Magnetic resonance spectroscopy reveals oral Lactobacillus promotion of increases in brain GABA, N-acetyl aspartate and glutamate

NeuroImage

Volumn 125, Issue , 2016, Pages 988-995

  Janik, Rafal ^a   Thomason, Lynsie A M ^b   Stanisz, Andrew M ^c   Forsythe, Paul ^c   Bienenstock, John ^c   Stanisz, Greg J ^a,b,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b Institute of Clinical Evaluative Sciences   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d MEDICAL UNIVERSITY OF LUBLIN   (Poland)

Author keywords

GABA; Glutamate; Magnetic resonance spectroscopy; Microbiome; NAA; Neurotransmitters

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; GLUTAMIC ACID; N ACETYLASPARTIC ACID; ASPARTIC ACID; N-ACETYLASPARTATE; PROBIOTIC AGENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BACTERIAL STRAIN; BRAIN FUNCTION; BRAIN LEVEL; BRAIN SIZE; BREATHING RATE; COLONY FORMING UNIT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; IMAGE ANALYSIS; LACTOBACILLUS RHAMNOSUS; MALE; MOUSE; NEUROTRANSMISSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXYGEN SATURATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PULSE RATE; SIGNAL NOISE RATIO; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BRAIN; BRAIN CHEMISTRY; DRUG EFFECTS; INTESTINE FLORA; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY;

ANIMALS; ASPARTIC ACID; BRAIN; BRAIN CHEMISTRY; ENZYME-LINKED IMMUNOSORBENT ASSAY; GAMMA-AMINOBUTYRIC ACID; GASTROINTESTINAL MICROBIOME; GLUTAMIC ACID; LACTOBACILLUS RHAMNOSUS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, INBRED BALB C; PROBIOTICS;

EID: 84947553551     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.11.018     Document Type: Article

References (59)

1. Adalsteinsson E., Sullivan E.V., Kleinhans N., Spielman D.M., Pfefferbaum A. Longitudinal decline of the neuronal marker N-acetyl aspartate in Alzheimer's disease. Lancet 2000, 355(9216):1696-1697. [Letter].
2. Ahlroos T., Tynkkynen S. Quantitative strain-specific detection of Lactobacillus rhamnosus GG in human faecal samples by real-time PCR. J. Appl. Microbiol. 2009, 106(2):506-514. 10.1111/j.1365-2672.2008.04018.x.
3. Alander M., Satokari R., Korpela R., Saxelin M., Vilpponen-Salmela T., Mattila-Sandholm T., von Wright A. Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl. Environ. Microbiol. 1999, 65(1):351-354.
4. Baslow M.H. N-acetylaspartate in the vertebrate brain: metabolism and function. Neurochem. Res. 2003, 28(6):941-953. [Review].
5. 1H NMR spectroscopy. NMR Biomed. 2002, 15(1):37-44. 10.1002/nbm.740.
6. Benton D., Williams C., Brown A. Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur. J. Clin. Nutr. 2007, 61(3):355-361. 10.1038/sj.ejcn.1602546.
7. Bercik P., Denou E., Collins J., Jackson W., Lu J., Jury J., Collins S.M. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 2011, 141(2). (599-U701). 10.1053/j.gastro.2011.04.052.
8. Bock N.A., Hashim E., Janik R., Konyer N.B., Weiss M., Stanisz G.J., Geyer S. Optimizing T1-weighted imaging of cortical myelin content at 3.0T. NeuroImage 2013, 65:1-12. 10.1016/j.neuroimage.2012.09.051.
9. Bottomley P.A. Spatial localization in NMR spectroscopy in vivo. Ann. N. Y. Acad. Sci. 1987, 508:333-348. [Review].
10. Braniste V., Al-Asmakh M., Kowal C., Anuar F., Abbaspour A., Toth M., Pettersson S. The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl. Med. 2014, 6(263). 10.1126/scitranslmed.3009759.
11. Bravo J.A., Forsythe P., Chew M.V., Escaravage E., Savignac H.M., Dinan T.G., Cryan J.F. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. 2011, 108(38):16050-16055. 10.1073/pnas.1102999108/-/DCSupplemental.
12. Chavez S., Stanisz G.J. A novel method for simultaneous 3D B1 and T1 mapping: the method of slopes (MoS). NMR Biomed. 2012, 25(9):1043-1055. 10.1002/nbm.2769.
13. Chung H., Kasper D.L. Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr. Opin. Immunol. 2010, 22(4):455-460. 10.1016/j.coi.2010.06.008.
14. Collins S.M., Surette M., Bercik P. The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 2012, 10(11):735-742. 10.1038/nrmicro2876.
15. Cryan J.F., Dinan T.G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012, 13(10):701-712. 10.1038/nrn3346.
16. Cryan J.F., O'Mahony S.M. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol. Motil. 2011, 23(3):187-192. 10.1111/j.1365-2982.2010.01664.x.
17. de Graaf R.A., Brown P.B., McIntyre S., Nixon T.W., Behar K.L., Rothman D.L. High magnetic field water and metabolite proton T-1 and T-2 relaxation in rat brain in vivo. Magn. Reson. Med. 2006, 56(2):386-394. 10.1002/mrm.20946.
18. De Vadder F., Kovatcheva-Datchary P., Goncalves D., Vinera J., Zitoun C., Duchampt A., Mithieux G. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 2014, 156(1-2):84-96. 10.1016/j.cell.2013.12.016.
19. de Vos W.M., de Vos E.A.J. Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr. Rev. 2012, 70:S45-S56. 10.1111/j.1753-4887.2012.00505.x.
20. Demougeot C., Garnier P., Mossiat C., Bertrand N., Giroud M., Beley A., Marie C. N-acetylaspartate, a marker of both cellular dysfunction and neuronal loss: its relevance to studies of acute brain injury. J. Neurochem. 2001, 77(2):408-415.
21. Diaz Heijtz R., Wang S., Anuar F., Qian Y., Bjorkholm B., Samuelsson A., Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(7):3047-3052. 10.1073/pnas.1010529108.
22. Dinan T.G., Stanton C., Cryan J.F. Psychobiotics: a novel class of psychotropic. Biol. Psychiatry 2013, 74(10):720-726. 10.1016/j.biopsych.2013.05.001.
23. Forsythe P., Kunze W.A. Voices from within: gut microbes and the CNS. Cell. Mol. Life Sci. 2013, 70(1):55-69. 10.1007/s00018-012-1028-z.
24. Forsythe P., Sudo N., Dinan T., Taylor V.H., Bienenstock J. Mood and gut feelings. Brain Behav. Immun. 2010, 24(1):9-16. 10.1016/j.bbi.2009.05.058.
25. Foster J.A., Neufeld K.-A.M. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013, 36(5):305-312. 10.1016/j.tins.2013.01.005.
26. Frazer A., Benmansour S. Delayed pharmacological effects of antidepressants. Mol. Psychiatry 2002, 7:S23-S28. 10.1038/sj.mp.4001015.
27. Friedman S.D., Brooks W.M., Jung R.E., Chiulli S.J., Sloan J.H., Montoya B.T., Yeo R.A. Quantitative proton MRS predicts outcome after traumatic brain injury. Neurology 1999, 52(7):1384-1391.
28. Gerner R.H., Hare T.A. CSF-GABA in normnal subjects and patients with depression, schizophrenia, mania and anorexia-nervosa. Am. J. Psychiatr. 1981, 138(8):1098-1101.
29. Gideon P., Henriksen O., Sperling B., Christiansen P., Olsen T.S., Jørgensen H.S., Arlien-Søborg P. Early time course of N-acetylaspartate, creatine and phosphocreatine, and compounds containing choline in the brain after acute stroke. A proton magnetic resonance spectroscopy study. Stroke 1992, 23(11):1566-1572.
30. Gilbert J.A., Jansson J.K., Knight R. The Earth Microbiome project: successes and aspirations. BMC Biol. 2014, 12. 10.1186/s12915-014-0069-1.
31. Groves D.A., Brown V.J. Vagal nerve stimulation: a review of its applications and potential mechanisms that mediate its clinical effects. Neurosci. Biobehav. Rev. 2005, 29(3):493-500. 10.1016/j.neubiorev.2005.01.004.
32. Hasler G., van der Veen J.W., Tumonis T., Meyers N., Shen J., Drevets W.C. Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Arch. Gen. Psychiatry 2007, 64(2):193-200. 10.1001/archpsyc.64.2.193.
33. Kuriyama K., Sze P.Y. Blood-brain barrier to H-3-gamma-aminobutyric acid in normal and amino oxyacetic acid-treated animals. Neuropharmacology 1971, 10(1):103-&. 10.1016/0028-3908(71)90013-x.
34. Li B.S.Y., Wang H., Gonen O. Metabolite ratios to assumed stable creatine level may confound the quantification of proton brain MR spectroscopy. Magn. Reson. Imaging 2003, 21(8):923-928. 10.1016/s0730-725x(03)00181-4.
35. Luykx J.J., Laban K.G., van den Heuvel M.P., Boks M.P.M., Mandl R.C.W., Kahn R.S., Bakker S.C. Region and state specific glutamate downregulation in major depressive disorder: a meta-analysis of H-1-MRS findings. Neurosci. Biobehav. Rev. 2012, 36(1):198-205. 10.1016/j.neubiorev.2011.05.014.
36. Mao Y.-K., Kasper D.L., Wang B., Forsythe P., Bienenstock J., Kunze W.A. Bacteroides fragilis polysaccharide A is necessary and sufficient for acute activation of intestinal sensory neurons. Nat. Commun. 2013, 4. 10.1038/ncomms2478.
37. Mayer E.A., Knight R., Mazmanian S.K., Cryan J.F., Tillisch K. Gut microbes and the brain: paradigm shift in neuroscience. J. Neurosci. 2014, 34(46):15490-15496. 10.1523/jneurosci.3299-14.2014.
38. Mohler H. The GABA system in anxiety and depression and its therapeutic potential. Neuropharmacology 2012, 62(1):42-53. 10.1016/j.neuropharm.2011.08.040.
39. Mugler J.P., Brookeman J.R. Three-dimensional magnetization-prepared rapid gradient-echo imaging (3D MP RAGE). Magn. Reson. Med. 1990, 15(1):152-157.
40. Oberg J., Spenger C., Wang F.-H., Andersson A., Westman E., Skoglund P., Lindberg M. Age related changes in brain metabolites observed by H-1 MRS in APP/PS1 mice. Neurobiol. Aging 2008, 29(9):1423-1433. 10.1016/j.neurobiolaging.2007.03.002.
41. O'Hara A.M., Shanahan F. The gut flora as a forgotten organ. Embo Rep. 2006, 7(7):688-693. 10.1038/sj.embor.7400731.
42. Perez-Burgos A., Wang B., Mao Y.-K., Mistry B., Neufeld K.-A.M., Bienenstock J., Kunze W. Psychoactive bacteria Lactobacillus rhamnosus (JB-1) elicits rapid frequency facilitation in vagal afferents. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304(2):G211-G220. 10.1152/ajpgi.00128.2012.
43. Pinheiro J.C., Bates D.M. Unconstrained parametrizations for variance-covariance matrices. Stat. Comput. 1996, 6(3):289-296. 10.1007/bf00140873.
44. Pinheiro J.C., Bates D.M., Lindstrom M.J., Amer Stat A. Model Building in Nonlinear Mixed Effects Models 1994.
45. Rakoff-Nahoum S., Kong Y., Kleinstein S.H., Subramanian S., Ahern P.P., Gordon J.I., Medzhitov R. Analysis of gene-environment interactions in postnatal development of the mammalian intestine. Proc. Natl. Acad. Sci. U. S. A. 2015, 112(7):1929-1936. 10.1073/pnas.1424886112.
46. Scheperjans F., Aho V., Pereira P.A.B., Koskinen K., Paulin L., Pekkonen E., Auvinen P. Gut microbiota are associated with Parkinson's disease and clinical phenotype-a case-control study. J. Neurol. 2014, 261:S488-S488.
47. Schirmer T., Auer D.P. On the reliability of quantitative clinical magnetic resonance spectroscopy of the human brain. NMR Biomed. 2000, 13(1):28-36. 10.1002/(sici)1099-1492(200002)13:1<28::aid-nbm606>3.0.co;2-l.
48. Schwarcz A., Natt O., Watanabe T., Boretius S., Frahm J., Michaelis T. Localized proton MRS of cerebral metabolite profiles in different mouse strains. Magn. Reson. Med. 2003, 49(5):822-827. 10.1002/mrm.10445.
49. Simister R.J., Woermann F.G., McLean M.A., Bartlett P.A., Barker G.J., Duncan J.S. A short-echo-time proton magnetic resonance spectroscopic imaging study of temporal lobe epilepsy. Epilepsia 2002, 43(9):1021-1031. 10.1046/j.1528-1157.2002.50701.x.
50. Smith S.A., Levante T.O., Meier B.H., Ernst R.R. Computer simulations in magnetic resonance. An object-oriented programming approach. J. Magn. Reson. Ser. A 1994, 106(1):75-105.
51. Sudo N., Chida Y., Aiba Y., Sonoda J., Oyama N., Yu X.N., Koga Y. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. Lond. 2004, 558(1):263-275. 10.1113/jphysiol.2004.063388.
52. Tkác I., Starcuk Z., Choi I.Y., Gruetter R. In vivo 1H NMR spectroscopy of rat brain at 1ms echo time. Magn. Reson. Med. 1999, 41(4):649-656.
53. Tkác I., Henry P.-G., Andersen P., Keene C.D., Low W.C., Gruetter R. Highly resolved in vivo 1H NMR spectroscopy of the mouse brain at 9.4T. Magn. Reson. Med. 2004, 52(3):478-484. 10.1002/mrm.20184.
54. Walter J., Ley R. The human gut microbiome: ecology and recent evolutionary changes. Annu. Rev. Microbiol. 2011, 65(65):411-429. 10.1146/annurev-micro-090110-102830.
55. Wang B., Mao Y.-K., Diorio C., Pasyk M., Wu R.Y., Bienenstock J., Kunze W.A. Luminal administration ex vivo of a live Lactobacillus species moderates mouse jejunal motility within minutes. FASEB J. 2010, 24(10):4078-4088. 10.1096/fj.09-153841.
56. Wilson M., Reynolds G., Kauppinen R.A., Arvanitis T.N., Peet A.C. A constrained least-squares approach to the automated quantitation of in vivo 1H magnetic resonance spectroscopy data. Magn. Reson. Med. 2010, 65(1):1-12. 10.1002/mrm.22579.
57. Winsberg M.E., Sachs N., Tate D.L., Adalsteinsson E., Spielman D., Ketter T.A. Decreased dorsolateral prefrontal N-acetyl aspartate in bipolar disorder. Biol. Psychiatry 2000, 47(6):475-481.
58. Xin L., Gambarota G., Mlynarik V., Gruetter R. Proton T-2 relaxation time of J-coupled cerebral metabolites in rat brain at 9.4T. NMR Biomed. 2008, 21(4):396-401. 10.1002/nbm.1205.
59. Zilber-Rosenberg I., Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 2008, 32(5):723-735. 10.1111/j.1574-6976.2008.00123.x.