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Notch activates Wnt-4 signalling to control medio-lateral patterning of the pronephros

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Naylor, Richard William, 1983- and Jones, E. A. (Elizabeth A.). (2009) Notch activates Wnt-4 signalling to control medio-lateral patterning of the pronephros. Development , Vol.136 (No.21). pp. 3585-3595. ISSN 0950-1991

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Official URL: http://dx.doi.org/10.1242/dev.042606

Abstract

Previous studies have highlighted a role for the Notch signalling pathway during pronephrogenesis in the amphibian Xenopus laevis, and in nephron development in the mammalian metanephros, yet a mechanism for this function remains elusive. Here, we further the understanding of how Notch signalling patterns the early X. laevis pronephros anlagen, a function that might be conserved in mammalian nephron segmentation. Our results indicate that early phase pronephric Notch signalling patterns the medio-lateral axis of the dorso-anterior pronephros anlagen, permitting the glomus and tubules to develop in isolation. We show that this novel function acts through the Notch effector gene hrt1 by upregulating expression of wnt4. Wnt-4 then patterns the proximal pronephric anlagen to establish the specific compartments that span the medio-lateral axis. We also identified pronephric expression of lunatic fringe and radical fringe that is temporally and spatially appropriate for a role in regulating Notch signalling in the dorso-anterior region of the pronephros anlagen. On the basis of these results, along with data from previous publications, we propose a mechanism by which the Notch signalling pathway regulates a Wnt-4 function that patterns the proximal pronephric anlagen.

Item Type:	Journal Article
Subjects:	Q Science > QH Natural history > QH426 Genetics
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Notch genes -- Research, Xenopus laevis, Gene expression -- Research, Cellular signal transduction
Journal or Publication Title:	Development
Publisher:	The Company of Biologists Ltd.
ISSN:	0950-1991
Date:	1 November 2009
Volume:	Vol.136
Number:	No.21
Page Range:	pp. 3585-3595
Identification Number:	10.1242/dev.042606
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC)
Grant number:	G1988 (BBSRC), G12713 (BBSRC)
References:	Ascano, J. M., Beverly, L. J. and Capobianco, A. J. (2003). The C-terminal PDZligand of JAGGED1 is essential for cellular transformation. J. Biol. Chem. 278, 8771-8779. Barisoni, L. (2008). Notch signaling: a common pathway of injury in podocytopathies? J. Am. Soc. Nephrol. 19, 1045-1046. Brändli, A. W. (1999). Towards a molecular anatomy of the Xenopus pronephric kidney. Int. J. Dev. Biol. 43, 381-395. Bray, S. J. (2006). Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689. Brennan, K. and Gardner, P. (2002). Notching up another pathway. BioEssays 24, 405-410. Brou, C., Logeat, F., Gupta, N., Bessia, C., LeBail, O., Doedens, J. R., Cumano, A., Roux, P., Black, R. A. and Israel, A. (2000). A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Mol. Cell 5, 207-216. Bruckner, K., Perez, L., Clausen, H. and Cohen, S. (2000). Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 406, 411-415. Bush, G., diSibio, G., Miyamoto, A., Denault, J. B., Leduc, R. and Weinmaster, G. (2001). Ligand-induced signaling in the absence of furin processing of Notch1. Dev. Biol. 229, 494-502. Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D. and Kintner, C. (1995). Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761-766. Dale, L. and Slack, J. M. (1987). Fate map for the 32-cell stage of Xenopus laevis. Development 99, 527-551. Dressler, G. R. (2006). The cellular basis of kidney development. Annu. Rev. Cell Dev. Biol. 22, 509-529. Dressler, G. R. (2008). Another niche for Notch. Kidney Int. 73, 1207-1209. Fiuza, U. M. and Arias, A. M. (2007). Cell and molecular biology of Notch. J. Endocrinol. 194, 459-474. Haines, N. and Irvine, K. D. (2003). Glycosylation regulates Notch signalling. Nat. Rev. Mol. Cell Biol. 4, 786-797. Harland, R. M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. Hayward, P., Kalmar, T. and Arias, A. M. (2008). Wnt/Notch signalling and information processing during development. Development 135, 411-424. Hicks, C., Johnston, S. H., diSibio, G., Collazo, A., Vogt, T. F. and Weinmaster, G. (2000). Fringe differentially modulates Jagged1 and Delta1 signalling through Notch1 and Notch2. Nat. Cell Biol. 2, 515-520. Howland, R. B. (1916). On the effect of removal of the pronephros of the amphibian embryo. Proc. Natl. Acad. Sci. USA 2, 231-234. Ikeuchi, T. and Sisodia, S. S. (2003). The Notch ligands, Delta1 and Jagged2, are substrates for presenilin-dependent ‘gamma-secretase’ cleavage. J. Biol. Chem. 278, 7751-7754. Jarriault, S., Brou, C., Logeat, F., Schroeter, E. H., Kopan, R. and Israel, A. (1995). Signalling downstream of activated mammalian Notch. Nature 377, 355- 358. Johnston, S. H., Rauskolb, C., Wilson, R., Prabhakaran, B., Irvine, K. D. and Vogt, T. F. (1997). A family of mammalian Fringe genes implicated in boundary determination and the Notch pathway. Development 124, 2245-2254. Jones, E. A. (2005). Xenopus: a prince among models for pronephric kidney development. J. Am. Soc. Nephrol. 16, 313-321. Jones, E. A. and Woodland, H. R. (1986). Development of the ectoderm in Xenopus: tissue specification and the role of cell association and division. Cell 44, 345-355. Kadesch, T. (2004). Notch signaling: the demise of elegant simplicity. Curr. Opin. Genet. Dev. 14, 506-512. Karsan, A. (2008). Notch and integrin affinity: a sticky situation. Sci. Signal. 1, pe2. Kolev, V., Kacer, D., Trifonova, R., Small, D., Duarte, M., Soldi, R., Graziani, I., Sideleva, O., Larman, B., Maciag, T. et al. (2005). The intracellular domain of Notch ligand Delta1 induces cell growth arrest. FEBS Lett. 579, 5798-5802. Kopan, R. and Goate, A. (2000). A common enzyme connects notch signaling and Alzheimer’s disease. Genes Dev. 14, 2799-2806. Kopan, R., Cheng, H. T. and Surendran, K. (2007). Molecular insights into segmentation along the proximal-distal axis of the nephron. J. Am. Soc. Nephrol. 18, 2014-2020. LaVoie, M. J. and Selkoe, D. J. (2003). The Notch ligands, Jagged and Delta, are sequentially processed by alpha-secretase and presenilin/gamma-secretase and release signaling fragments. J. Biol. Chem. 278, 34427-34437. Leimeister, C., Schumacher, N. and Gessler, M. (2003). Expression of Notch pathway genes in the embryonic mouse metanephros suggests a role in proximal tubule development. Gene Expr. Patterns 3, 595-598. Liu, Y., Pathak, N., Kramer-Zucker, A. and Drummond, I. A. (2007). Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134, 1111-1122. Mauch, T. J., Yang, G., Wright, M., Smith, D. and Schoenwolf, G. C. (2000). Signals from trunk paraxial mesoderm induce pronephros formation in chick intermediate mesoderm. Dev. Biol. 220, 62-75. McCright, B., Gao, X., Shen, L., Lozier, J., Lan, Y., Maguire, M., Herzlinger, D., Weinmaster, G., Jiang, R. and Gridley, T. (2001). Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 128, 491-502. McLaughlin, K. A., Rones, M. S. and Mercola, M. (2000). Notch regulates cell fate in the developing pronephros. Dev. Biol. 227, 567-580. Mertens, P. R., Raffetseder, U. and Rauen, T. (2008). Notch receptors: a new target in glomerular diseases. Nephrol. Dial. Transplant. 23, 2743-2745. Mitchell, T., Jones, E. A., Weeks, D. L. and Sheets, M. D. (2007). Chordin affects pronephros development in Xenopus embryos by anteriorizing presomitic mesoderm. Dev. Dyn. 236, 251-261. Moloney, D. J., Panin, V. M., Johnston, S. H., Chen, J., Shao, L., Wilson, R., Wang, Y., Stanley, P., Irvine, K. D., Haltiwanger, R. S. et al. (2000). Fringe is a glycosyltransferase that modifies Notch. Nature 406, 369-375. Moody, S. A. and Kline, M. J. (1990). Segregation of fate during cleavage of frog (Xenopus laevis) blastomeres. Anat. Embryol. (Berl.) 182, 347-362. Nieuwkoop, P. D. and Faber, J. (1994). Normal table of Xenopus laevis (Daudin), 4th edn. New York: Garland Publishing. Niranjan, T., Bielesz, B., Gruenwald, A., Ponda, M. P., Kopp, J. B., Thomas, D. B. and Susztak, K. (2008). The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat. Med. 14, 290-298. Pichon, B., Taelman, V., Kricha, S., Christophe, D. and Bellefroid, E. J. (2002). XHRT-1, a hairy and Enhancer of split related gene with expression in floor plate and hypochord during early Xenopus embryogenesis. Dev. Genes Evol. 212, 491-495. Raciti, D., Reggiani, L., Geffers, L., Jiang, Q., Bacchion, F., Subrizi, A. E., Clements, D., Tindal, C., Davidson, D. R., Kaissling, B. et al. (2008). Organization of the pronephric kidney revealed by large-scale gene expression mapping. Genome Biol. 9, R84. Rampal, R., Li, A. S., Moloney, D. J., Georgiou, S. A., Luther, K. B., Nita-Lazar, A. and Haltiwanger, R. S. (2005). Lunatic fringe, manic fringe, and radical fringe recognize similar specificity determinants in O-fucosylated epidermal growth factor-like repeats. J. Biol. Chem. 280, 42454-42463. Reggiani, L., Raciti, D., Airik, R., Kispert, A. and Brändli, A. W. (2007). The prepattern transcription factor Irx3 directs nephron segment identity. Genes Dev. 21, 2358-2370. Rones, M. S., Woda, J., Mercola, M. and McLaughlin, K. A. (2002). Isolation and characterization of Xenopus Hey-1: a downstream mediator of Notch signaling. Dev. Dyn. 225, 554-560. Saulnier, D. M., Ghanbari, H. and Brandli, A. W. (2002). Essential function of Wnt-4 for tubulogenesis in the Xenopus pronephric kidney. Dev. Biol. 248, 13- 28. Saxén, L. (1987). Organogesis of the Kidney. Cambridge: Cambridge University Press. Schroeter, E. H., Kisslinger, J. A. and Kopan, R. (1998). Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386. Seufert, D. W., Brennan, H. C., DeGuire, J., Jones, E. A. and Vize, P. D. (1999). Developmental basis of pronephric defects in Xenopus body plan phenotypes. Dev. Biol. 215, 233-242. Smith, J. C., Price, B. M., Green, J. B., Weigel, D. and Herrmann, B. G. (1991). Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79-87. Taelman, V., Van Campenhout, C., Solter, M., Pieler, T. and Bellefroid, E. J. (2006). The Notch-effector HRT1 gene plays a role in glomerular development and patterning of the Xenopus pronephros anlagen. Development 133, 2961- 2971. Taniguchi, Y., Karlstrom, H., Lundkvist, J., Mizutani, T., Otaka, A., Vestling, M., Bernstein, A., Donoviel, D., Lendahl, U. and Honjo, T. (2002). Notch receptor cleavage depends on but is not directly executed by presenilins. Proc. Natl. Acad. Sci. USA 99, 4014-4019. Tsukumo, S., Hirose, K., Maekawa, Y., Kishihara, K. and Yasutomo, K. (2006). Lunatic fringe controls T cell differentiation through modulating notch signaling. J. Immunol. 177, 8365-8371. Visan, I., Yuan, J. S., Tan, J. B., Cretegny, K. and Guidos, C. J. (2006). Regulation of intrathymic T-cell development by Lunatic Fringe-Notch1 interactions. Immunol. Rev. 209, 76-94. Vize, P. D., Jones, E. A. and Pfister, R. (1995). Development of the Xenopus pronephric system. Dev. Biol. 171, 531-540. Wu, J. Y., Wen, L., Zhang, W. J. and Rao, Y. (1996). The secreted product of Xenopus gene lunatic Fringe, a vertebrate signaling molecule. Science 273, 355- 358. Zhang, N., Norton, C. R. and Gridley, T. (2002). Segmentation defects of Notch pathway mutants and absence of a synergistic phenotype in lunatic fringe/radical fringe double mutant mice. Genesis 33, 21-28.
URI:	http://wrap.warwick.ac.uk/id/eprint/2518