Reconstituting pancreas development from purified progenitor cells reveals genes essential for islet differentiation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 31, 2013, Pages 12691-12696

  Sugiyama, Takuya ^a   Benitez, Cecil M ^a   Ghodasara, Amar ^a   Liu, Lucy ^a   McLean, Graeme W ^a,b   Lee, Jonghyeob ^a   Blauwkamp, Timothy A ^a   Nusse, Roeland ^a,b   Wright, Christopher V E ^c   Gu, Guoqiang ^c   Kim, Seung K ^a,b  

^a Department of Developmental Biology ^*  (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Endocrine; Exocrine; Insulin; Stem cell; Transcription factor

Indexed keywords

CHROMOGRANIN A; NEUROGENIN 3; TRANSCRIPTION FACTOR PAX4;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; GENETIC SCREENING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET CELL; PRIORITY JOURNAL; STEM CELL;

ENDOCRINE; EXOCRINE; INSULIN; STEM CELL; TRANSCRIPTION FACTOR;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; DIABETES MELLITUS; DNA-BINDING PROTEINS; FEMALE; GLUCAGON-SECRETING CELLS; HOMEODOMAIN PROTEINS; INSULIN-SECRETING CELLS; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PAIRED BOX TRANSCRIPTION FACTORS; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84881093237     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1304507110     Document Type: Article

References (49)

1. Puri S, Hebrok M (2010) Cellular plasticity within the pancreas-lessons learned from development. Dev Cell 18(3):342-356.
2. Gittes GK (2009) Developmental biology of the pancreas: A comprehensive review. Dev Biol 326(1):4-35.
3. Bonnefond A, Froguel P, Vaxillaire M (2010) The emerging genetics of type 2 diabetes. Trends Mol Med 16(9):407-416.
4. Lenoir O, et al. (2011) Specific control of pancreatic endocrine β-and δ-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9. Diabetes 60(11):2861-2871.
5. Mellitzer G, et al. (2006) IA1 is NGN3-dependent and essential for differentiation of the endocrine pancreas. EMBO J 25(6):1344-1352.
6. Prasadan K, et al. (2010) Endocrine-committed progenitor cells retain their differentiation potential in the absence of neurogenin-3 expression. Biochem Biophys Res Commun 396(4):1036-1041.
7. Seymour PA, et al. (2007) SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc Natl Acad Sci USA 104(6):1865-1870.
8. Lynn FC, et al. (2007) Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc Natl Acad Sci USA 104(25):10500-10505.
9. Furuyama K, et al. (2011) Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat Genet 43(1):34-41.
10. Kopp JL, 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(4):653-665.
11. Apelqvist A, et al. (1999) Notch signalling controls pancreatic cell differentiation. Nature 400(6747):877-881.
12. 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(4):1607-1611.
13. Schwitzgebel VM, et al. (2000) Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127(16):3533-3542.
14. Jensen J, et al. (2000) Independent development of pancreatic alpha-and beta-cells from neurogenin3-expressing precursors: A role for the notch pathway in repression of premature differentiation. Diabetes 49(2):163-176.
15. 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(10):2447-2457.
16. Wang J, et al. (2006) Mutant neurogenin-3 in congenital malabsorptive diarrhea. N Engl J Med 355(3):270-280.
17. Jensen JN, Rosenberg LC, Hecksher-Sorensen J, Serup P (2007) Mutant neurogenin-3 in congenital malabsorptive diarrhea. N Engl J Med 356(17):1781-1782.
18. Ashcroft FM, Rorsman P (2012) Diabetes mellitus and the β cell: The last ten years. Cell 148(6):1160-1171.
19. Kordowich S, Mansouri A, Collombat P (2010) Reprogramming into pancreatic endocrine cells based on developmental cues. Mol Cell Endocrinol 323(1):62-69.
20. Seale P, et al. (2008) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454(7207):961-967.
21. Pinheiro I, et al. (2012) Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 150(5):948-960.
22. Seymour PA, et al. (2008) A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev Biol 323(1):19-30.
23. 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(1):181-186.
24. Bhushan A, et al. (2001) Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 128(24):5109-5117.
25. Stanger BZ, Tanaka AJ, Melton DA (2007) Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver. Nature 445(7130): 886-891.
26. Simon MC, Keith B (2008) The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9(4):285-296.
27. Heinis M, et al. (2010) Oxygen tension regulates pancreatic beta-cell differentiation through hypoxia-inducible factor 1alpha. Diabetes 59(3):662-669.
28. Shah SR, et al. (2011) Embryonic mouse blood flow and oxygen correlate with early pancreatic differentiation. Dev Biol 349(2):342-349.
29. Wang S, et al. (2008) Myt1 and Ngn3 form a feed-forward expression loop to promote endocrine islet cell differentiation. Dev Biol 317(2):531-540.
30. Chuikov S, Levi BP, Smith ML, Morrison SJ (2010) Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nat Cell Biol 12(10): 999-1006.
31. Bjork BC, Turbe-Doan A, Prysak M, Herron BJ, Beier DR (2010) Prdm16 is required for normal palatogenesis in mice. Hum Mol Genet 19(5):774-789.
32. Collombat P, et al. (2007) Embryonic endocrine pancreas and mature beta cells acquire alpha and PP cell phenotypes upon Arx misexpression. J Clin Invest 117(4): 961-970.
33. Naujok O, Burns C, Jones PM, Lenzen S (2011) Insulin-producing surrogate β-cells from embryonic stem cells: Are we there yet? Mol Ther 19(10):1759-1768.
34. Zaret KS, Grompe M (2008) Generation and regeneration of cells of the liver and pancreas. Science 322(5907):1490-1494.
35. Oliver-Krasinski JM, Stoffers DA (2008) On the origin of the beta cell. Genes Dev 22(15):1998-2021.
36. Gong S, et al. (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425(6961):917-925.
37. Ventura A, et al. (2007) Restoration of p53 function leads to tumour regression in vivo. Nature 445(7128):661-665.
38. Hara M, et al. (2003) Transgenic mice with green fluorescent protein-labeled pancreatic beta-cells. Am J Physiol Endocrinol Metab 284(1):E177-E183.
39. 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(1):175-180.
40. Atkuri KR, Herzenberg LA, Niemi AK, Cowan T, Herzenberg LA (2007) Importance of culturing primary lymphocytes at physiological oxygen levels. Proc Natl Acad Sci USA 104(11):4547-4552.
41. Gu G, et al. (2004) Global expression analysis of gene regulatory pathways during endocrine pancreatic development. Development 131(1):165-179.
42. Soyer J, et al. (2010) Rfx6 is an Ngn3-dependent winged helix transcription factor required for pancreatic islet cell development. Development 137(2):203-212.
43. White P, May CL, Lamounier RN, Brestelli JE, Kaestner KH (2008) Defining pancreatic endocrine precursors and their descendants. Diabetes 57(3):654-668.
44. Juhl K, Sarkar SA, Wong R, Jensen J, Hutton JC (2008) Mouse pancreatic endocrine cell transcriptome defined in the embryonic Ngn3-null mouse. Diabetes 57(10): 2755-2761.
45. Hoffman BG, et al. (2008) Identification of transcripts with enriched expression in the developing and adult pancreas. Genome Biol 9(6):R99.
46. Sarkar SA, et al. (2012) Synergizing genomic analysis with biological knowledge to identify and validate novel genes in pancreatic development. Pancreas 41(6):962-969.
47. Dorrell C, et al. (2011) Transcriptomes of the major human pancreatic cell types. Diabetologia 54(11):2832-2844.
48. Hoffman BG, Zavaglia B, Beach M, Helgason CD (2008) Expression of Groucho/TLE proteins during pancreas development. BMC Dev Biol 8:81.
49. Pinho AV, Rooman I, Real FX (2011) p53-dependent regulation of growth, epithelialmesenchymal transition and stemness in normal pancreatic epithelial cells. Cell Cycle 10(8):1312-1321.