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

Author:

Chen Chun-Yuan12ORCID,Rao Shan-Shan23,Yue Tao12,Tan Yi-Juan12,Yin Hao12,Chen Ling-Jiao4,Luo Ming-Jie23,Wang Zun23,Wang Yi-Yi12,Hong Chun-Gu2,Qian Yu-Xuan12,He Ze-Hui12,Liu Jiang-Hua12,Yang Fei5,Huang Fei-Yu5,Tang Si-Yuan3,Xie Hui12678ORCID

Affiliation:

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.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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