Generation of Glucose-Responsive, Insulin-Producing Cells from Human Umbilical Cord Blood-Derived Mesenchymal Stem Cells

Cell Transplantation

Volumn 21, Issue 6, 2012, Pages 1321-1339

  Prabakar, Kamalaveni R ^a   Domínguez Bendala, Juan ^a   Damaris Molano, R ^a   Pileggi, Antonello ^a   Villate, Susana ^a   Ricordi, Camillo ^a   Inverardi, Luca ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Adult stem cells; Islets of Langerhans; Mesenchymal stem cells (MSCs); Pancreas; Umbilical cord blood

Indexed keywords

C PEPTIDE; GLUCOSE; INSULIN; PANCREAS HORMONE;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CONTROLLED STUDY; CORD BLOOD DERIVED MESENCHYMAL STEM CELL; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; MESENCHYMAL STEM CELL; PANCREAS ISLET BETA CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION; UMBILICAL CORD BLOOD;

ANIMALS; BIOLOGICAL MARKERS; C-PEPTIDE; CELL DIFFERENTIATION; CELLS, CULTURED; ENDOCRINE CELLS; GLUCOSE; HUMANS; IMMUNOPHENOTYPING; INSULIN; INSULIN-SECRETING CELLS; MAF TRANSCRIPTION FACTORS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED NOD; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS; UMBILICAL CORD;

ANIMALIA;

EID: 84865530076     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X612530     Document Type: Article

References (64)

1. Aguayo-Mazzucato, C.; Bonner-Weir, S. Stem cell therapy for type 1 diabetes mellitus. Nat. Rev. Endocrinol. 6(3):139-148; 2010.
2. Atlasi, Y.; Mowla, S. J.; Ziaee, S. A.; Gokhale, P. J.; Andrews, P. W. OCT4 spliced variants are differentially expressed in human pluripotent and nonpluripotent cells. Stem Cells 26(12):3068-3074; 2008.
3. Baertschiger, R. M.; Bosco, D.; Morel, P.; Serre-Beinier, V.; Berney, T.; Buhler, L. H.; Gonelle-Gispert, C. Mesenchymal stem cells derived from human exocrine pancreas express transcription factors implicated in beta-cell development. Pancreas 37(1):75-84; 2008.
4. Barachini, S.; Trombi, L.; Danti, S.; D'Alessandro, D.; Battolla, B.; Legitimo, A.; Nesti, C.; Mucci, I.; D'Acunto, M.; Cascone, M. G.; Lazzeri, L.; Mattii, L.; Consolini, R.; Petrini, M. Morpho-functional characterization of human mesenchymal stem cells from umbilical cord blood for potential uses in regenerative medicine. Stem Cells Dev. 18(2):293-305; 2009.
5. Bieback, K.; Kern, S.; Kluter, H.; Eichler, H. Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 22(4):625-634; 2004.
6. Chen, S.; Borowiak, M.; Fox, J. L.; Maehr, R.; Osafune, K.; Davidow, L.; Lam, K.; Peng, L. F.; Schreiber, S. L.; Rubin, L. L.; Melton, D. A small molecule that directs differentiation of human ESCs into the pancreatic lineage. Nat. Chem. Biol. 5(4):258-265; 2009.
7. D'Amour, K. A.; Bang, A. G.; Eliazer, S.; Kelly, O. G.; Agulnick, A. D.; Smart, N. G.; Moorman, M. A.; Kroon, E.; Carpenter, M. K.; Baetge, E. E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 24(11):1392-1401; 2006.
8. Denner, L.; Bodenburg, Y.; Zhao, J. G.; Howe, M.; Cappo, J.; Tilton, R. G.; Copland, J. A.; Forraz, N.; McGuckin, C.; Urban, R. Directed engineering of umbilical cord blood stem cells to produce C-peptide and insulin. Cell Prolif. 40(3):367-380; 2007.
9. Diez del Corral, R.; Storey, K. G. Markers in vertebrate neurogenesis. Nat. Rev. Neurosci. 2(11):835-839; 2001.
10. D'Ippolito, G.; Diabira, S.; Howard, G. A.; Menei, P.; Roos, B. A.; Schiller, P. C. Marrow-isolated adult multi lineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J. Cell Sci. 117(Pt. 14):2971-2981; 2004.
11. Dominguez-Bendala, J. Pancreatic stem cells. New York, NY: Humana Press; 2009.
12. Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.; Krause, D.; Deans, R.; Keating, A.; Prockop, D. J.; Horwitz, E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4): 315-317; 2006.
13. Ende, N.; Chen, R.; Reddi, A. S. Effect of human umbilical cord blood cells on glycemia and insulitis in type 1 diabetic mice. Biochem. Biophys. Res. Commun. 325(3): 665-669; 2004.
14. Fujikawa, T.; Oh, S. H.; Pi, L.; Hatch, H. M.; Shupe, T.; Petersen, B. E. Teratoma formation leads to failure of treatment for type I diabetes using embryonic stem cell-derived insulin-producing cells. Am. J. Pathol. 166(6): 1781-1791; 2005.
15. Furth, M. E.; Atala, A. Stem cell sources to treat diabetes. J. Cell. Biochem. 106(4):507-511; 2009.
16. Gang, E. J.; Bosnakovski, D.; Figueiredo, C. A.; Visser, J. W.; Perlingeiro, R. C. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 109(4):1743-1751; 2007.
17. Gao, F.; Wu, D. Q.; Hu, Y. H.; Jin, G. X. Extracellular matrix gel is necessary for in vitro cultivation of insulin producing cells from human umbilical cord blood derived mesenchymal stem cells. Chinese Med. J. 121(9):811-818; 2008.
18. Gao, F.; Wu, D. Q.; Hu, Y. H.; Jin, G. X.; Li, G. D.; Sun, T. W.; Li, F. J. In vitro cultivation of islet-like cell clusters from human umbilical cord blood-derived mesenchymal stem cells. Transl. Res. 151(6):293-302; 2008.
19. Greco, S. J.; Liu, K. G.; Rameshwar, P. Functional similarities among genes regulated by Oct4 in human mesenchymal and embryonic stem cells. Stem Cells 25(12): 3143-3154; 2007.
20. Guillot, P. V.; Gotherstrom, C.; Chan, J.; Kurata, H.; Fisk, N. M. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells 25(3):646-654; 2007.
21. Guo, T.; Hebrok, M. Stem cells to pancreatic beta-cells: New sources for diabetes cell therapy. Endocr. Rev. 30(3): 214-227; 2009.
22. Haller, M. J.; Viener, H. L.; Wasserfall, C.; Brusko, T.; Atkinson, M. A.; Schatz, D. A. Autologous umbilical cord blood infusion for type 1 diabetes. Exp. Hematol. 36(6): 710-715; 2008.
23. Haller, M. J.; Wasserfall, C. H.; McGrail, K. M.; Cintron, M.; Brusko, T. M.; Wingard, J. R.; Kelly, S. S.; Shuster, J. J.; Atkinson, M. A.; Schatz, D. A. Autologous umbilical cord blood infusion for type 1 diabetes. Diabetes Care 32(11):2041-2046; 2009.
24. Hu, Y. H.; Wu, D. Q.; Gao, F.; Li, G. D.; Yao, L.; Zhang, X. C. A secretory function of human insulin-producing cells in vivo. Hepatobiliary Pancreat. Dis. Int. 8(3):255-260; 2009.
25. Jiang, Y.; Jahagirdar, B. N.; Reinhardt, R. L.; Schwartz, R. E.; Keene, C. D.; Ortiz-Gonzalez, X. R.; Reyes, M.; Lenvik, T.; Lund, T.; Blackstad, M.; Du, J.; Aldrich, S.; Lisberg, A.; Low, W. C.; Largaespada, D. A.; Verfaillie, C. M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418(6893):41-49; 2002.
26. Jo, C. H.; Kim, O. S.; Park, E. Y.; Kim, B. J.; Lee, J. H.; Kang, S. B.; Lee, J. H.; Han, H. S.; Rhee, S. H.; Yoon, K. S. Fetal mesenchymal stem cells derived from human umbilical cord sustain primitive characteristics during extensive expansion. Cell Tissue Res. 334(3):423-433; 2008.
27. Juhl, K.; Bonner-Weir, S.; Sharma, A. Regenerating pancreatic beta-cells: Plasticity of adult pancreatic cells and the feasibility of in-vivo neogenesis. Curr. Opin. Organ Transplant. 15(1):79-85; 2010.
28. Kern, S.; Eichler, H.; Stoeve, J.; Kluter, H.; Bieback, K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24(5):1294-1301; 2006.
29. Koblas, T.; Zacharovovà, K.; Berkovà, Z.; Leontovic, I.; Dovolilovà, E.; Zàmecník, L.; Saudek, F. In vivo differentiation of human umbilical cord blood-derived cells into insulin-producing β cells. Folia Biol. (Praha) 55(6):224-232; 2009.
30. Kode, J. A.; Mukherjee, S.; Joglekar, M. V.; Hardikar, A. A. Mesenchymal stem cells: Immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 11(4):377-391; 2009.
31. Kögler, G.; Sensken, S.; Airey, J. A.; Trapp, T.; Müschen, M.; Feldhahn, N.; Liedtke, S.; Sorg, R. V.; Fischer, J.; Rosenbaum, C.; Greschat, S.; Knipper, A.; Bender, J.; Degistirici, O.; Gao, J.; Caplan, A. I.; Colletti, E. J.; Almeida-Porada, G.; Müller, H. W.; Zanjani, E.; Wernet, P. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J. Exp. Med. 200(2):123-135; 2004.
32. Kogler, G.; Sensken, S.; Wernet, P. Comparative generation and characterization of pluripotent unrestricted somatic stem cells with mesenchymal stem cells from human cord blood. Exp. Hematol. 34(11):1589-1595; 2006.
33. Kotoula, V.; Papamichos, S. I.; Lambropoulos, A. F. Revisiting OCT4 expression in peripheral blood mononuclear cells. Stem Cells 26(1):290-291; 2008.
34. Kroon, E.; Martinson, L. A.; Kadoya, K.; Bang, A. G.; Kelly, O. G.; Eliazer, S.; Young, H.; Richardson, M.; Smart, N. G.; Cunningham, J.; Agulnick, A. D.; D'Amour, K. A.; Carpenter, M. K.; Baetge, E. E. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 26(4):443-452; 2008.
35. Lee, O. K.; Kuo, T. K.; Chen, W. M.; Lee, K. D.; Hsieh, S. L.; Chen, T. H. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 103(5):1669-1675; 2004.
36. Lengner, C. J.; Camargo, F. D.; Hochedlinger, K.; Welstead, G. G.; Zaidi, S.; Gokhale, S.; Scholer, H. R.; Tomilin, A.; Jaenisch, R. Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cells 1(4):403-415; 2007.
37. Liedtke, S.; Enczmann, J.; Waclawczyk, S.; Wernet, P.; Kögler, G. Oct4 and its pseudogenes confuse stem cell research. Cell Stem Cells 1(4):364-366; 2007.
38. Markov, V.; Kusumi, K.; Tadesse, M. G.; Markov, V.; William, D. A.; Hall, D. M.; Lounev, V.; Carlton, A.; Leonard, J.; Cohen, R. I.; Rappaport, E. F.; Saitta, B. Identification of cord blood-derived mesenchymal stem/ stromal cell populations with distinct growth kinetics, differentiation potentials, and gene expression profiles. Stem Cells Dev. 16(1):53-73; 2007.
39. Mayhew, C. N.; Wells, J. M. Converting human pluripotent stem cells into beta-cells: Recent advances and future challenges. Curr. Opin. Organ Transplant. 15(1):54-60; 2010.
40. McCall, M. D.; Toso, C.; Baetge, E. E.; Shapiro, A. M. Are stem cells a cure for diabetes? Clin. Sci. (Lond.). 118(2):87-97; 2009.
41. McGuckin, C. P.; Forraz, N.; Baradez, M. O.; Navran, S.; Zhao, J.; Urban, R.; Tilton, R.; Denner, L. Production of stem cells with embryonic characteristics from human umbilical cord blood. Cell Prolif. 38(4):245-255; 2005.
42. McLean, A. B.; D'Amour, K. A.; Jones, K. L.; Krishnamoorthy, M.; Kulik, M. J.; Reynolds, D. M.; Sheppard, A. M.; Liu, H.; Xu, Y.; Baetge, E. E.; Dalton, S. Activin A efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 25(1):29-38; 2007.
43. Mishra, P. K.; Singh, S. R.; Joshua, I. G.; Tyagi, S. C. Stem cells as a therapeutic target for diabetes. Front. Biosci. 15:461-477; 2010.
44. Moriscot, C.; de Fraipont, F.; Richard, M. J.; Marchand, M.; Savatier, P.; Bosco, D.; Favrot, M.; Benhamou, P. Y. Human bone marrow mesenchymal stem cells can express insulin and key transcription factors of the endocrine pancreas developmental pathway upon genetic and/or microenvironmental manipulation in vitro. Stem Cells 23(4): 594-603; 2005.
45. Parekh, V. S.; Joglekar, M. V.; Hardikar, A. A. Differentiation of human umbilical cord blood-derived mononuclear cells to endocrine pancreatic lineage. Differentiation 78(4):232-240; 2009.
46. Pessina, A.; Eletti, B.; Croera, C.; Savalli, N.; Diodovich, C.; Gribaldo, L. Pancreas developing markers expressed on human mononucleated umbilical cord blood cells. Biochem. Biophys. Res. Commun. 323(1):315-322; 2004.
47. Poggioli, R.; Faradji, R. N.; Ponte, G.; Betancourt, A.; Messinger, S.; Baidal, D. A.; Froud, T.; Ricordi, C.; Alejandro, R. Quality of life after islet transplantation. Am. J. Transplant. 6(2):371-378; 2006.
48. Polak, M.; Bouchareb-Banaei, L.; Scharfmann, R.; Czernichow, P. Early pattern of differentiation in the human pancreas. Diabetes 49(2):225-232; 2000.
49. Rebelatto, C. K.; Aguiar, A. M.; Moretão, M. P.; Senegaglia, A. C.; Hansen, P.; Barchiki, F.; Oliveira, J.; Martins, J.; Kuligovski, C.; Mansur, F.; Christofis, A.; Amaral, V. F.; Brofman, P. S.; Goldenberg, S.; Nakao, L. S.; Correa, A. Dissimilar differentiation of mesenchymal stem cells from bone marrow, umbilical cord blood, and adipose tissue. Exp. Biol. Med. 233(7):901-913; 2008.
50. Riekstina, U.; Cakstina, I.; Parfejevs, V.; Hoogduijn, M.; Jankovskis, G.; Muiznieks, I.; Muceniece, R.; Ancans, J. Embryonic stem cell marker expression pattern in human mesenchymal stem cells derived from bone marrow, adipose tissue, heart and dermis. Stem Cell Rev. 5(4):378-386; 2009.
51. Rojas, A.; Khoo, A.; Tejedo, J. R.; Bedova, F. J.; Soria, B.; Martin, F. Islet cell development. Adv. Exp. Med. Biol. 654:59-75; 2010.
52. Roubelakis, M. G.; Pappa, K. I.; Bitsika, V.; Zagoura, D.; Vlahou, A.; Papadaki, H. A.; Antsaklis, A.; Anagnou, N. P. Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: Comparison to bone marrow mesenchymal stem cells. Stem Cells Dev. 16(6):931-952; 2007.
53. Seo, K. W.; Lee, S. R.; Bhandari, D. R.; Roh, K. H.; Park, S. B.; So, A. Y.; Jung, J. W.; Seo, M. S.; Kang, S. K.; Lee, Y. S.; Kang, K. S. OCT4A contributes to the stemness and multi-potency of human umbilical cord blood-derived multipotent stem cells (hUCB-MSCs). Biochem. Biophys. Res. Commun. 384(1):120-125; 2009.
54. Sun, B.; Roh, K. H.; Lee, S. R.; Lee, Y. S.; Kang, K. S. Induction of human umbilical cord blood-derived stem cells with embryonic stem cell phenotypes into insulin producing islet-like structure. Biochem. Biophys. Res. Commun. 354(4):919-923; 2007.
55. Thomson, J. A.; Itskovitz-Eldor, J.; Shapiro, S. S.; Waknitz, M. A.; Swiergiel, J. J.; Marshall, V. S.; Jones, J. M. Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145-1147; 1998.
56. Timper, K.; Seboek, D.; Eberhardt, M.; Linscheid, P.; Christ-Crain, M.; Keller, U.; Mller, B.; Zulewski, H. Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem. Biophys. Res. Commun. 341(4):1135-1140; 2006.
57. Van Hoof, D.; D'Amour, K. A.; German, M. S. Derivation of insulin-producing cells from human embryonic stem cells. Stem Cell Res. 3(2-3):73-87; 2009.
58. Vija, L.; Farge, D.; Gautier, J. F.; Vexiau, P.; Dumitrache, C.; Bourgarit, A.; Verrecchia, F.; Larghero, J. Mesenchymal stem cells: Stem cell therapy perspectives for type 1 diabetes. Diabetes Metab. 35(2):85-93; 2009.
59. Yechoor, V.; Chan, L. Minireview: Beta-cell replacement therapy for diabetes in the 21st century: Manipulation of cell fate by directed differentiation. Mol. Endocrinol. 24(8):1501-1511; 2010.
60. Yoshida, S.; Ishikawa, F.; Kawano, N.; Shimoda, K.; Nagafuchi, S.; Shimoda, S.; Yasukawa, M.; Kanemaru, T.; Ishibashi, H.; Shultz, L. D.; Harada, M. Human cord blood-derived cells generate insulin-producing cells in vivo. Stem Cells 23(9):1409-1416; 2005.
61. Zaibak, F.; Bello, P.; Kozlovski, J.; Crombie, D.; Ang, H.; Dottori, M.; Williamson, R. Unrestricted somatic stem cells from human umbilical cord blood grow in serum-free medium as spheres. BMC Biotechnol. 9:101-116; 2009.
62. Zhao, M.; Amiel, S. A.; Ajami, S.; Jiang, J.; Rela, M.; Heaton, N.; Huang, G. C. Amelioration of streptozotocininduced diabetes in mice with cells derived from human marrow stromal cells. PLoS One 3(7):e2666; 2008.
63. Zhao, Y.; Wang, H.; Mazzone, T. Identification of stem cells from human umbilical cord blood with embryonic and hematopoietic characteristics. Exp. Cell Res. 312(13): 2454-2464; 2006.
64. Zheng, C.; Yang, S.; Guo, Z.; Liao, W.; Zhang, L.; Yang, R.; Han, Z. C. Human multipotent mesenchymal stromal cells from fetal lung expressing pluripotent markers and differentiating into cell types of three germ layers. Cell Transplant. 18(10):1093-1109; 2009.