Co-transplantation of autologous MSCs delays islet allograft rejection and generates a local immunoprivileged site

Acta Diabetologica

Volumn 52, Issue 5, 2015, Pages 917-927

  Ben Nasr, Moufida ^a,b   Vergani, Andrea ^a,b   Avruch, James ^c   Liu, Liye ^c   Kefaloyianni, Eirini ^d   D’Addio, Francesca ^a,b   Tezza, Sara ^a   Corradi, Domenico ^e   Bassi, Roberto ^a   Valderrama Vasquez, Alessandro ^b   Usuelli, Vera ^b   Kim, James ^c   Azzi, Jamil ^d   El Essawy, Basset ^f   Markmann, James ^c   Abdi, Reza ^d   Fiorina, Paolo ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e UNIVERSITY OF PARMA   (Italy)

^f AL AZHAR UNIVERSITY   (Egypt)

Author keywords

Immunoprivileged site; Immunoregulation; Islet transplantation; Mesenchymal stem cells

Indexed keywords

ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BONE MARROW; C57BL 6 MOUSE; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; EX VIVO STUDY; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOLOGICAL PARAMETERS; IMMUNOMODULATION; IMMUNOPRIVILEGED SITE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CAPSULE; MESENCHYMAL STEM CELL TRANSPLANTATION; MIXED LYMPHOCYTE REACTION; MOUSE; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN CELL; TH2 CELL; ANIMAL; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CYTOLOGY; IMMUNOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; MIXED LYMPHOCYTE CULTURE; PROCEDURES; SPLEEN; TH17 CELL; ULTRASTRUCTURE;

CYTOKINE;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL PROLIFERATION; CYTOKINES; GRAFT REJECTION; GRAFT SURVIVAL; ISLETS OF LANGERHANS TRANSPLANTATION; LYMPHOCYTE CULTURE TEST, MIXED; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; SPLEEN; TH17 CELLS;

EID: 84941942966     PISSN: 09405429     EISSN: 14325233     Source Type: Journal    
DOI: 10.1007/s00592-015-0735-y     Document Type: Article

References (55)

1. Nathan DM, Cleary PA, Backlund JY et al (2005) Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 353:2643–2653
2. Nathan DM, Lachin J, Cleary P et al (2003) Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N Engl J Med 348:2294–2303
3. Bloomgarden ZT (2004) Consequences of diabetes: cardiovascular disease. Diabetes Care 27:1825–1831
4. Bloomgarden ZT (2004) Diabetes complications. Diabetes Care 27:1506–1514
5. Trento M, Raballo M, Trevisan M et al (2012) A cross-sectional survey of depression, anxiety, and cognitive function in patients with type 2 diabetes. Acta Diabetol 49:199–203
6. Piarulli F, Sartore G, Lapolla A (2013) Glyco-oxidation and cardiovascular complications in type 2 diabetes: a clinical update. Acta Diabetol 50:101–110
7. Tarallo S, Beltramo E, Berrone E, Porta M (2012) Human pericyte-endothelial cell interactions in co-culture models mimicking the diabetic retinal microvascular environment. Acta Diabetol 49(Suppl 1):S141–S151
8. Fiorina P, Shapiro AM, Ricordi C, Secchi A (2008) The clinical impact of islet transplantation. Am J Transplant 8:1990–1997
9. Fiorina P, Vergani A, Petrelli A et al (2008) Metabolic and immunological features of the failing islet-transplanted patient. Diabetes Care 31:436–438
10. Fiorina P, Vezzulli P, Bassi R et al (2012) Near normalization of metabolic and functional features of the central nervous system in type 1 diabetic patients with end-stage renal disease after kidney-pancreas transplantation. Diabetes Care 35:367–374
11. Venturini M, Fiorina P, Maffi P et al (2006) Early increase of retinal arterial and venous blood flow velocities at color Doppler imaging in brittle type 1 diabetes after islet transplant alone. Transplantation 81:1274–1277
12. Del Carro U, Fiorina P, Amadio S et al (2007) Evaluation of polyneuropathy markers in type 1 diabetic kidney transplant patients and effects of islet transplantation: neurophysiological and skin biopsy longitudinal analysis. Diabetes Care 30:3063–3069
13. Fiorina P, Secchi A (2007) Pancreatic islet cell transplant for treatment of diabetes. Endocrinol Metab Clin North Am 36:999–1013; ix
14. Shapiro AM, Ricordi C, Hering BJ et al (2006) International trial of the Edmonton protocol for islet transplantation. N Engl J Med 355:1318–1330
15. Ansari MJ, Fiorina P, Dada S et al (2008) Role of ICOS pathway in autoimmune and alloimmune responses in NOD mice. Clin Immunol 126:140–147
16. Guleria I, Gubbels Bupp M, Dada S et al (2007) Mechanisms of PDL1-mediated regulation of autoimmune diabetes. Clin Immunol 125:16–25
17. Vergani A, D’Addio F, Jurewicz M et al (2010) A novel clinically relevant strategy to abrogate autoimmunity and regulate alloimmunity in NOD mice. Diabetes 59:2253–2264
18. Vergani A, Fotino C, D’Addio F et al (2013) Effect of the purinergic inhibitor oxidized ATP in a model of islet allograft rejection. Diabetes 62:1665–1675
19. Maffi P, Bertuzzi F, De Taddeo F et al (2007) Kidney function after islet transplant alone in type 1 diabetes: impact of immunosuppressive therapy on progression of diabetic nephropathy. Diabetes Care 30:1150–1155
20. Friedenstein AJ, Chailakhjan RK, Lalykina KS (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3:393–403
21. Tyndall A, Walker UA, Cope A et al (2007) Immunomodulatory properties of mesenchymal stem cells: a review based on an interdisciplinary meeting held at the Kennedy Institute of Rheumatology Division, London, UK, 31 October 2005. Arthritis Res Ther 9:301
22. Cohen JA (2013) Mesenchymal stem cell transplantation in multiple sclerosis. J Neurol Sci 333:43–49
23. Fiorina P, Jurewicz M, Augello A et al (2009) Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J Immunol 183:993–1004
24. Fiorina P, Voltarelli J, Zavazava N (2011) Immunological applications of stem cells in type 1 diabetes. Endocr Rev 32:725–754
25. Oswald J, Boxberger S, Jorgensen B et al (2004) Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22:377–384
26. Le Blanc K, Samuelsson H, Lonnies L, Sundin M, Ringden O (2007) Generation of immunosuppressive mesenchymal stem cells in allogeneic human serum. Transplantation 84:1055–1059
27. De Miguel MP, Fuentes-Julian S, Blazquez-Martinez A et al (2012) Immunosuppressive properties of mesenchymal stem cells: advances and applications. Curr Mol Med 12:574–591
28. MacFarlane RJ, Graham SM, Davies PS et al (2013) Anti-inflammatory role and immunomodulation of mesenchymal stem cells in systemic joint diseases: potential for treatment. Expert Opin Ther Targets 17:243–254
29. Jurewicz M, Yang S, Augello A et al (2010) Congenic mesenchymal stem cell therapy reverses hyperglycemia in experimental type 1 diabetes. Diabetes 59:3139–3147
30. Papadopoulou A, Yiangou M, Athanasiou E et al (2012) Mesenchymal stem cells are conditionally therapeutic in preclinical models of rheumatoid arthritis. Ann Rheum Dis 71:1733–1740
31. Eggenhofer E, Renner P, Soeder Y et al (2011) Features of synergism between mesenchymal stem cells and immunosuppressive drugs in a murine heart transplantation model. Transpl Immunol 25:141–147
32. Ding Y, Xu D, Feng G, Bushell A, Muschel RJ, Wood KJ (2009) Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and -9. Diabetes 58:1797–1806
33. Carvello M, Petrelli A, Vergani A et al (2012) Inotuzumab ozogamicin murine analog-mediated B-cell depletion reduces anti-islet allo- and autoimmune responses. Diabetes 61:155–165
34. Serreze DV, Chapman HD, Varnum DS et al (1996) B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new “speed congenic” stock of NOD.Ig mu null mice. J Exp Med 184:2049–2053
35. Vergani A, Clissi B, Sanvito F, Doglioni C, Fiorina P, Pardi R (2009) Laser capture microdissection as a new tool to assess graft-infiltrating lymphocytes gene profile in islet transplantation. Cell Transplant 18:827–832
36. Vergani A, Tezza S, D’Addio F et al (2013) Long-term heart transplant survival by targeting the ionotropic purinergic receptor P2X7. Circulation 127:463–475
37. Astorri E, Fiorina P, Gavaruzzi G, Astorri A, Magnati G (1997) Left ventricular function in insulin-dependent and in non-insulin-dependent diabetic patients: radionuclide assessment. Cardiology 88:152–155
38. Paroni R, Fermo I, Fiorina P, Cighetti G (2005) Determination of asymmetric and symmetric dimethylarginines in plasma of hyperhomocysteinemic subjects. Amino Acids 28:389–394
39. Fiorina P, Vergani A, Dada S et al (2008) Targeting CD22 reprograms B-cells and reverses autoimmune diabetes. Diabetes 57:3013–3024
40. Francese R, Fiorina P (2010) Immunological and regenerative properties of cord blood stem cells. Clin Immunol 136:309–322
41. D’Addio F, Maffi P, Vezzulli P et al (2014) Islet transplantation stabilizes hemostatic abnormalities and cerebral metabolism in individuals with type 1 diabetes. Diabetes Care 37:267–276
42. Gu F, Molano I, Ruiz P, Sun L, Gilkeson GS (2012) Differential effect of allogeneic versus syngeneic mesenchymal stem cell transplantation in MRL/lpr and (NZB/NZW)F1 mice. Clin Immunol 145:142–152
43. Eliopoulos N, Stagg J, Lejeune L, Pommey S, Galipeau J (2005) Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 106:4057–4065
44. Ito T, Itakura S, Todorov I et al (2010) Mesenchymal stem cell and islet co-transplantation promotes graft revascularization and function. Transplantation 89:1438–1445
45. Borg DJ, Weigelt M, Wilhelm C et al (2014) Mesenchymal stromal cells improve transplanted islet survival and islet function in a syngeneic mouse model. Diabetologia 57:522–531
46. Rossignol J, Boyer C, Leveque X et al (2011) Mesenchymal stem cell transplantation and DMEM administration in a 3NP rat model of Huntington’s disease: morphological and behavioral outcomes. Behav Brain Res 217:369–378
47. Park KS, Kim YS, Kim JH et al (2010) Trophic molecules derived from human mesenchymal stem cells enhance survival, function, and angiogenesis of isolated islets after transplantation. Transplantation 89:509–517
48. Favaro E, Carpanetto A, Lamorte S et al (2014) Human mesenchymal stem cell-derived microvesicles modulate T cell response to islet antigen glutamic acid decarboxylase in patients with type 1 diabetes. Diabetologia 57:1664–1673
49. Cantaluppi V, Biancone L, Figliolini F et al (2012) Microvesicles derived from endothelial progenitor cells enhance neoangiogenesis of human pancreatic islets. Cell Transplant 21:1305–1320
50. Yagi H, Soto-Gutierrez A, Parekkadan B et al (2010) Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transplant 19:667–679
51. Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F (2005) Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105:2821–2827
52. Jiang XX, Zhang Y, Liu B et al (2005) Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105:4120–4126
53. Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L (2006) Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 107:1484–1490
54. Corcione A, Benvenuto F, Ferretti E et al (2006) Human mesenchymal stem cells modulate B-cell functions. Blood 107:367–372
55. Duprez IR, Johansson U, Nilsson B, Korsgren O, Magnusson PU (2011) Preparatory studies of composite mesenchymal stem cell islets for application in intraportal islet transplantation. Ups J Med Sci 116:8–17