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Open Access

The modulatory effect of oolong tea polyphenols on intestinal flora and hypothalamus gene expression in a circadian rhythm disturbance mouse model

Ruonan YanaChi-Tang Hob( )Yanan LiuaShengnan ZhanaZufang WuaXin Zhanga ( )
Department of Food Science and Engineering, Ningbo University, Ningbo 315211, China
Department of Food Science, Rutgers University, New Brunswick, New Jersey 08901, USA

Peer review under responsibility of Tsinghua University Press.

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Highlights

• OTP modulated the disrupted composition and function of gut microbiota induced by circadian rhythm disorder.

• OTP benefited the intestinal environment and the release of certain beneficial metabolites.

• OTP enhanced the expression of circadian rhythm genes in hypothalamic cells.

• OTP may serve as a promising dietary therapeutic strategy for treating circadian rhythm disorders and cognitive impairment.

Graphical Abstract

Abstract

The interaction between host circadian rhythm and gut microbes through the gut-brain axis provides new clues for tea polyphenols to improve host health. Our present research showed that oolong tea polyphenols (OTP) improved the structural disorder of the intestinal flora caused by continuous darkness, thereby modulating the production of metabolites related to pyruvate metabolism, glycolysis/gluconeogenesis, and tryptophan metabolism to alleviate the steady-state imbalance. After fecal microbiota transplantation from the OTP group, the single-cell transcriptomic analysis revealed that OTP significantly increased the number of hypothalamus cell clusters, up-regulated the number of astrocytes and fibroblasts, and enhanced the expression of circadian rhythm genes Cry2, Per3, Bhlhe41, Nr1d1, Nr1d2, Dbp and Rorb in hypothalamic cells. Our results confirmed that OTP can actively improve the intestinal environmental state as well as internal/peripheral circadian rhythm disorders and cognitive impairment, with potential prebiotic functional characteristics to notably contribute to host health.

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References

[1]

J. Husse, G. Eichele, H. Oster, Synchronization of the mammalian circadian timing system: light can control peripheral clocks independently of the SCN clock: alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time, BioEssays 37 (2015) 1119-1128. http://doi.org/10.1002/bies.201500026.

[2]

R.N. Yan, C.T. Ho, X. Zhang, Interaction between tea polyphenols and intestinal microbiota in host metabolic diseases from the perspective of the gut-brain axis, Mol. Nutr. Food Res. 64 (2020) 2000187. http://doi.org/10.1002/mnfr.202000187.

[3]

E.S. Musiek, D.M. Holtzman, Mechanisms linking circadian clocks, sleep, and neurodegeneration, Science 354 (2016) 1004-1008. http://doi.org/10.1126/science.aah4968.

[4]

N. Goel, M. Basner, H. Rao et al., Circadian rhythms, sleep deprivation, and human performance, Prog. Mol. Biol. Transl. Sci. 119 (2013) 155-190. http://doi.org/10.1016/B978-0-12-396971-2.00007-5.

[5]

R. Dallmann, A.U. Viola, L. Tarokh, et al., The human circadian metabolome, Proc. Natl. Acad. Sci. U.S.A. 109 (2012) 2625-2629. http://doi.org/10.1073/pnas.1114410109.

[6]

D. Song, C.S. Yang, X. Zhang et al., The relationship between host circadian rhythms and intestinal microbiota: a new cue to improve health by tea polyphenols, Crit. Rev. Food Sci. Nutr. 61 (2021) 139-148. http://doi.org/10.1080/10408398.2020.1719473.

[7]

C.L. Gentile, T.L. Weir, The gut microbiota at the intersection of diet and human health, Science 362 (2018) 776-780. http://doi.org/10.1126/science.aau5812.

[8]

J.Y. Wu, K. Wang, X.M. Wang, et al., The role of the gut microbiome and its metabolites in metabolic diseases, Protein Cell 12 (2021) 360-373. http://doi.org/10.1007/s13238-020-00814-7.

[9]

H.E. Vuong, J.M. Yano, T.C. Fung, et al., The microbiome and host behavior, Annu. Rev. Neurosci. 40 (2017) 21-49. http://doi.org/10.1146/annurev-neuro-072116-031347.

[10]

S.M. Jandhyala, R. Talukdar, C. Subramanyam, et al., Role of the normal gut microbiota, World J. Gastroenterol. 21 (2015) 8787-8803. http://doi.org/10.3748/wjg.v21.i29.8787.

[11]

G.Y. Qi, Y.S. Mi, Z.G. Liu, et al., Dietary tea polyphenols ameliorate metabolic syndrome and memory impairment via circadian clock related mechanisms, J. Funct. Foods 34 (2017) 168-180. http://doi.org/10.1016/j.jff.2017.04.031.

[12]

M. Zhang, X. Zhang, C.T. Ho, et al., Chemistry and health effect of tea polyphenol (–)-epigallocatechin 3-O-(3-O-Methyl) gallate, J. Agric. Food Chem. 67 (2019) 5374-5378. http://doi.org/10.1021/acs.jafc.8b04837.

[13]

T. Guo, C.T. Ho, X. Zhang, et al., Oolong tea polyphenols ameliorate circadian rhythm of intestinal microbiome and liver clock genes in mouse model, J. Agric. Food Chem. 67 (2019) 11969-11976. http://doi.org/10.1021/acs.jafc.9b04869.

[14]

X. Zhang, Y.H. Chen, J.Y. Zhu, et al., Metagenomics analysis of gut microbiota in a high fat diet-induced obesity mouse model fed with (–)-epigallocatechin 3-O-(3-O-Methyl) gallate (EGCG3”Me), Mol. Nutr. Food Res. 62 (2018) e1800274. http://doi.org/10.1002/mnfr.201800274.

[15]

Q.Q. Hou, S.M. Zhang, Y. Li, et al., New insights on association between circadian rhythm and lipid metabolism in spontaneously hypertensive rats, Life Sci. 271 (2021) 119145. http://doi.org/10.1016/j.lfs.2021.119145.

[16]

B. Hwang, J.H. Lee, D. Bang, Single-cell RNA sequencing technologies and bioinformatics pipelines, Exp. Mol. Med. 50 (2018) 1-14. http://doi.org/10.1038/s12276-018-0071-8.

[17]

M. Cheng, X. Zhang, J.Y. Zhu, et al., Metagenomics analysis of gut microbiota modulatory effect of green tea polyphenols by high fat diet-induced obesity mice model, J. Func. Foods 46 (2018) 268-277. http://doi.org/10.1039/c7fo01570d.

[18]

T.T. Guo, D. Song, C.T. Ho, et al., Omics analyses of gut microbiota in a circadian rhythm disorder mouse model fed with oolong tea polyphenols, J. Agric. Food Chem. 67 (2019) 8847-8854. http://doi.org/10.1021/acs.jafc.9b03000.

[19]

B.S.Y. Choi, N. Daniel, V.P. Houde, et al., Feeding diversified protein sources exacerbates hepatic insulin resistance via increased gut microbial branched-chain fatty acids and mTORC1 signaling in obese mice, Nat. Commun. 12 (2021) 3377. http://doi.org/10.1038/s41467-021-23782-w.

[20]

H. Khan, H. Ulla, M. Aschner, et al., Neuroprotective effects of quercetin in Alzheimer’s disease, Biomolecules 10 (2019) 59. http://doi.org/10.3390/biom10010059.

[21]

E.J. Want, I.D. Wilson, H. Gika, et al., Global metabolic profiling procedures for urine using UPLC-MS, Nat. Protoc. 5 (2010) 1005-1018. http://doi.org/10.1038/nprot.2010.50.

[22]

X.S. Zhu, H. D. Li, L.L. Guo, et al., Analysis of single-cell RNA-seq data by clustering approaches, Curr. Bioinform. 14 (2019) 314-322. http://doi.org/10.2174/1574893614666181120095038.

[23]

J.C. Dunlap, J.J. Loros, Yes, circadian rhythms actually do affect almost everything, Cell Res. 26 (2016) 759-760. http://doi.org/10.1038/cr.2016.65.

[24]

S. Yamazaki, R. Numano, M. Abe, et al., Resetting central and peripheral circadian oscillators in transgenic rats, Science 288 (2000) 682-685. http://doi.org/10.1126/science.288.5466.682.

[25]

S.G. Parkar, A. Kalsbeek, J.F. Cheeseman, Potential role for the gut microbiota in modulating host circadian rhythms and metabolic health, Microorganisms 7 (2019) 41. http://doi.org/10.3390/microorganisms7020041.

[26]

C.A. Thaiss, D. Zeevi, M. Levy, et al., Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis, Cell 159 (2014) 514-529. http://doi.org/10.1016/j.cell.2014.09.048.

[27]

C. Duclos, M. Dumont, J. Paquet, et al., Sleep-wake disturbances in hospitalized patients with traumatic brain injury: association with brain trauma but not with an abnormal melatonin circadian rhythm, Sleep 43 (2020) zsz191. http://doi.org/10.1093/sleep/zsz191.

[28]

L.M. C. Wang, J.M. Dragich, T. Kudo, et al., Expression of the circadian clock gene Period2 in the hippocampus: possible implications for synaptic plasticity and learned behaviour, ASN Neuro. 1 (2009) e00012. http://doi.org/10.1042/AN20090020.

[29]

K. Cho, Chronic ‘jet lag’ produces temporal lobe atrophy and spatial cognitive deficits, Nat. Neurosci. 4 (2001) 567-568. http://doi.org/10.1038/88384.

[30]

R. Biasibetti, A.C. Tramontina, A.P. Costa, et al., Green tea (–) epigallocatechin-3-gallate reverses oxidative stress and reduces acetylcholinesterase activity in a streptozotocin-induced model of dementia, Behav. Brain Res. 236 (2013) 186-193. http://doi.org/10.1016/j.bbr.2012.08.039.

[31]

R.M. Voigt, C.B. Forsyth, S.J. Green, et al., Circadian disorganization alters intestinal microbiota, PLoS One 9 (2014) e97500. http://doi.org/10.1371/journal.pone.0097500.

[32]

S. Piao, Z. Zhu, S. Tan, et al., An integrated fecal microbiome and metabolome in the aged mice reveal anti-aging effects from the intestines and biochemical mechanism of FuFang zhenshu TiaoZhi (FTZ), Biomed. Pharmacother. 121 (2020) 109421. http://doi.org/10.1016/j.biopha.2019.109421.

[33]

B.J. Smith, R.A. Miller, A.C. Ericsson, et al., Changes in the gut microbiome and fermentation products concurrent with enhanced longevity in acarbose-treated mice, BMC Microbiol. 19 (2019) 130. http://doi.org/10.1186/s12866-019-1494-7.

[34]

G. den Besten, K. van Eunen, A.K. Groen, et al., The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism, J. Lipid Res. 54 (2013) 2325-2340. http://doi.org/10.1194/jlr.R036012.

[35]

M. van de Wouw, M. Boehme, J.M. Lyte, et al., Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain-gut axis alterations, J. Physiol. 596 (2018) 4923-4944. http://doi.org/10.1113/JP276431.

[36]

J. Rutter, M. Reick, S.L. Mcknight, Metabolism and the control of circadian rhythms, Annu. Rev. Biochem. 71 (2002) 307-331. http://doi.org/10.1146/annurev.biochem.71.090501.142857.

[37]

Y. Tahara, M. Yamazaki, H. Sukigara, et al., Gut microbiota-derived short chain fatty acids induce circadian clock entrainment in mouse peripheral tissue, Sci. Rep. 8 (2018) 1395. http://doi.org/10.1038/s41598-018-19836-7.

[38]

A. Agus, J. Planchais, H. Sokol, Gut microbiota regulation of tryptophan metabolism in health and disease, Cell Host Microbe. 23 (2018) 716-724. http://doi.org/10.1016/j.chom.2018.05.003.

[39]

T. Tsukahara, Y. Matsuda, H. Haniu, Lysophospholipid-related diseases and PPARγ signaling pathway, Int. J. Mol. Sci. 18 (2017) 2730. http://doi.org/10.3390/ijms18122730.

[40]

A.M. Wiedeman, Dietary choline intake: current state of knowledge across the life cycle, Nutrients 10 (2018) 1513. http://doi.org/10.3390/nu10101513.

[41]

K. Ide, N. Matsuoka, H. Yamada, et al., Effects of tea catechins on Alzheimer’s disease: recent updates and perspectives, Molecules 23 (2018) 2357. http://doi.org/10.3390/molecules23092357.

[42]

X. Zhang, F.F.K. Choi, Y. Zhou, et al., Metabolite profiling of plasma and urine from rats with TNBS-induced acute colitis using UPLC-ESI-QTOF-MS-based metabonomics--a pilot study, FEBS J. 279 (2012) 2322-2338. http://doi.org/10.1111/j.1742-4658.2012.08612.x.

[43]

B.J. Deters, M. Saleem, The role of glutamine in supporting gut health and neuropsychiatric factors, Food Sci. Hum. Well. 10 (2021) 149-154. http://doi.org/10.1016/j.fshw.2021.02.003.

[44]

A.Z.Z. de Souza, A.Z. Zambom, K.Y. Abboud, et al., Oral supplementation with L-glutamine alters gut microbiota of obese and overweight adults: a pilot study, Nutrition 31 (2015) 884-889. http://doi.org/10.1016/j.nut.2015.01.004.

[45]

Y.H. Zhu, F. Huan, J.F. Wang, et al., 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine induced Parkinson’s disease in mouse: potential association between neurotransmitter disturbance and gut microbiota dysbiosis, ACS. Chem. Neurosci. 11 (2020) 3366-3376. http://doi.org/10.1021/acschemneuro.0c00475.

[46]

L.R. Gray, S.C. Tompkins, E.B. Taylor, Regulation of pyruvate metabolism and human disease, Cell Mol. Life Sci. 71 (2014) 2577-2604. http://doi.org/10.1007/s00018-013-1539-2.

[47]

A. Mukherji, S.M. Bailey, B. Staels, et al., The circadian clock and liver function in health and disease, J. Hepatol. 71 (2019) 200-211. http://doi.org/10.1016/j.jhep.2019.03.020.

[48]

B.A. Matenchuk, P.J. Mandhane, A.L. Kozyrskyj, Sleep, circadian rhythm, and gut microbiota, Sleep Med. Rev. 53 (2020) 101340. http://doi.org/10.1016/j.smrv.2020.101340.

[49]

A. Videnovic, A.S. Lazar, R.A. Barker, et al., ‘The clocks that time us’--circadian rhythms in neurodegenerative disorders, Nat. Rev. Neurol. 10 (2014) 683-693. http://doi.org/10.1038/nrneurol.2014.206.

[50]

G.K. Paschos, G.A. Fitzgerald. Circadian clocks and metabolism: Implications for microbiome and aging. Trends Genet. 33 (2017) 760-769. http://10.1016/j.tig.2017.07.010.

[51]

X. Pan, Y. Zhang, L. Wang, et al., Diurnal regulation of MTP and plasma triglyceride by CLOCK is mediated by SHP. Cell Metab. 12 (2010) 174-186. http://10.1016/j.cmet.2010.05.014.

[52]

E.S. Musiek, M.M. Lim, G. Yang, et al., Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration, J. Clin. Invest. 123 (2013) 5389-5400. http://doi.org/10.1172/JCI70317.

[53]

X.N. Han, M. Chen, F.S. Wang, et al., Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice, Cell Stem. Cell 12 (2013) 342-353. http://doi.org/10.1016/j.stem.2012.12.015.

[54]

P. Wasling, J. Daborg, I. Riebe, et al., Synaptic retrogenesis and amyloid-beta in Alzheimer’s disease, J. Alzheimers Dis. 16 (2009) 1-14. http://doi.org/10.3233/JAD-2009-0918.

[55]

M. Brancaccio, M.D. Edwards, A.P. Patton, et al., Cell-autonomous clock of astrocytes drives circadian behavior in mammals, Science 363 (2019) 187-192. http://doi.org/10.1126/science.aat4104.

Food Science and Human Wellness
Pages 748-764
Cite this article:
Yan R, Ho C-T, Liu Y, et al. The modulatory effect of oolong tea polyphenols on intestinal flora and hypothalamus gene expression in a circadian rhythm disturbance mouse model. Food Science and Human Wellness, 2024, 13(2): 748-764. https://doi.org/10.26599/FSHW.2022.9250064

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Received: 27 April 2022
Revised: 31 July 2022
Accepted: 09 August 2022
Published: 25 September 2023
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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