Host-microbiota neuroendocrine interactions influencing brain and behavior

Gut Microbes

Volumn 5, Issue 3, 2014, Pages 381-389

  Lyte, Mark ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Behavior; Enteric nervous system; Hormones; Microbial endocrinology; Neuroendocrine; Signaling

Indexed keywords

4 AMINOBUTYRIC ACID; CATECHOLAMINE; DOPAMINE; NEUROTRANSMITTER; NORADRENALIN; OXIDOPAMINE; SEROTONIN; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ANTIBIOTIC THERAPY; ARTICLE; BEHAVIOR; BIFIDOBACTERIUM; CELL COMMUNICATION; COMMENSALISM; DIARRHEA; FEEDING BEHAVIOR; HEPATIC ENCEPHALOPATHY; HUMAN; INTESTINE FLORA; LACTOBACILLUS; METABOLOME; MOLECULAR RECOGNITION; NEUROENDOCRINE SYSTEM; NONHUMAN; PORPHYROMONADACEAE; PREVALENCE; RECEPTOR DOWN REGULATION; SEQUENCE ANALYSIS; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; MICROFLORA; PHYSIOLOGY;

ANIMALS; BEHAVIOR; BRAIN; HUMANS; METABOLIC PHENOMENA; MICROBIOTA; NEUROTRANSMITTER AGENTS;

EID: 84900836517     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.28682     Document Type: Article

References (71)

1. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res 2013; 69:52-60; PMID:23147033; http://dx.doi.org/10.1016/j.phrs.2012.10.020
2. Forsythe P, Sudo N, Dinan T, Taylor VH, Bienenstock J. Mood and gut feelings. Brain Behav Immun 2010; 24:9-16; PMID:19481599; http://dx.doi.org/10.1016/j.bbi.2009.05.058
3. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13:701-12; PMID:22968153; http://dx.doi.org/10.1038/nrn3346
4. Pflughoeft KJ, Versalovic J. Human microbiome in health and disease. Annu Rev Pathol 2012; 7:99-122; PMID:21910623; http://dx.doi.org/10.1146/annurev-pathol-011811-132421
5. Fraher MH, O'Toole PW, Quigley EM. Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol 2012; 9:312-22; PMID:22450307; http://dx.doi.org/10.1038/nrgastro.2012.44
6. Maurice CF, Haiser HJ, Turnbaugh PJ. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 2013; 152:39-50; PMID:23332745; http://dx.doi.org/10.1016/j.cell.2012.10.052
7. Lyte M, Freestone PPE. Microbial endocrinology: interkingdom signaling in infectious disease and health. New York: Springer, 2010.
8. Lyte M. Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol 2004; 12:14-20; PMID:14700547; http://dx.doi.org/10.1016/j.tim.2003.11.004
9. Obata K. Synaptic inhibition and γ-aminobutyric acid in the mammalian central nervous system. Proc Jpn Acad Ser B Phys Biol Sci 2013; 89:139-56; PMID:23574805; http://dx.doi.org/10.2183/pjab.89.139
10. Bjurstöm H, Wang J, Ericsson I, Bengtsson M, Liu Y, Kumar-Mendu S, Issazadeh-Navikas S, Birnir B. GABA, a natural immunomodulator of T lymphocytes. J Neuroimmunol 2008; 205:44-50; PMID:18954912; http://dx.doi.org/10.1016/j.jneuroim.2008.08.017
11. Barrett E, Ross RP, O'Toole PW, Fitzgerald GF, Stanton C. γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 2012; 113:411-7; PMID:22612585; http://dx.doi.org/10.1111/j.1365-2672.2012.05344.x
12. Roshchina VV. Evolutionary considerations of neurotransmitters in microbial, plant and animal cells. In: Lyte M, Freestone PP, eds. Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health. New York: Springer, 2010:17-52.
13. Tsavkelova EA, Botvinko IV, Kudrin VS, Oleskin AV. Detection of neurotransmitter amines in microorganisms with the use of high-performance liquid chromatography. Dokl Biochem 2000; 372:115-7; PMID:10935181
14. Asano Y, Hiramoto T, Nishino R, Aiba Y, Kimura T, Yoshihara K, Koga Y, Sudo N. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol 2012; 303:G1288-95; PMID:23064760; http://dx.doi.org/10.1152/ajpgi.00341.2012
15. Stephenson M, Rowatt E. The production of acetylcholine by a strain of Lactobacillus plantarum. J Gen Microbiol 1947; 1:279-98; PMID:20270627; http://dx.doi.org/10.1099/00221287-1-3-279
16. Devalia JL, Grady D, Harmanyeri Y, Tabaqchali S, Davies RJ. Histamine synthesis by respiratory tract micro-organisms: possible role in pathogenicity. J Clin Pathol 1989; 42:516-22; PMID:2499609; http://dx.doi.org/10.1136/jcp.42.5.516
17. Shahkolahi AM, Donahue MJ. Bacterial flora, a possible source of serotonin in the intestine of adult female Ascaris suum. J Parasitol 1993; 79:17-22; PMID:8437056; http://dx.doi.org/10.2307/3283271
18. Uzbay TI. The pharmacological importance of agmatine in the brain. Neurosci Biobehav Rev 2012; 36:502-19; PMID:21893093; http://dx.doi.org/10.1016/j.neubiorev.2011.08.006
19. Arena ME, Manca de Nadra MC. Biogenic amine production by Lactobacillus. J Appl Microbiol 2001; 90:158-62; PMID:11168717; http://dx.doi.org/10.1046/j.1365-2672.2001.01223.x
20. Gale EF. The production of amines by bacteria: The decarboxylation of amino-acids by strains of Bacterium coli. Biochem J 1940; 34:392-413; PMID:16747177
21. Iyer LM, Aravind L, Coon SL, Klein DC, Koonin EV. Evolution of cell-cell signaling in animals: did late horizontal gene transfer from bacteria have a role? Trends Genet 2004; 20:292-9; PMID:15219393; http://dx.doi.org/10.1016/j.tig.2004.05.007
22. Riley DR, Sieber KB, Robinson KM, White JR, Ganesan A, Nourbakhsh S, Dunning Hotopp JC. Bacteria-human somatic cell lateral gene transfer is enriched in cancer samples. PLoS Comput Biol 2013; 9:e1003107; PMID:23840181; http://dx.doi.org/10.1371/journal.pcbi.1003107
23. Lyte M. The microbial organ in the gut as a driver of homeostasis and disease. Med Hypotheses 2010; 74:634-8; PMID:19900764; http://dx.doi.org/10.1016/j.mehy.2009.10.025
24. Lenard J. Mammalian hormones in microbial cells. Trends Biochem Sci 1992; 17:147-50; PMID:1585458; http://dx.doi.org/10.1016/0968-0004(92)90323-2
25. Matsumoto M, Kibe R, Ooga T, Aiba Y, Kurihara S, Sawaki E, Koga Y, Benno Y. Impact of intestinal microbiota on intestinal luminal metabolome. Sci Rep 2012; 2:233; PMID:22724057; http://dx.doi.org/10.1038/srep00233
26. Martin FP, Dumas ME, Wang Y, Legido-Quigley C, Yap IK, Tang H, Zirah S, Murphy GM, Cloarec O, Lindon JC, et al. A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model. Mol Syst Biol 2007; 3:112; PMID:17515922; http://dx.doi.org/10.1038/msb4100153
27. Lyte M. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics. Bioessays 2011; 33:574-81; PMID:21732396; http://dx.doi.org/10.1002/bies.201100024
28. Breer H, Eberle J, Frick C, Haid D, Widmayer P. Gastrointestinal chemosensation: chemosensory cells in the alimentary tract. Histochem Cell Biol 2012; 138:13-24; PMID:22527698; http://dx.doi.org/10.1007/s00418-012-0954-z
29. Schafer DF, Fowler JM, Jones EA. Colonic bacteria: a source of gamma-aminobutyric acid in blood. Proc Soc Exp Biol Med 1981; 167:301-3; PMID:7019921; http://dx.doi.org/10.3181/00379727-167-41169
30. Minuk GY. Gamma-aminobutyric acid (GABA) production by eight common bacterial pathogens. Scand J Infect Dis 1986; 18:465-7; PMID:3775273; http://dx.doi.org/10.3109/00365548609032366
31. Balcar VJ. Presence of a highly efficient "binding" to bacterial contamination can distort data from binding studies. Neurochem Res 1990; 15:1237-8; PMID:1965858; http://dx.doi.org/10.1007/BF01208585
32. Guthrie GD, Nicholson-Guthrie CS. gamma-Aminobutyric acid uptake by a bacterial system with neurotransmitter binding characteristics. Proc Natl Acad Sci U S A 1989; 86:7378-81; PMID:2552441; http://dx.doi.org/10.1073/pnas.86.19.7378
33. LeRoith D, Roberts C Jr., Lesniak MA, Roth J. Receptors for intercellular messenger molecules in microbes: similarities to vertebrate receptors and possible implications for diseases in man. Experientia 1986; 42:782-8; PMID:3015665; http://dx.doi.org/10.1007/BF01941525
34. Roth J, LeRoith D, Shiloach J, Rosenzweig JL, Lesniak MA, Havrankova J. The evolutionary origins of hormones, neurotransmitters, and other extracellular chemical messengers: implications for mammalian biology. N Engl J Med 1982; 306:523-7; PMID:6120460; http://dx.doi.org/10.1056/NEJM198203043060907
35. Lyte M. The role of catecholamines in gram-negative sepsis. Med Hypotheses 1992; 37:255-8; PMID:1625603; http://dx.doi.org/10.1016/0306-9877(92)90197-K
36. Lyte M, Ernst S. Catecholamine induced growth of gram negative bacteria. Life Sci 1992; 50:203-12; PMID:1731173; http://dx.doi.org/10.1016/0024-3205(92)90273-R
37. Lyte M. Microbial Endocrinology: A Personal Journey. In: Lyte M, Freestone PPE, eds. Microbial endocrinology: interkingdom signaling in infectious disease and health. New York: Springer, 2010:1-16.
38. Pullinger GD, Carnell SC, Sharaff FF, van Diemen PM, Dziva F, Morgan E, Lyte M, Freestone PP, Stevens MP. Norepinephrine augments Salmonella enterica-induced enteritis in a manner associated with increased net replication but independent of the putative adrenergic sensor kinases QseC and QseE. Infect Immun 2010; 78:372-80; PMID:19884332; http://dx.doi.org/10.1128/IAI.01203-09
39. Bearson BL, Bearson SM, Uthe JJ, Dowd SE, Houghton JO, Lee I, Toscano MJ, Lay DC Jr. Iron regulated genes of Salmonella enterica serovar Typhimurium in response to norepinephrine and the requirement of fepDGC for norepinephrine-enhanced growth. Microbes Infect 2008; 10:807-16; PMID:18554972; http://dx.doi.org/10.1016/j.micinf.2008.04.011
40. Hegde M, Wood TK, Jayaraman A. The neuroendocrine hormone norepinephrine increases Pseudomonas aeruginosa PA14 virulence through the las quorum-sensing pathway. Appl Microbiol Biotechnol 2009; 84:763-76; PMID:19517106; http://dx.doi.org/10.1007/s00253-009-2045-1
41. Oneal MJ, Schafer ER, Madsen ML, Minion FC. Global transcriptional analysis of Mycoplasma hyopneumoniae following exposure to norepinephrine. Microbiology 2008; 154:2581-8; PMID:18757792; http://dx.doi.org/10.1099/mic.0.2008/020230-0
42. Peterson G, Kumar A, Gart E, Narayanan S. Catecholamines increase conjugative gene transfer between enteric bacteria. Microb Pathog 2011; 51:1-8; PMID:21419838; http://dx.doi.org/10.1016/j.micpath.2011.03.002
43. Lyte M, Gaykema R, Goehler L. Behavior modification of host by microbes. In: Schaechter M, ed. Encyclopedia of Microbiology. Oxford: Elsevier, 2009:121-7.
44. Udenfriend S, Lovenberg W, Sjoerdsma A. Physiologically active amines in common fruits and vegetables. Arch Biochem Biophys 1959; 85:487-90; PMID:13840159; http://dx.doi.org/10.1016/0003-9861(59)90516-8
45. Von Roepenack-Lahaye E, Newman MA, Schornack S, Hammond-Kosack KE, Lahaye T, Jones JD, Daniels MJ, Dow JM. p-Coumaroylnoradrenaline, a novel plant metabolite implicated in tomato defense against pathogens. J Biol Chem 2003; 278:43373-83; PMID:12900412; http://dx.doi.org/10.1074/jbc.M305084200
46. Pitman RM. Transmitter substances in insects: a review. Comp Gen Pharmacol 1971; 2:347-71; PMID:4353991; http://dx.doi.org/10.1016/0010-4035(71)90060-7
47. Guerrero HY, Caceres G, Paiva CL, Marcano D. Hypothalamic and telencephalic catecholamine content in the brain of the teleost fish, Pygocentrus notatus, during the annual reproductive cycle. Gen Comp Endocrinol 1990; 80:257-63; PMID:2074003; http://dx.doi.org/10.1016/0016-6480(90)90170-Q
48. Moreira CG, Weinshenker D, Sperandio V. QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo. Infect Immun 2010; 78:914-26; PMID:20028809; http://dx.doi.org/10.1128/IAI.01038-09
49. Methner U, Rabsch W, Reissbrodt R, Williams PH. Effect of norepinephrine on colonisation and systemic spread of Salmonella enterica in infected animals: role of catecholate siderophore precursors and degradation products. Int J Med Microbiol 2008; 298:429-39; PMID:17888732; http://dx.doi.org/10.1016/j.ijmm.2007.07.013
50. Reissbrodt R, Rienaecker I, Romanova JM, Freestone PP, Haigh RD, Lyte M, Tschäpe H, Williams PH. Resuscitation of Salmonella enterica serovar typhimurium and enterohemorrhagic Escherichia coli from the viable but nonculturable state by heat-stable enterobacterial autoinducer. Appl Environ Microbiol 2002; 68:4788-94; PMID:12324321; http://dx.doi.org/10.1128/AEM.68.10.4788-4794.2002
51. Anderson MT, Armstrong SK. Norepinephrine mediates acquisition of transferrin-iron in Bordetella bronchiseptica. J Bacteriol 2008; 190:3940-7; PMID:18390651; http://dx.doi.org/10.1128/JB.00086-08
52. Lyte M, Freestone PP, Neal CP, Olson BA, Haigh RD, Bayston R, Williams PH. Stimulation of Staphylococcus epidermidis growth and biofilm formation by catecholamine inotropes. Lancet 2003; 361:130-5; PMID:12531580; http://dx.doi.org/10.1016/S0140-6736(03)12231-3
53. Le Roith D, Shiloach J, Berelowitz M, Frohman LA, Liotta AS, Krieger DT, Roth J. Are messenger molecules in microbes the ancestors of the vertebrate hormones and tissue factors? Fed Proc 1983; 42:2602-7; PMID:6133783
54. LeRoith D. Vertebrate hormones and neuropeptides in microbes: evolutionary origin of intercellular communication. In: Martini L, Ganong WF, eds. Front Neuroendocrinol. New York: Raven Press, 1984:1-25.
55. Lyte M, Bailey MT. Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. J Surg Res 1997; 70:195-201; PMID:9245571; http://dx.doi.org/10.1006/jsre.1997.5130
56. Lyte M, Bailey MT. Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. J Surg Res 1997; 70:195-201; PMID:9245571; http://dx.doi.org/10.1006/jsre.1997.5130
57. Freestone PP, Haigh RD, Williams PH, Lyte M. Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers. FEMS Microbiol Lett 1999; 172:53-60; PMID:10079527; http://dx.doi.org/10.1111/j.1574-6968.1999.tb13449.x
58. Vlisidou I, Lyte M, van Diemen PM, Hawes P, Monaghan P, Wallis TS, Stevens MP. The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157:H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infect Immun 2004; 72:5446-51; PMID:15322043; http://dx.doi.org/10.1128/IAI.72.9.5446-5451.2004
59. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 2010; 78:1509-19; PMID:20145094; http://dx.doi.org/10.1128/IAI.00862-09
60. Ko CY, Lin HTV, Tsai GJ. Gamma-aminobutyric acid production in black soybean milk by Lactobacillus brevis FPA 3709 and the antidepressant effect of the fermented product on a forced swimming rat model. Process Biochem 2013; 48:559-68; http://dx.doi.org/10.1016/j.procbio.2013.02.021
61. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. 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; 108:16050-5; PMID:21876150; http://dx.doi.org/10.1073/pnas.1102999108
62. Irwin MR, Rothermundt M. Clinical psychoneuroimmunology. Handb Clin Neurol 2012; 106:211-25; PMID:22608623; http://dx.doi.org/10.1016/B978-0-444-52002-9.00012-7
63. Smith TA. The occurrence, metabolism and functions of amines in plants. Biol Rev Camb Philos Soc 1971; 46:201-41; PMID:4942955; http://dx.doi.org/10.1111/j.1469-185X.1971.tb01182.x
64. Kuklin AI, Conger BV. CATECHOLAMINES IN PLANTS. J Plant Growth Regul 1995; 14:91-7; http://dx.doi.org/10.1007/BF00203119
65. Vijayakumari K, Siddhuraju P, Janardhanan K. Effect of different post-harvest treatments on antinutritional factors in seeds of the tribal pulse, Mucuna pruriens (L.) DC. Int J Food Sci Nutr 1996; 47:263-72; PMID:8735780; http://dx.doi.org/10.3109/09637489609012587
66. Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol Behav 2009; 96:557-67; PMID:19135464; http://dx.doi.org/10.1016/j.physbeh.2008.12.004
67. Furness JB. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 2012; 9:286-94; PMID:22392290; http://dx.doi.org/10.1038/nrgastro.2012.32
68. Wood JD. Enteric neuroimmunophysiology and pathophysiology. Gastroenterology 2004; 127:635-57; PMID:15300595; http://dx.doi.org/10.1053/j.gastro.2004.02.017
69. McFarland LV. Antibiotic-associated diarrhea: epidemiology, trends and treatment. Future Microbiol 2008; 3:563-78; PMID:18811240; http://dx.doi.org/10.2217/17460913.3.5.563
70. Rupnik M, Wilcox MH, Gerding DN. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 2009; 7:526-36; PMID:19528959; http://dx.doi.org/10.1038/nrmicro2164
71. Norris V, Molina F, Gewirtz AT. Hypothesis: bacteria control host appetites. J Bacteriol 2013; 195:411-6; PMID:23144247; http://dx.doi.org/10.1128/JB.01384-12