Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Lactobacillus mucosae and Bifidobacterium longum Synergistically Alleviate Immobilization Stress-Induced Anxiety/Depression in Mice by Suppressing Gut Dysbiosis

  • Han, Sang-Kap (Neurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee University) ;
  • Kim, Dong-Hyun (Neurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee University)
  • Received : 2019.07.21
  • Accepted : 2019.08.15
  • Published : 2019.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

We isolated Lactobacillus mucosae NK41 and Bifidobacterium longum NK46 from human feces, which induced BDNF expression in corticosterone-stimulated SH-SY5Y cells, and examined their anti-depressive effects in mice. NK41, NK46, and their (1:1) mixture significantly mitigated immobilization stress (IS)-induced anxiety-like/depressive behaviors, hippocampal $NF-{\kappa}B$ activation, BDNF expression, $Iba1^+$ cell population, and blood corticosterone, $TNF-{\alpha}$, IL-6, and lipopolysaccharide levels. Furthermore, they inhibited colitis marker $NF-{\kappa}B$ activation, and $TNF-{\alpha}$ expression in mice with IS-induced anxiety/depression. They additionally suppressed gut Proteobacteria and Bacteroidetes populations and bacterial lipopolysaccharide production. These findings suggest that NK41 and NK46 may alleviate anxiety/depression and colitis by suppressing gut dysbiosis.

Keywords

References

  1. Baxter AJ, Scott KM, Ferrari AJ, Norman RE, Vos T, Whiteford HA. 2014. Challenging the myth of an "epidemic" of common mental disorders: trends in the global prevalence of anxiety and depression between 1990 and 2010. Depress. Anxiety 31: 506-516. https://doi.org/10.1002/da.22230
  2. Hart PC, Bergner CL, Smolinsky AN, Dufour BD, Egan RJ, Laporte JL, et al. 2016. Experimental models of anxiety for drug discovery and brain research. Methods Mol. Biol. 1438: 271-291. https://doi.org/10.1007/978-1-4939-3661-8_16
  3. Sutanto D, Kloet ER. 1994. The use of various animal models in the study of stress and stress-related phenomena. Lab. Anim. 28: 293-306. https://doi.org/10.1258/002367794780745092
  4. Sekiyama A, Ueda H, Kashiwamura S, Nishida K, Yamaguchi S, Sasaki H, et al. 2006. A role of the adrenal gland in stress-induced up-regulation of cytokines in plasma. J. Neuroimmunol. 171: 38-44. https://doi.org/10.1016/j.jneuroim.2005.09.010
  5. Caviedes A, Lafourcade C, Soto C, Wyneken U. 2017. BDNF/NF-${\kappa}B$ signaling in the neurobiology of depression. Curr. Pharm. Des. 23: 3154-3163.
  6. Jang HM, Lee KE, Lee HJ, Kim DH. 2018. Immobilization stress-induced Escherichia coli causes anxiety by inducing NF-${\kappa}B$ activation through gut microbiota disturbance. Sci. Rep. 8: 13897. https://doi.org/10.1038/s41598-018-31764-0
  7. Hold GL, Hansen R. 2019. Impact of the gastrointestinal microbiome in health and disease: co-evolution with the host immune system. Curr. Top. Microbiol. Immunol. 421: 303-318.
  8. Molina-Torres G, Rodriguez-Arrastia M, Roman P, Sanchez-Labraca N, Cardona D. 2019. Stress and the gut microbiotabrain axis. Behav. Pharmacol. 30: 187-200. https://doi.org/10.1097/FBP.0000000000000478
  9. Jang HM, Lee KE, Kim DH. 2019. The preventive and curative effects of Lactobacillus reuteri NK33 and Bifidobacterium adolescentis NK98 on immobilization stress-induced anxiety/depression and colitis in mice. Nutrients 11: pii: E819. https://doi.org/10.3390/nu11040819
  10. Jang HM, Jang SE, Han MJ, Kim DH. 2018. Anxiolytic-like effect of Bifidobacterium adolescentis IM38 in mice with or without immobilisation stress. Benef. Microbes. 9: 123-132. https://doi.org/10.3920/BM2016.0226
  11. Davis DJ, Doerr HM, Grzelak AK, Busi SB, Jasarevic E, Ericsson AC, et al. 2016. Lactobacillus plantarum attenuates anxiety-related behavior and protects against stress-induced dysbiosis in adult zebrafish. Sci. Rep. 6: 33726. https://doi.org/10.1038/srep33726
  12. Liu X, Cao S, Zhang X. 2015. Modulation of gut microbiotabrain axis by probiotics, prebiotics, and diet. J. Agric. Food Chem. 63: 7885-7895. https://doi.org/10.1021/acs.jafc.5b02404
  13. Lee HJ, Lim SM, Ko DB, Jeong JJ, Hwang YH, Kim DH. 2017. Soyasapogenol B and genistein attenuate lipopolysaccharideinduced memory impairment in mice by the modulation of NF-${\kappa}B$-mediated BDNF expression. J. Agric. Food Chem. 65: 6877-6885. https://doi.org/10.1021/acs.jafc.7b02569
  14. Jang HM, Lee HJ, Jang SE, Han MJ, Kim DH. 2018. Evidence for interplay among antibacterial-induced gut microbiota disturbance, neuro-inflammation, and anxiety in mice. Mucosal Immunol. 11: 1386-1397. https://doi.org/10.1038/s41385-018-0042-3
  15. Mackos AR, Varaljay VA, Maltz R, Gur TL, Bailey MT. 2016. Role of the intestinal microbiota in host responses to stressor exposure. Int. Rev. Neurobiol. 131: 1-19. https://doi.org/10.1016/bs.irn.2016.08.002
  16. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, et al. 2004. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 558: 263-275. https://doi.org/10.1113/jphysiol.2004.063388
  17. Jang SE, Lim SM, Jeong JJ, Jang HM, Lee HJ, Han MJ, et al. 2018. Gastrointestinal inflammation by gut microbiota disturbance induces memory impairment in mice. Mucosal Immunol. 11: 369-379. https://doi.org/10.1038/mi.2017.49
  18. Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, et al. 2011. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol. Motil. 23: 1132-1139. https://doi.org/10.1111/j.1365-2982.2011.01796.x
  19. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG. 2010. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170: 1179-1188. https://doi.org/10.1016/j.neuroscience.2010.08.005

Cited by

  1. Microbiological Modification Therapy For Acute Medical Presentations Of Generalised Anxiety Disorder vol.11, 2019, https://doi.org/10.5234/cnpt.11.67
  2. Bifidobacteria-Fermented Red Ginseng and Its Constituents Ginsenoside Rd and Protopanaxatriol Alleviate Anxiety/Depression in Mice by the Amelioration of Gut Dysbiosis vol.12, pp.4, 2020, https://doi.org/10.3390/nu12040901
  3. The Gut Microbiome and Substance Use Disorder vol.15, 2019, https://doi.org/10.3389/fnins.2021.725500
  4. Early-Life Stress Modulates Gut Microbiota and Peripheral and Central Inflammation in a Sex-Dependent Manner vol.22, pp.4, 2019, https://doi.org/10.3390/ijms22041899
  5. Glucocorticoids and the Brain after Critical Illness vol.162, pp.3, 2021, https://doi.org/10.1210/endocr/bqaa242
  6. Chaihu-Shugan-San (Shihosogansan) alleviates restraint stress-generated anxiety and depression in mice by regulating NF-κB-mediated BDNF expression through the modulation of gut microbiota vol.16, pp.1, 2019, https://doi.org/10.1186/s13020-021-00492-5
  7. Homeostatic regulation of neuronal excitability by probiotics in male germ‐free mice vol.100, pp.2, 2019, https://doi.org/10.1002/jnr.24999