Complex cellular and subcellular regulation of notch expression during embryonic and imaginal development of Drosophila: implications for notch function

doi:10.1083/jcb.113.3.657

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Complex cellular and subcellular regulation of notch expression during embryonic and imaginal development of Drosophila: implications for notch function

RG Fehon, K Johansen, I Rebay and S Artavanis-Tsakonas
Department of Cell Biology, Howard Hughes Medical Institute, Yale University, New Haven, Connecticut 06511.

The Notch gene in Drosophila encodes a transmembrane protein with homology to EGF that appears to mediate cell-cell interactions necessary for proper epidermal vs. neural fate decisions. In this study, we examine Notch expression in detail throughout embryonic and imaginal development using confocal laser-scanning microscopy and specific mAb probes. We find that Notch is expressed in a tissue- specific manner as early as the cellular blastoderm stage, when cells of the presumptive mesoderm clearly express less Notch than adjacent ectodermal precursors. Notch is abundantly expressed during the initial determination of neuronal lineages, such as the embryonic neuroblasts and the precursors of sensory neurons in the imaginal disc epithelia, but expression quickly decreases during subsequent differentiation. These changing patterns of Notch expression do not correlate well with cell movements, and thus do not appear to support the notion that the major function of Notch is to maintain epithelial integrity via adhesive mechanisms. Our data suggest instead that Notch may act as a cell-surface receptor, perhaps functioning in the lateral inhibition mechanism that is necessary for proper spacing of neuronal precursors.
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Kong, Y., Glickman, J., Subramaniam, M., Shahsafaei, A., Allamneni, K. P., Aster, J. C., Sklar, J., Sunday, M. E. (2004). Functional diversity of notch family genes in fetal lung development. Am. J. Physiol. Lung Cell. Mol. Physiol. 286: L1075-L1083 [Abstract] [Full Text]
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Wesley, C. S., Mok, L.-P. (2003). Regulation of Notch Signaling by a Novel Mechanism Involving Suppressor of Hairless Stability and Carboxyl Terminus-Truncated Notch. Mol. Cell. Biol. 23: 5581-5593 [Abstract] [Full Text]
Li, Y., Fetchko, M., Lai, Z.-C., Baker, N. E. (2003). Scabrous and Gp150 are endosomal proteins that regulate Notch activity. Development 130: 2819-2827 [Abstract] [Full Text]
Li, Y., Li, L., Irvine, K. D., Baker, N. E. (2003). Notch activity in neural cells triggered by a mutant allele with altered glycosylation. Development 130: 2829-2840 [Abstract] [Full Text]
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St. Johnston, H. L.-S. a. D. (2001). Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev. 15: 1393-1405 [Abstract] [Full Text]
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de Celis, J., Bray, S. (2000). The Abruptex domain of Notch regulates negative interactions between Notch, its ligands and Fringe. Development 127: 1291-1302 [Abstract]
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Sherwood, D., McClay, D. (1999). LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126: 1703-1713 [Abstract]
Fostier, M., Evans, D. A. P., Artavanis-Tsakonas, S., Baron, M. (1998). Genetic Characterization of the Drosophila melanogaster Suppressor of deltex Gene: A Regulator of Notch Signaling. Genetics 150: 1477-1485 [Abstract] [Full Text]
Lamb, R. S., Ward, R. E., Schweizer, L., Fehon, R. G. (1998). Drosophila coracle, a Member of the Protein 4.1�Superfamily, Has Essential Structural Functions in the Septate Junctions and Developmental Functions in Embryonic and Adult Epithelial Cells. Mol. Biol. Cell 9: 3505-3519 [Abstract] [Full Text]
Greenwald, I. (1998). LIN-12/Notch signaling: lessons from worms and�flies. Genes Dev. 12: 1751-1762 [Full Text]
Ward, R. E. IV, Lamb, R. S., Fehon, R. G. (1998). A Conserved Functional Domain of Drosophila Coracle Is Required for Localization at the Septate Junction and Has Membrane-organizing Activity. JCB 140: 1463-1473 [Abstract] [Full Text]
de Celis, J., Tyler, D., de Celis, J, Bray, S. (1998). Notch signalling mediates segmentation of the Drosophila leg. Development 125: 4617-4626 [Abstract]
Levitan, D, Greenwald, I (1998). LIN-12 protein expression and localization during vulval development in C. elegans. Development 125: 3101-3109 [Abstract]
Go, M., Eastman, D., Artavanis-Tsakonas, S (1998). Cell proliferation control by Notch signaling in Drosophila development. Development 125: 2031-2040 [Abstract]
Hough, C. D., Woods, D. F., Park, S., Bryant, P. J. (1997). Organizing a functional junctional complex requires specific domains of the Drosophila MAGUK Discs�large. Genes Dev. 11: 3242-3253 [Abstract] [Full Text]
Majumdar, A, Nagaraj, R, Banerjee, U (1997). strawberry notch encodes a conserved nuclear protein that functions downstream of Notch and regulates gene expression along the developing wing margin of Drosophila.. Genes Dev. 11: 1341-1353 [Abstract]
Frankel, S, Sigel, E., Craig, C, Elgin, S., Mooseker, M., Artavanis-Tsakonas, S (1997). An actin-related protein in Drosophila colocalizes with heterochromatin protein 1 in pericentric heterochromatin. J. Cell Sci. 110: 1999-2012 [Abstract]
de Celis, J., Bray, S (1997). Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124: 3241-3251 [Abstract]
Huppert, S., Jacobsen, T., Muskavitch, M. (1997). Feedback regulation is central to Delta-Notch signalling required for Drosophila wing vein morphogenesis. Development 124: 3283-3291 [Abstract]
Sherwood, D., McClay, D. (1997). Identification and localization of a sea urchin Notch homologue: insights into vegetal plate regionalization and Notch receptor regulation. Development 124: 3363-3374 [Abstract]
Sun, X, Artavanis-Tsakonas, S (1997). Secreted forms of DELTA and SERRATE define antagonists of Notch signaling in Drosophila. Development 124: 3439-3448 [Abstract]
Fleming, R., Gu, Y, Hukriede, N. (1997). Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc. Development 124: 2973-2981 [Abstract]
de Celis, J., Bray, S, Garcia-Bellido, A (1997). Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development 124: 1919-1928 [Abstract]
Seugnet, L, Simpson, P, Haenlin, M (1997). Transcriptional regulation of Notch and Delta: requirement for neuroblast segregation in Drosophila. Development 124: 2015-2025 [Abstract]
Micchelli, C., Rulifson, E., Blair, S. (1997). The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124: 1485-1495 [Abstract]
de Celis, J. (1997). Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing. Development 124: 1007-1018 [Abstract]
He, Z.-H., Fujiki, M., Kohorn, B. D. (1996). A Cell Wall-associated, Receptor-like Protein Kinase. J. Biol. Chem. 271: 19789-19793 [Abstract] [Full Text]
Sun, X, Artavanis-Tsakonas, S (1996). The intracellular deletions of Delta and Serrate define dominant negative forms of the Drosophila Notch ligands. Development 122: 2465-2474 [Abstract]
Gho, M, Lecourtois, M, Geraud, G, Posakony, J., Schweisguth, F (1996). Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during Notch signalling. Development 122: 1673-1682 [Abstract]
Reiter, C, Schimansky, T, Nie, Z, Fischbach, K. (1996). Reorganization of membrane contacts prior to apoptosis in the Drosophila retina: the role of the IrreC-rst protein. Development 122: 1931-1940 [Abstract]
Hoskins, R, Hajnal, A., Harp, S., Kim, S. (1996). The C. elegans vulval induction gene lin-2 encodes a member of the MAGUK family of cell junction proteins. Development 122: 97-111 [Abstract]
Artavanis-Tsakonas, S, Matsuno, K, Fortini, M. (1995). Notch signaling. Science 268: 225-232 [Abstract]
Miyamoto, H, Nihonmatsu, I, Kondo, S, Ueda, R, Togashi, S, Hirata, K, Ikegami, Y, Yamamoto, D (1995). canoe encodes a novel protein containing a GLGF/DHR motif and functions with Notch and scabrous in common developmental pathways in Drosophila.. Genes Dev. 9: 612-625 [Abstract]
Rulifson, E., Blair, S. (1995). Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development 121: 2813-2824 [Abstract]
Gu, Y, Hukriede, N., Fleming, R. (1995). Serrate expression can functionally replace Delta activity during neuroblast segregation in the Drosophila embryo. Development 121: 855-865 [Abstract]
Kopan, R., Nye, J. S., Weintraub, H. (1994). The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development 120: 2385-2396 [Abstract]
Fristrom, D., Gotwals, P., Eaton, S., Kornberg, T. B., Sturtevant, M., Bier, E., Fristrom, J. W. (1994). Blistered: a gene required for vein/intervein formation in wings of Drosophila. Development 120: 2661-2671 [Abstract]
Singson, A, Leviten, M W, Bang, A G, Hua, X H, Posakony, J W (1994). Direct downstream targets of proneural activators in the imaginal disc include genes involved in lateral inhibitory signaling.. Genes Dev. 8: 2058-2071 [Abstract]
Crittenden, S., Troemel, E., Evans, T., Kimble, J (1994). GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120: 2901-2911 [Abstract]
Diederich, R., Matsuno, K, Hing, H, Artavanis-Tsakonas, S (1994). Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signaling pathway. Development 120: 473-481 [Abstract]
Fehon, R., Dawson, I., Artavanis-Tsakonas, S (1994). A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120: 545-557 [Abstract]
Lieber, T, Kidd, S, Alcamo, E, Corbin, V, Young, M W (1993). Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei.. Genes Dev. 7: 1949-1965 [Abstract]
Heitzler, P, Simpson, P (1993). Altered epidermal growth factor-like sequences provide evidence for a role of Notch as a receptor in cell fate decisions. Development 117: 1113-1123 [Abstract]
Giniger, E, Jan, L., Jan, Y. (1993). Specifying the path of the intersegmental nerve of the Drosophila embryo: a role for Delta and Notch. Development 117: 431-440 [Abstract]
Kooh, P., Fehon, R., Muskavitch, M. (1993). Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117: 493-507 [Abstract]
Weinmaster, G., Roberts, V. J., Lemke, G. (1992). Notch2: a second mammalian Notch gene. Development 116: 931-941 [Abstract]
Hartenstein, A. Y., Rugendorff, A., Tepass, U., Hartenstein, V. (1992). The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116: 1203-1220 [Abstract]
Xu, T, Caron, L., Fehon, R., Artavanis-Tsakonas, S (1992). The involvement of the Notch locus in Drosophila oogenesis. Development 115: 913-922 [Abstract]
Del Amo, F., Smith, D., Swiatek, P., Gendron-Maguire, M, Greenspan, R., McMahon, A., Gridley, T (1992). Expression pattern of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 115: 737-744 [Abstract]
Simpson, P., Bourouis, M., Heitzler, P., Ruel, L., Haenlin, M., Ramain, P. (1992). Delta, Notch, and shaggy: Elements of a Lateral Signaling Pathway in Drosophila. Cold Spring Harb Symp Quant Biol 57: 391-400 [Abstract]