Skip to main content
Top
Published in: Environmental Health and Preventive Medicine 1/2020

Open Access 01-12-2020 | Alzheimer's Disease | Research article

Transcriptome analysis of the hippocampus in environmental noise-exposed SAMP8 mice reveals regulatory pathways associated with Alzheimer’s disease neuropathology

Authors: Donghong Su, Wenlong Li, Huimin Chi, Honglian Yang, Xiaojun She, Kun Wang, Xiujie Gao, Kefeng Ma, Ming Zhang, Bo Cui

Published in: Environmental Health and Preventive Medicine | Issue 1/2020

Login to get access

Abstract

Background

Chronic noise exposure is one environmental hazard that is associated with genetic susceptibility factors that increase Alzheimer’s disease (AD) pathogenesis. However, the comprehensive understanding of the link between chronic noise stress and AD is limited. Herein, we investigated the effects of chronic noise exposure on AD-like changes in senescence-accelerated mouse prone 8 (SAMP8).

Methods

A total of 30 male SAMP8 mice were randomly divided into the noise-exposed group, the control group, and aging group (positive controls), and mice in the exposure group were exposed to 98 dB SPL white noise for 30 consecutive days. Transcriptome analysis and AD-like neuropathology of hippocampus were examined by RNA sequencing and immunoblotting. Enzyme-linked immunosorbent assay and real-time PCR were used to further determine the differential gene expression and explore the underlying mechanisms of chronic noise exposure in relation to AD at the genome level.

Results

Chronic noise exposure led to amyloid beta accumulation and increased the hyperphosphorylation of tau at the Ser202 and Ser404 sites in young SAMP8 mice; similar observations were noted in aging SAMP8 mice. We identified 21 protein-coding transcripts that were differentially expressed: 6 were downregulated and 15 were upregulated after chronic noise exposure; 8 genes were related to AD. qPCR results indicated that the expression of Arc, Egr1, Egr2, Fos, Nauk1, and Per2 were significantly high in the noise exposure group. These outcomes mirrored the results of the RNA sequencing data.

Conclusions

These findings further revealed that chronic noise exposure exacerbated aging-like impairment in the hippocampus of the SAMP8 mice and that the protein-coding transcripts discovered in the study may be key candidate regulators involved in environment-gene interactions.
Appendix
Available only for authorised users
Literature
1.
go back to reference Querfurth HW, LaFerla FM. Alzheimer’s disease. N Engl J Med. 2010;362:329–44.CrossRef Querfurth HW, LaFerla FM. Alzheimer’s disease. N Engl J Med. 2010;362:329–44.CrossRef
2.
go back to reference Cui B, Li K. Chronic noise exposure and Alzheimer disease: is there an etiological association? Med Hypotheses. 2013;81:623–6.CrossRef Cui B, Li K. Chronic noise exposure and Alzheimer disease: is there an etiological association? Med Hypotheses. 2013;81:623–6.CrossRef
3.
go back to reference Gandy S. Perspective: prevention is better than cure. Nature. 2011;475:S15.CrossRef Gandy S. Perspective: prevention is better than cure. Nature. 2011;475:S15.CrossRef
4.
go back to reference Sotiropoulos I, Cerqueira JJ, Catania C, Takashima A, Sousa N, Almeida OFX. Stress and glucocorticoid footprints in the brain-the path from depression to Alzheimer’s disease. Neurosci Biobehav Rev. 2008;32:1161–73.CrossRef Sotiropoulos I, Cerqueira JJ, Catania C, Takashima A, Sousa N, Almeida OFX. Stress and glucocorticoid footprints in the brain-the path from depression to Alzheimer’s disease. Neurosci Biobehav Rev. 2008;32:1161–73.CrossRef
5.
go back to reference Lupien SJ, Nair NPV, Briére S, Maheu F, Tu MT, Lemay Μ. Increased cortisol levels and impaired cognition in human aging: implication for depression and dementia in later life. Rev Neurosci. 1999;10:117–39.CrossRef Lupien SJ, Nair NPV, Briére S, Maheu F, Tu MT, Lemay Μ. Increased cortisol levels and impaired cognition in human aging: implication for depression and dementia in later life. Rev Neurosci. 1999;10:117–39.CrossRef
6.
go back to reference Fjell AM, Mcevoy L, Holland D, Dale AM, Walhovd KB, Alzheimer's Disease Neuroimaging Initiative. What is normal in normal aging? Effects of aging, amyloid and Alzheimer’s disease on the cerebral cortex and the hippocampus. Prog Neurobiol. 2014;117:20–40.CrossRef Fjell AM, Mcevoy L, Holland D, Dale AM, Walhovd KB, Alzheimer's Disease Neuroimaging Initiative. What is normal in normal aging? Effects of aging, amyloid and Alzheimer’s disease on the cerebral cortex and the hippocampus. Prog Neurobiol. 2014;117:20–40.CrossRef
7.
go back to reference Ma Q, Qiang J, Gu P, Wang Y, Geng Y, Wang M. Age-related autophagy alterations in the brain of senescence accelerated mouse prone 8(SAMP8) mice. Exp Gerontol. 2011;46:533–41.CrossRef Ma Q, Qiang J, Gu P, Wang Y, Geng Y, Wang M. Age-related autophagy alterations in the brain of senescence accelerated mouse prone 8(SAMP8) mice. Exp Gerontol. 2011;46:533–41.CrossRef
8.
go back to reference Wyss-Coray T. Ageing, neurodegeneration and brain rejuvenation. Nature. 2016;539:180–6.CrossRef Wyss-Coray T. Ageing, neurodegeneration and brain rejuvenation. Nature. 2016;539:180–6.CrossRef
9.
go back to reference Elobeid A, Libard S, Leino M, Popova SN, Alafuzoff I. Altered proteins in the aging brain. J Neuropathol Exp Neurol. 2016;75:316–25.CrossRef Elobeid A, Libard S, Leino M, Popova SN, Alafuzoff I. Altered proteins in the aging brain. J Neuropathol Exp Neurol. 2016;75:316–25.CrossRef
10.
go back to reference Basner M, Babisch W, Davis A, Brink M, Clark C, Janssen S, Stansfeld S. Auditory and non-auditory effects of noise on health. Lancet. 2014;383(9925):1325–32.CrossRef Basner M, Babisch W, Davis A, Brink M, Clark C, Janssen S, Stansfeld S. Auditory and non-auditory effects of noise on health. Lancet. 2014;383(9925):1325–32.CrossRef
11.
go back to reference 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.CrossRef 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.CrossRef
12.
go back to reference Cui B, Zhu L, She X, Wu M, Ma Q, Wang T. 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.CrossRef Cui B, Zhu L, She X, Wu M, Ma Q, Wang T. 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.CrossRef
13.
go back to reference Cui B, Su D, Li W, She X, Zhang M, Wang R, Zhai Q. Effects of chronic noise exposure on the microbiome-gut-brain axis in senescence-accelerated prone mice: implications for Alzheimer’s disease. J Neuroinflammation. 2018;15:190.CrossRef Cui B, Su D, Li W, She X, Zhang M, Wang R, Zhai Q. Effects of chronic noise exposure on the microbiome-gut-brain axis in senescence-accelerated prone mice: implications for Alzheimer’s disease. J Neuroinflammation. 2018;15:190.CrossRef
14.
go back to reference Gai Z, Su D, Wang Y, Li W, Cui B, Li K, She X, Wang R. Effects of chronic noise on the corticotropin-releasing factor system in the rat hippocampus: relevance to Alzheimer’s disease-like tau hyperphosphorylation. Environ Health Prev Med. 2017;22:79.CrossRef Gai Z, Su D, Wang Y, Li W, Cui B, Li K, She X, Wang R. Effects of chronic noise on the corticotropin-releasing factor system in the rat hippocampus: relevance to Alzheimer’s disease-like tau hyperphosphorylation. Environ Health Prev Med. 2017;22:79.CrossRef
15.
go back to reference Chen H, Kwong JC, Copes R, Tu K, Villeneuve PJ, Van DA, Hystad P, Martin RV, Muttay BJ, Jessiman B, Wilton AS, Kopp A, Burnett R. Living near major roads and the incidence of dementia, Parkinson’s disease, and multiple sclerosis: a population-based cohort study. Lancet. 2017;389:718–26.CrossRef Chen H, Kwong JC, Copes R, Tu K, Villeneuve PJ, Van DA, Hystad P, Martin RV, Muttay BJ, Jessiman B, Wilton AS, Kopp A, Burnett R. Living near major roads and the incidence of dementia, Parkinson’s disease, and multiple sclerosis: a population-based cohort study. Lancet. 2017;389:718–26.CrossRef
16.
go back to reference Clark C, Paunovic K. Who environmental noise guidelines for the European region: a systematic review on environmental noise and cognition. Int J Environ Res Public Health. 2018;15:285.CrossRef Clark C, Paunovic K. Who environmental noise guidelines for the European region: a systematic review on environmental noise and cognition. Int J Environ Res Public Health. 2018;15:285.CrossRef
17.
go back to reference Zhang S, Zhu D, Li H, Li H, Feng C, Zhang W. Characterization of circRNA-associated-ceRNA networks in a senescence-accelerated mouse prone 8 brain. Mol. Ther. 2017;25:2053–61.CrossRef Zhang S, Zhu D, Li H, Li H, Feng C, Zhang W. Characterization of circRNA-associated-ceRNA networks in a senescence-accelerated mouse prone 8 brain. Mol. Ther. 2017;25:2053–61.CrossRef
18.
go back to reference Kang L, Li S, Xing Z, Li J, Su Y, Fan P. Dihydrotestosterone treatment delays the conversion from mild cognitive impairment to Alzheimer’s disease in SAMP8 mice. Horm Behav. 2014;65:505–15.CrossRef Kang L, Li S, Xing Z, Li J, Su Y, Fan P. Dihydrotestosterone treatment delays the conversion from mild cognitive impairment to Alzheimer’s disease in SAMP8 mice. Horm Behav. 2014;65:505–15.CrossRef
19.
go back to reference Li K, Jia H, She X, Cui B, Zhang N, Chen X, Xu C, An G, Ma Q. Role of NMDA receptors in noise-induced tau hyperphosphorylation in rat hippocampus and prefrontal cortex. J Neurol Sci. 2014;340:191–7.CrossRef Li K, Jia H, She X, Cui B, Zhang N, Chen X, Xu C, An G, Ma Q. Role of NMDA receptors in noise-induced tau hyperphosphorylation in rat hippocampus and prefrontal cortex. J Neurol Sci. 2014;340:191–7.CrossRef
20.
go back to reference Cui B, Li K, Gai Z, She X, Zhang N, Xu C. 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.CrossRef Cui B, Li K, Gai Z, She X, Zhang N, Xu C. 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.CrossRef
21.
go back to reference Zhang S, Qin C, Cao G, Guo L, Feng C, Zhang W. Genome-wide analysis of DNA methylation profiles in a senescence-accelerated mouse prone 8 brain using whole-genome bisulfite sequencing. Bioinformatics. 2017;33:1591–5.PubMed Zhang S, Qin C, Cao G, Guo L, Feng C, Zhang W. Genome-wide analysis of DNA methylation profiles in a senescence-accelerated mouse prone 8 brain using whole-genome bisulfite sequencing. Bioinformatics. 2017;33:1591–5.PubMed
22.
go back to reference Wang S, Yu Y, Feng Y, Zou F, Zhang X, Huang J, Zhang Y, Zheng X, Huang XF, Zhu Y, Liu Y. Protective effect of the orientin on noise-induced cognitive impairments in mice. Behav Brain Res. 2015;296:290–300.CrossRef Wang S, Yu Y, Feng Y, Zou F, Zhang X, Huang J, Zhang Y, Zheng X, Huang XF, Zhu Y, Liu Y. Protective effect of the orientin on noise-induced cognitive impairments in mice. Behav Brain Res. 2015;296:290–300.CrossRef
23.
go back to reference Cui B, Wu M, She X, Liu H. Impulse noise exposure in rats causes cognitive deficits and changes in hippocampal neurotransmitter signaling and tau phosphorylation. Brain Res. 2012;1427:35–43.CrossRef Cui B, Wu M, She X, Liu H. Impulse noise exposure in rats causes cognitive deficits and changes in hippocampal neurotransmitter signaling and tau phosphorylation. Brain Res. 2012;1427:35–43.CrossRef
24.
go back to reference Ali F, Hossain MS, Sejimo S, Akashi K. Plasmalogens inhibit endocytosis of toll-like receptor 4 to attenuate the inflammatory signal in microglial cells. Mol Neurobiol. 2019;56(5):3404–19.CrossRef Ali F, Hossain MS, Sejimo S, Akashi K. Plasmalogens inhibit endocytosis of toll-like receptor 4 to attenuate the inflammatory signal in microglial cells. Mol Neurobiol. 2019;56(5):3404–19.CrossRef
25.
go back to reference Tarkowski E, Liljeroth AM, Minthon L, Tarkowski A, Wallin A, Blennow K. Cerebral pattern of pro- and anti-inflammatory cytokines in dementias. Brain Res Bull. 2003;61:255–60.CrossRef Tarkowski E, Liljeroth AM, Minthon L, Tarkowski A, Wallin A, Blennow K. Cerebral pattern of pro- and anti-inflammatory cytokines in dementias. Brain Res Bull. 2003;61:255–60.CrossRef
26.
go back to reference Sly LM, Krzesicki RF, Brashler JR, Buhl AE, McKinley DD, Carter DB, Chin JE. Endogenous brain cytokine mRNA and inflammatory responses to lipopolysaccharide are elevated in the Tg2576 transgenic mouse model of Alzheimer’s disease. Brain Res Bull. 2001;56:581–8.CrossRef Sly LM, Krzesicki RF, Brashler JR, Buhl AE, McKinley DD, Carter DB, Chin JE. Endogenous brain cytokine mRNA and inflammatory responses to lipopolysaccharide are elevated in the Tg2576 transgenic mouse model of Alzheimer’s disease. Brain Res Bull. 2001;56:581–8.CrossRef
27.
go back to reference Ghasemi R, Zarifkar A, Rastegar K, Maghsoudi N, Moosavi M. Insulin protects against Abeta-induced spatial memory impairment, hippocampal apoptosis and MAPKs signaling disruption. Neuropharmacology. 2014;85:113–20.CrossRef Ghasemi R, Zarifkar A, Rastegar K, Maghsoudi N, Moosavi M. Insulin protects against Abeta-induced spatial memory impairment, hippocampal apoptosis and MAPKs signaling disruption. Neuropharmacology. 2014;85:113–20.CrossRef
28.
go back to reference Cui B, Wu MQ, Zhu LX, She XJ, Ma Q, Liu HT. 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, Wu MQ, Zhu LX, She XJ, Ma Q, Liu HT. 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
29.
go back to reference Dickson DW. Apoptotic mechanisms in Alzheimer neurofibrillary degeneration: cause or effect? J Clin Invest. 2004;114:23–7.CrossRef Dickson DW. Apoptotic mechanisms in Alzheimer neurofibrillary degeneration: cause or effect? J Clin Invest. 2004;114:23–7.CrossRef
30.
31.
go back to reference Lu W, Mi R, Tang H, Liu S, Fan M, Wang L. Over-expression of c-fos mRNA in the hippocampal neurons in Alzheimer’s disease. Chin Med J. 1998;111:35–7.PubMed Lu W, Mi R, Tang H, Liu S, Fan M, Wang L. Over-expression of c-fos mRNA in the hippocampal neurons in Alzheimer’s disease. Chin Med J. 1998;111:35–7.PubMed
32.
go back to reference Zhang P, Hirsch EC, Damier P, Duyckaerts C, Javoy-Agid F. c-fos protein-like immunoreactivity: distribution in the human brain and over-expression in the hippocampus of patients with Alzheimer’s disease. Neuroscience. 1992;46:9–21.CrossRef Zhang P, Hirsch EC, Damier P, Duyckaerts C, Javoy-Agid F. c-fos protein-like immunoreactivity: distribution in the human brain and over-expression in the hippocampus of patients with Alzheimer’s disease. Neuroscience. 1992;46:9–21.CrossRef
33.
go back to reference Morin JP, Cerón-Solano G, Velázquez-Campos G, Pacheco-López G, Bermúdez-Rattoni F, Díaz-Cintra S. Spatial memory impairment is associated with intraneural amyloid-β immunoreactivity and dysfunctional arc expression in the hippocampal-CA3 region of a transgenic mouse model of Alzheimer’s disease. J Alzheimers Dis. 2016;51:69–79.CrossRef Morin JP, Cerón-Solano G, Velázquez-Campos G, Pacheco-López G, Bermúdez-Rattoni F, Díaz-Cintra S. Spatial memory impairment is associated with intraneural amyloid-β immunoreactivity and dysfunctional arc expression in the hippocampal-CA3 region of a transgenic mouse model of Alzheimer’s disease. J Alzheimers Dis. 2016;51:69–79.CrossRef
34.
go back to reference von der Kammer H, Demiralay C, Andresen B, Albrecht C, Mayhaus M, Nitsch RM. Regulation of gene expression by muscarinic acetylcholine receptors. Biochem Soc Symp. 2001;67:131–40.CrossRef von der Kammer H, Demiralay C, Andresen B, Albrecht C, Mayhaus M, Nitsch RM. Regulation of gene expression by muscarinic acetylcholine receptors. Biochem Soc Symp. 2001;67:131–40.CrossRef
35.
go back to reference Leduc V, Théroux L, Dea D, Dufour R, Poirer J. Effects of rs3846662 variants on HMGCR mRNA and protein levels and on markers of Alzheimer’s disease pathology. J Mol Neurosci. 2016;58:109–19.CrossRef Leduc V, Théroux L, Dea D, Dufour R, Poirer J. Effects of rs3846662 variants on HMGCR mRNA and protein levels and on markers of Alzheimer’s disease pathology. J Mol Neurosci. 2016;58:109–19.CrossRef
36.
go back to reference Yin Z, Raj D, Saiepour N, Van Dam D, Brouwer N, Holtman IR, Eggen BJL, Möller T, Tamm JA, Abdourahman A, Hol EM, Kamphuis W, Bayer TA, De Deyn PP, Boddeke E. Immune hyperreactivity of Aβ plaque-associated microglia in Alzheimer’s disease. Neurobiol Aging. 2017;55:115–22.CrossRef Yin Z, Raj D, Saiepour N, Van Dam D, Brouwer N, Holtman IR, Eggen BJL, Möller T, Tamm JA, Abdourahman A, Hol EM, Kamphuis W, Bayer TA, De Deyn PP, Boddeke E. Immune hyperreactivity of Aβ plaque-associated microglia in Alzheimer’s disease. Neurobiol Aging. 2017;55:115–22.CrossRef
37.
go back to reference Macgibbon GA, Lawlor PA, Walton M, Sirimanne E, Faull RLM, Synek B, Mee E, Connor B, Draqunow M. Expression of Fos, Jun, and Krox family proteins in Alzheimer’s disease. Exp Neurol. 1997;147:316–32.CrossRef Macgibbon GA, Lawlor PA, Walton M, Sirimanne E, Faull RLM, Synek B, Mee E, Connor B, Draqunow M. Expression of Fos, Jun, and Krox family proteins in Alzheimer’s disease. Exp Neurol. 1997;147:316–32.CrossRef
38.
go back to reference Lu Y, Li T, Qureshi HY, Han D, Paudel HK. Early growth response 1 (Egr-1) regulates phosphorylation of microtubule-associated protein tau in mammalian brain. J Biol Chem. 2011;286:20569–81.CrossRef Lu Y, Li T, Qureshi HY, Han D, Paudel HK. Early growth response 1 (Egr-1) regulates phosphorylation of microtubule-associated protein tau in mammalian brain. J Biol Chem. 2011;286:20569–81.CrossRef
39.
go back to reference Yang GZ, Yang M, Lim Y, Lu JJ, Wang TH, Qi JG, Zhong JH, Zhou XF. Huntingtin associated protein 1 regulates trafficking of the amyloid precursor protein and modulates amyloid beta levels in neurons. J Neurochem. 2012;122:1010–22.CrossRef Yang GZ, Yang M, Lim Y, Lu JJ, Wang TH, Qi JG, Zhong JH, Zhou XF. Huntingtin associated protein 1 regulates trafficking of the amyloid precursor protein and modulates amyloid beta levels in neurons. J Neurochem. 2012;122:1010–22.CrossRef
40.
go back to reference Gai Z, Li K, Sun H, She X, Cui B, Wang R. Effects of chronic noise on mRNA and protein expression of CRF family molecules and its relationship with p-tau in the rat prefrontal cortex. J Neurol Sci. 2016;368:307–13.CrossRef Gai Z, Li K, Sun H, She X, Cui B, Wang R. Effects of chronic noise on mRNA and protein expression of CRF family molecules and its relationship with p-tau in the rat prefrontal cortex. J Neurol Sci. 2016;368:307–13.CrossRef
Metadata
Title
Transcriptome analysis of the hippocampus in environmental noise-exposed SAMP8 mice reveals regulatory pathways associated with Alzheimer’s disease neuropathology
Authors
Donghong Su
Wenlong Li
Huimin Chi
Honglian Yang
Xiaojun She
Kun Wang
Xiujie Gao
Kefeng Ma
Ming Zhang
Bo Cui
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Environmental Health and Preventive Medicine / Issue 1/2020
Print ISSN: 1342-078X
Electronic ISSN: 1347-4715
DOI
https://doi.org/10.1186/s12199-019-0840-6

Other articles of this Issue 1/2020

Environmental Health and Preventive Medicine 1/2020 Go to the issue