Abstract

The host genome may influence the composition of the intestinal microbiota, and the intestinal microbiota has a significant effect on muscle growth and development. In this study, we found that the deletion of the myostatin (MSTN) gene positively regulates the expression of the intestinal tight junction-related genes TJP1 and OCLN through the myosin light-chain kinase/myosin light chain pathway. The intestinal structure of MSTN−/− pigs differed from wild-type, including by the presence of a thicker muscularis and longer plicae. Together, these changes affect the structure of intestinal microbiota. Mice transplanted with the intestinal microbiota of MSTN−/− pigs had myofibers with larger cross-sectional areas and higher fast-twitch glycolytic muscle mass. Microbes responsible for the production of short-chain fatty acids (SCFAs) were enriched in both the MSTN−/− pigs and recipient mice, and SCFAs levels were elevated in the colon contents. We also demonstrated that valeric acid stimulates type IIb myofiber growth by activating the Akt/mTOR pathway via G protein-coupled receptor 43 and ameliorates dexamethasone-induced muscle atrophy. This is the first study to identify the MSTN gene-gut microbiota-SCFA axis and its regulatory role in fast-twitch glycolytic muscle growth.

Data availability

The raw reads of 16s rRNA gene sequences have been submitted to the NCBI BioSample database (Porcine data: PRJNA743164; Mice data: PRJNA743401).

The following data sets were generated
    1. Luo ZB
    (2022) Original data of Luo et al
    Science Data Bank, doi:10.57760/sciencedb.06767.

Article and author information

Author details

  1. Zhao-Bo Luo

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Shengzhong Han

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Xi-Jun Yin

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Hongye Liu

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Junxia Wang

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Meifu Xuan

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Chunyun Hao

    College of Integration Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Danqi Wang

    College of Integration Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0009-0001-7656-9901
  9. Yize Liu

    Key Laboratory of Natural Medicines of the Changbai Mountain, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Shuangyan Chang

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Dongxu Li

    College of Integration Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Kai Gao

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Huiling Li

    Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Biaohu Quan

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  15. Lin-Hu Quan

    Key Laboratory of Natural Medicines of the Changbai Mountain, Yanbian University, Yanji, China
    For correspondence
    lhquan@ybu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7195-8078
  16. Jin-Dan Kang

    Department of Animal Science, Yanbian University, Yanji, China
    For correspondence
    jdkang@ybu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Natural Science Foundation of China (32260817)

  • Jin-Dan Kang

National Natural Science Foundation of China (32260026)

  • Lin-Hu Quan

Changbai Mountain Talent Project of Jilin Province (000007)

  • Lin-Hu Quan

Higher Education Discipline Innovation Project (D18012)

  • Lin-Hu Quan

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The animal study was approved by the Ethics Committee of Yanbian University (approval number SYXK2020-0009).

Copyright

© 2023, Luo et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,359
    views
  • 320
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Zhao-Bo Luo
  2. Shengzhong Han
  3. Xi-Jun Yin
  4. Hongye Liu
  5. Junxia Wang
  6. Meifu Xuan
  7. Chunyun Hao
  8. Danqi Wang
  9. Yize Liu
  10. Shuangyan Chang
  11. Dongxu Li
  12. Kai Gao
  13. Huiling Li
  14. Biaohu Quan
  15. Lin-Hu Quan
  16. Jin-Dan Kang
(2023)
Fecal transplant from myostatin deletion pigs positively impacts the gut-muscle axis
eLife 12:e81858.
https://doi.org/10.7554/eLife.81858

Share this article

https://doi.org/10.7554/eLife.81858

Further reading

    1. Developmental Biology
    Emily Delgouffe, Samuel Madureira Silva ... Ellen Goossens
    Research Article

    Although the impact of gender-affirming hormone therapy (GAHT) on spermatogenesis in trans women has already been studied, data on its precise effects on the testicular environment is poor. Therefore, this study aimed to characterize, through histological and transcriptomic analysis, the spermatogonial stem cell niche of 106 trans women who underwent standardized GAHT, comprising estrogens and cyproterone acetate. A partial dedifferentiation of Sertoli cells was observed, marked by the co-expression of androgen receptor and anti-Müllerian hormone which mirrors the situation in peripubertal boys. The Leydig cells also exhibited a distribution analogous to peripubertal tissue, accompanied by a reduced insulin-like factor 3 expression. Although most peritubular myoid cells expressed alpha-smooth muscle actin 2, the expression pattern was disturbed. Besides this, fibrosis was particularly evident in the tubular wall and the lumen was collapsing in most participants. A spermatogenic arrest was also observed in all participants. The transcriptomic profile of transgender tissue confirmed a loss of mature characteristics - a partial rejuvenation - of the spermatogonial stem cell niche and, in addition, detected inflammation processes occurring in the samples. The present study shows that GAHT changes the spermatogonial stem cell niche by partially rejuvenating the somatic cells and inducing fibrotic processes. These findings are important to further understand how estrogens and testosterone suppression affect the testis environment, and in the case of orchidectomized testes as medical waste material, their potential use in research.

    1. Developmental Biology
    2. Stem Cells and Regenerative Medicine
    Kara A Nelson, Kari F Lenhart ... Stephen DiNardo
    Research Article

    Niches are often found in specific positions in tissues relative to the stem cells they support. Consistency of niche position suggests that placement is important for niche function. However, the complexity of most niches has precluded a thorough understanding of how their proper placement is established. To address this, we investigated the formation of a genetically tractable niche, the Drosophila Posterior Signaling Center (PSC), the assembly of which had not been previously explored. This niche controls hematopoietic progenitors of the lymph gland (LG). PSC cells were previously shown to be specified laterally in the embryo, but ultimately reside dorsally, at the LG posterior. Here, using live-imaging, we show that PSC cells migrate as a tight collective and associate with multiple tissues during their trajectory to the LG posterior. We find that Slit emanating from two extrinsic sources, visceral mesoderm and cardioblasts, is required for the PSC to remain a collective, and for its attachment to cardioblasts during migration. Without proper Slit-Robo signaling, PSC cells disperse, form aberrant contacts, and ultimately fail to reach their stereotypical position near progenitors. Our work characterizes a novel example of niche formation and identifies an extrinsic signaling relay that controls precise niche positioning.