New perspectives of Lactobacillus plantarum as a probiotic: The gut-heart-brain axis

Abstract

Lactobacillus plantarum is a non-gas-producing lactic acid bacterium that is generally regarded as safe (GRAS) with Qualified Presumption of Safety (QPS) status. Although traditionally used for dairy, meat and vegetable fermentation, L. plantarum is gaining increasing significance as a probiotic. With the newly acclaimed gut-heart-brain axis, strains of L. plantarum have proven to be a valuable species for the development of probiotics, with various beneficial effects on gut health, metabolic disorders and brain health. In this review, the classification and taxonomy, and the relation of these with safety aspects are introduced. Characteristics of L. plantarum to fulfill the criteria as a probiotic are discussed. Emphasis are also given to the beneficial functions of L. plantarum in gut disorders such as inflammatory bowel diseases, metabolic syndromes, dyslipidemia, hypercholesteromia, obesity, and diabetes, and brain health aspects involving psychological disorders.

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References

  1. Aggarwal, B.B. 2003. Signalling pathways of the TNF superfamily: a double-edged sword. Nat. Rev. Immunol. 3, 745–756.

    PubMed  Article  CAS  Google Scholar 

  2. Axling, U., Olsson, C., Xu, J., Fernandez, C., Larsson, S., Strom, K., Ahrne, S., Holm, C., Molin, G., and Berger, K. 2012. Green tea powder and Lactobacillus plantarum affect gut microbiota, lipid metabolism and inflammation in high-fat fed C57BL/6J mice. Nutr. Metab. (Lond) 9, 105.

    Article  CAS  Google Scholar 

  3. Backhed, F., Ding, H., Wang, T., Hooper, L.V., Koh, G.Y., Nagy, A., Semenkovich, C.F., and Gordon, J.I. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 101, 15718–15723.

    PubMed  Article  CAS  Google Scholar 

  4. Bejar, W., Hamden, K., Ben Salah, R., and Chouayekh, H. 2013. Lactobacillus plantarum TN627 significantly reduces complications of alloxan-induced diabetes in rats. Anaerobe 24, 4–11.

    PubMed  Article  CAS  Google Scholar 

  5. Belicova, A., Mikulasova, M., and Dusinsky, R. 2013. Probiotic potential and safety properties of Lactobacillus plantarum from Slovak Bryndza cheese. Biomed. Res. Int. 2013, 760298.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  6. Beutler, B. 2004. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430, 257–263.

    PubMed  Article  CAS  Google Scholar 

  7. Booijink, C.C., Zoetendal, E.G., Kleerebezem, M., and de Vos, W.M. 2007. Microbial communities in the human small intestine: coupling diversity to metagenomics. Future Microbiol. 2, 285–295.

    PubMed  Article  CAS  Google Scholar 

  8. Bosch, M., Rodriguez, M., Garcia, F., Fernandez, E., Fuentes, M.C., and Cune, J. 2012. Probiotic properties of Lactobacillus plantarum CEC 7315 and CEC 7316 isolated from faeces of healthy children. Lett. Appl. Microbiol. 54, 240–246.

    PubMed  Article  CAS  Google Scholar 

  9. Cario, E. 2010. Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm. Bowel Dis. 16, 1583–1597.

    PubMed  PubMed Central  Article  Google Scholar 

  10. Cario, E. and Podolsky, D.K. 2000. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect. Immun. 68, 7010–7017.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  11. Cebeci, A. and Gürakan, C. 2003. Properties of potential probiotic Lactobacillus plantarum strains. Food Microbiol. 20, 511–518.

    Article  Google Scholar 

  12. Chao, S.H., Wu, R.J., Watanabe, K., and Tsai, Y.C. 2009. Diversity of lactic acid bacteria in suan-tsai and fu-tsai, traditional fermented mustard products of Taiwan. Int. J. Food Microbiol. 135, 203–210.

    PubMed  Article  Google Scholar 

  13. Chen, Y.Y., Lee, M.H., Hsu, C.C., Wei, C.L., and Tsai, Y.C. 2012. Methyl cinnamate inhibits adipocyte differentiation via activation of the CaMKK2-AMPK pathway in 3T3-L1 preadipocytes. J. Agric. Food Chem. 60, 955–963.

    PubMed  Article  CAS  Google Scholar 

  14. Chu, Z.X., Chen, H.Q., Ma, Y.L., Zhou, Y.K., Zhang, M., Zhang, P., and Qin, H.L. 2010. Lactobacillus plantarum prevents the upregulation of adhesion molecule expression in an experimental colitis model. Dig. Dis. Sci. 55, 2505–2513.

    PubMed  Article  CAS  Google Scholar 

  15. Coelho, R., Viola, T.W., Walss-Bass, C., Brietzke, E., and Grassi-Oliveira, R. 2014. Childhood maltreatment and inflammatory markers: a systematic review. Acta Psychiatr. Scand. 129, 180–192.

    PubMed  Article  CAS  Google Scholar 

  16. Cryan, J.F. and Holmes, A. 2005. The ascent of mouse: advances in modelling human depression and anxiety. Nat. Rev. Drug Discov. 4, 775–790.

    PubMed  Article  CAS  Google Scholar 

  17. de Goffau, M.C., Luopajarvi, K., Knip, M., Ilonen, J., Ruohtula, T., Harkonen, T., Orivuori, L., Hakala, S., Welling, G.W., Harmsen, H.J., et al. 2013. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes 62, 1238–1244.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  18. de Vos, W.M. and de Vos, E.A. 2012. Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr. Rev. 70 Suppl 1, S45–S56.

    PubMed  Article  Google Scholar 

  19. de Vos, W.M. and Hugenholtz, J. 2004. Engineering metabolic highways in Lactococci and other lactic acid bacteria. Trends Biotechnol. 22, 72–79.

    PubMed  Article  CAS  Google Scholar 

  20. Dinan, T.G. and Cryan, J.F. 2017. Gut-brain axis i 2016: Brain-gutmicrobiota axis - mood, metabolism and behaviour. Nat. Rev. Gastroenterol. Hepatol. 14, 69–70.

    PubMed  Article  CAS  Google Scholar 

  21. Dinan, T.G., Stanton, C., and Cryan, J.F. 2013. Psychobiotics: a novel class of psychotropic. Biol. Psychiatry 74, 720–726.

    PubMed  Article  CAS  Google Scholar 

  22. Donia, M.S. and Fischbach, M.A. 2015. Human microbiota. Small molecules from the human microbiota. Science 349, 1254766.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  23. Duary, R.K., Bhausaheb, M.A., Batish, V.K., and Grover, S. 2012. Anti-inflammatory and immunomodulatory efficacy of indigenous probiotic Lactobacillus plantarum Lp91 in colitis mouse model. Mol. Biol. Rep. 39, 4765–4775.

    PubMed  Article  CAS  Google Scholar 

  24. European Food Safety Authority (EFSA). 2018. Update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA 7: suitability of taxonomic units notified to EFSA until Septembe 2017. EFSA J. 16, 5131.

    Google Scholar 

  25. EFSA Panel on Dietetic Products, Nutrition and Allergies. 2010. Scientific Opinion on the substantiation of health claims related to live yoghurt cultures and improved lactose digestion (ID 1143, 2976) pursuant to Article 13(1) of Regulation (EC) N 1924 2006. EFSA J. 8, 1736.

    Article  CAS  Google Scholar 

  26. Fairweather, D. and Rose, N.R. 2005. Inflammatory heart disease: a role for cytokines. Lupus 14, 646–651.

    PubMed  Article  CAS  Google Scholar 

  27. Farmer, S.R. 2006. Transcriptional control of adipocyte formation. Cell. Metab. 4, 263–273.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  28. Food and Agriculture Organization/World Health Organization (FAO/WHO). 2002. Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. Food and Agriculture Organization/World Health Organization, London Ontario, Canada

  29. Francque, S.M., van der Graaff, D., and Kwanten, W.J. 2016. Nonalcoholic fatty liver disease and cardiovascular risk: Pathophysiological mechanisms and implications. J. Hepatol. 65, 425–443.

    PubMed  Article  CAS  Google Scholar 

  30. Fukata, M., Chen, A., Vamadevan, A.S., Cohen, J., Breglio, K., Krishnareddy, S., Hsu, D., Xu, R., Harpaz, N., Dannenberg, A.J., et al. 2007. Toll-like receptor-4 promotes the development of colitisassociated colorectal tumors. Gastroenterology 133, 1869–1881.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  31. Furusawa, Y., Obata, Y., and Hase, K. 2015. Commensal microbiota regulates T cell fate decision in the gut. Semin. Immunopathol. 37, 17–25.

    PubMed  Article  Google Scholar 

  32. Greenhalgh, C.J., Miller, M.E., Hilton, D.J., and Lund, P.K. 2002. Suppressors of cytokine signaling: Relevance to gastrointestinal function and disease. Gastroenterology 123, 2064–2081.

    PubMed  Article  CAS  Google Scholar 

  33. Gupta, A. and Tiwari, S.K. 2014. Probiotic potential of Lactobacillus plantarum LD1 isolated from batter of Dosa, a South Indian fermented food. Probiotics Antimicrob. Proteins 6, 73–81.

    PubMed  Article  CAS  Google Scholar 

  34. Ha, C.G., Cho, J.K., Lee, C.H., Chai, Y.G., Ha, Y.A., and Shin, S.H. 2006. Cholesterol lowering effect of Lactobacillus plantarum isolated from human feces. J. Microbiol. Biotechnol. 16, 1201–1209.

    CAS  Google Scholar 

  35. Hill-Burns, E.M., Debelius, J.W., Morton, J.T., Wissemann, W.T., Lewis, M.R., Wallen, Z.D., Peddada, S.D., Factor, S.A., Molho, E., Zabetian, C.P., et al. 2017. Parkinson’s disease and Parkinson’s disease medications have distinct signatures of the gut microbiome. Mov. Disord. 32, 739–749.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  36. Holzapfel, W.H. and Wood, B.J.B. 2014. Introduction to the LAB, pp. 1–12. In Holzapfel, W.H. and Wood, B.J.B. (eds.), Lactic acid bacteria: Biodiversity and taxonomy. John Wiley & Sons, Ltd, Chichester, UK.

    Google Scholar 

  37. Huang, H.Y., Korivi, M., Tsai, C.H., Yang, J.H., and Tsai, Y.C. 2013a. Supplementation of Lactobacillus plantarum K68 and fruit-vegetable ferment along with high fat-fructose diet attenuates metabolic syndrome in rats with insulin resistance. Evid. Based Complement. Alternat. Med. 2013, 943020.

    PubMed  PubMed Central  Google Scholar 

  38. Huang, R., Tao, X., Wan, C., Li, S., Xu, H., Xu, F., Shah, N.P., and Wei, H. 2015. In vitro probiotic characteristics of Lactobacillus plantarum ZD 2013 and its modulatory effect on gut microbiota of mice. J. Dairy Sci. 98, 5850–5861.

    PubMed  Article  CAS  Google Scholar 

  39. Huang, Y., Wang, X., Wang, J., Wu, F., Sui, Y., Yang, L., and Wang, Z. 2013b. Lactobacillus plantarum strains as potential probiotic cultures with cholesterol-lowering activity. J. Dairy Sci. 96, 2746–2753.

    PubMed  Article  CAS  Google Scholar 

  40. Ivanovic, N., Minic, R., Dimitrijevic, L., Radojevic Skodric, S., Zivkovic, I., and Djordjevic, B. 2015. Lactobacillus rhamnosus LA68 and Lactobacillus plantarum WCFS1 differently influence metabolic and immunological parameters in high fat diet-induced hypercholesterolemia and hepatic steatosis. Food Funct. 6, 558–565.

    PubMed  Article  CAS  Google Scholar 

  41. Izcue, A., Hue, S., Buonocore, S., Arancibia-Carcamo, C.V., Ahern, P.P., Iwakura, Y., Maloy, K.J., and Powrie, F. 2008. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 28, 559–570.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  42. Jang, S.E., Han, M.J., Kim, S.Y., and Kim, D.H. 2014. Lactobacillus plantarum CLP-0611 ameliorates colitis in mice by polarizing M1 to M2-like macrophages. Int. Immunopharmacol. 21, 186–192.

    PubMed  Article  CAS  Google Scholar 

  43. Jeong, J.J., Woo, J.Y., Kim, K.A., Han, M.J., and Kim, D.H. 2015. Lactobacillus pentosus var. plantarum C29 ameliorates age-dependent memory impairment in Fischer 344 rats. Lett. Appl. Microbiol. 60, 307–314.

    PubMed  Article  CAS  Google Scholar 

  44. Jeun, J., Kim, S., Cho, S.Y., Jun, H.J., Park, H.J., Seo, J.G., Chung, M.J., and Lee, S.J. 2010. Hypocholesterolemic effects of Lactobacillus plantarum KCTC3928 by increased bile acid excretion in C57BL/6 mice. Nutrition 26, 321–330.

    PubMed  Article  CAS  Google Scholar 

  45. Jiang, M., Zhang, F., Wan, C., Xiong, Y., Shah, N.P., Wei, H., and Tao, X. 2016. Evaluation of probiotic properties of Lactobacillus plantarum WLPL04 isolated from human breast milk. J. Dairy Sci. 99, 1736–1746.

    PubMed  Article  CAS  Google Scholar 

  46. Jung, I.H., Jung, M.A., Kim, E.J., Han, M.J., and Kim, D.H. 2012. Lactobacillus pentosus var. plantarum C29 protects scopolamineinduced memory deficit in mice. J. Appl. Microbiol. 113, 1498–1506.

    PubMed  Article  CAS  Google Scholar 

  47. Khan, M.J., Gerasimidis, K., Edwards, C.A., and Shaikh, M.G. 2016. Role of gut microbiota in the aetiology of obesity: Proposed mechanisms and review of the literature. J. Obes. 2016, 7353642.

    PubMed  PubMed Central  Google Scholar 

  48. Knosp, C.A., Schiering, C., Spence, S., Carroll, H.P., Nel, H.J., Osbourn, M., Jackson, R., Lyubomska, O., Malissen, B., Ingram, R., et al. 2013. Regulation of Foxp3+ inducible regulatory T cell stability by SOCS2. J. Immunol. 190, 3235–3245.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  49. Krawisz, J.E., Sharon, P., and Stenson, W.F. 1984. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 87, 1344–1350.

    PubMed  CAS  Google Scholar 

  50. Kubo, M., Hanada, T., and Yoshimura, A. 2003. Suppressors of cytokine signaling and immunity. Nat. Immunol. 4, 1169–1176.

    PubMed  Article  CAS  Google Scholar 

  51. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K., and Muller, W. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263–274.

    PubMed  Article  CAS  Google Scholar 

  52. Lee, I.A., Bae, E.A., Hyun, Y.J., and Kim, D.H. 2010. Dextran sulfate sodium and 2,4,6-trinitrobenzene sulfonic acid induce lipid peroxidation by the proliferation of intestinal gram-negative bacteria in mice. J. Inflamm. (Lond) 7, 7.

    Article  CAS  Google Scholar 

  53. Lee, H.A., Bong, Y.J., Kim, H., Jeong, J.K., Kim, H.Y., Lee, K.W., and Park, K.Y. 2015. Effect of nanometric Lactobacillus plantarum in kimchi on dextran sulfate sodium-induced colitis in mice. J. Med. Food 18, 1073–1080.

    PubMed  Article  CAS  Google Scholar 

  54. Lee, H.J., Jeong, J.J., Han, M.J., and Kim, D.H. 2018. Lactobacillus plantarum C29 Alleviates TNBS-induced memory impairment in mice. J. Microbiol. Biotechnol. 28, 175–179.

    PubMed  Google Scholar 

  55. Letunic, I. and Bork, P. 2016. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  56. Ley, R.E., Turnbaugh, P.J., Klein, S., and Gordon, J.I. 2006. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023.

    PubMed  Article  CAS  Google Scholar 

  57. Li, Y., de Haar, C., Chen, M., Deuring, J., Gerrits, M.M., Smits, R., Xia, B., Kuipers, E.J., and van der Woude, C.J. 2010. Disease-related expression of the IL6/STAT3/SOCS3 signalling pathway in ulcerative colitis and ulcerative colitis-related carcinogenesis. Gut 59, 227–235.

    PubMed  Article  CAS  Google Scholar 

  58. Li, C., Nie, S.P., Zhu, K.X., Ding, Q., Xiong, T., and Xie, M.Y. 2014. Lactobacillus plantarum NCU116 improves liver function, oxidative stress and lipid metabolism in rats with high fat diet induced non-alcoholic fatty liver disease. Food Funct. 5, 3216–3223.

    PubMed  Article  CAS  Google Scholar 

  59. Li, Q. and Verma, I.M. 2002. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2, 725–734.

    PubMed  Article  CAS  Google Scholar 

  60. Li, X., Wang, N., Yin, B., Fang, D., Jiang, T., Fang, S., Zhao, J., Zhang, H., Wang, G., and Chen, W. 2016a. Effects of Lactobacillus plantarum CCFM0236 on hyperglycaemia and insulin resistance in high-fat and streptozotocin-induced type 2 diabetic mice. J. Appl. Microbiol. 121, 1727–1736.

    PubMed  Article  CAS  Google Scholar 

  61. Li, X., Wang, N., Yin, B., Fang, D., Zhao, J., Zhang, H., Wang, G., and Chen, W. 2016b. Lactobacillus plantarum X1 with α-glucosidase inhibitory activity ameliorates type 2 diabetes in mice. RSC Advances 6, 63536–63547.

    Article  CAS  Google Scholar 

  62. Liu, W.H., Chuang, H.L., Huang, Y.T., Wu, C.C., Chou, G.T., Wang, S., and Tsai, Y.C. 2016a. Alteration of behavior and monoamine levels attributable to Lactobacillus plantarum PS128 in germ-free mice. Behav. Brain Res. 298, 202–209.

    PubMed  Article  CAS  Google Scholar 

  63. Liu, Y.W., Liu, W.H., Wu, C.C., Juan, Y.C., Wu, Y.C., Tsai, H.P., Wang, S., and Tsai, Y.C. 2016b. Psychotropic effects of Lactobacillus plantarum PS128 in early life-stressed and naive adult mice. Brain Res. 1631, 1–12.

    PubMed  Article  CAS  Google Scholar 

  64. Liu, Y.W., Su, Y.W., Ong, W.K., Cheng, T.H., and Tsai, Y.C. 2011a. Oral administration of Lactobacillus plantarum K68 ameliorates DSS-induced ulcerative colitis in BALB/c mice via the anti-inflammatory and immunomodulatory activities. Int. Immunopharmacol. 11, 2159–2166.

    PubMed  Article  CAS  Google Scholar 

  65. Liu, Z., Zhang, P., Ma, Y., Chen, H., Zhou, Y., Zhang, M., Chu, Z., and Qin, H. 2011b. Lactobacillus plantarum prevents the development of colitis in IL-10-deficient mouse by reducing the intestinal permeability. Mol. Biol. Rep. 38, 1353–1361.

    PubMed  Article  CAS  Google Scholar 

  66. Liu, Z.J., Yadav, P.K., Su, J.L., Wang, J.S., and Fei, K. 2009. Poten tial role of Th17 cells in the pathogenesis of inflammatory bowel disease. World J. Gastroenterol. 15, 5784–5788.

    CAS  Google Scholar 

  67. Logan, A.C., Jacka, F.N., Craig, J.M., and Prescott, S.L. 2016. The microbiome and mental health: Looking back, moving forward with lessons from allergic diseases. Clin. Psychopharmacol. Neurosci. 14, 131–147.

    PubMed  PubMed Central  Article  Google Scholar 

  68. Lozupone, C.A., Stombaugh, J.I., Gordon, J.I., Jansson, J.K., and Knight, R. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  69. Lupien, S.J., McEwen, B.S., Gunnar, M.R., and Heim, C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 10, 434–445.

    PubMed  Article  CAS  Google Scholar 

  70. Madsen, K.L., Doyle, J.S., Jewell, L.D., Tavernini, M.M., and Fedorak, R.N. 1999. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116, 1107–1114.

    PubMed  Article  CAS  Google Scholar 

  71. Mancuso, C. and Santangelo, R. 2017. Alzheimer’s disease and gut microbiota modifications: The long way between preclinical studies and clinical evidence. Pharmacol. Res. 129, 329–336.

    PubMed  Article  CAS  Google Scholar 

  72. Martino, M.E., Bayjanov, J.R., Caffrey, B.E., Wels, M., Joncour, P., Hughes, S., Gillet, B., Kleerebezem, M., van Hijum, S.A., and Leulier, F. 2016. Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats. Environ. Microbiol. 18, 4974–4989.

    PubMed  Article  CAS  Google Scholar 

  73. Medzhitov, R. 2008. Origin and physiological roles of inflammation. Nature 454, 428–435.

    PubMed  Article  CAS  Google Scholar 

  74. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., and O’Garra, A. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683–765.

    PubMed  Article  CAS  Google Scholar 

  75. Mouzaki, M., Comelli, E.M., Arendt, B.M., Bonengel, J., Fung, S.K., Fischer, S.E., McGilvray, I.D., and Allard, J.P. 2013. Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology 58, 120–127.

    PubMed  Article  CAS  Google Scholar 

  76. Mulders, R.J., de Git, K.C.G., Schele, E., Dickson, S.L., Sanz, Y., and Adan, R.A.H. 2018. Microbiota in obesity: interactions with enteroendocrine, immune and central nervous systems. Obes. Rev. 19, 435–451.

    PubMed  Article  CAS  Google Scholar 

  77. Murri, M., Leiva, I., Gomez-Zumaquero, J.M., Tinahones, F.J., Cardona, F., Soriguer, F., and Queipo-Ortuno, M.I. 2013. Gut microbiota in children with type 1 diabetes differs from that in healthy children: a case-control study. BMC Med. 11, 46.

    PubMed  PubMed Central  Article  Google Scholar 

  78. O’Hara, A.M. and Shanahan, F. 2006. The gut flora as a forgotten organ. EMBO Rep. 7, 688–693.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  79. O’Mahony, S.M., Hyland, N.P., Dinan, T.G., and Cryan, J.F. 2011. Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl) 214, 71–88.

    Article  CAS  Google Scholar 

  80. Okumura, R. and Takeda, K. 2018. Maintenance of intestinal homeostasis by mucosal barriers. Inflamm. Regen. 38, 5.

    PubMed  PubMed Central  Article  Google Scholar 

  81. Park, D.Y., Ahn, Y.T., Park, S.H., Huh, C.S., Yoo, S.R., Yu, R., Sung, M.K., McGregor, R.A., and Choi, M.S. 2013a. Supplementation of Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032 in diet-induced obese mice is associated with gut microbial changes and reduction in obesity. PLoS One 8, e59470.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  82. Park, S.Y., Cho, S.A., Kim, S.H., and Lim, S.D. 2014a. Physiological characteristics and anti-obesity effect of Lactobacillus plantarum Q180 isolated from feces. Korean J. Food Sci. Anim. Resour. 34, 647–655.

    Article  Google Scholar 

  83. Park, S.Y., Cho, S.A., Lee, M.K., and Lim, S.D. 2015. Effect of Lactobacillus plantarum FH185 on the reduction of adipocyte size and gut microbial changes in mice with diet-induced obesity. Korean J. Food Sci. Anim. Resour. 35, 171–178.

    Article  Google Scholar 

  84. Park, S., Ji, Y., Jung, H.Y., Park, H., Kang, J., Choi, S.H., Shin, H., Hyun, C.K., Kim, K.T., and Holzapfel, W.H. 2017. Lactobacillus plantarum HAC01 regulates gut microbiota and adipose tissue accumulation in a diet-induced obesity murine model. Appl. Microbiol. Biotechnol. 101, 1605–1614.

    PubMed  Article  CAS  Google Scholar 

  85. Park, S.Y. and Lim, S.D. 2015. Probiotic characteristics of Lactobacillus plantarum FH185 isolated from human feces. Korean J. Food Sci. Anim. Resour. 35, 615–621.

    Article  Google Scholar 

  86. Park, J.E., Oh, S.H., and Cha, Y.S. 2013b. Lactobacillus plantarum LG42 isolated from gajami sik-hae inhibits adipogenesis in 3T3- L1 adipocyte. Biomed. Res. Int. 2013, 460927.

    PubMed  PubMed Central  Google Scholar 

  87. Park, J.E., Oh, S.H., and Cha, Y.S. 2014b. Lactobacillus plantarum LG42 isolated from gajami sik-hae decreases body and fat pad weights in diet-induced obese mice. J. Appl. Microbiol. 116, 145–156.

    PubMed  Article  CAS  Google Scholar 

  88. Parte, A.C. 2014. LPSN-list of prokaryotic names with standing in nomenclature. Nucleic Acids Res. 42, D613–D616.

    PubMed  Article  CAS  Google Scholar 

  89. Perez-Lopez, A., Behnsen, J., Nuccio, S.P., and Raffatellu, M. 2016. Mucosal immunity to pathogenic intestinal bacteria. Nat. Rev. Immunol. 16, 135–148.

    PubMed  Article  CAS  Google Scholar 

  90. Perse, M. and Cerar, A. 2011. Morphological and molecular alterations in 1,2 dimethylhydrazine and azoxymethane induced colon carcinogenesis in rats. J. Biomed. Biotechnol. 2011, 473964.

    PubMed  Article  CAS  Google Scholar 

  91. Raman, M., Ahmed, I., Gillevet, P.M., Probert, C.S., Ratcliffe, N.M., Smith, S., Greenwood, R., Sikaroodi, M., Lam, V., Crotty, P., et al. 2013. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin. Gastroenterol. Hepatol. 11, 868–875.

    PubMed  Article  CAS  Google Scholar 

  92. Sakaguchi, S. 2005. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6, 345–352.

    PubMed  Article  CAS  Google Scholar 

  93. Sakai, T., Taki, T., Nakamoto, A., Shuto, E., Tsutsumi, R., Toshimitsu, T., Makino, S., and Ikegami, S. 2013. Lactobacillus plantarum OLL2712 regulates glucose metabolism in C57BL/6 mice fed a high-fat diet. J. Nutr. Sci. Vitaminol. (Tokyo) 59, 144–147.

    Article  CAS  Google Scholar 

  94. Salaj, R., Stofilova, J., Soltesova, A., Hertelyova, Z., Hijova, E., Bertkova, I., Strojny, L., Kruzliak, P., and Bomba, A. 2013. The effects of two Lactobacillus plantarum strains on rat lipid metabolism receiving a high fat diet. Sci. World J. 2013, 135142.

    Article  CAS  Google Scholar 

  95. Saraiva, M. and O’Garra, A. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10, 170–181.

    PubMed  Article  CAS  Google Scholar 

  96. Satish Kumar, C.S., Kondal Reddy, K., Reddy, A.G., Vinoth, A., Ch, S.R., Boobalan, G., and Rao, G.S. 2015. Protective effect of Lactobacillus plantarum 21, a probiotic on trinitrobenzenesulfonic acid-induced ulcerative colitis in rats. Int. Immunopharmacol. 25, 504–510.

    PubMed  Article  CAS  Google Scholar 

  97. Schultz, J. and Kaminker, K. 1962. Myeloperoxidase of the leucocyte of normal human blood. I. Content and localization. Arch. Biochem. Biophys. 96, 465–467.

    PubMed  Article  CAS  Google Scholar 

  98. Schultz, M., Veltkamp, C., Dieleman, L.A., Grenther, W.B., Wyrick, P.B., Tonkonogy, S.L., and Sartor, R.B. 2002. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel Dis. 8, 71–80.

    PubMed  Article  Google Scholar 

  99. Seki, Y., Inoue, H., Nagata, N., Hayashi, K., Fukuyama, S., Matsumoto, K., Komine, O., Hamano, S., Himeno, K., Inagaki-Ohara, K., et al. 2003. SOCS-3 regulates onset and maintenance of T(H)2-mediated allergic responses. Nat. Med. 9, 1047–1054.

    PubMed  Article  Google Scholar 

  100. Song, J.J., Tian, W.J., Kwok, L.Y., Wang, Y.L., Shang, Y.N., Menghe, B., and Wang, J.G. 2017. Effects of microencapsulated Lactobacillus plantarum LIP-1 on the gut microbiota of hyperlipidaemic rats. Br. J. Nutr. 118, 481–492.

    PubMed  Article  CAS  Google Scholar 

  101. Stenkula, K.G. and Erlanson-Albertsson, C. 2018. Adipose cell size: Importance in health and disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. DOI: 10.1152/ajpregu.00257.2017

    Google Scholar 

  102. Stofilova, J., Szabadosova, V., Hrckova, G., Salaj, R., Bertkova, I., Hijova, E., Strojny, L., and Bomba, A. 2015. Co-administration of a probiotic strain Lactobacillus plantarum LS/07 CCM7766 with prebiotic inulin alleviates the intestinal inflammation in rats exposed to N,N-dimethylhydrazine. Int. Immunopharmacol. 24, 361–368.

    PubMed  Article  CAS  Google Scholar 

  103. Strati, F., Cavalieri, D., Albanese, D., De Felice, C., Donati, C., Hayek, J., Jousson, O., Leoncini, S., Renzi, D., Calabro, A., et al. 2017. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 5, 24.

    PubMed  PubMed Central  Article  Google Scholar 

  104. Suzuki, A., Hanada, T., Mitsuyama, K., Yoshida, T., Kamizono, S., Hoshino, T., Kubo, M., Yamashita, A., Okabe, M., Takeda, K., et al. 2001. CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J. Exp. Med. 193, 471–481.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  105. Sydora, B.C., Tavernini, M.M., Wessler, A., Jewell, L.D., and Fedorak, R.N. 2003. Lack of interleukin-10 leads to intestinal inflammation, independent of the time at which luminal microbial colonization occurs. Inflamm. Bowel Dis. 9, 87–97.

    PubMed  Article  Google Scholar 

  106. Taylor, A., Verhagen, J., Blaser, K., Akdis, M., and Akdis, C.A. 2006. Mechanisms of immune suppression by interleukin-10 and transforming growth factor-beta: the role of T regulatory cells. Immunology 117, 433–442.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  107. Turchi, B., Mancini, S., Fratini, F., Pedonese, F., Nuvoloni, R., Bertelloni, F., Ebani, V.V., and Cerri, D. 2013. Preliminary evaluation of probiotic potential of Lactobacillus plantarum strains isolated from Italian food products. World J. Microbiol. Biotechnol. 29, 1913–1922.

    Article  Google Scholar 

  108. Turnbaugh, P.J. and Gordon, J.I. 2009. The core gut microbiome, energy balance and obesity. J. Physiol. 587, 4153–4158.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  109. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A., Affourtit, J.P., et al. 2009. A core gut microbiome in obese and lean twins. Nature 457, 480–484.

    PubMed  Article  CAS  Google Scholar 

  110. Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., and Gordon, J.I. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031.

    PubMed  Article  Google Scholar 

  111. U.S. Food and Drug Administration (U.S. FDA). 2015. Generally recognized as safe: Microorganisms & microbial-derived ingredients used in food. Vol 2017.

    Google Scholar 

  112. Vanderpool, C., Yan, F., and Polk, D.B. 2008. Mechanisms of probiotic action: Implications for therapeutic applications in inflammatory bowel diseases. Inflamm. Bowel Dis. 14, 1585–1596.

    PubMed  Article  Google Scholar 

  113. Vazquez-Vela, M.E., Torres, N., and Tovar, A.R. 2008. White adipose tissue as endocrine organ and its role in obesity. Arch. Med. Res. 39, 715–728.

    PubMed  Article  CAS  Google Scholar 

  114. Wang, Z., Klipfell, E., Bennett, B.J., Koeth, R., Levison, B.S., Dugar, B., Feldstein, A.E., Britt, E.B., Fu, X., Chung, Y.M., et al. 2011. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57–63.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  115. Wang, L.X., Liu, K., Gao, D.W., and Hao, J.K. 2013. Protective effects of two Lactobacillus plantarum strains in hyperlipidemic mice. World J. Gastroenterol. 19, 3150–3156.

    CAS  Google Scholar 

  116. Whiteford, H.A., Ferrari, A.J., Degenhardt, L., Feigin, V., and Vos, T. 2015. The global burden of mental, neurological and substance use disorders: an analysis from the Global Burden of Disease Stud 2010. PLoS One 10, e0116820.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  117. Woese, C.R. 1987. Bacterial evolution. Microbiol. Rev. 51, 221–271.

    PubMed  PubMed Central  CAS  Google Scholar 

  118. Woo, J.Y., Gu, W., Kim, K.A., Jang, S.E., Han, M.J., and Kim, D.H. 2014. Lactobacillus pentosus var. plantarum C29 ameliorates memory impairment and inflammaging in a D-galactose-induced accelerated aging mouse model. Anaerobe 27, 22–26.

    PubMed  Article  CAS  Google Scholar 

  119. World Health Organization (WHO). 2015. Fact sheet: Obesity and overweight. http://www.who.int/mediacentre/factsheets/fs311/en/ (Assessed date: Feb. 13, 2018)

    Google Scholar 

  120. World Health Organization (WHO). 2016. Fact sheet: Mental health: strengthening our response. http://www.who.int/mediacentre/ factsheets/fs220/en/ (Assessed date: Feb. 13, 2018)

    Google Scholar 

  121. World Health Organization (WHO). 2017. Fact Sheets: Diabetes. http://www.who.int/en/news-room/fact-sheets/detail/diabetes (Assessed date: Aug. 3, 2018)

    Google Scholar 

  122. Wu, C.C., Weng, W.L., Lai, W.L., Tsai, H.P., Liu, W.H., Lee, M.H., and Tsai, Y.C. 2015. Effect of Lactobacillus plantarum strain K21 on high-fat diet-fed obese mice. Evid. Based Complement Alternat. Med. 2015, 391767.

    PubMed  PubMed Central  Google Scholar 

  123. Xu, H., Barnes, G.T., Yang, Q., Tan, G., Yang, D., Chou, C.J., Sole, J., Nichols, A., Ross, J.S., Tartaglia, L.A., et al. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Investing. 112, 1821–1830.

    Article  CAS  Google Scholar 

  124. Yakovlieva, M., Tacheva, T., Mihaylova, S., Tropcheva, R., Trifonova, K., Tolesmall ka, C.A., Danova, S., and Vlaykova, T. 2015. Influence of Lactobacillus brevis 15 and Lactobacillus plantarum 13 on blood glucose and body weight in rats after high-fructose diet. Benef. Microbes 6, 505–512.

    PubMed  Article  CAS  Google Scholar 

  125. Yu, Z., Zhang, X., Li, S., Li, C., Li, D., and Yang, Z. 2013. Evaluation of probiotic properties of Lactobacillus plantarum strains isolated from Chinese sauerkraut. World J. Microbiol. Biotechnol. 29, 489–498.

    Article  CAS  Google Scholar 

  126. Zago, M., Fornasari, M.E., Carminati, D., Burns, P., Suarez, V., Vinderola, G., Reinheimer, J., and Giraffa, G. 2011. Characterization and probiotic potential of Lactobacillus plantarum strains isolated from cheeses. Food Microbiol. 28, 1033–1040.

    PubMed  Article  CAS  Google Scholar 

  127. Zhang, J., Zhang, X., Zhang, L., Zhao, Y., Niu, C., Yang, Z., and Li, S. 2014. Potential probiotic characterization of Lactobacillus plantarum strains isolated from Inner Mongolia “Hurood” cheese. J. Microbiol. Biotechnol. 24, 225–235.

    PubMed  Article  CAS  Google Scholar 

  128. Zheng, Y., Lu, Y., Wang, J., Yang, L., Pan, C., and Huang, Y. 2013. Probiotic properties of Lactobacillus strains isolated from Tibetan kefir grains. PLoS One 8, e69868.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. Zuccato, C. and Cattaneo, E. 2009. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 5, 311–322.

    PubMed  Article  CAS  Google Scholar 

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Correspondence to Min-Tze Liong or Ying-Chieh Tsai.

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Liu, YW., Liong, MT. & Tsai, YC. New perspectives of Lactobacillus plantarum as a probiotic: The gut-heart-brain axis. J Microbiol. 56, 601–613 (2018). https://doi.org/10.1007/s12275-018-8079-2

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Keywords

  • Lactobacillus plantarum
  • gut-heart-brain axis
  • gut
  • metabolic syndromes
  • psychobiotics