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Effects of different probiotic strains B. lactis, L. rhamnosus and L. reuteri on brain-intestinal axis immunomodulation in an endotoxin-induced inflammation

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Abstract

The study evaluated the effects of supplementation with three different probiotic strains Bifidobacterium lactis (LACT GB™), Lactobacillus rhamnosus (RHAM GB™) and Lactobacillus reuteri (REUT GB™) on brain-intestinal immunomodulation in an animal model of LPS-induced inflammation. Fifty mice Balb/C were distributed into five groups: control; lipopolysaccharide (LPS); LPS + B. lactis (LACT GB™); LPS + L. rhamnosus (RHAM GB™); and LPS + L. reuteri (REUT GB™). The animals were supplemented with their respective probiotic microorganisms daily, for 30 days, at a concentration of 1 × 109 CFU/animal/day. After 30 days of supplementation, animals received the inflammatory insult by LPS (15 mg/kg). Behavioral tests, oxidative stress and inflammation were performed, as well as gut and brain histology. In the behavioral test, LPS + B. lactis group was less anxious than the other groups. Serum interleukin IL-1β and IL-6 levels increased in all groups that received the LPS insult, and there was a reduction in inflammation in the supplemented groups when compared to the LPS group in brain and gut. There is a reduction in myeloperoxidase activity and oxidative stress in groups supplemented with probiotics. In intestine histological analysis occurs damage to the tissue integrity in the LPS group, in the other hand, occurs preservation of integrity in the probiotic supplemented animals. In the brain, infiltrates of perivascular inflammatory cells can be seen in the LPS group. The three probiotic studies showed efficient immunomodulating activity and ensured integrity of the intestinal barrier function, even after the severe insult by LPS. These results show the important role of probiotics in the gut–brain axis.

Graphical abstract

Graphical abstract illustratively represents the gut–brain axis and how different probiotic strains influence the immunomodulatory response releasing different pro- and anti-inflammatory cytokines, and their role in the balance of dysbiosis.

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References

  1. Sanders ME, Lenoir-Wijnkoop I, Salminen S, Merenstein DJ, Gibson GR, Petschow BW, Pot B (2014) Probiotics and prebiotics: prospects for public health and nutritional recommendations. Ann N Y Acad Sci 1309(1):19–29

    Article  CAS  PubMed  Google Scholar 

  2. AlFaleh K, Anabrees J (2014) Probiotics for prevention of necrotizing enterocolitis in preterm infants. Evid-Based Child Health: A Cochrane Rev J 9(3):584–671

    Article  Google Scholar 

  3. Goldenberg JZ, Yap C, Lytvyn L, Lo CKF, Beardsley J, Mertz D, Johnston BC (2017) Probiotics for the prevention of Clostridium difficile ‐ associated diarrhea in adults and children. Cochrane Database Syst Rev (12)

  4. Aponte GB, Mancilla CAB, Carreazo NY, Galarza RAR (2013) Probiotics for treating persistent diarrhoea in children. Cochrane Database Syst Rev (8)

  5. Miller LE, Ouwehand AC (2013) Probiotic supplementation decreases intestinal transit time: meta-analysis of randomized controlled trials. World J Gastroenterol: WJG 19(29):4718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Moayyedi P, Ford AC, Talley NJ, Cremonini F, Foxx-Orenstein AE, Brandt LJ, Quigley EM (2010) The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut 59(3):325–332

    Article  CAS  PubMed  Google Scholar 

  7. Hao Q, Dong, BR, Wu T (2015) Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst Rev (2)

  8. Azad MAK, Sarker M, Wan D. (2018). Immunomodulatory Effects of Probiotics on Cytokine Profiles. Biomed Res Int 23

  9. Gill HS, Cross ML, Rutherford KJ, Gopal PK (2001) Dietary probiotic supplmentation to enhance cellular immunity in the elderly. Br J Biomed Sci 58(2):94

    CAS  PubMed  Google Scholar 

  10. Wood C, Keeling S, Bradley S, Johnson-Green P, Green-Johnson JM (2007) Interactions in the mucosal microenvironment: vasoactive intestinal peptide modulates the down-regulatory action of Lactobacillus rhamnosus on LPS-induced interleukin-8 production by intestinal epithelial cells. Microb Ecol Health Dis 19(3):191–200

    CAS  Google Scholar 

  11. Villena J, Medina M, Vintiñi E, Alvarez S (2008) Stimulation of respiratory immunity by oral administration of Lactococcus lactis. Can J Microbiol 54(8):630–638

    Article  CAS  PubMed  Google Scholar 

  12. Yadav H, Jain S, Sinha PR (2008) Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. J Dairy Res 75(2):189

    Article  CAS  PubMed  Google Scholar 

  13. Di Mauro A, Neu J, Riezzo G, Raimondi F, Martinelli D, Francavilla R, Indrio F (2013) Gastrointestinal function development and microbiota. Ital J Pediatr 39(1):15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13(10):701–712

    Article  CAS  PubMed  Google Scholar 

  15. Mayer EA (2011) Gut feelings: the emerging biology of gut–brain communication. Nat Rev Neurosci 12(8):453–466

    Article  CAS  PubMed  Google Scholar 

  16. Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain–gut–enteric microbiota axis. Nat Rev Gastroenterol Hepatol 6(5):306

    Article  CAS  PubMed  Google Scholar 

  17. Fijan S (2014) Microorganisms with claimed probiotic properties: An overview of recent literature. Int J Environ Res Public Health 11:4745–4767

    Article  PubMed  PubMed Central  Google Scholar 

  18. Zelaya H, Tsukida K, Chiba E, Marranzino G, Alvarez S, Kitazawa H, Agüero G, Villena J (2014) Immunobiotic Lactobacilli reduce viral-associated pulmonary damage through the modulation of inflammation-coagulation interactions. Int Immunopharmacol 19:161–173

    Article  CAS  PubMed  Google Scholar 

  19. Gänzle MG, Vogel RF (2003) Studies on the mode of action of reutericyclin. Appl Environ Microbiol 69:1305–1307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Yang F, Wang A, Zeng X, Hou C, Liu H, Qiao S (2015) Lactobacillus reuteri I5007 modulates tight junction protein expression in IPEC-J2 cells with LPS stimulation and in newborn piglets under normal conditions. BMC Microbiol 15:32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Chen J, Cai W, Feng Y (2007) Development of intestinal bifidobacteria and Lactobacilli in breast-fed neonates. Clin Nutr 26:559–566

    Article  CAS  PubMed  Google Scholar 

  22. Chmielewska A, Szajewska H (2010) Systematic review of randomised controlled trials: Probiotics for functional constipation. World J Gastroenterol 16:69–75

    PubMed  PubMed Central  Google Scholar 

  23. Hempel S, Newberry SJ, Maher AR, Wang Z, Miles JN, Shanman R, Johnsen B, Shekelle PG (2012) Probiotics for the prevention and treatment of antibiotic- associated diarrhea: A systematic review and meta-analysis. JAMA 307:1959–1969

    Article  CAS  PubMed  Google Scholar 

  24. Dylag K, Hubalewska-Mazgaj M, Surmiak M, Szmyd J, Brzozowski T (2014) Probiotics in the mechanism of protection against gut inflammation and therapy of gastrointestinal disorders. Curr Pharm Des 20:1149–1155

    Article  CAS  PubMed  Google Scholar 

  25. Aloisio I, Santini C, Biavati B, Dinelli G, Cenci A, Chingwaru W, Mogna L, Di Gioia D (2012) Characterization of Bifidobacterium spp. strains for the treatment of enteric disorders in newborns. Appl Microbiol Biotechnol 96:561–576

    Article  CAS  Google Scholar 

  26. Di Gioia D, Aloisio I, Mazzola G, Biavati B (2014) Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants. Appl Microbiol Biotechnol 98:563–577

    Article  PubMed  CAS  Google Scholar 

  27. Isolauri E, Rautava S, Salminen S (2012) Probiotics in the development and treatment of allergic disease. Gastroenterol Clin North Am 41:747–762

    Article  PubMed  Google Scholar 

  28. Ortiz L, Ruiz F, Pascual L, Barberis L (2014) Effect of two probiotic strains of Lactobacillus on in vitro adherence of Listeria monocytogenes, Streptococcus agalactiae, and Staphylococcus aureus to vaginal epithelial cells. Curr Microbiol 68(6):679–84

    Article  CAS  PubMed  Google Scholar 

  29. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, Guyonnet D, Legrain-Raspaud S et al (2013) Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144:1394–1401

    Article  CAS  PubMed  Google Scholar 

  30. Jacobs SE, Tobin JM, Opie GF, Donath S, Tabrizi SN, Pirotta M, Morley CJ, Garland SM (2013) ProPrems Study Group Probiotic effects on late-onset sepsis in very preterm infants: A randomized controlled trial. Pediatrics 132:1055–1062

    Article  PubMed  Google Scholar 

  31. West NP, Horn PL, Pyne DB, Gebski VJ, Lahtinen SJ, Fricker PA, Cripps AW (2014) Probiotic supplementation for respiratory and gastrointestinal illness symptoms in healthy physically active individuals. Clin Nutr 33(4):581–587

    Article  CAS  PubMed  Google Scholar 

  32. Komada M, Takao K, Miyakawa T (2008) Elevated plus maze for mice. JoVE (J Vis Exp) 22:e1088

    Google Scholar 

  33. De Young LM, Kheifets JB, Ballaron SJ, Young JM (1989) Edema and cell infiltration in the phorbol ester-treated mouse ear are temporally separate and can be differentially modulated by pharmacologic agents. Agents Actions 26(3–4):335–341

    Article  PubMed  Google Scholar 

  34. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126(1):131–138

    Article  CAS  PubMed  Google Scholar 

  35. Draper HH, Hadley M (1990) Malondialdehyde determination as índex of lipid peroxidation. Methods Enzymol 186:421–431

    Article  CAS  PubMed  Google Scholar 

  36. Erben U et al (2014) A guide to histomorphological evaluation of intestinal inflammation in mouse models. Int J Clin Exp Pathol 7:4557–4576

    PubMed  PubMed Central  Google Scholar 

  37. Grenham S, Clarke G, Cryan JF, Dinan TG (2011) Brain-gut-microbe communication in health and disease Front. Physiol 7(2):94

    Google Scholar 

  38. Saulnier DM, Ringel Y, Heyman MB, Foster JA, Bercik P, Shulman RJ, Versalovic J, Verdu EF et al (2013) The intestinal microbiome, probiotics and prebiotics in neurogastroenterology. Gut Microbes 4(1):17–27

    Article  PubMed  PubMed Central  Google Scholar 

  39. Conti LH, Costello DG, Martin LA, White MF, Abreu ME (1994) Mouse strain differences in the behavioral effects of corticotropin-releasing factor (CRF) and the CRF antagonist alpha-helical CRF9–41. Pharmacol Biochem Behav 48(2):497–503

    Article  CAS  PubMed  Google Scholar 

  40. Kalinichev M, Bate ST, Coggon SA, Jones DN (2008) Locomotor reactivity to a novel environment and sensitivity to MK-801 in five strains of mice Behav. Pharmacol 19(1):71–75

    CAS  Google Scholar 

  41. Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P, Collins SM (2013) Altered colonic function and microbiota profile in a mouse model of chronic depression Neurogastroenterol. Motil 25(9):733-e575

    CAS  Google Scholar 

  42. Barden N (2004) Implication of the hypothalamic-pituitary-adrenal axis in the physiopathology of depression. J Psychiatry Neurosci 29:185–193

    PubMed  PubMed Central  Google Scholar 

  43. Heijtz RD et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108:3047–3052

    Article  CAS  PubMed Central  Google Scholar 

  44. Neufeld KM et al (2011) Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 23:255–264

    Article  CAS  PubMed  Google Scholar 

  45. Clarke G et al (2012) The microbiome-gut–brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry. https://doi.org/10.1038/mp.2012.77

    Article  PubMed  PubMed Central  Google Scholar 

  46. Choi HJ, Lee NK, Paik HD (2015) Health benefits of lactic acid bacteria isolated from kimchi, with respect to immunomodulatory effects. Food Sci Biotechnol 24:783–789

    Article  Google Scholar 

  47. Tang J, Xu L, Zeng Y, Gong F (2021) Effect of gut microbiota on LPS-induced acute lung injury by regulating the TLR4/NF-kB signaling pathway. Int Immunopharmacol 91(107272)

  48. Réus GZ, Fries GR, Stertz L, Badawy M, Passos IC, Barichello T, Quevedo J (2015) The role of inflammation and microglial activation in the pathophysiology of psychiatric disorders. Neuroscience 300:141–154

    Article  PubMed  CAS  Google Scholar 

  49. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Cazaubiel JM (2011) Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 105:755–764

    Article  CAS  PubMed  Google Scholar 

  50. Kim N, Yun M, On YJ, Choi HJ (2018) Mind-altering with the gut: Modulation of the gut-brain axis with probiotics. J Microbiol 56:172–182

    Article  CAS  PubMed  Google Scholar 

  51. Ong IM, Gonzalez JG, McIlwain SJ, Sawin EA, Schoen AJ, Adluru N, Alexander AL, Yu JJ (2018) Gut microbiome populations are associated with structure-specific changes in white matter architecture. Transl Psychiatry 8:6

    Article  PubMed  PubMed Central  Google Scholar 

  52. Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A (2019) Mechanisms of Action of Probiotics. Adv Nutr 10(suppl_1):S49–S66

    Article  PubMed  PubMed Central  Google Scholar 

  53. Mi GL, Zhao L, Qiao DD, Kang WQ, Tang MQ, Xu JK (2015) Effectiveness of Lactobacillus reuteri in infantile colic and colicky induced maternal depression: A prospective single blind randomized trial. Antonie Van Leeuwenhoek 107:1547–1553

    Article  PubMed  Google Scholar 

  54. Piccioni A, Franza L, Vaccaro V et al (2021) Microbiota and Probiotics: The Role of Limosilactobacillus Reuteri in Diverticulitis. Medicina (Kaunas) 57(8):802

    Article  Google Scholar 

  55. Mu Q, Tavella VJ, Luo XM (2018) Role of Lactobacillus reuteri in Human Health and Diseases. Front Microbiol 9:757

    Article  PubMed  PubMed Central  Google Scholar 

  56. Talarico TL, Dobrogosz WJ (1989) Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri. Antimicrob Agents Chemother 33:674–679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Candelli M, Franza L, Pignataro G, Ojetti V, Covino M, Piccioni A, Gasbarrini A, Franceschi F (2021) Interaction between Lipopolysaccharide and Gut Microbiota in Inflammatory Bowel Diseases. Int J Mol Sci 22:6242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Salas-Jara MJ, Ilabaca A, Vega M, García A (2016) Biofilm Forming Lactobacillus: New Challenges for the Development of Probiotics. Microorganisms 4:35

    Article  PubMed Central  CAS  Google Scholar 

  59. Ashraf R, Shah NP (2014) Immune system stimulation by probiotic microorganisms. Crit Rev Food Sci Nutr 54:938–956

    Article  CAS  PubMed  Google Scholar 

  60. Han X, Lee A, Huang S, Gao J, Spence JR, Owyang C (2019) Lactobacillus rhamnosus GG prevents epithelial barrier dysfunction induced by interferon-gamma and fecal supernatants from irritable bowel syndrome patients in human intestinal enteroids and colonoids. Gut Microbes 10:59–76

    Article  CAS  PubMed  Google Scholar 

  61. Berni-Canani R, Sangwan N, Stefka AT, Nocerino R, Paparo L, Aitoro R, Calignano A, Khan AA et al (2016) Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J 10:742–750

    Article  CAS  PubMed  Google Scholar 

  62. Spacova I, Petrova MI, Fremau A, Pollaris L, Vanoirbeek J, Ceuppens JL, Seys S, Lebeer S (2019) Intranasal administration of probiotic Lactobacillus rhamnosus GG prevents birch pollen-induced allergic asthma in a murine model. Allergy 74:100–110

    Article  CAS  PubMed  Google Scholar 

  63. Huang R, Ning H, Shen M, Li J, Zhang J, Chen X (2017) Probiotics for the treatment of atopic dermatitis in children: A systematic review and meta-analysis of randomized controlled trials. Front Cell Infect Microbiol 7:392

    Article  PubMed  PubMed Central  Google Scholar 

  64. Chen L, Li H, Li J, Chen Y, Yang Y (2019) Lactobacillus rhamnosus GG treatment improves intestinal permeability and modulates microbiota dysbiosis in an experimental model of sepsis. Int J Mol Med 43:1139–1148

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Tsui KC, Yen TL, Huang CJ, Hong KJ (2021) Lactobacillus rhamnosus GG as dietary supplement improved survival from lipopolysaccharides-induced sepsis in mice. Food Sci Nutr 9(12):6786–6793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Kim JH, Doo EH, Jeong M, Kim S, Lee YY, Yang J, Lee JS, Kim JH et al (2019). Enhancing Immunomodulatory Function of Red Ginseng Through Fermentation Using Bifidobacteriumanimalis Subsp. lactis LT 19–2. Nutrients. 11(7):1481

  67. Le Barz M, Daniel N, Varin TV, Naimi S, Demers-Mathieu V, Pilon G, Audy J, Laurin É et al (2019) In vivo screening of multiple bacterial strains identifies Lactobacillus rhamnosus Lb102 and Bifidobacterium animalis ssp. lactis Bf141 as probiotics that improve metabolic disorders in a mouse model of obesity. FASEB J 33(4):4921–4935

  68. Goehler LE et al (2008) Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 22:354–366

    Article  CAS  PubMed  Google Scholar 

  69. Lyte M et al (2006) Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Physiol Behav 89:350–357

    Article  CAS  PubMed  Google Scholar 

  70. Neufeld KA (A) et al Effects of intestinal microbiota on anxiety-like behavior. CommunIntegr Biol 4 (2011), pp. 492–494

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Acknowledgements

Authors acknowledge GABBIA Biotechnology and UNESC–Criciúma.

Funding

This study was funded by GABBIA Biotechnology and UNESC.

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Authors and Affiliations

  1. Gabbia Biotechnology, Barra Velha - Santa Catarina, Brazil

    Monique Michels, Gabriel Fernandes Alves Jesus, Ana Paula Lorenzen Voytena, Marina Rossetto & Fernanda Ramlov

  2. Biohall Research and Innovation, Itajaí, SC, Brazil

    Monique Michels

  3. Laboratory of Experimental Pathophysiology, Graduate Program in Health Sciences, University of Southern Santa Catarina (UNESC), Criciúma, Brazil

    Mariane Rocha Abatti, Emily Córneo, Luana Cucker, Heloisa de Medeiros Borges, Natan da Silva Matos, Luana Bezerra Rocha, Rodrigo Dias, Carla Sasso Simon & Felipe Dal-Pizzol

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Contributions

MM and GFAJ contributed to the conceptualization and design of the study; data curation; formal analysis and methodology; roles/writing—original draft. MRA, EC and LC were involved in the conceptualization and design of the study; methodology. HMB, NSM, LBR and RD helped in the conceptualization and design of the study; methodology; and data curation. CSS, APV, MR and FR contributed to the data curation; formal analysis; and methodology. FDP was involved in the conceptualization and design of the study; project administration; supervision; funding acquisition; writing—review and editing. All authors approved the final version submitted.

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Correspondence to Monique Michels.

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Gabbia Biotechnology are developing probiotics strains for commercial purposes. Gabriel Jesus, Fernanda Ramlov, Marina Rosseto and Ana Paula Voytena are members of Gabbia Biotechnology. The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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Michels, M., Jesus, G.F.A., Abatti, M.R. et al. Effects of different probiotic strains B. lactis, L. rhamnosus and L. reuteri on brain-intestinal axis immunomodulation in an endotoxin-induced inflammation. Mol Neurobiol 59, 5168–5178 (2022). https://doi.org/10.1007/s12035-022-02906-3

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