Regulation of Neurod1 Contributes to the Lineage Potential of Neurogenin3+ Endocrine Precursor Cells in the Pancreas

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Mastracci, Teresa L ^a,c   Anderson, Keith R ^b,d   Papizan, James B ^a   Sussel, Lori ^a,b  

^a Columbia University ^*  (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCAGON; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIN 3; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL LINEAGE; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYO; GENE DELETION; GENE INTERACTION; GENE REPRESSION; IN VITRO STUDY; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REPORTER GENE; STEM CELL;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCAGON-SECRETING CELLS; HOMEODOMAIN PROTEINS; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; PANCREAS; SIGNAL TRANSDUCTION; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84874778569     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003278     Document Type: Article

References (48)

1. 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.
2. 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.
3. Nostro MC, Sarangi F, Ogawa S, Holtzinger A, Corneo B, et al. (2011) Stage-specific signaling through TGFbeta family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 138: 861-871.
4. 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 U S A 97: 1607-1611.
5. 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: 2447-2457.
6. Heller RS, Jenny M, Collombat P, Mansouri A, Tomasetto C, et al. (2005) Genetic determinants of pancreatic epsilon-cell development. Dev Biol 286: 217-224.
7. Desgraz R, Herrera PL, (2009) Pancreatic neurogenin 3-expressing cells are unipotent islet precursors. Development 136: 3567-3574.
8. Collombat P, Hecksher-Sorensen J, Krull J, Berger J, Riedel D, et al. (2007) Embryonic endocrine pancreas and mature beta cells acquire alpha and PP cell phenotypes upon Arx misexpression. J Clin Invest 117: 961-970.
9. Johansson KA, Dursun U, Jordan N, Gu G, Beermann F, et al. (2007) Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev Cell 12: 457-465.
10. Yang YP, Thorel F, Boyer DF, Herrera PL, Wright CV, (2011) Context-specific alpha-to-beta cell reprogramming by forced Pdx1 expression. Genes Dev 25.
11. Jorgensen MC, Ahnfelt-Ronne J, Hald J, Madsen OD, Serup P, et al. (2007) An illustrated review of early pancreas development in the mouse. Endocr Rev 28: 685-705.
12. Sussel L, Kalamaras J, Hartigan-O'Connor DJ, Meneses JJ, Pedersen RA, et al. (1998) Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 125: 2213-2221.
13. Arnes L, Leclerc K, Friel JM, Hipkens SB, Magnuson MA, et al. (2012) Generation of Nkx2.2:lacZ mice using recombination-mediated cassette exchange technology. Genesis.
14. Papizan JB, Singer RA, Tschen SI, Dhawan S, Friel JM, et al. (2011) Nkx2.2 repressor complex regulates islet beta-cell specification and prevents beta-to-alpha-cell reprogramming. Genes Dev 25: 2291-2305.
15. Dasen JS, Tice BC, Brenner-Morton S, Jessell TM, (2005) A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123: 477-491.
16. Kitamura T, Kitamura YI, Funahashi Y, Shawber CJ, Castrillon DH, et al. (2007) A Foxo/Notch pathway controls myogenic differentiation and fiber type specification. J Clin Invest 117: 2477-2485.
17. Li H, de Faria JP, Andrew P, Nitarska J, Richardson WD, (2011) Phosphorylation regulates OLIG2 cofactor choice and the motor neuron-oligodendrocyte fate switch. Neuron 69: 918-929.
18. Meadows SM, Myers CT, Krieg PA, (2011) Regulation of endothelial cell development by ETS transcription factors. Semin Cell Dev Biol 22: 976-984.
19. Collombat P, Mansouri A, Hecksher-Sorensen J, Serup P, Krull J, et al. (2003) Opposing actions of Arx and Pax4 in endocrine pancreas development. Genes Dev 17: 2591-2603.
20. Mellitzer G, Bonne S, Luco RF, Van De Casteele M, Lenne-Samuel N, et al. (2006) IA1 is NGN3-dependent and essential for differentiation of the endocrine pancreas. Embo J 25: 1344-1352.
21. Schaffer AE, Freude KK, Nelson SB, Sander M, (2010) Nkx6 transcription factors and Ptf1a function as antagonistic lineage determinants in multipotent pancreatic progenitors. Dev Cell 18: 1022-1029.
22. Collombat P, Hecksher-Sorensen J, Broccoli V, Krull J, Ponte I, et al. (2005) The simultaneous loss of Arx and Pax4 genes promotes a somatostatin-producing cell fate specification at the expense of the alpha- and beta-cell lineages in the mouse endocrine pancreas. Development 132: 2969-2980.
23. Kordowich S, Collombat P, Mansouri A, Serup P, (2011) Arx and Nkx2.2 compound deficiency redirects pancreatic alpha- and beta-cell differentiation to a somatostatin/ghrelin co-expressing cell lineage. BMC Dev Biol 11: 52.
24. Mastracci TL, Wilcox CL, Panea C, Golden JA, May CL, et al. (2011) Nkx2.2 and Arx genetically interact to regulate pancreatic endocrine cell development and endocrine hormone expression. Dev Biol 359: 1-11.
25. Chao CS, Loomis ZL, Lee JE, Sussel L, (2007) Genetic identification of a novel NeuroD1 function in the early differentiation of islet alpha, PP and epsilon cells. Dev Biol 312: 523-532.
26. Naya FJ, Huang HP, Qiu Y, Mutoh H, DeMayo FJ, et al. (1997) Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev 11: 2323-2334.
27. Prado CL, Pugh-Bernard AE, Elghazi L, Sosa-Pineda B, Sussel L, (2004) Ghrelin cells replace insulin-producing beta cells in two mouse models of pancreas development. Proc Natl Acad Sci U S A 101: 2924-2929.
28. Anderson KR, Torres CA, Solomon K, Becker TC, Newgard CB, et al. (2009) Cooperative transcriptional regulation of the essential pancreatic islet gene NeuroD1 (beta2) by Nkx2.2 and neurogenin 3. J Biol Chem 284: 31236-31248.
29. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, et al. (2003) Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4: 437-450.
30. Gu C, Stein GH, Pan N, Goebbels S, Hornberg H, et al. (2011) Pancreatic beta cells require NeuroD to achieve and maintain functional maturity. Cell Metab 11: 298-310.
31. Schonhoff SE, Giel-Moloney M, Leiter AB, (2004) Neurogenin 3-expressing progenitor cells in the gastrointestinal tract differentiate into both endocrine and non-endocrine cell types. Dev Biol 270: 443-454.
32. Herrera PL, (2000) Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127: 2317-2322.
33. Gasa R, Mrejen C, Lynn FC, Skewes-Cox P, Sanchez L, et al. (2008) Induction of pancreatic islet cell differentiation by the neurogenin-neuroD cascade. Differentiation 76: 381-391.
34. Huang HP, Liu M, El-Hodiri HM, Chu K, Jamrich M, et al. (2000) Regulation of the pancreatic islet-specific gene BETA2 (neuroD) by neurogenin 3. Mol Cell Biol 20: 3292-3307.
35. Miyata T, Maeda T, Lee JE, (1999) NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev 13: 1647-1652.
36. Pictet R, Rutter WJ (1972) Development of the embryonic endocrine pancreas; Steiner DF, Frenkel N, editors. Washington, DC: Williams and Wilkins. 25-66 p.
37. Seymour PA, Freude KK, Dubois CL, Shih HP, Patel NA, et al. (2008) A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev Biol 323: 19-30.
38. Pan FC, Wright C, (2011) Pancreas organogenesis: from bud to plexus to gland. Dev Dyn 240: 530-565.
39. Thorel F, Nepote V, Avril I, Kohno K, Desgraz R, et al. (2010) Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 464: 1149-1154.
40. Mastracci TL, Sussel L, (2012) The Endocrine Pancreas: insights into development, differentiation and diabetes. WIREs Dev Biol doi:10.1002/wdev.44.
41. Wang S, Hecksher-Sorensen J, Xu Y, Zhao A, Dor Y, et al. (2008) Myt1 and Ngn3 form a feed-forward expression loop to promote endocrine islet cell differentiation. Dev Biol 317: 531-540.
42. Goebbels S, Bode U, Pieper A, Funfschilling U, Schwab MH, et al. (2005) Cre/loxP-mediated inactivation of the bHLH transcription factor gene NeuroD/BETA2. Genesis 42: 247-252.
43. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140.
44. Soriano P, (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
45. Larsson LI, Madsen OD, Serup P, Jonsson J, Edlund H, (1996) Pancreatic-duodenal homeobox 1-role in gastric endocrine patterning. Mech Dev 60: 175-184.
46. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, et al. (1996) PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122: 983-995.
47. Xuan S, Borok MJ, Decker KJ, Battle MA, Duncan SA, et al. (2012) Pancreas-specific deletion of mouse Gata4 and Gata6 causes pancreatic agenesis. J Clin Invest 122: 3516-3528.
48. Tuteja G, Jensen ST, White P, Kaestner KH, (2008) Cis-regulatory modules in the mammalian liver: composition depends on strength of Foxa2 consensus site. Nucleic Acids Res 36: 4149-4157.