Persistent circulating human insulin in sheep transplanted in utero with human mesenchymal stem cells

Experimental Hematology

Volumn 38, Issue 4, 2010, Pages 311-320

  Ersek, Adel ^a   Pixley, John S ^b   Goodrich, A Daisy ^a   Porada, Christopher D ^a   Almeida Porada, Graca ^a   Thain, David S ^a   Zanjani, Esmail D ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN;

ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; ENGRAFTMENT; FETUS; FETUS CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN UTERO STEM CELL TRANSPLANTATION; INSULIN BLOOD LEVEL; INSULIN RELEASE; LIVER; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PANCREAS; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN; ISLETS OF LANGERHANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; PREGNANCY; REFERENCE STANDARDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SHEEP;

OVIS ARIES;

EID: 77950854541     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2010.02.005     Document Type: Article

References (51)

1. Eisenbarth G.S. Type I diabetes mellitus. A chronic autoimmune disease. N Engl J Med 1986, 314:1360-1368.
2. Mathis D., Vence L., Benoist C. B-cell death during progression to diabetes. Nature 2001, 414:792-798.
3. Knip M., Siljander H. Autoimmune mechanisms in type 1 diabetes. Autoimmun Rev 2008, 7:550-557.
4. Inzucchi S.E., Sherwin R.S. Type 1 diabetes mellitus. Cecil Medicine 2008, Saunders Elsevier, Philadelphia. 23rd ed. L. Goldman, D. Ausiello (Eds.).
5. Alemzadeh R., Wyatt D.T. Diabetes mellitus in children. Nelson Textbook of Pediatrics 2007, Saunders Elsevier, Philadelphia. 18th ed. R.M. Kliegman, B.R. Behrman, H.B. Jenson, B.F. Stanton (Eds.).
6. Davani B., Ikonomou L., Raaka B.M., et al. Human islet-derived precursor cells are mesenchymal stromal cells that differentiate and mature to hormone-expressing cells in vivo. Stem Cells 2007, 25:3215-3222.
7. Kayali A.G., Flores L.E., Lopez A.D., et al. Limited capacity of human adult islets expanded in vitro to redifferentiate into insulin-producing beta-cells. Diabetes 2007, 56:703-708.
8. Bonner-Weir S., Weir G.C. New sources of pancreatic β-cells. Nat Biotechnol 2005, 23:857-861.
9. Heimberg H. Boosting β-cell numbers. N Engl J Med 2008, 359:2723-2724.
10. Pixley J.S., Mackintosh F.R., Zanjani E.D. Experimental and clinical basis of intrauterine stem cell transplantation. Rev Clin Exp Hematol 1999, 8:11-32.
11. Skopal-Chase J.L., Pixley J.S., Torabi A., et al. Immune ontogeny and engraftment receptivity in the sheep fetus. Fetal Diagn Ther 2009, 25:102-110.
12. Tran N.D., Porada C.D., Almeida-Porada G., Glimp H.A., Anderson W.F., Zanjani E.D. Induction of stable prenatal tolerance to b-galactosidase by in utero gene transfer into preimmune sheep fetuses. Blood 2001, 97:3417-3423.
13. Zanjani E.D., Almeida-Porada G., Livingston A.G., Zeng H., Ogawa M. Reversible expression of CD34 by adult human bone marrow long-term engrafting hematopoietic stem cells. Exp Hematol 2003, 31:406-412.
14. Zanjani E.D. The human sheep xenograft model for the study of the in vivo potential of human HSC and in utero gene transfer. Stem Cells 2000, 18:151.
15. Almeida-Porada G., Porada C., Gupta N., Torabi A., Thain D., Zanjani E.D. The human-sheep chimeras as a model for human stem cell mobilization and evaluation of hematopoietic grafts' potential. Exp Hematol 2007, 35:1594-1600.
16. Owen R.D. Immunogenetic consequences of vascular anastomoses between bovine twins. Science 1945, 102:400-401.
17. Ohki H., Martin C., Corbel C., Coltey M., Le Douarin N.M. Tolerance induced by thymic epithelial grafts in birds. Science 1987, 237:1032-1035.
18. Flake A.W., Harrison M.R., Adzick N.S., Zanjani E.D. Transplantation of fetal hematopoietic stem cells in utero: the creation of hematopoietic chimeras. Science 1986, 233:776-778.
19. Zanjani E.D., Flake A.W., Rice H., Hedrick M., Tavassoli M. Long-term repopulating ability of xenogeneic transplanted human fetal liver hematopoietic stem cells in sheep. J Clin Invest 1994, 93:1051-1055.
20. Schwartz R.H. Immunologic tolerance. Fundamental Immunology 2008, 898-942. Lippincott Williams & Wilkins, Philadelphia. 6th ed. W.E. Paul (Ed.).
21. Huang H., Tang X. Phenotypic determination and characterization of nestin-positive precursors derived from human fetal pancreas. Lab Invest 2003, 83:539-547.
22. Zhang L., Hong T.P., Hu J., Liu Y., Wu Y., Li L. Nestin-positive progenitor cells isolated from human fetal pancreas have phenotypic markers identical to mesenchymal stem cells. World J Gastroenterol 2005, 11:2906-2911.
23. Stenderup K., Justesen J., Clausen C., Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003, 33:919-926.
24. Banfi A., Muraglia A., Dozin B., Mastrogiacomo M., Cancedda R., Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp Hematol 2000, 28:707-715.
25. Guillot P.V., Gotherstrom C., Chan J., Kurataa H., Fiska M.N. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells 2007, 25:646-654.
26. Olivier E.N., Rybicki A.C., Bouhassira E.E. Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 2006, 24:1914-1922.
27. Martin D.R., Cox N.R., Hathcock T.L., Niemeyer G.P., Baker H.J. Isolation and characterization of multipotential mesenchymal stem cells from feline bone marrow. Exp Hematol 2002, 30:879-886.
28. Le Blanc K., Tammik L., Sundberg B., Haynesworth S.E., Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 2003, 57:11-20.
29. Chang W., Tu C., Bajra R., et al. Calcium sensing in cultured chondrogenic RCJ3.1C5.18 cells. Endocrinology 1999, 140:1911-1919.
30. Narayan A.D., Chase J.L., Lewis R.L., et al. Human embryonic stem cell-derived hematopoietic cells are capable of engrafting primary as well as secondary fetal sheep recipients. Blood 2006, 107:2180-2183.
31. Zou C., Suen P.M., Zhang Y., et al. Isolation and in vitro characterization of pancreatic progenitor cells from the islets of diabetic monkey models. Int J Biochem Cell Biol 2006, 38:973-984.
32. Banfi A., Muraglia A., Dozin B., Mastrogiacomo M., Cancedda R., Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp Hematol 2000, 28:707-715.
33. Ozdogu H., Sozer O., Boga C., Kozanoglu I., Maytalman E., Guzey M. Flow cytometric evaluation of circulating endothelial cells: a new protocol for identifying endothelial cells at several stages of differentiation. Am J Hematol 2007, 82:706-711.
34. Soria B. In-vitro differentiation of pancreatic beta-cells. Differentiation 2001, 68:205-219.
35. Wiese C., Rolletschek A., Kania G., et al. Nestin expression-a property of multi-lineage progenitor cells?. Cell Mol Life Sci 2004, 61:2510-2522.
36. Huurman V.A., Hilbrands R., Pinkse G.G., et al. Cellular islet autoimmunity associates with clinical outcome of islet cell transplantation. PLoS ONE 2008, 3. e2435.
37. Chen X., Armstrong M.A., Li G. Mesenchymal stem cells in immunoregulation. Immunol Cell Biol 2006, 84:413-421.
38. Chen L.B., Jiang X.B., Yang L. Differentiation of rat marrow mesenchymal stem cells into pancreatic islet beta-cells. World J Gastroenterol 2004, 10:3016-3020.
39. Colter D.C., Class R., DiGirolamo C.M., Prockop D.J. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. PNAS 2000, 97:3213-3218.
40. Smith F.O., Lampkin B.C., Versteeg C., et al. Expression of lymphoid-associated cell surface antigens by childhood acute myeloid leukemia cells lacks prognostic significance. Blood 1992, 79:2415-2422.
41. Bodnar C.A., Sen A., Kallos M.S., Behie L.A., Petropavlovskaia M., Rosenberg L. Characterization of human islet-like structures generated from pancreatic precursor cells in culture. Biotechnol Bioeng 2006, 93:980-988.
42. Calvo E.L., Boucher C., Pelletier G., Morisset J. Ontogeny of hepatocyte growth factor and c-met/hgf receptor in rat pancreas. Biochem Biophys Res Commun 1996, 229:257-263.
43. Otonkoski T., Cirulli V., Beattie M., et al. A role for hepatocyte growth factor/scatter factor in fetal mesenchyme-induced pancreatic beta-cell growth. Endocrinology 1996, 137:3131-3139.
44. Wojakowski W., Tendera M., Zebzda A., et al. Mobilization of CD34+, CD117+, CXCR4+, c-met+ stem cells is correlated with left ventricular ejection fraction and plasma NT-proBNP levels in patients with acute myocardial infarction. Eur Heart J 2006, 27:283-289.
45. Neuss S., Becher E., Woltje M., Tietze L., Jahnen-Dechent W. Functional Expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggests a role in cell mobilization, tissue repair, and wound healing. Stem Cells 2004, 22:405-414.
46. Pozzan R., Dimetz T., Gazzola H.M., Gomes M.B. The C-peptide response to a standard mixed meal in a group of Brazilian type 1 diabetic patients. Braz J Med Biol Res 1997, 30:1169-1174.
47. Alvarez-Dolado M., Pardal R., Garcia-Verdugo J.M., et al. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 2003, 425:968-973.
48. Sato Y., Araki H., Kato J., et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005, 106:756-763.
49. Colletti E.J., Airey J.A., Liu W., et al. Generation of tissue-specific cells from MSC does not require fusion or donor-to host mitochondrial/membrane transfer. Stem Cell Res 2009, 2:125-138.
50. Jiang Y., Jahagirdar B.N., Reinhardt R.L., et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
51. Ianus A., Holz G.G., Theise N.D., Hussain M.A. In vivo derivation of glucose-competent pancreatic endocrine cells from bone marrow without evidence of cell fusion. J Clin Invest 2003, 111:843-850.