Autologous bone marrow-derived rat mesenchymal stem cells promote PDX-1 and insulin expression in the islets, alter T cell cytokine pattern and preserve regulatory T cells in the periphery and induce sustained normoglycemia

Journal of Autoimmunity

Volumn 32, Issue 1, 2009, Pages 33-42

  Boumaza, Imene ^a   Srinivasan, Suganya ^a   Witt, William T ^a   Feghali Bostwick, Carol ^a   Dai, Yifan ^a   Garcia Ocana, Adolfo ^a   Feili Hariri, Maryam ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cellular therapy; Diabetes; Mesencymal stem cells; PDX 1; Regulatory T cells

Indexed keywords

CYTOKINE; INSULIN; INTERLEUKIN 10; INTERLEUKIN 13; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR PDX 1;

ANIMAL EXPERIMENT; ARTICLE; AUTOLOGOUS BONE MARROW TRANSPLANTATION; B LYMPHOCYTE ACTIVATION; CD4 CD8 RATIO; CELL TYPE; CONTROLLED STUDY; EXPERIMENTAL RAT; FEMALE; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; MALE; MESENCHYMAL STEM CELL; MICROENVIRONMENT; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD; BLOOD GLUCOSE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HOMEODOMAIN PROTEINS; INSULIN; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISLETS OF LANGERHANS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; PANCREAS; RATS; RATS, INBRED LEW; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TRANS-ACTIVATORS; TRANSPLANTATION, AUTOLOGOUS;

EID: 59149098948     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2008.10.004     Document Type: Article

References (55)

1. Le Blanc K. Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 8 (2006) 559-561
2. Krampera M., Pasini A., Pizzolo G., Cosmi L., Romagnani S., and Annunziato F. Regenerative and immunomodulatory potential of mesenchymal stem cells. Curr Opin Pharmacol 6 (2006) 435-441
3. Uccelli A., Pistoia V., and Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression?. Trends Immunol 28 (2007) 219-226
4. Phinney D.G., and Prockop D.J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 25 (2007) 2896-2902
5. Abdi R., Fiorina P., Adra C.N., Atkinson M., and Sayegh M.H. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes 57 (2008) 1759-1767
6. Prockop D.I. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276 (1997) 71-74
7. Deans R.J., and Moseley A.B. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 28 (2000) 875-884
8. Chapel A., Bertho J.M., Bensidhoum M., Fouillard L., Young R.G., Frick J., et al. Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J Gene Med 5 (2003) 1028-1038
9. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99 (2002) 3838-3843
10. Aggarwal S., and Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105 (2005) 1815-1822
11. Xu G., Zhang Y., Zhang L., Ren G., and Shi Y. The role of IL-6 in inhibition of lymphocyte apoptosis by mesenchymal stem cells. Biochem Biophs Res Commun 361 (2007) 745-750
12. Djouad F., Charbonnier L.-M., Bouffi C., Louis-Plence P., Bony C., Apparailly F., et al. Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependendent mechanism. Stem Cells 25 (2007) 2025-2032
13. Aksu A.E., Horibe E., Sacks J., Ikeguchi R., Breitinger J., Scozio M., et al. Co-infusion of donor bone marrow with host mesenchymal stem cells treats GVHD and promotes vascularized skin graft survival in rats. Clin Immunol 127 (2008) 348-358
14. Tse W.T., Pendleeton J.D., Beyer W.M., Egalka M.C., and Guinan E.C. Suppression of allogeneic T cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75 (2003) 389-397
15. Maitra B., Szekely E., Gjini K., Laughlin M.J., Dennis J., Haynesworth S.E., et al. Mesenchymal stem cells: human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T cell activation. Bone Marrow Transplant 33 (2004) 597-604
16. Itakura S., Asari S., Rawson J., Ito T., Todorov I., Liu C.-P., et al. Mesenchymal stem cells facilitate the induction of mixed hematopoietic chimerism and islet allograft tolerance without GVHD in the rat. Am J Transplant 7 (2007) 336-346
17. Caplan A.I., and Dennis J.E. Mesenchymal stem cells as tropic mediators. J Cell Biochem 98 (2006) 1076-1084
18. Peterson B.E., Bowen W.C., Patrene K.D., Mars W.M., Sullivan A.K., Murase N., et al. Bone marrow as a potential source of hepatic oval cells. Science 284 (1999) 1168-1170
19. Woodbury D., Schwarz E.J., Prockop D.J., and Black I.B. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61 (2000) 364-370
20. Sanvito F., Herrera P.L., Huarte J., Nichols A., Montesano R., Orci L., et al. TGF-β influences the relative development of the exocrine and endocrine pancreas in vitro. Development 120 (1994) 3451-3462
21. Otonkoski T., Cirulli V., Beattie G.M., Mally M.I., Soto G., Rubin J.S., et al. A role for hepatocyte growth factor/scatter factor in fetal mesenchyme induced pancreatic beta-cell growth. Endocrinalogy 137 (1996) 3131-3139
22. Krakowski M.L., Kritzik M.R., Jones E.M., Krahl T., Lee J., Arnush M., et al. Transgenic expression of epidermal growth factor and keratinocyte growth factor in b-cells results in substantial morphological changes. J Endocrinol (1999) 167-175
23. Suarez-Pinzon W.L., Lakey J.R., Brand S.J., and Rabinovitch A. Combination therapy with epidermal growth factor and gastrin induces neogenesis of human islet beta-cells from pancreatic duct cells and an increase in functional beta-cell mass. J Clin Endocrinol Metab 90 (2005) 3401-3409
24. Kozawa J., Tokui Y., Moriwaki M., Li M., Dohmoto H., Yuan M., et al. Regenerative and therapeutic effects of heparin-binding epidermal growth factor-like growth factor on diabetes by gene transduction through retrograde pancreatic duct injection of adenovirous vector. Pancreas 31 (2005) 32-42
25. Vasavada R.C., Gonzalez-Pertusa J.A., Fujinaka Y., Fiaschi-Taesch N., Cozar-Castellano I., and Garcia-Ocana A. Growth factors and beta cell replication. Int J Biochem Cell Biol 38 (2006) 931-950
26. Dai C., Yingjian L., Yang J., and Liu Y. Hepatocyte growth factor preserves beta cell mass and mitigates hyperglycemia in streptozotocin-induced diabetic mice. J Biol Chem 278 (2003) 27080-27087
27. Garcia-Ocana A., Takane K.K., Teddy V.T., Lopez-Talavera J.-C., Vasavada R.C., and Stewart A.F. Adenovirus-mediated hepatocyte growth factor expression in mouse islets improves pancreatic islet transplant performance and reduces beta cell death. J Biol Chem 278 (2003) 343-351
28. Lopez-Talavera J.C., Garcia-Ocana A., Sipula I., Takane K.K., Cozar-Casteliano I., and Stewart A.F. Hepatocyte growth factor gene therapy for pancreatic islets in diabetes: reducing the minimal islet transplant mass required in a glucocorticoid-free rat model of allogeneic portal vein islet transplantation. Endocrinology 145 (2004) 467-474
29. + regulatory cells, restores self-tolerance, and facilitates regeneration of beta cell function in overtly diabetic nonobese diabetic mice. Transplantation 79 (2005) 1091-1096
30. An J., Beauchemin N., Albanese J., Abney T.O., and Sullivan A.K. Use of a rat cDNA probe specific for the Y chromosome to detect male-derived cells. J Androl 18 (1997) 289-293
31. Liechty K.W., MacKenzie T.C., Shaaban A.F., Radu A., Moseley A.M., Deans R., et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6 (2000) 1282-1286
32. Devine S.M., Bartholomew A.M., Mahmud N., Nelson M., Patil S., Hardy W., et al. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hemotol 29 (2001) 244-255
33. Pochampally R.R., Neville B.T., Schwartz E.J., Li M.M., and Prockop D.J. Rat adult stem cells (marrow stromal cells) engraft and differentiate in chick embryos without evidence of cell fusion. Proc Natl Acad Sci U S A 101 (2004) 9282-9285
34. Nauta A.J., Westerhuis G., Kruisselbrink A.B., Lurvink E.G., Willemze R., and Fibbe W.E. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood 108 (2006) 2114-2120
35. Melloul D., Marshak S., and Cerasi E. b-cell genes: functional aspects: regulation of pdx-1 gene expression. Diabetes 51 (2002) S320-S325
36. Marshak S., Totary H., Cerasi E., and Melloul D. Purification of the beta-cell glucose sensitive factor that transactivates the insulin gene differentially in normal and transformed islet cells. Proc Natl Acad Sci USA 93 (1996) 15057-15062
37. Watada H., Kajimoto Y., Umayahara Y., Matsuoka T., Kaneto H., Fujitani Y., et al. The human glucokinase gene beta-cell-type promoter: an essential role of insulin promoter factor 1/PDX-1 in its activation in HIT-TI5 cells. Diabetes 45 (1996) 1478-1488
38. Ferber S., Halkin A., Cohen H., Ber I., Einav Y., Goldberg I., et al. Pancreatic and duodental homeobox gene 1 induces express of insulin genes in liver and ameliorates streptozotocin-induced hyperglycemia. Nat Med 6 (2000) 568-572
39. Ianus A., Holz G.G., Theise N.D., and Hussain M.A. In vivo derivation of glucose-competent pancreatic endocrine cells from bone marrow without evidence of cell fusion. J Clin Invest 111 (2003) 843-850
40. Lechner A., Yang Y.G., Blacken R.A., Wang L., Nolan A.L., and Habener J.F. No evidence for significant transdifferentiation of bone marrow into pancreatic beta-cells in vivo. Diabetes 53 (2004) 616-623
41. Mutskov v., Raaka B.M., Felsenfeld G., and Gershengorn M.C. The human insulin gene displays transcriptionally active epigenetic marks in islet-derived mesenchymal precursor cells in the absence of insulin expression. Stem Cells 25 (2007) 3223-3233
42. Davani B., Ikonomou L., Raaka B.M., Geras-Raaka E., Morton R.A., Marcus-Samuels B., et al. Human islet-derived precursor cells are mesenchymal stromal cells that differentiate and mature to hormone-expressing cells in vivo. Stem Cells 25 (2007) 3215-3222
43. Baertschiger R.M., Bosco D., Morel P., Serre-Beinier V., Berney T., Buhler L.H., et al. Mesenchymal stem cells derived from human exocrine pancreas express transcription factors implicated in beta-cell development. Pancreas 37 (2008) 75-84
44. Hess D., Li l., Martin M., Sakano S., Hill D., Strutt B., et al. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat Biotechnol 21 (2003) 763-770
45. Izumida Y., Aoki T., Yasuda D., Koizumi T., Suganuma C., Saito K., et al. Hepatocyte growth factor is constitutively produced by donor-derived bone marrow cells and promotes regeneration of pancreatic b-cells. Biochem Biophys Res Commun 333 (2005) 273-282
46. Kayali A.G., Van Gunt K., Campbell I., Stotland A., Kritzik M., Liu G., et al. The stromal cell-derived factor-1alpha/CXCR4 ligand-receptor axis is critical for progenitor survival and migration in the pancreas. J Cell Biol 163 (2003) 859-869
47. + progenitors to peripheral blood. J Exp Med 185 (1997) 111-120
48. Ferrara N., and Gerber H. The role of vascular endothelial growth factor in angiogenesis. Acta Haematol 106 (2001) 148-156
49. Zhang Y.-Q., Kritzik M.R., and Sarvetnick N. Identification and expansion of pancreatic stem/progenitor cells. J Cell Mol Med 9 (2005) 331-344
50. Zappia E., Casazza S., Pedemonte E., Benvenuto F., Bonanni I., Gerdoni E., et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T cell anergy. Blood 106 (2005) 1755-1761
51. Augello A., Tasso R., Negrini S.M., Cancedda R., and Pennesi G. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 56 (2007) 1175-1186
52. Lee R.H., MJ S., Reger R.L., Spees J.L., Pulin A.A., Olson S.D., et al. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/Scid mice. Proc Natl Acad Sci USA 103 (2006) 17438-17443
53. + regulatory T cells. Stem Cells 26 (2008) 212-222
54. + regulatory T cells responsible for protection against diabetes. Proc Natl Acad Sci USA 101 (2004) 4572-4577
55. + regulatory T cells from peripheral Foxp3- precursors. Blood 110 (2007) 4293-4302