Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

Lactococcus lactis and Resveratrol Decrease Body Weight and Increase Benefic Gastrointestinal Microbiota in Mice

Author(s): Keila Lopes Mendes, Deborah de Farias Lelis, Letícia Antunes Athayde Souza, Ronize Viviane Jorge Brito, Mariléia Chaves Andrade, Sérgio Avelino Mota Nobre, André Luiz Sena Guimarães, Alfredo Maurício Batista de Paula, Juliana Pinto de Lima, Aline M. Hilzendeger and Sérgio Henrique Sousa Santos*

Volume 28, Issue 7, 2021

Published on: 09 December, 2020

Page: [761 - 768] Pages: 8

DOI: 10.2174/0929866527999201209214850

Price: $65

Abstract

Background: The microbiome is now known for its important role in whole-body homeostasis. A dysbiosis of the normal microbiota is correlated with metabolic disorders. In this sense, the search for compounds able to modulate the microbiome is needed. Resveratrol, a natural compound found in grapes seems to be a promising candidate.

Objective: In this study, our motivation was to evaluate the effects of the association between Resveratrol and Lactococcus lactis, a probiotic, on the composition of the gastrointestinal microbiota and body weight of mice.

Methods: Twenty female mice were divided into 4 groups: (1) standard diet, (2) standard diet plus Lactococcus lactis, (3) standard diet plus resveratrol, and (4) standard diet plus Lactococcus lactis and resveratrol. At the end of the treatment period, samples of blood, mucus, stomach, and small and large intestines were collected for analysis. Total levels of Immunoglobulin A and Immunoglobulin E, Lac+ and Lac- bacteria and Lactobacillus were measured.

Results: The main results indicate that the association between resveratrol and probiotics was able to decrease mice body weight, as compared to the other groups, in addition to decrease the number of Lac- bacteria and increasing the number of Lac+ bacteria. The levels of secretory IgA were also decreased, compared to the animals treated with only probiotics or resveratrol.

Conclusion: We observed potential synergism between Resveratrol and Lactococcus lactis mainly in modulating the stomach and intestinal microbiota.

Keywords: Probiotic, phenolic, immune system, secretory IgA, weight reduction, synergism, microbiome modulation.

Graphical Abstract

[1]
Bull, M.J.; Plummer, N.T. Part 1: The human gut microbiome in health and disease. Integr. Med. (Encinitas), 2014, 13(6), 17-22.
[PMID: 26770121]
[2]
Sekirov, I.; Russell, S.L.; Antunes, L.C.; Finlay, B.B. Gut microbiota in health and disease. Physiol. Rev., 2010, 90(3), 859-904.
[http://dx.doi.org/10.1152/physrev.00045.2009] [PMID: 20664075]
[3]
Le Chatelier, E.; Nielsen, T.; Qin, J.; Prifti, E.; Hildebrand, F.; Falony, G.; Almeida, M.; Arumugam, M.; Batto, J.M.; Kennedy, S.; Leonard, P.; Li, J.; Burgdorf, K.; Grarup, N.; Jørgensen, T.; Brandslund, I.; Nielsen, H.B.; Juncker, A.S.; Bertalan, M.; Levenez, F.; Pons, N.; Rasmussen, S.; Sunagawa, S.; Tap, J.; Tims, S.; Zoetendal, E.G.; Brunak, S.; Clément, K.; Doré, J.; Kleerebezem, M.; Kristiansen, K.; Renault, P.; Sicheritz-Ponten, T.; de Vos, W.M.; Zucker, J.D.; Raes, J.; Hansen, T.; Bork, P.; Wang, J.; Ehrlich, S.D.; Pedersen, O. MetaHIT consortium. Richness of human gut microbiome correlates with metabolic markers. Nature, 2013, 500(7464), 541-546.
[http://dx.doi.org/10.1038/nature12506] [PMID: 23985870]
[4]
Ferrer, M.; Ruiz, A.; Lanza, F.; Haange, S.B.; Oberbach, A.; Till, H.; Bargiela, R.; Campoy, C.; Segura, M.T.; Richter, M.; von Bergen, M.; Seifert, J.; Suarez, A. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ. Microbiol., 2013, 15(1), 211-226.
[http://dx.doi.org/10.1111/j.1462-2920.2012.02845.x] [PMID: 22891823]
[5]
Patil, D.P.; Dhotre, D.P.; Chavan, S.G.; Sultan, A.; Jain, D.S.; Lanjekar, V.B.; Gangawani, J.; Shah, P.S.; Todkar, J.S.; Shah, S.; Ranade, D.R.; Patole, M.S.; Shouche, Y.S. Molecular analysis of gut microbiota in obesity among Indian individuals. J. Biosci., 2012, 37(4), 647-657.
[http://dx.doi.org/10.1007/s12038-012-9244-0] [PMID: 22922190]
[6]
Everard, A.; Lazarevic, V.; Gaïa, N.; Johansson, M.; Ståhlman, M.; Backhed, F.; Delzenne, N.M.; Schrenzel, J.; François, P.; Cani, P.D. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J., 2014, 8(10), 2116-2130.
[http://dx.doi.org/10.1038/ismej.2014.45] [PMID: 24694712]
[7]
Bleau, C.; Karelis, A.D.; St-Pierre, D.H.; Lamontagne, L. Crosstalk between intestinal microbiota, adipose tissue and skeletal muscle as an early event in systemic low-grade inflammation and the development of obesity and diabetes. Diabetes Metab. Res. Rev., 2015, 31(6), 545-561.
[http://dx.doi.org/10.1002/dmrr.2617] [PMID: 25352002]
[8]
Dugas, L.R.; Fuller, M.; Gilbert, J.; Layden, B.T. The obese gut microbiome across the epidemiologic transition. Emerg. Themes Epidemiol., 2016, 13(2), 2.
[http://dx.doi.org/10.1186/s12982-015-0044-5] [PMID: 26759600]
[9]
Butel, M.J. Probiotics, gut microbiota and health. Med. Mal. Infect., 2014, 44(1), 1-8.
[http://dx.doi.org/10.1016/j.medmal.2013.10.002] [PMID: 24290962]
[10]
Cavanagh, D.; Fitzgerald, G.F.; McAuliffe, O. From field to fermentation: the origins of Lactococcus lactis and its domestication to the dairy environment. Food Microbiol., 2015, 47, 45-61.
[http://dx.doi.org/10.1016/j.fm.2014.11.001] [PMID: 25583337]
[11]
Qiao, Y.; Sun, J.; Xia, S.; Tang, X.; Shi, Y.; Le, G. Effects of resveratrol on gut microbiota and fat storage in a mouse model with high-fat-induced obesity. Food Funct., 2014, 5(6), 1241-1249.
[http://dx.doi.org/10.1039/c3fo60630a] [PMID: 24722352]
[12]
Larrosa, M.; Yanez-Gascon, M.J.; Selma, M.V.; Gonzalez-Sarrias, A.; Toti, S.; Ceron, J.J.; Tomás-Barberán, F.; Dolara, P.; Espín, J.C. Effect of a low dose of dietary resveratrol on colon microbiota, inflammation and tissue damage in a DSS-induced colitis rat model J. Agric. Food Chem., 2009, 57(6), 2211-2220.
[http://dx.doi.org/10.1021/jf803638d]
[13]
Mallappa, R.H.; Rokana, N.; Duary, R.K.; Panwar, H.; Batish, V.K.; Grover, S. Management of metabolic syndrome through probiotic and prebiotic interventions. Indian J. Endocrinol. Metab., 2012, 16(1), 20-27.
[http://dx.doi.org/10.4103/2230-8210.91178] [PMID: 22276249]
[14]
Luerce, T.D.; Gomes-Santos, A.C.; Rocha, C.S.; Moreira, T.G.; Cruz, D.N.; Lemos, L.; Sousa, A.L.; Pereira, V.B.; de Azevedo, M.; Moraes, K.; Cara, D.C.; LeBlanc, J.G.; Azevedo, V.; Faria, A.M.C.; Miyoshi, A. Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically induced colitis. Gut Pathog., 2014, 6(33), 33.
[http://dx.doi.org/10.1186/1757-4749-6-33] [PMID: 25110521]
[15]
Kahouli, I.; Tomaro-Duchesneau, C.; Prakash, S. Probiotics in colorectal cancer (CRC) with emphasis on mechanisms of action and current perspectives. J. Med. Microbiol., 2013, 62(Pt 8), 1107-1123.
[http://dx.doi.org/10.1099/jmm.0.048975-0] [PMID: 23558140]
[16]
Gerritsen, J.; Smidt, H.; Rijkers, G.T.; de Vos, W.M. Intestinal microbiota in human health and disease: the impact of probiotics Genes Nutr., 2011, 6(3), 209-240.
[http://dx.doi.org/10.1007/s12263-011-0229-7]
[17]
Cho, S.J; Jung, U.J.; Choi, M.S. Differential effects of low-dose resveratrol on adiposity and hepatic steatosis in diet-induced obese mice Br. J. Nutr., 2012, 108(12), 2166-2175.
[http://dx.doi.org/10.1017/S0007114512000347]
[18]
Aguirre, L.; Fernández-Quintela, A.; Arias, N.; Portillo, M.P. Resveratrol: anti-obesity mechanisms of action. Molecules, 2014, 19(11), 18632-18655.
[http://dx.doi.org/10.3390/molecules191118632] [PMID: 25405284]
[19]
Novelle, M.G.; Wahl, D.; Diéguez, C.; Bernier, M.; de Cabo, R. Resveratrol supplementation: where are we now and where should we go? Ageing Res. Rev., 2015, 21, 1-15.
[http://dx.doi.org/10.1016/j.arr.2015.01.002] [PMID: 25625901]
[20]
Wang, B.; Sun, J.; Li, X.; Zhou, Q.; Bai, J.; Shi, Y.; Le, G. Resveratrol prevents suppression of regulatory T-cell production, oxidative stress, and inflammation of mice prone or resistant to high-fat diet-induced obesity. Nutr. Res., 2013, 33(11), 971-981.
[http://dx.doi.org/10.1016/j.nutres.2013.07.016] [PMID: 24176237]
[21]
Poulsen, M.M.; Fjeldborg, K.; Ornstrup, M.J.; Kjær, T.N.; Nøhr, M.K.; Pedersen, S.B. Resveratrol and inflammation: challenges in translating pre-clinical findings to improved patient outcomes. Biochim. Biophys. Acta, 2015, 1852(6), 1124-1136.
[http://dx.doi.org/10.1016/j.bbadis.2014.12.024] [PMID: 25583116]
[22]
Timmers, S.; Konings, E.; Bilet, L.; Houtkooper, R.H.; Van de Weijer, T.; Goossens, G.H.; Hoeks, J.; van der Krieken, S.; Ryu, D.; Kersten, S.; Moonen-Kornips, E.; Hesselink, M.K.C.; Kunz, I.; Schrauwen-Hinderling, V.B.; Blaak, E.; Auwerx, J.; Schrauwen, P. Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans Cell Metab., 2011, 14(5), 612-22.
[http://dx.doi.org/10.1016/j.cmet.2011.10.002]
[23]
Chung, S.; Yao, H.; Caito, S.; Hwang, J.W.; Arunachalam, G.; Rahman, I. Regulation of SIRT1 in cellular functions: role of polyphenols Arch. Biochem. Biophys., 2010, 501(1), 79-90.
[http://dx.doi.org/10.1016/j.abb.2010.05.003]
[24]
Wang, S.; Moustaid-Moussa, N.; Chen, L.; Mo, H.; Shastri, A.; Su, R.; Bapat, P.; Kwun, I.; Shen, C.L. Novel insights of dietary polyphenols and obesity. J. Nutr. Biochem., 2014, 25(1), 1-18.
[http://dx.doi.org/10.1016/j.jnutbio.2013.09.001] [PMID: 24314860]
[25]
Mendes, K.L.; de Pinho, L.; Andrade, J.M.; Paraíso, A.F.; Lula, J.F.; Macedo, S.M.; Feltenberger, J.D.; Guimarães, A.L.; de Paula, A.M.; Santos, S.H. Distinct metabolic effects of resveratrol on lipogenesis markers in mice adipose tissue treated with high-polyunsaturated fat and high-protein diets. Life Sci., 2016, 153, 66-73.
[http://dx.doi.org/10.1016/j.lfs.2016.04.014] [PMID: 27085216]
[26]
Andrade, J.M.; Frade, A.C.; Guimarães, J.B.; Freitas, K.M.; Lopes, M.T.; Guimarães, A.L.; de Paula, A.M.; Coimbra, C.C.; Santos, S.H. Resveratrol increases brown adipose tissue thermogenesis markers by increasing SIRT1 and energy expenditure and decreasing fat accumulation in adipose tissue of mice fed a standard diet. Eur. J. Nutr., 2014, 53(7), 1503-1510.
[http://dx.doi.org/10.1007/s00394-014-0655-6] [PMID: 24468941]
[27]
Núñez, I.N.; Galdeano, C.M.; de LeBlanc, Ade.M.; Perdigón, G. Evaluation of immune response, microbiota, and blood markers after probiotic bacteria administration in obese mice induced by a high-fat diet. Nutrition, 2014, 30(11-12), 1423-1432.
[http://dx.doi.org/10.1016/j.nut.2014.03.025] [PMID: 25280423]
[28]
Kadooka, Y.; Sato, M.; Ogawa, A.; Miyoshi, M.; Uenishi, H.; Ogawa, H.; Ikuyama, K.; Kagoshima, M.; Tsuchida, T. Effect of Lactobacillus gasseri SBT2055 in fermented milk on abdominal adiposity in adults in a randomised controlled trial Br. Journal Nutr., 2013, 110(9), 1696-1703.
[http://dx.doi.org/10.1017/S0007114513001037]
[29]
Hakansson, A.; Molin, G. Gut microbiota and inflammation. Nutrients, 2011, 3(6), 637-682.
[http://dx.doi.org/10.3390/nu3060637] [PMID: 22254115]
[30]
Мokrozub, V.V.; Lazarenko, L.M.; Sichel, L.M.; Babenko, L.P.; Lytvyn, P.M.; Demchenko, O.M.; Melnichenko, Y.O.; Boyko, N.V.; Biavati, B.; DiGioia, D.; Bubnov, R.V.; Spivak, M.Y. The role of beneficial bacteria wall elasticity in regulating innate immune response. EPMA J., 2015, 6(1), 13.
[http://dx.doi.org/10.1186/s13167-015-0035-1] [PMID: 26110044]
[31]
Selma, M.V.; Espín, J.C.; Tomás-Barberán, F.A. Interaction between phenolics and gut microbiota: role in human health. J. Agric. Food Chem., 2009, 57(15), 6485-6501.
[http://dx.doi.org/10.1021/jf902107d] [PMID: 19580283]
[32]
Guinane, C.M.; Cotter, P.D. Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Therap. Adv. Gastroenterol., 2013, 6(4), 295-308.
[http://dx.doi.org/10.1177/1756283X13482996] [PMID: 23814609]
[33]
Okai, S.; Usui, F.; Yokota, S.; Hori-I, Y.; Hasegawa, M.; Nakamura, T.; Kurosawa, M.; Okada, S.; Yamamoto, K.; Nishiyama, E.; Mori, H.; Yamada, T.; Kurokawa, K.; Matsumoto, S.; Nanno, M.; Naito, T.; Watanabe, Y.; Kato, T.; Miyauchi, E.; Ohno, H.; Shinkura, R. High-affinity monoclonal IgA regulates gut microbiota and prevents colitis in mice. Nat. Microbiol., 2016, 1(9), 16103.
[http://dx.doi.org/10.1038/nmicrobiol.2016.103] [PMID: 27562257]
[34]
Pabst, O.; Cerovic, V.; Hornef, M. Secretory IgA in the coordination of establishment and maintenance of the microbiota. Trends Immunol., 2016, 37(5), 287-296.
[http://dx.doi.org/10.1016/j.it.2016.03.002] [PMID: 27066758]
[35]
Yuan, J.; Lu, L.; Zhang, Z.; Zhang, S. Dietary intake of resveratrol enhances the adaptive immunity of aged rats. Rejuvenation Res., 2012, 15(5), 507-515.
[http://dx.doi.org/10.1089/rej.2012.1321] [PMID: 22950432]
[36]
van Hylckama Vlieg, J.E.; Veiga, P.; Zhang, C.; Derrien, M.; Zhao, L. Impact of microbial transformation of food on health - from fermented foods to fermentation in the gastro-intestinal tract. Curr. Opin. Biotechnol., 2011, 22(2), 211-219.
[http://dx.doi.org/10.1016/j.copbio.2010.12.004] [PMID: 21247750]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy