Enrichment of human embryonic stem cell-derived NKX6.1-Expressing pancreatic progenitor cells accelerates the maturation of insulin-secreting cells in vivo

Stem Cells

Volumn 31, Issue 11, 2013, Pages 2432-2442

  Rezania, Alireza ^a   Bruin, Jennifer E ^b   Xu, Jean ^a   Narayan, Kavitha ^a   Fox, Jessica K ^a   O'Neil, John J ^b   Kieffer, Timothy J ^b,c  

^a JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^b Life Sciences Institute   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Beta cells; Cell therapy; Diabetes; Human embryonic stem cells; Transplantation

Indexed keywords

ARGININE; C PEPTIDE; GLUCAGON; GLUCOSE; INSULIN; TRANSCRIPTION FACTOR NKX6.1;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL MATURATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDODERM; HUMAN; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; STEM CELL TRANSPLANTATION;

MUS;

BETA CELLS; CELL THERAPY; DIABETES; HUMAN EMBRYONIC STEM CELLS; TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; ENDODERM; HOMEODOMAIN PROTEINS; HUMANS; INSULIN-SECRETING CELLS; MALE; MICE; MICE, SCID; PANCREAS;

EID: 84887940137     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1489     Document Type: Article

References (35)

1. Robertson RP. Update on transplanting beta cells for reversing type 1 diabetes. Endocrinol Metab Clin North Am 2010; 39: 655-667.
2. Ryan EA, Lakey JR, Rajotte RV et al. Clinical outcomes and insulin secretion after islet transplantation with the Edmonton protocol. Diabetes 2001; 50: 710-719. (Pubitemid 32242625)
3. Shapiro AM, Lakey JR, Ryan EA et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 2000; 343: 230-238. (Pubitemid 30490390)
4. Shapiro AM. State of the art of clinical islet transplantation and novel protocols of immunosuppression. Curr Diab Rep 2011; 11: 345-354.
5. Bruin JE, Kieffer TJ. Differentiation of human embryonic stem cells into pancreatic endocrine cells. In: Hayat MA, ed. Stem Cells and Cancer Stem Cells: Therapeutic Applications in Disease and Injury. New York: Springer, 2012: 192-206.
6. Kelly OG, Chan MY, Martinson LA et al. Cell-surface markers for the isolation of pancreatic cell types derived from human embryonic stem cells. Nat Biotechnol 2011; 29: 750-756.
7. Jiang J, Au M, Lu K et al. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells 2007; 25: 1940-1953. (Pubitemid 47258172)
8. Jiang W, Shi Y, Zhao D et al. In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 2007; 17: 333-344. (Pubitemid 46639938)
9. Zhang D, Jiang W, Liu M et al. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res 2009; 19: 429-438.
10. Nostro MC, Sarangi F, Ogawa S et al. Stage-specific signaling through TGFbeta family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 2011; 138: 861-871.
11. D'Amour K.A., Bang AG, Eliazer S et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006; 24: 1392-1401. (Pubitemid 44722103)
12. Kroon E, Martinson LA, Kadoya K et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008; 26: 443-452. (Pubitemid 351501814)
13. Mfopou JK, Chen B, Mateizel I et al. Noggin, retinoids, and fibroblast growth factor regulate hepatic or pancreatic fate of human embryonic stem cells. Gastroenterology 2010; 138: 2233-2245, 2245 e2231-2214.
14. Shim JH, Kim SE, Woo DH et al. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 2007; 50: 1228-1238. (Pubitemid 46701546)
15. Cai J, Yu C, Liu Y et al. Generation of homogeneous PDX1(+) pancreatic progenitors from human ES cell-derived endoderm cells. J Mol Cell Biol 2010; 2: 50-60.
16. Rezania A, Riedel MJ, Wideman RD et al. Production of functional glucagon-secreting alpha-cells from human embryonic stem cells. Diabetes 2011; 60: 239-247.
17. Rezania A, Bruin JE, Riedel MJ et al. Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice. Diabetes 2012; 61: 2016-2029.
18. Bruin JE, Rezania A, Xu J et al. Maturation and function of human embryonic stem cell-derived pancreatic progenitors in macroencapsulation devices following transplant into mice. Diabetologia 2013; 56: 1987-1998.
19. Rieck S, Bankaitis ED, Wright CV. Lineage determinants in early endocrine development. Semin Cell Dev Biol 2012; 23: 673-684.
20. Basford CL, Prentice KJ, Hardy AB et al. The functional and molecular characterisation of human embryonic stem cell-derived insulin-positive cells compared with adult pancreatic beta cells. Diabetologia 2012; 55: 358-371.
21. Brauker JH, Carr-Brendel VE, Martinson LA et al. Neovascularization of synthetic membranes directed by membrane microarchitecture. J Biomed Mater Res 1995; 29: 1517-1524.
22. Lindskog C, Korsgren O, Ponten F et al. Novel pancreatic beta cell-specific proteins: Antibody-based proteomics for identification of new biomarker candidates. J Proteomics 2012; 75: 2611-2620.
23. Halban PA, German MS, Kahn SE et al. Current status of islet cell replacement and regeneration therapy. J Clin Endocrinol Metab 2010; 95: 1034-1043.
24. Coppieters KT, Wiberg A, Amirian N et al. Persistent glucose transporter expression on pancreatic beta cells from longstanding type 1 diabetic individuals. Diabetes Metab Res Rev 2011; 27: 746-754.
25. De Vos A., Heimberg H, Quartier E et al. Human and rat beta cells differ in glucose transporter but not in glucokinase gene expression. J Clin Invest 1995; 96: 2489-2495.
26. Jermendy A, Toschi E, Aye T et al. Rat neonatal beta cells lack the specialised metabolic phenotype of mature beta cells. Diabetologia 2011; 54: 594-604.
27. Zhu X, Orci L, Carroll R et al. Severe block in processing of proinsulin to insulin accompanied by elevation of des-64,65 proinsulin intermediates in islets of mice lacking prohormone convertase 1/3. Proc Natl Acad Sci USA 2002; 99: 10299-10304.
28. Wang H, Brun T, Kataoka K et al. MAFA controls genes implicated in insulin biosynthesis and secretion. Diabetologia 2007; 50: 348-358.
29. Zhang C, Moriguchi T, Kajihara M et al. MafA is a key regulator of glucose-stimulated insulin secretion. Mol Cell Biol 2005; 25: 4969-4976. (Pubitemid 40781098)
30. Aguayo-Mazzucato C., Koh A, El Khattabi I et al. Mafa expression enhances glucose-responsive insulin secretion in neonatal rat beta cells. Diabetologia 2011; 54: 583-593.
31. Harmon JS, Bogdani M, Parazzoli SD et al. beta-Cell-specific overex-pression of glutathione peroxidase preserves intranuclear MafA and reverses diabetes in db/db mice. Endocrinology 2009; 150: 4855-4862.
32. Butler AE, Robertson RP, Hernandez R et al. Beta cell nuclear muscu-loaponeurotic fibrosarcoma oncogene family A (MafA) is deficient in type 2 diabetes. Diabetologia 2012; 55: 2985-2988.
33. Johansson KA, Dursun U, Jordan N et al. Temporal control of neuro-genin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev Cell 2007; 12: 457-465.
34. Herrera PL, Nepote V, Delacour A. Pancreatic cell lineage analyses in mice. Endocrine 2002; 19: 267-278.
35. Riedel MJ, Asadi A, Wang R et al. Immunohistochemical characterisation of cells co-producing insulin and glucagon in the developing human pancreas. Diabetologia 2012; 55: 372-381.