Labial gland-derived mesenchymal stem cells and their exosomes ameliorate murine Sjögren&apos;s syndrome by modulating the balance of Treg and Th17 cells

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Abstract

Background

Sjögren's syndrome (SS) is a chronic, systemic autoimmune disorder characterized by sicca syndrome and/or systemic manifestations. The disease severely affects the health and life of patients, and the treatment of SS has always been a clinical challenge and essentially palliative. Mesenchymal stem cells (MSCs) have been reported to exert immunomodulatory effects and as a potential novel therapeutic strategy for SS. Labial gland-derived MSCs (LGMSCs) are a population of resident stem cells in the labial gland, first isolated by our group. Exosomes released by MSCs contain a large variety of bioactive molecules and considered to function as an extension of MSCs.

Methods

LGMSCs were isolated from patients who were needed surgery to remove the lip mucocele and LGMSCs derived exosomes (LGMSC-Exos) were isolated by ultracentrifugation. The non-obese diabetic (NOD) mice were treated with LGMSCs or LGMSC-Exos by tail vein injection. The saliva flow rate of mice was determined and salivary glands were dissected and stained with hematoxylin and eosin. In vitro, peripheral blood mononuclear cells (PBMCs) from SS patients were cocultured with LGMSCs or LGMSC-Exos. Percentage of T helper 17 (Th17) cells and regulatory T (Treg) cells were determined by flow cytometry. The serum levels of cytokines in NOD mice and in the supernatant of the co-culture system by ELISA.

Results

Treatment with LGMSCs or LGMSC-Exos reduced inflammatory infiltration in the salivary glands, and restored salivary gland secretory function in NOD mice. Importantly, LGMSCs or LGMSC-Exos were demonstrated to inhibit the differentiation of Th17 cells but promote the induction of Treg cells in NOD mice and PBMCs from SS patients in vitro, accompanied by reduced interleukin 17 (IL-17), interferon gamma, and IL-6 levels and enhanced transforming growth factor beta and IL-10 secretion by T cells.

Conclusions

LGMSCs are potential candidates for MSCs-based therapy and LGMSC-Exos might be utilized for establishing a new cell-free therapy against SS.

Supplementary Information

The online version contains supplementary material available at 10.1186/s13287-021-02541-0.

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Most cited references 48

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The biology, function, and biomedical applications of exosomes

Raghu Kalluri, Valerie LeBleu (2020)

The study of extracellular vesicles (EVs) has the potential to identify unknown cellular and molecular mechanisms in intercellular communication and in organ homeostasis and disease. Exosomes, with an average diameter of ~100 nanometers, are a subset of EVs. The biogenesis of exosomes involves their origin in endosomes, and subsequent interactions with other intracellular vesicles and organelles generate the final content of the exosomes. Their diverse constituents include nucleic acids, proteins, lipids, amino acids, and metabolites, which can reflect their cell of origin. In various diseases, exosomes offer a window into altered cellular or tissue states, and their detection in biological fluids potentially offers a multicomponent diagnostic readout. The efficient exchange of cellular components through exosomes can inform their applied use in designing exosome-based therapeutics.

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Review of the Isolation, Characterization, Biological Function, and Multifarious Therapeutic Approaches of Exosomes

Sangiliyandi Gurunathan, Min-Hee Kang, Muniyandi Jeyaraj … (2019)

Exosomes are extracellular vesicles that contain a specific composition of proteins, lipids, RNA, and DNA. They are derived from endocytic membranes and can transfer signals to recipient cells, thus mediating a novel mechanism of cell-to-cell communication. They are also thought to be involved in cellular waste disposal. Exosomes play significant roles in various biological functions, including the transfer of biomolecules such as RNA, proteins, enzymes, and lipids and the regulation of numerous physiological and pathological processes in various diseases. Because of these properties, they are considered to be promising biomarkers for the diagnosis and prognosis of various diseases and may contribute to the development of minimally invasive diagnostics and next generation therapies. The biocompatible nature of exosomes could enhance the stability and efficacy of imaging probes and therapeutics. Due to their potential use in clinical applications, exosomes have attracted much research attention on their roles in health and disease. To explore the use of exosomes in the biomedical arena, it is essential that the basic molecular mechanisms behind the transport and function of these vesicles are well-understood. Herein, we discuss the history, biogenesis, release, isolation, characterization, and biological functions of exosomes, as well as the factors influencing their biogenesis and their technical and biological challenges. We conclude this review with a discussion on the future perspectives of exosomes.

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Primary Sjögren’s Syndrome

Caren G. Solomon, Xavier Mariette, Lindsey A. Criswell (2018)

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Author and article information

Contributors

Jing He: hejing1105@126.com

Hong Hua:

ORCID: http://orcid.org/0000-0003-1198-508X

honghua1968@aliyun.com

Journal

Journal ID (nlm-ta): Stem Cell Res Ther

Journal ID (iso-abbrev): Stem Cell Res Ther

Title: Stem Cell Research & Therapy

Publisher: BioMed Central (London )

ISSN (Electronic): 1757-6512

Publication date (Electronic): 26 August 2021

Publication date PMC-release: 26 August 2021

Publication date Collection: 2021

Volume: 12

Electronic Location Identifier: 478

Affiliations

[1 ]GRID grid.11135.37, ISNI 0000 0001 2256 9319, Department of Oral Medicine, , Peking University School and Hospital of Stomatology, ; No. 22, Zhongguancun South Avenue, Haidian District, Beijing, 100081 People’s Republic of China

[2 ]GRID grid.11135.37, ISNI 0000 0001 2256 9319, Central Laboratory, , Peking University School and Hospital of Stomatology, ; No. 22, Zhongguancun South Avenue, Haidian District, Beijing, 100081 People’s Republic of China

[3 ]GRID grid.411634.5, ISNI 0000 0004 0632 4559, Department of Rheumatology and Immunology, , Peking University People’s Hospital, ; No. 11, Xizhimen South Street, Xicheng District, Beijing, 100044 People’s Republic of China

Author information

Hong Hua http://orcid.org/0000-0003-1198-508X

Article

Publisher ID: 2541

DOI: 10.1186/s13287-021-02541-0

PMC ID: 8390194

PubMed ID: 34446113

SO-VID: 95e9badb-4843-4075-a5a1-c424b9b9ffe1

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 22 April 2021

Date accepted : 6 August 2021

Funding

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

Award ID: 81970952

Award Recipient : Hong Hua

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ScienceOpen disciplines: Molecular medicine

Keywords: sjögren's syndrome,autoimmune,mesenchymal stem cells,exosomes,t helper 17 cells,regulatory t cells

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ScienceOpen disciplines: Molecular medicine

Keywords: sjögren's syndrome, autoimmune, mesenchymal stem cells, exosomes, t helper 17 cells, regulatory t cells

Labial gland-derived mesenchymal stem cells and their exosomes ameliorate murine Sjögren's syndrome by modulating the balance of Treg and Th17 cells

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Abstract

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Methods

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Supplementary Information

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Regulatory T cell (Treg) therapy

Most cited references 48

The biology, function, and biomedical applications of exosomes

Review of the Isolation, Characterization, Biological Function, and Multifarious Therapeutic Approaches of Exosomes

Primary Sjögren’s Syndrome

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