Alterations of Gut Virome with Close Interaction in the Progression of Estrogen Deficiency-induced Osteoporosis

Overview

Journal Gut Microbes

Specialties Gastroenterology
Microbiology

Date 2024 Dec 9

PMID 39653684

Authors

Yueqi Chen

Chuan Yang

Zihan Deng

Tingwen Xiang

Jiulin Tan

Jianzhong Xu

Dong Sun

Fei Luo

Affiliations

Soon will be listed here.

Abstract

Previous research has established a link between gut microbiota and osteoporosis (OP) advancement. However, there remains a limited understanding of the crucial contribution of the gut virome in the onset and progression of OP. We employed metagenomic shotgun sequencing and gut virome sequencing to process the ovariectomy (OVX)-induced OP murine model, which revealed significant disparities in bacteriome and virome compositions between subjects with OP and healthy controls. One hundred and seventy-four altered viral strains were identified to participate in the multifaceted regulation of bone loss, involving immune modulation, microbial metabolic activity, and intricate host-virus dynamics. Our findings suggested that the gut virome may influence bone metabolism, potentially altering the balance of bone-modulating compounds like short-chain fatty acids. This comprehensive analysis of the gut virome in OP highlighted the diagnostic potential of combined gut viral and bacterial biomarkers for OP.

References

Seely K, Kotelko C, Douglas H, Bealer B, Brooks A . The Human Gut Microbiota: A Key Mediator of Osteoporosis and Osteogenesis. Int J Mol Sci. 2021; 22(17). PMC: 8431678. DOI: 10.3390/ijms22179452. View

Donald K, Finlay B . Early-life interactions between the microbiota and immune system: impact on immune system development and atopic disease. Nat Rev Immunol. 2023; 23(11):735-748. DOI: 10.1038/s41577-023-00874-w. View

Barr J, Auro R, Furlan M, Whiteson K, Erb M, Pogliano J . Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc Natl Acad Sci U S A. 2013; 110(26):10771-6. PMC: 3696810. DOI: 10.1073/pnas.1305923110. View

Illiano P, Brambilla R, Parolini C . The mutual interplay of gut microbiota, diet and human disease. FEBS J. 2020; 287(5):833-855. DOI: 10.1111/febs.15217. View

Cui Y, Zhang L, Wang X, Yi Y, Shan Y, Liu B . Roles of intestinal Parabacteroides in human health and diseases. FEMS Microbiol Lett. 2022; 369(1). DOI: 10.1093/femsle/fnac072. View

De Sordi L, Lourenco M, Debarbieux L . The Battle Within: Interactions of Bacteriophages and Bacteria in the Gastrointestinal Tract. Cell Host Microbe. 2019; 25(2):210-218. DOI: 10.1016/j.chom.2019.01.018. View

Xiang T, Deng Z, Yang C, Tan J, Dou C, Luo F . Bile acid metabolism regulatory network orchestrates bone homeostasis. Pharmacol Res. 2023; 196:106943. DOI: 10.1016/j.phrs.2023.106943. View

Yang K, Niu J, Zuo T, Sun Y, Xu Z, Tang W . Alterations in the Gut Virome in Obesity and Type 2 Diabetes Mellitus. Gastroenterology. 2021; 161(4):1257-1269.e13. DOI: 10.1053/j.gastro.2021.06.056. View

Zeng S, Liu Y, Zeng Z, Xie H, Liu J . Potential Effects of Akkermansia Muciniphila in Aging and Aging-Related Diseases: Current Evidence and Perspectives. Aging Dis. 2023; 14(6):2015-2027. PMC: 10676789. DOI: 10.14336/AD.2023.0325. View

10.

Jansen D, Matthijnssens J . The Emerging Role of the Gut Virome in Health and Inflammatory Bowel Disease: Challenges, Covariates and a Viral Imbalance. Viruses. 2023; 15(1). PMC: 9861652. DOI: 10.3390/v15010173. View

11.

Oh J, Alexander L, Pan M, Schueler K, Keller M, Attie A . Dietary Fructose and Microbiota-Derived Short-Chain Fatty Acids Promote Bacteriophage Production in the Gut Symbiont Lactobacillus reuteri. Cell Host Microbe. 2019; 25(2):273-284.e6. DOI: 10.1016/j.chom.2018.11.016. View

12.

de Jonge P, Wortelboer K, Scheithauer T, van den Born B, Zwinderman A, Nobrega F . Gut virome profiling identifies a widespread bacteriophage family associated with metabolic syndrome. Nat Commun. 2022; 13(1):3594. PMC: 9226167. DOI: 10.1038/s41467-022-31390-5. View

13.

Woo K, Jung H, Oh J, Rahman S, Kim S, Baek J . Synergistic effects of dimethyloxalylglycine and butyrate incorporated into α-calcium sulfate on bone regeneration. Biomaterials. 2014; 39:1-14. DOI: 10.1016/j.biomaterials.2014.10.054. View

14.

Shkoporov A, Hill C . Bacteriophages of the Human Gut: The "Known Unknown" of the Microbiome. Cell Host Microbe. 2019; 25(2):195-209. DOI: 10.1016/j.chom.2019.01.017. View

15.

Kular J, Tickner J, Chim S, Xu J . An overview of the regulation of bone remodelling at the cellular level. Clin Biochem. 2012; 45(12):863-73. DOI: 10.1016/j.clinbiochem.2012.03.021. View

16.

Wang Z, Chen K, Wu C, Chen J, Pan H, Liu Y . An emerging role of Prevotella histicola on estrogen deficiency-induced bone loss through the gut microbiota-bone axis in postmenopausal women and in ovariectomized mice. Am J Clin Nutr. 2021; 114(4):1304-1313. DOI: 10.1093/ajcn/nqab194. View

17.

Chen Y, Yang C, Dai Q, Tan J, Dou C, Luo F . Gold-nanosphere mitigates osteoporosis through regulating TMAO metabolism in a gut microbiota-dependent manner. J Nanobiotechnology. 2023; 21(1):125. PMC: 10088181. DOI: 10.1186/s12951-023-01872-9. View

18.

Rastelli M, Cani P, Knauf C . The Gut Microbiome Influences Host Endocrine Functions. Endocr Rev. 2019; 40(5):1271-1284. DOI: 10.1210/er.2018-00280. View

19.

Pavia G, Marascio N, Matera G, Quirino A . Does the Human Gut Virome Contribute to Host Health or Disease?. Viruses. 2023; 15(11). PMC: 10674713. DOI: 10.3390/v15112271. View

20.

Harris K, Zagar C, Lawrence K . Osteoporosis: Common Questions and Answers. Am Fam Physician. 2023; 107(3):238-246. View