A scalable system for production of functional pancreatic progenitors from human embryonic stem cells

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Schulz, Thomas C ^a   Young, Holly Y ^a   Agulnick, Alan D ^a   Babin, M Josephine ^a   Baetge, Emmanuel E ^a   Bang, Anne G ^a   Bhoumik, Anindita ^a   Cepa, Igor ^a   Cesario, Rosemary M ^a   Haakmeester, Carl ^a   Kadoya, Kuniko ^a   Kelly, Jonathan R ^a   Kerr, Justin ^a   Martinson, Laura A ^a   McLean, Amanda B ^b   Moorman, Mark A ^a   Payne, Janice K ^a   Richardson, Mike ^a   Ross, Kelly G ^a   Sherrer, Eric S ^a   Song, Xuehong ^a   Wilson, Alistair Z ^a   Brandon, Eugene P ^a   Green, Chad E ^a   Kroon, Evert J ^a   Kelly, Olivia G ^a   D'Amour, Kevin A ^a   Robins, Allan J ^a   more..

^a Georgia Biobusiness Center   (United States)

^b University of Georgia ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; GLUCOSE; MESSENGER RNA; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL LINEAGE; CELL POPULATION; CELL STRAIN; CELL STRAIN CYT49; CELL SUSPENSION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS CELL; PANCREAS ISLET BETA CELL; PROCESS OPTIMIZATION; PROTEIN EXPRESSION; SUSPENSION CELL CULTURE; THAWING; ANALYSIS OF VARIANCE; ANIMAL; BATCH CELL CULTURE; CRYOPRESERVATION; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; INSULIN DEPENDENT DIABETES MELLITUS; MALE; METHODOLOGY; MOUSE MUTANT; PHYSIOLOGY; TRANSPLANTATION;

MUS;

ANALYSIS OF VARIANCE; ANIMALS; BATCH CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CRYOPRESERVATION; DIABETES MELLITUS, TYPE 1; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HUMANS; INSULIN-SECRETING CELLS; MALE; MICE; MICE, SCID; STREPTOZOCIN;

EID: 84862059081     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037004     Document Type: Article

References (47)

1. Shapiro AM, Lakey JR, Ryan EA, Korbutt GS, Toth E, et al. (2000) Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 343: 230-238.
2. Matsumoto S, (2011) Clinical allogeneic and autologous islet cell transplantation: update. Diabetes Metab J 35: 199-206.
3. Dominguez-Bendala J, Inverardi L, Ricordi C, (2011) Stem cell-derived islet cells for transplantation. Curr Opin Organ Transplant 16 (1): 76-82.
4. McCall MD, Toso C, Baetge EE, Shapiro AM, (2009) Are stem cells a cure for diabetes? Clin Sci (Lond) 118: 87-97.
5. D'Amour KA, Bang AG, Eliazer S, Kelly OG, Agulnick AD, et al. (2006) Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24: 1392-1401.
6. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, et al. (2008) Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26: 443-452.
7. Kelly OG, Chan MY, Martinson LA, Kadoya K, Ostertag TM, et al. (2011) Cell-surface markers for the isolation of pancreatic cell types derived from human embryonic stem cells. Nat Biotechnol 29: 750-756.
8. Cai J, Yu C, Liu Y, Chen S, Guo Y, et al. (2009) Generation of homogeneous PDX1(+) pancreatic progenitors from human ES cell-derived endoderm cells. J Mol Cell Biol 2: 50-60.
9. Johannesson M, Stahlberg A, Ameri J, Sand FW, Norrman K, et al. (2009) FGF4 and retinoic acid direct differentiation of hESCs into PDX1-expressing foregut endoderm in a time- and concentration-dependent manner. PLoS One 4: e4794.
10. Mfopou JK, Chen B, Mateizel I, Sermon K, Bouwens L, (2010) Noggin, retinoids, and fibroblast growth factor regulate hepatic or pancreatic fate of human embryonic stem cells. Gastroenterology 138: 2233-2245.
11. Ungrin MD, Clarke G, Yin T, Niebrugge S, Nostro MC, et al. (2011) Rational bioprocess design for human pluripotent stem cell expansion and endoderm differentiation based on cellular dynamics. Biotechnol Bioeng. Dec 2 doi:10.1002/bit.24375.
12. Clark GO, Yochem RL, Axelman J, Sheets TP, Kaczorowski DJ, et al. (2007) Glucose responsive insulin production from human embryonic germ (EG) cell derivatives. Biochem Biophys Res Commun 356: 587-593.
13. Jiang W, Shi Y, Zhao D, Chen S, Yong J, et al. (2007) In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 17: 333-344.
14. Shim JH, Kim SE, Woo DH, Kim SK, Oh CH, et al. (2007) Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 50: 1228-1238.
15. Chen X, Chen A, Woo TL, Choo AB, Reuveny S, et al. (2010) Investigations into the metabolism of two-dimensional colony and suspended microcarrier cultures of human embryonic stem cells in serum-free media. Stem Cells Dev 19: 1781-1792.
16. Schulz TC, Robins AJ, (2009) Media and extracellular matrix requirements for large-scale ESC growth. In: Lakshmipathy U, Chesnut JD, Thyagarajan B, editors. Emerging Technology Platforms for Stem Cells Hoboken, NJ John Wiley and Sons pp. 251-274.
17. Maitra A, Arking DE, Shivapurkar N, Ikeda M, Stastny V, et al. (2005) Genomic alterations in cultured human embryonic stem cells. Nat Genet 37: 1099-1103.
18. Wang L, Schulz TC, Sherrer ES, Dauphin DS, Shin S, et al. (2007) Self-renewal of human embryonic stem cells requires insulin-like growth factor-1 receptor and ERBB2 receptor signaling. Blood 110: 4111-4119.
19. Barbaric I, Jones M, Buchner K, Baker D, Andrews PW, et al. (2011) Pinacidil enhances survival of cryopreserved human embryonic stem cells. Cryobiology 63 (3): 298-305.
20. Ley K, Lundgren E, Berger E, Arfors KE, (1989) Shear-dependent inhibition of granulocyte adhesion to cultured endothelium by dextran sulfate. Blood 73: 1324-1330.
21. Van Winkle AP, Gates ID, Kallos MS, (2012) Mass Transfer Limitations in Embryoid Bodies during Human Embryonic Stem Cell Differentiation. Cells Tissues Organs doi:10.1159/000330691.
22. Nostro MC, Sarangi F, Ogawa S, Holtzinger A, Corneo B, et al. (2011) Stage-specific signaling through TGF beta family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 138: 861-871.
23. Rezania A, Riedel MJ, Wideman RD, Karanu F, Ao Z, et al. (2010) Production of functional glucagon-secreting alpha-cells from human embryonic stem cells. Diabetes 60: 239-247.
24. Fortina P, Surrey S, (2008) Digital mRNA profiling. Nat Biotechnol 26: 293-294.
25. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, et al. (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26: 317-325.
26. Straub SG, Sharp GW, (2002) Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 18: 451-463.
27. Okamoto H, (1985) The role of poly(ADP-ribose) synthetase in the development of insulin-dependent diabetes and islet B-cell regeneration. Biomed Biochim Acta 44: 15-20.
28. Eizirik DL, Pipeleers DG, Ling Z, Welsh N, Hellerstrom C, et al. (1994) Major species differences between humans and rodents in the susceptibility to pancreatic beta-cell injury. Proc Natl Acad Sci U S A 91: 9253-9256.
29. Hosokawa M, Dolci W, Thorens B, (2001) Differential sensitivity of GLUT1- and GLUT2-expressing beta cells to streptozotocin. Biochem Biophys Res Commun 289: 1114-1117.
30. Quimby FW, Luong RH, (2007) Clinical chemistry of the laboratory mouse. In: Fox JG, Barthold SW, Davisson MT, Newcomer CD, Quimby FW, editors. The mouse in biomedical research Burlington, MA Academic Press pp. 171-216.
31. Crook JM, Peura TT, Kravets L, Bosman AG, Buzzard JJ, et al. (2007) The generation of six clinical-grade human embryonic stem cell lines. Cell Stem Cell 1: 490-494.
32. Draper JS, Smith K, Gokhale P, Moore HD, Maltby E, et al. (2004) Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 22: 53-54.
33. Olariu V, Harrison NJ, Coca D, Gokhale PJ, Baker D, et al. (2009) Modeling the evolution of culture-adapted human embryonic stem cells. Stem Cell Res 4: 50-56.
34. Olmer R, Haase A, Merkert S, Cui W, Palecek J, et al. (2010) Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium. Stem Cell Res 5: 51-64.
35. Amit M, Chebath J, Margulets V, Laevsky I, Miropolsky Y, et al. (2010) Suspension culture of undifferentiated human embryonic and induced pluripotent stem cells. Stem Cell Rev 6: 248-259.
36. Lock LT, Tzanakakis ES, (2009) Expansion and differentiation of human embryonic stem cells to endoderm progeny in a microcarrier stirred-suspension culture. Tissue Eng Part A 15: 2051-2063.
37. Oh SK, Chen AK, Mok Y, Chen X, Lim UM, et al. (2009) Long-term microcarrier suspension cultures of human embryonic stem cells. Stem Cell Res 2: 219-230.
38. Phillips BW, Horne R, Lay TS, Rust WL, Teck TT, et al. (2008) Attachment and growth of human embryonic stem cells on microcarriers. J Biotechnol 138: 24-32.
39. Kehoe DE, Jing D, Lock LT, Tzanakakis ES, (2009) Scalable stirred-suspension bioreactor culture of human pluripotent stem cells. Tissue Eng Part A 16: 405-421.
40. Singh H, Mok P, Balakrishnan T, Rahmat SN, Zweigerdt R, (2010) Up-scaling single cell-inoculated suspension culture of human embryonic stem cells. Stem Cell Res 4: 165-179.
41. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, et al. (2005) Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23: 1534-1541.
42. Li L, Wang BH, Wang S, Moalim-Nour L, Mohib K, et al. (2010) Individual cell movement, asymmetric colony expansion, rho-associated kinase, and E-cadherin impact the clonogenicity of human embryonic stem cells. Biophys J 98: 2442-2451.
43. Verdier C, Couzon C, Duperray A, Singh P, (2009) Modeling cell interactions under flow. J Math Biol 58: 235-259.
44. Blum B, Hrvatin SS, Schuetz C, Bonal C, Rezania A, et al. (2012) Functional beta-cell maturation is marked by an increased glucose threshold and by expression of urocortin 3. Nat Biotechnol. 30: 261-4.
45. Shapiro AM, Ricordi C, Hering BJ, Auchincloss H, Lindblad R, et al. (2006) International trial of the Edmonton protocol for islet transplantation. N Engl J Med 355: 1318-1330.
46. Young HY, Schulz TC, Carpenter MK, (2009) Feeder-free Culture. In: Lanza R, editors. Essentials of stem cell biology, 2nd ed San Diego, CA Elsevier pp. 397-408.
47. Brimble SN, Zeng X, Weiler DA, Luo Y, Liu Y, et al. (2004) Karyotypic stability, genotyping, differentiation, feeder-free maintenance, and gene expression sampling in three human embryonic stem cell lines derived prior to August 9, 2001. Stem Cells Dev 13: 585-97.