#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Neurobehavioral dysfunction in non-alcoholic steatohepatitis is associated with hyperammonemia, gut dysbiosis, and metabolic and functional brain regional deficits


Autoři: Sara G. Higarza aff001;  Silvia Arboleya aff003;  Miguel Gueimonde aff003;  Eneritz Gómez-Lázaro aff004;  Jorge L. Arias aff001;  Natalia Arias aff001
Působiště autorů: Institute of Neurosciences of the Principality of Asturias (INEUROPA), Asturias, Spain aff001;  Laboratory of Neuroscience, Department of Psychology, University of Oviedo, Oviedo, Asturias, Spain aff002;  Department of Microbiology and Biochemistry of Dairy Products, Institute of Dairy Products of the Principality of Asturias (IPLA-CSIC), Asturias, Spain aff003;  Department of Basic Psychological Processes and their Development, Basque Country University, San Sebastián, Basque Country, Spain aff004;  Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, England, United Kingdom aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223019

Souhrn

Non-alcoholic steatohepatitis (NASH) is one of the most prevalent diseases worldwide. While it has been suggested to cause nervous impairment, its neurophysiological basis remains unknown. Therefore, the aim of this study is to unravel the effects of NASH, through the interrelationship of liver, gut microbiota, and nervous system, on the brain and human behavior. To this end, 40 Sprague-Dawley rats were divided into a control group that received normal chow and a NASH group that received a high-fat, high-cholesterol diet. Our results show that 14 weeks of the high-fat, high-cholesterol diet induced clinical conditions such as NASH, including steatosis and increased levels of ammonia. Rats in the NASH group also demonstrated evidence of gut dysbiosis and decreased levels of short-chain fatty acids in the gut. This may explain the deficits in cognitive ability observed in the NASH group, including their depressive-like behavior and short-term memory impairment characterized in part by deficits in social recognition and prefrontal cortex-dependent spatial working memory. We also reported the impact of this NASH-like condition on metabolic and functional processes. Brain tissue demonstrated lower levels of metabolic brain activity in the prefrontal cortex, thalamus, hippocampus, amygdala, and mammillary bodies, accompanied by a decrease in dopamine levels in the prefrontal cortex and cerebellum and a decrease in noradrenalin in the striatum. In this article, we emphasize the important role of ammonia and gut-derived bacterial toxins in liver-gut-brain neurodegeneration and discuss the metabolic and functional brain regional deficits and behavioral impairments in NASH.

Klíčová slova:

Biology and life sciences – Nutrition – Diet – Neuroscience – Cognitive science – Cognitive neuroscience – Working memory – Cognition – Memory – Learning and memory – Anatomy – Brain – Prefrontal cortex – Biochemistry – Lipids – Cholesterol – Psychology – Behavior – Medicine and health sciences – Neurology – Cognitive neurology – Cognitive impairment – Gastroenterology and hepatology – Liver diseases – Fatty liver – Social sciences


Zdroje

1. Tomic D, Kemp WW, Roberts SK. Nonalcoholic fatty liver disease: current concepts, epidemiology and management strategies. Eur J Gastroenterol Hepatol. 2018;30(10):1103–15. doi: 10.1097/MEG.0000000000001235 30113367

2. Carr RM, Oranu A, Khungar V. Non-alcoholic fatty liver disease: pathophysiology and management. Gastroenterol Clin North Am. 2016;45(4):639–52. doi: 10.1016/j.gtc.2016.07.003 27837778

3. Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43(2 Suppl 1):S99–112. doi: 10.1002/hep.20973 16447287

4. Carter-Kent C, Zein NN, Feldstein AE. Cytokines in the pathogenesis of fatty liver and disease progression to steatohepatitis: implications for treatment. Am J Gastroenterol. 2008;103(4):1036–42. 18177455

5. Santhekadur PK, Kumar D, Sanyal A. Preclinical models of nonalcoholic fatty liver. J Hepatol. 2018;68(2):230–7. doi: 10.1016/j.jhep.2017.10.031 29128391

6. Thomsen KL, Grønbæk H, Glavind E, Hebbard L, Jessen N, Clouston A, et al. Experimental nonalcoholic steatohepatitis compromises ureagenesis, an essential hepatic metabolic function. Am J Physiol Gastrointest Liver Physiol. 2014;307(3):G295–301. doi: 10.1152/ajpgi.00036.2014 24924745

7. De Chiara F, Heebøll S, Marrone G, Montoliu C, Hamilton-Dutoit S, Ferrandez A, et al. Urea cycle dysregulation in non-alcoholic fatty liver disease. J Hepatol. 2018;69(4):905–15. doi: 10.1016/j.jhep.2018.06.023 29981428

8. Christensen CU, Glavind E, Thomsen KL, Kim YO, Heebøll S, Schuppan D, et al. Niemann-Pick type C2 protein supplementation in experimental nonalcoholic fatty liver disease. PLoS One. 2018;13(3):e0192728. doi: 10.1371/journal.pone.0192728 29522534

9. Heebøll S, Thomsen KL, Clouston A, Sundelin EI, Radko Y, Christensen LP, et al. Effect of resveratrol on experimental non-alcoholic steatohepatitis. Pharmacol Res. 2015;95–96:34–41. doi: 10.1016/j.phrs.2015.03.005 25814186

10. Thomsen KL, Aagaard NK, Grønbæk H, Holst JJ, Jessen N, Frystyk J, et al. IL-6 has no acute effect on the regulation of urea synthesis in vivo in rats. Scand J Clin Lab Invest. 2011;71(2):150–6. doi: 10.3109/00365513.2010.547213 21190512

11. Morris MC, Tangney CC, Wang Y, Sacks FM, Barnes LL, Bennett DA, et al. MIND diet slows cognitive decline with aging. Alzheimer’s Dement. 2015;11(9):1015–22.

12. Deshpande NG, Saxena J, Pesaresi TG, Carrell CD, Ashby GB, Liao M-K, et al. High fat diet alters gut microbiota but not spatial working memory in early middle-aged Sprague Dawley rats. PLoS One. 2019;14(5):e0217553. doi: 10.1371/journal.pone.0217553 31141574

13. Granholm A- C, Bimonte-Nelson HA, Moore AB, Nelson ME, Freeman LR, Sambamurti K. Effects of a saturated fat and high cholesterol diet on memory and hippocampal morphology in the middle-aged rat. J Alzheimer’s Dis. 2008;14(2):133–45.

14. Ledreux A, Wang X, Schultzberg M, Granholm AC, Freeman LR. Detrimental effects of a high fat/high cholesterol diet on memory and hippocampal markers in aged rats. Behav Brain Res. 2016;312:294–304. doi: 10.1016/j.bbr.2016.06.012 27343935

15. Stam R, Akkermans LMA, Wiegant VM. Trauma and the gut: interactions between stressful experience and intestinal function. Gut. 1997;40(6):704–9. doi: 10.1136/gut.40.6.704 9245921

16. Klooker TK, Braak B, Painter RC, de Rooij SR, van Elburg RM, van den Wijngaard RM, et al. Exposure to severe wartime conditions in early life is associated with an increased risk of irritable bowel syndrome: a population-based cohort study. Am J Gastroenterol. 2009;104(9):2250–6. 19513027

17. Moloney RD, Johnson AC, O’Mahony SM, Dinan TG, Greenwood-Van Meerveld B, Cryan JF. Stress and the microbiota-gut-brain axis in visceral pain: relevance to irritable bowel syndrome. CNS Neurosci Ther. 2016;22(2):102–17. doi: 10.1111/cns.12490 26662472

18. Bharwani A, Mian MF, Foster JA, Surette MG, Bienenstock J, Forsythe P. Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinology. 2016;63:217–27. doi: 10.1016/j.psyneuen.2015.10.001 26479188

19. 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(1–2):84–96. doi: 10.1016/j.cell.2013.12.016 24412651

20. Li Z, Yi CX, Katiraei S, Kooijman S, Zhou E, Chung CK, et al. Butyrate reduces appetite and activates brown adipose tissue via the gut-brain neural circuit. Gut. 2018;67(7):1269–79. doi: 10.1136/gutjnl-2017-314050 29101261

21. Chambers ES, Viardot A, Psichas A, Morrison DJ, Murphy KG, Zac-Varghese SEK, et al. Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut. 2015;64(11):1744–54. doi: 10.1136/gutjnl-2014-307913 25500202

22. Reigstad CS, Salmonson CE, Rainey JF, Szurszewski JH, Linden DR, Sonnenburg JL, et al. Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J. 2015;29(4):1395–403. doi: 10.1096/fj.14-259598 25550456

23. Agrawal R, Noble E, Vergnes L, Ying Z, Reue K, Gomez-Pinilla F. Dietary fructose aggravates the pathobiology of traumatic brain injury by influencing energy homeostasis and plasticity. J Cereb Blood Flow Metab. 2016;36(5):941–53. doi: 10.1177/0271678X15606719 26661172

24. Mastrocola R, Nigro D, Cento AS, Chiazza F, Collino M, Aragno M. High-fructose intake as risk factor for neurodegeneration: key role for carboxy methyllysine accumulation in mice hippocampal neurons. Neurobiol Dis. 2016;89:65–75. doi: 10.1016/j.nbd.2016.02.005 26851500

25. Rojas JC, Bruchey AK, Gonzalez-Lima F. Low-level light therapy improves cortical metabolic capacity and memory retention. J Alzheimer’s Dis. 2012;32(3):741–52.

26. Wouters K, van Gorp PJ, Bieghs V, Gijbels MJ, Duimel H, Lütjohann D, et al. Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology. 2008;48(2):474–86. doi: 10.1002/hep.22363 18666236

27. Ikemoto S, Takahashi M, Tsunoda N, Maruyama K, Itakura H, Kawanaka K, et al. Cholate inhibits and obesity with acyl-CoA synthetase hyperglycemia mRNA decrease. Am J Physiol. 1997;273(1 Pt 1):E37–45.

28. Kucera O, Cervinkova Z. Experimental models of non-alcoholic fatty liver disease in rats. World J Gastroenterol. 2014;20(26):8364–76. doi: 10.3748/wjg.v20.i26.8364 25024595

29. Arboleya S, Binetti A, Salazar N, Ferna N, Solís G, Hernández-Barranco A, et al. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol. 2012;79(3):763–72. doi: 10.1111/j.1574-6941.2011.01261.x 22126419

30. Milani C, Hevia A, Foroni E, Duranti S, Turroni F, Gueimonde M, et al. Assessing the fecal microbiota: an optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS One. 2013;8(7):e68739. doi: 10.1371/journal.pone.0068739 23869230

31. Nogacka A, Salazar N, Suárez M, Milani C, Arboleya S, Solís G, et al. Impact of intrapartum antimicrobial prophylaxis upon the intestinal microbiota and the prevalence of antibiotic resistance genes in vaginally delivered full-term neonates. Microbiome. 2017;5(1):93. doi: 10.1186/s40168-017-0313-3 28789705

32. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1. doi: 10.1093/bioinformatics/btq461 20709691

33. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Glo FO, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–596. doi: 10.1093/nar/gks1219 23193283

34. Arboleya S, Sánchez B, Ventura M, Margolles A, Fernández N, de los Reyes-Gavilán CG, et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr. 2015;166(3):538–44. doi: 10.1016/j.jpeds.2014.09.041 25444008

35. Valdés L, Salazar N, González S, Arboleya S, Ríos-Covián D, Genovés S, et al. Selection of potential probiotic bifidobacteria and prebiotics for elderly by using in vitro faecal batch cultures. Eur Food Res Technol. 2017;243(1):157–65.

36. Moris G, Arboleya S, Mancabelli L, Milan C, Ventura M, Re CGDL, et al. Fecal microbiota profile in a group of myasthenia gravis patients. Sci Rep. 2018;8(1):14384. doi: 10.1038/s41598-018-32700-y 30258104

37. Jones BJ, Roberts DJ. The quantitative measurement of motor inco-ordination in naive mice using an accelerating rotarod. J Pharm Pharmacol. 1968;20(4):302–4. doi: 10.1111/j.2042-7158.1968.tb09743.x 4384609

38. Slattery DA, Markou A, Cryan JF. Evaluation of reward processes in an animal model of depression. Psychopharmacology (Berl). 2007;190(4):555–68.

39. Porsolt RD, Anton G, Blavet N, Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol. 1978;47(4):379–91. doi: 10.1016/0014-2999(78)90118-8 204499

40. Prado VF, Martins-Silva C, de Castro BM, Lima RF, Barros DM, Amaral E, et al. Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition. Neuron. 2006;51(5):601–12. doi: 10.1016/j.neuron.2006.08.005 16950158

41. Méndez M, Méndez-López M, López L, Aller MA, Arias J, Arias JL. Working memory impairment and reduced hippocampal and prefrontal cortex c-Fos expression in a rat model of cirrhosis. Physiol Behav. 2008;95(3):302–7. doi: 10.1016/j.physbeh.2008.06.013 18634813

42. Gonzalez-Lima F, Cada A. Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study. Neuroscience. 1994;63(2):559–78. doi: 10.1016/0306-4522(94)90550-9 7891865

43. Wong-Riley MTT. Cytochrome oxidase: an endogenous metabolic marker for neuron activity. Trends Neurosci. 1989;12(3):94–101. doi: 10.1016/0166-2236(89)90165-3 2469224

44. González-Pardo H, Novelli A, Menéndez-Patterson A, Arias JL. The developmental of oxidative metabolism in diencephalic structures of the rat: a quantitative study. Brain Res Bull. 1996;41(1):31–8. doi: 10.1016/0361-9230(96)00007-x 8883913

45. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 5th ed. Elsevier Academic Press; 2004.

46. Francque S, Verrijken A, Mertens I, Hubens G, Van Marck E, Pelckmans P, et al. Noncirrhotic human nonalcoholic fatty liver disease induces portal hypertension in relation to the histological degree of steatosis. Eur J Gastroenterol Hepatol. 2010;22(12):1449–57. 21389796

47. Marques C, Meireles M, Norberto S, Leite J, Freitas J, Pestana D, et al. High-fat diet-induced obesity rat model: a comparison between Wistar and Sprague-Dawley rat. Adipocyte. 2016;5(1):11–21. doi: 10.1080/21623945.2015.1061723 27144092

48. Xu ZJ, Fan JG, Ding XD, Qiao L, Wang GL. Characterization of high-fat, diet-induced, non-alcoholic steatohepatitis with fibrosis in rats. Dig Dis Sci. 2010;55(4):931–40. doi: 10.1007/s10620-009-0815-3 19459046

49. Byrne CD, Targher G. NAFLD: a multisystem disease. J Hepatol. 2015;62(1 Suppl):S47–64. doi: 10.1016/j.jhep.2014.12.012 25920090

50. Yki-Järvinen H. Diagnosis of non-alcoholic fatty liver disease (NAFLD). Diabetologia. 2016;59(6):1104–11. doi: 10.1007/s00125-016-3944-1 27091184

51. Neuman MG, Cohen LB, Nanau RM. Biomarkers in nonalcoholic fatty liver disease. Can J Gastroenterol Hepatol. 2014;28(11):607–18. 25575111

52. Skowrońska M, Albrecht J. Alterations of blood brain barrier function in hyperammonemia: an overview. Neurotox Res. 2012;21(2):236–44. doi: 10.1007/s12640-011-9269-4 21874372

53. Hernández-Rabaza V, Cabrera-Pastor A, Taoro-González L, Malaguarnera M, Agustí A, Llansola M, et al. Hyperammonemia induces glial activation, neuroinflammation and alters neurotransmitter receptors in hippocampus, impairing spatial learning: reversal by sulforaphane. J Neuroinflammation. 2016;13:41. doi: 10.1186/s12974-016-0505-y 26883214

54. Rodrigo R, Cauli O, Gomez-Pinedo U, Agusti A, Hernandez-Rabaza V, Garcia-Verdugo JM, et al. Hyperammonemia induces neuroinflammation that contributes to cognitive impairment in rats with hepatic encephalopathy. Gastroenterology. 2010;139(2):675–84. doi: 10.1053/j.gastro.2010.03.040 20303348

55. Freeman LR, Zhang L, Nair A, Dasuri K, Francis J, Fernandez-Kim S-O, et al. Obesity increases cerebrocortical reactive oxygen species and impairs brain function. Free Radic Biol Med. 2013;56:226–33. doi: 10.1016/j.freeradbiomed.2012.08.577 23116605

56. Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann R, Egan JM, et al. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus. 2008;18(11):1085–8. doi: 10.1002/hipo.20470 18651634

57. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011;108(7):3047–52. doi: 10.1073/pnas.1010529108 21282636

58. Neufeld KM, Kang N, Bienenstock J, Foster JA. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil. 2011;23(3):255–65. doi: 10.1111/j.1365-2982.2010.01620.x 21054680

59. Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology. 2011;141(2):599–609. doi: 10.1053/j.gastro.2011.04.052 21683077

60. 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(7122):1027–31. doi: 10.1038/nature05414 17183312

61. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Marked alterations in the distal gut microbiome linked to diet-induced obesity. Cell Host Microbe. 2008;3(4):213–23. 18407065

62. Bruce-Keller AJ, Salbaum JM, Luo M, Iv EB, Taylor CM, Welsh DA, et al. Obese-type gut microbiota induce neurobehavioral changes in the absence of obesity. Biol Psychiatry. 2015;77(7):607–15. doi: 10.1016/j.biopsych.2014.07.012 25173628

63. Shawcross DL. Is it time to target gut dysbiosis and immune dysfunction in the therapy of hepatic encephalopathy? Expert Rev Gastroenterol Hepatol. 2015;9(5):539–42. doi: 10.1586/17474124.2015.1035257 25846450

64. Kang DJ, Betrapally NS, Gosh SA, Sartor RB, Hylemon PB, Gillevet PM, et al. Gut microbiota drive the development of neuro-inflammatory response in cirrhosis. Hepatology. 2016;64(4):1232–48. doi: 10.1002/hep.28696 27339732

65. Boulangé CL, Neves AL, Chilloux J, Nicholson JK, Dumas ME. Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med. 2016;8(1):42. doi: 10.1186/s13073-016-0303-2 27098727

66. Ma J, Zhou Q, Li H. Gut microbiota and nonalcoholic fatty liver disease: insights on mechanisms and therapy. Nutrients. 2017;9(10).

67. Plaza-Díaz J, Ruiz-Ojeda FJ, Vilchez-Padial LM, Gil A. Evidence of the anti-inflammatory effects of probiotics and synbiotics in intestinal chronic diseases. Nutrients. 2017;9(6).

68. Nagpal R, Kumar M, Yadav AK, Hemalatha R, Yadav H, Marotta F, et al. Gut microbiota in health and disease: an overview focused on metabolic inflammation. Benef Microbes. 2016;7(2):181–94. doi: 10.3920/bm2015.0062 26645350

69. Bravo JA, Forsythe P, Chew M V., 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(38):16050–5. doi: 10.1073/pnas.1102999108 21876150

70. Perez-Burgos A, Wang B, Mao Y-K, Mistry B, Neufeld K-AM, Bienenstock J, et al. Psychoactive bacteria Lactobacillus rhamnosus (JB-1) elicits rapid frequency facilitation in vagal afferents. Am J Physiol Liver Physiol. 2013;304(2):G211–20.

71. Dinan TG, Cryan JF. Melancholic microbes: a link between gut microbiota and depression? Neurogastroenterol Motil. 2013;25(9):713–9. doi: 10.1111/nmo.12198 23910373

72. Tedelind S, Westberg F, Kjerrulf M, Vidal A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World J Gastroenterol. 2007;13(20):2826–32. doi: 10.3748/wjg.v13.i20.2826 17569118

73. Al-Lahham SH, Roelofsen H, Priebe M, Weening D, Dijkstra M, Hoek A, et al. Regulation of adipokine production in human adipose tissue by propionic acid. Eur J Clin Invest. 2010;40(5):401–7. doi: 10.1111/j.1365-2362.2010.02278.x 20353437

74. Fukae J, Amasaki Y, Yamashita Y, Bohgaki T, Yasuda S, Jodo S, et al. Butyrate suppresses tumor necrosis factor α production by regulating specific messenger RNA degradation mediated through a cis-acting AU-rich element. Arthritis Rheum. 2005;52(9):2697–707. doi: 10.1002/art.21258 16142751

75. Säemann MD, Böhmig GA, Österreicher CH, Burtscher H, Parolini O, Diakos C, et al. Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000;14(15):2380–2. doi: 10.1096/fj.00-0359fje 11024006

76. Saad MJA, Santos A, Prada PO. Linking gut microbiota and inflammation to obesity and insulin resistance. Physiology. 2016;31(4):283–93. doi: 10.1152/physiol.00041.2015 27252163

77. van de Wouw M, Boehme M, Lyte JM, Wiley N, Strain C, O’Sullivan O, et al. Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain–gut axis alterations. J Physiol. 2018;596(20):4923–44. doi: 10.1113/JP276431 30066368

78. Bogdanova O V, Kanekar S, Renshaw PF. Factors influencing behavior in the forced swim test. Physiol Behav. 2017;118:227–39.

79. Mebel DM, Wong JCY, Dong YJ, Borgland SL. Insulin in the ventral tegmental area reduces hedonic feeding and suppresses dopamine concentration via increased reuptake. Eur J Neurosci. 2012;36(3):2336–46. doi: 10.1111/j.1460-9568.2012.08168.x 22712725

80. Strekalova T, Evans M, Costa-Nunes J, Bachurin S, Yeritsyan N, Couch Y, et al. Tlr4 upregulation in the brain accompanies depression- and anxiety-like behaviors induced by a high-cholesterol diet. Brain Behav Immun. 2015;48:42–7. doi: 10.1016/j.bbi.2015.02.015 25712260

81. Del Rosario A, McDermott MM, Panee J. Effects of high fat diet and bamboo extract supplement on anxiety- an depression-like neurobehaviors in mice. Br J Nutr. 2015;33(4):395–401.

82. McNeilly AD, Stewart CA, Sutherland C, Balfour DJK. High fat feeding is associated with stimulation of the hypothalamic-pituitary-adrenal axis and reduced anxiety in the rat. Psychoneuroendocrinology. 2015;52:272–80. doi: 10.1016/j.psyneuen.2014.12.002 25544739

83. Prasad A, Prasad C. Short-term consumption of a diet rich in fat decreases anxiety response in adult male rats. Physiol Behav. 1996;60(3):1039–42. doi: 10.1016/0031-9384(96)00135-7 8873290

84. Gonda X, Pompili M, Serafini G, Carvalho AF, Rihmer Z, Dome P. The role of cognitive dysfunction in the symptoms and remission from depression. Ann Gen Psychiatry. 2015;14:27. doi: 10.1186/s12991-015-0068-9 26396586

85. Tangvarasittichai S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes. 2015;6(3):456. doi: 10.4239/wjd.v6.i3.456 25897356

86. Caricilli AM, Saad MJA. The role of gut microbiota on insulin resistance. Nutrients. 2013;5(3):829–51. doi: 10.3390/nu5030829 23482058

87. Deuschle M, Blum WF, Strasburger CJ, Weber B, Krner A, Standhardt H, et al. Insulin-like growth factor (IGF-I) plasma concentrations are increased in depressed patients. Psychoneuroendocrinology. 1997;22(7):493–503. doi: 10.1016/s0306-4530(97)00046-2 9373883

88. Bot M, Milaneschi Y, Penninx BWJH, Drent ML. Plasma insulin-like growth factor I levels are higher in depressive and anxiety disorders, but lower in antidepressant medication users. Psychoneuroendocrinology. 2016;68:148–55. doi: 10.1016/j.psyneuen.2016.02.028 26974499

89. Baldini S, Restani L, Baroncelli L, Coltelli M, Franco R, Cenni MC, et al. Enriched early life experiences reduce adult anxiety-like behavior in rats: a role for insulin-like growth factor 1. J Neurosci. 2013;33(28):11715–23. doi: 10.1523/JNEUROSCI.3541-12.2013 23843538

90. Mitschelen M, Yan H, Farley JA, Warrington JP, Han S, Hereñú CB, et al. Long-term deficiency of circulating and hippocampal insulin-like growth factor I induces depressive behavior in adult mice: a potential model of geriatric depression. Neuroscience. 2011;185:50–60. doi: 10.1016/j.neuroscience.2011.04.032 21524689

91. Hoshaw BA, Hill TI, Crowley JJ, Malberg JE, Khawaja X, Rosenzweig-Lipson S, et al. Antidepressant-like behavioral effects of IGF-I produced by enhanced serotonin transmission. Eur J Pharmacol. 2008;594(1–3):109–16. doi: 10.1016/j.ejphar.2008.07.023 18675266

92. Santi A, Bot M, Aleman A, Penninx BWJH, Aleman IT. Circulating insulin-like growth factor I modulates mood and is a biomarker of vulnerability to stress: from mouse to man. Transl Psychiatry. 2018;8(1):142. doi: 10.1038/s41398-018-0196-5 30068974

93. Ross AP, Bruggeman EC, Kasumu AW, Mielke JG, Parent MB. Non-alcoholic fatty liver disease impairs hippocampal-dependent memory in male rats. Physiol Behav. 2012;106(2):133–41. doi: 10.1016/j.physbeh.2012.01.008 22280920

94. Darling JN, Ross AP, Bartness TJ, Parent MB. Predicting the effects of a high-energy diet on fatty liver and hippocampal-dependent memory in male rats. Obesity. 2013;21(5):910–7. doi: 10.1002/oby.20167 23784893

95. Hargrave SL, Davidson TL, Zheng W, Kinzig KP. Western diets induce blood-brain barrier leakage and alter spatial strategies in rats. Behav Neurosci. 2016;130(1):123–35. doi: 10.1037/bne0000110 26595878

96. Boitard C, Cavaroc A, Sauvant J, Aubert A, Castanon N, Layé S, et al. Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain Behav Immun. 2014;40:9–17. doi: 10.1016/j.bbi.2014.03.005 24662056

97. Wang D, Yan J, Chen J, Wu W, Zhu X, Wang Y. Naringin improves neuronal insulin signaling, brain mitochondrial function, and cognitive function in high-fat diet-induced obese mice. Cell Mol Neurobiol. 2015;35(7):1061–71. doi: 10.1007/s10571-015-0201-y 25939427

98. Spencer SJ, D’Angelo H, Soch A, Watkins LR, Maier SF, Barrientos RM. High-fat diet and aging interact to produce neuroinflammation and impair hippocampal- and amygdalar-dpendent memory. Neurobiol Aging. 2017;58:88–101. doi: 10.1016/j.neurobiolaging.2017.06.014 28719855

99. Pintana H, Apaijai N, Pratchayasakul W, Chattipakorn N, Chattipakorn SC. Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats. Life Sci. 2012;91(11–12):409–14. doi: 10.1016/j.lfs.2012.08.017 22925597

100. Hu X, Wang T, Luo J, Liang S, Li W, Wu X, et al. Age-dependent effect of high cholesterol diets on anxiety-like behavior in elevated plus maze test in rats. Behav Brain Funct. 2014;10:30. doi: 10.1186/1744-9081-10-30 25179125

101. Wang Z, Fan J, Wang J, Li Y, Xiao L, Duan D, et al. Protective effect of lycopene on high-fat diet-induced cognitive impairment in rats. Neurosci Lett. 2016;627:185–91. doi: 10.1016/j.neulet.2016.05.014 27177726

102. de la Monte SM, Longato L, Tong M, Wands JR. Insulin resistance and neurodegeneration: roles of obesity, type 2 diabetes mellitus and non-alcoholic steatohepatitis. Curr Opin Investig Drugs. 2009;10(10):1049–60. 19777393

103. Egorin MJ, Yuan ZM, Sentz DL, Plaisance K, Eiseman JL. Plasma pharmacokinetics of butyrate after intravenous administration of sodium butyrate or oral administration of tributyrin or sodium butyrate to mice and rats. Cancer Chemother Pharmacol. 1999;43(6):445–53. doi: 10.1007/s002800050922 10321503

104. Schönfeld P, Wojtczak L. Short- and medium-chain fatty acids in energy metabolism: the cellular perspective. J Lipid Res. 2016;57(6):943–54. doi: 10.1194/jlr.R067629 27080715

105. Boets E, Gomand S V., Deroover L, Preston T, Vermeulen K, De Preter V, et al. Systemic availability and metabolism of colonic-derived short-chain fatty acids in healthy subjects: a stable isotope study. J Physiol. 2017;595(2):541–55. doi: 10.1113/JP272613 27510655

106. Hoyles L, Snelling T, Umlai UK, Nicholson JK, Carding SR, Glen RC, et al. Microbiome–host systems interactions: protective effects of propionate upon the blood–brain barrier. Microbiome. 2018;6(1):55. doi: 10.1186/s40168-018-0439-y 29562936

107. Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, et al. Acetate mediates a microbiome-brain-B cell axis promoting metabolic syndrome. Nature. 2016;534(7606):213–7. doi: 10.1038/nature18309 27279214

108. Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Oxidative stress, cardiolipin and mitochondrial dysfunction in nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20(39):14205–18. doi: 10.3748/wjg.v20.i39.14205 25339807

109. Méndez M, Méndez-López M, López L, Aller MÁ, Arias J, Arias JL. Basal and learning task-related brain oxidative metabolism in cirrhotic rats. Brain Res Bull. 2009;78(4–5):195–201. doi: 10.1016/j.brainresbull.2008.10.008 19015011

110. Arias N, Méndez M, Fidalgo C, Aller MÁ, Arias J, Arias JL. Mapping metabolic brain activity in three models of hepatic encephalopathy. Int J Hypertens. 2013;2013:390872. doi: 10.1155/2013/390872 23573412

111. Kolb B. Animal models for human PFC-related disorders. Prog Brain Res. 1990;85:501–19. doi: 10.1016/s0079-6123(08)62697-7 2094912

112. Wang GW, Cai JX. Disconnection of the hippocampal-prefrontal cortical circuits impairs spatial working memory performance in rats. Behav Brain Res. 2006;175(2):329–36. doi: 10.1016/j.bbr.2006.09.002 17045348

113. Gordon JA. Oscillations and hippocampal-prefrontal synchrony. Curr Opin Neurobiol. 2011;21(3):486–91. doi: 10.1016/j.conb.2011.02.012 21470846

114. Xia M, Liu T, Bai W, Zheng X, Tian X. Information transmission in HPC-PFC network for spatial working memory in rat. Behav Brain Res. 2019;356:170–8. doi: 10.1016/j.bbr.2018.08.024 30170031

115. Ito HT, Zhang SJ, Witter MP, Moser EI, Moser MB. A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation. Nature. 2015;522(7554):50–5. doi: 10.1038/nature14396 26017312

116. Griffin AL. Role of the thalamic nucleus reuniens in mediating interactions between the hippocampus and medial prefrontal cortex during spatial working memory. Front Syst Neurosci. 2015;9:29. doi: 10.3389/fnsys.2015.00029 25805977

117. Radyushkin K, Anokhin K, Meyer BI, Jiang Q, Alvarez-Bolado G, Gruss P. Genetic ablation of the mammillary bodies in the Foxb1 mutant mouse leads to selective deficit of spatial working memory. Eur J Neurosci. 2005;21(1):219–29. doi: 10.1111/j.1460-9568.2004.03844.x 15654859

118. Jha SK, Jha NK, Kumar D, Ambasta RK, Kumar P. Linking mitochondrial dysfunction, metabolic syndrome and stress signaling in Neurodegeneration. Biochim Biophys Acta—Mol Basis Dis. 2017;1863(5):1132–46. doi: 10.1016/j.bbadis.2016.06.015 27345267

119. Fusco S, Pani G. Brain response to calorie restriction. Cell Mol Life Sci. 2013;70(17):3157–70. doi: 10.1007/s00018-012-1223-y 23269433

120. Meunier CNJ, Chameau P, Fossier PM. Modulation of synaptic plasticity in the cortex needs to understand all the players. Front Synaptic Neurosci. 2017;9:2. doi: 10.3389/fnsyn.2017.00002 28203201

121. Harris KM, Weinberg RJ. Ultrastructure of synapses in the mammalian brain. Cold Spring Harb Perspect Biol. 2012;4(5):a005587. doi: 10.1101/cshperspect.a005587 22357909

122. Xing B, Li Y, Gao W-J. Norepinephrine versus dopamine and their interaction in modulating synaptic function in the prefrontal cortex. Brain Res. 2016;1641(Pt B):217–33. doi: 10.1016/j.brainres.2016.01.005 26790349

123. Kleinridders A, Cai W, Cappellucci L, Ghazarian A, Collins WR, Vienberg SG, et al. Insulin resistance in brain alters dopamine turnover and causes behavioral disorders. Proc Natl Acad Sci U S A. 2015;112(11):3463–8. doi: 10.1073/pnas.1500877112 25733901

124. Pidoplichko VI, Dani JA. Acid-sensitive ionic channels in midbrain dopamine neurons are sensitive to ammonium, which may contribute to hyperammonemia damage. Proc Natl Acad Sci U S A. 2006;103(30):11376–80. doi: 10.1073/pnas.0600768103 16847263

125. Ronan PJ, Gaikowski MP, Hamilton SJ, Buhl KJ, Summers CH. Ammonia causes decreased brain monoamines in fathead minnows (Pimephales promelas). Brain Res. 2007;1147(1):184–91.

126. Llansola M, Montoliu C, Cauli O, Hernández-Rabaza V, Agustí A, Cabrera-Pastor A, et al. Chronic hyperammonemia, glutamatergic neurotransmission and neurological alterations. Metab Brain Dis. 2013;28(2):151–4. doi: 10.1007/s11011-012-9337-3 23010935

127. Strandwitz P. Neurotransmitter modulation by the gut microbiota. Brain Res. 2018;1693(Pt B):128–33. doi: 10.1016/j.brainres.2018.03.015 29903615

128. Morris G, Berk M, Carvalho A, Caso JR, Sanz Y, Walder K, et al. 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. 2017;54(6):4432–51. doi: 10.1007/s12035-016-0004-2 27349436

129. Nestler EJ, Carlezon WA. The mesolimbic dopamine reward circuit in depression. Biol Psychiatry. 2006;59(12):1151–9. doi: 10.1016/j.biopsych.2005.09.018 16566899

130. Vaugeois JM, Pouhé D, Zuccaro F, Costentin J. Indirect dopamine agonists effects on despair test: Dissociation from hyperactivity. Pharmacol Biochem Behav. 1996;54(1):235–9. doi: 10.1016/0091-3057(95)02131-0 8728563

131. Fernández M, Mollinedo-Gajate I, Peñagarikano O. Neural circuits for social cognition- implications for autism. Neuroscience. 2018;370:148–62. doi: 10.1016/j.neuroscience.2017.07.013 28729065

132. Ott T, Nieder A. Dopamine and cognitive control in prefrontal cortex. Trends Cogn Sci. 2019;23(3):213–34. doi: 10.1016/j.tics.2018.12.006 30711326

133. Lammel S, Kook Lim B, Malenka RC. Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology. 2014;76(Pt B):351–9.

134. Kempadoo KA, Mosharov E V., Choi SJ, Kandel ER, Sulzer D. Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory. Proc Natl Acad Sci U S A. 2016;113(51):14835–40. doi: 10.1073/pnas.1616515114 27930324

135. Kolasiewicz W, Kuter K, Nowak P, Pastuszka A, Ossowska K. Lesion of the cerebellar noradrenergic innervation enhances the harmaline-induced tremor in rats. Cerebellum. 2011;10(2):267–80. doi: 10.1007/s12311-011-0250-9 21279489

136. Sokolov AA. The cerebellum in social cognition. Front Cell Neurosci. 2018;12(145):554–72.

137. Locke TM, Soden ME, Miller SM, Hunker A, Knakal C, Licholai JA, et al. Dopamine D1 receptor–positive neurons in the lateral nucleus of the cerebellum contribute to cognitive behavior. Biol Psychiatry. 2018;84(6):401–12. doi: 10.1016/j.biopsych.2018.01.019 29478701

138. Li Y, South T, Han M, Chen J, Wang R, Huang XF. High-fat diet decreases tyrosine hydroxylase mRNA expression irrespective of obesity susceptibility in mice. Brain Res. 2009;1268:181–9. doi: 10.1016/j.brainres.2009.02.075 19285041

139. Felger JC, Treadway MT. Inflammation effects on motivation and motor activity: role of dopamine. Neuropsychopharmacology. 2017;42(1):216–41. doi: 10.1038/npp.2016.143 27480574

140. Dandash O, Pantelis C, Fornito A. Dopamine, fronto-striato-thalamic circuits and risk for psychosis. Schizophr Res. 2016;180:48–57. doi: 10.1016/j.schres.2016.08.020 27595552

141. Gonzalo-Ruiz A, Alonso A, Sanz JM, Llinás RR. A dopaminergic projection to the rat mammillary nuclei demonstrated by retrograde transport of wheat germ agglutinin–horseradish peroxidase and tyrosine hydroxylase immunohistochemistry. J Comp Neurol. 1992;321(2):300–11. doi: 10.1002/cne.903210209 1380016

142. Del Campo N, Chamberlain SR, Sahakian BJ, Robbins TW. The roles of dopamine and noradrenaline in the pathophysiology and treatment of attention-deficit/hyperactivity disorder. Biol Psychiatry. 2011;69(12):e145–57. doi: 10.1016/j.biopsych.2011.02.036 21550021

143. Brenes JC, Rodríguez O, Fornaguera J. Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacol Biochem Behav. 2008;89(1):85–93. doi: 10.1016/j.pbb.2007.11.004 18096212

144. Felipo V, Butterworth RF. Neurobiology of ammonia. Prog Neurobiol. 2002;67(4):259–79. 12207972

145. Grippon P, le Poncin Lafitte M, Boschat M, Wang S, Faure G, Dutertre D, et al. Evidence for the role of ammonia in the intracerebral transfer and metabolism of tryptophan. Hepatology. 1986;6(4):682–6. doi: 10.1002/hep.1840060424 2426170


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#