Gastrin producing syngeneic mesenchymal stem cells protect non-obese diabetic mice from type 1 diabetes

References

• Lagani V, Koumakis L, Chiarugi F, et al. A systematic review of predictive risk models for diabetes complications based on large scale clinical studies. J Diabetes Complications. 2013;27(4):407–413.
   PubMed Web of Science ®Google Scholar
• Best CH. Some thoughts on the etiology of human diabetes. Can Med Assoc J. 1962;87:731–734.
   PubMed Web of Science ®Google Scholar
• Giannopoulou EZ, Puff R, Beyerlein A, et al. Effect of a single autologous cord blood infusion on beta-cell and immune function in children with new onset type 1 diabetes: a non-randomized, controlled trial. Pediatr Diabetes. 2014;15(2):100–109.
   PubMed Web of Science ®Google Scholar
• Haller MJ, Wasserfall CH, Hulme MA, et al. Autologous umbilical cord blood infusion followed by oral docosahexaenoic acid and vitamin D supplementation for C-peptide preservation in children with type 1 diabetes. Biol Blood Marrow Transpl. 2013;19(7):1126–1129.
   PubMed Web of Science ®Google Scholar
• Seay HR, Putnam AL, Cserny J, et al. Expansion of human tregs from cryopreserved umbilical cord blood for GMP-Compliant autologous adoptive cell transfer therapy. Mol Ther Methods Clin Dev. 2017;4:178–191.
   PubMed Web of Science ®Google Scholar
• 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 Web of Science ®Google Scholar
• Diaz-de-Durana Y, Lau J, Knee D, et al. IL-2 immunotherapy reveals potential for innate beta cell regeneration in the non-obese diabetic mouse model of autoimmune diabetes. PLoS One. 2013;8(10):e78483.
   PubMed Web of Science ®Google Scholar
• Manzoor F, Johnson MC, Li C, et al. β-cell-specific IL-35 therapy suppresses ongoing autoimmune diabetes in NOD mice. Eur J Immunol. 2017;47(1):144–154.
   PubMed Web of Science ®Google Scholar
• Goudy KS, Tisch R. Immunotherapy for the prevention and treatment of type 1 diabetes. Int Rev Immunol. 2005;24(5–6):307–326.
   PubMed Web of Science ®Google Scholar
• Alhadj Ali M, Liu YF, Arif S, et al. Metabolic and immune effects of immunotherapy with proinsulin peptide in human new-onset type 1 diabetes. Sci Transl Med. 2017;9:402.
   Web of Science ®Google Scholar
• Cho J, D’Antuono M, Glicksman M, et al. A review of clinical trials: mesenchymal stem cell transplant therapy in type 1 and type 2 diabetes mellitus. Am J Stem Cells. 2018;7(4):82–93.
   PubMed Web of Science ®Google Scholar
• Sambathkumar R, Migliorini A, Nostro MC. Pluripotent stem cell-derived pancreatic progenitors and β-like cells for type 1 diabetes treatment. Physiology. 2018;33(6):394–402.
   PubMed Web of Science ®Google Scholar
• Ma H, Wert KJ, Shvartsman D, et al. Establishment of human pluripotent stem cell-derived pancreatic β-like cells in the mouse pancreas. Proc Natl Acad Sci USA. 2018;115(15):3924–3929.
   PubMed Web of Science ®Google Scholar
• Abdi R, Fiorina P, Adra CN, et al. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes. 2008;57(7):1759–1767.
   PubMed Web of Science ®Google Scholar
• Madec AM, Mallone R, Afonso G, et al. Mesenchymal stem cells protect NOD mice from diabetes by inducing regulatory T cells. Diabetologia. 2009;52(7):1391–1399.
   PubMed Web of Science ®Google Scholar
• Glenn JD, Whartenby KA. Mesenchymal stem cells: emerging mechanisms of immunomodulation and therapy. World J Stem Cells. 2014;6(5):526–539.
   PubMedGoogle Scholar
• Le Blanc K, Ringden O. Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med. 2007;262(5):509–525.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276(5309):71–74.
   PubMed Web of Science ®Google Scholar
• Kucia M, Reca R, Jala VR, et al. Bone marrow as a home of heterogenous populations of nonhematopoietic stem cells. Leukemia. 2005;19(7):1118–1127.
   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
• Li M, Ikehara S. Bone-marrow-derived mesenchymal stem cells for organ repair. Stem Cells Int. 2013;2013:132642.
   PubMed Web of Science ®Google Scholar
• Patel DM, Shah J, Srivastava AS. Therapeutic potential of mesenchymal stem cells in regenerative medicine. Stem Cells Int. 2013;2013:496218.
   PubMed Web of Science ®Google Scholar
• Horwitz EM, Prockop DJ, Fitzpatrick LA, et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 1999;5(3):309–313.
   PubMed Web of Science ®Google Scholar
• Ji JF, He BP, Dheen ST, et al. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells. 2004;22(3):415–427.
   PubMed Web of Science ®Google Scholar
• Sordi V, Malosio ML, Marchesi F, et al. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood. 2005;106(2):419–427.
   PubMed Web of Science ®Google Scholar
• Wang B, Wu SM, Wang T, et al. Pre-treatment with bone marrow-derived mesenchymal stem cells inhibits systemic intravascular coagulation and attenuates organ dysfunction in lipopolysaccharide-induced disseminated intravascular coagulation rat model. Chin Med J. 2012;125(10):1753–1759.
   PubMed Web of Science ®Google Scholar
• Yu Y, Wu RX, Gao LN, et al. Stromal cell-derived factor-1-directed bone marrow mesenchymal stem cell migration in response to inflammatory and/or hypoxic stimuli. Cell Adh Migr. 2016;10(4):342–359.
   PubMed Web of Science ®Google Scholar
• Spaeth E, Klopp A, Dembinski J, et al. Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther. 2008;15(10):730–738.
   PubMed Web of Science ®Google Scholar
• Kallmeyer K, Pepper MS. Homing properties of mesenchymal stromal cells. Expert Opin Biol Ther. 2015;15(4):477–479.
   PubMed Web of Science ®Google Scholar
• Canibano-Hernandez A, Saenz Del Burgo L, Espona-Noguera A, et al. Hyaluronic acid promotes differentiation of mesenchymal stem cells from different sources toward pancreatic progenitors within three-dimensional alginate matrixes. Mol Pharm. 2019;16(2):834–845.
   PubMedGoogle Scholar
• Ojaghi M, Soleimanifar F, Kazemi A, et al. Electrospun poly-l-lactic acid/polyvinyl alcohol nanofibers improved insulin-producing cell differentiation potential of human adipose-derived mesenchymal stem cells. J Cell Biochem. 2019;120(6):9917–9926.
   PubMed Web of Science ®Google Scholar
• Kharat A, Chandravanshi B, Gadre S, et al. IGF-1 and somatocrinin trigger islet differentiation in human amniotic membrane derived mesenchymal stem cells. Life Sci. 2019;216:287–294.
   PubMed Web of Science ®Google Scholar
• Bassi EJ, Moraes-Vieira PM, Moreira-Sa CS, et al. Immune regulatory properties of allogeneic adipose-derived mesenchymal stem cells in the treatment of experimental autoimmune diabetes. Diabetes. 2012;61(10):2534–2545.
   PubMed Web of Science ®Google Scholar
• Fiorina P, Jurewicz M, Augello A, et al. Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J Immunol. 2009;183(2):993–1004.
   PubMed Web of Science ®Google Scholar
• Jurewicz M, Yang S, Augello A, et al. Congenic mesenchymal stem cell therapy reverses hyperglycemia in experimental type 1 diabetes. Diabetes. 2010;59(12):3139–3147.
   PubMed Web of Science ®Google Scholar
• de Lima KA, de Oliveira GL, Yaochite JN, et al. Transcriptional profiling reveals intrinsic mRNA alterations in multipotent mesenchymal stromal cells isolated from bone marrow of newly-diagnosed type 1 diabetes patients. Stem Cell Res Ther. 2016;7(1):92.
   PubMedGoogle Scholar
• Dang LT, Bui AN, Le-Thanh Nguyen C, et al. Intravenous infusion of human adipose tissue-derived mesenchymal stem cells to treat type 1 diabetic mellitus in mice: an evaluation of grafted cell doses. Adv Exp Med Biol. 2018;1083:145–156.
   PubMed Web of Science ®Google Scholar
• Suissa Y, Magenheim J, Stolovich-Rain M, et al. Gastrin: a distinct fate of neurogenin3 positive progenitor cells in the embryonic pancreas. PLoS One. 2013;8(8):e70397.
   PubMed Web of Science ®Google Scholar
• Dahan T, Ziv O, Horwitz E, et al. Pancreatic β-cells express the fetal islet hormone gastrin in rodent and human diabetes. Diabetes. 2017;66(2):426–436.
   PubMed Web of Science ®Google Scholar
• Khan D, Vasu S, Moffett RC, et al. Expression of gastrin family peptides in pancreatic islets and their role in β-cell function and survival. Pancreas. 2018;47(2):190–199.
   PubMed Web of Science ®Google Scholar
• Rooman I, Lardon J, Flamez D, et al. Mitogenic effect of gastrin and expression of gastrin receptors in duct-like cells of rat pancreas. Gastroenterology. 2001;121(4):940–949.
   PubMed Web of Science ®Google Scholar
• Perez N, Karumuthil-Melethil S, Li R, et al. Preferential costimulation by CD80 results in IL-10-dependent TGF-beta1(+) -adaptive regulatory T cell generation. J Immunol. 2008;180(10):6566–6576.
   PubMed Web of Science ®Google Scholar
• Li R, Perez N, Karumuthil-Melethil S, et al. Bone marrow is a preferential homing site for autoreactive T-cells in type 1 diabetes. Diabetes. 2007;56(9):2251–2259.
   PubMed Web of Science ®Google Scholar
• Karumuthil-Melethil S, Perez N, Li R, et al. Dendritic cell-directed CTLA-4 engagement during pancreatic beta cell antigen presentation delays type 1 diabetes. J Immunol. 2010;184(12):6695–6708.
   PubMed Web of Science ®Google Scholar
• Karumuthil-Melethil S, Sofi MH, Gudi R, et al. TLR2- and dectin 1-associated innate immune response modulates T-cell response to pancreatic β-cell antigen and prevents type 1 diabetes. Diabetes. 2015;64(4):1341–1357.
   PubMed Web of Science ®Google Scholar
• Karumuthil-Melethil S, Gudi R, Johnson BM, et al. Fungal β-glucan, a Dectin-1 ligand, promotes protection from type 1 diabetes by inducing regulatory innate immune response. J Immunol. 2014;193(7):3308–3321.
   PubMed Web of Science ®Google Scholar
• Gudi RR, Karumuthil-Melethil S, Perez N, et al. Engineered dendritic Cell-Directed concurrent activation of multiple T cell inhibitory pathways induces robust immune tolerance. Sci Rep. 2019;9(1):12065.
   PubMedGoogle Scholar
• Throm RE, Ouma AA, Zhou S, et al. Efficient construction of producer cell lines for a SIN lentiviral vector for SCID-X1 gene therapy by concatemeric array transfection. Blood. 2009;113(21):5104–5110.
   PubMed Web of Science ®Google Scholar
• Sofi MH, Gudi R, Karumuthil-Melethil S, et al. pH of drinking water influences the composition of gut microbiome and type 1 diabetes incidence. Diabetes. 2014;63(2):632–644.
   PubMed Web of Science ®Google Scholar
• Karumuthil-Melethil S, Perez N, Li R, et al. Induction of innate immune response through TLR2 and dectin 1 prevents type 1 diabetes. J Immunol. 2008;181(12):8323–8334.
   PubMed Web of Science ®Google Scholar
• Hu J, Wang Y, Wang F, et al. Effect and mechanisms of human Wharton’s jelly-derived mesenchymal stem cells on type 1 diabetes in NOD model. Endocrine. 2015;48(1):124–134.
   PubMed Web of Science ®Google Scholar
• Shulkes A, Baldwin GS. Biology of gut cholecystokinin and gastrin receptors. Clin Exp Pharmacol Physiol. 1997;24(3–4):209–216.
   PubMed Web of Science ®Google Scholar
• Dockray GJ, Varro A, Dimaline R, et al. The gastrins: their production and biological activities. Annu Rev Physiol. 2001;63:119–139.
   PubMed Web of Science ®Google Scholar
• Baldwin GS. The role of gastrin and cholecystokinin in normal and neoplastic gastrointestinal growth. J Gastroenterol Hepatol. 1995;10(2):215–232.
   PubMed Web of Science ®Google Scholar
• Logan CJ, Connell AM. The effect of a synthetic gastrin-like pentapeptide (I.C.I. 50,123) on intestinal motility in man. Lancet. 1966;1(7445):996–999.
   PubMed Web of Science ®Google Scholar
• Gittes GK, Rutter WJ, Debas HT. Initiation of gastrin expression during the development of the mouse pancreas. Am J Surg. 1993;165(1):23–25.
   PubMed Web of Science ®Google Scholar
• Smith JP, Fonkoua LK, Moody TW. The role of gastrin and CCK receptors in pancreatic cancer and other malignancies. Int J Biol Sci. 2016;12(3):283–291.
   PubMed Web of Science ®Google Scholar
• Larsson LI, Rehfeld JF, Sundler F, et al. Pancreatic gastrin in foetal and neonatal rats. Nature. 1976;262(5569):609–610.
   PubMed Web of Science ®Google Scholar
• Brand SJ, Fuller PJ. Differential gastrin gene expression in rat gastrointestinal tract and pancreas during neonatal development. J Biol Chem. 1988;263(11):5341–5347.
   PubMed Web of Science ®Google Scholar
• Brand SJ, Tagerud S, Lambert P, et al. Pharmacological treatment of chronic diabetes by stimulating pancreatic beta-cell regeneration with systemic co-administration of EGF and gastrin. Pharmacol Toxicol. 2002;91(6):414–420.
   PubMedGoogle Scholar
• Suarez-Pinzon WL, Yan Y, Power R, et al. Combination therapy with epidermal growth factor and gastrin increases beta-cell mass and reverses hyperglycemia in diabetic NOD mice. Diabetes. 2005;54(9):2596–2601.
   PubMed Web of Science ®Google Scholar
• Rooman I, Lardon J, Bouwens L. Gastrin stimulates beta-cell neogenesis and increases islet mass from transdifferentiated but not from normal exocrine pancreas tissue. Diabetes. 2002;51(3):686–690.
   PubMed Web of Science ®Google Scholar
• Song I, Patel O, Himpe E, et al. Beta cell mass restoration in alloxan-diabetic mice treated with EGF and gastrin. PLoS One. 2015;10(10):e0140148.
   PubMed Web of Science ®Google Scholar
• Tellez N, Montanya E. Gastrin induces ductal cell dedifferentiation and β-cell neogenesis after 90% pancreatectomy. J Endocrinol. 2014;223(1):67–78.
   PubMed Web of Science ®Google Scholar
• Sasaki S, Miyatsuka T, Matsuoka TA, et al. Activation of GLP-1 and gastrin signalling induces in vivo reprogramming of pancreatic exocrine cells into beta cells in mice. Diabetologia. 2015;58(11):2582–2591.
   PubMed Web of Science ®Google Scholar
• Skarbaliene J, Secher T, Jelsing J, et al. The anti-diabetic effects of GLP-1-gastrin dual agonist ZP3022 in ZDF rats. Peptides. 2015;69:47–55.
   PubMed Web of Science ®Google Scholar
• Tellez N, Vilaseca M, Marti Y, et al. Beta-cell dedifferentiation, reduced duct cell plasticity and impaired beta-cell mass regeneration in middle-aged rats. Am J Physiol Endocrinol Metab. 2016;311(3):E554–E563.
   PubMed Web of Science ®Google Scholar
• Tellez N, Joanny G, Escoriza J, et al. Gastrin treatment stimulates beta-cell regeneration and improves glucose tolerance in 95% pancreatectomized rats. Endocrinology. 2011;152(7):2580–2588.
   PubMed Web of Science ®Google Scholar
• Suarez-Pinzon WL, Lakey JR, Rabinovitch A. Combination therapy with glucagon-like peptide-1 and gastrin induces beta-cell neogenesis from pancreatic duct cells in human islets transplanted in immunodeficient diabetic mice. Cell Transplant. 2008;17(6):631–640.
   PubMed Web of Science ®Google Scholar
• Wang TC, Bonner-Weir S, Oates PS, et al. Pancreatic gastrin stimulates islet differentiation of transforming growth factor alpha-induced ductular precursor cells. J Clin Invest. 1993;92(3):1349–1356.
   PubMed Web of Science ®Google Scholar
• Suarez-Pinzon WL, Power RF, Yan Y, et al. Combination therapy with glucagon-like peptide-1 and gastrin restores normoglycemia in diabetic NOD mice. Diabetes. 2008;57(12):3281–3288.
   PubMed Web of Science ®Google Scholar
• Fosgerau K, Jessen L, Lind Tolborg J, et al. The novel GLP-1-gastrin dual agonist, ZP3022, increases beta-cell mass and prevents diabetes in db/db mice. Diabetes Obes Metab. 2013;15(1):62–71.
   PubMed Web of Science ®Google Scholar
• Caballero F, Siniakowicz K, Hollister-Lock J, et al. Birth and death of human β-cells in pancreases from cadaver donors, autopsies, surgical specimens, and islets transplanted into mice. Cell Transplant. 2014;23(2):139–151.
   PubMed Web of Science ®Google Scholar
• Krause DS. BM-derived stem cells for the treatment of nonhematopoietic diseases. Cytotherapy. 2002;4(6):503–506.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. Marrow stromal cells as stem cells for continual renewal of nonhematopoietic tissues and as potential vectors for gene therapy. J Cell Biochem Suppl. 1998;30–31:284–285.
   PubMedGoogle Scholar
• Ratajczak J, Wysoczynski M, Zuba-Surma E, et al. Adult murine bone marrow-derived very small embryonic-like stem cells differentiate into the hematopoietic lineage after coculture over OP9 stromal cells. Exp Hematol. 2011;39(2):225–237.
   PubMed Web of Science ®Google Scholar
• Barbash IM, Chouraqui P, Baron J, et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation. 2003;108(7):863–868.
   PubMed Web of Science ®Google Scholar
• Meyerrose TE, De Ugarte DA, Hofling AA, et al. In vivo distribution of human adipose-derived mesenchymal stem cells in novel xenotransplantation models. Stem Cells. 2007;25(1):220–227.
   PubMed Web of Science ®Google Scholar
• Zhang XY, La Russa VF, Bao L, et al. Lentiviral vectors for sustained transgene expression in human bone marrow-derived stromal cells. Mol Ther. 2002;5(5):555–565.
   PubMed Web of Science ®Google Scholar
• Reiser J, Zhang XY, Hemenway CS, et al. Potential of mesenchymal stem cells in gene therapy approaches for inherited and acquired diseases. Expert Opin Biol Ther. 2005;5(12):1571–1584.
   PubMed Web of Science ®Google Scholar
• Bosch P, Stice SL. Adenoviral transduction of mesenchymal stem cells. Methods Mol Biol. 2007;407:265–274.
   PubMedGoogle Scholar
• Fan L, Lin C, Zhuo S, et al. Transplantation with survivin-engineered mesenchymal stem cells results in better prognosis in a rat model of myocardial infarction. Eur J Heart Fail. 2009;11(11):1023–1030.
   PubMed Web of Science ®Google Scholar
• Nomura T, Honmou O, Harada K, et al. I.V. infusion of brain-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Neuroscience. 2005;136(1):161–169.
   PubMed Web of Science ®Google Scholar
• Kurozumi K, Nakamura K, Tamiya T, et al. BDNF gene-modified mesenchymal stem cells promote functional recovery and reduce infarct size in the rat Middle cerebral artery occlusion model. Mol Ther. 2004;9(2):189–197.
   PubMed Web of Science ®Google Scholar
• Zhao MZ, Nonoguchi N, Ikeda N, et al. Novel therapeutic strategy for stroke in rats by bone marrow stromal cells and ex vivo HGF gene transfer with HSV-1 vector. J Cereb Blood Flow Metab. 2006;26(9):1176–1188.
   PubMed Web of Science ®Google Scholar
• Guo QS, Zhu MY, Wang L, et al. Combined transfection of the three transcriptional factors, PDX-1, NeuroD1, and MafA, causes differentiation of bone marrow mesenchymal stem cells into insulin-producing cells. Exp Diabetes Res. 2012;2012:672013.
   PubMedGoogle Scholar
• Lin HT, Kao CL, Lee KH, et al. Enhancement of insulin-producing cell differentiation from embryonic stem cells using pax4-nucleofection method. World J Gastroenterol. 2007;13(11):1672–1679.
   PubMed Web of Science ®Google Scholar
• Soyer J, Flasse L, Raffelsberger W, et al. Rfx6 is an Ngn3-dependent winged helix transcription factor required for pancreatic islet cell development. Development. 2010;137(2):203–212.
   PubMed Web of Science ®Google Scholar
• Sacerdote P, Ruff MR, Pert CB. Cholecystokinin and the immune system: receptor-mediated chemotaxis of human and rat monocytes. Peptides. 1988;9(1):29–34.
   PubMedGoogle Scholar
• Xu SJ, Gao WJ, Cong B, et al. Effect of cholecystokinin octapeptide on diacylglycerol-PKC signaling pathway in rat pulmonary interstitial macrophages stimulated by lipopolysaccharide. Acta Pharmacol Sin. 2005;26(12):1497–1504.
   PubMed Web of Science ®Google Scholar
• Thaiss CA, Levy M, Grosheva I, et al. Hyperglycemia drives intestinal barrier dysfunction and risk for enteric infection. Science. 2018;359(6382):1376–1383.
   PubMed Web of Science ®Google Scholar
• Nielsen TB, Pantapalangkoor P, Yan J, et al. Diabetes exacerbates infection via hyperinflammation by signaling through TLR4 and RAGE. MBio. 2017;8(4):e00818–e00817.
   PubMed Web of Science ®Google Scholar
• Gyurko R, Siqueira CC, Caldon N, et al. Chronic hyperglycemia predisposes to exaggerated inflammatory response and leukocyte dysfunction in Akita mice. J Immunol. 2006;177(10):7250–7256.
   PubMed Web of Science ®Google Scholar
• Esposito K, Nappo F, Marfella R, et al. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation. 2002;106(16):2067–2072.
   PubMed Web of Science ®Google Scholar