Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo

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JOURNAL ARTICLES

Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo

SL Dunwoodie, D Henrique, SM Harrison and RS Beddington
Department of Mammalian Development, National Institute for Medical Research, Mill Hill, London, UK.

Mouse delta-like 3 (Dll3), a novel vertebrate homologue of the Drosophila gene Delta was isolated by a subtracted library screen. In Drosphila, the Delta/Notch signalling pathway functions in many situations in both embryonic and adult life where cell fate specification occurs. In addition, a patterning role has been described in the establishment of the dorsoventral compartment boundary in the wing imaginal disc. Dll3 is the most divergent Delta homologue identified to date. We confirm that Dll3 can inhibit primary neurogenesis when ectopically expressed in Xenopus, suggesting that it can activate the Notch receptor and therefore is a functional Delta homologue. An extensive expression study during gastrulation and early organogenesis in the mouse reveals a diverse and dynamic pattern of expression. The three major sites of expression implicate Dll3 in somitogenesis and neurogenesis and in the production of tissue from the primitive streak and tailbud. A careful comparison of Dll3 and Dll1 expression by double RNA in situ hybridisation demonstrates that these genes have distinct patterns of expression, but implies that together they operate in many of the same processes. We postulate that during somitogenesis Dll3 and Dll1 coordinate in establishing the intersomitic boundaries. We confirm that, during neurogenesis in the spinal cord, Dll1 and Dll3 are expressed by postmitotic cells and suggest that expression is sequential such that cells express Dll1 first followed by Dll3. We hypothesise that Dll1 is involved in the release of cells from the precursor population and that Dll3 is required later to divert neurons along a specific differentiation pathway.

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				V. Bolos, J. Grego-Bessa, and J. L. de la Pompa Notch Signaling in Development and Cancer Endocr. Rev., May 1, 2007; 28(3): 339 - 363. [Abstract] [Full Text] [PDF]

				I. Rubio-Aliaga, D. Soewarto, S. Wagner, M. Klaften, H. Fuchs, S. Kalaydjiev, D. H. Busch, M. Klempt, B. Rathkolb, E. Wolf, et al. A Genetic Screen for Modifiers of the Delta1-Dependent Notch Signaling Function in the Mouse Genetics, March 1, 2007; 175(3): 1451 - 1463. [Abstract] [Full Text] [PDF]

				J. B. Rutenberg, A. Fischer, H. Jia, M. Gessler, T. P. Zhong, and M. Mercola Developmental patterning of the cardiac atrioventricular canal by Notch and Hairy-related transcription factors Development, November 1, 2006; 133(21): 4381 - 4390. [Abstract] [Full Text] [PDF]

				A. Miyamoto, R. Lau, P. W. Hein, J. M. Shipley, and G. Weinmaster Microfibrillar Proteins MAGP-1 and MAGP-2 Induce Notch1 Extracellular Domain Dissociation and Receptor Activation J. Biol. Chem., April 14, 2006; 281(15): 10089 - 10097. [Abstract] [Full Text] [PDF]

				C. K. Williams, J.-L. Li, M. Murga, A. L. Harris, and G. Tosato Up-regulation of the Notch ligand Delta-like 4 inhibits VEGF-induced endothelial cell function Blood, February 1, 2006; 107(3): 931 - 939. [Abstract] [Full Text] [PDF]

				F Laumonnier, S Holbert, N Ronce, F Faravelli, S Lenzner, C E Schwartz, J Lespinasse, H Van Esch, D Lacombe, C Goizet, et al. Mutations in PHF8 are associated with X linked mental retardation and cleft lip/cleft palate J. Med. Genet., October 1, 2005; 42(10): 780 - 786. [Abstract] [Full Text] [PDF]

				E. Ladi, J. T. Nichols, W. Ge, A. Miyamoto, C. Yao, L.-T. Yang, J. Boulter, Y. E. Sun, C. Kintner, and G. Weinmaster The divergent DSL ligand Dll3 does not activate Notch signaling but cell autonomously attenuates signaling induced by other DSL ligands J. Cell Biol., September 12, 2005; 170(6): 983 - 992. [Abstract] [Full Text] [PDF]

				E. Mizuhara, T. Nakatani, Y. Minaki, Y. Sakamoto, Y. Ono, and Y. Takai MAGI1 Recruits Dll1 to Cadherin-based Adherens Junctions and Stabilizes It on the Cell Surface J. Biol. Chem., July 15, 2005; 280(28): 26499 - 26507. [Abstract] [Full Text] [PDF]

				S. L. DeHart, M. J. Heikens, and S. Tsai Jagged2 promotes the development of natural killer cells and the establishment of functional natural killer cell lines Blood, May 1, 2005; 105(9): 3521 - 3527. [Abstract] [Full Text] [PDF]

				N M Solomon, S A Ross, T Morgan, J L Belsky, F A Hol, P S Karnes, N J Hopwood, S E Myers, A S Tan, G L Warne, et al. Array comparative genomic hybridisation analysis of boys with X linked hypopituitarism identifies a 3.9 Mb duplicated critical region at Xq27 containing SOX3 J. Med. Genet., September 1, 2004; 41(9): 669 - 678. [Abstract] [Full Text] [PDF]

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				C. H. Jensen, E. I. Jauho, E. Santoni-Rugiu, U. Holmskov, B. Teisner, N. Tygstrup, and H. C. Bisgaard Transit-Amplifying Ductular (Oval) Cells and Their Hepatocytic Progeny Are Characterized by a Novel and Distinctive Expression of Delta-Like Protein/Preadipocyte Factor 1/Fetal Antigen 1 Am. J. Pathol., April 1, 2004; 164(4): 1347 - 1359. [Abstract] [Full Text] [PDF]

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				M. Sciaudone, E. Gazzerro, L. Priest, A. M. Delany, and E. Canalis Notch 1 Impairs Osteoblastic Cell Differentiation Endocrinology, December 1, 2003; 144(12): 5631 - 5639. [Abstract] [Full Text] [PDF]

				R. Sousa-Nunes, A. A. Rana, R. Kettleborough, J. M. Brickman, M. Clements, A. Forrest, S. Grimmond, P. Avner, J. C. Smith, S. L. Dunwoodie, et al. Characterizing Embryonic Gene Expression Patterns in the Mouse Using Nonredundant Sequence-Based Selection Genome Res., December 1, 2003; 13(12): 2609 - 2620. [Abstract] [Full Text] [PDF]

				Y. Takahashi, T. Inoue, A. Gossler, and Y. Saga Feedback loops comprising Dll1, Dll3 and Mesp2, and differential involvement of Psen1 are essential for rostrocaudal patterning of somites Development, September 15, 2003; 130(18): 4259 - 4268. [Abstract] [Full Text] [PDF]

				P D Turnpenny, N Whittock, J Duncan, S Dunwoodie, K Kusumi, and S Ellard Novel mutations in DLL3, a somitogenesis gene encoding a ligand for the Notch signalling pathway, cause a consistent pattern of abnormal vertebral segmentation in spondylocostal dysostosis J. Med. Genet., May 1, 2003; 40(5): 333 - 339. [Abstract] [Full Text] [PDF]

				P. H. White, D. R. Farkas, E. E. McFadden, and D. L. Chapman Defective somite patterning in mouse embryos with reduced levels of Tbx6 Development, April 15, 2003; 130(8): 1681 - 1690. [Abstract] [Full Text] [PDF]

				T. Iso, Y. Hamamori, and L. Kedes Notch Signaling in Vascular Development Arterioscler. Thromb. Vasc. Biol., April 1, 2003; 23(4): 543 - 553. [Abstract] [Full Text] [PDF]

				T. Yamada, H. Yamazaki, T. Yamane, M. Yoshino, H. Okuyama, M. Tsuneto, T. Kurino, S.-I. Hayashi, and S. Sakano Regulation of osteoclast development by Notch signaling directed to osteoclast precursors and through stromal cells Blood, March 15, 2003; 101(6): 2227 - 2234. [Abstract] [Full Text] [PDF]

				N. Cambray and V. Wilson Axial progenitors with extensive potency are localised to the mouse chordoneural hinge Development, March 12, 2003; 129(20): 4855 - 4866. [Abstract] [Full Text] [PDF]

				S. Lutolf, F. Radtke, M. Aguet, U. Suter, and V. Taylor Notch1 is required for neuronal and glial differentiation in the cerebellum Development, March 3, 2003; 129(2): 373 - 385. [Abstract] [Full Text] [PDF]

				G. K. H. Przemeck, U. Heinzmann, J. Beckers, and M. Hrabe de Angelis Node and midline defects are associated with left-right development in Delta1 mutant embryos Development, January 1, 2003; 130(1): 3 - 13. [Abstract] [Full Text] [PDF]

				M. Dorsch, G. Zheng, D. Yowe, P. Rao, Y. Wang, Q. Shen, C. Murphy, X. Xiong, Q. Shi, J.-C. Gutierrez-Ramos, et al. Ectopic expression of Delta4 impairs hematopoietic development and leads to lymphoproliferative disease Blood, August 28, 2002; 100(6): 2046 - 2055. [Abstract] [Full Text] [PDF]

				Y. Sato, K. Yasuda, and Y. Takahashi Morphological boundary forms by a novel inductive event mediated by Lunatic fringe and Notch during somitic segmentation Development, August 1, 2002; 129(15): 3633 - 3644. [Abstract] [Full Text] [PDF]

				S. S. Nijjar, L. Wallace, H. A. Crosby, S. G. Hubscher, and A. J. Strain Altered Notch Ligand Expression in Human Liver Disease : Further Evidence for a Role of the Notch Signaling Pathway in Hepatic Neovascularization and Biliary Ductular Defects Am. J. Pathol., May 1, 2002; 160(5): 1695 - 1703. [Abstract] [Full Text] [PDF]

				Y. Sasaki, S. Ishida, I. Morimoto, T. Yamashita, T. Kojima, C. Kihara, T. Tanaka, K. Imai, Y. Nakamura, and T. Tokino The p53 Family Member Genes Are Involved in the Notch Signal Pathway J. Biol. Chem., January 4, 2002; 277(1): 719 - 724. [Abstract] [Full Text]