Glucocorticoid-induced loss of beneficial gut bacterial extracellular vesicles is associated with the pathogenesis of osteonecrosis

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Abstract

Osteonecrosis of the femoral head (ONFH) commonly occurs after glucocorticoid (GC) therapy. The gut microbiota (GM) participates in regulating host health, and its composition can be altered by GC. Here, this study demonstrates that cohousing with healthy mice or colonization with GM from normal mice attenuates GC-induced ONFH. 16 S rRNA gene sequencing shows that cohousing with healthy mice rescues the GC-induced reduction of gut Lactobacillus animalis. Oral supplementation of L. animalis mitigates GC-induced ONFH by increasing angiogenesis, augmenting osteogenesis, and reducing cell apoptosis. Extracellular vesicles from L. animalis ( L. animalis-EVs) contain abundant functional proteins and can enter the femoral head to exert proangiogenic, pro-osteogenic, and antiapoptotic effects, while its abundance is reduced after exposure to GC. Our study suggests that the GM is involved in protecting the femoral head by transferring bacterial EVs, and that loss of L. animalis and its EVs is associated with the development of GC-induced ONFH.

Abstract

Gut bacteria secrete extracellular vesicles that prevent glucocorticoid-induced osteonecrosis.

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Most cited references 56

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Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy.

Ayelet Sivan, Leticia Corrales, Nathaniel A Hubert … (2015)

T cell infiltration of solid tumors is associated with favorable patient outcomes, yet the mechanisms underlying variable immune responses between individuals are not well understood. One possible modulator could be the intestinal microbiota. We compared melanoma growth in mice harboring distinct commensal microbiota and observed differences in spontaneous antitumor immunity, which were eliminated upon cohousing or after fecal transfer. Sequencing of the 16S ribosomal RNA identified Bifidobacterium as associated with the antitumor effects. Oral administration of Bifidobacterium alone improved tumor control to the same degree as programmed cell death protein 1 ligand 1 (PD-L1)-specific antibody therapy (checkpoint blockade), and combination treatment nearly abolished tumor outgrowth. Augmented dendritic cell function leading to enhanced CD8(+) T cell priming and accumulation in the tumor microenvironment mediated the effect. Our data suggest that manipulating the microbiota may modulate cancer immunotherapy.

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Gut microbiota-derived metabolites as key actors in inflammatory bowel disease

Aonghus Lavelle, Harry Sokol (2020)

A key role of the gut microbiota in the establishment and maintenance of health, as well as in the pathogenesis of disease, has been identified over the past two decades. One of the primary modes by which the gut microbiota interacts with the host is by means of metabolites, which are small molecules that are produced as intermediate or end products of microbial metabolism. These metabolites can derive from bacterial metabolism of dietary substrates, modification of host molecules, such as bile acids, or directly from bacteria. Signals from microbial metabolites influence immune maturation, immune homeostasis, host energy metabolism and maintenance of mucosal integrity. Alterations in the composition and function of the microbiota have been described in many studies on IBD. Alterations have also been described in the metabolite profiles of patients with IBD. Furthermore, specific classes of metabolites, notably bile acids, short-chain fatty acids and tryptophan metabolites, have been implicated in the pathogenesis of IBD. This Review aims to define the key classes of microbial-derived metabolites that are altered in IBD, describe the pathophysiological basis of these associations and identify future targets for precision therapeutic modulation.

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Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi.

Lisa Brown, Julie Wolf, Rafael Prados-Rosales … (2015)

Extracellular vesicles (EVs) are produced by all domains of life. In Gram-negative bacteria, EVs are produced by the pinching off of the outer membrane; however, how EVs escape the thick cell walls of Gram-positive bacteria, mycobacteria and fungi is still unknown. Nonetheless, EVs have been described in a variety of cell-walled organisms, including Staphylococcus aureus, Mycobacterium tuberculosis and Cryptococcus neoformans. These EVs contain varied cargo, including nucleic acids, toxins, lipoproteins and enzymes, and have important roles in microbial physiology and pathogenesis. In this Review, we describe the current status of vesiculogenesis research in thick-walled microorganisms and discuss the cargo and functions associated with EVs in these species.

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Author and article information

Contributors

Chun-Yuan Chen:

ORCID: https://orcid.org/0000-0001-7808-533X

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Shan-Shan Rao: Role: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Validation

Tao Yue: Role: Investigation

Yi-Juan Tan: Role: Investigation

Hao Yin: Role: InvestigationRole: Validation

Ling-Jiao Chen: Role: Investigation

Ming-Jie Luo: Role: Investigation

Zun Wang: Role: Investigation

Yi-Yi Wang: Role: Investigation

Chun-Gu Hong: Role: Investigation

Yu-Xuan Qian: Role: Investigation

Ze-Hui He: Role: Investigation

Jiang-Hua Liu: Role: Resources

Fei Yang: Role: Resources

Fei-Yu Huang: Role: Investigation

Si-Yuan Tang: Role: ResourcesRole: Software

Hui Xie:

ORCID: https://orcid.org/0000-0002-8526-2637

Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: April 2022

Publication date (Electronic, pub): 13 April 2022

Volume: 8

Issue: 15

Electronic Location Identifier: eabg8335

Affiliations

[1 ]Department of Orthopaedics, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China.

[2 ]Movement System Injury and Repair Research Center, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China.

[3 ]Xiangya School of Nursing, Central South University, Changsha, Hunan 410013, China.

[4 ]Department of Pathology, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou, Guangdong 510220, China.

[5 ]Department of Occupational and Environmental Health, Xiangya School of Public Health, Central South University, Changsha, Hunan 410078, China.

[6 ]Department of Sports Medicine, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China.

[7 ]Hunan Key Laboratory of Organ Injury, Aging and Regenerative Medicine, Changsha, Hunan 410008, China.

[8 ]Hunan Key Laboratory of Bone Joint Degeneration and Injury, Changsha, Hunan 410008, China.

[9 ]National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China.

Author notes

[* ]Corresponding author. Email: huixie@ 123456csu.edu.cn

Author information

Chun-Yuan Chen https://orcid.org/0000-0001-7808-533X

Hui Xie https://orcid.org/0000-0002-8526-2637

Article

Publisher ID: abg8335

DOI: 10.1126/sciadv.abg8335

PMC ID: 9007505

PubMed ID: 35417243

SO-VID: 77a7d9bc-dc9b-4f3b-91d2-8516198cc2fa

Copyright © Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

History

Date received : 30 January 2021

Date accepted : 24 February 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: Grant Nos. 81871822, 82072504, 81670807, 81522012, 81702237, 81974127

Funded by: Non-profit Central Research Institute Fund of Chinese Academy of Medical Sciences;

Award ID: Grant No. 2019-RC-HL-024

Funded by: Innovation Driven Project of Central South University;

Award ID: Grant No. 2019CX014

Funded by: Hunan Province Natural Science Foundation of China;

Award ID: Grant No. 2020JJ5883

Funded by: Free Exploration Program of Central South University;

Award ID: Grant No. 502221901

Funded by: Science and Technology Innovation Program of Hunan Province;

Award ID: Grant No. 2020RC4008

Funded by: Special Funding for the Construction of Innovative Provinces in Hunan;

Award ID: Grant Nos. 2019SK2301, 2020SK3002

Funded by: Science and Technology Plan Project of Hunan Province;

Award ID: Grant Nos. 2017XK2039, 2018RS3029

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Glucocorticoid-induced loss of beneficial gut bacterial extracellular vesicles is associated with the pathogenesis of osteonecrosis

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Bacterial extracellular vesicles

Most cited references 56

Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy.

Gut microbiota-derived metabolites as key actors in inflammatory bowel disease

Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi.

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Cited by 26

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