Dietary magnesium deficiency alters gut microbiota and leads to depressive-like behaviour

Acta Neuropsychiatrica

Volumn 27, Issue 3, 2015, Pages 168-176

  Winther, Gudrun ^a   Pyndt Jørgensen, Betina M ^b   Elfving, Betina ^a   Nielsen, Denis Sandris ^b   Kihl, Pernille ^b   Lund, Sten ^c   Sorensen, Dorte Bratbo ^b   Wegener, Gregers ^a,d  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

^d NORTH WEST UNIVERSITY   (South Africa)

Author keywords

animal models; behaviour; depression; gut microbiota; magnesium deficiency

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; INTERLEUKIN 6; AUTACOID; IL6 PROTEIN, HUMAN; MAGNESIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN; CONTROLLED STUDY; DEPRESSION; FORCED SWIM TEST; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; HIPPOCAMPUS; HUMAN; INTESTINE FLORA; MAGNESIUM DEFICIENCY; MAGNESIUM INTAKE; MALE; MOUSE; NONHUMAN; OPEN FIELD TEST; REAL TIME POLYMERASE CHAIN REACTION; ADVERSE EFFECTS; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; DIET; DIET THERAPY; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSION; DIET; DISEASE MODELS, ANIMAL; GASTROINTESTINAL MICROBIOME; GLUCOSE TOLERANCE TEST; HIPPOCAMPUS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; MAGNESIUM; MAGNESIUM DEFICIENCY; MALE; MICE; MICE, INBRED C57BL; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84929276065     PISSN: 09242708     EISSN: 16015215     Source Type: Journal    
DOI: 10.1017/neu.2015.7     Document Type: Article

References (58)

1. GRUBBS RD, MAGUIRE ME. Magnesium as a regulatory cation: criteria and evaluation. Magnesium 1987; 6:113-127.
2. SARIS NE, MERVAALA E, KARPPANEN H, KHAWAJA JA, LEWENSTAM A. Magnesium. An update on physiological, clinical and analytical aspects. Clin Chim Acta 2000;294:1-26.
3. WOLF FI, TRAPANI V, CITTADINI A. Magnesium and the control of cell proliferation: looking for a needle in a haystack. Magnes Res 2008;21:83-91.
4. BARBAGALLO M, DOMINGUEZ LJ. Magnesium and aging. Curr Pharm Des 2010;16:832-839.
5. RYAN MF. The role of magnesium in clinical biochemistry: an overview. Ann Clin Biochem 1991;28(Pt 1):19-26.
6. KOENIG JH, IKEDA K. Synaptic vesicles have two distinct recycling pathways. J Cell Biol 1996;135 :797-808.
7. ZARATE CA, JR., DU J, QUIROZ J et al. Regulation of cellular plasticity cascades in the pathophysiology and treatment of mood disorders: role of the glutamatergic system. Ann N Y Acad Sci 2003;1003:273-291.
8. MURCK H. Magnesium and affective disorders. Nutr Neurosci 2002;5:375-389.
9. RASMUSSEN HH, MORTENSEN PB, JENSEN IW. Depression and magnesium deficiency. Int J Psychiatry Med 1989;19:57-63.
10. LEVINE J, STEIN D, RAPOPORT A, KURTZMAN L. High serum and cerebrospinal fluid Ca/Mg ratio in recently hospitalized acutely depressed patients. Neuropsychobiology 1999;39: 63-70.
11. COX IM, CAMPBELL MJ, DOWSON D. Red blood cell magnesium and chronic fatigue syndrome. Lancet 1991;337:757-760.
12. BARRAGAN-RODRIGUEZ L, RODRIGUEZ-MORAN M, GUERRERO-ROMERO F. Efficacy and safety of oral magnesium supplementation in the treatment of depression in the elderly with type 2 diabetes: a randomized, equivalent trial. Magnes Res 2008;21:218-223.
13. CHAUDHARY DP, SHARMA R, BANSAL DD. Implications of magnesium deficiency in type 2 diabetes: a review. Biol Trace Elem Res 2010;134:119-129.
14. CELIK N, ANDIRAN. N, YILMAZ AE. The relationship between serum magnesium levels with childhood obesity and insulin resistance: a review of the literature. J Pediatr Endocrinol Metab 2011;24:675-678.
15. GARFINKEL D, GARFINKEL L. Magnesium and regulation of carbohydrate metabolism at the molecular level. Magnesium 1988;7:249-261.
16. SUAREZ A, PULIDO N, CASLA A, CASANOVA B, ARRIETA FJ, ROVIRA A. Impaired tyrosine-kinase activity of muscle insulin receptors from hypomagnesaemic rats. Diabetologia 1995;38:1262-1270.
17. NADLER JL, BUCHANAN T, NATARAJAN R, ANTONIPILLAI I, BERGMAN R, RUDE R. Magnesium deficiency produces insulin resistance and increased thromboxane synthesis. Hypertension 1993;21:1024-1029.
18. PAOLISSO G, SGAMBATO S, GIUGLIANO D et al. Impaired insulin-induced erythrocyte magnesium accumulation is correlated to impaired insulin-mediated glucose disposal in type 2 (non-insulin-dependent) diabetic patients. Diabetologia 1988;31:910-915.
19. WEGLICKI WB, PHILLIPS TM, FREEDMAN AM, CASSIDY MM, DICKENS BF. Magnesium-de ficiency elevates circulating levels of inflammatory cytokines and endothelin. Mol Cell Biochem 1992;110:169-173.
20. PACHIKIAN BD, NEYRINCK AM, DELDICQUE L et al. Changes in intestinal bifidobacteria levels are associated with the inflammatory response in magnesium-deficient mice. J Nutr 2010;140:509-514.
21. COLLINS SM, KASSAM Z, BERCIK P. The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications. Curr Opin Microbiol 2013;16:240-245.
22. BANGSGAARD BENDTSEN KM, KRYCH L, SORENSEN DB et al. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PloS One 2012;7:e46231.
23. CRYAN JF, DINAN TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012;13:701-712.
24. CRYAN JF, O'MAHONY SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 2011;23:187-192.
25. JOHNSON S. The multifaceted and widespread pathology of magnesium deficiency. Med Hypotheses 2001;56:163-170.
26. KANTAK KM. Magnesium deficiency alters aggressive behavior and catecholamine function. Behav Neurosci 1988;102:304-311.
27. SINGEWALD N, SINNER C, HETZENAUER A, SARTORI SB, MURCK H. Magnesium-deficient diet alters depression- and anxietyrelated behavior in mice -influence of desipramine and Hypericum perforatum extract. Neuropharmacology 2004;47:1189-1197.
28. PORSOLT RD, LE PICHON M, JALFRE M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977;266:730-732.
29. PYNDT JBHJ, KRYCH L, LARSEN C et al. A possible link between food and mood: dietary impact on gut microbiota and behavior in balb/c mice. PloS One 2014;9:1-15.
30. ELFVING B, BONEFELD BE, ROSENBERG R, WEGENER G. Differential expression of synaptic vesicle proteins after repeated electroconvulsive seizures in rat frontal cortex and hippocampus. Synapse 2008;62:662-670.
31. ANDERSEN CL, JENSEN JL, ORNTOFT TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004;64:5245-5250.
32. LUNDBERG R, CLAUSEN SK, PANG W et al. Gastrointestinal microbiota and local inflammation during oxazolone-induced dermatitis in BALB/cA mice. Comp Med 2012;62:371-380.
33. MUYZER G, SMALLA K. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 1998;73:127-141.
34. DECOLLOGNE S, TOMAS A, LECERF C, ADAMOWICZ E, SEMAN M. NMDA receptor complex blockade by oral administration of magnesium: comparison with MK-801. Pharmacol, Biochem Behav 1997;58:261-268.
35. POLESZAK E, SZEWCZYK B, K'DZIERSKA E, WLAZ P, PILC A, NOWAK G. Antidepressant- and anxiolytic-like activity of magnesium in mice. Pharmacol Biochem Behav 2004;78: 7-12.
36. EBY GA, EBY KL. Rapid recovery from major depression using magnesium treatment. Med Hypotheses 2006;67: 362-370.
37. 2+ dependence of membrane resistance increases evoked by NMDA in hippocampal neurones. Brain Res 1984;311:392-396.
38. ENNIS M, ASTON-JONES G, SHIEKHATTAR R. Activation of locus coeruleus neurons by nucleus paragigantocellularis or noxious sensory stimulation is mediated by intracoerulear excitatory amino acid neurotransmission. Brain Res 1992;598:185-195.
39. SHIEKHATTAR R, ASTON-JONES G. NMDA-receptor-mediated sensory responses of brain noradrenergic neurons are suppressed by in vivo concentrations of extracellular magnesium. Synapse 1992;10:103-109.
40. WHITTLE N, LI L, CHEN WQ et al. Changes in brain protein expression are linked to magnesium restriction-induced depression-like behavior. Amino Acids 2011;40:1231-1248.
41. TIZABI Y, BHATTI BH, MANAYE KF, DAS JR, AKINFIRESOYE L. Antidepressant-like effects of low ketamine dose is associated with increased hippocampal AMPA/NMDA receptor density ratio in female wistar-kyoto rats. Neuroscience 2012;72-80.
42. SARTORI SB, WHITTLE N, HETZENAUER A, SINGEWALD N. Magnesium deficiency induces anxiety and HPA axis dysregulation: modulation by therapeutic drug treatment. Neuropharmacology 2012;62:304-312.
43. POLESZAK E, SZEWCZYK B, KEDZIERSKA E, WLAZ P, PILC A, NOWAK G. Antidepressant- and anxiolytic-like activity of magnesium in mice. Pharmacol, Biochem Behav 2004; 78:7-12.
44. BOADLE-BIBER MC. Activation of tryptophan hydroxylase from central serotonergic neurons by calcium and depolarization. Biochem Pharmacol 1978;27:1069-1079.
45. CAO BJ, PENG NA. Magnesium valproate attenuates hyperactivity induced by dexamphetamine-chlordiazepoxide mixture in rodents. Eur J Pharmacol 1993;237:177-181.
46. DJURHUUS MS, KLITGAARD NA, BECK-NIELSEN H. Magnesium deficiency and development of late diabetic complications. Ugeskr Laeger 1991;153:2108-2110.
47. TURNBAUGH PJ, LEY RE, MAHOWALD MA, MAGRINI V, MARDIS ER, GORDON JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006;444:1027-1031.
48. O'MAHONY SM, MARCHESI JR, SCULLY P et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009;65:263-267.
49. COLLINS S, VERDU E, DENOU E, BERCIK P. The role of pathogenic microbes and commensal bacteria in irritable bowel syndrome. Dig Dis 2009;27 (Suppl. 1):85-89.
50. DESBONNET L, GARRETT L, CLARKE G, KIELY B, CRYAN JF, DINAN TG. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010;170:1179-1188.
51. CRYAN JF, MARKOU A, LUCKI I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002;23:238-245.
52. PETIT-DEMOULIERE B, CHENU F, BOURIN M. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacol (Berl) 2005;177:245-255.
53. WU TH, LIN CH. IL-6 mediated alterations on immobile behavior of rats in the forced swim test via ERK1/2 activation in specific brain regions. Behav Brain Res 2008;193:183-191.
54. BATICIC L, DETEL D, KUCIC N, BULJEVIC S, PUGEL EP, VARLJEN J. Neuroimmunomodulative properties of dipeptidyl peptidase IV/CD26 in a TNBS-induced model of colitis in mice. J Cell Biochem 2011;112:3322-3333.
55. KANARIK M, ALTTOA A, MATROV D et al. Brain responses to chronic social defeat stress: effects on regional oxidative metabolism as a function of a hedonic trait, and gene expression in susceptible and resilient rats. Eur Neuropsychopharmacol 2011;21:92-107.
56. IOSIFESCU DV, BOLO NR, NIERENBERG AA, JENSEN JE, FAVA M, RENSHAW PF. Brain bioenergetics and response to triiodothyronine augmentation in major depressive disorder. Biol Psychiatry 2008;63:1127-1134.
57. MOLES KW, MCMULLEN JK. Insulin resistance and hypomagnesaemia: case report. Br Med J (Clin Res Ed) 1982; 285(6337):262.
58. KANDEEL FR, BALON E, SCOTT S, NADLER JL. Magnesium deficiency and glucose metabolism in rat adipocytes. Metabolism 1996;45:838-843.