Assessing the immunosuppressive activity of alginate-encapsulated mesenchymal stromal cells on splenocytes

References

• Rashidghamat E, Kadiyirire T, Ayis S, et al. Phase I/II open-label trial of intravenous allogeneic mesenchymal stromal cell therapy in adults with recessive dystrophic epidermolysis bullosa. J Am Acad Dermatol. 2020;83(2):447–454.
   PubMed Web of Science ®Google Scholar
• Galleu A, Riffo-Vasquez Y, Trento C, et al. Apoptosis in mesenchymal stromal cells induces in vivo recipient-mediated immunomodulation. Sci Transl Med. 2017;9(416):eaam7828.
   PubMed Web of Science ®Google Scholar
• Muller L, Tunger A, Wobus M, et al. Immunomodulatory properties of mesenchymal stromal cells: an update. Front Cell Dev Biol. 2021;9(637725):637725.
   PubMedGoogle Scholar
• Wu X, Jiang J, Gu Z, et al. Mesenchymal stromal cell therapies: immunomodulatory properties and clinical progress. Stem Cell Res Ther. 2020;11(1):345.
   PubMed Web of Science ®Google Scholar
• Burnham AJ, Foppiani EM, Horwitz EM. Key metabolic pathways in MSC-Mediated immunomodulation: Implications for the prophylaxis and treatment of graft versus host disease. Front Immunol. 2020;11:609277.
   PubMed Web of Science ®Google Scholar
• Dotoli GM, De Santis GC, Orellana MD, et al. Mesenchymal stromal cell infusion to treat steroid-refractory acute GvHD III/IV after hematopoietic stem cell transplantation. Bone Marrow Transplant. 2017;52(6):859–862.
   PubMed Web of Science ®Google Scholar
• Mao F, Tu Q, Wang L, et al. Mesenchymal stem cells and their therapeutic applications in inflammatory bowel disease. Oncotarget. 2017;8(23):38008–38021.
   PubMedGoogle Scholar
• Khan S, Khan RS, Newsome PN. Cellular therapies for the treatment of immune-mediated GI and liver disease. Br Med Bull. 2020;136(1):127–141.
   PubMed Web of Science ®Google Scholar
• Zhao X, Zhao Y, Sun X, et al. Immunomodulation of MSCs and MSC-derived extracellular vesicles in osteoarthritis. Front Bioeng Biotechnol. 2020;8(575057):575057.
   PubMedGoogle Scholar
• Harrell CR, Markovic BS, Fellabaum C, et al. Mesenchymal stem cell-based therapy of osteoarthritis: current knowledge and future perspectives. Biomed Pharmacother. 2019;109:2318–2326.
   PubMed Web of Science ®Google Scholar
• de Witte SFH, Luk F, Sierra Parraga JM, et al. Immunomodulation by therapeutic mesenchymal stromal cells (MSC) is triggered through phagocytosis of MSC by monocytic cells. Stem Cells. 2018;36(4):602–615.
   PubMed Web of Science ®Google Scholar
• Riazifar M, Mohammadi MR, Pone EJ, et al. Stem Cell-Derived exosomes as nanotherapeutics for autoimmune and neurodegenerative disorders. ACS Nano. 2019;13(6):6670–6688.
   PubMed Web of Science ®Google Scholar
• Mohammadi M, Luong JC, Rodriguez SM, et al. Controlled release of stem cell secretome attenuates inflammatory response against implanted biomaterials. Adv Healthcare Mater. 2020;9(12):e1901874.
   Web of Science ®Google Scholar
• Cheung TS, Bertolino GM, Giacomini C, et al. Mesenchymal stromal cells for graft versus host disease: Mechanism-Based biomarkers. Front Immunol. 2020;11:1338.
   PubMed Web of Science ®Google Scholar
• Prasanna SJ, Gopalakrishnan D, Shankar SR, et al. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLOS One. 2010;5(2):e9016.
   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
• Poggi A, Varesano S, Zocchi MR. How to hit mesenchymal stromal cells and make the tumor microenvironment immunostimulant rather than immunosuppressive. Front Immunol. 2018;9:262.
   PubMed Web of Science ®Google Scholar
• English K, Ryan JM, Tobin L, et al. Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4 + CD25(high) forkhead box P3+ regulatory T cells. Clin Exp Immunol. 2009;156(1):149–160.
   PubMed Web of Science ®Google Scholar
• Bazzoni R, Kamga T, Tanasi P, et al. Extracellular vesicle-dependent communication between mesenchymal stromal cells and immune effector cells. Front Cell Dev Biol. 2020;8:596079.
   PubMed Web of Science ®Google Scholar
• Mohammadi MR, Rodriguez SM, Luong JC, et al. Exosome loaded immunomodulatory biomaterials alleviate local immune response in immunocompetent diabetic mice post islet xenotransplantation. Commun Biol. 2021;4(1):685.
   PubMed Web of Science ®Google Scholar
• Kraitchman DL, Tatsumi M, Gilson WD, et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation. 2005;112(10):1451–1461.
   PubMed Web of Science ®Google Scholar
• Eggenhofer E, Benseler V, Kroemer A, et al. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front Immunol. 2012;3:297.
   PubMed Web of Science ®Google Scholar
• Eggenhofer E, Luk F, Dahlke MH, et al. The life and fate of mesenchymal stem cells. Front Immunol. 2014;5(148):148.
   PubMedGoogle Scholar
• Li L, Chen X, Wang WE, et al. How to improve the survival of transplanted mesenchymal stem cell in ischemic heart? Stem Cells Int. 2016;2016:9682757.
   PubMed Web of Science ®Google Scholar
• Hocking AM. The role of chemokines in mesenchymal stem cell homing to wounds. Adv Wound Care. 2015;4(11):623–630.
   Web of Science ®Google Scholar
• Stucky EC, Schloss RS, Yarmush ML, et al. Alginate micro-encapsulation of mesenchymal stromal cells enhances modulation of the neuro-inflammatory response. Cytotherapy. 2015;17(10):1353–1364.
   PubMed Web of Science ®Google Scholar
• Bujoli B, Scimeca JC, Verron E. Fibrin as a multipurpose physiological platform for bone tissue engineering and targeted delivery of bioactive compounds. Pharmaceutics. 2019;11(11):556.
   PubMed Web of Science ®Google Scholar
• Gomez-Florit M, Pardo A, Domingues RMA, et al. Natural-Based hydrogels for tissue engineering applications. Molecules. 2020;25(24):5858.
   PubMed Web of Science ®Google Scholar
• Heher P, Mühleder S, Mittermayr R, et al. Fibrin-based delivery strategies for acute and chronic wound healing. Adv Drug Deliv Rev. 2018;129:134–147.
   PubMed Web of Science ®Google Scholar
• Heo DN, Hospodiuk M, Ozbolat IT. Synergistic interplay between human MSCs and HUVECs in 3D spheroids laden in collagen/fibrin hydrogels for bone tissue engineering. Acta Biomater. 2019;95:348–356.
   PubMed Web of Science ®Google Scholar
• Zhang F, King MW. Biodegradable polymers as the pivotal player in the design of tissue engineering scaffolds. Adv Healthc Mater. 2020;9(13):e1901358.
   PubMed Web of Science ®Google Scholar
• Ho SS, Murphy KC, Binder BY, et al. Increased survival and function of mesenchymal stem cell spheroids entrapped in instructive alginate hydrogels. Stem Cells Transl Med. 2016;5(6):773–781.
   PubMed Web of Science ®Google Scholar
• Liu ZC, Chang TMS. Artificial cell microencapsulated stem cells in regenerative medicine, tissue engineering and cell therapy. Adv Exp Med Biol. 2010;670:68–79.
   PubMed Web of Science ®Google Scholar
• Bulman SE, Coleman CM, Murphy JM, et al. Pullulan: a new cytoadhesive for cell-mediated cartilage repair. Stem Cell Res Ther. 2015;6:34.
   PubMed Web of Science ®Google Scholar
• Gao Y, Kong W, Li B, et al. Fabrication and characterization of collagen-based injectable and self-crosslinkable hydrogels for cell encapsulation. Colloids Surf B Biointerfaces. 2018;167:448–456.
   PubMed Web of Science ®Google Scholar
• Lam D, Enright HA, Peters SKG, et al. Optimizing cell encapsulation condition in ECM-Collagen I hydrogels to support 3D neuronal cultures. J Neurosci Methods. 2020;329:108460.
   PubMed Web of Science ®Google Scholar
• Orive G, Ponce S, Hernández RM, et al. Biocompatibility of microcapsules for cell immobilization elaborated with different type of alginates. Biomaterials. 2002;23(18):3825–3831.
   PubMed Web of Science ®Google Scholar
• Farah S, Doloff JC, Müller P, et al. Long-term implant fibrosis prevention in rodents and non-human primates using crystallized drug formulations. Nat Mater. 2019;18(8):892–904.
   PubMed Web of Science ®Google Scholar
• Chen T, Yuan J, Duncanson S, et al. Alginate encapsulant incorporating CXCL12 supports long-term allo- and xenoislet transplantation without systemic immune suppression. Am J Transplant. 2015;15(3):618–627.
   PubMed Web of Science ®Google Scholar
• Khatab S, Leijs MJ, van Buul G, et al. MSC encapsulation in alginate microcapsules prolongs survival after intra-articular injection, a longitudinal in vivo cell and bead integrity tracking study. Cell Biol Toxicol. 2020;36(6):553–570.
   PubMed Web of Science ®Google Scholar
• McKinney JM, Pucha KA, Doan TN, et al. Sodium alginate microencapsulation of human mesenchymal stromal cells modulates paracrine signaling response and enhances efficacy for treatment of established osteoarthritis. Acta Biomater. 2021;15(141):315–332.
   PubMed Web of Science ®Google Scholar
• Fathi E, Farahzadi R, Valipour B. Alginate/gelatin encapsulation promotes NK cells differentiation potential of bone marrow resident C-kit + hematopoietic stem cells. Int J Biol Macromol. 2021;177:317–327.
   PubMed Web of Science ®Google Scholar
• Putra A, Ridwan FB, Putridewi AI, et al. The role of TNF-α induced MSCs on suppressive inflammation by increasing TGF-Î2 and IL-10. Open Access Maced J Med Sci. 2018;6(10):1779–1783.
   PubMedGoogle Scholar
• Polchert D, Sobinsky J, Douglas G, et al. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol. 2008;38(6):1745–1755.
   PubMed Web of Science ®Google Scholar
• Meisel R, Zibert A, Laryea M, et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004;103(12):4619–4621.
   PubMed Web of Science ®Google Scholar
• Vladimirovna IL, Sosunova E, Nikolaev A, et al. Mesenchymal stem cells and myeloid derived suppressor cells: common traits in immune regulation. J Immunol Res. 2016;2016:7121580.
   PubMed Web of Science ®Google Scholar
• Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99(10):3838–3843.
   PubMed Web of Science ®Google Scholar
• Weiss ARR, Dahlke MH. Immunomodulation by mesenchymal stem cells (MSCs): mechanisms of action of living, apoptotic, and dead MSCs. Front Immunol. 2019;10(1191):1191.
   PubMedGoogle Scholar
• Lenzini S, Bargi R, Chung G, et al. Matrix mechanics and water permeation regulate extracellular vesicle transport. Nat Nanotechnol. 2020;15(3):217–223.
   PubMed Web of Science ®Google Scholar
• Iansante V, Dhawan A, Masmoudi F, et al. A new high throughput screening platform for cell encapsulation in alginate hydrogel shows improved hepatocyte functions by mesenchymal stromal cells co-encapsulation. Front Med. 2018;5:216.
   Web of Science ®Google Scholar
• Syanda AM, Kringstad VI, Blackford SJI, et al. Sulfated alginate reduces pericapsular fibrotic overgrowth on encapsulated cGMP-Compliant hPSC-Hepatocytes in mice. Front Bioeng Biotechnol. 2022;9:816542.
   PubMed Web of Science ®Google Scholar
• Vegas AJ, Veiseh O, Doloff JC, et al. Combinatorial hydrogel library enables identification of materials that mitigate the foreign body response in primates. Nat Biotechnol. 2016;34(3):345–352.
   PubMed Web of Science ®Google Scholar
• Mao AS, Ozkale B, Shah NJ, et al. Programmable microencapsulation for enhanced mesenchymal stem cell persistence and immunomodulation. Proc Natl Acad Sci USA. 2019;116(31):15392–15397.
   PubMed Web of Science ®Google Scholar