Notch3 is essential for oligodendrocyte development and vascular integrity in zebrafish

DMM Disease Models and Mechanisms

Volumn 6, Issue 5, 2013, Pages 1246-1259

  Zaucker, Andreas ^a   Mercurio, Sara ^b   Sternheim, Nitzan ^b   Talbot, William S ^b   Marlow, Florence L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN BASIC PROTEIN; NOTCH RECEPTOR; NOTCH3 RECEPTOR;

ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTERY WALL; ARTICLE; BLEEDING; BLOOD CELL; BLOOD VESSEL TONE; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; GENE; GENE EXPRESSION; GENE FREQUENCY; GENE INSERTION; GENE MUTATION; HETEROZYGOTE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LARVAL DEVELOPMENT; MORPHOLOGY; NONHUMAN; NOTCH3 GENE; NUCLEOTIDE SEQUENCE; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; STRESS; TELENCEPHALON; ULTRASTRUCTURE; VASCULAR DISEASE; VASODILATATION; ZEBRA FISH;

ANIMALS; APOPTOSIS; BLOOD VESSELS; BODY PATTERNING; HEMORRHAGE; HETEROZYGOTE; HUMANS; LARVA; MUTATION; MYELIN BASIC PROTEIN; NEUROGENESIS; OLIGODENDROGLIA; PHENOTYPE; RECEPTORS, NOTCH; RNA, MESSENGER; TELENCEPHALON; VASODILATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84883850872     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.012005     Document Type: Article

References (62)

1. Andersson, E. R., Sandberg, R. and Lendahl, U. (2011). Notch signaling: simplicity in design, versatility in function. Development 138, 3593-3612.
2. Arboleda-Velasquez, J. F., Rampal, R., Fung, E., Darland, D. C., Liu, M., Martinez, M. C., Donahue, C. P., Navarro-Gonzalez, M. F., Libby, P., D'Amore, P. A. et al. (2005). CADASIL mutations impair Notch3 glycosylation by Fringe. Hum. Mol. Genet. 14, 1631-1639.
3. Arboleda-Velasquez, J. F., Zhou, Z., Shin, H. K., Louvi, A., Kim, H.-H., Savitz, S. I., Liao, J. K., Salomone, S., Ayata, C., Moskowitz, M. A. et al. (2008). Linking Notch signaling to ischemic stroke. Proc. Natl. Acad. Sci. USA 105, 4856-4861.
4. Arboleda-Velasquez, J. F., Manent, J., Lee, J. H., Tikka, S., Ospina, C., Vanderburg, C. R., Frosch, M. P., Rodríguez-Falcón, M., Villen, J., Gygi, S. et al. (2011). Hypomorphic Notch 3 alleles link Notch signaling to ischemic cerebral small-vessel disease. Proc. Natl. Acad. Sci. USA 108, E128-E135.
5. Ayata, C. (2010). CADASIL: experimental insights from animal models. Stroke 41 Suppl., S129-S134.
6. Baudrimont, M., Dubas, F., Joutel, A., Tournier-Lasserve, E. and Bousser, M. G. (1993). Autosomal dominant leukoencephalopathy and subcortical ischemic stroke. A clinicopathological study. Stroke 24, 122-125.
7. Belin de Chantemèle, E. J., Retailleau, K., Pinaud, F., Vessières, E., Bocquet, A., Guihot, A. L., Lemaire, B., Domenga, V., Baufreton, C., Loufrani, L. et al. (2008). Notch3 is a major regulator of vascular tone in cerebral and tail resistance arteries. Arterioscler. Thromb. Vasc. Biol. 28, 2216-2224.
8. Bierkamp, C. and Campos-Ortega, J. A. (1993). A zebrafish homologue of the Drosophila neurogenic gene Notch and its pattern of transcription during early embryogenesis. Mech. Dev. 43, 87-100.
9. Bingham, S., Chaudhari, S., Vanderlaan, G., Itoh, M., Chitnis, A. and Chandrasekhar, A. (2003). Neurogenic phenotype of mind bomb mutants leads to severe patterning defects in the zebrafish hindbrain. Dev. Dyn. 228, 451-463.
10. Campos-Ortega, J. A. (1985). Genetics of early neurogenesis in Drosophila melanogaster. Trends Neurosci. 8, 245-250.
11. Carmeliet, P. and Collen, D. (1999). Role of vascular endothelial growth factor and vascular endothelial growth factor receptors in vascular development. Curr. Top. Microbiol. Immunol. 237, 133-158.
12. Carmeliet, P. and Storkebaum, E. (2002). Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders. Semin. Cell Dev. Biol. 13, 39-53.
13. Cotanche, D. A. and Kaiser, C. L. (2010). Hair cell fate decisions in cochlear development and regeneration. Hear. Res. 266, 18-25.
14. Crosnier, C., Vargesson, N., Gschmeissner, S., Ariza-McNaughton, L., Morrison, A. and Lewis, J. (2005). Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132, 1093-1104.
15. Domenga, V., Fardoux, P., Lacombe, P., Monet, M., Maciazek, J., Krebs, L. T., Klonjkowski, B., Berrou, E., Mericskay, M., Li, Z. et al. (2004). Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 18, 2730-2735.
16. Durbin, L., Brennan, C., Shiomi, K., Cooke, J., Barrios, A., Shanmugalingam, S., Guthrie, B., Lindberg, R. and Holder, N. (1998). Eph signaling is required for segmentation and differentiation of the somites. Genes Dev. 12, 3096-3109.
17. Dutton, K. A., Pauliny, A., Lopes, S. S., Elworthy, S., Carney, T. J., Rauch, J., Geisler, R., Haffter, P. and Kelsh, R. N. (2001). Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128, 4113-4125.
18. Gazave, E., Lapébie, P., Richards, G. S., Brunet, F., Ereskovsky, A. V., Degnan, B. M., Borchiellini, C., Vervoort, M. and Renard, E. (2009). Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol. Biol. 9, 249.
19. Gridley, T. (2010). Notch signaling in the vasculature. Curr. Top. Dev. Biol. 92, 277-309.
20. Haddon, C., Jiang, Y. J., Smithers, L. and Lewis, J. (1998a). Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development 125, 4637-4644.
21. Haddon, C., Smithers, L., Schneider-Maunoury, S., Coche, T., Henrique, D. and Lewis, J. (1998b). Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125, 359-370.
22. Hans, S. and Campos-Ortega, J. A. (2002). On the organisation of the regulatory region of the zebrafish deltaD gene. Development 129, 4773-4784.
23. Heath, J. K. (2010). Transcriptional networks and signaling pathways that govern vertebrate intestinal development. Curr. Top. Dev. Biol. 90, 159-192.
24. Hervé, D. and Chabriat, H. (2010). Cadasil. J. Geriatr. Psychiatry Neurol. 23, 269-276.
25. Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K. and Kageyama, R. (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 30, 3489-3498.
26. Irvin, D. K., Zurcher, S. D., Nguyen, T., Weinmaster, G. and Kornblum, H. I. (2001). Expression patterns of Notch1, Notch2, and Notch3 suggest multiple functional roles for the Notch-DSL signaling system during brain development. J. Comp. Neurol. 436, 167-181.
27. Itoh, M., Kim, C. H., Palardy, G., Oda, T., Jiang, Y. J., Maust, D., Yeo, S. Y., Lorick, K., Wright, G. J., Ariza-McNaughton, L. et al. (2003). Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82.
28. Joutel, A. (2011). Pathogenesis of CADASIL: transgenic and knock-out mice to probe function and dysfunction of the mutated gene, Notch3, in the cerebrovasculature. Bioessays 33, 73-80.
29. Joutel, A., Vahedi, K., Corpechot, C., Troesch, A., Chabriat, H., Vayssière, C., Cruaud, C., Maciazek, J., Weissenbach, J., Bousser, M. G. et al. (1997). Strong clustering and stereotyped nature of Notch3 mutations in CADASIL patients. Lancet 350, 1511-1515.
30. Joutel, A., Monet, M., Domenga, V., Riant, F. and Tournier-Lasserve, E. (2004). Pathogenic mutations associated with cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy differently affect Jagged1 binding and Notch3 activity via the RBP/JK signaling Pathway. Am. J. Hum. Genet. 74, 338-347.
31. Kalimo, H., Ruchoux, M. M., Viitanen, M. and Kalaria, R. N. (2002). CADASIL: a common form of hereditary arteriopathy causing brain infarcts and dementia. Brain Pathol. 12, 371-384.
32. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
33. Kitamoto, T., Takahashi, K., Takimoto, H., Tomizuka, K., Hayasaka, M., Tabira, T. and Hanaoka, K. (2005). Functional redundancy of the Notch gene family during mouse embryogenesis: analysis of Notch gene expression in Notch3-deficient mice. Biochem. Biophys. Res. Commun. 331, 1154-1162.
34. Kopan, R. and Ilagan, M. X. (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233.
35. Krebs, L. T., Xue, Y., Norton, C. R., Sundberg, J. P., Beatus, P., Lendahl, U., Joutel, A. and Gridley, T. (2003). Characterization of Notch3-deficient mice: normal embryonic development and absence of genetic interactions with a Notch1 mutation. Genesis 37, 139-143.
36. Lawson, N. D. and Weinstein, B. M. (2002a). Arteries and veins: making a difference with zebrafish. Nat. Rev. Genet. 3, 674-682.
37. Lawson, N. D. and Weinstein, B. M. (2002b). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
38. Lawson, N. D., Scheer, N., Pham, V. N., Kim, C. H., Chitnis, A. B., Campos-Ortega, J. A. and Weinstein, B. M. (2001). Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128, 3675-3683.
39. Lawson, N. D., Vogel, A. M. and Weinstein, B. M. (2002). Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 3, 127-136.
40. Lee, J. H., Bacskai, B. J. and Ayata, C. (2012). Genetic animal models of cerebral vasculopathies. Prog. Mol. Biol. Transl. Sci. 105, 25-55.
41. Leslie, J. D., Ariza-McNaughton, L., Bermange, A. L., McAdow, R., Johnson, S. L. and Lewis, J. (2007). Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134, 839-844.
42. Lewis, J. (1996). Neurogenic genes and vertebrate neurogenesis. Curr. Opin. Neurobiol. 6, 3-10.
43. Lindsell, C. E., Boulter, J., diSibio, G., Gossler, A. and Weinmaster, G. (1996). Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol. Cell. Neurosci. 8, 14-27.
44. Lyons, D. A., Pogoda, H. M., Voas, M. G., Woods, I. G., Diamond, B., Nix, R., Arana, N., Jacobs, J. and Talbot, W. S. (2005). erbb3 and erbb2 are essential for schwann cell migration and myelination in zebrafish. Curr. Biol. 15, 513-524.
45. Lyons, D. A., Naylor, S. G., Mercurio, S., Dominguez, C. and Talbot, W. S. (2008). KBP is essential for axonal structure, outgrowth and maintenance in zebrafish, providing insight into the cellular basis of Goldberg-Shprintzen syndrome. Development 135, 599-608.
46. Mahler, J., Filippi, A. and Driever, W. (2010). DeltaA/DeltaD regulate multiple and temporally distinct phases of notch signaling during dopaminergic neurogenesis in zebrafish. J. Neurosci. 30, 16621-16635.
47. Miano, J. M., Georger, M. A., Rich, A. and De Mesy Bentley, K. L. (2006). Ultrastructure of zebrafish dorsal aortic cells. Zebrafish 3, 455-463.
48. Monet-Leprêtre, M., Bardot, B., Lemaire, B., Domenga, V., Godin, O., Dichgans, M., Tournier-Lasserve, E., Cohen-Tannoudji, M., Chabriat, H. and Joutel, A. (2009). Distinct phenotypic and functional features of CADASIL mutations in the Notch3 ligand binding domain. Brain 132, 1601-1612.
49. Monk, K. R., Naylor, S. G., Glenn, T. D., Mercurio, S., Perlin, J. R., Dominguez, C., Moens, C. B. and Talbot, W. S. (2009). A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 325, 1402-1405.
50. Moriyama, M., Osawa, M., Mak, S. S., Ohtsuka, T., Yamamoto, N., Han, H., Delmas, V., Kageyama, R., Beermann, F., Larue, L. et al. (2006). Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J. Cell Biol. 173, 333-339.
51. Okeda, R., Arima, K. and Kawai, M. (2002). Arterial changes in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) in relation to pathogenesis of diffuse myelin loss of cerebral white matter: examination of cerebral medullary arteries by reconstruction of serial sections of an autopsy case. Stroke 33, 2565-2569.
52. Opherk, C., Duering, M., Peters, N., Karpinska, A., Rosner, S., Schneider, E., Bader, B., Giese, A. and Dichgans, M. (2009). CADASIL mutations enhance spontaneous multimerization of NOTCH3. Hum. Mol. Genet. 18, 2761-2767.
53. Owens, G. K. (1995). Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 75, 487-517.
54. Owens, G. K. (1998). Molecular control of vascular smooth muscle cell differentiation. Acta Physiol. Scand. 164, 623-635.
55. Owens, G. K. and Wise, G. (1997). Regulation of differentiation/ maturation in vascular smooth muscle cells by hormones and growth factors. Agents Actions Suppl. 48, 3-24.
56. Owens, G. K., Kumar, M. S. and Wamhoff, B. R. (2004). Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801.
57. Pantoni, L. (2010). Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 9, 689-701.
58. Park, H. C. and Appel, B. (2003). Delta-Notch signaling regulates oligodendrocyte specification. Development 130, 3747-3755.
59. Park, H. C., Kim, C. H., Bae, Y. K., Yeo, S. Y., Kim, S. H., Hong, S. K., Shin, J., Yoo, K. W., Hibi, M., Hirano, T. et al. (2000). Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev. Biol. 227, 279-293.
60. Park, H. C., Mehta, A., Richardson, J. S. and Appel, B. (2002). olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev. Biol. 248, 356-368.
61. Park, H. C., Shin, J., Roberts, R. K. and Appel, B. (2007). An olig2 reporter gene marks oligodendrocyte precursors in the postembryonic spinal cord of zebrafish. Dev. Dyn. 236, 3402-3407.
62. Pierfelice, T., Alberi, L. and Gaiano, N. (2011). Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 69, 840-855.