Neuro-active compounds produced by probiotics: Towards a microbiota-(Gut-) brain axis control?

Interactive Probiotics

Volumn , Issue , 2014, Pages 148-176

  Mazzoli, Roberto ^a  

^a NONE

Author keywords

Bio active amines; Enteric nervous system; Enterotypes; GABA; Glutamate; Lactic acid bacteria; Microbial endocrinology; Opioid and antiopioid peptides; Short chain fatty acids

Indexed keywords

EID: 85017037000     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/b16439     Document Type: Chapter

References (109)

1. Adams, J.B., L.J. Johansen, L.D. Powell, D. Quig and R.A. Rubin. 2011. Gastrointestinal fl ora and gastrointestinal status in children with autism-comparisons to typical children and correlation with autism severity. BMC Gastroenterol. 11: 22.
2. Akiba, Y., C. Watanabe, M. Mizumori and J.D. Kaunitz. 2009. Luminal L-glutamate enhances duodenal mucosal defense mechanisms via multiple glutamate receptors in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 297: G781-G791.
3. Arseneault-Breard, J., I. Rondeau, K. Gilbert, S.A. Girard, T.A. Tompkins, R. Godbout and G. Rousseau. 2012. Combination of Lactobacillus helveticus R0052 and Bifi dobacterium longum R0175 reduces post-myocardial infarction depression symptoms and restores intestinal permeability in a rat model. Br. J. Nutr. 107: 1793-1799.
4. Artemova, N.V., Z.M. Bumagina, A.S. Kasakov, V.V. Shubin and B.Y. Gurvits. 2010. Opioid peptides derived from food proteins suppress aggregation and promote reactivation of partly unfolded stressed proteins. Peptides 31: 332-338.
5. Artis, D. 2008. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nature Rev. Immunol. 8: 411-420.
6. Arumugam, M., J. Raes, E. Pelletier, D. Le Paslier, T. Yamada, D.R. Mende, G.R. Fernandes, J. Tap, T. Bruls, J.M. Batto, M. Bertalan, N. Borruel, F. Casellas, L. Fernandez, L. Gautier, T. Hansen, M. Hattori, T. Hayashi, M. Kleerebezem, K. Kurokawa, M. Leclerc, F. Levenez, C. Manichanh, H.B. Nielsen, T. Nielsen, N. Pons, J. Poulain, J. Qin, T. Sicheritz-Ponten, S. Tims, D. Torrents, E. Ugarte, E.g. Zoetendal, J. Wang, F. Guarner, O. Pedersen, W.M. de Vos, S. Brunak, J. Doré, J. MetaHIT Consortium, M. Antolín, F. Artiguenave, H.M. Blottiere, M. Almeida, C. Brechot, C. Cara, C. Chervaux, A. Cultrone, C. Delorme, G. Denariaz, R. Dervyn, K.U. Foerstner, C. Friss, M. van de Guchte, E. Guedon, F. Haimet, W. Huber, J. van Hylckama-Vlieg, A. Jamet, C. Juste, G. Kaci, J. Knol, O. Lakhdari, S. Layec, K. Le Roux, E. Maguin, A. Mérieux, R. Melo Minardi, C. M’rini, J. Muller, R. Oozeer, J. Parkhill, P. Renault, M. Rescigno, N. Sanchez, S. Sunagawa, A. Torrejon, K. Turner, G. Vandemeulebrouck, E. Varela, Y. Winogradsky, G. Zeller, J. Weissenbach, S.D. Ehrlich and P. Bork. 2011. Enterotypes of the human gut microbiome. Nature 473: 174-180.
7. Aziz, Q., J. Doré, A. Emmanuel, F. Guarner and E.M. Quigley. 2013. Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroenterol. Motil. 25: 4-15.
8. Barbara, G., B. Wang, V. Stanghellini, R. de Giorgio, C. Cremon, G. Di Nardo, M. Trevisani, B. Campi, P. Geppetti, M. Tonini, N.W. Bunnett, D. Grundy and R. Corinaldesi. 2007. Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 132: 26-37.
9. Bercik, P., E.F. Verdu, J.A. Foster, J. Macri, M. Potter, X. Huang, P. Malinowski, W. Jackson, P. Blennerhassett, K.A. Neufeld, J. Lu, W.I. Khan, I. Corthesy-Theulaz, C. Cherbut, G.E. Bergonzelli and S.M. Collins. 2010. Chronic gastrointestinal infl ammation induces anxietylike behavior and alters central nervous system biochemistry in mice. Gastroenterology 139: 2102-2112.
10. Bercik, P., A.J. Park, D. Sinclair, A. Khoshdel, J. Lu, X. Huang, Y. Deng, P.A. Blennerhassett, M. Fahnestock, D. Moine, B. Berger, J.D. Huizinga, W. Kunze, P.G. McLean, G.E. Bergonzelli, S.M. Collins and E.F. Verdu. 2011. The anxiolytic effect of Bifi dobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol. Motil. 23: 1132-1139.
11. Bercik, P., E. Denou, J. Collins, W. Jackson, J. Lu, J. Jury, Y. Deng, P. Blennerhassett, J. Macri, K.D. McCoy, E.F. Verdu, S.M. Collins. 2011. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141: 599-609.
12. Bercik, P., S.M. Collins and E.F. Verdu. 2012. Microbes and the gut-brain axis. Neurogastroenterol. Motil. 24: 405-413.
13. Berer, K., M. Mues, M. Koutrolos, Z.A. Rasbi, M. Boziki, C. Johner, H. Wekerle and G. Krishnamoorthy. 2011. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479: 538-541.
14. Berntson, G.G., M. Sarter and J.T. Cacioppo. 2003. Ascending visceral regulation of cortical affective information processing. Eur. J. Neurosci. 18: 2103-2109.
15. Bienenstock, J. and S. Collins. 2010. 99th Dahlem conference on infection, infl ammation and chronic infl ammatory disorders: psycho-neuroimmunology and the intestinal microbiota: clinical observations and basic mechanisms. Clin. Exp. Immunol. 160: 85-91.
16. Bjurstöm, H., J. Wang, I. Ericsson, M. Bengtsson, Y. Liu, S. Kumar-Mendu, S. Issazadeh- Navikas and B. Birnir. 2008. GABA, a natural immunomodulator of T lymphocytes. J. Neuroimmunol. 205: 44-50.
17. Blachier, F., C. Boutry, C. Bos and D. Tome. 2009. Metabolism and functions of L-glutamate in the epithelial cells of the small and large intestines. Am. J. Clin. Nutr. 90: 814S-821S.
18. Blackshaw, L.A. 2001. Receptors and transmission in the brain-gut axis: potential for novel therapies. IV. GABA(B) receptors in the brain-gastroesophageal axis. Am. J. Physiol. Gastrointest. Liver Physiol. 281: G311-315.
19. Bravo, J.A., P. Forsythe, M.V. Chew, E. Escaravage, H.M. Savignac, T.G. Dinan, J. Bienenstock and J.F. Cryan. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central gaba receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. USA 108: 16050-16055.
20. Burchett, S.A. and T.P. Hicks. 2006. The mysterious trace amines: protean neuromodulators of synaptic transmission in mammalian brain. Prog. Neurobiol. 79: 223-246.
21. Burks, T.F. 1995. Opioid peptides in gastrointestinal functions. In: Tseng L.F. The Pharmacology of Opioid Peptides. Harwood Academic, New York, USA, pp. 397-409.
22. Cao, J.H., S.L. Huang, J. Qian, J.L. Huang, L.X. Jin, Z. Su, J. Yang and J.F. Liu. 2009. Evolution of the class C GPCR Venus fl ytrap modules involved positive selected functional divergence. BMC Evol. Biol. 9: 67.
23. Clare, D.A. and H.E. Swaisgood. 2000. Bioactive milk peptides: a prospectus. J. Dairy Sci. 83: 1187-1195.
24. Clarke, G., J.F. Cryan, T.G. Dinan and E.M. Quigley. 2012. Review article: probiotics for the treatment of irritable bowel syndrome-focus on lactic acid bacteria. Aliment. Pharmacol. Ther. 35: 403-413.
25. Costedio, M.M., N. Hyman and G.M. Mawe. 2007. Serotonin and its role in colonic function and in gastrointestinal disorders. Dis. Colon Rectum 50: 376-388.
26. Cryan, J.F. and S.M. O’Mahony. 2011. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol. Motil. 23: 187-192.
27. Cryan, J.F. and T.G. Dinan. 2012. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13: 701-712.
28. den Hengst, C.D., P. Curley, R. Larsen, G. Buist, A. Nauta, D. van Sinderen, O.P Kuipers and J. Kok. 2005. Probing direct interactions between CodY and the oppD promoter of Lactococcus lactis. J. Bacteriol. 187: 512-521.
29. Desbonnet, L., L. Garrett, G. Clarke, J. Bienenstock and T.G. Dinan. 2008. The probiotic Bifi dobacteria infantis: An assessment of potential antidepressant properties in the rat. J. Psychiatr. Res. 43: 164-174.
30. Doeven, M.K., J. Kok and B. Poolman. 2005. Specifi city and selectivity determinants of peptide transport in Lactococcus lactis and other microorganisms. Mol. Microbiol. 57: 640-649.
31. Engelstoft, M.S., K.L. Egerod, B. Holst and T.W. Schwartz. 2008. A gut feeling for obesity: 7TM sensors on enteroendocrine cells. Cell Metab. 8: 447-449.
32. Fallarino, F., C. Volpi, F. Fazio, S. Notartomaso, C. Vacca, C. Busceti, S. Bicciato, G. Battaglia, V. Bruno, P. Puccetti, M.C. Fioretti, F. Nicoletti, U. Grohmann and R. Di Marco. 2010. Metabotropic glutamate receptor-4 modulates adaptive immunity and restrains neuroinfl ammation. Nat. Med. 16: 897-902.
33. Forsythe, P. and W.A. Kunze. 2012. Voices from within: gut microbes and the CNS. Cell. Mol. Life Sci. 26 May 2012 (doI:10.1007/s00018-012-1028-z).
34. Furness, J.B. 2006. The Enteric Nervous System. Blackwell, Oxford, U.K.
35. Gershon, M.D. 1998. The Second Brain. Harper Collins, New York, USA.
36. Gershon, M.D. 2005. Nerves, refl exes, and the enteric nervous system: pathogenesis of the irritable bowel syndrome. J. Clin. Gastroenterol. 39: S184-S193.
37. Gershon, M.D. and J. Tack. 2007. The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology 132: 397-414.
38. Gobbetti, M., L. Stepaniak, M. De Angelis, A. Corsetti and R. Di Cagno. 2002. Latent bioactive peptides in milk proteins: proteolytic activation and signifi cance in dairy processing. CRC Crit. Rev. Food. Sci. Nutr. 42: 223-239.
39. Gou, Z.H., X. Wang and W. Wang. 2012. Evolution of neurotransmitter gamma-aminobutyric acid, glutamate and their receptors. Dongwuxue Yanjiu 33: E75-81.
40. Graham, T.E., V. Sgro, D. Friars and M.J. Gibala. 2000. Glutamate ingestion: the plasma and muscle free amino acid pools of resting humans. Am. J. Physiol. Endocrinol. Metab. 278: E83-E89.
41. Hara, K., Y. Saito, Y. Kirihara, Y. Yamada, S. Sakura and Y. Kosaka. 1999. The interaction of antinociceptive effects of morphine and GABA receptor agonists within the rat spinal cord. Anesth. Analg. 89: 422-427.
42. Hara, K., Y. Saito, Y. Kirihara and S. Sakura. 2004. The interaction between gamma-aminobutyric acid agonists and diltiazem in visceral antino ciception in rats. Anesth. Analg. 98: 1380-1384.
43. Hawkins, R.A. 2009. The blood-brain barrier and glutamate. Am. J. Clin. Nutr. 90: 867S-874S.
44. Hayes, M., C. Stanton, G.F. Fitzgerald and R.P. Ross. 2007a. Putting microbes to work: dairy fermentation, cell factories and bioactive peptides. Part II: bioactive peptide functions. Biotechnol. J. 2: 435-449.
45. Hayes, M., R.P. Ross, G.F. Fitzgerald and C. Stanton. 2007b. Putting microbes to work: dairy fermentation, cell factories and bioactive peptides. Part I: overview. Biotechnol. J. 2: 426-434.
46. Hernández-Ledesma, B., I. Recio and L. Amigo. 2008. Beta-lactoglobulin as source of bioactive peptides. Amino Acids 35: 257-265.
47. Hiraga, K., Y. Ueno and K. Oda. 2008. Glutamate decarboxylase from Lactobacillus brevis: activation by ammonium sulfate. Biosci. Biotechnol. Biochem. 72: 1299-1306.
48. Hughes, D.T. and V. Sperandio. 2008. Inter-kingdom signalling: communication between bacteria and their hosts. Nat. Rev. Microbiol. 6: 111-120.
49. Hyland, N.P. and J.F. Cryan. 2010. A Gut Feeling about GABA: Focus on GABA(B) Receptors. Front. Pharmacol. 1: 124.
50. Julio-Pieper, M., R.M. O’Connor, T.G. Dinan and J.F. Cryan. 2013. Regulation of the brain-gut axis by group III metabotropic glutamate receptors. Eur. J. Pharmacol. 698: 19-30.
51. Kandler, O. 1983. Carbohydrate metabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 49: 209-224.
52. Kaneko, K., M. Iwasaki, M. Yoshikawa and K. Ohinata. 2010. Orally administered soymorphins, soy-derived opioid peptides, suppress feeding and intestinal transit via gut mu(1)- receptor coupled to 5-HT(1A), D(2), and GABA(B) systems. Am. J. Physiol. Gastrointest. Liver Physiol. 299: G799-805.
53. Keita, A.V. and J.D. Söderholm. 2010. The intestinal barrier and its regulation by neuroimmune factors. Neurogastroenterol. Motil. 22: 718-733.
54. Klaenhammer, T.R., R. Barrangou, B.L. Buck, M.A. Azcarate-Peril and E. Altermann. 2005. Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol. Rev. 29: 393-409.
55. Konings, W.N. 2006. Microbial transport: adaptations to natural environments. Antonie Van Leeuwenhoek 90: 325-342.
56. Kunji, E.R.S., I. Mierau, A. Hagting, B. Poolman and W.N. Konings. 1996. The proteolytic systems of lactic acid bacteria. Antonie Van Leeuwenhoek 70: 187-221.
57. Li, H. and Y. Cao. 2010. Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids 39: 1107-1116.
58. Logan, A. C. and M. Katzman. 2005. Major depressive disorder: probiotics may be an adjuvant therapy. Med. Hypotheses 64: 533-538.
59. Lyte, M. 2011. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics. Bioessays. 33: 574-581.
60. Lyte, M. and P.P.E. Freestone (eds.). 2010. Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health. Springer, New York, USA.
61. Ma, X., Y.K. Mao, B. Wang, J.D. Huizinga, J. Bienenstock and W. Kunze. 2009. Lactobacillus reuteri ingestion prevents hyperexcitability of colonic DRG neurons induced by noxious stimuli. Am. J. Physiol. Gastrointest. Liver Physiol. 296: G868-G875.
62. Matur, E. and E. Eraslan. 2012. The Impact of Probiotics on the Gastrointestinal Physiology. In: T. Brzozowski (ed.). New Advances in the Basic and Clinical Gastroenterology. In Tech, Rijeka, Croatia, pp 51-74.
63. Mawe, G.M., D.S. Strong and K.A. Sharkey. 2009. Plasticity of enteric nerve functions in the infl amed and postinfl amed gut. Neurogastroenterol. Motil. 21: 481-491.
64. Mayer, E.A. 2011. Gut feelings: the emerging biology of gut-brain communication. Nat. Rev. Neurosci. 12: 453-466.
65. Mazzoli, R., E. Pessione, M. Dufour, V. Laroute, M.G. Giuffrida, C. Giunta, M. Cocaign-Bousquet and P. Loubière. 2010. Glutamate-induced metabolic changes in Lactococcus lactis NCDO during GABA production: combined transcriptomic and proteomic analysis. Amino Acids 39: 727-737.
66. McDermott, J.R., F.C. Leslie, M. D’Amato, D.G. Thompson, R.K. Grencis and J.T. McLaughlin. 2006. Immune control of food intake: enteroendocrine cells are regulated by CD4+ T lymphocytes during small intestinal infl ammation. Gut. 55: 492-497.
67. Medzhitov, R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826.
68. Meisel, H. and R.J. FitzGerald. 2000. Opioid peptides encrypted in intact milk protein sequences. Br. J. Nutr. 84 Suppl 1: S27-31.
69. Meisel, H. 2004. Multifunctional peptides encrypted in milk proteins. Biofactors 21: 55-61.
70. Messaoudi, M., R. Lalonde, N. Violle, H. Javelot, D. Desor, A. Nejdi, J.F. Bisson, C. Rougeot, M. Pichelin, M. Cazaubiel and J.M. Cazaubiel. 2011. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifi dobacterium longum R0175) in rats and human subjects. Br. J. Nutr. 105: 755-764.
71. Mollereau, C., M. Parmentier, P. Mailleux, J.L. Butour, C. Moisand, P. Chalon, D. Caput, G. Vassart and J.C. Meunier. 1994. ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett. 341: 33-38.
72. Nazzaro, F., F. Fratianni, B. Nicolaus, A. Poli and P. Orlando. 2012. The prebiotic source infl uences the growth, biochemical features and survival under simulated gastrointestinal conditions of the probiotic Lactobacillus acidophilus. Anaerobe 18: 280-285.
73. Neufeld, K.M., N. Kang, J. Bienenstock and J.A. Foster. 2010. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 23: 255-264.
74. Nicholson, J.K., E. Holmes, J. Kinross, R. Burcelin, G. Gibson, W. Jia and S. Pettersson. 2012. Host-gut microbiota metabolic interactions. Science 336: 1262-1267.
75. Nock, B., A.L. Giordano, B.W. Moore and T.J. Cicero. 1993. Properties of the putative epsilon opioid receptor: identifi cation in rat, guinea pig, cow, pig and chicken brain. J. Pharmacol. Exp. Ther. 264: 349-359.
76. Parracho, H.M., M.O.Bingham, G.R. Gibson and A.L. McCartney. 2005. Differences between the gut microfl ora of children with autistic spectrum disorders and that of healthy children. J. Med. Microbiol. 54: 987-991.
77. Pederson, J.A., G.J. Mileski, B.C. Weimer and J.L. Steele. 1999. Genetic characterization of a cell envelope-associated proteinase from Lactobacillus helveticus CNRZ32. J. Bacteriol. 181: 4592-4597.
78. Pessione, A, C. Lamberti and E. Pessione. 2010. Proteomics as a tool for studying energy metabolism in lactic acid bacteria. Mol. Biosyst. 6: 1419-1430.
79. Pessione, E., A. Pessione, C. Lamberti, D.J. Coïsson, K. Riedel, R. Mazzoli, S. Bonetta, L. Eberl and C. Giunta. 2009. First evidence of a membrane-bound, tyramine and betaphenylethylamine producing, tyrosine decarboxylase in Enterococcus faecalis: a twodimensional electrophoresis proteomic study. Proteomics 9: 2695-2710.
80. Pessione, E. 2012. Lactic acid bacteria contribution to gut microbiota complexity: lights and shadows. Front. Cell. Infect. Microbiol. 2: 86.
81. Pfl uger, P.T., S.C. Schriever and M.H. Tschöp. 2012. Nutropioids, hedonism in the gut? Cell Metab. 16: 137-139.
82. Pihlanto, A. 2001. Bioactive peptides derived from bovine whey proteins: opioid and aceinhibitory peptides. Trends Food Sci. Technol. 11: 347-356.
83. Power, O., P. Jakeman and R.J. Fitzgerald. 2013. Antioxidative peptides: enzymatic production, in vitro and in vivo antioxidant activity and potential applications of milk-derived antioxidative peptides. Amino Acids 44: 797-820.
84. Raybould, H.E. 2010. Gut chemosensing: interactions between gut endocrine cells and visceral afferents. Auton. Neurosci. 153: 41-46.
85. Reid, G. 2011. Neuroactive probiotics. Bioessays 33: 562.
86. Rousseaux, C., X. Thuru, A. Gelot, N. Barnich, C. Neut, L. Dubuquoy, C. Dubuquoy, E. Merour, K. Geboes, M. Chamaillard, A. Ouwehand, G. Leyer, D. Carcano, J.F. Colombel, D. Ardid and O. Desreumaux. 2007. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat. Med. 13: 35-37.
87. Rozengurt, E. and C. Sternini. 2007. Taste receptor signaling in the mammalian gut. Curr. Opin. Pharmacol. 7: 557-562.
88. Rudolph, U. and H. Möhler. 2006. GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr. Opin. Pharmacol. 6: 18-23.
89. Samuel, B.S., A. Shaito, T. Motoike, F.E. Rey, F. Backhed, J.K. Manchester, R.E. Hammer, S.C. Williams, J. Crowley, M. Yanagisawa and J.I. Gordon. 2008. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein coupled receptor, Gpr41. Proc. Natl. Acad. Sci. USA 105: 16767-16772.
90. Sanders, J.W., K. Leenhouts, J. Burghoorn, J.R. Brands, G. Venema and J. Kok. 1998. A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol. Microbiol. 27: 299-310.
91. Savijoki, K., H. Ingmer and P. Varmanen. 2006. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 71: 394-406.
92. Shimazu, S. and I. Miklya. 2004. Pharmacological studies with endogenous enhancer substances: beta phenylethylamine, tryptamine and their synthetic derivatives. Prog. Neuropsychopharmacol. Biol. Psichiatry 28: 421-427.
93. Silva, S.V. and F.X. Malcata. 2005. Caseins as source of bioactive peptides. Int. Dairy J. 15: 1-15.
94. Stefanitsi, D., G. Sakellaris and J.R. Garel. 1995. The presence of two proteinases associated with the cell wall of Lactobacillus bulgaricus. FEMS Microbiol. Lett. 128: 53-58.
95. Sternini, C. 2001. Receptors and transmission in the brain-gut axis: potential for novel therapies III. µ-opioid receptors in the enteric nervous system. Am. J. Physiol. Gastrointest. Liver. Physiol. 281: G8-G15.
96. Sudo, N., Y. Chida, Y. Aiba, J. Sonoda, N. Oyama, X.N. Yu, C. Kubo and Y. Koga. 2004. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 558: 263-275.
97. Tanida, M., T. Yamano, K. Maeda, N. Okumura, Y. Fukushima and K. Nagai. 2005. Effects of intraduodenal injection of Lactobacillus johnsonii La1 on renal sympathetic nerve activity and blood pressure in urethane-anesthetized rats. Neurosci. Lett. 389: 109-114.
98. Tanous, C., E. Chambellon, A.M. Sepulchre and M. Yvon. 2005. The gene encoding the glutamate dehydrogenase in Lactococcus lactis is part of a remnant Tn3 transposon carried by a large plasmid. J. Bacteriol. 187: 5019-5022.
99. Teschemacher, H., G. Koch and V. Brantl. 1997. Milk protein-derived opioid receptor ligands. Biopolymers 43: 99-117.
100. Tillisch, K., J.S. Labus, B. Ebrat, J. Stains, B.D. Naliboff, D. Guyonnet, S. Legrain-Raspaud, B. Trotin and E.A. Mayer. 2012. Modulation of the brain-gut axis after 4-week intervention with a probiotic fermented dairy product. Gastroenterology 142: S-115.
101. Tramonti, A., M. De Canio, I. Delany, V. Scarlato and D. De Biase. 2006. Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate based acid resistance system in Escherichia coli. J. Bacteriol. 188: 8118-8127.
102. Tynkkynen, S., G. Buist, E. Kunji, J. Kok, B. Poolman, G. Venema and A. Haandrikman. 1993. Genetic and biochemical characterization of the oligopeptide transport system of Lactococcus lactis. J. Bacteriol. 175: 7523-7532.
103. Van Oudenhove, L., S. McKie, D. Lassman, B. Uddin, P. Paine, S. Coen, L. Gregory, J. Tack and Q. Aziz. 2011. Fatty acid-induced gut-brain signaling attenuates neural and behavioral effects of sad emotion in humans. J. Clin. Invest. 121: 3094-3099.
104. Vaughan, E.E., G.W. Tannock, S. Salminen and L. Morelli. 2011. Healthy heroes: LABs and gut microbes. In: A. Ledeboer, J. Hugenholtz, J. Kok, W. Konings and J. Wouters (eds.). Thirthy years of research on lactic acid bacteria. M. Bingham, 24 Media Labs, Rotterdam, The Netherlands, pp. 151-169.
105. Wang, L., C.T. Christophersen, M.J. Sorich, J.P. Gerber, M.T. Angley and M.A. Conlon. 2012. Elevated fecal short chain fatty acid and ammonia concentrations in children with autism spectrum disorder. Dig. Dis. Sci. 57: 2096-2102.
106. Wikoff, W., A. Anfora, J. Liu, P. Schultz, S.A. Lesley, E.C. Peters and G. Siuzdak. 2009. Metabolomics analysis reveals large effects of gut microfl ora on mammalian blood metabolites. Proc. Natl. Acad. Sci. USA 106: 3698-3703.
107. Williams, B.L., M. Hornig, T. Buie, M.L. Bauman, M. Cho Paik, I. Wick, A. Bennett, O. Jabado, D.L. Hirschberg and W.I. Lipkin. 2011. Impaired carbohydrate digestion and transport and mucosal dysbiosis in the intestines of children with autism and gastrointestinal disturbances. PLoS ONE 6: e24585.
108. Wu, S.V. and H. Hui. 2011. Treat your bug right. Front. Physiol. 2: 9.
109. Zareian, M., A. Ebrahimpour, F.A. Bakar, A.K. Mohamed, B. Forghan, M.S. Ab-Kadir and N. Saari. 2012. A glutamic acid-producing lactic acid bacteria isolated from Malaysian fermented foods. Int. J. Mol. Sci. 13: 5482-5497.