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Protein & Peptide Letters

Editor-in-Chief

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

Research Article

Lactococcus lactis Administration Modulates IgE and IL-4 Production and Promotes Enterobacteria Growth in the Gut from Ethanol-Intake Mice

Author(s): Letícia Antunes Athayde, Sarah Leão Fiorini de Aguiar, Mariana Camila Gonçalves Miranda, Ronize Viviane Jorge Brito, Ana Maria Caetano de Faria, Sergio Avelino Mota Nobre and Mariléia Chaves Andrade*

Volume 28, Issue 10, 2021

Published on: 26 July, 2021

Page: [1164 - 1179] Pages: 16

DOI: 10.2174/0929866528666210727102019

Price: $65

Abstract

Background: It is well known that alcohol can trigger inflammatory effects in the gastrointestinal tract (GIT), interfering with mucosal homeostasis.

Objectives: This study evaluated the effectiveness of Lactococcus lactis treatment in controlling the increase in molecular biomarkers related to allergic inflammation and the effect on the diversity and abundance of the Enterobacteriaceae family in the GIT after high-dose acute administration of ethanol.

Methods: Mice received ethanol or saline solution by gavage for four consecutive days, and 24 h after the last administration, the animals were given L. lactis or M17 broth orally ad libitum for two consecutive days. The animals were subsequently sacrificed and dissected.

Results: L. lactis treatment was able to restore basal levels of secretory immunoglobulin A in the gastric mucosa, serum total immunoglobulin E, interleukin (IL)-4 production in gastric and intestinal tissues, and IL-10 levels in gastric tissue. L. lactis treatment encouraged the diversification of the Enterobacteriaceae population, particularly the commensal species, in the GIT.

Conclusion: This research opens a field of studies regarding the modulatory effect of L. lactis on immunological and microbial changes induced after alcohol intake.

Keywords: Alcohol, gut, immunoglobulin E, interleukin-4, Lactococcus lactis, gastric tissue.

Graphical Abstract

[1]
Szabo, G.; Saha, B. Alcohol’s effect on host defense. Alcohol Res., 2015, 37(2), 159-170.
[PMID: 26695755]
[2]
Andrade, M.C.; Menezes, J.S.; Cassali, G.D.; Martins-Filho, O.A.; Cara, D.C.; Faria, A.M. Alcohol-induced gastritis prevents oral tolerance induction in mice. Clin. Exp. Immunol., 2006, 146(2), 312-322.
[http://dx.doi.org/10.1111/j.1365-2249.2006.03207.x] [PMID: 17034584]
[3]
Andrade, M.C.; Martins-Filho, O.A.; Coelho-Neto, J.; Mesquita, O.N.; Faria, A.M. The long-term impaired macrophages functions are already observed early after high-dose ethanol administration. Scand. J. Immunol., 2008, 68(3), 306-314.
[http://dx.doi.org/10.1111/j.1365-3083.2008.02142.x] [PMID: 18782259]
[4]
Alvarenga, D.M.; Perez, D.A.; Gomes-Santos, A.C.; Miyoshi, A.; Azevedo, V.; Coelho-Dos-Reis, J.G.; Martins-Filho, O.A.; Faria, A.M.; Cara, D.C.; Andrade, M.C. Previous ngestion of Lactococcus lactis by ethanol-treated mice preserves antigen presentation hierarchy in the gut and oral tolerance susceptibility. Alcohol. Clin. Exp. Res., 2015, 39(8), 1453-1464.
[http://dx.doi.org/10.1111/acer.12770] [PMID: 26110492]
[5]
Engen, P.A.; Green, S.J.; Voigt, R.M.; Forsyth, C.B.; Keshavarzian, A. The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res., 2015, 37(2), 223-236.
[PMID: 26695747]
[6]
Ragia, G.; Manolopoulos, V.G. Personalized medicine of alcohol addiction: pharmacogenomics and beyond. Curr. Pharm. Biotechnol., 2017, 18(3), 221-230.
[http://dx.doi.org/10.2174/1389201018666170224105025] [PMID: 28240173]
[7]
Dervaux, A.; Laqueille, X. Thiamine (vitamin B1) treatment in patients with alcohol dependence. Presse Med., 2017, 46(2 Pt 1), 165-171.
[http://dx.doi.org/10.1016/j.lpm.2016.07.025] [PMID: 27818067]
[8]
Yoshimura, A.; Kimura, M.; Nakayama, H.; Matsui, T.; Okudaira, F.; Akazawa, S.; Ohkawara, M.; Cho, T.; Kono, Y.; Hashimoto, K.; Kumagai, M.; Sahashi, Y.; Roh, S.; Higuchi, S. Efficacy of disulfiram for the treatment of alcohol dependence assessed with a multicenter randomized controlled trial. Alcohol. Clin. Exp. Res., 2014, 38(2), 572-578.
[http://dx.doi.org/10.1111/acer.12278] [PMID: 24117666]
[9]
Rolland, B.; Paille, F.; Gillet, C.; Rigaud, A.; Moirand, R.; Dano, C.; Dematteis, M.; Mann, K.; Aubin, H.J. Pharmacotherapy for alcohol dependence: the 2015 recommendations of the French alcohol society, issued in partnership with the European Federation of Addiction Societies. CNS Neurosci. Ther., 2016, 22(1), 25-37.
[http://dx.doi.org/10.1111/cns.12489] [PMID: 26768685]
[10]
Canesso, MCC; Lacerda, NL; Ferreira, CM Comparing the effects of acute alcohol consumption in germ-free and conventional mice: the role of the gut microbiota. BMC Microbiol, 2014, 240-250.
[11]
Sanders, M.E. Probiotics: Considerations for human health. Nutr. Rev., 2003, 61(3), 91-99.
[http://dx.doi.org/10.1301/nr.2003.marr.91-99] [PMID: 12723641]
[12]
Mutlu, E.; Keshavarzian, A.; Engen, P.; Forsyth, C.B.; Sikaroodi, M.; Gillevet, P. Intestinal dysbiosis: a possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol. Clin. Exp. Res., 2009, 33(10), 1836-1846.
[http://dx.doi.org/10.1111/j.1530-0277.2009.01022.x] [PMID: 19645728]
[13]
Yan, A.W.; Fouts, D.E.; Brandl, J.; Stärkel, P.; Torralba, M.; Schott, E.; Tsukamoto, H.; Nelson, K.E.; Brenner, D.A.; Schnabl, B. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology, 2011, 53(1), 96-105.
[http://dx.doi.org/10.1002/hep.24018] [PMID: 21254165]
[14]
Tavares, L.M.; de Jesus, L.C.L.; da Silva, T.F.; Barroso, F.A.L.; Batista, V.L.; Coelho-Rocha, N.D.; Azevedo, V.; Drumond, M.M.; Mancha-Agresti, P. Novel strategies for efficient production and delivery of live biotherapeutics and biotechnological uses of Lactococcus lactis: the lactic acid bacterium model. Front. Bioeng. Biotechnol., 2020, 8, 517166.
[http://dx.doi.org/10.3389/fbioe.2020.517166] [PMID: 33251190]
[15]
Song, A.A.; In, L.L.A.; Lim, S.H.E.; Rahim, R.A. A review on Lactococcus lactis: from food to factory. Microb. Cell Fact., 2017, 16(1), 55.
[http://dx.doi.org/10.1186/s12934-017-0669-x] [PMID: 28376880]
[16]
Carvalho, R.D.O.; do Carmo, F.L.R.; de Oliveira Junior, A.; Langella, P.; Chatel, J.M.; Bermúdez-Humarán, L.G.; Azevedo, V.; de Azevedo, M.S. Use of wild type or recombinant lactic acid bacteria as an alternative treatment for gastrointestinal inflammatory diseases: a focus on inflammatory bowel diseases and mucositis. Front. Microbiol., 2017, 8(8), 800.
[http://dx.doi.org/10.3389/fmicb.2017.00800] [PMID: 28536562]
[17]
Cronin, M.; Ventura, M.; Fitzgerald, G.F.; van Sinderen, D. Progress in genomics, metabolism and biotechnology of bifidobacteria. Int. J. Food Microbiol., 2011, 149(1), 4-18.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2011.01.019] [PMID: 21320731]
[18]
Wescombe, P.A.; Heng, N.C.; Burton, J.P.; Chilcott, C.N.; Tagg, J.R. Streptococcal bacteriocins and the case for Streptococcus salivarius as model oral probiotics. Future Microbiol., 2009, 4(7), 819-835.
[http://dx.doi.org/10.2217/fmb.09.61] [PMID: 19722837]
[19]
Nanda Kumar, N.S.; Balamurugan, R.; Jayakanthan, K.; Pulimood, A.; Pugazhendhi, S.; Ramakrishna, B.S. Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J. Gastroenterol. Hepatol., 2008, 23(12), 1834-1839.
[http://dx.doi.org/10.1111/j.1440-1746.2008.05723.x] [PMID: 19120873]
[20]
Castillo, N.A.; de Moreno de LeBlanc, A.; M Galdeano, C.; Perdigón, G. Comparative study of the protective capacity against Salmonella infection between probiotic and nonprobiotic Lactobacilli. J. Appl. Microbiol., 2013, 114(3), 861-876.
[http://dx.doi.org/10.1111/jam.12074] [PMID: 23163296]
[21]
Isolauri, E.; Rautava, S.; Salminen, S. Probiotics in the development and treatment of allergic disease. Gastroenterol. Clin. North Am., 2012, 41(4), 747-762.
[http://dx.doi.org/10.1016/j.gtc.2012.08.007] [PMID: 23101685]
[22]
Reiff, C.; Kelly, D. Inflammatory bowel disease, gut bacteria and probiotic therapy. Int. J. Med. Microbiol., 2010, 300(1), 25-33.
[http://dx.doi.org/10.1016/j.ijmm.2009.08.004] [PMID: 19800289]
[23]
Riedel, C.U.; Foata, F.; Philippe, D.; Adolfsson, O.; Eikmanns, B.J.; Blum, S. Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappaB activation. World J. Gastroenterol., 2006, 12(23), 3729-3735.
[http://dx.doi.org/10.3748/wjg.v12.i23.3729] [PMID: 16773690]
[24]
Santos Rocha, C.; Lakhdari, O.; Blottière, H.M.; Blugeon, S.; Sokol, H.; Bermúdez-Humarán, L.G.; Azevedo, V.; Miyoshi, A.; Doré, J.; Langella, P.; Maguin, E.; van de Guchte, M. Anti-inflammatory properties of dairy lactobacilli. Inflamm. Bowel Dis., 2012, 18(4), 657-666.
[http://dx.doi.org/10.1002/ibd.21834] [PMID: 21837773]
[25]
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.
[http://dx.doi.org/10.1186/1757-4749-6-33] [PMID: 25110521]
[26]
Miyoshi, A.; Jamet, E.; Commissaire, J.; Renault, P.; Langella, P.; Azevedo, V. A xylose-inducible expression system for Lactococcus lactis. FEMS Microbiol. Lett., 2004, 239(2), 205-212.
[http://dx.doi.org/10.1016/j.femsle.2004.08.018] [PMID: 15476967]
[27]
Winn, W.; Allen, S.; Janda, W.; Koneman, E.; Procop, G.; Schreckenberger, P. Diagnóstico microbiológico: texto e atlas colorido, 6th ed.; Guanabara Koogan: Rio de Janeiro, 2008, p. 1565.
[28]
Saldanha, J.C.; Gargiulo, D.L.; Silva, S.S.; Carmo-Pinto, F.H.; Andrade, M.C.; Alvarez-Leite, J.I.; Teixeira, M.M.; Cara, D.C. A model of chronic IgE-mediated food allergy in ovalbumin-sensitized mice. Braz. J. Med. Biol. Res., 2004, 37(6), 809-816.
[http://dx.doi.org/10.1590/S0100-879X2004000600005] [PMID: 15264023]
[29]
Bode, C.; Bode, J.C. Alcohol’s role in gastrointestinal tract disorders. Alcohol Health Res. World, 1997, 21(1), 76-83.
[PMID: 15706765]
[30]
Bode, C.; Bode, J.C. Effect of alcohol consumption on the gut. Best Pract. Res. Clin. Gastroenterol., 2003, 17(4), 575-592.
[http://dx.doi.org/10.1016/S1521-6918(03)00034-9] [PMID: 12828956]
[31]
Maillot, F.; Farad, S.; Lamisse, F. Alcohol and nutrition. Pathol. Biol. (Paris), 2001, 49(9), 683-688.
[http://dx.doi.org/10.1016/S0369-8114(01)00234-6] [PMID: 11762129]
[32]
Lee, S.J.; Kang, M.H.; Min, H. Folic acid supplementation reduces oxidative stress and hepatic toxicity in rats treated chronically with ethanol. Nutr. Res. Pract., 2011, 5(6), 520-526.
[http://dx.doi.org/10.4162/nrp.2011.5.6.520] [PMID: 22259676]
[33]
Wang, Z.; Wu, X.; Zhang, Y.; Zhou, L.; Li, L.; Yu, Y.; Wang, L. Discrepant roles of CpG ODN on acute alcohol-induced liver injury in mice. Int. Immunopharmacol., 2012, 12(3), 526-533.
[http://dx.doi.org/10.1016/j.intimp.2012.01.007] [PMID: 22293535]
[34]
Qing, L.; Wang, T. Lactic acid bacteria prevent alcohol-induced steatohepatitis in rats by acting on the pathways of alcohol metabolism. Clin. Exp. Med., 2008, 8(4), 187-191.
[http://dx.doi.org/10.1007/s10238-008-0002-4] [PMID: 18813871]
[35]
Caballería, J. Current concepts in alcohol metabolism. Ann. Hepatol., 2003, 2(2), 60-68.
[http://dx.doi.org/10.1016/S1665-2681(19)32143-X] [PMID: 15041893]
[36]
Lacy, E.R.; Ito, S. Rapid epithelial restitution of the rat gastric mucosa after ethanol injury. Lab. Invest., 1984, 51(5), 573-583.
[PMID: 6492759]
[37]
Laine, L.; Takeuchi, K.; Tarnawski, A. Gastric mucosal defense and cytoprotection: bench to bedside. Gastroenterology, 2008, 135(1), 41-60.
[http://dx.doi.org/10.1053/j.gastro.2008.05.030] [PMID: 18549814]
[38]
Woof, J.M.; Kerr, M.A. The function of immunoglobulin A in immunity. J. Pathol., 2006, 208(2), 270-282.
[http://dx.doi.org/10.1002/path.1877] [PMID: 16362985]
[39]
Palm, N.W.; de Zoete, M.R.; Flavell, R.A. Immune-microbiota interactions in health and disease. Clin. Immunol., 2015, 159(2), 122-127.
[http://dx.doi.org/10.1016/j.clim.2015.05.014] [PMID: 26141651]
[40]
Boullier, S.; Tanguy, M.; Kadaoui, K.A.; Caubet, C.; Sansonetti, P.; Corthésy, B.; Phalipon, A. Secretory IgA-mediated neutralization of Shigella flexneri prevents intestinal tissue destruction by down-regulating inflammatory circuits. J. Immunol., 2009, 183(9), 5879-5885.
[http://dx.doi.org/10.4049/jimmunol.0901838] [PMID: 19828639]
[41]
Waszkiewicz, N.; Szajda, S.D.; Jankowska, A.; Zwierz, P.; Czernikiewicz, A.; Szulc, A.; Zwierz, K. The effect of acute ethanol intoxication on salivary proteins of innate and adaptive immunity. Alcohol. Clin. Exp. Res., 2008, 32(4), 652-656.
[http://dx.doi.org/10.1111/j.1530-0277.2007.00613.x] [PMID: 18241314]
[42]
Gonzalez-Quintela, A.; Vidal, C.; Gude, F. Alcohol, IgE and allergy. Addict. Biol., 2004, 9(3-4), 195-204.
[http://dx.doi.org/10.1080/13556210412331292235] [PMID: 15511713]
[43]
Heinz, R.; Waltenbaugh, C. Ethanol consumption modifies dendritic cell antigen presentation in mice. Alcohol. Clin. Exp. Res., 2007, 31(10), 1759-1771.
[http://dx.doi.org/10.1111/j.1530-0277.2007.00479.x] [PMID: 17850646]
[44]
González-Quintela, A.; Vidal, C.; Gude, F.; Tomé, S.; Lojo, S.; Lorenzo, M.J.; Becerra, E.P.; Martínez-Vazquez, J.M.; Barrio, E. Increased serum IgE in alcohol abusers. Clin. Exp. Allergy, 1995, 25(8), 756-764.
[http://dx.doi.org/10.1111/j.1365-2222.1995.tb00014.x] [PMID: 7584688]
[45]
González-Quintela, A.; Vidal, C.; Lojo, S.; Pérez, L.F.; Otero-Antón, E.; Gude, F.; Barrio, E. Serum cytokines and increased total serum IgE in alcoholics. Ann. Allergy Asthma Immunol., 1999, 83(1), 61-67.
[http://dx.doi.org/10.1016/S1081-1206(10)63514-4] [PMID: 10437818]
[46]
Peterson, J.D.; Herzenberg, L.A.; Vasquez, K.; Waltenbaugh, C. Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc. Natl. Acad. Sci. USA, 1998, 95(6), 3071-3076.
[http://dx.doi.org/10.1073/pnas.95.6.3071] [PMID: 9501217]
[47]
Bacharier, L.B.; Geha, R.S. Molecular mechanisms of IgE regulation. J. Allergy Clin. Immunol., 2000, 105(2 Pt 2), S547-S558.
[http://dx.doi.org/10.1016/S0091-6749(00)90059-9] [PMID: 10669540]
[48]
Prakash, S.; Tomaro-Duchesneau, C.; Saha, S.; Rodes, L.; Kahouli, I.; Malhotra, M. Probiotics for the prevention and treatment of allergies, with an emphasis on mode of delivery and mechanism of action. Curr. Pharm. Des., 2014, 20(6), 1025-1037.
[http://dx.doi.org/10.2174/138161282006140220145154] [PMID: 23701572]
[49]
Aitoro, R.; Paparo, L.; Amoroso, A.; Di Costanzo, M.; Cosenza, L.; Granata, V.; Di Scala, C.; Nocerino, R.; Trinchese, G.; Montella, M.; Ercolini, D.; Berni Canani, R. Gut microbiota as a target for preventive and therapeutic intervention against food allergy. Nutrients, 2017, 9(7), E672.
[http://dx.doi.org/10.3390/nu9070672] [PMID: 28657607]
[50]
Simpson, M.R.; Dotterud, C.K.; Storrø, O.; Johnsen, R.; Øien, T. Perinatal probiotic supplementation in the prevention of allergy related disease: 6 year follow up of a randomised controlled trial. BMC Dermatol., 2015, 15, 13.
[http://dx.doi.org/10.1186/s12895-015-0030-1] [PMID: 26232126]
[51]
Ai, C.; Zhang, Q.; Ren, C.; Wang, G.; Liu, X.; Tian, F.; Zhao, J.; Zhang, H.; Chen, Y.Q.; Chen, W. Genetically engineered Lactococcus lactis protect against house dust mite allergy in a BALB/c mouse model. PLoS One, 2014, 9(10), e109461.
[http://dx.doi.org/10.1371/journal.pone.0109461] [PMID: 25290938]
[52]
Gore, C.; Custovic, A.; Tannock, G.W.; Munro, K.; Kerry, G.; Johnson, K.; Peterson, C.; Morris, J.; Chaloner, C.; Murray, C.S.; Woodcock, A. Treatment and secondary prevention effects of the probiotics Lactobacillus paracasei or Bifidobacterium lactis on early infant eczema: randomized controlled trial with follow-up until age 3 years. Clin. Exp. Allergy, 2012, 42(1), 112-122.
[http://dx.doi.org/10.1111/j.1365-2222.2011.03885.x] [PMID: 22092692]
[53]
de Azevedo, M.S.; Innocentin, S.; Dorella, F.A.; Rocha, C.S.; Mariat, D.; Pontes, D.S.; Miyoshi, A.; Azevedo, V.; Langella, P.; Chatel, J.M. Immunotherapy of allergic diseases using probiotics or recombinant probiotics. J. Appl. Microbiol., 2013, 115(2), 319-333.
[http://dx.doi.org/10.1111/jam.12174] [PMID: 23437848]
[54]
Debarry, J.; Garn, H.; Hanuszkiewicz, A.; Dickgreber, N.; Blümer, N.; von Mutius, E.; Bufe, A.; Gatermann, S.; Renz, H.; Holst, O.; Heine, H. Acinetobacter lwoffii and Lactococcus lactis strains isolated from farm cowsheds possess strong allergy-protective properties. J. Allergy Clin. Immunol., 2007, 119(6), 1514-1521.
[http://dx.doi.org/10.1016/j.jaci.2007.03.023] [PMID: 17481709]
[55]
Stein, K.; Brand, S.; Jenckel, A.; Sigmund, A.; Chen, Z.J.; Kirschning, C.J.; Kauth, M.; Heine, H. Endosomal recognition of Lactococcus lactis G121 and its RNA by dendritic cells is key to its allergy-protective effects. J. Allergy Clin. Immunol., 2017, 139(2), 667-678.e5.
[http://dx.doi.org/10.1016/j.jaci.2016.06.018] [PMID: 27544739]
[56]
Franke, A.; Nakchbandi, I.A.; Schneider, A.; Harder, H.; Singer, M.V. The effect of ethanol and alcoholic beverages on gastric emptying of solid meals in humans. Alcohol Alcohol., 2005, 40(3), 187-193.
[http://dx.doi.org/10.1093/alcalc/agh138] [PMID: 15699055]
[57]
Rao, R. Endotoxemia and gut barrier dysfunction in alcoholic liver disease. Hepatology, 2009, 50(2), 638-644.
[http://dx.doi.org/10.1002/hep.23009] [PMID: 19575462]
[58]
Rajendram, R.; Preedy, V.R. Effect of alcohol consumption on the gut. Dig. Dis., 2005, 23(3-4), 214-221.
[http://dx.doi.org/10.1159/000090168] [PMID: 16508285]
[59]
Bradley, L.M.; Dalton, D.K.; Croft, M. A direct role for IFN-gamma in regulation of Th1 cell development. J. Immunol., 1996, 157(4), 1350-1358.
[PMID: 8759714]
[60]
Kühn, R.; Löhler, J.; Rennick, D.; Rajewsky, K.; Müller, W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell, 1993, 75(2), 263-274.
[http://dx.doi.org/10.1016/0092-8674(93)80068-P] [PMID: 8402911]

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