Autophagy controls mesenchymal stem cell therapy in psychological stress colitis mice

References

• Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002;418(6893):41–49.
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–147.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang L, Kikuiri T, et al. Mesenchymal stem cell-based tissue regeneration is governed by recipient T lymphocytes via IFN-gamma and TNF-alpha. Nat Med. 2011;17(12):1594–1601.
   PubMed Web of Science ®Google Scholar
• Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007;110(10):3499–3506.
   PubMed Web of Science ®Google Scholar
• Bernardo ME, Fibbe WE. Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell. 2013;13(4):392–402.
   PubMed Web of Science ®Google Scholar
• Akiyama K, Chen C, Wang D, et al. Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell. 2012;10(5):544–555.
   PubMed Web of Science ®Google Scholar
• Chen C, Wang D, Moshaverinia A, et al. Mesenchymal stem cell transplantation in tight-skin mice identifies miR-151-5p as a therapeutic target for systemic sclerosis. Cell Res. 2017;27(4):559–577.
   PubMed Web of Science ®Google Scholar
• Sun L, Akiyama K, Zhang H, et al. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells. 2009;27(6):1421–1432.
   PubMed Web of Science ®Google Scholar
• Nemeth K, Keane-Myers A, Brown JM, et al. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci U S A. 2010;107(12):5652–5657.
   PubMed Web of Science ®Google Scholar
• Nemeth K, Leelahavanichkul A, Yuen PS, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 2009;15(1):42–49.
   PubMed Web of Science ®Google Scholar
• Ren G, Zhang L, Zhao X, et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell. 2008;2(2):141–150.
   PubMed Web of Science ®Google Scholar
• Dang S, Xu H, Xu C, et al. Autophagy regulates the therapeutic potential of mesenchymal stem cells in experimental autoimmune encephalomyelitis. Autophagy. 2014;10(7):1301–1315.
   PubMed Web of Science ®Google Scholar
• Sala E, Genua M, Petti L, et al. Mesenchymal stem cells reduce colitis in mice via release of TSG6, independently of their localization to the intestine. Gastroenterology. 2015;149(1):163–176 e120.
   PubMed Web of Science ®Google Scholar
• Wang Y, Chen X, Cao W, et al. Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat Immunol. 2014;15(11):1009–1016.
   PubMed Web of Science ®Google Scholar
• Shi Y, Wang Y, Li Q, et al. Immunoregulatory mechanisms of mesenchymal stem and stromal cells in inflammatory diseases. Nat Rev Nephrol. 2018;14(8):493–507.
   PubMed Web of Science ®Google Scholar
• Pegtel DM, Gould SJ. Exosomes. Annu Rev Biochem. 2019;88:487–514.
   PubMed Web of Science ®Google Scholar
• Pluchino S, Smith JA. Explicating exosomes: reclassifying the rising stars of intercellular communication. Cell. 2019;177(2):225–227.
   PubMed Web of Science ®Google Scholar
• Beninson LA, Fleshner M. Exosomes: an emerging factor in stress-induced immunomodulation. Semin Immunol. 2014;26(5):394–401.
   PubMed Web of Science ®Google Scholar
• Huang X, Yuan T, Liang M, et al. Exosomal miR-1290 and miR-375 as prognostic markers in castration-resistant prostate cancer. Eur Urol. 2015;67(1):33–41.
   PubMed Web of Science ®Google Scholar
• Tan KH, Tan SS, Ng MJ, et al. Extracellular vesicles yield predictive pre-eclampsia biomarkers. J Extracell Vesicles. 2017;6(1):1408390.
   PubMed Web of Science ®Google Scholar
• Zeng Z, Li Y, Pan Y, et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun. 2018;9(1):5395.
   PubMed Web of Science ®Google Scholar
• Bjornetro T, Redalen KR, Meltzer S, et al. An experimental strategy unveiling exosomal microRNAs 486-5p, 181a-5p and 30d-5p from hypoxic tumour cells as circulating indicators of high-risk rectal cancer. J Extracell Vesicles. 2019;8(1):1567219.
   PubMed Web of Science ®Google Scholar
• Chen G, Huang AC, Zhang W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 2018;560(7718):382–386.
   PubMed Web of Science ®Google Scholar
• Heidt T, Sager HB, Courties G, et al. Chronic variable stress activates hematopoietic stem cells. Nat Med. 2014;20(7):754–758.
   PubMed Web of Science ®Google Scholar
• Wu L, Lu Y, Jiao Y, et al. Paternal psychological stress reprograms hepatic gluconeogenesis in offspring. Cell Metab. 2016;23(4):735–743.
   PubMed Web of Science ®Google Scholar
• Song H, Fang F, Tomasson G, et al. Association of stress-related disorders with subsequent autoimmune disease. JAMA. 2018;319(23):2388–2400.
   PubMed Web of Science ®Google Scholar
• Guerrero-Alba R, Valdez-Morales EE, Jimenez-Vargas NN, et al. Stress activates pronociceptive endogenous opioid signalling in DRG neurons during chronic colitis. Gut. 2017;66(12):2121–2131.
   PubMed Web of Science ®Google Scholar
• Fleshner M, Crane CR. Exosomes, DAMPs and miRNA: features of stress physiology and immune homeostasis. Trends Immunol. 2017;38(10):768–776.
   PubMed Web of Science ®Google Scholar
• Yang X, Han ZP, Zhang SS, et al. Chronic restraint stress decreases the repair potential from mesenchymal stem cells on liver injury by inhibiting TGF-beta1 generation. Cell Death Dis. 2014;5:e1308.
   PubMed Web of Science ®Google Scholar
• Zhang S, Lv C, Yang X, et al. Corticosterone mediates the inhibitory effect of restraint stress on the migration of mesenchymal stem cell to carbon tetrachloride-induced fibrotic liver by downregulating CXCR4/7 expression. Stem Cells Dev. 2015;24(5):587–596.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40(2):280–293.
   PubMed Web of Science ®Google Scholar
• Matsuzawa-Ishimoto Y, Hwang S, Cadwell K. Autophagy and Inflammation. Annu Rev Immunol. 2018;36:73–101.
   PubMed Web of Science ®Google Scholar
• Puri D, Subramanyam D. Stress - (self) eating: epigenetic regulation of autophagy in response to psychological stress. Febs J. 2019;286(13):2447–2460.
   PubMed Web of Science ®Google Scholar
• Lu X-T, Liu X-Q, Wang B, et al. The role of psychological stress on heart autophagy in mice with heart failure. Psychosom Med. 2017;79(9):1036–1044.
   PubMed Web of Science ®Google Scholar
• Qin A, Zhong T, Zou H, et al. Critical role of Tim-3 mediated autophagy in chronic stress induced immunosuppression. Cell Biosci. 2019;9:13.
   PubMed Web of Science ®Google Scholar
• Ceccariglia S, Cargnoni A, Silini AR, et al. Autophagy: a potential key contributor to the therapeutic action of mesenchymal stem cells. Autophagy. 2020;16(1):28–37.
   PubMed Web of Science ®Google Scholar
• Mawdsley JE, Rampton DS. Psychological stress in IBD: new insights into pathogenic and therapeutic implications. Gut. 2005;54(10):1481–1491.
   PubMed Web of Science ®Google Scholar
• Seifi M, Rodaway S, Rudolph U, et al. GABA(A) Receptor Subtypes Regulate Stress-Induced Colon Inflammation in Mice. Gastroenterology. 2018;155(3):852–864.e853.
   PubMed Web of Science ®Google Scholar
• Terrasini N, Lionetti V. Exosomes in Critical Illness. Crit Care Med. 2017;45(6):1054–1060.
   PubMed Web of Science ®Google Scholar
• Jansen F, Nickenig G, Werner N. Extracellular vesicles in cardiovascular disease: potential applications in diagnosis, prognosis, and epidemiology. Circ Res. 2017;120(10):1649–1657.
   PubMed Web of Science ®Google Scholar
• Tian T, Zhu YL, Zhou YY, et al. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem. 2014;289(32):22258–22267.
   PubMed Web of Science ®Google Scholar
• Jakovljevic J, Harrell CR, Fellabaum C, et al. Modulation of autophagy as new approach in mesenchymal stem cell-based therapy. Biomed Pharmacother. 2018;104:404–410.
   PubMed Web of Science ®Google Scholar
• You L, Wang Z, Li H, et al. The role of STAT3 in autophagy. Autophagy. 2015;11(5):729–739.
   PubMed Web of Science ®Google Scholar
• Beninson LA, Brown PN, Loughridge AB, et al. Acute stressor exposure modifies plasma exosome-associated heat shock protein 72 (Hsp72) and microRNA (miR-142-5p and miR-203). PLoS One. 2014;9(9):e108748.
   PubMed Web of Science ®Google Scholar
• Vicencio JM, Yellon DM, Sivaraman V, et al. Plasma exosomes protect the myocardium from ischemia-reperfusion injury. J Am Coll Cardiol. 2015;65(15):1525–1536.
   PubMed Web of Science ®Google Scholar
• Cheng L, Zhang K, Wu S, et al. Focus on Mesenchymal Stem Cell-Derived Exosomes: opportunities and Challenges in Cell-Free Therapy. Stem Cells Int. 2017;2017:6305295.
   PubMed Web of Science ®Google Scholar
• Phinney DG, Pittenger MF. Concise Review: MSC-Derived Exosomes for Cell-Free Therapy. Stem Cells. 2017;35(4):851–858.
   PubMed Web of Science ®Google Scholar
• Phinney DG, Di Giuseppe M, Njah J, et al. Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs. Nat Commun. 2015;6:8472.
   PubMed Web of Science ®Google Scholar
• Liu S, Liu D, Chen C, et al. MSC transplantation improves osteopenia via epigenetic regulation of notch signaling in lupus. Cell Metab. 2015;22(4):606–618.
   PubMed Web of Science ®Google Scholar
• Lopez-Santalla M, Hervas-Salcedo R, Fernandez-Garcia M, et al. Cell therapy with mesenchymal stem cells induces an innate immune memory response that attenuates experimental colitis in the long-term. J Crohns Colitis. 2020. DOI:https://doi.org/10.1093/ecco-jcc/jjaa079
   Google Scholar
• Sbrana FV, Cortini M, Avnet S, et al. The role of autophagy in the maintenance of stemness and differentiation of mesenchymal stem cells. Stem Cell Rev. 2016;12(6):621–633.
   Web of Science ®Google Scholar
• Guan JL, Simon AK, Prescott M, et al. Autophagy in stem cells. Autophagy. 2013;9(6):830–849.
   PubMed Web of Science ®Google Scholar
• Kota DJ, Wiggins LL, Yoon N, et al. TSG-6 produced by hMSCs delays the onset of autoimmune diabetes by suppressing Th1 development and enhancing tolerogenicity. Diabetes. 2013;62(6):2048–2058.
   PubMed Web of Science ®Google Scholar
• Sharma S, Yang SC, Zhu L, et al. Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res. 2005;65(12):5211–5220.
   PubMed Web of Science ®Google Scholar
• Ghannam S, Pène J, Moquet-Torcy G, et al. Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol. 2010;185(1):302–312.
   PubMed Web of Science ®Google Scholar
• Duffy MM, Pindjakova J, Hanley SA, et al. Mesenchymal stem cell inhibition of T-helper 17 cell- differentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor. Eur J Immunol. 2011;41(10):2840–2851.
   PubMed Web of Science ®Google Scholar
• Gao L, Cen S, Wang P, et al. Autophagy Improves the Immunosuppression of CD4+ T Cells by Mesenchymal Stem Cells Through Transforming Growth Factor-beta1. Stem Cells Transl Med. 2016;5(11):1496–1505.
   PubMed Web of Science ®Google Scholar
• Kim KW, Moon SJ, Park MJ, et al. Optimization of adipose tissue-derived mesenchymal stem cells by rapamycin in a murine model of acute graft-versus-host disease. Stem Cell Res Ther. 2015;6:202.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008;9(12):1004–1010.
   PubMed Web of Science ®Google Scholar
• Sun L, Hu L, Cogdell D, et al. MIR506 induces autophagy-related cell death in pancreatic cancer cells by targeting the STAT3 pathway. Autophagy. 2017;13(4):703–714.
   PubMed Web of Science ®Google Scholar
• Miao LJ, Huang FX, Sun ZT, et al. Stat3 inhibits Beclin 1 expression through recruitment of HDAC3 in nonsmall cell lung cancer cells. Tumour Biol. 2014;35(7):7097–7103.
   PubMedGoogle Scholar
• Feng Y, Ke C, Tang Q, et al. Metformin promotes autophagy and apoptosis in esophageal squamous cell carcinoma by downregulating Stat3 signaling. Cell Death Dis. 2014;5:e1088.
   PubMed Web of Science ®Google Scholar
• Tai WT, Shiau CW, Chen HL, et al. Mcl-1-dependent activation of Beclin 1 mediates autophagic cell death induced by sorafenib and SC-59 in hepatocellular carcinoma cells. Cell Death Dis. 2013;4:e485.
   PubMed Web of Science ®Google Scholar
• Shen S, Niso-Santano M, Adjemian S, et al. Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity. Mol Cell. 2012;48(5):667–680.
   PubMed Web of Science ®Google Scholar
• Vigo T, Procaccini C, Ferrara G, et al. IFN-gamma orchestrates mesenchymal stem cell plasticity through the signal transducer and activator of transcription 1 and 3 and mammalian target of rapamycin pathways. J Allergy Clin Immunol. 2017;139(5):1667–1676.
   PubMed Web of Science ®Google Scholar
• Cheng L, Sharples RA, Scicluna BJ, et al. Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J Extracell Vesicles. 2014;3. DOI:https://doi.org/10.3402/jev.v3.23743
   PubMedGoogle Scholar
• Ohshima K, Inoue K, Fujiwara A, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One. 2010;5(10):e13247.
   PubMed Web of Science ®Google Scholar
• Hodson R. Precision medicine. Nature. 2016;537(7619):S49.
   PubMed Web of Science ®Google Scholar
• Kimmelman J, Tannock I. The paradox of precision medicine. Nat Rev Clin Oncol. 2018;15(6):341–342.
   PubMed Web of Science ®Google Scholar
• Salgado R, Moore H, Martens JWM, et al. Steps forward for cancer precision medicine. Nat Rev Drug Discov. 2018;17(1):1–2.
   PubMed Web of Science ®Google Scholar
• Alex P, Zachos NC, Nguyen T, et al. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis. 2009;15(3):341–352.
   PubMed Web of Science ®Google Scholar
• Kim HS, Shin TH, Lee BC, et al. Human umbilical cord blood mesenchymal stem cells reduce colitis in mice by activating NOD2 signaling to COX2. Gastroenterology. 2013;145(6):1392–1403 e1391–1398.
   Web of Science ®Google Scholar
• Yosef N, Shalek AK, Gaublomme JT, et al. Dynamic regulatory network controlling TH17 cell differentiation. Nature. 2013;496(7446):461–468.
   PubMed Web of Science ®Google Scholar
• Chen C, Akiyama K, Yamaza T, et al. Telomerase governs immunomodulatory properties of mesenchymal stem cells by regulating FAS ligand expression. EMBO Mol Med. 2014;6(3):322–334.
   PubMed Web of Science ®Google Scholar