PMC:6141714 / 42000-53011
Annnotations
{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/6141714","sourcedb":"PMC","sourceid":"6141714","source_url":"https://www.ncbi.nlm.nih.gov/pmc/6141714","text":"Treatment of type I diabetes mellitus\nType 1 diabetes mellitus is a chronic metabolic disease characterized by an insulin deficiency caused by the cellular-mediated autoimmune destruction of the β-cells of the pancreas (175). The process of destruction of pancreatic β cells, called insulitis, is a consequence of an immunological attack mediated by lymphocytes, macrophages and NK cells and leads to a permanent hyperglycemia and the need for exogenous insulin replacement (176). CD8+ T lymphocytes are the predominant type of immune cell responsible for the insulitis process, but the presence of CD4+ T lymphocytes and B lymphocytes can also be detected in the lymphocytic infiltrate in pancreatic islets (177). Furthermore, the cytokine secretion profile during the development of type 1 diabetes is typical of a Th1 pattern immune response, with the inflammatory cytokines IL-2, TNF-α, and IFN-γ being secreted in high quantities (178). The treatment of type I diabetes mellitus was conducted through the administration of hMSCs in a total of eight studies (74–80, 164). Among them, only one study (78) was conducted in humans and the other seven studies (74–77, 79, 80, 164) used mice as the experimental model. Among the studies conducted in mice, the fasting and post-prandial plasma glucose level, the C-peptide level, the rate of change in body weight, the serum insulin level, the total number of islets and the ratio of β and α cells per islet were the outcomes used by most animal studies selected in this systematic review to assess the potential of hMSCs administration for the treatment of type 1 diabetes mellitus. In the human clinical trial selected, the primary study endpoints used were: feasibility of the stem cell therapy; safety of the therapy through 24 months post-treatment; and the preliminary evaluation of the efficacy of the therapy for improving β cell function through 24 weeks. The secondary study endpoint used was the evidence of the efficacy of the therapy in modulating autoimmunity. We propose that the levels of glycated hemoglobin is the most appropriate primary endpoint for future clinical trials as this endpoint give us an overall picture of the average serum glucose levels over a period of weeks or months. In addition, we propose that secondary endpoints such as weight gain, occurrence of episodes of hypoglycemia, systolic and diastolic blood pressure and the level of circulating lipids should be used in conjunction with the primary endpoint selected to identify the existence of multiple effects associated with hMSC administration in the pathological course of type 1 diabetes mellitus. Regarding the source of hMSCs, in four studies hMSCs were isolated from the bone marrow (77, 79, 80, 164), in three (75, 76, 78) the umbilical cord was used as the source of hMSCs and in only one study (74) hMSCs were isolated from the adipose tissue. The administration of hMSCs affected both clinical and laboratory parameters of type I diabetes. In most of the studies selected, the administration of hMSCs resulted in a decrease in the blood glucose level (74–80) and in an increase in both the survival rates (75) and in the insulin level in the blood (75, 77, 79, 80). Furthermore, treatment with hMSCs delayed the onset of the disease (76, 164), reduced the weight loss resulting from the disease (74), inhibited insulitis in islets (75, 76, 164) and increased pancreatic islet number and function (74–78, 80).\nAmong the mechanisms proposed by the articles selected are included effects in the proliferation and differentiation of immune cells and changes in the expression pattern of growth factors, cytokines, enzymes, prostaglandins and surface receptors. A reduction in the levels of pro-inflammatory cytokines such as TNF-α (74, 75, 76), IFN-γ (75, 76, 77, 80), CCL2 (75), IL-1β (75), IL-2 (76, 77, 80), and IL-17 (75) and an increase in the expression of immunoregulatory cytokines such as IL-4 (74, 75), IL-10 (74, 75, 80), and IL-13 (74) was observed by the majority of the articles selected. In addition, in a study conducted by Wen et al. (80), the expression of the IL-2 receptor was also found to be decreased after the administration of hMSCs. In other studies, the expression of PGE2 (80) and growth factors such as TGF-β (75, 80), VEGF (80), and HGF (80) increased after hMSCs administration. Furthermore, according to Sun et al. (74), hMSCs exert an anti-apoptotic effect in pancreatic islets through the upregulation of the anti-apoptotic proteins XIAP, Bcl-xL, and Bcl-2 and the downregulation of the anti-apoptotic protein caspase 3. As a consequence, some studies reported a decrease in the amount of apoptotic cells when hMSCs were present (74, 80). Finally, a study conducted by Sun et al. (74) demonstrated that the expression of important transcription factors in islet development and differentiation such as Ngn3 and Pax6 was upregulated in pancreatic islets due to the presence of hMSCs. On the other hand, in a study by Zhang and Dou (79), hMSCs were differentiated into islet-like cells and their characteristics were compared to those of fetal pancreatic islets. This study demonstrated that the islet-like cells expressed the pancreatic islet cells-related genes pdx1, ngn3, pax4, neuroD1, nkx2.2, nkx6.1, PCSK1, insulin, glucagon, SST, and PP at levels similar to the expression profile of fetal pancreatic islets. Regarding the effects of hMSCs on the proliferation and differentiation of immune cells, some studies reported a stimulatory effect on the proliferation of CD4+CD25+Foxp3+ Treg (75, 76, 80, 164) cells while other results showed that the presence of hMSCs was found to be associated with the inhibition in the clonal expansion of CD4+IFN-γ+ Th1 (75) and CD4+IL17+ Th17 (75) cells. In addition, a study conducted by Tsai et al. (75) demonstrated that the administration of hMSCs inhibited the proliferation of CD11c+ dendritic cells in non-obese diabetic mice. Finally, a decrease in the infiltration of inflammatory T cells (77) and an increase in the proportion ofCD4+CD25+Foxp3+ Tregs (164) in the pancreatic islets were also observed. Table 2 summarizes the methodology employed and the results obtained in the studies selected in this systematic review regarding the effects of the administration of hMSCs for the treatment of type I diabetes mellitus. It is possible that the secretion of immunomodulatory cytokines and growth factors such as IL-4, IL-10, IL-13, TGF-β, PGE2, VEGF, and HGF by the hMSCs administered plays a crucial role in the inhibition in the development of the insulitis process mediated by CD4+ lymphocytes, as suggested by the inhibition in the clonal expansion of Th1 and Th17 lymphocytes after hMSCs administration. In addition, the stimulatory effect in the proliferation of Treg cells observed after hMSCs administration may exert an inhibitory effect in the proliferation and activation of dendritic cells, in clonal expansion of both T4+ and T8+ lymphocytes and in the infiltration of inflammatory T cells in pancreatic islets. Therefore, the decrease in the levels of pro-inflammatory cytokines such as TNF-α, IFN-γ, CCL2, IL-1β, IL-2, IL-17 observed by some of the studies selected can also be successfully explained by the inhibitory effects that hMSCs exert on inflammatory cells.\nTable 2 List of in vivo studies in which the therapeutic potential of the administration of hMSCs for the treatment of type I diabetes mellitus was evaluated and the results obtained.\nReferences Autoimmune disease Source of hMSC Variables Experimental model Clinical and laboratory effects Mechanism proposed\n(164) Type I diabetes mellitus Bone marrow None Mice ↓Disease onset↓Insulitis in the pancreas ↑Tregs in the pancreas\n(74) Type I diabetes mellitus Adipose tissue Administration of adipose tissue-derived MSCs overexpressing betatrophin Administration of adipose tissue-derived MSCs alone Mice ↓Hyperglycemia↓Weight loss Effectiveness of adipose tissue-derived MSCs overexpressing betatrophin \u003e Effectiveness of adipose tissue-derived MSCs alone ↑Islet proliferation↑Ngn3 transcription factor↑Pax6 transcription factor↑Islet production of insulin↑β-cells ratio↑IL-4↑IL-10↑IL-13↓TNF-α↓NADP-cytochrome P450 reductase↑XIAP in the islets↑Bcl-xL in the islets↑Bcl-2 in the islets↓Caspase-3 in the islets↓Apoptotic cells\n(75) Type I diabetes mellitus Umbilical cord stroma None Mice ↑Survival rates↓Blood glucose↑Serum insulin levels↑Glucose tolerance↑C-peptide↓Insulitis ↓Th1 cells↓Th17 cells↑Tregs↓Dendritic cells↓IFN-γ in the serum↓IL-1β in the serum↓TNF-α in the serum↓CCL2 in the serum↓IL-17 in the serum↑IL-4 in the serum↑IL-10 in the serum↑TGF-β1↑Intact islets↑Insulin-producing cells devided from the differentiation of umbilical cord stroma-derived MSCs\n(76) Type I diabetes mellitus Umbilical cord stroma Administration of umbilical cord-derived MSCs before the onset of type I diabetes Mice ↓Disease onset↑Fasting C-peptide↓Insulitis ↑CD4+CD25+Foxp3+ Tregs↓IL-2↓IFN-γ↓TNF- α↑Islet β-cells\nTreatment of type I diabetes with umbilical cord-derived MSCs after the onset of the disease ↓Fasting plasma glucose↓Fed blood glucose↑Fasting C-peptide↓Insulitis\n(77) Type I diabetes mellitus Bone marrow None Mice ↓Hyperglycemia↓Area under the glycemia curve↓Fasting glycemia↑Serum insulin ↑Islet β-cells function↓CD3+ cells↓Islet infiltration↑Larger pancreatic islets↓IL-2 in the pancreas↓IFN-γ in the pancreas↓IL-4 in the pancreas\n(79) Type I diabetes mellitus Bone marrow None Mice ↓Hyperglycemia↑Insulin production↑Human insulin in mice↑C-peptide production ↑Nestin↑Pdx1 transcription factor↑Ngn3 transcription factor↑Pax4 transcription factor↑NeuroD1 transcription factor↑Nkx2.2 transcription factor↑Nkx6.1 transcription factor↑PCSK1 gene↑Insulin gene↑Glucagon gene↑PCSK1 gene↑PP gene\n(80) Type I diabetes mellitus Bone marrow None Mice ↓Hyperglycemia↑Insulin levels ↓Fas in human islets↓MiR-375 in human islets↓PBMC activation↓PBMC proliferation↓IL-2↓IFN-γ↓IL-2 receptor↑HGF↑IL-10↑VEGF↑PGE-2↑TGF-β↑Treg function↓Islet β-cells apoptosis↑Islet β-cells function against inflammatory cytokines↓Immune reaction against transplanted islets after humanization of mice\n(78) Type I diabetes mellitus Umbilical cord stroma None Humans ↓Post-prandial plasma glucose↓Hemoglobin HbA1c↑Fasting C peptide↑C-peptide/glucose ratio ↑Islet β-cells function\nBoth the methodology employed and the results obtained by each article are represented in this table. Ngn3, neurogenin-3; Pax4, paired box gene 4; Pax6, paired box gene 6; IL-13, interleukin 13; XIAP, X-linked inhibitor of apoptosis protein; Bcl-xL, B-cell lymphoma-extra large; Bcl-2, B-cell lymphoma 2; Pdx1, pancreatic and duodenal homeobox 1; NeuroD1, neurogenic differentiation 1; Nkx2.2, homeobox protein Nkx-2.2; Nkx6.1, homeobox protein Nkx-6.1; PCSK1, proprotein convertase 1; PP, protein phosphatase; Fas, first apoptosis signal receptor; PBMC, peripheral blood mononuclear 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