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Journal of Neuroinflammation

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Open Access 01-12-2018 | Research

Effects of chronic noise exposure on the microbiome-gut-brain axis in senescence-accelerated prone mice: implications for Alzheimer’s disease

Authors: Bo Cui, Donghong Su, Wenlong Li, Xiaojun She, Ming Zhang, Rui Wang, Qingfeng Zhai

Published in: Journal of Neuroinflammation | Issue 1/2018

Abstract

Background

Chronic noise exposure is associated with neuroinflammation and gut microbiota dysregulation and increases the risk of Alzheimer’s disease (AD). Environmental hazards are also thought to be associated with genetic susceptibility factors that increase AD pathogenesis. However, there is limited experimental evidence regarding the link between chronic noise stress and microbiome-gut-brain axis alterations, which may be closely related to AD development.

Methods

The aim of the present study was to systematically investigate the effects of chronic noise exposure on the microbiome-gut-brain axis in the senescence-accelerated mouse prone 8 (SAMP8) strain. We established SAMP8 mouse models to examine the consequences of noise exposure on the microbiome-gut-brain axis. Hippocampal amyloid-β (Aβ) assessment and the Morris water maze were used to evaluate AD-like changes, 16S ribosomal RNA sequencing analyses were used for intestinal flora measurements, and assessment of endothelial tight junctions and serum neurotransmitter and inflammatory mediator levels, as well as fecal microbiota transplant, was conducted to explore the underlying pathological mechanisms.

Results

Chronic noise exposure led to cognitive impairment and Aβ accumulation in young SAMP8 mice, similar to that observed in aging SAMP8 mice. Noise exposure was also associated with decreased gut microbiota diversity and compositional alterations. Axis-series studies showed that endothelial tight junction proteins were decreased in both the intestine and brain, whereas serum neurotransmitter and inflammatory mediator levels were elevated in young SAMP8 mice exposed to chronic noise, similar to the observations made in the aging group. The importance of intestinal bacteria in noise exposure-induced epithelial integrity impairment and Aβ accumulation was further confirmed through microbiota transplantation experiments. Moreover, the effects of chronic noise were generally intensity-dependent.

Conclusion

Chronic noise exposure altered the gut microbiota, accelerated age-related neurochemical and inflammatory dysregulation, and facilitated AD-like changes in the brain of SAMP8 mice.

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Blennow K, de Leon MJ, Zetterberg H. Alzheimer’s disease. Lancet. 2006;368:387–403.CrossRefPubMed

Gandy S. Perspective: prevention is better than cure. Nature. 2011;475:S15.CrossRefPubMedPubMedCentral

Hirtz D, Thurman DJ, Gwinn-Hardy K, Mohamed M, Chaudhuri AR, Zalutsky R. How common are the “common” neurologic disorders? Neurology. 2007;68:326–37.CrossRefPubMed

Wainaina MN, Chen Z, Zhong C. Environmental factors in the development and progression of late-onset Alzheimer’s disease. Neurosci Bull. 2014;30(2):253–70.CrossRefPubMedPubMedCentral

Cheng L, Wang SH, Chen QC, Liao XM. Moderate noise induced cognition impairment of mice and its underlying mechanisms. Physio Behav. 2011;104:981–8.CrossRef

Cui B, Zhu L, She X, Wu M, Ma Q, Wang T, Liu H. Chronic noise exposure causes persistence of tau hyperphosphorylation and formation of nft tau in the rat hippocampus and prefrontal cortex. Exp Neurol. 2012;238:122–9.CrossRefPubMed

Cui B, Wu MQ, Zhu L, She X, Ma Q, Liu H. Effect of chronic noise exposure on expression of N-methyl-D-aspartic acid receptor 2B and tau phosphorylation in hippocampus of rats. Biomed Environ Sci. 2013;26:163–8.PubMed

Cui B, Li K, Gai Z, She X, Zhang N, Xu C, Chen X, An G, Ma Q, Wang R. Chronic noise exposure acts cumulatively to exacerbate Alzheimer’s disease-like amyloid-β pathology and neuroinflammation in the rat hippocampus. Sci Rep. 2015;5:12943.CrossRefPubMedPubMedCentral

Manikandan S, Padma MK, Srikumar R, Jeya Parthasarathy N, Muthuvel A, Sheela Devi R. Effects of chronic noise stress on spatial memory of rats in relation to neuronal dendritic alteration and free radical-imbalance in hippocampus and medial prefrontal cortex. Neurosci Lett. 2006;399:17–22.CrossRefPubMed

10.

Hooper LV, Gordon JI. Commensal host-bacterial relationships in the gut. Science. 2001;292:1115–8.CrossRefPubMed

11.

Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701–12.CrossRefPubMed

12.

Cryan JF, O’Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011;23:187–92.CrossRefPubMed

13.

Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, Green JA. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe. 2010;16:444–53.CrossRefPubMed

14.

Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linløkken A, Wilson R, Rudi K. Correlation between the human fecal microbiota and depression. Neurogastroenterol Motil. 2014;26:1155–62.CrossRefPubMed

15.

Scheperjans F, Aho V, Pereira PA, Koskinen K, Paulin L, Pekkonen E, Auvinen P. Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov Disord. 2015;30:350–8.CrossRefPubMed

16.

Lanctôt KL, Herrmann N, Mazzotta P, Khan LR, Ingber N. GABAergic function in Alzheimer’s disease: evidence for dysfunction and potential as a therapeutic target for the treatment of behavioural and psychological symptoms of dementia. Can J Psychiatr. 2004;49:439–53.CrossRef

17.

Cui B, Wu M, She X. Effects of chronic noise exposure on spatial learning and memory of rats in relation to neurotransmitters and NMDAR2B alteration in the hippocampus. J Occup Health. 2009;51:152–8.CrossRefPubMed

18.

Ravindran R, Rathinasamy SD, Samson J, Senthilvelan M. Noise-stress-induced brain neurotransmitter changes and the effect of Ocimum sanctum (Linn) treatment in albino rats. J Pharmacol Sci. 2005;98:354–60.CrossRefPubMed

19.

Cui B, Gai Z, She X, Wang R, Xi Z. Effects of chronic noise on glucose metabolism and gut microbiota-host inflammatory homeostasis in rats. Sci Rep. 2016;6:36693.CrossRefPubMedPubMedCentral

20.

Cowan TE, Palmnäs MS, Yang J, Bomhof MR, Ardell KL, Reimer RA, Shearer J. Chronic coffee consumption in the diet-induced obese rat: impact on gut microbiota and serum metabolomics. J Nutr Biochem. 2014;25:489–95.CrossRefPubMed

21.

Christensen JS, Raaschou NO, Tjønneland A, Nordsborg RB, Jensen SS, Sørensen TI, Sørensen M. Long-term exposure to residential traffic noise and changes in body weight and waist circumference: a cohort study. Environ Res. 2015;143:154–61.CrossRefPubMed

22.

Christensen JS, Raaschou NO, Tjønneland A, Overvad K, Nordsborg RB, Ketzel M, Sørensen M. Road traffic and railway noise exposures and adiposity in adults: a cross-sectional analysis of the danish diet, cancer, and health cohort. Environ Health Perspect. 2016;124:329–35.PubMedCrossRef

23.

Gur TL, Bailey MT. Effects of stress on commensal microbes and immune system activity. Adv Exp Med Biol. 2016;874:289–300.PubMed

24.

Sørensen M, Andersen ZJ, Nordsborg RB, Becker T, Tjønneland A, Overvad K, Raaschou-Nielsen O. Long-term exposure to road traffic noise and incident diabetes: a cohort study. Environ Health Perspect. 2013;121:217–22.PubMedCrossRef

25.

Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 2009;10:434–45.CrossRefPubMed

26.

Issa AM, Rowe W, Gauthier S, Meaney MJ. Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J Neurosci. 1990;10:3247–54.CrossRefPubMed

27.

Lupien SJ, Nair NP, Brière S, Maheu F, Tu MT, Lemay M, Meaney MJ. Increased cortisol levels and impaired cognition in human aging: implication for depression and dementia in later life. Rev Neurosci. 1999;10:117–39.CrossRefPubMed

28.

Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, Costea PI, Godneva A, Kalka IN, Bar N, et al. Environment dominates over host genetics in haping human gut microbiota. Nature. 2018;555:210–5.CrossRefPubMed

29.

Franceschi C. Inflammaging as a major characteristic of old people: can it be prevented or cured? Nutr Rev. 2007;65:S173–6.CrossRefPubMed

30.

Guigoz Y, Doré J, Schiffrin EJ. The inflammatory status of old age can be nurtured from the intestinal environment. Curr Opin Clin Nutr Metab Care. 2008;11:13–20.CrossRefPubMed

31.

O’Toole PW, Claesson MJ. Gut microbiota: changes throughout the lifespan from infancy to elderly. Int Dairy J. 2010;20:281–91.CrossRef

32.

Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, De VW. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One. 2010;5:e10667.CrossRefPubMedPubMedCentral

33.

Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, O’Toole PW. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488:178–84.CrossRefPubMed

34.

Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C. Gamma-aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol. 2012;113:411–7.CrossRefPubMed

35.

Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, Hsiao EY. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell. 2015;161:264–76.CrossRefPubMedPubMedCentral

36.

Matsumoto M, Kibe R, Ooga T, Aiba Y, Sawaki E, Koga Y, Benno Y. Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study. Front Syst Neurosci. 2013;7:9.CrossRefPubMedPubMedCentral

37.

Solas M, Puerta E, Ramirez MJ. Treatment options in Alzheimer’s disease: the GABA story. Curr Pharm Des. 2015;21:4960–71.CrossRefPubMed

38.

Spiegel K, Tasali E, Leproult R, Van Cauter E. Effects of poor and short sleep on glucose metabolism and obesity risk. Nat Rev Endocrinol. 2009;5:253–61.CrossRefPubMedPubMedCentral

39.

Tasali E, Leproult R, Ehrmann DA, Van Cauter E. Slow-wave sleep and the risk of type 2 diabetes in humans. Proc Natl Acad Sci U S A. 2008;105:1044–9.CrossRefPubMedPubMedCentral

40.

Tasali E, Leproult R, Spiegel K. Reduced sleep duration or quality: relationships with insulin resistance and type 2 diabetes. Prog Cardiovasc Dis. 2009;51:381–91.CrossRefPubMed

41.

Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol. 1986;103:755–66.CrossRefPubMed

42.

Cappuccio FP, D’Elia L, Strazzullo P, Miller MA. Quantity and quality of sleep and incidence of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care. 2010;33:414–20.CrossRefPubMed

43.

Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009;9:799–809.CrossRefPubMed

44.

Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burceli R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470–81.CrossRefPubMed

45.

Kahn MS, Kranjac D, Alonzo CA, Haase JH, Cedillos RO, McLinden KA, Chumley MJ. Prolonged elevation in hippocampal Aβ and cognitive deficits following repeated endotoxin exposure in the mouse. Behav Brain Res. 2012;229:176–84.CrossRefPubMed

46.

Zhang R, Miller RG, Gascon R, Champion S, Katz J, Lancero M, McGrath MS. Circulating endotoxin and systemic immune activation in sporadic amyotrophic lateral sclerosis (sALS). J Neuroimmunol. 2009;206:121–4.CrossRefPubMed

47.

Bajaj JS, Hylemon PB, Ridlon JM, Heuman DM, Daita K, White MB, Gillevet PM. Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am J Physiol Gastrointest Liver Physiol. 2012;303:G675–85.CrossRefPubMedPubMedCentral

48.

Yunes RA, Poluektova EU, Dyachkova MS, Klimina KM, Kovtun AS, Averina OV, Danilenko VN. GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strainsfrom human microbiota. Anaerobe. 2016;42:197–204.CrossRefPubMed

49.

de Theije CG, Wopereis H, Ramadan M, van Eijndthoven T, Lambert J, Knol J, Oozeer R. Altered gut microbiota and activity in a murine model of autism spectrum disorders. Brain Behav Immun. 2014;37:197–206.CrossRefPubMed

50.

Turner JG, Parrish JL, Hughes LF, Toth LA, Caspary DM. Hearing in laboratory animals: strain differences and nonauditory effects of noise. Comp Med. 2005;55(1):12–23.PubMedPubMedCentral

Title: Effects of chronic noise exposure on the microbiome-gut-brain axis in senescence-accelerated prone mice: implications for Alzheimer’s disease
Authors: Bo Cui
Donghong Su
Wenlong Li
Xiaojun She
Ming Zhang
Rui Wang
Qingfeng Zhai
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: Journal of Neuroinflammation / Issue 1/2018
Electronic ISSN: 1742-2094
DOI: https://doi.org/10.1186/s12974-018-1223-4

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Effects of chronic noise exposure on the microbiome-gut-brain axis in senescence-accelerated prone mice: implications for Alzheimer’s disease

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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