journal article·2021-03Open access

Exosomes from TNF-α-treated human gingiva-derived MSCs enhance M2 macrophage polarization and inhibit periodontal bone loss

Yuki Nakao, Takao Fukuda, Qunzhou Zhang, Terukazu Sanui, Takanori Shinjo, Xiaoxing Kou, Chider Chen, Dawei Liu, Yukari Watanabe, Chikako Hayashi, Hiroaki Yamato, Karen Yotsumoto, Urara Tanaka, Takaharu Taketomi, Takeshi Uchiumi, Anh D. Le, Songtao Shi, Fusanori Nishimura

Acta Biomaterialia· Volume 122

Abstract

Mesenchymal stem cell (MSC)-derived exosome plays a central role in the cell-free therapeutics involving MSCs and the contents can be customized under disease-associated microenvironments. However, optimal MSC-preconditioning to enhance its therapeutic potential is largely unknown. Here, we show that preconditioning of gingival tissue-derived MSCs (GMSCs) with tumor necrosis factor-alpha (TNF-α) is ideal for the treatment of periodontitis. TNF-α stimulation not only increased the amount of exosome secreted from GMSCs, but also enhanced the exosomal expression of CD73, thereby inducing anti-inflammatory M2 macrophage polarization. The effect of GMSC-derived exosomes on inflammatory bone loss were examined by ligature-induced periodontitis model in mice. Local injection of GMSC-derived exosomes significantly reduced periodontal bone resorption and the number of tartrate-resistant acid phosphatase (TRAP)-positive osteoclasts, and these effects were further enhanced by preconditioning of GMSCs with TNF-α. Thus, GMSC-derived exosomes also exhibited anti-osteoclastogenic activity. Receptor activator of NF-κB ligand (RANKL) expression was regulated by Wnt5a in periodontal ligament cells (PDLCs), and exosomal miR-1260b was found to target Wnt5a-mediated RANKL pathway and inhibit its osteoclastogenic activity. These results indicate that significant ability of the TNF-α-preconditioned GMSC-derived exosomes to regulate inflammation and osteoclastogenesis paves the way for establishment of a therapeutic approach for periodontitis.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Extracellular vesicles in disease · Mesenchymal stem cell research · MicroRNA in disease regulation

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (96)

Show source-provided references
1. Multilineage potential of adult human mesenchymal stem cells10.1126/science.284.5411.143 ↗
2. Mesenchymal stem cells and their therapeutic applications in inflammatory bowel disease10.18632/oncotarget.16682 ↗
3. “Stemness” does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs)10.1038/sj.clpt.6100313 ↗
4. Strategies to enhance paracrine potency of transplanted mesenchymal stem cells in intractable neonatal disorders10.1038/pr.2017.249 ↗
5. Mesenchymal stromal cells: sensors and switchers of inflammation10.1016/j.stem.2013.09.006 ↗
6. Mesenchymal stem cells in health and disease10.1038/nri2395 ↗
7. Requirement of IFN-gamma-mediated indoleamine 2,3-dioxygenase expression in the modulation of lymphocyte proliferation by human adipose-derived stem cells10.1089/ten.tea.2008.0630 ↗
8. Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs10.1038/ncomms9472 ↗
9. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells10.1038/ncb1596 ↗
10. The therapeutic potential of mesenchymal stem cell-derived extracellular vesicles10.1002/pmic.201200373 ↗
11. Periodontitis: from microbial immune subversion to systemic inflammation10.1038/nri3785 ↗
12. Osteoimmunology: evolving concepts in bone-immune interactions in health and disease10.1038/s41577-019-0178-8 ↗
13. Host defense against oral microbiota by bone-damaging T cells10.1038/s41467-018-03147-6 ↗
14. Macrophage immunomodulation in chronic osteolytic diseases-the case of periodontitis10.1002/JLB.1RU0818-310R ↗
15. M-1/M-2 macrophages and the Th1/Th2 paradigm10.4049/jimmunol.164.12.6166 ↗
16. Alternative activation of macrophages: mechanism and functions10.1016/j.immuni.2010.05.007 ↗
17. The role of adenosine receptors A2A and A2B signaling in renal fibrosis10.1038/ki.2014.244 ↗
18. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression10.1084/jem.20062512 ↗
19. Nucleotide signalling during inflammation10.1038/nature13085 ↗
20. Regulation of inflammation by adenosine10.3389/fimmu.2013.00085 ↗
21. TLR stimulation initiates a CD39-based autoregulatory mechanism that limits macrophage inflammatory responses10.1182/blood-2013-04-496216 ↗
22. The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin-4 receptor alpha (IL-4Rα) signaling10.1007/s10753-013-9621-3 ↗
23. Bone homeostasis10.1073/pnas.95.23.13361 ↗
24. Macrophages in Bone Homeostasis10.2174/1574888X14666190214163815 ↗
25. Macrophage plasticity and polarization in tissue repair and remodelling10.1002/path.4133 ↗
26. Dental stem cell-derived secretome/conditioned medium: the future for regenerative therapeutic applications10.1155/2020/7593402 ↗
27. Gingivae contain neural-crest- and mesoderm-derived mesenchymal stem cells10.1177/0022034513497961 ↗
28. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis10.4049/jimmunol.0902318 ↗
29. Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing10.1002/stem.503 ↗
30. The Fas/Fap-1/Cav-1 complex regulates IL-1RA secretion in mesenchymal stem cells to accelerate wound healing10.1126/scitranslmed.aai8524 ↗
31. Interferon-gamma improves impaired dentinogenic and immunosuppressive functions of irreversible pulpitis-derived human dental pulp stem cells10.1038/srep19286 ↗
32. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines10.1080/20013078.2018.1535750 ↗
33. A novel affinity-based method for the isolation of highly purified extracellular vesicles10.1038/srep33935 ↗
34. Dental pulp cell-derived powerful inducer of TNF-α comprises PKR containing stress granule rich microvesicles10.1038/s41598-019-40046-2 ↗
35. Optimization of the ligature-induced periodontitis model in mice10.1016/j.jim.2013.05.002 ↗
36. SOCS-3 regulates alveolar bone loss in experimental periodontitis10.1177/0022034516645332 ↗
37. Grp78 is critical for amelogenin-induced cell migration in a multipotent clonal human periodontal ligament cell line10.1002/jcp.25087 ↗
38. Stromal mechanisms of bone marrow: cloning in vitro and retransplantation in vivo
39. Alternative activation of macrophages: an immunologic functional perspective10.1146/annurev.immunol.021908.132532 ↗
40. Dual regulation of osteoclast differentiation by periodontal ligament cells through RANKL stimulation and OPG inhibition10.1177/00220345010800030801 ↗
41. Wnt5a induces collagen production by human periodontal ligament cells through TGFbeta1-mediated upregulation of periostin expression10.1002/jcp.24950 ↗
42. Efficacy of stem cells on periodontal regeneration: systematic review of pre-clinical studies10.1111/jre.12455 ↗
43. Mesenchymal stem cells: isolation, in vitro expansion and characterization10.1007/3-540-31265-X_11 ↗
44. Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production10.4049/jimmunol.1003884 ↗
45. MSC surface markers (CD44, CD73, and CD90) can identify human MSC-derived extracellular vesicles by conventional flow cytometry10.1186/s12964-015-0124-8 ↗
46. Regulation of ecto-5′-nucleotidase by TNF-alpha in human endothelial cells10.1023/A:1014806916844 ↗
47. Regulation of ecto-5′-nucleotidase (CD73) in cultured cortical astrocytes by different inflammatory factors10.1016/j.neuint.2012.06.017 ↗
48. Negative effects of a high tumour necrosis factor-alpha concentration on human gingival mesenchymal stem cell trophism: the use of natural compounds as modulatory agents10.1186/s13287-018-0880-7 ↗
49. Rab27a and Rab27b control different steps of the exosome secretion pathway10.1038/ncb2000 ↗
50. Rab27A mediated by NF-κB promotes the stemness of colon cancer cells via up-regulation of cytokine secretion10.18632/oncotarget.11454 ↗
51. Immune regulatory targets of mesenchymal stromal cell exosomes/small extracellular vesicles in tissue regeneration10.1016/j.jcyt.2018.09.008 ↗
52. Exosomes from adipose-derived stem cells attenuate adipose inflammation and obesity through polarizing M2 macrophages and beiging in white adipose tissue10.2337/db17-0356 ↗
53. Mesenchymal stem cell-derived extracellular vesicles as mediators of anti-inflammatory effects: endorsement of macrophage polarization10.1002/sctm.16-0363 ↗
54. Human mesenchymal stem cells stimulated by TNF-alpha, LPS, or hypoxia produce growth factors by an NF kappa B- but not JNK-dependent mechanism10.1152/ajpcell.00437.2007 ↗
55. LPS-preconditioned mesenchymal stromal cells modify macrophage polarization for resolution of chronic inflammation via exosome-shuttled let-7b10.1186/s12967-015-0642-6 ↗
56. Pharmacologic stem cell based intervention as a new approach to osteoporosis treatment in rodents10.1371/journal.pone.0002615 ↗
57. Defining GM-CSF- and macrophage-CSF-dependent macrophage responses by in vitro models10.4049/jimmunol.1103426 ↗
58. Human gingiva-derived mesenchymal stem cells inhibit xeno-graft-versus-host disease via CD39-CD73-adenosine and IDO signals10.3389/fimmu.2017.00068 ↗
59. Human gingiva-derived mesenchymal stem cells modulate monocytes/macrophages and alleviate atherosclerosis10.3389/fimmu.2018.00878 ↗
60. MSC-exosome: a novel cell-free therapy for cutaneous regeneration10.1016/j.jcyt.2017.11.002 ↗
61. Differential roles of macrophages in diverse phases of skin repair10.4049/jimmunol.0903356 ↗
62. DEL-1 restrains osteoclastogenesis and inhibits inflammatory bone loss in nonhuman primates10.1126/scitranslmed.aac5380 ↗
63. Immunomodulatory effects of stem cells10.1111/prd.12024 ↗
64. Macrophage polarization in periodontal ligament stem cells enhanced periodontal regeneration10.1186/s13287-019-1409-4 ↗
65. M2 Macrophages enhance the cementoblastic differentiation of periodontal ligament stem cells via the Akt and JNK pathways10.1002/stem.3076 ↗
66. Role of extracellular RNA-carrying vesicles in cell differentiation and reprogramming10.1186/s13287-015-0150-x ↗
67. An emerging role for adenosine and its receptors in bone homeostasis10.3389/fendo.2012.00113 ↗
68. Wnt and beta-catenin signaling target the expression of ecto-5′-nucleotidase and increase extracellular adenosine generation10.1016/j.yexcr.2003.11.001 ↗
69. CD73-generated adenosine promotes osteoblast differentiation10.1002/jcp.23001 ↗
70. Dysregulation of ectonucleotidase-mediated extracellular adenosine during postmenopausal bone loss10.1126/sciadv.aax1387 ↗
71. Human gingival tissue-derived MSC suppress osteoclastogenesis and bone erosion via CD39-adenosine signal pathway in autoimmune arthritis10.1016/j.ebiom.2019.04.058 ↗
72. The RANKL-OPG system in clinical periodontology10.1111/j.1600-051X.2011.01810.x ↗
73. Lipopolysaccharide stimulates expression of osteoprotegerin and receptor activator of NF-kappa B ligand in periodontal ligament fibroblasts through the induction of interleukin-1 beta and tumor necrosis factor-alpha10.1016/j.bone.2004.04.023 ↗
74. Cells with osteoblastic phenotypes can be explanted from human gingiva and periodontal ligament10.1902/jop.1997.68.7.701 ↗
75. LPS-stimulated human gingival fibroblasts inhibit the differentiation of monocytes into osteoclasts through the production of osteoprotegerin10.1046/j.1365-2249.2002.01990.x ↗
76. Toll gates to periodontal host modulation and vaccine therapy10.1111/j.1600-0757.2009.00304.x ↗
77. WNT signalling in the immune system: WNT is spreading its wings10.1038/nri2360 ↗
78. Functions of the WNT Signaling Network in Shaping Host Responses to Infection10.3389/fimmu.2019.02521 ↗
79. Wnt/TLR Dialog in Neuroinflammation, Relevance in Alzheimer’s Disease10.3389/fimmu.2017.00187 ↗
80. Wnt signaling mediates TLR pathway and promote unrestrained adipogenesis and metaflammation: Therapeutic targets for obesity and type 2 diabetes10.1016/j.phrs.2019.104602 ↗
81. Modulation of Wnt5a expression by periodontopathic bacteria10.1371/journal.pone.0034434 ↗
82. Differential Expression and Roles of Secreted Frizzled-Related Protein 5 and the Wingless Homolog Wnt5a in Periodontitis10.1177/0022034516687248 ↗
83. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation10.1182/blood-2005-12-5046 ↗
84. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis10.1038/nm.2653 ↗
85. Regulatory mechanisms of microRNA expression10.1186/s12967-016-0893-x ↗
86. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles10.1146/annurev-cellbio-101512-122326 ↗
87. Wnt5a regulates dental follicle stem/progenitor cells of the periodontium10.1186/scrt525 ↗
88. JNK1 modulates osteoclastogenesis through both c-Jun phosphorylation-dependent and -independent mechanisms10.1242/jcs.00082 ↗
89. Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells10.1182/blood-2014-03-562439 ↗
90. MSC exosomes mediate cartilage repair by enhancing proliferation, attenuating apoptosis and modulating immune reactivity10.1016/j.biomaterials.2017.11.028 ↗
91. RANK-mediated amplification of TRAF6 signaling leads to NFATc1 induction during osteoclastogenesis10.1038/sj.emboj.7600564 ↗
92. A RANKL-PKCβ-TFEB signaling cascade is necessary for lysosomal biogenesis in osteoclasts10.1101/gad.213827.113 ↗
93. Colony stimulating factor-1 plays a role in osteoclast formation and function in bone resorption induced by parathyroid hormone and parathyroid hormone-related protein10.1002/jbmr.5650111014 ↗
94. MicroRNAs and their target genes in gingival tissues10.1177/0022034512456551 ↗
95. MicroRNAs as molecular switches in macrophage activation10.3389/fimmu.2019.00799 ↗
96. MicroRNA let-7 modulates the immune response to Mycobacterium tuberculosis infection via control of A20, an inhibitor of the NF-κB pathway10.1016/j.chom.2015.01.007 ↗