nathalie M., Microbiome and metabolic disorders related to obesity: Which lessons to learn from experimental models?, 10.1016/j.tifs.2016.08.012
  19. Nakamura Noriko, Lin Henry C., McSweeney Christopher S., Mackie Roderick I., Gaskins H. Rex, Mechanisms of Microbial Hydrogen Disposal in the Human Colon and Implications for Health and Disease, 10.1146/annurev.food.102308.124101
  20. Devkota Suzanne, Wang Yunwei, Musch Mark W., Leone Vanessa, Fehlner-Peach Hannah, Nadimpalli Anuradha, Antonopoulos Dionysios A., Jabri Bana, Chang Eugene B., Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice, 10.1038/nature11225
  21. Barlow Gillian M., Yu Allen, Mathur Ruchi, Role of the Gut Microbiome in Obesity and Diabetes Mellitus, 10.1177/0884533615609896
  22. David Lawrence A., Maurice Corinne F., Carmody Rachel N., Gootenberg David B., Button Julie E., Wolfe Benjamin E., Ling Alisha V., Devlin A. Sloan, Varma Yug, Fischbach Michael A., Biddinger Sudha B., Dutton Rachel J., Turnbaugh Peter J., Diet rapidly and reproducibly alters the human gut microbiome, 10.1038/nature12820
  23. Schneeberger Marc, Everard Amandine, Gómez-Valadés Alicia G., Matamoros Sébastien, Ramírez Sara, Delzenne Nathalie M., Gomis Ramon, Claret Marc, Cani Patrice D., Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice, 10.1038/srep16643
  24. Usharani, Adv. Biol. Res., 9, 292 (2015)
  25. Nuhu Abdulmumin A., Spirulina (Arthrospira): An Important Source of Nutritional and Medicinal Compounds, 10.1155/2013/325636
  26. Balachandran Premalatha, Pugh Nirmal D., Ma Guoyi, Pasco David S., Toll-like receptor 2-dependent activation of monocytes by Spirulina polysaccharide and its immune enhancing action in mice, 10.1016/j.intimp.2006.08.001
  27. Miura Kouichi, Role of gut microbiota and Toll-like receptors in nonalcoholic fatty liver disease, 10.3748/wjg.v20.i23.7381
  28. Sato A., Hashiguchi M., Toda E., Iwasaki A., Hachimura S., Kaminogawa S., CD11b+ Peyer's Patch Dendritic Cells Secrete IL-6 and Induce IgA Secretion from Naive B Cells, 10.4049/jimmunol.171.7.3684
  29. Santiago Andrezza F., Alves Andréa C., Oliveira Rafael P., Fernandes Raphaela M., Paula-Silva Josiely, Assis Frankcineia A., Carvalho Cláudia R., Weiner Howard L., Faria Ana Maria C., Aging correlates with reduction in regulatory-type cytokines and T cells in the gut mucosa, 10.1016/j.imbio.2011.05.007
  30. Beutler Bruce, Microbe sensing, positive feedback loops, and the pathogenesis of inflammatory diseases, 10.1111/j.1600-065x.2008.00733.x
  31. Pak Wing, Takayama Fusako, Mine Manaka, Nakamoto Kazuo, Kodo Yasumasa, Mankura Mitsumasa, Egashira Toru, Kawasaki Hiromu, Mori Akitane, Anti-oxidative and anti-inflammatory effects of spirulina on rat model of non-alcoholic steatohepatitis, 10.3164/jcbn.12-18
  32. Remirez D., Fernández V., Tapia G., González R., Videla L. A., Influence of C-phycocyanin on hepatocellular parameters related to liver oxidative stress and Kupffer cell functioning, 10.1007/pl00000314
  33. Romay, Arzneimittelforschung, 51, 733 (2001)
Bibliographic reference Neyrinck, Audrey M. ; Taminiau, Bernard ; Walgrave, Hannah ; Daube, Georges ; Cani, Patrice D. ; et. al. Spirulina Protects against Hepatic Inflammation in Aging: An Effect Related to the Modulation of the Gut Microbiota?. In: Nutrients, Vol. 9, no.6, p. 633 [1-13] (2017)
Permanent URL http://hdl.handle.net/2078.1/185760