Limosilactobacillus fermentum CECT5716: Mechanisms and Therapeutic Insights
Abstract
:1. Introduction
- Competitive exclusion of pathogenic microorganisms. This occurs when one species of bacteria competes for receptor sites in the intestinal tract more actively than other species [2].
- Enhancement of intestinal barrier function. The intestinal barrier function plays an important role in the absorption of nutrients from food and, at the same time, prevents the access of potentially harmful bacteria to the human body [3]. When the gut barrier is disrupted, food antigens and pathogenic microorganisms can develop intestinal disorders, mainly associated with a local inflammatory response [4]. It has been proposed that probiotics maintain the epithelial barrier function, through increased expression of junction proteins or mucins, and promote intestinal epithelial cell activation in response to bacterial infection [5,6].
- Production of bacteriocins. These are antimicrobial peptides that prevent the proliferation of selected pathogens [7].
- Improvement of the altered microbiota composition. In normal conditions, the gut is colonized by a large number of microorganisms in balance, to provide energy and nutrition, maintain the intestinal immune homeostasis and protect the intestinal structure [8]. This balance is altered in many diseases, leading to a situation known as dysbiosis [9].
2. Limosilactobacillus fermentum
2.1. Limosilactobacillus fermentum CECT5716
2.1.1. Preclinical Studies
- In vitro studies
- Epithelial cells.
- CMT-93 cell line.
- b.
- Caco-2 cell line.
- 2.
- Macrophages
- Bone marrow-derived macrophages (BMDM).
- b.
- RAW 264.7 cells.
- c.
- Peripheral blood mononuclear cells.
- Animal models.
- Models of experimental colitis.
- TNBS-induced colitis in rats.
- b.
- DNBS-induced colitis in mice.
- c.
- DSS-induced colitis in mice.
- Metabolic syndrome.
- Systemic Lupus Erythematosus.
- Pregnancy and lactation.
2.1.2. Human Trials
- Mastitis
- Viral infections
- Pediatric infections
3. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Health and Nutritional Properties and Guidelines for Evaluation; FAO Food and Nutrition Paper; WHO: Geneva, Switzerland; FAO: Rome, Italy, 2006.
- Munoz-Quezada, S.; Bermudez-Brito, M.; Chenoll, E.; Genoves, S.; Gomez-Llorente, C.; Plaza-Diaz, J.; Matencio, E.; Bernal, M.J.; Romero, F.; Ramon, D.; et al. Competitive inhibition of three novel bacteria isolated from faeces of breast milk-fed infants against selected enteropathogens. Br. J. Nutr. 2013, 109 (Suppl. 2), S63–S69. [Google Scholar] [CrossRef] [Green Version]
- Ohland, C.L.; Macnaughton, W.K. Probiotic bacteria and intestinal epithelial barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298, G807–G819. [Google Scholar] [CrossRef] [Green Version]
- Camilleri, M.; Madsen, K.; Spiller, R.; Greenwood-Van Meerveld, B.; Verne, G.N. Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol. Motil. 2012, 24, 503–512. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Zhu, Y.H.; Yang, J.C.; Yang, G.Y.; Zhou, D.; Wang, J.F. A selected Lactobacillus rhamnosus strain promotes EGFR-independent Akt activation in an enterotoxigenic Escherichia coli K88-infected IPEC-J2 cell model. PLoS ONE 2015, 10, e0125717. [Google Scholar] [CrossRef] [PubMed]
- Hummel, S.; Veltman, K.; Cichon, C.; Sonnenborn, U.; Schmidt, M.A. Differential targeting of the E-Cadherin/beta-Catenin complex by gram-positive probiotic lactobacilli improves epithelial barrier function. Appl. Environ. Microbiol. 2012, 78, 1140–1147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bermudez-Brito, M.; Plaza-Diaz, J.; Munoz-Quezada, S.; Gomez-Llorente, C.; Gil, A. Probiotic mechanisms of action. Ann. Nutr. Metab. 2012, 61, 160–174. [Google Scholar] [CrossRef]
- Azad, M.A.K.; Sarker, M.; Li, T.; Yin, J. Probiotic species in the modulation of gut microbiota: An overview. Biomed. Res. Int. 2018, 2018, 9478630. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tojo, R.; Suarez, A.; Clemente, M.G.; de los Reyes-Gavilan, C.G.; Margolles, A.; Gueimonde, M.; Ruas-Madiedo, P. Intestinal microbiota in health and disease: Role of bifidobacteria in gut homeostasis. World J. Gastroenterol. 2014, 20, 15163–15176. [Google Scholar] [CrossRef] [PubMed]
- Azad, M.A.K.; Sarker, M.; Wan, D. Immunomodulatory effects of robiotics on cytokine profiles. Biomed. Res. Int. 2018, 2018, 8063647. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guarner, F.; Malagelada, J.R. Gut flora in health and disease. Lancet 2003, 361, 512–519. [Google Scholar] [CrossRef]
- Bintsis, T. Lactic acid bacteria as starter cultures: An update in their metabolism and genetics. AIMS Microbiol. 2018, 4, 665–684. [Google Scholar] [CrossRef]
- Engesser, D.M.; Hammes, W.P. Non-heme catalase activity of lactic acid bacteria. Syst. Appl. Microbiol. 1994, 17, 11–19. [Google Scholar] [CrossRef]
- Stiles, M.E.; Holzapfel, W.H. Lactic acid bacteria of foods and their current taxonomy. Int. J. Food Microbiol. 1997, 36, 1–29. [Google Scholar] [CrossRef]
- Ait Seddik, H.; Bendali, F.; Cudennec, B.; Drider, D. Anti-pathogenic and probiotic attributes of Lactobacillus salivarius and Lactobacillus plantarum strains isolated from feces of Algerian infants and adults. Res. Microbiol. 2017, 168, 244–254. [Google Scholar] [CrossRef] [PubMed]
- Haakensen, M.; Dobson, C.M.; Hill, J.E.; Ziola, B. Reclassification of Pediococcus dextrinicus (Coster and White 1964) back 1978 (Approved Lists 1980) as Lactobacillus dextrinicus comb. nov., and emended description of the genus Lactobacillus. Int. J. Syst. Evol. Microbiol. 2009, 59, 615–621. [Google Scholar] [CrossRef] [PubMed]
- Salvetti, E.; Torriani, S.; Felis, G.E. The genus Lactobacillus: A axonomic update. Probiotics Antimicrob. Proteins 2012, 4, 217–226. [Google Scholar] [CrossRef] [PubMed]
- Zheng, J.; Wittouck, S.; Salvetti, E.; Franz, C.; Harris, H.M.B.; Mattarelli, P.; O’Toole, P.W.; Pot, B.; Vandamme, P.; Walter, J.; et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 2020, 70, 2782–2858. [Google Scholar] [CrossRef]
- Nielsen, D.S.; Cho, G.S.; Hanak, A.; Huch, M.; Franz, C.M.; Arneborg, N. The effect of bacteriocin-producing Lactobacillus plantarum strains on the intracellular pH of sessile and planktonic Listeria monocytogenes single cells. Int. J. Food Microbiol. 2010, 141 (Suppl. 1), S53–S59. [Google Scholar] [CrossRef]
- Coton, M.; Berthier, F.; Coton, E. Rapid identification of the three major species of dairy obligate heterofermenters Lactobacillus brevis, Lactobacillus fermentum and Lactobacillus parabuchneri by species-specific duplex PCR. FEMS Microbiol. Lett. 2008, 284, 150–157. [Google Scholar] [CrossRef]
- Russo, P.; Capozzi, V.; Arena, M.P.; Spadaccino, G.; Duenas, M.T.; Lopez, P.; Fiocco, D.; Spano, G. Riboflavin-overproducing strains of Lactobacillus fermentum for riboflavin-enriched bread. Appl. Microbiol. Biotechnol. 2014, 98, 3691–3700. [Google Scholar] [CrossRef]
- Kaban, G.; Kaya, M. Identification of lactic acid bacteria and Gram-positive catalase-positive cocci isolated from naturally fermented sausage (sucuk). J. Food Sci. 2008, 73, M385–M388. [Google Scholar] [CrossRef]
- Martin, R.; Langa, S.; Reviriego, C.; Jiminez, E.; Marin, M.L.; Xaus, J.; Fernandez, L.; Rodriguez, J.M. Human milk is a source of lactic acid bacteria for the infant gut. J. Pediatr. 2003, 143, 754–758. [Google Scholar] [CrossRef] [PubMed]
- Dal Bello, F.; Hertel, C. Oral cavity as natural reservoir for intestinal lactobacilli. Syst. Appl. Microbiol. 2006, 29, 69–76. [Google Scholar] [CrossRef] [PubMed]
- Jang, Y.J.; Kim, W.K.; Han, D.H.; Lee, K.; Ko, G. Lactobacillus fermentum species ameliorate dextran sulfate sodium-induced colitis by regulating the immune response and altering gut microbiota. Gut Microbes 2019, 10, 696–711. [Google Scholar] [CrossRef]
- Naghmouchi, K.; Belguesmia, Y.; Bendali, F.; Spano, G.; Seal, B.S.; Drider, D. Lactobacillus fermentum: A bacterial species with potential for food preservation and biomedical applications. Crit. Rev. Food Sci. Nutr. 2020, 60, 3387–3399. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez-Nogales, A.; Algieri, F.; Garrido-Mesa, J.; Vezza, T.; Utrilla, M.P.; Chueca, N.; Garcia, F.; Olivares, M.; Rodriguez-Cabezas, M.E.; Galvez, J. Differential intestinal anti-inflammatory effects of Lactobacillus fermentum and Lactobacillus salivarius in DSS mouse colitis: Impact on microRNAs expression and microbiota composition. Mol. Nutr. Food Res. 2017, 61, 1700144. [Google Scholar] [CrossRef] [PubMed]
- Maldonado, J.; Canabate, F.; Sempere, L.; Vela, F.; Sanchez, A.R.; Narbona, E.; Lopez-Huertas, E.; Geerlings, A.; Valero, A.D.; Olivares, M.; et al. Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. J. Pediatr. Gastroenterol. Nutr. 2012, 54, 55–61. [Google Scholar] [CrossRef]
- Nardone, G.; Compare, D.; Liguori, E.; Di Mauro, V.; Rocco, A.; Barone, M.; Napoli, A.; Lapi, D.; Iovene, M.R.; Colantuoni, A. Protective effects of Lactobacillus paracasei F19 in a rat model of oxidative and metabolic hepatic injury. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G669–G676. [Google Scholar] [CrossRef] [Green Version]
- Melo, T.A.; Dos Santos, T.F.; Pereira, L.R.; Passos, H.M.; Rezende, R.P.; Romano, C.C. Functional profile evaluation of Lactobacillus fermentum tcuesc01: A new potential probiotic strain isolated during cocoa fermentation. Biomed. Res. Int. 2017, 2017, 5165916. [Google Scholar] [CrossRef] [Green Version]
- Strompfova, V.; Kubasova, I.; Laukova, A. Health benefits observed after probiotic Lactobacillus fermentum CCM 7421 application in dogs. Appl. Microbiol. Biotechnol. 2017, 101, 6309–6319. [Google Scholar] [CrossRef]
- Barone, M.V.; Zimmer, K.P. Endocytosis and transcytosis of gliadin peptides. Mol. Cell Pediatr. 2016, 3, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garcia-Castillo, V.; Komatsu, R.; Clua, P.; Indo, Y.; Takagi, M.; Salva, S.; Islam, M.A.; Alvarez, S.; Takahashi, H.; Garcia-Cancino, A.; et al. Evaluation of the immunomodulatory activities of the probiotic strain Lactobacillus fermentum UCO-979C. Front. Immunol. 2019, 10, 1376. [Google Scholar] [CrossRef] [Green Version]
- Kang, M.S.; Lim, H.S.; Oh, J.S.; Lim, Y.J.; Wuertz-Kozak, K.; Harro, J.M.; Shirtliff, M.E.; Achermann, Y. Antimicrobial activity of Lactobacillus salivarius and Lactobacillus fermentum against Staphylococcus aureus. Pathog. Dis. 2017, 75. [Google Scholar] [CrossRef]
- Rossoni, R.D.; Dos Santos Velloso, M.; Figueiredo, L.M.A.; Martins, C.P.; Jorge, A.O.C.; Junqueira, J.C. Clinical strains of Lactobacillus reduce the filamentation of Candida albicans and protect Galleria mellonella against experimental candidiasis. Folia Microbiol. 2018, 63, 307–314. [Google Scholar] [CrossRef] [Green Version]
- Garcia, A.; Saez, K.; Delgado, C.; Gonzalez, C.L. Low co-existence rates of Lactobacillus spp. and Helicobacter pylori detected in gastric biopsies from patients with gastrointestinal symptoms. Rev. Esp. Enferm. Dig. 2012, 104, 473–478. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lehri, B.; Seddon, A.M.; Karlyshev, A.V. Lactobacillus fermentum 3872 as a potential tool for combatting Campylobacter jejuni infections. Virulence 2017, 8, 1753–1760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ghazvini, R.D.; Kouhsari, E.; Zibafar, E.; Hashemi, S.J.; Amini, A.; Niknejad, F. Antifungal activity and aflatoxin degradation of Bifidobacterium bifidum and Lactobacillus fermentum against toxigenic Aspergillus parasiticus. Open Microbiol. J. 2016, 10, 197–201. [Google Scholar] [CrossRef] [PubMed]
- Fuochi, V.; Volti, G.L.; Furneri, P.M. Probiotic properties of Lactobacillus fermentum strains isolated from human oral samples and description of their antibacterial activity. Curr. Pharm. Biotechnol. 2017, 18, 138–149. [Google Scholar] [CrossRef] [PubMed]
- Truusalu, K.; Kullisaar, T.; Hutt, P.; Mahlapuu, R.; Aunapuu, M.; Arend, A.; Zilmer, M.; Mikelsaar, R.H.; Mikelsaar, M. Immunological, antioxidative, and morphological response in combined treatment of ofloxacin and Lactobacillus fermentum ME-3 probiotic in Salmonella typhimurium murine model. APMIS 2010, 118, 864–872. [Google Scholar] [CrossRef]
- Mikelsaar, M.; Zilmer, M. Lactobacillus fermentum ME-3—An antimicrobial and antioxidative probiotic. Microb. Ecol. Health Dis. 2009, 21, 1–27. [Google Scholar]
- Garcia-Castillo, V.; Zelaya, H.; Ilabaca, A.; Espinoza-Monje, M.; Komatsu, R.; Albarracin, L.; Kitazawa, H.; Garcia-Cancino, A.; Villena, J. Lactobacillus fermentum UCO-979C beneficially modulates the innate immune response triggered by Helicobacter pylori infection in vitro. Benef. Microbes 2018, 9, 829–841. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.S.; Kim, S.H. Anti-inflammatory and anti-osteoporotic potential of Lactobacillus plantarum A41 and L. fermentum SRK414 as probiotics. Probiotics Antimicrob. Proteins 2020, 12, 623–634. [Google Scholar] [CrossRef]
- Kang, C.H.; Kim, Y.; Han, S.H.; Kim, J.S.; Paek, N.S.; So, J.S. In vitro probiotic properties of vaginal Lactobacillus fermentum MG901 and Lactobacillus plantarum MG989 against Candida albicans. Eur. J. Obstet. Gynecol Reprod. Biol. 2018, 228, 232–237. [Google Scholar] [CrossRef]
- Daniele, M.; Pascual, L.; Barberis, L. Curative effect of the probiotic strain Lactobacillus fermentum L23 in a murine model of vaginal infection by Gardnerella vaginalis. Lett. Appl. Microbiol. 2014, 59, 93–98. [Google Scholar] [CrossRef]
- Persichetti, E.; De Michele, A.; Codini, M.; Traina, G. Antioxidative capacity of Lactobacillus fermentum LF31 evaluated in vitro by oxygen radical absorbance capacity assay. Nutrition 2014, 30, 936–938. [Google Scholar] [CrossRef] [PubMed]
- Zhang, D.I.; Li, C.; Shi, R.; Zhao, F.; Yang, Z. Lactobacillus fermentum JX306 Restrain D-galactose-induced oxidative stress of mice through its antioxidant activity. Pol. J. Microbiol. 2020, 69, 205–215. [Google Scholar] [CrossRef]
- Reid, G.; Charbonneau, D.; Erb, J.; Kochanowski, B.; Beuerman, D.; Poehner, R.; Bruce, A.W. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: Randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol. Med. Microbiol. 2003, 35, 131–134. [Google Scholar] [CrossRef] [Green Version]
- West, N.P.; Pyne, D.B.; Cripps, A.W.; Hopkins, W.G.; Eskesen, D.C.; Jairath, A.; Christophersen, C.T.; Conlon, M.A.; Fricker, P.A. Lactobacillus fermentum (PCC(R)) supplementation and gastrointestinal and respiratory-tract illness symptoms: A randomised control trial in athletes. Nutr. J. 2011, 10, 30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weston, S.; Halbert, A.; Richmond, P.; Prescott, S.L. Effects of probiotics on atopic dermatitis: A randomised controlled trial. Arch. Dis. Child. 2005, 90, 892–897. [Google Scholar] [CrossRef] [PubMed]
- Murina, F.; Graziottin, A.; Vicariotto, F.; De Seta, F. Can Lactobacillus fermentum LF10 and Lactobacillus acidophilus LA02 in a slow-release vaginal product be useful for prevention of recurrent vulvovaginal candidiasis?: A clinical study. J. Clin. Gastroenterol. 2014, 48 (Suppl. 1), S102–S105. [Google Scholar] [CrossRef] [Green Version]
- Vicariotto, F.; Mogna, L.; Del Piano, M. Effectiveness of the two microorganisms Lactobacillus fermentum LF15 and Lactobacillus plantarum LP01, formulated in slow-release vaginal tablets, in women affected by bacterial vaginosis: A pilot study. J. Clin. Gastroenterol. 2014, 48 (Suppl. 1), S106–S112. [Google Scholar] [CrossRef] [PubMed]
- Songisepp, E.; Kals, J.; Kullisaar, T.; Mandar, R.; Hutt, P.; Zilmer, M.; Mikelsaar, M. Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers. Nutr. J. 2005, 4, 22. [Google Scholar] [CrossRef] [Green Version]
- Kullisaar, T.; Zilmer, K.; Salum, T.; Rehema, A.; Zilmer, M. The use of probiotic L. fermentum ME-3 containing Reg’Activ Cholesterol supplement for 4 weeks has a positive influence on blood lipoprotein profiles and inflammatory cytokines: An open-label preliminary study. Nutr. J. 2016, 15, 93. [Google Scholar] [CrossRef] [Green Version]
- Hutt, P.; Andreson, H.; Kullisaar, T.; Vihalemm, T.; Unt, E.; Kals, J.; Kampus, P.; Zilmer, M.; Mikelsaar, M. Effects of a synbiotic product on blood antioxidative activity in subjects colonized with Helicobacter pylori. Lett. Appl. Microbiol. 2009, 48, 797–800. [Google Scholar]
- Ehrstrom, S.; Daroczy, K.; Rylander, E.; Samuelsson, C.; Johannesson, U.; Anzen, B.; Pahlson, C. Lactic acid bacteria colonization and clinical outcome after probiotic supplementation in conventionally treated bacterial vaginosis and vulvovaginal candidiasis. Microbes Infect. 2010, 12, 691–699. [Google Scholar] [CrossRef] [PubMed]
- Toral, M.; Robles-Vera, I.; Romero, M.; de la Visitacion, N.; Sanchez, M.; O’Valle, F.; Rodriguez-Nogales, A.; Galvez, J.; Duarte, J.; Jimenez, R. Lactobacillus fermentum CECT5716: A novel alternative for the prevention of vascular disorders in a mouse model of systemic lupus erythematosus. FASEB J. 2019, 33, 10005–10018. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Algieri, F.; Garrido-Mesa, J.; Vezza, T.; Rodriguez-Sojo, M.J.; Rodriguez-Cabezas, M.E.; Olivares, M.; Garcia, F.; Galvez, J.; Moron, R.; Rodriguez-Nogales, A. Intestinal anti-inflammatory effects of probiotics in DNBS-colitis via modulation of gut microbiota and microRNAs. Eur. J. Nutr. 2020. [Google Scholar] [CrossRef]
- Jimenez, E.; Langa, S.; Martin, V.; Arroyo, R.; Martin, R.; Fernandez, L.; Rodriguez, J.M. Complete genome sequence of Lactobacillus fermentum CECT 5716, a probiotic strain isolated from human milk. J. Bacteriol. 2010, 192, 4800. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, N.; Heruth, D.P.; Wu, W.; Zhang, L.Q.; Nsumu, M.N.; Shortt, K.; Li, K.; Jiang, X.; Wang, B.; Friesen, C.; et al. Functional characterization of SLC26A3 c.392C>G (p.P131R) mutation in intestinal barrier function using CRISPR/CAS9-created cell models. Cell Biosci. 2019, 9, 40. [Google Scholar] [CrossRef] [Green Version]
- Lee, Y.S.; Lee, E.K.; Han, I.O.; Park, S.H. Etoposide-induced Smad6 expression is required for the G1 to S phase transition of the cell cycle in CMT-93 mouse intestinal epithelial cells. Exp. Mol. Med. 2008, 40, 43–51. [Google Scholar] [CrossRef]
- Ponce de Leon-Rodriguez, M.D.C.; Guyot, J.P.; Laurent-Babot, C. Intestinal in vitro cell culture models and their potential to study the effect of food components on intestinal inflammation. Crit. Rev. Food Sci. Nutr. 2019, 59, 3648–3666. [Google Scholar] [CrossRef]
- Arribas, B.; Garrido-Mesa, N.; Peran, L.; Camuesco, D.; Comalada, M.; Bailon, E.; Olivares, M.; Xaus, J.; Kruidenier, L.; Sanderson, I.R.; et al. The immunomodulatory properties of viable Lactobacillus salivarius ssp. salivarius CECT5713 are not restricted to the large intestine. Eur. J. Nutr. 2012, 51, 365–374. [Google Scholar]
- Vezza, T.; Algieri, F.; Garrido-Mesa, J.; Utrilla, M.P.; Rodriguez-Cabezas, M.E.; Banos, A.; Guillamon, E.; Garcia, F.; Rodriguez-Nogales, A.; Galvez, J. The immunomodulatory properties of propyl-propane thiosulfonate contribute to its intestinal anti-inflammatory effect in experimental colitis. Mol. Nutr. Food Res. 2019, 63, e1800653. [Google Scholar] [CrossRef]
- Rodriguez-Nogales, A.; Algieri, F.; Vezza, T.; Garrido-Mesa, N.; Olivares, M.; Comalada, M.; Riccardi, C.; Utrilla, M.P.; Rodriguez-Cabezas, M.E.; Galvez, J. The viability of Lactobacillus fermentum CECT5716 is not essential to exert intestinal anti-inflammatory properties. Food Funct. 2015, 6, 1176–1184. [Google Scholar] [CrossRef]
- Arpa, L.; Valledor, A.F.; Lloberas, J.; Celada, A. IL-4 blocks M-CSF-dependent macrophage proliferation by inducing p21Waf1 in a STAT6-dependent way. Eur. J. Immunol. 2009, 39, 514–526. [Google Scholar] [CrossRef]
- Garrido-Mesa, J.; Rodriguez-Nogales, A.; Algieri, F.; Vezza, T.; Hidalgo-Garcia, L.; Garrido-Barros, M.; Utrilla, M.P.; Garcia, F.; Chueca, N.; Rodriguez-Cabezas, M.E.; et al. Immunomodulatory tetracyclines shape the intestinal inflammatory response inducing mucosal healing and resolution. Br. J. Pharmacol. 2018, 175, 4353–4370. [Google Scholar] [CrossRef] [PubMed]
- Sundaramurthy, V.; Barsacchi, R.; Samusik, N.; Marsico, G.; Gilleron, J.; Kalaidzidis, I.; Meyenhofer, F.; Bickle, M.; Kalaidzidis, Y.; Zerial, M. Integration of chemical and RNAi multiparametric profiles identifies triggers of intracellular mycobacterial killing. Cell Host Microbe 2013, 13, 129–142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shishodia, S.; Sodhi, A.; Shrivastava, A. Cisplatin-induced activation of murine bone marrow-derived macrophages require protein tyrosine phosphorylation. Int. J. Immunopharmacol. 1997, 19, 683–690. [Google Scholar] [CrossRef]
- Campbell, G.M.; Nicol, M.Q.; Dransfield, I.; Shaw, D.J.; Nash, A.A.; Dutia, B.M. Susceptibility of bone marrow-derived macrophages to influenza virus infection is dependent on macrophage phenotype. J. Gen. Virol. 2015, 96, 2951–2960. [Google Scholar] [CrossRef] [Green Version]
- Diaz-Ropero, M.P.; Martin, R.; Sierra, S.; Lara-Villoslada, F.; Rodriguez, J.M.; Xaus, J.; Olivares, M. Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response. J. Appl. Microbiol. 2007, 102, 337–343. [Google Scholar] [CrossRef]
- Chapman, C.G.; Pekow, J. The emerging role of miRNAs in inflammatory bowel disease: A review. Therap. Adv. Gastroenterol. 2015, 8, 4–22. [Google Scholar] [CrossRef] [Green Version]
- Evel-Kabler, K.; Song, X.T.; Aldrich, M.; Huang, X.F.; Chen, S.Y. SOCS1 restricts dendritic cells’ ability to break self tolerance and induce antitumor immunity by regulating IL-12 production and signaling. J. Clin. Investig. 2006, 116, 90–100. [Google Scholar] [CrossRef] [Green Version]
- Goto, Y.; Kiyono, H. Epithelial cell microRNAs in gut immunity. Nat. Immunol. 2011, 12, 195–197. [Google Scholar] [CrossRef]
- Garikipati, V.N.S.; Verma, S.K.; Jolardarashi, D.; Cheng, Z.; Ibetti, J.; Cimini, M.; Tang, Y.; Khan, M.; Yue, Y.; Benedict, C.; et al. Therapeutic inhibition of miR-375 attenuates post-myocardial infarction inflammatory response and left ventricular dysfunction via PDK-1-AKT signalling axis. Cardiovasc. Res. 2017, 113, 938–949. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, C.; Shi, Y.; Wu, R.; Sun, M.; Fang, L.; Wu, W.; Liu, C.; Tang, M.; Li, Z.; Wang, P.; et al. miR-301a promotes intestinal mucosal inflammation through induction of IL-17A and TNF-alpha in IBD. Gut 2016, 65, 1938–1950. [Google Scholar] [CrossRef] [PubMed]
- Raschke, W.C.; Baird, S.; Ralph, P.; Nakoinz, I. Functional macrophage cell lines transformed by Abelson leukemia virus. Cell 1978, 15, 261–267. [Google Scholar] [CrossRef]
- Cheng, L.; Ren, Y.; Lin, D.; Peng, S.; Zhong, B.; Ma, Z. The anti-inflammatory properties of Citrus wilsonii tanaka extract in LPS-induced RAW 264.7 and primary mouse bone marrow-derived dendritic cells. Molecules 2017, 22, 1213. [Google Scholar] [CrossRef] [PubMed]
- Abiodun, O.O.; Rodriguez-Nogales, A.; Algieri, F.; Gomez-Caravaca, A.M.; Segura-Carretero, A.; Utrilla, M.P.; Rodriguez-Cabezas, M.E.; Galvez, J. Antiinflammatory and immunomodulatory activity of an ethanolic extract from the stem bark of Terminalia catappa L. (Combretaceae): In vitro and in vivo evidences. J. Ethnopharmacol. 2016, 192, 309–319. [Google Scholar] [CrossRef]
- Germolec, D.R.; Shipkowski, K.A.; Frawley, R.P.; Evans, E. Markers of inflammation. Methods Mol. Biol. 2018, 1803, 57–79. [Google Scholar] [PubMed]
- Roussev, R.G.; Dons’koi, B.V.; Stamatkin, C.; Ramu, S.; Chernyshov, V.P.; Coulam, C.B.; Barnea, E.R. Preimplantation factor inhibits circulating natural killer cell cytotoxicity and reduces CD69 expression: Implications for recurrent pregnancy loss therapy. Reprod. Biomed. Online 2013, 26, 79–87. [Google Scholar] [CrossRef] [Green Version]
- Vezza, T.; Algieri, F.; Rodriguez-Nogales, A.; Garrido-Mesa, J.; Utrilla, M.P.; Talhaoui, N.; Gomez-Caravaca, A.M.; Segura-Carretero, A.; Rodriguez-Cabezas, M.E.; Monteleone, G.; et al. Immunomodulatory properties of Olea europaea leaf extract in intestinal inflammation. Mol. Nutr. Food Res. 2017, 61, 1601066. [Google Scholar] [CrossRef] [PubMed]
- Perez-Cano, F.J.; Dong, H.; Yaqoob, P. In vitrolee immunomodulatory activity of Lactobacillus fermentum CECT5716 and Lactobacillus salivarius CECT5713: Two probiotic strains isolated from human breast milk. Immunobiology 2010, 215, 996–1004. [Google Scholar] [CrossRef]
- Bi, K.; Zhang, X.; Chen, W.; Diao, H. MicroRNAs Regulate intestinal immunity and gut microbiota for gastrointestinal health: A comprehensive review. Genes 2020, 11, 1075. [Google Scholar] [CrossRef] [PubMed]
- Gosiewski, T.; Strus, M.; Fyderek, K.; Kowalska-Duplaga, K.; Wedrychowicz, A.; Jedynak-Wasowicz, U.; Sladek, M.; Pieczarkowski, S.; Adamski, P.; Heczko, P.B. Horizontal distribution of the fecal microbiota in adolescents with inflammatory bowel disease. J. Pediatr. Gastroenterol. Nutr. 2012, 54, 20–27. [Google Scholar] [CrossRef] [PubMed]
- Scharl, M.; Rogler, G. Inflammatory bowel disease pathogenesis: What is new? Curr. Opin. Gastroenterol. 2012, 28, 301–309. [Google Scholar] [CrossRef] [Green Version]
- Basson, A.R.; Lam, M.; Cominelli, F. Complementary and alternative medicine strategies for therapeutic gut microbiota modulation in inflammatory bowel disease and their next-generation approaches. Gastroenterol. Clin. N. Am. 2017, 46, 689–729. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zuo, T.; Ng, S.C. The gut microbiota in the pathogenesis and therapeutics of inflammatory bowel disease. Front. Microbiol. 2018, 9, 2247. [Google Scholar] [CrossRef]
- Dixon, L.J.; Kabi, A.; Nickerson, K.P.; McDonald, C. Combinatorial effects of diet and genetics on inflammatory bowel disease pathogenesis. Inflamm. Bowel Dis. 2015, 21, 912–922. [Google Scholar] [CrossRef]
- Cheng, H.; Guan, X.; Chen, D.; Ma, W. The Th17/Treg cell balance: A gut microbiota-modulated story. Microorganisms 2019, 7, 583. [Google Scholar] [CrossRef] [Green Version]
- Tedelind, S.; Westberg, F.; Kjerrulf, M.; Vidal, A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: A study with relevance to inflammatory bowel disease. World J. Gastroenterol. 2007, 13, 2826–2832. [Google Scholar] [CrossRef]
- Morampudi, V.; Bhinder, G.; Wu, X.; Dai, C.; Sham, H.P.; Vallance, B.A.; Jacobson, K. DNBS/TNBS colitis models: Providing insights into inflammatory bowel disease and effects of dietary fat. J. Vis. Exp. 2014, e51297. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morris, G.P.; Beck, P.L.; Herridge, M.S.; Depew, W.T.; Szewczuk, M.R.; Wallace, J.L. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 1989, 96, 795–803. [Google Scholar] [CrossRef]
- da Silva, M.S.; Sanchez-Fidalgo, S.; Talero, E.; Cardeno, A.; da Silva, M.A.; Villegas, W.; Souza Brito, A.R.; de La Lastra, C.A. Anti-inflammatory intestinal activity of Abarema cochliacarpos (Gomes) Barneby & Grimes in TNBS colitis model. J. Ethnopharmacol. 2010, 128, 467–475. [Google Scholar] [PubMed]
- Peran, L.; Camuesco, D.; Comalada, M.; Nieto, A.; Concha, A.; Adrio, J.L.; Olivares, M.; Xaus, J.; Zarzuelo, A.; Galvez, J. Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int. J. Colorectal Dis. 2006, 21, 737–746. [Google Scholar] [CrossRef] [PubMed]
- van Dieren, J.M.; van Bodegraven, A.A.; Kuipers, E.J.; Bakker, E.N.; Poen, A.C.; van Dekken, H.; Nieuwenhuis, E.E.; van der Woude, C.J. Local application of tacrolimus in distal colitis: Feasible and safe. Inflamm. Bowel Dis. 2009, 15, 193–198. [Google Scholar] [CrossRef] [PubMed]
- Krawisz, J.E.; Sharon, P.; Stenson, W.F. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 1984, 87, 1344–1350. [Google Scholar] [CrossRef]
- Sido, B.; Hack, V.; Hochlehnert, A.; Lipps, H.; Herfarth, C.; Droge, W. Impairment of intestinal glutathione synthesis in patients with inflammatory bowel disease. Gut 1998, 42, 485–492. [Google Scholar] [CrossRef] [Green Version]
- Schonauen, K.; Le, N.; von Arnim, U.; Schulz, C.; Malfertheiner, P.; Link, A. Circulating and fecal micrornas as biomarkers for inflammatory bowel diseases. Inflamm. Bowel Dis. 2018, 24, 1547–1557. [Google Scholar] [CrossRef] [PubMed]
- O’Neill, S.; O’Driscoll, L. Metabolic syndrome: A closer look at the growing epidemic and its associated pathologies. Obes. Rev. 2015, 16, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 2006, 444, 860–867. [Google Scholar] [CrossRef]
- Ding, S.; Chi, M.M.; Scull, B.P.; Rigby, R.; Schwerbrock, N.M.; Magness, S.; Jobin, C.; Lund, P.K. High-fat diet: Bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS ONE 2010, 5, e12191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Esser, N.; Legrand-Poels, S.; Piette, J.; Scheen, A.J.; Paquot, N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res. Clin. Pract. 2014, 105, 141–150. [Google Scholar] [CrossRef] [Green Version]
- Festi, D.; Schiumerini, R.; Eusebi, L.H.; Marasco, G.; Taddia, M.; Colecchia, A. Gut microbiota and metabolic syndrome. World J. Gastroenterol. 2014, 20, 16079–16094. [Google Scholar] [CrossRef] [PubMed]
- Chakaroun, R.M.; Massier, L.; Kovacs, P. Gut microbiome, intestinal permeability, and tissue bacteria in metabolic disease: Perpetrators or bystanders? Nutrients 2020, 12, 1082. [Google Scholar] [CrossRef] [Green Version]
- Leyva-Jimenez, F.J.; Ruiz-Malagon, A.J.; Molina-Tijeras, J.A.; Diez-Echave, P.; Vezza, T.; Hidalgo-Garcia, L.; Lozano-Sanchez, J.; Arraez-Roman, D.; Cenis, J.L.; Lozano-Perez, A.A.; et al. Comparative study of the antioxidant and anti-inflammatory effects of leaf extracts from four different Morus alba genotypes in high fat diet-induced obesity in mice. Antioxidants 2020, 9, 733. [Google Scholar] [CrossRef] [PubMed]
- Kondo, S.; Xiao, J.Z.; Satoh, T.; Odamaki, T.; Takahashi, S.; Sugahara, H.; Yaeshima, T.; Iwatsuki, K.; Kamei, A.; Abe, K. Antiobesity effects of Bifidobacterium breve strain B-3 supplementation in a mouse model with high-fat diet-induced obesity. Biosci. Biotechnol. Biochem. 2010, 74, 1656–1661. [Google Scholar] [CrossRef] [Green Version]
- Zuo, K.; Li, J.; Li, K.; Hu, C.; Gao, Y.; Chen, M.; Hu, R.; Liu, Y.; Chi, H.; Wang, H.; et al. Disordered gut microbiota and alterations in metabolic patterns are associated with atrial fibrillation. Gigascience 2019, 8. [Google Scholar] [CrossRef] [Green Version]
- Zuo, K.; Li, J.; Wang, P.; Liu, Y.; Liu, Z.; Yin, X.; Liu, X.; Yang, X. Duration of persistent atrial fibrillation is associated with alterations in human gut microbiota and metabolic phenotypes. mSystems 2019, 4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Robles-Vera, I.; Toral, M.; de la Visitacion, N.; Sanchez, M.; Gomez-Guzman, M.; Romero, M.; Yang, T.; Izquierdo-Garcia, J.L.; Jimenez, R.; Ruiz-Cabello, J.; et al. Probiotics prevent dysbiosis and the rise in blood pressure in genetic hypertension: Role of short-chain fatty acids. Mol. Nutr. Food Res. 2020, 64, e1900616. [Google Scholar] [CrossRef]
- Gomez-Guzman, M.; Toral, M.; Romero, M.; Jimenez, R.; Galindo, P.; Sanchez, M.; Zarzuelo, M.J.; Olivares, M.; Galvez, J.; Duarte, J. Antihypertensive effects of probiotics Lactobacillus strains in spontaneously hypertensive rats. Mol. Nutr. Food Res. 2015, 59, 2326–2336. [Google Scholar] [CrossRef]
- Rivero-Gutierrez, B.; Gamez-Belmonte, R.; Suarez, M.D.; Lavin, J.L.; Aransay, A.M.; Olivares, M.; Martinez-Augustin, O.; Sanchez de Medina, F.; Zarzuelo, A. A synbiotic composed of Lactobacillus fermentum CECT5716 and FOS prevents the development of fatty acid liver and glycemic alterations in rats fed a high fructose diet associated with changes in the microbiota. Mol. Nutr. Food Res. 2017, 61, 1600622. [Google Scholar] [CrossRef]
- Robles-Vera, I.; Toral, M.; de la Visitacion, N.; Sanchez, M.; Romero, M.; Olivares, M.; Jimenez, R.; Duarte, J. The probiotic Lactobacillus fermentum prevents dysbiosis and vascular oxidative stress in rats with hypertension induced by chronic nitric oxide blockade. Mol. Nutr. Food Res. 2018, 62, e1800298. [Google Scholar] [CrossRef] [PubMed]
- Molina-Tijeras, J.A.; Diez-Echave, P.; Vezza, T.; Hidalgo-Garcia, L.; Ruiz-Malagon, A.J.; Rodriguez-Sojo, M.J.; Romero, M.; Robles-Vera, I.; Garcia, F.; Plaza-Diaz, J.; et al. Lactobacillus fermentum CECT5716 ameliorates high fat diet-induced obesity in mice through modulation of gut microbiota dysbiosis. Pharmacol. Res. 2021, 105471. [Google Scholar] [CrossRef] [PubMed]
- Kim, A.Y.; Park, Y.J.; Pan, X.; Shin, K.C.; Kwak, S.H.; Bassas, A.F.; Sallam, R.M.; Park, K.S.; Alfadda, A.A.; Xu, A.; et al. Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance. Nat. Commun. 2015, 6, 7585. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, W.J.; Dong, H.J.; Jeong, H.U.; Jung, H.H.; Kim, Y.H.; Kim, T.H. Antiobesity effects of Lactobacillus plantarum LMT1-48 accompanied by inhibition of Enterobacter cloacae in the intestine of diet-induced obese mice. J. Med. Food 2019, 22, 560–566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kwon, J.; Kim, B.; Lee, C.; Joung, H.; Kim, B.K.; Choi, I.S.; Hyun, C.K. Comprehensive amelioration of high-fat diet-induced metabolic dysfunctions through activation of the PGC-1alpha pathway by probiotics treatment in mice. PLoS ONE 2020, 15, e0228932. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vargas, E.; Podder, V.; Carrillo Sepulveda, M.A. Physiology, Glucose Transporter Type 4. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2020. [Google Scholar]
- Shepherd, P.R.; Kahn, B.B. Glucose transporters and insulin action--implications for insulin resistance and diabetes mellitus. N. Engl. J. Med. 1999, 341, 248–257. [Google Scholar] [CrossRef]
- Huby, A.C.; Otvos, L., Jr.; Belin de Chantemele, E.J. Leptin induces hypertension and endothelial dysfunction via aldosterone-dependent mechanisms in obese female mice. Hypertension 2016, 67, 1020–1028. [Google Scholar] [CrossRef] [Green Version]
- Teixeira, T.F.; Collado, M.C.; Ferreira, C.L.; Bressan, J.; Peluzio Mdo, C. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr. Res. 2012, 32, 637–647. [Google Scholar] [CrossRef]
- Cani, P.D.; Amar, J.; Iglesias, M.A.; Poggi, M.; Knauf, C.; Bastelica, D.; Neyrinck, A.M.; Fava, F.; Tuohy, K.M.; Chabo, C.; et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007, 56, 1761–1772. [Google Scholar] [CrossRef] [Green Version]
- Ley, R.E.; Backhed, F.; Turnbaugh, P.; Lozupone, C.A.; Knight, R.D.; Gordon, J.I. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA 2005, 102, 11070–11075. [Google Scholar] [CrossRef] [Green Version]
- De Filippo, C.; Cavalieri, D.; Di Paola, M.; Ramazzotti, M.; Poullet, J.B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107, 14691–14696. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bagarolli, R.A.; Tobar, N.; Oliveira, A.G.; Araujo, T.G.; Carvalho, B.M.; Rocha, G.Z.; Vecina, J.F.; Calisto, K.; Guadagnini, D.; Prada, P.O.; et al. Probiotics modulate gut microbiota and improve insulin sensitivity in DIO mice. J. Nutr. Biochem. 2017, 50, 16–25. [Google Scholar] [CrossRef] [Green Version]
- Backhed, F.; Ding, H.; Wang, T.; Hooper, L.V.; Koh, G.Y.; Nagy, A.; Semenkovich, C.F.; Gordon, J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 2004, 101, 15718–15723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanz, I.; Lee, F.E. B cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 2010, 6, 326–337. [Google Scholar] [CrossRef]
- La Paglia, G.M.C.; Leone, M.C.; Lepri, G.; Vagelli, R.; Valentini, E.; Alunno, A.; Tani, C. One year in review 2017: Systemic lupus erythematosus. Clin. Exp. Rheumatol. 2017, 35, 551–561. [Google Scholar]
- Kim, J.W.; Kwok, S.K.; Choe, J.Y.; Park, S.H. Recent advances in our understanding of the link between the intestinal microbiota and systemic lupus erythematosus. Int. J. Mol. Sci. 2019, 20, 4871. [Google Scholar] [CrossRef] [Green Version]
- Lopez, P.; de Paz, B.; Rodriguez-Carrio, J.; Hevia, A.; Sanchez, B.; Margolles, A.; Suarez, A. Th17 responses and natural IgM antibodies are related to gut microbiota composition in systemic lupus erythematosus patients. Sci. Rep. 2016, 6, 24072. [Google Scholar] [CrossRef] [PubMed]
- Toral, M.; Romero, M.; Rodriguez-Nogales, A.; Jimenez, R.; Robles-Vera, I.; Algieri, F.; Chueca-Porcuna, N.; Sanchez, M.; de la Visitacion, N.; Olivares, M.; et al. Lactobacillus fermentum improves tacrolimus-induced hypertension by restoring vascular redox state and improving eNOS coupling. Mol. Nutr. Food Res. 2018, e1800033. [Google Scholar] [CrossRef]
- de la Visitacion, N.; Robles-Vera, I.; Toral, M.; O’Valle, F.; Moleon, J.; Gomez-Guzman, M.; Romero, M.; Duarte, M.; Sanchez, M.; Jimenez, R.; et al. Lactobacillus fermentum CECT5716 prevents renal damage in the NZBWF1 mouse model of systemic lupus erythematosus. Food Funct. 2020, 11, 5266–5274. [Google Scholar] [CrossRef]
- Mueller, N.T.; Bakacs, E.; Combellick, J.; Grigoryan, Z.; Dominguez-Bello, M.G. The infant microbiome development: Mom matters. Trends Mol. Med. 2015, 21, 109–117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spears, J.W.; Weiss, W.P. Role of antioxidants and trace elements in health and immunity of transition dairy cows. Vet. J. 2008, 176, 70–76. [Google Scholar] [CrossRef]
- Azagra-Boronat, I.; Tres, A.; Massot-Cladera, M.; Franch, A.; Castell, M.; Guardiola, F.; Perez-Cano, F.J.; Rodriguez-Lagunas, M.J. Lactobacillus fermentum CECT5716 supplementation in rats during pregnancy and lactation impacts maternal and offspring lipid profile, immune system and microbiota. Cells 2020, 9, 575. [Google Scholar] [CrossRef] [PubMed]
- Delgado, S.; Arroyo, R.; Martin, R.; Rodriguez, J.M. PCR-DGGE assessment of the bacterial diversity of breast milk in women with lactational infectious mastitis. BMC Infect. Dis. 2008, 8, 51. [Google Scholar] [CrossRef] [Green Version]
- Hurtado, J.A.; Maldonado-Lobon, J.A.; Díaz-Ropero, M.P.; Flores-Rojas, K.; Uberos, J.; Leante, J.L.; Affumicato, L.; Couce, M.L.; Garrido, J.M.; Olivares, M.; et al. Oral administration to nursing women of Lactobacillus fermentum CECT5716 prevents lactational mastitis development: A randomized controlled trial. Breastfeed. Med. 2017, 12, 202–209. [Google Scholar] [CrossRef] [Green Version]
- Maldonado-Lobon, J.A.; Diaz-Lopez, M.A.; Carputo, R.; Duarte, P.; Diaz-Ropero, M.P.; Valero, A.D.; Sanudo, A.; Sempere, L.; Ruiz-Lopez, M.D.; Banuelos, O.; et al. Lactobacillus fermentum CECT 5716 reduces Staphylococcus load in the breastmilk of lactating mothers suffering breast pain: A randomized controlled trial. Breastfeed. Med. 2015, 10, 425–432. [Google Scholar] [CrossRef]
- Arroyo, R.; Martin, V.; Maldonado, A.; Jimenez, E.; Fernandez, L.; Rodriguez, J.M. Treatment of infectious mastitis during lactation: Antibiotics versus oral administration of lactobacilli isolated from breast milk. Clin. Infect. Dis. 2010, 50, 1551–1558. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olivares, M.; Diaz-Ropero, M.P.; Sierra, S.; Lara-Villoslada, F.; Fonolla, J.; Navas, M.; Rodriguez, J.M.; Xaus, J. Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 2007, 23, 254–260. [Google Scholar] [CrossRef] [PubMed]
- Tamura, S.; Samegai, Y.; Kurata, H.; Nagamine, T.; Aizawa, C.; Kurata, T. Protection against influenza virus infection by vaccine inoculated intranasally with cholera toxin B subunit. Vaccine 1988, 6, 409–413. [Google Scholar] [CrossRef]
- Tamura, S.; Yamanaka, A.; Shimohara, M.; Tomita, T.; Komase, K.; Tsuda, Y.; Suzuki, Y.; Nagamine, T.; Kawahara, K.; Danbara, H.; et al. Synergistic action of cholera toxin B subunit (and Escherichia coli heat-labile toxin B subunit) and a trace amount of cholera whole toxin as an adjuvant for nasal influenza vaccine. Vaccine 1994, 12, 419–426. [Google Scholar] [CrossRef]
- Tamura, S.; Ito, Y.; Asanuma, H.; Hirabayashi, Y.; Suzuki, Y.; Nagamine, T.; Aizawa, C.; Kurata, T. Cross-protection against influenza virus infection afforded by trivalent inactivated vaccines inoculated intranasally with cholera toxin B subunit. J. Immunol. 1992, 149, 981–988. [Google Scholar] [PubMed]
- Mutsch, M.; Zhou, W.; Rhodes, P.; Bopp, M.; Chen, R.T.; Linder, T.; Spyr, C.; Steffen, R. Use of the inactivated intranasal influenza vaccine and the risk of Bell’s palsy in Switzerland. N. Engl. J. Med. 2004, 350, 896–903. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stuebe, A. The risks of not breastfeeding for mothers and infants. Rev. Obstet. Gynecol. 2009, 2, 222–231. [Google Scholar] [PubMed]
- Bezirtzoglou, E.; Tsiotsias, A.; Welling, G.W. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 2011, 17, 478–482. [Google Scholar] [CrossRef]
- Harmsen, H.J.; Wildeboer-Veloo, A.C.; Raangs, G.C.; Wagendorp, A.A.; Klijn, N.; Bindels, J.G.; Welling, G.W. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 2000, 30, 61–67. [Google Scholar] [CrossRef]
- Stark, P.L.; Lee, A. The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J. Med. Microbiol. 1982, 15, 189–203. [Google Scholar] [CrossRef]
- Brink, L.R.; Mercer, K.E.; Piccolo, B.D.; Chintapalli, S.V.; Elolimy, A.; Bowlin, A.K.; Matazel, K.S.; Pack, L.; Adams, S.H.; Shankar, K.; et al. Neonatal diet alters fecal microbiota and metabolome profiles at different ages in infants fed breast milk or formula. Am. J. Clin. Nutr. 2020, 111, 1190–1202. [Google Scholar] [CrossRef]
- Walker, W.A.; Iyengar, R.S. Breast milk, microbiota, and intestinal immune homeostasis. Pediatr. Res. 2015, 77, 220–228. [Google Scholar] [CrossRef] [Green Version]
- Stewart, C.J.; Ajami, N.J.; O’Brien, J.L.; Hutchinson, D.S.; Smith, D.P.; Wong, M.C.; Ross, M.C.; Lloyd, R.E.; Doddapaneni, H.; Metcalf, G.A.; et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature 2018, 562, 583–588. [Google Scholar] [CrossRef]
- Nolan, L.S.; Parks, O.B.; Good, M. A review of the immunomodulating components of maternal breast milk and protection against necrotizing enterocolitis. Nutrients 2019, 12, 14. [Google Scholar] [CrossRef] [Green Version]
- Gil-Campos, M.; Lopez, M.A.; Rodriguez-Benitez, M.V.; Romero, J.; Roncero, I.; Linares, M.D.; Maldonado, J.; Lopez-Huertas, E.; Berwind, R.; Ritzenthaler, K.L.; et al. Lactobacillus fermentum CECT 5716 is safe and well tolerated in infants of 1-6 months of age: A randomized controlled trial. Pharmacol. Res. 2012, 65, 231–238. [Google Scholar] [CrossRef] [PubMed]
Strain/Origin | Properties | Mechanism of Action | Model | Reference |
---|---|---|---|---|
L. fermentum UCO-979C/human gastric tissue | Anti-inflammatory effect | ↑ IL-10 production | THP-1 cell line | [42] |
L. fermentum SRK414/ unknown (Food Microbiology Laboratory, Korea University (Seoul, South Korea)) | ↓ TNF-α and IL-1β expression in LPS-stimulated inflamed | HT-29 cell line | [43] | |
L. fermentum KBL374 and L. fermentum KBL375/feces of healthy Koreans | ↓ Leukocyte infiltration and Disease Activity Index | DSS-induced colitis in C57BL/6N mice | [25] | |
L. fermentum MG901 and L. fermentum MG989/healthy woman’s vagina | Urogenital and intestinal anti-infective activity | Inhibit the Candida albicans growth | HT-29 cell line | [44] |
L. fermentum 3872/milk of healthy women | Inhibition of Campylobacter jejuni growth and attachment to collagen I | Collagen I coated plates | [37] | |
L. fermentum L23/vaginal smears of healthy woman | Growth inhibition of Gardnerella vaginalis | Vaginal infected BALB/C mice with Gardnerella vaginalis | [45] | |
L. fermentum LF31/unknown (Milonet, Bromatech s.r.l., Milan, Italy) | Antioxidant capacity | Antioxidant capacity detectable with the oxigenic radical absorbance capacity (ORAC) assay | HT-29 cell line | [46] |
L. fermentum JX306/Chinese traditional fermented vegetable | ↓ Malondialdehyde (MDA) levels ↑ Activity of glutathione peroxidase (GSH-Px) | D-galactose-induced aging KM mice | [47] |
Strain/Origin | Main Properties | Physiological Conditions | References |
---|---|---|---|
L. fermentum RC-14/female urogenital tract | −37% of improvement in vaginal flora - ↑ lactobacilli population - ↓ yeast levels | Healthy women | [48] |
L. fermentum VRI-003 PCC/unknown (®Probiomics Ltd., Eveleigh, NSW, Australia) | - ↑ lactobacilli population - ↓ in the severity of gastrointestinal and respiratory illness in sportive males. | Competitive athletes | [49] |
- ↓ Severity Scoring of Atopic Dermatitis (SCORAD) index. - ↑ the cases of mild atopic dermatitis. | Children with atopic dermatitis | [50] | |
Combination of L. fermentum LF10 and L. acidophilus La02/vaginal swabs of healthy women or from direct brushing of gut mucosa of healthy humans | ↓ 72% of clinical recurrences vaginal infections of vulvovaginal candidiasis | Women with recurrent vulvovaginal candidiasis | [51] |
Combination of L. fermentum LF15 and L. plantarum LP01/feces of healthy humans or vaginal swabs of healthy female subjects | Reduction in the Nugent score and restoration (58%) of the vaginal microbiota of women | Women diagnosed with bacterial vaginosis | [52] |
L. fermentum ME-3/healthy Human intestinal tract | - ↑ lactobacilli in feces -Improvement the blood Total Antioxidative Activity and Total Antioxidative Status | Healthy humans | [53] |
Combination of L. fermentum ME-3 and a food supplement/healthy human intestinal tract | -Improvement cardiovascular and diabetes risk profile. - ↓ total cholesterol | Clinically asymptomatic humans | [54] |
Combination of L. fermentum ME-3, L. paracasei 8700:2 and Bifidobacterium longum 46/healthy human intestinal tract and human feces | - ↑ the blood Total Antioxidative Status - ↓ oxidized/reduced glutathione ratio | Adult volunteers without gastric symptoms | [55] |
Combination of L. fermentum LN99, L. gasseri LN40, L. casei subsp. rhamnosus LN113 and Pediococcus acidilactici LN23)/vaginal flora of healthy women | -Vaginal colonization of lactobacilli - ↓ recurrences of bacterial vaginosis and vulvovaginal candidiasis | Women diagnosed and treated for vulvovaginal candidiasis and bacterial vaginosis | [56] |
Experimental Models | Mechanisms of Action | Cell Model | Reference |
---|---|---|---|
Epithelial cell lines | ↓ Expression of pro-inflammatory profile (Il-6) and ↑ the mucins in stimulated cells | CMT-93 | [58] |
Restoration of miRNA-150, miRNA-155, and miRNA-375 expression | |||
↓ NO, IL-8, and IL-1β in stimulated cells | Caco-2 | [65] | |
↓ MAPK p42/44 ERK and p38 in stimulated cells | |||
Immune cells | ↓ Pro-inflammatory mediators of stimulated cells (TNF-ɑ and IL-1β) and ↑ anti-inflammatory mediators (IL-10) | BMDM | [71] |
Restoration of miRNA-150, miRNA-155, and miRNA-375 expression | [58] | ||
↓ IL-1β and NO production in stimulated cells | RAW-264.7 | [65] | |
Enhanced immune responses: Induction of the production of cytokines (TNFα, IL-1β, IL-8, MIP-1α, MIP-1β, and GM-CSF), activation of NK and T cell subsets, expansion of Treg cells | PBMC | [83] |
Experimental Models | Mechanisms of Action | Animal Model | Reference |
---|---|---|---|
Experimental colitis | ↓ Immune response: - Tnf-ɑ, iNos, and Il-6 expression. - LTB4 and TNF-ɑ protein levels. - MPO activity. | Rat | [65,95] |
↑ Antioxidant activity: GSH content. | |||
Induced growth of Lactobacilli species and increased more than doubled the production of the SCFAs (acetate, butyrate, and propionate) | |||
Amelioration of the weight decrease in a 20% and amelioration of diarrhea incidence and gut dysbiosis | Mouse | [27,58] | |
↓ Tnf-ɑ, Il-1β, iNOS and Mmp-9 expression | |||
Restoration of miR-155 and miR-223 expression | |||
Microbiota restoration: increase microbial diversity and restore the F/B ratio. | |||
Metabolic syndrome | Prevent liver steatosis and inflammatory status | Rat | [112] |
↓ Glucose and insulin levels in plasma | |||
Gut dysbiosis restoration by preventing the increase in Bacteroidetes and the reduction in Firmicutes. Increase the levels of Akkermansia muciniphila | |||
Prevention of hypertriglyceridemia and hyperleptinemia | |||
↓ Body weight gain in 15–20% | Mouse | [114] | |
Amelioration of glucose and lipid metabolism | |||
↑ Glut-4 expression | |||
↓ Tnf-α and Il-1β expression and inhibition of NADPH activity in aortic tissue | |||
Restoration of impaired endothelial disfunction | |||
Anti-inflammatory properties: ↓ Il-6, Tnf-α, Mcp-1, and Jnk-1 expression in liver and fat | |||
Amelioration of obesity-associated dysbiosis: - ↑ Richness and diversity - Restore F/B ratio, decreasing it. - Restore levels of Verrumicrobia, Akkermansia and Bacteroides. - ↑ Lactate- and acetate-producing genera. | |||
Enhanced intestinal epithelial integrity (↑ occludin levels) and ↓ LPS plasma level | |||
Systemic lupus erythematosus | Prevention gut dysbiosis: - Restore F/B ratio. - ↑ Bifidobacterium and Parabacteroides genera. - ↓ Blautia and Lachnospira. | Mouse | [57] |
↓ Pro-inflammatory cytokine (Tnf-α and Il-1β expression) /plasma levels of LPS | |||
Intestinal integrity amelioration (↑ Zo-1 and Occludin expression) | |||
↓ Hypertension | |||
Prevention of the endothelial dysfunction (↑ acetylcholine-induced vasodilation) | |||
↓ NAPDH oxidase activity | |||
Prevention of the altered T-cell polarization | |||
Pregnancy and lactation stage | ↓ Cytotoxic T cells | Rat | [135] |
↑ γ-linolenic acid ↓ Saturated fatty acids |
Disease | Mechanism of Action | References |
---|---|---|
Mastitis | Prevention of lactational mastitis symptoms | [143,144] |
↓ IL-8 levels | ||
↓ Staphylococcus load in the breast milk | ||
Pediatric infections | ↓ Incidence of gastrointestinal and respiratory infection | [28,153] |
↓ Incidence of conjunctivitis and the load of Staphylococcus | [28] | |
Vaccination stage | ↑ Th1, NK cells, and Tnf-α and Il-12 expression | [145] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rodríguez-Sojo, M.J.; Ruiz-Malagón, A.J.; Rodríguez-Cabezas, M.E.; Gálvez, J.; Rodríguez-Nogales, A. Limosilactobacillus fermentum CECT5716: Mechanisms and Therapeutic Insights. Nutrients 2021, 13, 1016. https://doi.org/10.3390/nu13031016
Rodríguez-Sojo MJ, Ruiz-Malagón AJ, Rodríguez-Cabezas ME, Gálvez J, Rodríguez-Nogales A. Limosilactobacillus fermentum CECT5716: Mechanisms and Therapeutic Insights. Nutrients. 2021; 13(3):1016. https://doi.org/10.3390/nu13031016
Chicago/Turabian StyleRodríguez-Sojo, María Jesús, Antonio Jesús Ruiz-Malagón, María Elena Rodríguez-Cabezas, Julio Gálvez, and Alba Rodríguez-Nogales. 2021. "Limosilactobacillus fermentum CECT5716: Mechanisms and Therapeutic Insights" Nutrients 13, no. 3: 1016. https://doi.org/10.3390/nu13031016