Faecalibacterium prausnitzii Supplementation Prevents Intestinal Barrier Injury and Gut Microflora Dysbiosis Induced by Sleep Deprivation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animal and Experimental Design
2.2. Probiotic Culture
2.3. Hematoxylin and Eosin (H&E) Staining
2.4. AB-PAS Staining
2.5. Immunohistochemical Staining
2.6. Real-Time Reverse Transcription-Polymerase Chain Reaction (RT-PCR)
2.7. Enzyme-Linked Immunosorbent Assay (ELISA)
2.8. Gut Microbiota Analysis
2.9. Detection of SCFAs Using Ion Chromatography
2.10. Statistical Analysis
3. Results
3.1. F. prausnitzii Colonization Alleviated Intestinal Mucosal Barrier Disruption Induced by SD
3.2. The Colonization of F. prausnitzii Suppressed the Production of Inflammatory Cytokines in SD Mice
3.3. Colonization of F. prausnitzii Mitigated Gut Microbiota Dysbiosis Induced by SD in Mice
3.4. F. prausnitzii Colonization Alleviated Colon SCFAs Reduction in SD Mice
3.5. F. prausnitzii Colonization Reduced Intestinal Apoptosis Level Induced by SD
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Kroese, F.M.; Evers, C.; Adriaanse, M.A.; de Ridder, D.T.D. Bedtime procrastination: A self-regulation perspective on sleep insufficiency in the general population. J. Health Psychol. 2016, 21, 853–862. [Google Scholar] [CrossRef] [PubMed]
- Zamore, Z.; Veasey, S.C. Neural consequences of chronic sleep disruption. Trends Neurosci. 2022, 45, 678–691. [Google Scholar] [CrossRef]
- Neroni, B.; Evangelisti, M.; Radocchia, G.; Di Nardo, G.; Pantanella, F.; Villa, M.P.; Schippa, S. Relationship between sleep disorders and gut dysbiosis: What affects what? Sleep. Med. 2021, 87, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Zeng, Y.; Zhang, Z.; Liang, S.; Chang, X.; Qin, R.; Chen, H.; Guo, L. Paternal sleep deprivation induces metabolic perturbations in male offspring via altered LRP5 DNA methylation of pancreatic islets. J. Pineal Res. 2023, 74, e12863. [Google Scholar] [CrossRef]
- Fang, D.; Xu, T.; Sun, J.; Shi, J.; Li, F.; Yin, Y.; Wang, Z.; Liu, Y. Nicotinamide Mononucleotide Ameliorates Sleep Deprivation-Induced Gut Microbiota Dysbiosis and Restores Colonization Resistance against Intestinal Infections. Adv. Sci. 2023, 10, e2207170. [Google Scholar] [CrossRef]
- Martel, J.; Chang, S.H.; Ko, Y.F.; Hwang, T.L.; Young, J.D.; Ojcius, D.M. Gut barrier disruption and chronic disease. Trends Endocrinol. Metab. 2022, 33, 247–265. [Google Scholar] [CrossRef]
- Cani, P.D.; Jordan, B.F. Gut microbiota-mediated inflammation in obesity: A link with gastrointestinal cancer. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 671–682. [Google Scholar] [CrossRef] [PubMed]
- Gong, Y.; Xia, W.; Wen, X.; Lyu, W.; Xiao, Y.; Yang, H.; Zou, X. Early inoculation with caecal fermentation broth alters small intestine morphology, gene expression of tight junction proteins in the ileum, and the caecal metabolomic profiling of broilers. J. Anim. Sci. Biotechnol. 2020, 11, 8. [Google Scholar] [CrossRef]
- Carloni, S.; Bertocchi, A.; Mancinelli, S.; Bellini, M.; Erreni, M.; Borreca, A.; Braga, D.; Giugliano, S.; Mozzarelli, A.M.; Manganaro, D.; et al. Identification of a choroid plexus vascular barrier closing during intestinal inflammation. Science 2021, 374, 439–448. [Google Scholar] [CrossRef]
- Chen, H.; Wang, C.; Bai, J.; Song, J.; Bu, L.; Liang, M.; Suo, H. Targeting microbiota to alleviate the harm caused by sleep deprivation. Microbiol. Res. 2023, 275, 127467. [Google Scholar] [CrossRef]
- Gao, T.; Wang, Z.; Dong, Y.; Cao, J.; Lin, R.; Wang, X.; Yu, Z.; Chen, Y. Role of melatonin in sleep deprivation-induced intestinal barrier dysfunction in mice. J. Pineal Res. 2019, 67, e12574. [Google Scholar] [CrossRef] [PubMed]
- Horowitz, A.; Chanez-Paredes, S.D.; Haest, X.; Turner, J.R. Paracellular permeability and tight junction regulation in gut health and disease. Nat. Rev. Gastroenterol. Hepatol. 2023, 20, 417–432. [Google Scholar] [CrossRef] [PubMed]
- Duan, J.; Matute, J.D.; Unger, L.W.; Hanley, T.; Schnell, A.; Lin, X.; Krupka, N.; Griebel, P.; Lambden, C.; Sit, B.; et al. Endoplasmic reticulum stress in the intestinal epithelium initiates purine metabolite synthesis and promotes Th17 cell differentiation in the gut. Immunity 2023, 56, 1115–1131.e9. [Google Scholar] [CrossRef] [PubMed]
- Pontarollo, G.; Kollar, B.; Mann, A.; Khuu, M.P.; Kiouptsi, K.; Bayer, F.; Brandão, I.; Zinina, V.V.; Hahlbrock, J.; Malinarich, F.; et al. Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling. Nat. Metab. 2023, 5, 1174–1187. [Google Scholar] [CrossRef] [PubMed]
- Doré, E.; Joly-Beauparlant, C.; Morozumi, S.; Mathieu, A.; Lévesque, T.; Allaeys, I.; Duchez, A.C.; Cloutier, N.; Leclercq, M.; Bodein, A.; et al. The interaction of secreted phospholipase A2-IIA with the microbiota alters its lipidome and promotes inflammation. JCI Insight 2022, 7, e152638. [Google Scholar] [CrossRef]
- Lopez-Siles, M.; Duncan, S.H.; Garcia-Gil, L.J.; Martinez-Medina, M. Faecalibacterium prausnitzii: From microbiology to diagnostics and prognostics. ISME J. 2017, 11, 841–852. [Google Scholar] [CrossRef] [PubMed]
- Lopez-Siles, M.; Martinez-Medina, M.; Abellà, C.; Busquets, D.; Sabat-Mir, M.; Duncan, S.H.; Aldeguer, X.; Flint, H.J.; Garcia-Gil, L.J. Mucosa-associated Faecalibacterium prausnitzii phylotype richness is reduced in patients with inflammatory bowel disease. Appl. Environ. Microbiol. 2015, 81, 7582–7592. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.; Ou, R.; Tang, N.; Su, W.; Yang, R.; Yu, X.; Zhang, G.; Jiao, J.; Zhou, X. Alternation of the gut microbiota in irritable bowel syndrome: An integrated analysis based on multicenter amplicon sequencing data. J. Transl. Med. 2023, 21, 117. [Google Scholar] [CrossRef]
- Ueda, A.; Shinkai, S.; Shiroma, H.; Taniguchi, Y.; Tsuchida, S.; Kariya, T.; Kawahara, T.; Kobayashi, Y.; Kohda, N.; Ushida, K.; et al. Identification of Faecalibacterium prausnitzii strains for gut microbiome-based intervention in Alzheimer’s-type dementia. Cell Rep. Med. 2021, 2, 100398. [Google Scholar] [CrossRef]
- Khan, M.T.; Dwibedi, C.; Sundh, D.; Pradhan, M.; Kraft, J.D.; Caesar, R.; Tremaroli, V.; Lorentzon, M.; Bäckhed, F. Synergy and oxygen adaptation for development of next-generation probiotics. Nature 2023, 620, 381–385. [Google Scholar] [CrossRef]
- Zhang, L.; Liu, C.; Jiang, Q.; Yin, Y. Butyrate in Energy Metabolism: There Is Still More to Learn. Trends Endocrinol. Metab. 2021, 32, 159–169. [Google Scholar] [CrossRef] [PubMed]
- Liang, L.; Liu, L.; Zhou, W.; Yang, C.; Mai, G.; Li, H.; Chen, Y. Gut microbiota-derived butyrate regulates gut mucus barrier repair by activating the macrophage/WNT/ERK signaling pathway. Clin. Sci. 2022, 136, 291–307. [Google Scholar] [CrossRef] [PubMed]
- Song, Q.; Cheng, S.W.; Zou, J.; Li, K.S.L.; Cheng, H.; Wai Lau, D.T.; Han, Q.; Yang, X.; Shaw, P.C.; Zuo, Z. Role of gut microbiota on regulation potential of Dendrobium officinale Kimura & Migo in metabolic syndrome: In-vitro fermentation screening and in-vivo verification in db/db mice. J. Ethnopharmacol. 2024, 321, 117437. [Google Scholar] [PubMed]
- Li, H.B.; Xu, M.L.; Xu, X.D.; Tang, Y.Y.; Jiang, H.L.; Li, L.; Xia, W.J.; Cui, N.; Bai, J.; Dai, Z.M.; et al. Faecalibacterium prausnitzii Attenuates CKD via Butyrate-Renal GPR43 Axis. Circ. Res. 2022, 131, e120–e134. [Google Scholar] [CrossRef] [PubMed]
- Pan, W.; Zhao, J.; Wu, J.; Xu, D.; Meng, X.; Jiang, P.; Shi, H.; Ge, X.; Yang, X.; Hu, M.; et al. Dimethyl itaconate ameliorates cognitive impairment induced by a high-fat diet via the gut-brain axis in mice. Microbiome 2023, 11, 30. [Google Scholar]
- Ma, L.; Shen, Q.; Lyu, W.; Lv, L.; Wang, W.; Yu, M.; Yang, H.; Tao, S.; Xiao, Y. Clostridium butyricum and Its Derived Extracellular Vesicles Modulate Gut Homeostasis and Ameliorate Acute Experimental Colitis. Microbiol. Spectr. 2022, 10, e0136822. [Google Scholar] [CrossRef]
- Wu, J.; Lin, Z.; Wang, X.; Zhao, Y.; Zhao, J.; Liu, H.; Johnston, L.J.; Lu, L.; Ma, X. Limosilactobacillus reuteri SLZX19-12 Protects the Colon from Infection by Enhancing Stability of the Gut Microbiota and Barrier Integrity and Reducing Inflammation. Microbiol. Spectr. 2022, 10, e0212421. [Google Scholar] [CrossRef]
- Palmer, C.A.; Bower, J.L.; Cho, K.W.; Clementi, M.A.; Lau, S.; Oosterhoff, B.; Alfano, C.A. Sleep loss and emotion: A systematic review and meta-analysis of over 50 years of experimental research. Psychol. Bull. 2023. [Google Scholar] [CrossRef]
- Hyun, M.K.; Baek, Y.; Lee, S. Association between digestive symptoms and sleep disturbance: A cross-sectional community-based study. BMC Gastroenterol. 2019, 19, 34. [Google Scholar] [CrossRef] [PubMed]
- Sang, D.; Lin, K.; Yang, Y.; Ran, G.; Li, B.; Chen, C.; Li, Q.; Ma, Y.; Lu, L.; Cui, X.Y.; et al. Prolonged sleep deprivation induces a cytokine-storm-like syndrome in mammals. Cell 2023, 186, 5500–5516.e21. [Google Scholar] [CrossRef]
- Touch, S.; Godefroy, E.; Rolhion, N.; Danne, C.; Oeuvray, C.; Straube, M.; Galbert, C.; Brot, L.; Alonso Salgueiro, I.; Chadi, S.; et al. Human CD4+CD8α+ Tregs induced by Faecalibacterium prausnitzii protect against intestinal inflammation. JCI Insight 2022, 7, e154722. [Google Scholar] [CrossRef] [PubMed]
- Li, N.; Tan, S.; Wang, Y.; Deng, J.; Wang, N.; Zhu, S.; Tian, W.; Xu, J.; Wang, Q. Akkermansia muciniphila supplementation prevents cognitive impairment in sleep-deprived mice by modulating microglial engulfment of synapses. Gut Microbes. 2023, 15, 2252764. [Google Scholar] [CrossRef] [PubMed]
- Furter, M.; Sellin, M.E.; Hansson, G.C.; Hardt, W.D. Mucus Architecture and Near-Surface Swimming Affect Distinct Salmonella Typhimurium Infection Patterns along the Murine Intestinal Tract. Cell Rep. 2019, 27, 2665–2678.e2663. [Google Scholar] [CrossRef] [PubMed]
- McLoughlin, K.; Schluter, J.; Rakoff-Nahoum, S.; Smith, A.L.; Foster, K.R. Host Selection of Microbiota via Differential Adhesion. Cell Host Microbe. 2016, 19, 550–559. [Google Scholar] [CrossRef] [PubMed]
- Birchenough, G.M.H.; Schroeder, B.O.; Sharba, S.; Arike, L.; Recktenwald, C.V.; Puértolas-Balint, F.; Subramani, M.V.; Hansson, K.T.; Yilmaz, B.; Lindén, S.K.; et al. Muc2-dependent microbial colonization of the jejunal mucus layer is diet sensitive and confers local resistance to enteric pathogen infection. Cell Rep. 2023, 42, 112084. [Google Scholar] [CrossRef] [PubMed]
- Turpin, W.; Lee, S.H.; Raygoza Garay, J.A.; Madsen, K.L.; Meddings, J.B.; Bedrani, L.; Power, N.; Espin-Garcia, O.; Xu, W.; Smith, M.I.; et al. Increased Intestinal Permeability Is Associated with Later Development of Crohn’s Disease. Gastroenterology 2020, 159, 2092–2100.e2095. [Google Scholar] [CrossRef] [PubMed]
- Pedersen, T.K.; Brown, E.M.; Plichta, D.R.; Johansen, J.; Twardus, S.W.; Delorey, T.M.; Lau, H.; Vlamakis, H.; Moon, J.J.; Xavier, R.J.; et al. The CD4(+) T cell response to a commensal-derived epitope transitions from a tolerant to an inflammatory state in Crohn’s disease. Immunity 2022, 55, 1909–1923.e6. [Google Scholar] [CrossRef] [PubMed]
- Carlsson, A.H.; Yakymenko, O.; Olivier, I.; Håkansson, F.; Postma, E.; Keita, A.V.; Söderholm, J.D. Faecalibacterium prausnitzii supernatant improves intestinal barrier function in mice DSS colitis. Scand. J. Gastroenterol. 2013, 48, 1136–1144. [Google Scholar] [CrossRef] [PubMed]
- Martin, R.M.; Bachman, M.A. Colonization, Infection, and the Accessory Genome of Klebsiella pneumoniae. Front. Cell Infect. Microbiol. 2018, 8, 4. [Google Scholar] [CrossRef]
- Zhang, Q.; Su, X.; Zhang, C.; Chen, W.; Wang, Y.; Yang, X.; Liu, D.; Zhang, Y.; Yang, R. Klebsiella pneumoniae Induces Inflammatory Bowel Disease Through Caspase-11-Mediated IL18 in the Gut Epithelial Cells. Cell Mol. Gastroenterol. Hepatol. 2023, 15, 613–632. [Google Scholar] [CrossRef]
- Wasfi, R.; Hamed, S.M.; Amer, M.A.; Fahmy, L.I. Proteus mirabilis Biofilm: Development and Therapeutic Strategies. Front. Cell Infect. Microbiol. 2020, 10, 414. [Google Scholar] [CrossRef]
- Zhou, X.; Lu, J.; Wei, K.; Wei, J.; Tian, P.; Yue, M.; Wang, Y.; Hong, D.; Li, F.; Wang, B.; et al. Neuroprotective Effect of Ceftriaxone on MPTP-Induced Parkinson’s Disease Mouse Model by Regulating Inflammation and Intestinal Microbiota. Oxid. Med. Cell Longev. 2021, 2021, 9424582. [Google Scholar] [CrossRef] [PubMed]
- Howden, B.P.; Giulieri, S.G.; Wong Fok Lung, T.; Baines, S.L.; Sharkey, L.K.; Lee, J.Y.H.; Hachani, A.; Monk, I.R.; Stinear, T.P. Staphylococcus aureus host interactions and adaptation. Nat. Rev. Microbiol. 2023, 21, 380–395. [Google Scholar] [CrossRef] [PubMed]
- Cani, P.D.; Depommier, C.; Derrien, M.; Everard, A.; de Vos, W.M. Akkermansia muciniphila: Paradigm for next-generation beneficial microorganisms. Nat. Rev. Gastroenterol. Hepatol. 2022, 19, 625–637. [Google Scholar] [CrossRef] [PubMed]
- Lukovac, S.; Belzer, C.; Pellis, L.; Keijser, B.J.; de Vos, W.M.; Montijn, R.C.; Roeselers, G. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio 2014, 5, e01438-14. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Kang, R.; Tang, D. Lipopolysaccharide delivery systems in innate immunity. Trends Immunol. 2024. [Google Scholar] [CrossRef] [PubMed]
- Lai, J.L.; Liu, Y.H.; Liu, C.; Qi, M.P.; Liu, R.N.; Zhu, X.F.; Zhou, Q.G.; Chen, Y.Y.; Guo, A.Z.; Hu, C.M. Indirubin Inhibits LPS-Induced Inflammation via TLR4 Abrogation Mediated by the NF-kB and MAPK Signaling Pathways. Inflammation 2017, 40, 1–12. [Google Scholar] [CrossRef]
- Ju, M.; Liu, B.; He, H.; Gu, Z.; Liu, Y.; Su, Y.; Zhu, D.; Cang, J.; Luo, Z. MicroRNA-27a alleviates LPS-induced acute lung injury in mice via inhibiting inflammation and apoptosis through modulating TLR4/MyD88/NF-κB pathway. Cell Cycle 2018, 17, 2001–2018. [Google Scholar] [CrossRef]
- Zhou, L.; Zhang, M.; Wang, Y.; Dorfman, R.G.; Liu, H.; Yu, T.; Chen, X.; Tang, D.; Xu, L.; Yin, Y.; et al. Faecalibacterium prausnitzii Produces Butyrate to Maintain Th17/Treg Balance and to Ameliorate Colorectal Colitis by Inhibiting Histone Deacetylase 1. Inflamm Bowel Dis. 2018, 24, 1926–1940. [Google Scholar] [CrossRef]
- Gao, T.; Wang, Z.; Dong, Y.; Cao, J.; Chen, Y. Melatonin-Mediated Colonic Microbiota Metabolite Butyrate Prevents Acute Sleep Deprivation-Induced Colitis in Mice. Int. J. Mol. Sci. 2021, 22, 11894. [Google Scholar] [CrossRef]
- Singh, V.; Lee, G.; Son, H.; Koh, H.; Kim, E.S.; Unno, T.; Shin, J.H. Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics. Front. Microbiol. 2022, 13, 1103836. [Google Scholar] [CrossRef]
- Fu, X.; Liu, Z.; Zhu, C.; Mou, H.; Kong, Q. Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria. Crit. Rev. Food Sci. Nutr. 2019, 59, S130–S152. [Google Scholar] [CrossRef]
- Recharla, N.; Geesala, R.; Shi, X.Z. Gut Microbial Metabolite Butyrate and Its Therapeutic Role in Inflammatory Bowel Disease: A Literature Review. Nutrients 2023, 15, 2275. [Google Scholar] [CrossRef]
- Chen, Y.; Liu, Y.; Wang, Y.; Chen, X.; Wang, C.; Chen, X.; Yuan, X.; Liu, L.; Yang, J.; Zhou, X. Prevotellaceae produces butyrate to alleviate PD-1/PD-L1 inhibitor-related cardiotoxicity via PPARα-CYP4X1 axis in colonic macrophages. J. Exp. Clin. Cancer Res. 2022, 41, 1. [Google Scholar] [CrossRef]
- Couto, M.R.; Gonçalves, P.; Magro, F.; Martel, F. Microbiota-derived butyrate regulates intestinal inflammation: Focus on inflammatory bowel disease. Pharmacol. Res. 2020, 159, 104947. [Google Scholar] [CrossRef]
- Martín, R.; Rios-Covian, D.; Huillet, E.; Auger, S.; Khazaal, S.; Bermúdez-Humarán, L.G.; Sokol, H.; Chatel, J.M.; Langella, P. Faecalibacterium: A bacterial genus with promising human health applications. FEMS Microbiol. Rev. 2023, 47, fuad039. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, X.; Li, Y.; Wang, X.; Wang, R.; Hao, Y.; Ren, F.; Wang, P.; Fang, B. Faecalibacterium prausnitzii Supplementation Prevents Intestinal Barrier Injury and Gut Microflora Dysbiosis Induced by Sleep Deprivation. Nutrients 2024, 16, 1100. https://doi.org/10.3390/nu16081100
Wang X, Li Y, Wang X, Wang R, Hao Y, Ren F, Wang P, Fang B. Faecalibacterium prausnitzii Supplementation Prevents Intestinal Barrier Injury and Gut Microflora Dysbiosis Induced by Sleep Deprivation. Nutrients. 2024; 16(8):1100. https://doi.org/10.3390/nu16081100
Chicago/Turabian StyleWang, Xintong, Yixuan Li, Xifan Wang, Ran Wang, Yanling Hao, Fazheng Ren, Pengjie Wang, and Bing Fang. 2024. "Faecalibacterium prausnitzii Supplementation Prevents Intestinal Barrier Injury and Gut Microflora Dysbiosis Induced by Sleep Deprivation" Nutrients 16, no. 8: 1100. https://doi.org/10.3390/nu16081100
APA StyleWang, X., Li, Y., Wang, X., Wang, R., Hao, Y., Ren, F., Wang, P., & Fang, B. (2024). Faecalibacterium prausnitzii Supplementation Prevents Intestinal Barrier Injury and Gut Microflora Dysbiosis Induced by Sleep Deprivation. Nutrients, 16(8), 1100. https://doi.org/10.3390/nu16081100