Bifidobacterium pseudocatenulatum CECT 7765 Ameliorates Neuroendocrine Alterations Associated with an Exaggerated Stress Response and Anhedonia in Obese Mice

Molecular Neurobiology

Volumn 55, Issue 6, 2018, Pages 5337-5352

  Agusti, Ana ^a,b   Moya Perez A ^a,b   Campillo, I ^a,b   Montserrat de la Paz, S ^a,b   Cerrudo, V ^a,b   Perez Villalba, A ^a,b   Sanz, Yolanda ^a,b  

^a INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Bifidobacterium; Depression; Microbiota; Obesity; Serotonin; Stress; TLR2

Indexed keywords

CORTICOSTERONE; EPINEPHRINE; LEPTIN; NEUROTRANSMITTER; TOLL LIKE RECEPTOR 2; CATECHOLAMINE; GLUCOCORTICOID RECEPTOR; LEPTIN RECEPTOR; SEROTONIN;

ADULT; ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BIFIDOBACTERIUM PSEUDOCATENULATUM; BODY WEIGHT GAIN; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; ENERGY BALANCE; FAT MASS; GENE EXPRESSION; HORMONE DETERMINATION; HYPERLEPTINEMIA; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; SOCIAL STRESS; STRESS; TLR2 GENE; UPREGULATION; ANIMAL; ANXIETY; BIFIDOBACTERIUM; BLOOD; C57BL MOUSE; FECES; METABOLISM; MICROBIOLOGY; MOTOR ACTIVITY; MOUSE MUTANT; NEUROENDOCRINE SYSTEM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ADIPOSITY; ANHEDONIA; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BIFIDOBACTERIUM; CATECHOLAMINES; CORTICOSTERONE; DEPRESSION; FECES; LEPTIN; MALE; MICE, INBRED C57BL; MICE, OBESE; MOTOR ACTIVITY; NEUROSECRETORY SYSTEMS; RECEPTORS, GLUCOCORTICOID; RECEPTORS, LEPTIN; SEROTONIN; STRESS, PHYSIOLOGICAL; TOLL-LIKE RECEPTOR 2; WEIGHT GAIN;

EID: 85029585850     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-017-0768-z     Document Type: Article

References (74)

1. Luppino FS, de Wit LM, Bouvy PF, Stijnen T, Cuijpers P, Penninx BW, Zitman FG (2010) Overweight, obesity, and depression: a systematic review and meta-analysis of longitudinal studies. Arch Gen Psychiatry 67(3):220–229
2. Needham BL, Epel ES, Adler NE, Kiefe C (2010) Trajectories of change in obesity and symptoms of depression: the Cardia study. Am J Public Health 100(6):1040–1046
3. Ma J, Xiao L (2010) Obesity and depression in US women: results from the 2005-2006 National Health and Nutritional Examination Survey. Obesity (Silver Spring) 18(2):347–353
4. Farshim P, Walton G, Chakrabarti B, Givens I, Saddy D, Kitchen I, Swann J R, Bailey A (2016) Maternal weaning modulates emotional behavior and regulates the gut-brain axis. Sci Rep 6:21958
5. Morris G, Berk M, Carvalho A, Caso JR, Sanz Y, Walder K, Maes M (2016) The role of the microbial metabolites including tryptophan catabolites and short chain fatty acids in the pathophysiology of immune-inflammatory and neuroimmune disease. Mol Neurobiol 54(6):4432–4451
6. Sharma S, Fulton S (2013) Diet-induced obesity promotes depressive-like behaviour that is associated with neural adaptations in brain reward circuitry. Int J Obes 37(3):382–389
7. Pan A, Sun Q, Czernichow S, Kivimaki M, Okereke OI, Lucas M, Manson JE, Ascherio A et al (2012) Bidirectional association between depression and obesity in middle-aged and older women. Int J Obes 36(4):595–602
8. Cooke AA, Connaughton RM, Lyons CL, McMorrow AM, Roche HM (2016) Fatty acids and chronic low grade inflammation associated with obesity and the metabolic syndrome. Eur J Pharmacol 785:207–214
9. Sanz Y, Moya-Perez A (2014) Microbiota, inflammation and obesity. Adv Exp Med Biol 817:291–317
10. Latorre E, Layunta E, Grasa L, Castro M, Pardo J, Gomollon F, Alcalde AI, Mesonero JE (2016) Intestinal serotonin transporter inhibition by Toll-like receptor 2 activation. A feedback modulation. PLoS One 11(12):e0169303
11. Himes RW, Smith CW (2010) Tlr2 is critical for diet-induced metabolic syndrome in a murine model. FASEB J 24(3):731–739
12. Mawe GM, Hoffman JM (2013) Serotonin signalling in the gut—functions, dysfunctions and therapeutic targets. Nat Rev Gastroenterol Hepatol 10(8):473–486
13. Spiller R (2008) Serotonin and Gi clinical disorders. Neuropharmacology 55(6):1072–1080
14. Dale E, Pehrson AL, Jeyarajah T, Li Y, Leiser SC, Smagin G, Olsen CK, Sanchez C (2016) Effects of serotonin in the hippocampus: how SSRIs and multimodal antidepressants might regulate pyramidal cell function. CNS Spectr 21(2):143–161
15. Yamada N, Katsuura G, Ochi Y, Ebihara K, Kusakabe T, Hosoda K, Nakao K (2011) Impaired CNS leptin action is implicated in depression associated with obesity. Endocrinology 152(7):2634–2643
16. Collins SM, Surette M, Bercik P (2012) The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10:735–742
17. De Palma G, Blennerhassett P, Lu J, Deng Y, Park AJ, Green W, Denou E, Silva MA et al (2015) Microbiota and host determinants of behavioral phenotype in maternally separated mice. Nat Commun 6:7735
18. Sanz Y (2016) The encyclopedia of food and health. Academic Press, Oxford
19. Hanstock TL, Mallet PE, Clayton EH (2010) Increased plasma D-lactic acid associated with impaired memory in rats. Physiol Behav 101(5):653–659
20. Tana C, Umesaki Y, Imaoka A, Handa T, Kanazawa M, Fukudo S (2010) Neurogastroenterol Motil. Neurogastroenterol Motil 22(5):512–519
21. Schroeder FA, Lin CL, Crusio WE, Akbarian S (2007) Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 62(1):55–64
22. Logan AC, Katzman M (2005) Major depressive disorder: probiotics may be an adjuvant therapy. Med Hypotheses 64(3):533–538
23. Shadnoush M, Shaker Hosseini R, Mehrabi Y, Delpisheh A, Alipoor E, Faghfoori Z, Mohammadpour N, Zaringhalam Moghadam J (2013) Probiotic yogurt affects pro- and anti-inflammatory factors in patients with inflammatory bowel disease. Iran J Pharm Res 12(4):929–936
24. Barouei J, Moussavi M, Hodgson DM (2015) Perinatal maternal probiotic intervention impacts immune responses and ileal mucin gene expression in a rat model of irritable bowel syndrome. Benefic Microbes 6(1):83–95
25. Moya-Perez A, Neef A, Sanz Y (2015) Bifidobacterium pseudocatenulatum Cect 7765 reduces obesity-associated inflammation by restoring the lymphocyte-macrophage balance and gut microbiota structure in high-fat diet-fed mice. PLoS One 10(7):e0126976
26. Moya-Perez A, Romo-Vaquero M, Tomas-Barberan F, Sanz Y, Garcia-Conesa MT (2014) Hepatic molecular responses to Bifidobacterium pseudocatenulatum Cect 7765 in a mouse model of diet-induced obesity. Nutr Metab Cardiovasc Dis 24(1):57–64
27. Cano PG, Santacruz A, Trejo FM, Sanz Y (2013) Bifidobacterium Cect 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet-fed mice. Obesity (Silver Spring) 21(11):2310–2321
28. Moratalla A, Gomez-Hurtado I, Santacruz A, Moya A, Peiro G, Zapater P, Gonzalez-Navajas JM, Gimenez P et al (2014) Protective effect of Bifidobacterium pseudocatenulatum Cect7765 against induced bacterial antigen translocation in experimental cirrhosis. Liver Int 34(6):850–858
29. Moratalla A, Caparros E, Juanola O, Portune K, Puig-Kroger A, Estrada-Capetillo L, Bellot P, Gomez-Hurtado I et al (2016) Bifidobacterium pseudocatenulatum Cect7765 induces an M2 anti-inflammatory transition in macrophages from patients with cirrhosis. J Hepatol 64(1):135–145
30. Stetz J, Hunt K, Kendall KC, Wasser SK (2013) Effects of exposure, diet, and thermoregulation on fecal glucocorticoid measures in wild bears. PLoS One 8(2):e55967
31. Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, Nagler CR, Ismagilov RF et al (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161(2):264–276
32. Duncko R, Brtko J, Kvetnansky R, Jezova D (2001) Altered function of peripheral organ systems in rats exposed to chronic mild stress model of depression. Cell Mol Neurobiol 21(4):403–411
33. Crawley J, Goodwin FK (1980) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13(2):167–170
34. Liu J, Guo M, Lu XY (2015) Leptin/Leprb in the ventral tegmental area mediates anxiety-related behaviors. Int J Neuropsychopharmacol 19(2). 10.1093/ijnp/pyv115
35. Porsolt RD, Bertin A, Jalfre M (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229(2):327–336
36. Mahanti S, Majhi A, Chongdar S, Kundu K, Dutta K, Basu A, Bishayi B (2013) Increased resistance of immobilized-stressed mice to infection: correlation with behavioral alterations. Brain Behav Immun 28:115–127
37. Tamashiro KL, Nguyen MM, Sakai RR (2005) Social stress: from rodents to primates. Front Neuroendocrinol 26(1):27–40
38. De Miguel Z, Vegas O, Garmendia L, Arregi A, Beitia G, Azpiroz A (2011) Behavioral coping strategies in response to social stress are associated with distinct neuroendocrine, monoaminergic and immune response profiles in mice. Behav Brain Res 225(2):554–561
39. De Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6(6):463–475
40. Wilkening JL, Ray C, Varner J (2016) When can we measure stress noninvasively? Postdeposition effects on a fecal stress metric confound a multiregional assessment. Ecol Evol 6(2):502–513
41. Denenberg VH (1969) Open-field behavior in the rat: what does it mean? Ann N Y Acad Sci 159(3):852–859
42. Seibenhener ML, Wooten MC (2015) Use of the open field maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp (96):e52434. 10.3791/52434
43. Hageman I, Nielsenb M, Wortweina G, Diemerc NH, Jorgensen MB (2009) Electroconvulsive stimulation normalize stress-induced changes in the glucocorticoid receptor and behaviour. Behav Brain Res 196(1):71–77
44. Colelli V, Campus P, Conversi D, Orsini C, Cabib S (2014) Either the dorsal hippocampus or the dorsolateral striatum is selectively involved in consolidation of forced swim-induced immobility depending on genetic background. Neurobiol Learn Mem 111:49–55
45. Castagne V, Moser P, Porsolt RD (2009) Behavioral assessment of antidepressant activity in rodents. In: Buccafusco JJ (ed) Methods of behavior analysis in neuroscience, 2nd edn. CRC Press, Boca Raton
46. Yang JL, Liu X, Jiang H, Pan F, Ho CS, Ho RC (2016) The effects of high-fat-diet combined with chronic unpredictable mild stress on depression-like behavior and leptin/Leprb in male rats. Sci Rep 6:35239
47. Lopresti AL, Maker GL, Hood SD, Drummond PD (2014) A review of peripheral biomarkers in major depression: the potential of inflammatory and oxidative stress biomarkers. Prog Neuro-Psychopharmacol Biol Psychiatry 48:102–111
48. Moya-Perez A, Perez-Villalba A, Benitez-Paez A, Campillo I, Sanz Y (2017) Bifidobacterium Cect 7765 modulates early stress-induced immune, neuroendocrine and behavioral alterations in mice. Brain Behav Immun 65:43–56
49. Sharma S, Zhuang Y, Gomez-Pinilla F (2012) High-fat diet transition reduces brain Dha levels associated with altered brain plasticity and behaviour. Sci Rep 2:431
50. Hamer M, Batty GD, Kivimaki M (2012) Risk of future depression in people who are obese but metabolically healthy: the English longitudinal study of ageing. Mol Psychiatry 17(9):940–945
51. Slyepchenko AMM, Jacka FN, Köhler CA, Barichello T, RS MI, Berk M, Grande I, Foster JA et al (2017) Gut microbiota, bacterial translocation, and interactions with diet: pathophysiological links between major depressive disorder and non-communicable medical comorbidities. Psychother Psychosom 86(1):31–46
52. Tanaka M, Yoshida M, Emoto H, Ishii H (2000) Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies. Eur J Pharmacol 405(1–3):397–406
53. Kesby JP, Kim JJ, Scadeng M, Woods G, Kado DM, Olefsky JM, Jeste DV, Achim CL et al (2015) Spatial cognition in adult and aged mice exposed to high-fat diet. PLoS One 10(10):e0140034
54. Stepanichev MY, Tishkina AO, Novikova MR, Levshina IP, Freiman SV, Onufriev MV, Levchenko OA, Lazareva NA et al (2016) Anhedonia but not passive floating is an indicator of depressive-like behavior in two chronic stress paradigms. Acta Neurobiol Exp (Wars) 76(4):324–333
55. Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, Fei H, Kim S et al (1995) Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1(11):1155–1161
56. Stieg MR, Sievers C, Farr O, Stalla GK, Mantzoros CS (2015) Leptin: a hormone linking activation of neuroendocrine axes with neuropathology. Psychoneuroendocrinology 51:47–57
57. Carvalho AF, Rocha DQ, RS MI, Mesquita LM, Köhler CA, Hyphantis TN, Sales PM, Machado-Vieira R et al (2014) Adipokines as emerging depression biomarkers: a systematic review and meta-analysis. J Psychiatr Res 59:28–37
58. Liu CS, Carvalho AF, McIntyre RS (2014) Towards a “metabolic” subtype of major depressive disorder: shared pathophysiological mechanisms may contribute to cognitive dysfunction. CNS Neurol Disord Drug Targets 13(10):1693–1707
59. Vogelzangs N, Beekman AT, van Reedt Dortland AK, Schoevers RA, Giltay EJ, de Jonge P, Penninx BW (2014) Inflammatory and metabolic dysregulation and the 2-year course of depressive disorders in antidepressant users. Neuropsychopharmacology 39(7):1624–1634
60. Sharma A, Bartell SM, Baile CA, Chen B, Podolsky RH, McIndoe RA, She JX (2010) Hepatic gene expression profiling reveals key pathways involved in leptin-mediated weight loss in Ob/Ob mice. PLoS One 5(8):e12147
61. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R (1987) Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 93(3):358–364
62. Lu XY, Kim CS, Frazer A, Zhang W (2006) Leptin: a potential novel antidepressant. Proc Natl Acad Sci U S A 103(5):1593–1598
63. Buyse M, Ovesjo ML, Goiot H, Guilmeau S, Peranzi G, Moizo L, Walker F, Lewin MJ et al (2001) Expression and regulation of leptin receptor proteins in afferent and efferent neurons of the vagus nerve. Eur J Neurosci 14(1):64–72
64. De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, Saad MJ, Velloso LA (2005) Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 146(10):4192–4199
65. Jeon BT, Jeong EA, Shin HJ, Lee Y, Lee DH, Kim HJ, Kang SS, Cho GJ et al (2012) Resveratrol attenuates obesity-associated peripheral and central inflammation and improves memory deficit in mice fed a high-fat diet. Diabetes 61(6):1444–1454
66. Puig KL, Floden AM, Adhikari R, Golovko MY, Combs CK (2012) Amyloid precursor protein and proinflammatory changes are regulated in brain and adipose tissue in a murine model of high fat diet-induced obesity. PLoS One 7(1):e30378
67. Kempuraj D, Thangavel R, Natteru PA, Selvakumar GP, Saeed D, Zahoor H, Zaheer S, Iyer SS et al (2016) Neuroinflammation induces neurodegeneration. J Neurol Neurosurg Spine 1(1):1003
68. Hayward JH, Lee SJ (2014) A decade of research on Tlr2 discovering its pivotal role in glial activation and neuroinflammation in neurodegenerative diseases. Exp Neurobiol 23(2):138–147
69. Kim C, Ho DH, Suk JE, You S, Michael S, Kang J, Joong Lee S, Masliah E et al (2013) Neuron-released oligomeric alpha-synuclein is an endogenous agonist of Tlr2 for paracrine activation of microglia. Nat Commun 4:1562
70. Hwang DH, Kim JA, Lee JY (2016) Mechanisms for the activation of toll-like receptor 2/4 by saturated fatty acids and inhibition by docosahexaenoic acid. Eur J Pharmacol 785:24–35
71. Boukouvalas G, Gerozissis K, Kitraki E (2010) Adult consequences of post-weaning high fat feeding on the limbic-Hpa axis of female rats. Cell Mol Neurobiol 30(4):521–530
72. Maniam J, Morris MJ (2010) Voluntary exercise and palatable high-fat diet both improve behavioral profile and stress responses in male rats exposed to early life stress: role of hippocampus. Psychoneuroendocrinology 35(10):1553–1564
73. Reimann M, Qin N, Gruber M, Bornstein SR, Kirschbaum C, Ziemssen T, Eisenhofer G (2017) Adrenal medullary dysfunction as a feature of obesity. Int J Obes (Lond) 41(5):714–721
74. Gotthardt JD, Verpeut JL, Yeomans BL, Yang JA, Yasrebi A, Roepke TA, Bello NT (2016) Intermittent fasting promotes fat loss with lean mass retention, increased hypothalamic norepinephrine content, and increased neuropeptide Y gene expression in diet-induced obese male mice. Endocrinology 157(2):679–691