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Review

Cell therapy for type 1 diabetes

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Pages 887-897 | Received 30 Oct 2019, Accepted 25 Mar 2020, Published online: 17 Apr 2020

References

  • Nathan DM, Genuth S, Lachin J, et al. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993 Sep 30;329(14):977–986. PubMed PMID: 8366922.
  • Pepper AR, Bruni A, Shapiro AMJ. Clinical islet transplantation: is the future finally now? Curr Opin Organ Transplant. 2018 Aug;23(4):428–439. PubMed PMID: 29847441.
  • Bassi R, Fiorina P. Impact of islet transplantation on diabetes complications and quality of life. Curr Diab Rep. 2011 Oct;11(5):355–363. PubMed PMID: 21748256.
  • Nir T, Melton DA, Dor Y. Recovery from diabetes in mice by beta cell regeneration. J Clin Invest. 2007 Sep;117(9):2553–2561. PubMed PMID: 17786244; PubMed Central PMCID: PMCPMC1957545.
  • Shapiro AM, Pokrywczynska M, Ricordi C. Clinical pancreatic islet transplantation. Nat Rev Endocrinol. 2017 May;13(5):268–277. PubMed PMID: 27834384.
  • Ben Nasr M, D’Addio F, Usuelli V, et al. The rise, fall, and resurgence of immunotherapy in type 1 diabetes. Pharmacol Res. 2015 Aug;98:31–38. PubMed PMID: 25107501.
  • Navarro-Tableros V, Gomez Y, Brizzi MF, et al. Generation of human stem cell-derived Pancreatic Organoids (POs) for regenerative medicine. New York, NY: Springer; 2019. p. 1–42.
  • Sneddon JB, Tang Q, Stock P, et al. Stem cell therapies for treating diabetes: progress and remaining challenges. Cell Stem Cell. 2018 Jun 1;22(6):810–823. PubMed PMID: 29859172; PubMed Central PMCID: PMCPMC6007036.
  • Liu X, Li X, Zhang N, et al. Engineering beta-cell islets or islet-like structures for type 1 diabetes treatment. Med Hypotheses. 2015 Jul;85(1):82–84. PubMed PMID: 25892491.
  • Spence A, Tang Q. Restoring regulatory T cells in Type 1 diabetes. Curr Diab Rep. 2016 Nov;16(11):110. PubMed PMID: 27664043.
  • Brusko TM, Wasserfall CH, Clare-Salzler MJ, et al. Functional defects and the influence of age on the frequency of CD4+ CD25+ T-cells in type 1 diabetes. Diabetes. 2005 May;54(5):1407–1414. PubMed PMID: 15855327.
  • Kukreja A, Cost G, Marker J, et al. Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest. 2002 Jan;109(1):131–140. PubMed PMID: 11781358; PubMed Central PMCID: PMCPMC150819.
  • Putnam AL, Vendrame F, Dotta F, et al. CD4+CD25high regulatory T cells in human autoimmune diabetes. J Autoimmun. 2005 Feb;24(1):55–62. PubMed PMID: 15725577.
  • Bluestone JA, Buckner JH, Fitch M, et al. Type 1 diabetes immunotherapy using polyclonal regulatory T cells. Sci Transl Med. 2015 Nov 25;7(315):315ra189. PubMed PMID: 26606968; PubMed Central PMCID: PMCPMC4729454.
  • Bluestone JA, Tang Q. Treg cells-the next frontier of cell therapy. Science. 2018 Oct 12;362(6411):154–155. PubMed PMID: 30309932.
  • Marek-Trzonkowska N, Mysliwiec M, Dobyszuk A, et al. Therapy of type 1 diabetes with CD4(+)CD25(high)CD127-regulatory T cells prolongs survival of pancreatic islets - results of one year follow-up. Clin Immunol. 2014 Jul;153(1):23–30. PubMed PMID: 24704576.
  • Marek-Trzonkowska N, Mysliwiec M, Iwaszkiewicz-Grzes D, et al. Factors affecting long-term efficacy of T regulatory cell-based therapy in type 1 diabetes. J Transl Med. 2016 Dec 1;14(1):332. PubMed PMID: 27903296; PubMed Central PMCID: PMCPMC5131539.
  • Visperas A, Vignali DA. Are regulatory T cells defective in Type 1 diabetes and can we fix them? J Immunol. 2016 Nov 15;197(10):3762–3770. PubMed PMID: 27815439; PubMed Central PMCID: PMCPMC5119643.
  • Masteller EL, Warner MR, Tang Q, et al. Expansion of functional endogenous antigen-specific CD4+CD25+ regulatory T cells from nonobese diabetic mice. J Immunol. 2005 Sep 1;175(5):3053–3059. PubMed PMID: 16116193.
  • Tarbell KV, Petit L, Zuo X, et al. Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med. 2007 Jan 22;204(1):191–201. PubMed PMID: 17210729; PubMed Central PMCID: PMCPMC2118426.
  • Hull CM, Nickolay LE, Estorninho M, et al. Generation of human islet-specific regulatory T cells by TCR gene transfer. J Autoimmun. 2017 May;79:63–73. PubMed PMID: 28117148.
  • Tenspolde M, Zimmermann K, Weber LC, et al. Regulatory T cells engineered with a novel insulin-specific chimeric antigen receptor as a candidate immunotherapy for type 1 diabetes. J Autoimmun. 2019 Jun 5:102289. PubMed PMID: 31176558. DOI:10.1016/j.jaut.2019.05.017
  • Izquierdo C, Ortiz AZ, Presa M, et al. Treatment of T1D via optimized expansion of antigen-specific Tregs induced by IL-2/anti-IL-2 monoclonal antibody complexes and peptide/MHC tetramers. Sci Rep. 2018 May 25;8(1):8106. PubMed PMID: 29802270; PubMed Central PMCID: PMCPMC5970271.
  • D’Addio F, Valderrama Vasquez A, Ben Nasr M, et al. Autologous nonmyeloablative hematopoietic stem cell transplantation in new-onset type 1 diabetes: a multicenter analysis. Diabetes. 2014 Sep;63(9):3041–3046. PubMed PMID: 24947362.
  • Couri CE, Oliveira MC, Stracieri AB, et al. C-peptide levels and insulin independence following autologous nonmyeloablative hematopoietic stem cell transplantation in newly diagnosed type 1 diabetes mellitus. JAMA. 2009 Apr 15;301(15):1573–1579. PubMed PMID: 19366777.
  • Ben Nasr M, Vergani A, Avruch J, et al. Co-transplantation of autologous MSCs delays islet allograft rejection and generates a local immunoprivileged site. Acta Diabetol. 2015;52:917–927.
  • Montanucci P, Pescara T, Alunno A, et al. Remission of hyperglycemia in spontaneously diabetic NOD mice upon transplant of microencapsulated human umbilical cord Wharton jelly-derived mesenchymal stem cells (hUCMS). Xenotransplantation. 2019 Mar;26(2):e12476. PubMed PMID: 30552781.
  • Ohmura Y, Tanemura M, Kawaguchi N, et al. Combined transplantation of pancreatic islets and adipose tissue-derived stem cells enhances the survival and insulin function of islet grafts in diabetic mice. Transplantation. 2010 Dec 27;90(12):1366–1373. PubMed PMID: 21076379.
  • Carlsson PO, Schwarcz E, Korsgren O, et al. Preserved beta-cell function in type 1 diabetes by mesenchymal stromal cells. Diabetes. 2015 Feb;64(2):587–592. PubMed PMID: 25204974.
  • Fallarino F, Luca G, Calvitti M, et al. Therapy of experimental type 1 diabetes by isolated Sertoli cell xenografts alone. J Exp Med. 2009 Oct 26;206(11):2511–2526. PubMed PMID: 19822646; PubMed Central PMCID: PMCPMC2768846.
  • Penaforte-Saboia JG, Montenegro RM Jr., Couri CE, et al. Microvascular complications in Type 1 diabetes: a comparative analysis of patients treated with autologous nonmyeloablative hematopoietic stem-cell transplantation and conventional medical therapy. Front Endocrinol (Lausanne). 2017:8:331. PubMed PMID: 29218029; PubMed Central PMCID: PMCPMC5703738.
  • van Megen KM, van ‘T Wout ET, Forman SJ, et al. A future for autologous hematopoietic stem cell transplantation in Type 1 diabetes. Front Immunol. 2018;9:690. PubMed PMID: 29696017; PubMed Central PMCID: PMCPMC5904498.
  • Ben Nasr M, Bassi R, Usuelli V, et al. The use of hematopoietic stem cells in autoimmune diseases. Regen Med. 2016 Jun;11(4):395–405. PubMed PMID: 27165670.
  • Muraro PA, Robins H, Malhotra S, et al. T cell repertoire following autologous stem cell transplantation for multiple sclerosis. J Clin Invest. 2014 Mar;124(3):1168–1172. PubMed PMID: 24531550; PubMed Central PMCID: PMCPMC3934160.
  • Alexander T, Thiel A, Rosen O, et al. Depletion of autoreactive immunologic memory followed by autologous hematopoietic stem cell transplantation in patients with refractory SLE induces long-term remission through de novo generation of a juvenile and tolerant immune system. Blood. 2009 Jan 1;113(1):214–223. PubMed PMID: 18824594.
  • Darlington PJ, Touil T, Doucet JS, et al. Diminished Th17 (not Th1) responses underlie multiple sclerosis disease abrogation after hematopoietic stem cell transplantation. Ann Neurol. 2013 Mar;73(3):341–354. PubMed PMID: 23463494.
  • Malmegrim KC, de Azevedo JT, Arruda LC, et al. Immunological balance is associated with clinical outcome after autologous hematopoietic stem cell transplantation in Type 1 diabetes. Front Immunol. 2017;8:167. PubMed PMID: 28275376; PubMed Central PMCID: PMCPMC5319960.
  • Ben Nasr M, Tezza S, D’Addio F, et al. PD-L1 genetic overexpression or pharmacological restoration in hematopoietic stem and progenitor cells reverses autoimmune diabetes. Sci Transl Med. 2017 Nov 15;9(416). PubMed PMID: 29141886; PubMed Central PMCID: PMCPMC6171337. DOI:10.1126/scitranslmed.aam7543.
  • Mukherjee G, Dilorenzo TP. The immunotherapeutic potential of dendritic cells in type 1 diabetes. Clin Exp Immunol. 2010 Aug;161(2):197–207. PubMed PMID: 20491789; PubMed Central PMCID: PMCPMC2909402.
  • Serreze DV, Gaskins HR, Leiter EH. Defects in the differentiation and function of antigen presenting cells in NOD/Lt mice. J Immunol. 1993 Mar 15;150(6):2534–2543. PubMed PMID: 8450229.
  • Vasquez AC, Feili-Hariri M, Tan RJ, et al. Qualitative and quantitative abnormalities in splenic dendritic cell populations in NOD mice. Clin Exp Immunol. 2004 Feb;135(2):209–218. PubMed PMID: 14738447; PubMed Central PMCID: PMCPMC1808940.
  • Morel PA. Dendritic cell subsets in type 1 diabetes: friend or foe? Front Immunol. 2013 Dec 6;4:415. PubMed PMID: 24367363; PubMed Central PMCID: PMCPMC3853773.
  • Danova K, Grohova A, Strnadova P, et al. Tolerogenic dendritic cells from poorly compensated Type 1 diabetes patients have decreased ability to induce stable antigen-specific T cell hyporesponsiveness and generation of suppressive regulatory T cells. J Immunol. 2017 Jan 15;198(2):729–740. PubMed PMID: 27927966.
  • Maldonado RA, von Andrian UH. How tolerogenic dendritic cells induce regulatory T cells. Adv Immunol. 2010;108:111–165. PubMed PMID: 21056730; PubMed Central PMCID: PMCPMC3050492.
  • Morel PA, Turner MS. Dendritic cells and the maintenance of self-tolerance. Immunol Res. 2011 Aug;50(2–3):124–129. PubMed PMID: 21717078.
  • Kleffel S, Vergani A, Tezza S, et al. Interleukin-10+ regulatory B cells arise within antigen-experienced CD40+ B cells to maintain tolerance to islet autoantigens. Diabetes. 2015 Jan;64(1):158–171. PubMed PMID: 25187361; PubMed Central PMCID: PMCPMC4274804.
  • Stojanovic I, Dimitrijevic M, Vives-Pi M, et al. Cell-based Tolerogenic Therapy, Experience from Animal Models of Multiple Sclerosis, Type 1 Diabetes and Rheumatoid Arthritis. Curr Pharm Des. 2017;23(18):2623–2643. PubMed PMID: 28201972.
  • Funda DP, Palova-Jelinkova L, Golias J, et al. Optimal Tolerogenic Dendritic Cells in Type 1 Diabetes (T1D) Therapy: what Can We Learn From Non-obese Diabetic (NOD) Mouse Models? Front Immunol. 2019;10:967. PubMed PMID: 31139178; PubMed Central PMCID: PMCPMC6527741.
  • Clare-Salzler MJ, Brooks J, Chai A, et al. Prevention of diabetes in nonobese diabetic mice by dendritic cell transfer. J Clin Invest. 1992 Sep;90(3):741–748. PubMed PMID: 1522229; PubMed Central PMCID: PMCPMC329925.
  • Creusot RJ, Giannoukakis N, Trucco M, et al. It’s time to bring dendritic cell therapy to type 1 diabetes. Diabetes. 2014 Jan;63(1):20–30. PubMed PMID: 24357690; PubMed Central PMCID: PMCPMC3968436.
  • Worbs T, Hammerschmidt SI, Forster R. Dendritic cell migration in health and disease. Nat Rev Immunol. 2017 Jan;17(1):30–48. PubMed PMID: 27890914.
  • Feili-Hariri M, Falkner DH, Gambotto A, et al. Dendritic cells transduced to express interleukin-4 prevent diabetes in nonobese diabetic mice with advanced insulitis. Hum Gene Ther. 2003 Jan 1;14(1):13–23. PubMed PMID: 12573055.
  • Tai N, Yasuda H, Xiang Y, et al. IL-10-conditioned dendritic cells prevent autoimmune diabetes in NOD and humanized HLA-DQ8/RIP-B7.1 mice. Clin Immunol. 2011 Jun;139(3):336–349. PubMed PMID: 21458378.
  • Ten Brinke A, Hilkens CM, Cools N, et al. Clinical use of tolerogenic dendritic cells-harmonization approach in european collaborative effort. Mediators Inflamm. 2015;2015:471719. PubMed PMID: 26819498; PubMed Central PMCID: PMCPMC4706930.
  • Giannoukakis N, Phillips B, Finegold D, et al. Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients. Diabetes Care. 2011 Sep;34(9):2026–2032. PubMed PMID: 21680720; PubMed Central PMCID: PMCPMC3161299.
  • Di Caro V, Phillips B, Engman C, et al. Involvement of suppressive B-lymphocytes in the mechanism of tolerogenic dendritic cell reversal of type 1 diabetes in NOD mice. PLoS One. 2014;9(1):e83575. PubMed PMID: 24465383; PubMed Central PMCID: PMCPMC3894962.
  • Phillips BE, Garciafigueroa Y, Engman C, et al. Tolerogenic dendritic cells and T-regulatory cells at the clinical trials crossroad for the treatment of autoimmune disease; emphasis on Type 1 diabetes therapy. Front Immunol. 2019;10:148. PubMed PMID: 30787930; PubMed Central PMCID: PMCPMC6372505.
  • Dalod M, Chelbi R, Malissen B, et al. Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. Embo J. 2014 May 16;33(10):1104–1116. PubMed PMID: 24737868; PubMed Central PMCID: PMCPMC4193918.
  • D’Amour KA, Agulnick AD, Eliazer S, et al. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol. 2005 Dec;23(12):1534–1541. PubMed PMID: 16258519. .
  • Kroon E, Martinson LA, Kadoya K, et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol. 2008;26:443–452.
  • D’Amour KA, Bang AG, Eliazer S, et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol. 2006;24:1392–1401.
  • Rezania A, Bruin JE, Riedel MJ, et al. Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice. Diabetes. 2012 Aug;61(8):2016–2029. PubMed PMID: 22740171; PubMed Central PMCID: PMCPMC3402300.
  • Rezania A, Bruin JE, Arora P, et al. Reversal of diabetes with insulin-producing cells derived in vitro from human pluripotent stem cells. Nat Biotechnol. 2014;32:1121–1133.
  • Pagliuca FW, Millman JR, Gurtler M, et al. Generation of functional human pancreatic beta cells in vitro. Cell. 2014 Oct 9;159(2):428–439. PubMed PMID: 25303535; PubMed Central PMCID: PMCPMC4617632.
  • Russ HA, Parent AV, Ringler JJ, et al. Controlled induction of human pancreatic progenitors produces functional beta-like cells in vitro. Embo J. 2015;34:1759–1772.
  • Rosado-Olivieri EA, Anderson K, Kenty JH, et al. YAP inhibition enhances the differentiation of functional stem cell-derived insulin-producing β cells. Nat Commun. 2019;10:1464.
  • Velazco-Cruz L, Song J, Maxwell KG, et al. Acquisition of dynamic function in human stem cell-derived β cells. Stem Cell Reports. 2019;12:351–365.
  • Sharon N, Vanderhooft J, Straubhaar J, et al. Wnt signaling separates the progenitor and endocrine compartments during pancreas development. Cell Rep. 2019;27:2281–2291.e5.
  • Veres A, Faust AL, Bushnell HL, et al. Charting cellular identity during human in vitro β-cell differentiation. Nature. 2019;569:368–373.
  • Shahjalal HM, Abdal Dayem A, Lim KM, et al. Generation of pancreatic β cells for treatment of diabetes: advances and challenges. Stem Cell Res Ther. 2018:9:355. PubMed PMID: 30594258.
  • Henry RR, Pettus J, Wilensky J, et al. Initial clinical evaluation of VC-01TM combination product—a stem cell–derived islet replacement for Type 1 Diabetes (T1D). Diabetes. 2018;67:138–OR.
  • Chayosumrit M, Tuch B, Sidhu K. Alginate microcapsule for propagation and directed differentiation of hESCs to definitive endoderm. Biomaterials. 2010 Jan;31(3):505–514. PubMed PMID: 19833385.
  • Tuch BE, Keogh GW, Williams LJ, et al. Safety and viability of microencapsulated human islets transplanted into diabetic humans. Diabetes Care. 2009 Oct;32(10):1887–1889. PubMed PMID: 19549731; PubMed Central PMCID: PMCPMC2752920.
  • Calafiore R, Basta G, Luca G, et al. Microencapsulated pancreatic islet allografts into nonimmunosuppressed patients with type 1 diabetes: first two cases. Diabetes Care. 2006 Jan;29(1):137–138. PubMed PMID: 16373911.
  • Calafiore R. Microencapsulation for cell therapy of type 1 diabetes mellitus: the interplay between common beliefs, prejudices and real progress. J Diabetes Investig. 2018 Mar;9(2):231–233. PubMed PMID: 29215800; PubMed Central PMCID: PMCPMC5835460.
  • Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–676. PubMed PMID: 16904174.
  • Teo AKK, Wagers AJ, Kulkarni RN. New opportunities: harnessing induced pluripotency for discovery in diabetes and metabolism. Cell Metab. 2013;18:775–791. PubMed PMID: 24035588.
  • Tateishi K, He J, Taranova O, et al. Generation of insulin-secreting islet-like clusters from human skin fibroblasts. J Biol Chem. 2008;283:31601–31607. PubMed PMID: 18782754.
  • Bai Q, Desprat R, Klein B, et al. Embryonic stem cells or induced pluripotent stem cells? A DNA integrity perspective. Curr Gene Ther. 2013;13:93–98. PubMed PMID: 23317057.
  • Kondo Y, Toyoda T, Inagaki N, et al. iPSC technology-based regenerative therapy for diabetes. J Diabetes Investig. 2018;9:234–243. PubMed PMID: 28609558.
  • Pagliuca FW, Melton DA. How to make a functional β-cell. Development. 2013;140:2472–2483. PubMed PMID: 23715541.
  • Alagpulinsa DA, Cao JJL, Driscoll RK, et al. Alginate-microencapsulation of human stem cell-derived beta cells with CXCL12 prolongs their survival and function in immunocompetent mice without systemic immunosuppression. Am J Transplant. 2019 Jul;19(7):1930–1940. PubMed PMID: 30748094. .
  • Omole AE, Fakoya AOJ. Ten years of progress and promise of induced pluripotent stem cells: historical origins, characteristics, mechanisms, limitations, and potential applications. PeerJ. 2018;6:e4370.
  • Medvedev SP, Shevchenko AI, Zakian SM. Induced pluripotent stem cells: problems and advantages when applying them in regenerative medicine. Acta naturae. 2010;2:18–28. PubMed PMID: 22649638.
  • Warlich E, Kuehle J, Cantz T, et al. Lentiviral vector design and imaging approaches to visualize the early stages of cellular reprogramming. Mol Ther. 2011;19:782–789. PubMed PMID: 21285961.
  • González F, Boué S, Belmonte JCI. Methods for making induced pluripotent stem cells: reprogramming à la carte. Nat Rev Genet. 2011;12:231–242. PubMed PMID: 21339765.
  • Doi D, Samata B, Katsukawa M, et al. Isolation of human induced pluripotent stem cell-derived dopaminergic progenitors by cell sorting for successful transplantation. Stem Cell Reports. 2014;2:337–350. PubMed PMID: 24672756.
  • Okubo T, Iwanami A, Kohyama J, et al. Pretreatment with a γ-secretase inhibitor prevents tumor-like overgrowth in human iPSC-derived transplants for spinal cord injury. Stem Cell Reports. 2016;7:649–663. PubMed PMID: 27666789.
  • Itakura G, Kawabata S, Ando M, et al. Stem Cell Reports Ar ticle Fail-Safe System against Potential Tumorigenicity after Transplantation of iPSC Derivatives. 2017. doi: 10.1016/j.stemcr.2017.02.003.
  • Ben Jehuda R, Shemer Y, Binah O. Genome editing in induced pluripotent stem cells using CRISPR/Cas9. Stem Cell Rev Rep. 2018;14:323–336.
  • Kim K, Doi A, Wen B, et al. Epigenetic memory in induced pluripotent stem cells. Nature. 2010;467:285–290. PubMed PMID: 20644535.
  • Maehr R. iPS cells in Type 1 diabetes research and treatment. Clin Pharmacol Ther. 2011;89:750–753.
  • Sneddon JB, Tang Q, Stock P, et al. Cell stem cell perspective stem cell therapies for treating diabetes: progress and remaining challenges. Stem Cell. 2018;22:810–823.
  • Odorico J, Markmann J, Melton D, et al. Report of the key opinion leaders meeting on stem cell-derived beta cells. Transplantation. 2018 Aug;102(8):1223–1229. PubMed PMID: 29781950.
  • Han X, Wang M, Duan S, et al. Generation of hypoimmunogenic human pluripotent stem cells. Proc Nat Acad Sci. 2019:116:10441–10446. PubMed PMID: 31040209.
  • Qadir MMF, Álvarez-Cubela S, Belle K, et al. A double fail-safe approach to prevent tumorigenesis and select pancreatic β cells from human embryonic stem cells. Stem Cell Reports. 2019;12:611–623. .

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