Expansion and conversion of human pancreatic ductal cells into insulin-secreting endocrine cells

eLife

Volumn 2013, Issue 2, 2013, Pages

  Lee, Jonghyeob ^a   Sugiyama, Takuya ^a   Liu, Yinghua ^a   Wang, Jing ^a   Gu, Xueying ^a   Lei, Ji ^b   Markmann, James F ^b   Miyazaki, Satsuki ^c   Miyazaki, Jun Ichi ^c   Szot, Gregory L ^d   Bottino, Rita ^e   Kim, Seung K ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; CD133 ANTIGEN; CYTOKERATIN 19; GLUCOKINASE; GLUCOSE; INSULIN; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; KI 67 ANTIGEN; NEUROGENIN 3; PROINSULIN; PROPROTEIN CONVERTASE 1; SOMATOSTATIN; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PDX 1;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL EXPANSION; CELL FRACTIONATION; CELL RENEWAL; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS; PANCREAS ISLET BETA CELL; PANCREATIC DUCTAL CELL; PROGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRAL GENE DELIVERY SYSTEM; CELL DIFFERENTIATION; CELL SEPARATION; CYTOLOGY; ENDOCRINE GLAND; FLOW CYTOMETRY; IMMUNOLOGY; IMMUNOPHENOTYPING; MIDDLE AGED; PANCREAS DUCT; SECRETION (PROCESS); YOUNG ADULT;

ADULT; CELL DIFFERENTIATION; CELL SEPARATION; ENDOCRINE GLANDS; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOPHENOTYPING; INSULIN; MALE; MIDDLE AGED; PANCREATIC DUCTS; YOUNG ADULT;

EID: 84888096421     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00940     Document Type: Article

References (70)

1. Al-Hasani K, Pfeifer A, Courtney M, Ben-Othman N, Gjernes E, Vieira A, et al. 2013. Adult duct-lining cells can reprogram into beta-like cells able to counter repeated cycles of toxin-induced diabetes. Dev Cell 26:86-100. doi: 10.1016/j.devcel.2013.05.018.
2. Alipio Z, Liao W, Roemer EJ, Waner M, Fink LM, Ward DC, et al. 2010. Reversal of hyperglycemia in diabetic mouse models using induced-pluripotent stem (iPS)-derived pancreatic beta-like cells. Proc Natl Acad Sci USA 107:13426-31. doi: 10.1073/pnas.1007884107.
3. Ashcroft FM, Rorsman P. 2012. Diabetes mellitus and the beta cell: the last ten years. Cell 148:1160-71. doi: 10.1016/j.cell.2012.02.010.
4. Benitez CM, Goodyer WR, Kim SK. 2012. Deconstructing pancreas developmental biology. Cold Spring Harbor Perspect Biol 4:a012401. doi: 10.1101/cshperspect.a012401.
5. Blum B, Hrvatin SS, Schuetz C, Bonal C, Rezania A, Melton DA. 2012. Functional beta-cell maturation is marked by an increased glucose threshold and by expression of urocortin 3. Nat Biotechnol 30:261-4. doi: 10.1038/ nbt.2141.
6. Bonner-Weir S, Taneja M, Weir GC, Tatarkiewicz K, Song KH, Sharma A, et al. 2000. In vitro cultivation of human islets from expanded ductal tissue. Proc Natl Acad Sci USA 97:7999-8004. doi: 10.1073/pnas.97.14.7999.
7. Bonner-Weir S, Toschi E, Inada A, Reitz P, Fonseca SY, Aye T, et al. 2004. The pancreatic ductal epithelium serves as a potential pool of progenitor cells. Pediatr Diabetes 5:16-22. doi: 10.1111/j.1399-543X.2004.00075.x.
8. Bouwens L, Pipeleers DG. 1998. Extra-insular beta cells associated with ductules are frequent in adult human pancreas. Diabetologia 41:629-33. doi: 10.1007/s001250050960.
9. Chen H, Carlson EC, Pellet L, Moritz JT, Epstein PN. 2001. Overexpression of metallothionein in pancreatic beta-cells reduces streptozotocin-induced DNA damage and diabetes. Diabetes 50:2040-6. doi: 10.2337/ diabetes.50.9.2040.
10. Cheng X, Ying L, Lu L, Galvao AM, Mills JA, Lin HC, et al. 2012. Self-renewing endodermal progenitor lines generated from human pluripotent stem cells. Cell Stem Cell 10:371-84. doi: 10.1016/j.stem.2012.02.024.
11. Cleveland MH, Sawyer JM, Afelik S, Jensen J, Leach SD. 2012. Exocrine ontogenies: on the development of pancreatic acinar, ductal and centroacinar cells. Semin Cell Dev Biol 23:711-9. doi: 10.1016/j.semcdb.2012.06.008.
12. D'Amour KA, Bang AG, Eliazer S, Kelly OG, Agulnick AD, Smart NG, et al. 2006. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24:1392-401. doi: 10.1038/nbt1259.
13. Fujikawa T, Oh SH, Pi L, Hatch HM, Shupe T, Petersen BE. 2005. Teratoma formation leads to failure of treatment for type I diabetes using embryonic stem cell-derived insulin-producing cells. Am J Pathol 166:1781-91. doi: 10.1016/S0002-9440(10)62488-1.
14. Furuyama K, Kawaguchi Y, Akiyama H, Horiguchi M, Kodama S, Kuhara T, et al. 2011. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat Genet 43:34-41. doi: 10.1038/ng.722.
15. Gao R, Ustinov J, Korsgren O, Otonkoski T. 2005. In vitro neogenesis of human islets reflects the plasticity of differentiated human pancreatic cells. Diabetologia 48:2296-2304. doi: 10.1007/s00125-005-1935-8.
16. Gradwohl G, Dierich A, LeMeur M, Guillemot F. 2000. neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci USA 97:1607-11. doi: 10.1073/pnas.97.4.1607.
17. Gu G, Dubauskaite J, Melton DA. 2002. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129:2447-57.
18. Hanna J, Saha K, Pando B, van Zon J, Lengner CJ, Creyghton MP, et al. 2009. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462:595-601. doi: 10.1038/nature08592.
19. Hao E, Tyrberg B, Itkin-Ansari P, Lakey JR, Geron I, Monosov EZ, et al. 2006. Beta-cell differentiation from nonendocrine epithelial cells of the adult human pancreas. Nat Med 12:310-6. doi: 10.1038/nm1367.
20. Hebrok M. 2012. Generating beta cells from stem cells-the story so far. Cold Spring Harbor Perspect Med 2:a007674. doi: 10.1101/cshperspect.a007674.
21. Henquin J-C. 2005. Cell biology of insulin secretion. In: Kahn CR, Weir GC, King GL, Jacobsen AM, Moses AC, et al, editors. Joslin's diabetes mellitus. Boston, MA, USA: Lippincott Williams & Wilkins. p. 83-107.
22. Heremans Y, Van De Casteele M, in't Veld P, Gradwohl G, Serup P, Madsen O, et al. 2002. Recapitulation of embryonic neuroendocrine differentiation in adult human pancreatic duct cells expressing neurogenin 3. J Cell Biol 159:303-12. doi: 10.1083/jcb.200203074.
23. Hoesli CA, Johnson JD, Piret JM. 2012. Purified human pancreatic duct cell culture conditions defined by serum-free high-content growth factor screening. PLOS ONE 7:e33999. doi: 10.1371/journal.pone.0033999.
24. Immervoll H, Hoem D, Sakariassen PO, Steffensen OJ, Molven A. 2008. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer 8:48. doi: 10.1186/1471-2407-8-48.
25. Inada A, Nienaber C, Katsuta H, Fujitani Y, Levine J, Morita R, et al. 2008. Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc Natl Acad Sci USA 105:19915-9. doi: 10.1073/pnas.0805803105.
26. Klimstra DS, Hruban RH, Pitman MB. 2007. VII - Alimentary Tract, 30 - Pancreas. In: Mills SE, editor. Histology for Pathologists. Philadelphia: Lippincott Williams & Wilkins. p. 723-60.
27. Koblas T, Pektorova L, Zacharovova K, Berkova Z, Girman P, Dovolilova E, et al. 2008. Differentiation of CD133-positive pancreatic cells into insulin-producing islet-like cell clusters. Transplant Proc 40:415-8. doi: 10.1016/j.transproceed.2008.02.017.
28. Kopp JL, Dubois CL, Schaffer AE, Hao E, Shih HP, Seymour PA, et al. 2011. Sox9+ ductal cells are multipotent progenitors throughout development but do not produce new endocrine cells in the normal or injured adult pancreas. Development 138:653-65. doi: 10.1242/dev.056499.
29. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, Eliazer S, et al. 2008. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26:443-52. doi: 10.1038/nbt1393.
30. Lardon J, Corbeil D, Huttner WB, Ling Z, Bouwens L. 2008. Stem cell marker prominin-1/AC133 is expressed in duct cells of the adult human pancreas. Pancreas 36:e1-6. doi: 10.1097/mpa.0b013e318149f2dc.
31. Lawson DA, Xin L, Lukacs RU, Cheng D, Witte ON. 2007. Isolation and functional characterization of murine prostate stem cells. Proc Natl Acad Sci USA 104:181-6. doi: 10.1073/pnas.0609684104.
32. Lupi R, Del Guerra S, Tellini C, Giannarelli R, Coppelli A, Lorenzetti M, et al. 1999. The biguanide compound metformin prevents desensitization of human pancreatic islets induced by high glucose. Eur J Pharmacol 364:205-9. doi: 10.1016/S0014-2999(98)00807-3.
33. McKnight KD, Wang P, Kim SK. 2010. Deconstructing pancreas development to reconstruct human islets from pluripotent stem cells. Cell Stem Cell 6:300-8. doi: 10.1016/j.stem.2010.03.003.
34. Mellitzer G, Bonne S, Luco RF, Van De Casteele M, Lenne-Samuel N, Collombat P, et al. 2006. IA1 is NGN3- dependent and essential for differentiation of the endocrine pancreas. EMBO J 25:1344-52. doi: 10.1038/ sj.emboj.7601011.
35. Minami K, Okuno M, Miyawaki K, Okumachi A, Ishizaki K, Oyama K, et al. 2005. Lineage tracing and characterization of insulin-secreting cells generated from adult pancreatic acinar cells. Proc Natl Acad Sci USA 102:15116-21. doi: 10.1073/pnas.0507567102.
36. Miyatsuka T, Kosaka Y, Kim H, German MS. 2011. Neurogenin3 inhibits proliferation in endocrine progenitors by inducing Cdkn1a. Proc Natl Acad Sci USA 108:185-90. doi: 10.1073/pnas.1004842108.
37. Miyatsuka T, Li Z, German MS. 2009. Chronology of islet differentiation revealed by temporal cell labeling. Diabetes 58:1863-8. doi: 10.2337/db09-0390.
38. Noguchi H, Xu G, Matsumoto S, Kaneto H, Kobayashi N, Bonner-Weir S, et al. 2006. Induction of pancreatic stem/progenitor cells into insulin-producing cells by adenoviral-mediated gene transfer technology. Cell Transplant 15:929-38. doi: 10.3727/000000006783981431.
39. Nostro MC, Keller G. 2012. Generation of beta cells from human pluripotent stem cells: potential for regenerative medicine. Semin Cell Dev Biol 23:701-10. doi: 10.1016/j.semcdb.2012.06.010.
40. Pan FC, Wright C. 2011. Pancreas organogenesis: from bud to plexus to gland. Dev Dyn 240:530-65. doi: 10.1002/dvdy.22584.
41. Pictet R, Rutter WJ. 1972. Development of the embryonic endocrine pancreas. In: Steiner DF, Freinkel N, editors. Handbook of physiology: a critical, comprehensive presentation of physiological knowledge and concepts. section 7: Endocrinology. American Physiological Society. p. 25-55.
42. Rescan C, Le Bras S, Lefebvre VH, Frandsen U, Klein T, Foschi M, et al. 2005. EGF-induced proliferation of adult human pancreatic duct cells is mediated by the MEK/ERK cascade. Lab Invest 85:65-74. doi: 10.1038/labinvest.3700204.
43. Rovira M, Scott SG, Liss AS, Jensen J, Thayer SP, Leach SD. 2010. Isolation and characterization of centroacinar/ terminal ductal progenitor cells in adult mouse pancreas. Proc Natl Acad Sci USA 107:75-80. doi: 10.1073/ pnas.0912589107.
44. Rozzo A, Meneghel-Rozzo T, Delakorda SL, Yang SB, Rupnik M. 2009. Exocytosis of insulin: in vivo maturation of mouse endocrine pancreas. Ann N Y Acad Sci 1152:53-62. doi: 10.1111/j.1749-6632.2008.04003.x.
45. Sander M, Neubuser A, Kalamaras J, Ee HC, Martin GR, German MS. 1997. Genetic analysis reveals that PAX6 is required for normal transcription of pancreatic hormone genes and islet development. Genes Dev 11:1662-73. doi: 10.1101/gad.11.13.1662.
46. Sapir T, Shternhall K, Meivar-Levy I, Blumenfeld T, Cohen H, Skutelsky E, et al. 2005. Cell-replacement therapy for diabetes: generating functional insulin-producing tissue from adult human liver cells. Proc Natl Acad Sci USA 102:7964-9. doi: 10.1073/pnas.0405277102.
47. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262-5. doi: 10.1038/nature07935.
48. Smith SB, Qu HQ, Taleb N, Kishimoto NY, Scheel DW, Lu Y, et al. 2010. Rfx6 directs islet formation and insulin production in mice and humans. Nature 463:775-80. doi: 10.1038/nature08748.
49. Solar M, Cardalda C, Houbracken I, Martin M, Maestro MA, De Medts N, et al. 2009. Pancreatic exocrine duct cells give rise to insulin-producing beta cells during embryogenesis but not after birth. Dev Cell 17:849-60. doi: 10.1016/j.devcel.2009.11.003.
50. Sosa-Pineda B, Chowdhury K, Torres M, Oliver G, Gruss P. 1997. The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature 386:399-402. doi: 10.1038/386399a0.
51. Suckale J, Solimena M. 2010. The insulin secretory granule as a signaling hub. Trends Endocrinol Metab 21:599-609. doi: 10.1016/j.tem.2010.06.003.
52. Sugiyama T, Rodriguez RT, McLean GW, Kim SK. 2007. Conserved markers of fetal pancreatic epithelium permit prospective isolation of islet progenitor cells by FACS. Proc Natl Acad Sci USA 104:175-80. doi: 10.1073/ pnas.0609490104.
53. Sussel L, Kalamaras J, Hartigan-O'Connor DJ, Meneses JJ, Pedersen RA, Rubenstein JL, et al. 1998. Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 125:2213-21.
54. Swales N, Martens GA, Bonne S, Heremans Y, Borup R, Van de Casteele M, et al. 2012. Plasticity of adult human pancreatic duct cells by neurogenin3-mediated reprogramming. PLOS ONE 7:e37055. doi: 10.1371/journal.pone.0037055.
55. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-72. doi: 10.1016/j.cell.2007.11.019.
56. Tashiro F, Niwa H, Miyazaki J. 1999. Constructing adenoviral vectors by using the circular form of the adenoviral genome cloned in a cosmid and the Cre-loxP recombination system. Hum Gene Ther 10:1845-52. doi: 10.1089/10430349950017527.
57. Thatava T, Nelson TJ, Edukulla R, Sakuma T, Ohmine S, Tonne JM, et al. 2011. Indolactam V/GLP-1-mediated differentiation of human iPS cells into glucose-responsive insulin-secreting progeny. Gene Ther 18:283-93. doi: 10.1038/gt.2010.145.
58. Trautmann B, Schlitt HJ, Hahn EG, Lohr M. 1993. Isolation, culture, and characterization of human pancreatic duct cells. Pancreas 8:248-54. doi: 10.1097/00006676-199303000-00017.
59. Vardanyan M, Parkin E, Gruessner C, Rodriguez Rilo HL. 2010. Pancreas vs. islet transplantation: a call on the future. Curr Opin Organ Transplant 15:124-30. doi: 10.1097/MOT.0b013e32833553f8.
60. Vierbuchen T, Wernig M. 2011. Direct lineage conversions: unnatural but useful? Nat Biotechnol 29:892-907. doi: 10.1038/nbt.1946.
61. Wang P, Rodriguez RT, Wang J, Ghodasara A, Kim SK. 2011. Targeting SOX17 in human embryonic stem cells creates unique strategies for isolating and analyzing developing endoderm. Cell Stem Cell 8:335-46. doi: 10.1016/j.stem.2011.01.017.
62. Wang S, Jensen JN, Seymour PA, Hsu W, Dor Y, Sander M, et al. 2009. Sustained Neurog3 expression in hormone-expressing islet cells is required for endocrine maturation and function. Proc Natl Acad Sci USA 106:9715-20. doi: 10.1073/pnas.0904247106.
63. Wang S, Yan J, Anderson DA, Xu Y, Kanal MC, Cao Z, et al. 2010. Neurog3 gene dosage regulates allocation of endocrine and exocrine cell fates in the developing mouse pancreas. Dev Biol 339:26-37. doi: 10.1016/j.ydbio. 2009.12.009.
64. Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, et al. 2010. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7:618-30. doi: 10.1016/j.stem.2010.08.012.
65. Xu X, D'Hoker J, Stange G, Bonne S, De Leu N, Xiao X, et al. 2008. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132:197-207. doi: 10.1016/j.cell.2007.12.015.
66. Yatoh S, Dodge R, Akashi T, Omer A, Sharma A, Weir GC, et al. 2007. Differentiation of affinity-purified human pancreatic duct cells to beta-cells. Diabetes 56:1802-9. doi: 10.2337/db06-1670.
67. Yoo AS, Sun AX, Li L, Shcheglovitov A, Portmann T, Li Y, et al. 2011. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476:228-31. doi: 10.1038/nature10323.
68. Zhang D, Jiang W, Liu M, Sui X, Yin X, Chen S, et al. 2009. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res 19:429-38. doi: 10.1038/cr.2009.28.
69. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. 2008. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455:627-32. doi: 10.1038/nature07314.
70. Zhou Q, Law AC, Rajagopal J, Anderson WJ, Gray PA, Melton DA. 2007. A multipotent progenitor domain guides pancreatic organogenesis. Dev Cell 13:103-14. doi: 10.1016/j.devcel.2007.06.001.