Presenilins, Notch dose control the fate of pancreatic endocrine progenitors during a narrow developmental window

Genes and Development

Volumn 23, Issue 17, 2009, Pages 2088-2101

  Cras Méneur, Corentin ^a,b   Li, Lin ^a   Kopan, Raphael ^a   Permutt, M Alan ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Cell fate; Endocrine progenitor; Lineage tracing; Notch; Pancreatic development; Presenilins

Indexed keywords

GAMMA SECRETASE; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NEUROGENIN 3; NOTCH1 RECEPTOR; PRESENILIN 1; PRESENILIN 2; TRANSCRIPTION FACTOR PAX6;

ACINAR CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; GENE DELETION; MOUSE; NONHUMAN; PANCREAS CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYONIC DEVELOPMENT; ENDOCRINE CELLS; ISLETS OF LANGERHANS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; ORGAN SIZE; PRESENILINS; RECEPTORS, NOTCH; STEM CELLS;

EID: 69749084211     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1800209     Document Type: Article

References (69)

1. Apelqvist Å, Li H, Sommer L, Beatus P, Anderson DJ, Honjo T, Hrabe de Angelis M, Lendahl U, Edlund H. 1999. Notch signalling controls pancreatic cell differentiation. Nature 400: 877-881. (Pubitemid 29406724)
2. Baki L, Shioi J, Wen P, Shao Z, Schwarzman A, Gama-Sosa M, Neve R, Robakis NK. 2004. PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: Effects of FAD mutations. EMBO J 23: 2586-2596. (Pubitemid 38988230)
3. Beres TM, Masui T, Swift GH, Shi L, Henke RM, Macdonald RJ. 2006. PTF1 is an organ-specific and Notch-independent basic helix-loop-helix complex containing the mammalian suppressor of hairless (RBP-J) or its paralogue, RBP-L. Mol Cell Biol 26: 117-130.
4. Bernal-Mizrachi E, Wen W, Stahlhut S, Welling CM, Permutt MA. 2001. Islet β cell expression of constitutively active Akt1/PKB α induces striking hypertrophy, hyperplasia, and hyperinsulinemia. J Clin Invest 108: 1631-1638. (Pubitemid 33144873)
5. Cheng HT, Miner JH, Lin M, Tansey MG, Roth K, Kopan R. 2003. γ-Secretase activity is dispensable for mesenchyme-toepithelium transition but required for podocyte and proximal tubule formation in developing mouse kidney. Development 130: 5031-5042. (Pubitemid 37321884)
6. Chiang MK, Melton DA. 2003. Single-cell transcript analysis of pancreas development. Dev Cell 4: 383-393.
7. Cras-Méneur C, Elghazi L, Czernichow P, Scharfmann R. 2001. Epidermal growth factor increases undifferentiated pancreatic embryonic cells in vitro: A balance between proliferation and differentiation. Diabetes 50: 1571-1579. (Pubitemid 33639597)
8. de la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Rossant J, et al. 1997. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124: 1139-1148. (Pubitemid 27142068)
9. Doerfler P, Shearman MS, Perlmutter RM. 2001. Presenilin-dependent γ-secretase activity modulates thymocyte development. Proc Natl Acad Sci 98: 9312-9317. (Pubitemid 32743913)
10. Donoviel DB, Hadjantonakis AK, Ikeda M, Zheng H, Hyslop PS, Bernstein A. 1999. Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes & Dev 13: 2801-2810.
11. Esni F, Ghosh B, Biankin AV, Lin JW, Albert MA, Yu X, MacDonald RJ, Civin CI, Real FX, Pack MA, et al. 2004. Notch inhibits Ptf1 function and acinar cell differentiation in developing mouse and zebrafish pancreas. Development 131: 4213-4422 (Pubitemid 39276191)
12. Fujikura J, Hosoda K, Kawaguchi Y, Noguchi M, Iwakura H, Odori S, Mori E, Tomita T, Hirata M, Ebihara K, et al. 2007. Rbp-j regulates expansion of pancreatic epithelial cells and their differentiation into exocrine cells during mouse development. Dev Dyn 236: 2779-2791. (Pubitemid 47613240)
13. Fujitani Y, Fujitani S, Luo H, Qiu F, Burlison J, Long Q, Kawaguchi Y, Edlund H, MacDonald RJ, Furukawa T, et al. 2006. Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development 133: 4439-4450. (Pubitemid 46017819)
14. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C. 2002. A γ-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 3: 688-694. (Pubitemid 34884995)
15. Girish V, Vijayalakshmi A. 2004. Affordable image analysis using NIH Image/ImageJ. Indian J Cancer 41: 47. (Pubitemid 38623932)
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 97: 1607-1611. (Pubitemid 30118489)
17. + cells are islet progenitors and are distinct from duct progenitors. Development 129: 2447-2457.
18. Gu G, Brown JR, Melton DA. 2003. Direct lineage tracing reveals the ontogeny of pancreatic cell fates during mouse embryogenesis. Mech Dev 120: 35-43. (Pubitemid 35462094)
19. Hadland BK, Manley NR, Su D, Longmore GD, Moore CL,Wolfe MS, Schroeter EH, Kopan R. 2001. γ-Secretase inhibitors repress thymocyte development. Proc Natl Acad Sci 98: 7487-7491. (Pubitemid 32567975)
20. Hald J, Hjorth JP, German MS, Madsen OD, Serup P, Jensen J. 2003. Activated Notch1 prevents differentiation of pancreatic acinar cells and attenuate endocrine development. Dev Biol 260: 426-437. (Pubitemid 36966084)
21. Hartmann D, de Strooper B, Serneels L, Craessaerts K, Herreman A, AnnaertW, Umans L, Lubke T, Lena Illert A, von Figura K, et al. 2002. The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for α-secretase activity in fibroblasts. Hum Mol Genet 11: 2615-2624. (Pubitemid 35174691)
22. Herreman A, Hartmann D, Annaert W, Saftig P, Craessaerts K, Serneels L, Umans L, Schrijvers V, Checler F, Vanderstichele H, et al. 1999. Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 deficiency. Proc Natl Acad Sci 96: 11872-11877. (Pubitemid 29502825)
23. Hori K, Cholewa-Waclaw J, Nakada Y, Glasgow SM, Masui T, Henke RM, Wildner H, Martarelli B, Beres TM, Epstein JA, et al. 2008. A nonclassical bHLH Rbpj transcription factor complex is required for specification of GABAergic neurons independent of Notch signaling. Genes & Dev 22: 166-178.
24. Huotari MA, Miettinen PJ, Palgi J, Koivisto T, Ustinov J, Harari D, Yarden Y, Otonkoski T. 2002. ErbB signaling regulates lineage determination of developing pancreatic islet cells in embryonic organ culture. Endocrinology 143: 4437-4446. (Pubitemid 35239578)
25. Jensen J, Heller RS, Funder-Nielsen T, Pedersen EE, Lindsell C, Weinmaster G, Madsen OD, Serup P. 2000. Independent development of pancreatic α- and β-cells from neurogenin3- expressing precursors: A role for the notch pathway in repression of premature differentiation. Diabetes 49: 163-176. (Pubitemid 30070993)
26. Jørgensen MC, Ahnfelt-Ronne J, Hald J, Madsen OD, Serup P, Hecksher-Sorensen J. 2007. An illustrated review of early pancreas development in the mouse. Endocr Rev 28: 685-705. (Pubitemid 47606652)
27. Kageyama R, Masamizu Y, Niwa Y. 2007. Oscillator mechanism of Notch pathway in the segmentation clock. Dev Dyn 236: 1403-1409. (Pubitemid 46932346)
28. Kang DE, Soriano S, Frosch MP, Collins T, Naruse S, Sisodia SS, Leibowitz G, Levine F, Koo EH. 1999. Presenilin 1 facilitates the constitutive turnover of β-catenin: Differential activity of Alzheimer's disease-linked PS1 mutants in the β-catenin-signaling pathway. J Neurosci 19: 4229-4237. (Pubitemid 29241077)
29. Kim MY, Park JH, Choi EJ, Park HS. 2005. Presenilin acts as a positive regulator of basal level activity of ERK through the Raf-MEK1 signaling pathway. Biochem Biophys Res Commun 332: 609-613.
30. Koo EH, Kopan R. 2004. Potential role of presenilin-regulated signaling pathways in sporadic neurodegeneration. Nat Med 10: S26-S33. doi: 10.1038/nm1065. (Pubitemid 38901864)
31. Kopan R, Ilagan MX. 2004. γ-Secretase: Proteasome of the membrane? Nat Rev Mol Cell Biol 5: 499-504.
32. Kopan R, Ilagan MX. 2009. The canonical notch signaling pathway: Unfolding the activation mechanism. Cell 137: 216-233.
33. Kritzik MR, Krahl T, Good A, Gu D, Lai C, Fox H, Sarvetnick N. 2000. Expression of ErbB receptors during pancreatic islet development and regrowth. J Endocrinol 165: 67-77. (Pubitemid 30210567)
34. Lanz TA, Fici GJ, Merchant KM. 2005. Lack of specific amyloid-β(1-42) suppression by nonsteroidal anti-inflammatory drugs in young, plaque-free tg2576 mice and in guinea pig neuronal cultures. J Pharmacol Exp Ther 312: 399-406.
35. Lee JC, Smith SB, Watada H, Lin J, Scheel D, Wang J, Mirmira RG, German MS. 2001. Regulation of the pancreatic proendocrine gene neurogenin3. Diabetes 50: 928-936. (Pubitemid 32374521)
36. Lee CS, De Leon DD, Kaestner KH, Stoffers DA. 2006. Regeneration of pancreatic islets after partial pancreatectomy in mice does not involve the reactivation of neurogenin-3. Diabetes 55: 269-272.
37. Li T, Wen H, Brayton C, Laird FM, Ma G, Peng S, Placanica L, Wu TC, Crain BJ, Price DL, et al. 2007. Moderate reduction of γ-secretase attenuates amyloid burden and limits mechanism-based liabilities. J Neurosci 27: 10849-10859. (Pubitemid 47535873)
38. Lubman OY, Ilagan MX, Kopan R, Barrick D. 2007. Quantitative dissection of the Notch:CSL interaction: Insights into the Notch-mediated transcriptional switch. J Mol Biol 365: 577-589. (Pubitemid 44960348)
39. Lyu J, Yamamoto V, Lu W. 2008. Cleavage of the Wnt receptor Ryk regulates neuronal differentiation during cortical neurogenesis. Dev Cell 15: 773-780.
40. Masui T, Long Q, Beres TM, Magnuson MA, Macdonald RJ. 2007. Early pancreatic development requires the vertebrate Suppressor of Hairless (RBPJ) in the PTF1 bHLH complex. Genes & Dev 21: 2629-2643. (Pubitemid 47607672)
41. Micchelli CA, The I, Selva E, Mogila V, Perrimon N. 2002. Rasp, a putative transmembrane acyltransferase, is required for Hedgehog signaling. Development 129: 843-851.
42. Miralles F, Czernichow P, Ozaki K, Itoh N, Scharfmann R. 1999a. Signaling through fibroblast growth factor receptor 2b plays a key role in the development of the exocrine pancreas. Proc Natl Acad Sci 96: 6267-6272. (Pubitemid 29256654)
43. Miralles F, Serup P, Cluzeaud F, Vandewalle A, Czernichow P, Scharfmann R. 1999b. Characterization of β cells developed in vitro from rat embryonic pancreatic epithelium. Dev Dyn 214: 116-126. (Pubitemid 29070048)
44. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA. 2003. Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci 100: 14920-14925.
45. Nakhai H, Siveke JT, Klein B, Mendoza-Torres L, Mazur PK, Algul H, Radtke F, Strobl L, Zimber-Strobl U, Schmid RM. 2008. Conditional ablation of Notch signaling in pancreatic development. Development 135: 2757-2765.
46. Novak A, Guo C, Yang W, Nagy A, Lobe CG. 2000. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28: 147-155. (Pubitemid 32110525)
47. Obata J, Yano M, Mimura H, Goto T, Nakayama R, Mibu Y, Oka C, Kawaichi M. 2001. p48 subunit of mouse PTF1 binds to RBP-Jk/CBF-1, the intracellular mediator of Notch signalling, and is expressed in the neural tube of early stage embryos. Genes Cells 6: 345-360. (Pubitemid 32401280)
48. Pan Y, Lin MH, Tian X, Cheng HT, Gridley T, Shen J, Kopan R. 2004. γ-Secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev Cell 7: 731-743. (Pubitemid 39462693)
49. Pan Y, Liu Z, Shen J, Kopan R. 2005. Notch1 and 2 cooperate in limb ectoderm to receive an early Jagged2 signal regulating interdigital apoptosis. Dev Biol 285: 472-482. (Pubitemid 41443286)
50. Parks AL, Curtis D. 2007. Presenilin diversifies its portfolio. Trends Genet 23: 140-150.
51. Petersen PH, Tang H, Zou K, Zhong W. 2006. The enigma of the numb-Notch relationship during mammalian embryogenesis. Dev Neurosci 28: 156-168. (Pubitemid 43320059)
52. Pictet R, Rutter W. 1972. Development of the embryonic pancreas. In Handbook of physiology (eds. DF Steiner, N Frenkel), pp. 25-66. The Williams & Wilkins Co., Washington, DC.
53. Pigino G, Morfini G, Pelsman A, Mattson MP, Brady ST, Busciglio J. 2003. Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J Neurosci 23: 4499-4508. (Pubitemid 36706180)
54. Qyang Y, Chambers SM, Wang P, Xia X, Chen X, Goodell MA, Zheng H. 2004. Myeloproliferative disease in mice with reduced presenilin gene dosage: Effect of γ-secretase blockage. Biochemistry 43: 5352-5359. (Pubitemid 38620927)
55. Saura CA, Choi SY, Beglopoulos V, Malkani S, Zhang D, Shankaranarayana Rao BS, Chattarji S, Kelleher RJ III, Kandel ER, Duff K, et al. 2004. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42: 23-36. (Pubitemid 38456965)
56. 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. (Pubitemid 38748564)
57. Schuster-Gossler K, Cordes R, Gossler A. 2007. Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc Natl Acad Sci 104: 537-542. (Pubitemid 46123060)
58. Sisodia SS, St George-Hyslop PH. 2002. γ-Secretase, Notch, Aβ and Alzheimer's disease: Where do the presenilins fit in? Nat Rev Neurosci 3: 281-290.
59. St-Onge L, Sosa-Pineda B, Chowdhury K, Mansouri A, Gruss P. 1997. Pax6 is required for differentiation of glucagon-producing α-cells in mouse pancreas. Nature 387: 406-409. (Pubitemid 27227205)
60. Struhl G, Greenwald I. 2001. Presenilin-mediated transmembrane cleavage is required for Notch signal transduction in Drosophila. Proc Natl Acad Sci 98: 229-234. (Pubitemid 32095892)
61. Tournoy J, Bossuyt X, Snellinx A, Regent M, Garmyn M, Serneels L, Saftig P, Craessaerts K, De Strooper B, Hartmann D. 2004. Partial loss of presenilins causes seborrheic keratosis and autoimmune disease in mice. Hum Mol Genet 13: 1321-1331. (Pubitemid 38961640)
62. van den Brandt J, Voss K, Schott M, Hunig T, Wolfe MS, Reichardt HM. 2004. Inhibition of Notch signaling biases rat thymocyte development towards the NK cell lineage. Eur J Immunol 34: 1405-1413. (Pubitemid 39256020)
63. Vooijs M, Ong CT, Hadland B, Huppert S, Liu Z, Korving J, van den Born M, Stappenbeck T, Wu Y, Clevers H, et al. 2007. Mapping the consequence of Notch1 proteolysis in vivo with NIP-CRE. Development 134: 535-544. (Pubitemid 46332490)
64. Weihofen A, Lemberg MK, Friedmann E, Rueeger H, Schmitz A, Paganetti P, Rovelli G, Martoglio B. 2003. Targeting presenilin-type aspartic protease signal peptide peptidase with γ-secretase inhibitors. J Biol Chem 278: 16528-16533. (Pubitemid 36799513)
65. Wines-Samuelson M, Shen J. 2005. Presenilins in the developing, adult, and aging cerebral cortex. Neuroscientist 11: 441-451. (Pubitemid 41339229)
66. Wood DR, Nye JS, Lamb NJ, Fernandez A, Kitzmann M. 2005. Intracellular retention of caveolin 1 in presenilin-deficient cells. J Biol Chem 280: 6663-6668. (Pubitemid 40341219)
67. Xu X, D'Hoker J, Stangé G, Bonne S, De Leu N, Xiao X, Van De Casteele M, Mellitzer G, Ling Z, Pipeleers DG, et al. 2008. β Cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132: 197-207. (Pubitemid 351181232)
68. Zeggini E, Scott LR, Saxena R, Voight BF, Marchini JL, Hu T, de Bakker PI, Abecasis GR, Almgren P, Andersen G, et al. 2008. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 40: 638-645. (Pubitemid 351601209)
69. Zhang YW, Wang R, Liu Q, Zhang H, Liao FF, Xu H. 2007. Presenilin/γ-secretase-dependent processing of β-amyloid precursor protein regulates EGF receptor expression. Proc Natl Acad Sci 104: 10613-10618. (Pubitemid 47185713)