3,833
Views
78
CrossRef citations to date
0
Altmetric
Translational Research Paper

Autophagy regulates the therapeutic potential of mesenchymal stem cells in experimental autoimmune encephalomyelitis

, , , , , , , , , , , , & show all
Pages 1301-1315 | Received 24 Oct 2013, Accepted 03 Apr 2014, Published online: 14 May 2014

References

  • Mc Guire C, Beyaert R, van Loo G. Death receptor signalling in central nervous system inflammation and demyelination. Trends Neurosci 2011; 34:619 - 28; http://dx.doi.org/10.1016/j.tins.2011.09.002; PMID: 21999927
  • Gold R, Linington C, Lassmann H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006; 129:1953 - 71; http://dx.doi.org/10.1093/brain/awl075; PMID: 16632554
  • Constantinescu CS, Farooqi N, O’Brien K, Gran B. Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS). Br J Pharmacol 2011; 164:1079 - 106; http://dx.doi.org/10.1111/j.1476-5381.2011.01302.x; PMID: 21371012
  • Probert L, Eugster HP, Akassoglou K, Bauer J, Frei K, Lassmann H, Fontana A. TNFR1 signalling is critical for the development of demyelination and the limitation of T-cell responses during immune-mediated CNS disease. Brain 2000; 123:2005 - 19; http://dx.doi.org/10.1093/brain/123.10.2005; PMID: 11004118
  • Stoll G, Jander S, Schroeter M. Cytokines in CNS disorders: neurotoxicity versus neuroprotection. J Neural Transm Suppl 2000; 59:81 - 9; PMID: 10961421
  • Jadidi-Niaragh F, Mirshafiey A. Th17 cell, the new player of neuroinflammatory process in multiple sclerosis. Scand J Immunol 2011; 74:1 - 13; http://dx.doi.org/10.1111/j.1365-3083.2011.02536.x; PMID: 21338381
  • Jiang HR, Milovanović M, Allan D, Niedbala W, Besnard AG, Fukada SY, Alves-Filho JC, Togbe D, Goodyear CS, Linington C, et al. IL-33 attenuates EAE by suppressing IL-17 and IFN-γ production and inducing alternatively activated macrophages. Eur J Immunol 2012; 42:1804 - 14; http://dx.doi.org/10.1002/eji.201141947; PMID: 22585447
  • Trapp BD, Nave KA. Multiple sclerosis: an immune or neurodegenerative disorder?. Annu Rev Neurosci 2008; 31:247 - 69; http://dx.doi.org/10.1146/annurev.neuro.30.051606.094313; PMID: 18558855
  • Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression?. Trends Immunol 2007; 28:219 - 26; http://dx.doi.org/10.1016/j.it.2007.03.001; PMID: 17400510
  • Bai L, Lennon DP, Eaton V, Maier K, Caplan AI, Miller SD, Miller RH. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 2009; 57:1192 - 203; http://dx.doi.org/10.1002/glia.20841; PMID: 19191336
  • Rafei M, Birman E, Forner K, Galipeau J. Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis. Mol Ther 2009; 17:1799 - 803; http://dx.doi.org/10.1038/mt.2009.157; PMID: 19602999
  • Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105:1815 - 22; http://dx.doi.org/10.1182/blood-2004-04-1559; PMID: 15494428
  • Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007; 56:1175 - 86; http://dx.doi.org/10.1002/art.22511; PMID: 17393437
  • Németh K, Leelahavanichkul A, Yuen PST, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, 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; 15:42 - 9; http://dx.doi.org/10.1038/nm.1905; PMID: 19098906
  • Liu Y, Wang L, Kikuiri T, Akiyama K, Chen C, Xu X, Yang R, Chen W, Wang S, Shi S. Mesenchymal stem cell-based tissue regeneration is governed by recipient T lymphocytes via IFN-γ and TNF-α. Nat Med 2011; 17:1594 - 601; http://dx.doi.org/10.1038/nm.2542; PMID: 22101767
  • Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005; 106:1755 - 61; http://dx.doi.org/10.1182/blood-2005-04-1496; PMID: 15905186
  • Rafei M, Campeau PM, Aguilar-Mahecha A, Buchanan M, Williams P, Birman E, Yuan S, Young YK, Boivin MN, Forner K, et al. Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent manner. J Immunol 2009; 182:5994 - 6002; http://dx.doi.org/10.4049/jimmunol.0803962; PMID: 19414750
  • Shi Y, Hu G, Su J, Li W, Chen Q, Shou P, Xu C, Chen X, Huang Y, Zhu Z, et al. Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Res 2010; 20:510 - 8; http://dx.doi.org/10.1038/cr.2010.44; PMID: 20368733
  • Le Blanc K, Mougiakakos D. Multipotent mesenchymal stromal cells and the innate immune system. Nat Rev Immunol 2012; 12:383 - 96; http://dx.doi.org/10.1038/nri3209; PMID: 22531326
  • Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008; 2:141 - 50; http://dx.doi.org/10.1016/j.stem.2007.11.014; PMID: 18371435
  • Mougiakakos D, Jitschin R, Johansson CC, Okita R, Kiessling R, Le Blanc K. The impact of inflammatory licensing on heme oxygenase-1-mediated induction of regulatory T cells by human mesenchymal stem cells. Blood 2011; 117:4826 - 35; http://dx.doi.org/10.1182/blood-2010-12-324038; PMID: 21389316
  • Ren G, Su J, Zhang L, Zhao X, Ling W, L’huillie A, Zhang J, Lu Y, Roberts AI, Ji W, et al. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells 2009; 27:1954 - 62; http://dx.doi.org/10.1002/stem.118; PMID: 19544427
  • Levine B, Deretic V. Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 2007; 7:767 - 77; http://dx.doi.org/10.1038/nri2161; PMID: 17767194
  • Kuballa P, Nolte WM, Castoreno AB, Xavier RJ. Autophagy and the immune system. Annu Rev Immunol 2012; 30:611 - 46; http://dx.doi.org/10.1146/annurev-immunol-020711-074948; PMID: 22449030
  • Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323 - 35; http://dx.doi.org/10.1038/nature09782; PMID: 21248839
  • Singh R, Xiang Y, Wang Y, Baikati K, Cuervo AM, Luu YK, Tang Y, Pessin JE, Schwartz GJ, Czaja MJ. Autophagy regulates adipose mass and differentiation in mice. J Clin Invest 2009; 119:3329 - 39; PMID: 19855132
  • Ugland H, Naderi S, Brech A, Collas P, Blomhoff HK. cAMP induces autophagy via a novel pathway involving ERK, cyclin E and Beclin 1. Autophagy 2011; 7:1199 - 211; http://dx.doi.org/10.4161/auto.7.10.16649; PMID: 21750416
  • Pyo JO, Nah J, Kim HJ, Lee HJ, Heo J, Lee H, Jung YK. Compensatory activation of ERK1/2 in Atg5-deficient mouse embryo fibroblasts suppresses oxidative stress-induced cell death. Autophagy 2008; 4:315 - 21; PMID: 18196969
  • Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, Semprun-Prieto L, Delafontaine P, Prockop DJ. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009; 5:54 - 63; http://dx.doi.org/10.1016/j.stem.2009.05.003; PMID: 19570514
  • Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, Uccelli A, Lanzavecchia A, Engelhardt B, Sallusto F. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 2009; 10:514 - 23; http://dx.doi.org/10.1038/ni.1716; PMID: 19305396
  • Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 2009; 9:393 - 407; http://dx.doi.org/10.1038/nri2550; PMID: 19444307
  • Xu J, Zhang Y, Xiao Y, Ma S, Liu Q, Dang S, Jin M, Shi Y, Wan B, Zhang Y. Inhibition of 12/15-lipoxygenase by baicalein induces microglia PPARβ/δ: a potential therapeutic role for CNS autoimmune disease. Cell Death Dis 2013; 4:e569; http://dx.doi.org/10.1038/cddis.2013.86; PMID: 23559003
  • Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012; 24:981 - 90; http://dx.doi.org/10.1016/j.cellsig.2012.01.008; PMID: 22286106
  • Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, Wenk MR, Ong CN, Codogno P, Shen HM. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 2010; 285:10850 - 61; http://dx.doi.org/10.1074/jbc.M109.080796; PMID: 20123989
  • Shin JYPH, Park HJ, Kim HN, Oh SH, Bae JS, Ha HJ, Lee PH. Mesenchymal stem cells enhance autophagy and increase β-amyloid clearance in Alzheimer disease models. Autophagy 2014; 10:32 - 44; http://dx.doi.org/10.4161/auto.26508; PMID: 24149893
  • Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, Santarlasci V, Mazzinghi B, Pizzolo G, Vinante F, et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006; 24:386 - 98; http://dx.doi.org/10.1634/stemcells.2005-0008; PMID: 16123384
  • Miller E. Multiple sclerosis. Adv Exp Med Biol 2012; 724:222 - 38; http://dx.doi.org/10.1007/978-1-4614-0653-2_17; PMID: 22411246
  • Shi Y, Su J, Roberts AI, Shou P, Rabson AB, Ren G. How mesenchymal stem cells interact with tissue immune responses. Trends Immunol 2012; 33:136 - 43; http://dx.doi.org/10.1016/j.it.2011.11.004; PMID: 22227317
  • Tu SP, Quante M, Bhagat G, Takaishi S, Cui G, Yang XD, Muthuplani S, Shibata W, Fox JG, Pritchard DM, et al. IFN-γ inhibits gastric carcinogenesis by inducing epithelial cell autophagy and T-cell apoptosis. Cancer Res 2011; 71:4247 - 59; http://dx.doi.org/10.1158/0008-5472.CAN-10-4009; PMID: 21512143
  • Djavaheri-Mergny M, Amelotti M, Mathieu J, Besançon F, Bauvy C, Souquère S, Pierron G, Codogno P. NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem 2006; 281:30373 - 82; http://dx.doi.org/10.1074/jbc.M602097200; PMID: 16857678
  • Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 2008; 111:1327 - 33; http://dx.doi.org/10.1182/blood-2007-02-074997; PMID: 17951526
  • Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS One 2010; 5:e9016; http://dx.doi.org/10.1371/journal.pone.0009016; PMID: 20126406
  • Crop MJ, Baan CC, Korevaar SS, Ijzermans JN, Pescatori M, Stubbs AP, van Ijcken WF, Dahlke MH, Eggenhofer E, Weimar W, et al. Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesenchymal stem cells. Clin Exp Immunol 2010; 162:474 - 86; http://dx.doi.org/10.1111/j.1365-2249.2010.04256.x; PMID: 20846162
  • Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007; 26:1749 - 60; http://dx.doi.org/10.1038/sj.emboj.7601623; PMID: 17347651
  • Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 2011; 36:30 - 8; http://dx.doi.org/10.1016/j.tibs.2010.07.007; PMID: 20728362
  • Jain A, Lamark T, Sjøttem E, Larsen KB, Awuh JA, Øvervatn A, McMahon M, Hayes JD, Johansen T. p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem 2010; 285:22576 - 91; http://dx.doi.org/10.1074/jbc.M110.118976; PMID: 20452972
  • Song S, Guha S, Liu K, Buttar NS, Bresalier RS. COX-2 induction by unconjugated bile acids involves reactive oxygen species-mediated signalling pathways in Barrett’s oesophagus and oesophageal adenocarcinoma. Gut 2007; 56:1512 - 21; http://dx.doi.org/10.1136/gut.2007.121244; PMID: 17604323
  • Cai C, Teng L, Vu D, He JQ, Guo Y, Li Q, Tang XL, Rokosh G, Bhatnagar A, Bolli R. The heme oxygenase 1 inducer (CoPP) protects human cardiac stem cells against apoptosis through activation of the extracellular signal-regulated kinase (ERK)/NRF2 signaling pathway and cytokine release. J Biol Chem 2012; 287:33720 - 32; http://dx.doi.org/10.1074/jbc.M112.385542; PMID: 22879597
  • Su J, Chen X, Huang Y, Li W, Li J, Cao K, Cao G, Zhang L, Li F, Roberts AI, et al. Phylogenetic distinction of iNOS and IDO function in mesenchymal stem cell-mediated immunosuppression in mammalian species. Cell Death Differ 2014; 21:388 - 96; http://dx.doi.org/10.1038/cdd.2013.149; PMID: 24162664
  • Bernardo ME, Fibbe WE. Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell 2013; 13:392 - 402; http://dx.doi.org/10.1016/j.stem.2013.09.006; PMID: 24094322
  • Najar M, Raicevic G, Boufker HI, Fayyad Kazan H, De Bruyn C, Meuleman N, Bron D, Toungouz M, Lagneaux L. Mesenchymal stromal cells use PGE2 to modulate activation and proliferation of lymphocyte subsets: Combined comparison of adipose tissue, Wharton’s Jelly and bone marrow sources. Cell Immunol 2010; 264:171 - 9; http://dx.doi.org/10.1016/j.cellimm.2010.06.006; PMID: 20619400
  • Ghannam S, Pène J, Moquet-Torcy G, Jorgensen C, Yssel H. Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol 2010; 185:302 - 12; http://dx.doi.org/10.4049/jimmunol.0902007; PMID: 20511548
  • Lee Y, Jung J, Cho KJ, Lee SK, Park JW, Oh IH, Kim GJ. Increased SCF/c-kit by hypoxia promotes autophagy of human placental chorionic plate-derived mesenchymal stem cells via regulating the phosphorylation of mTOR. J Cell Biochem 2013; 114:79 - 88; http://dx.doi.org/10.1002/jcb.24303; PMID: 22833529
  • Herberg S, Shi X, Johnson MH, Hamrick MW, Isales CM, Hill WD. Stromal cell-derived factor-1β mediates cell survival through enhancing autophagy in bone marrow-derived mesenchymal stem cells. PLoS One 2013; 8:e58207; http://dx.doi.org/10.1371/journal.pone.0058207; PMID: 23472159
  • Sridhar S, Botbol Y, Macian F, Cuervo AM. Autophagy and disease: always two sides to a problem. J Pathol 2012; 226:255 - 73; http://dx.doi.org/10.1002/path.3025; PMID: 21990109
  • Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003; 112:1809 - 20; http://dx.doi.org/10.1172/JCI20039; PMID: 14638851
  • Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 2003; 100:15077 - 82; http://dx.doi.org/10.1073/pnas.2436255100; PMID: 14657337
  • Aita VM, Liang XH, Murty VV, Pincus DL, Yu W, Cayanis E, Kalachikov S, Gilliam TC, Levine B. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 1999; 59:59 - 65; http://dx.doi.org/10.1006/geno.1999.5851; PMID: 10395800