The Notch signaling pathway in retinal dysplasia and retina vascular homeostasis

Minhua Zheng; Zifeng Zhang; Xingcheng Zhao; Yuqiang Ding; Hua Han

doi:10.1016/S1673-8527(09)60077-1

Volume 37 Issue 9

Sep. 2010

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2010 > 37(9): 573-582

PDF( 459 KB)

The Notch signaling pathway in retinal dysplasia and retina vascular homeostasis

doi: 10.1016/S1673-8527(09)60077-1

a
Department of Medical Genetics and Developmental Biology, Fourth Military Medical University, Xi'an 710032, China
b
Department of Ophthalmology, Xijing Hospital, Fourth Military Medical University, Xi'an 710032, China
c
Department of Anatomy and Neurobiology, Tongji University School of Medicine, Shanghai 200092, China

More Information

Corresponding author: E-mail address: huahan@fmmu.edu.cn (Hua Han)
Received Date: 2010-06-11
Accepted Date: 2010-08-18
Rev Recd Date: 2010-08-12

Available Online: 2010-10-07

Publish Date: 2010-09-20

Abstract

Abstract

The retina is one of the most essential elements of vision pathway in vertebrate. The dysplasia of retina cause congenital blindness or vision disability in individuals, and the misbalance in adult retinal vascular homeostasis leads to neovascularization-associated diseases in adults, such as diabetic retinopathy or age-related macular degeneration. Many developmental signaling pathways are involved in the process of retinal development and vascular homeostasis. Among them, Notch signaling pathway has long been studied, and Notch signaling-interfered mouse models show both neural retina dysplasia and vascular abnormality. In this review, we discuss the roles of Notch signaling in the maintenance of retinal progenitor cells, specification of retinal neurons and glial cells, and the sustaining of retina vascular homeostasis, especially from the aspects of conditional knockout mouse models. The potential of Notch signal manipulation may provide a powerful cell fate- and neovascularization-controlling tool that could have important applications in treatment of retinal diseases.
- Notch signaling,
- retinal dysplasia,
- vascular homeostasis,
- neovascularization,
- knockout mice

These authors contributed equally to this study.

FullText(HTML)

References(55)

References

[1]	Benedito, R., Roca, C., Sorensen, I. et al. The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis Cell, 137 (2009),pp. 1124-1135
[2]	Bray, S.J. Notch signalling: a simple pathway becomes complex Nat. Rev. Mol. Cell Biol., 7 (2006),pp. 678-689
[3]	Campochiaro, P.A. Retinal and choroidal neovascularization J. Cell Physiol., 184 (2000),pp. 301-310
[4]	Carmeliet, P. Mechanisms of angiogenesis and arteriogenesis Nat. Med., 6 (2000),pp. 389-395
[5]	Chiba, S. Notch signaling in stem cell systems Stem Cells, 24 (2006),pp. 2437-2447
[6]	Chow, R.L., Lang, R.A. Early eye development in vertebrates Annu. Rev. Cell Dev. Biol., 17 (2001),pp. 255-296
[7]	Delaney, C., Heimfeld, S., Brashem-Stein, C. et al. Notch-mediated expansion of human cord blood progenitor cells capable of rapid myeloid reconstitution Nat. Med., 16 (2010),pp. 232-236
[8]	Dorsky, R.I., Rapaport, D.H., Harris, W.A. Neuron, 14 (1995),pp. 487-496
[9]	Dou, G.R., Wang, Y.C., Hu, X.B. et al. RBP-J, the transcription factor downstream of Notch receptors, is essential for the maintenance of vascular homeostasis in adult mice FASEB J., 22 (2008),pp. 1606-1617
[10]	Fischer, A., Schumacher, N., Maier, M. et al. Genes Dev., 18 (2004),pp. 901-911
[11]	Fruttiger, M. Development of the retinal vasculature Angiogenesis, 10 (2007),pp. 77-88
[12]	Fu, X., Sun, H., Klein, W.H. et al. Beta-catenin is essential for lamination but not neurogenesis in mouse retinal development Dev. Biol., 299 (2006),pp. 424-437
[13]	Gale, N.W., Dominguez, M.G., Noguera, I. et al. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 15949-15954
[14]	Gao, F., Zhang, Q., Zheng, M.H. et al. Transcription factor RBP-J-mediated signaling represses the differentiation of neural stem cells into intermediate neural progenitors Mol. Cell. Neurosci., 40 (2009),pp. 442-450
[15]	Gariano, R.F. Cellular mechanisms in retinal vascular development Prog. Retin. Eye Res., 22 (2003),pp. 295-306
[16]	Gerhart, J. 1998 Warkany lecture: signaling pathways in development Teratology, 60 (1999),pp. 226-239
[17]	Grandbarbe, L., Bouissac, J., Rand, M. et al. Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process Development, 130 (2003),pp. 1391-1402
[18]	Haines, N., Irvine, K.D. Glycosylation regulates Notch signalling Nat. Rev. Mol. Cell Biol., 4 (2003),pp. 786-797
[19]	Han, H., Tanigaki, K., Yamamoto, N. et al. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision Int. Immunol., 14 (2002),pp. 637-645
[20]	Hatakeyama, J., Kageyama, R. Retinal cell fate determination and bHLH factors Semin. Cell Dev. Biol., 15 (2004),pp. 83-89
[21]	Hayward, P., Kalmar, T., Arias, A.M. Wnt/Notch signalling and information processing during development Development, 135 (2008),pp. 411-424
[22]	Hellstrom, M., Phng, L.K., Hofmann, J.J. et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis Nature, 445 (2007),pp. 776-780
[23]	Hinds, J.W., Hinds, P.L. Early ganglion cell differentiation in the mouse retina: an electron microscopic analysis utilizing serial sections Dev. Biol., 37 (1974),pp. 381-416
[24]	Hinds, J.W., Hinds, P.L. Differentiation of photoreceptors and horizontal cells in the embryonic mouse retina: an electron microscopic, serial section analysis J. Comp. Neurol., 187 (1979),pp. 495-511
[25]	Hojo, M., Ohtsuka, T., Hashimoto, N. et al. Development, 127 (2000),pp. 2515-2522
[26]	Ilagan, M.X., Kopan, R. SnapShot: Notch signaling pathway Cell, 128 (2007),p. 1246
[27]	Jadhav, A.P., Cho, S.H., Cepko, C.L. Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 18998-19003
[28]	Jadhav, A.P., Mason, H.A., Cepko, C.L. Notch 1 inhibits photoreceptor production in the developing mammalian retina Development, 133 (2006),pp. 913-923
[29]	Joutel, A., Corpechot, C., Ducros, A. et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia Nature, 383 (1996),pp. 707-710
[30]	Joutel, A., Tournier-Lasserve, E. Notch signalling pathway and human diseases Semin. Cell Dev. Biol., 9 (1998),pp. 619-625
[31]	Kopan, R., Ilagan, M.X. The canonical Notch signaling pathway: unfolding the activation mechanism Cell, 137 (2009),pp. 216-233
[32]	Krebs, L.T., Xue, Y., Norton, C.R. et al. Notch signaling is essential for vascular morphogenesis in mice Genes Dev., 14 (2000),pp. 1343-1352
[33]	Kume, T. Novel insights into the differential functions of Notch ligands in vascular formation J. Angiogenes. Res., 1 (2009),p. 8
[34]	Lawson, N.D., Vogel, A.M., Weinstein, B.M. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation Dev. Cell, 3 (2002),pp. 127-136
[35]	Leslie, J.D., Ariza-McNaughton, L., Bermange, A.L. et al. Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis Development, 134 (2007),pp. 839-844
[36]	Limbourg, F.P., Takeshita, K., Radtke, F. et al. Essential role of endothelial Notch1 in angiogenesis Circulation, 111 (2005),pp. 1826-1832
[37]	Liu, Z.J., Xiao, M., Balint, K. et al. Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1 FASEB J., 20 (2006),pp. 1009-1011
[38]	Lobov, I.B., Renard, R.A., Papadopoulos, N. et al. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 3219-3224
[39]	Louvi, A., Artavanis-Tsakonas, S. Notch signalling in vertebrate neural development Nat. Rev. Neurosci., 7 (2006),pp. 93-102
[40]	Marquardt, T., Gruss, P. Generating neuronal diversity in the retina: one for nearly all Trends Neurosci., 25 (2002),pp. 32-38
[41]	Martinez Arias, A., Zecchini, V., Brennan, K. CSL-independent Notch signalling: a checkpoint in cell fate decisions during development? CurrOpin. Genet. Dev., 12 (2002),pp. 524-533
[42]	Neumann, C.J. Pattern formation in the zebrafish retina Semin. Cell Dev. Biol., 12 (2001),pp. 485-490
[43]	Osakada, F., Ikeda, H., Mandai, M. et al. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells Nat. Biotechnol., 26 (2008),pp. 215-224
[44]	Poggi, L., Zolessi, F.R., Harris, W.A. Time-lapse analysis of retinal differentiation Curr. Opin. Cell Biol., 17 (2005),pp. 676-681
[45]	Radtke, F., Fasnacht, N., Macdonald, H.R. Notch signaling in the immune system Immunity, 32 (2010),pp. 14-27
[46]	Redmond, L., Oh, S.R., Hicks, C. et al. Nuclear Notch1 signaling and the regulation of dendritic development Nat. Neurosci., 3 (2000),pp. 30-40
[47]	Riesenberg, A.N., Liu, Z., Kopan, R. et al. Rbpj cell autonomous regulation of retinal ganglion cell and cone photoreceptor fates in the mouse retina J. Neurosci., 29 (2009),pp. 12865-12877
[48]	Rocha, S.F., Lopes, S.S., Gossler, A. et al. Dll1 and Dll4 function sequentially in the retina and pV2 domain of the spinal cord to regulate neurogenesis and create cell diversity Dev. Biol., 328 (2009),pp. 54-65
[49]	Sestan, N., Artavanis-Tsakonas, S., Rakic, P. Contact-dependent inhibition of cortical neurite growth mediated by notch signaling Science, 286 (1999),pp. 741-746
[50]	Suchting, S., Freitas, C., le Noble, F. et al. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 3225-3230
[51]	Takatsuka, K., Hatakeyama, J., Bessho, Y. et al. Brain Res., 1004 (2004),pp. 148-155
[52]	Williams, C.K., Li, J.L., Murga, M. et al. Up-regulation of the Notch ligand Delta-like 4 inhibits VEGF-induced endothelial cell function Blood, 107 (2006),pp. 931-939
[53]	Xue, Y., Gao, X., Lindsell, C.E. et al. Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1 Hum. Mol. Genet., 8 (1999),pp. 723-730
[54]	Yaron, O., Farhy, C., Marquardt, T. et al. Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina Development, 133 (2006),pp. 1367-1378
[55]	Zheng, M.H., Shi, M., Pei, Z. et al. The transcription factor RBP-J is essential for retinal cell differentiation and lamination Mol. Brain, 2 (2009),p. 38