GABA-producing Bifidobacterium dentium modulates visceral sensitivity in the intestine

Neurogastroenterology and Motility

Volumn 29, Issue 1, 2017, Pages

  Pokusaeva, K ^a,b   Johnson, C ^a,b   Luk, B ^a,b   Uribe, G ^a   Fu, Y ^c   Oezguen, N ^a,b   Matsunami, R K ^d   Lugo, M ^a   Major, A ^b   Mori Akiyama, Y ^a,b   Hollister, E B ^a,b   Dann, S M ^c   Shi, X Z ^c   Engler, D A ^d   Savidge, T ^a,b   Versalovic, J ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

Bifidobacterium; brain gut axis; GABA; microbiome; neuromodulation

Indexed keywords

4 AMINOBUTYRIC ACID; GADB PROTEIN; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; PROBIOTIC AGENT; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BIFIDOBACTERIUM; BIFIDOBACTERIUM DENTIUM; COMMENSAL; CONTROLLED STUDY; DECARBOXYLATION; ENZYME ASSAY; HYPERALGESIA; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; VISCERAL PAIN; ABDOMINAL PAIN; ANIMAL; BIOSYNTHESIS; CELL LINE; DRUG EFFECTS; FECES; GENETICS; HUMAN; INTESTINE; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; SPRAGUE DAWLEY RAT;

ABDOMINAL PAIN; ANIMALS; BASE SEQUENCE; BIFIDOBACTERIUM; CELL LINE; FECES; GAMMA-AMINOBUTYRIC ACID; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINES; MALE; MICE; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY; VISCERAL PAIN;

EID: 84979256685     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12904     Document Type: Article

References (79)

1. Bercik P, Collins SM, Verdu EF. Microbes and the gut-brain axis. Neurogastroenterol Motil. 2012;24:405–413.
2. Forsythe P, Kunze WA. Voices from within: gut microbes and the CNS. Cell Mol Life Sci. 2013;70:55–69.
3. Reid G. Neuroactive probiotics. BioEssays. 2011;33:562.
4. Lyte M. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design and use of probiotics. BioEssays. 2011;33:574–581.
5. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701–712.
6. Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011;23:187–192.
7. van De Sande MM, van Buul VJ, Brouns FJ. Autism and nutrition: the role of the gut-brain axis. Nutr Res Rev. 2014;27:199–214.
8. Unger MM, Ekman R, Bjorklund AK, Karlsson G, Andersson C, Mankel K, et al. Unimpaired postprandial pancreatic polypeptide secretion in Parkinson's disease and REM sleep behavior disorder. Mov Disord. 2013;28:529–533.
9. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011;108:16050–16055.
10. Rousseaux C, Thuru X, Gelot A, Barnich N, Neut C, Dubuquoy L, et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med. 2007;13:35–37.
11. Neufeld KM, Kang N, Bienenstock J, Foster JA. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil. 2011;23:255–264, e119.
12. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011;108:3047–3052.
13. Nishino R, Mikami K, Takahashi H, Tomonaga S, Furuse M, Hiramoto T, et al. Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods. Neurogastroenterol Motil. 2013;25:521–528.
14. Dupont HL. Review article: evidence for the role of gut microbiota in irritable bowel syndrome and its potential influence on therapeutic targets. Aliment Pharmacol Ther. 2014;39:1033–1042.
15. Collins SM. A role for the gut microbiota in IBS. Nat Rev Gastroenterol Hepatol. 2014;11:497–505.
16. Zhou Q, Verne GN. New insights into visceral hypersensitivity–clinical implications in IBS. Nat Rev Gastroenterol Hepatol. 2011;8:349–355.
17. Whorwell PJ, Altringer L, Morel J, Bond Y, Charbonneau D, O'Mahony L, et al. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am J Gastroenterol. 2006;101:1581–1590.
18. McKernan DP, Fitzgerald P, Dinan TG, Cryan JF. The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat. Neurogastroenterol Motil. 2010;22:1029–1035, e268.
19. Francavilla R, Miniello V, Magista AM, De Canio A, Bucci N, Gagliardi F, et al. A randomized controlled trial of Lactobacillus GG in children with functional abdominal pain. Pediatrics. 2010;126:e1445–e1452.
20. Nobaek S, Johansson ML, Molin G, Ahrne S, Jeppsson B. Alteration of intestinal microflora is associated with reduction in abdominal bloating and pain in patients with irritable bowel syndrome. Am J Gastroenterol. 2000;95:1231–1238.
21. Kamiya T, Wang L, Forsythe P, Goettsche G, Mao Y, Wang Y, et al. Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut. 2006;55:191–196.
22. Ait-Belgnaoui A, Han W, Lamine F, Eutamene H, Fioramonti J, Bueno L, et al. Lactobacillus farciminis treatment suppresses stress induced visceral hypersensitivity: a possible action through interaction with epithelial cell cytoskeleton contraction. Gut. 2006;55:1090–1094.
23. Verdu EF, Bercik P, Verma-Gandhu M, Huang XX, Blennerhassett P, Jackson W, et al. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut. 2006;55:182–190.
24. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214.
25. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65.
26. Li H, Li W, Liu X, Cao Y. gadA gene locus in Lactobacillus brevis NCL912 and its expression during fed-batch fermentation. FEMS Microbiol Lett. 2013;349:108–116.
27. Barrett E, Ross RP, O'Toole PW, Fitzgerald GF, Stanton C. gamma-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol. 2012;113:411–417.
28. Liu S, Zhao L, Ren F, Sun E, Zhang M, Guo H. Complete genome sequence of Bifidobacterium adolesentis BBMN23, a probiotic strain from healthy centenarian. J Biotechnol. 2015;198:44–45.
29. Wong CG, Bottiglieri T, Snead OC 3rd. GABA, gamma-hydroxybutyric acid, and neurological disease. Ann Neurol. 2003;54(Suppl 6):S3–S12.
30. Hyland NP, Cryan JF. A gut feeling about GABA: focus on GABA(B) receptors. Front Pharmacol. 2010;1:124.
31. Chen CY, Bonham AC. Postexercise hypotension: central mechanisms. Exerc Sport Sci Rev. 2010;38:122–127.
32. Jin Z, Mendu SK, Birnir B. GABA is an effective immunomodulatory molecule. Amino Acids. 2013;45:87–94.
33. Small PL, Waterman SR. Acid stress, anaerobiosis and gadCB: lessons from Lactococcus lactis and Escherichia coli. Trends Microbiol. 1998;6:214–216.
34. Su MS, Schlicht S, Ganzle MG. Contribution of glutamate decarboxylase in Lactobacillus reuteri to acid resistance and persistence in sourdough fermentation. Microb Cell Fact. 2011;10(Suppl 1):S8.
35. Sanders JW, Leenhouts K, Burghoorn J, Brands JR, Venema G, Kok J. A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol Microbiol. 1998;27:299–310.
36. Cotter PD, Gahan CG, Hill C. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol Microbiol. 2001;40:465–475.
37. Feehily C, Karatzas KA. Role of glutamate metabolism in bacterial responses towards acid and other stresses. J Appl Microbiol. 2013;114:11–24.
38. Sze PY. L-Glutamate decarboxylase. Adv Exp Med Biol. 1979;123:59–78.
39. De Man JC, Rogosa A, Sharpe ME. A medium for the cultivation of lactobacilli. J Appl Bacteriol. 1960;23:130–135.
40. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol. 2012;8:e1002358.
41. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Pillay M, et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 2014;42(Database issue):D560–D567.
42. Hollister EB, Riehle K, Luna RA, Weidler EM, Rubio-Gonzales M, Mistretta TA, et al. Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome. 2015;3:36.
43. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods. 2012;9:811–814.
44. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359.
45. Parks DH, Beiko RG. Identifying biologically relevant differences between metagenomic communities. Bioinformatics. 2010;26:715–721.
46. Koradi R, Billeter M, Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph. 1996;14:51–55, 29-32.
47. Shkoporov AN, Efimov BA, Khokhlova EV, Kafarskaia LI, Smeianov VV. Production of human basic fibroblast growth factor (FGF-2) in Bifidobacterium breve using a series of novel expression/secretion vectors. Biotechnol Lett. 2008;30:1983–1988.
48. Pokusaeva K, O'Connell-Motherway M, Zomer A, Fitzgerald GF, Van Sinderen D. Characterization of two novel alpha-glucosidases from Bifidobacterium breve UCC2003. Appl Environ Microbiol. 2009;75:1135–1143.
49. Hiraga K, Ueno Y, Oda K. Glutamate decarboxylase from Lactobacillus brevis: activation by ammonium sulfate. Biosci Biotechnol Biochem. 2008;72:1299–1306.
50. Maze A, O'Connell-Motherway M, Fitzgerald GF, Deutscher J, Van Sinderen D. Identification and characterization of a fructose phosphotransferase system in Bifidobacterium breve UCC2003. Appl Environ Microbiol. 2007;73:545–553.
51. Winston JH, Xu GY, Sarna SK. Adrenergic stimulation mediates visceral hypersensitivity to colorectal distension following heterotypic chronic stress. Gastroenterology. 2010;138:294–304 e3.
52. Kim S-H, Shin B-H, Kim Y-H, Nam S-W, Jeon S-J. Cloning and expression of a full-length glutamate decarboxylase gene from Lactobacillus brevis BH2. Biotechnol Bioprocess Eng. 2007;12:707–712.
53. O'Connell Motherway M, O'Driscoll J, Fitzgerald GF, Van Sinderen D. Overcoming the restriction barrier to plasmid transformation and targeted mutagenesis in Bifidobacterium breve UCC2003. Microb Biotechnol. 2009;2:321–332.
54. Heredia DJ, Grainger N, McCann CJ, Smith TK. Insights from a novel model of slow-transit constipation generated by partial outlet obstruction in the murine large intestine. Am J Physiol Gastrointest Liver Physiol. 2012;303:G1004–G1016.
55. Shi XZ, Lin YM, Powell DW, Sarna SK. Pathophysiology of motility dysfunction in bowel obstruction: role of stretch-induced COX-2. Am J Physiol Gastrointest Liver Physiol. 2011;300:G99–G108.
56. Xu GY, Shenoy M, Winston JH, Mittal S, Pasricha PJ. P2X receptor-mediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity. Gut. 2008;57:1230–1237.
57. Arbuckle RA, Carson RT, Abetz-Webb L, Hyams J, Di Lorenzo C, Lewis BE, et al. Measuring the symptoms of pediatric constipation and irritable bowel syndrome with constipation: expert commentary and literature review. Patient. 2014;7:343–364.
58. Tsai MF, McCarthy P, Miller C. Substrate selectivity in glutamate-dependent acid resistance in enteric bacteria. Proc Natl Acad Sci U S A. 2013;110:5898–5902.
59. Rhee SH, Keates AC, Moyer MP, Pothoulakis C. MEK is a key modulator for TLR5-induced interleukin-8 and MIP3alpha gene expression in non-transformed human colonic epithelial cells. J Biol Chem. 2004;279:25179–25188.
60. Rhee SH, Kim H, Moyer MP, Pothoulakis C. Role of MyD88 in phosphatidylinositol 3-kinase activation by flagellin/toll-like receptor 5 engagement in colonic epithelial cells. J Biol Chem. 2006;281:18560–18568.
61. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, et al. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS ONE. 2012;7:e31951.
62. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell. 2014;156:84–96.
63. Sobko T, Huang L, Midtvedt T, Norin E, Gustafsson LE, Norman M, et al. Generation of NO by probiotic bacteria in the gastrointestinal tract. Free Radic Biol Med. 2006;41:985–991.
64. Rey FE, Gonzalez MD, Cheng J, Wu M, Ahern PP, Gordon JI. Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc Natl Acad Sci U S A. 2013;110:13582–13587.
65. Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG. Minireview: gut microbiota: the neglected endocrine organ. Mol Endocrinol. 2014;28:1221–1238.
66. Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell. 2015;161:264–276.
67. Raghupathi R, Duffield MD, Zelkas L, Meedeniya A, Brookes SJ, Sia TC, et al. Identification of unique release kinetics of serotonin from guinea-pig and human enterochromaffin cells. J Physiol. 2013;591(Pt 23):5959–5975.
68. Freestone PP, Haigh RD, Lyte M. Specificity of catecholamine-induced growth in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica. FEMS Microbiol Lett. 2007;269:221–228.
69. Li Y, Xiang YY, Lu WY, Liu C, Li J. A novel role of intestine epithelial GABAergic signaling in regulating intestinal fluid secretion. Am J Physiol Gastrointest Liver Physiol. 2012;303:G453–G460.
70. Watanabe M, Maemura K, Kanbara K, Tamayama T, Hayasaki H. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol. 2002;213:1–47.
71. Auteri M, Zizzo MG, Mastropaolo M, Serio R. Opposite role played by GABAA and GABAB receptors in the modulation of peristaltic activity in mouse distal colon. Eur J Pharmacol. 2014;731:93–99.
72. Collares EF, Vinagre AM. Effect of baclofen on liquid and solid gastric emptying in rats. Arq Gastroenterol. 2010;47:290–296.
73. Beaumont H, Smout A, Aanen M, Rydholm H, Lei A, Lehmann A, et al. The GABA(B) receptor agonist AZD9343 inhibits transient lower oesophageal sphincter relaxations and acid reflux in healthy volunteers: a phase I study. Aliment Pharmacol Ther. 2009;30:937–946.
74. Huang D, Huang S, Peers C, Du X, Zhang H, Gamper N. GABAB receptors inhibit low-voltage activated and high-voltage activated Ca(2+) channels in sensory neurons via distinct mechanisms. Biochem Biophys Res Commun. 2015;465:188–193.
75. Hanack C, Moroni M, Lima WC, Wende H, Kirchner M, Adelfinger L, et al. GABA blocks pathological but not acute TRPV1 pain signals. Cell. 2015;160:759–770.
76. Matsumoto M, Kibe R, Ooga T, Aiba Y, Kurihara S, Sawaki E, et al. Impact of intestinal microbiota on intestinal luminal metabolome. Sci Rep. 2012;2:233.
77. Ponnusamy K, Choi JN, Kim J, Lee SY, Lee CH. Microbial community and metabolomic comparison of irritable bowel syndrome faeces. J Med Microbiol. 2011;60(Pt 6):817–827.
78. de Ruyter PG, Kuipers OP, de Vos WM. Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol. 1996;62:3662–3667.
79. Pokusaeva K, Neves AR, Zomer A, O'Connell Motherway M, MacSharry J, Curley P, et al. Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb Biotechnol. 2009;3:311–323.