A Disintegrin and Metalloproteinase10 (ADAM10) Regulates NOTCH Signaling During Early Retinal Development

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2016 May 26

PMID 27224017

Citations 12

Authors

Joseph A Toonen

Adam Ronchetti

D J Sidjanin

Affiliations

Soon will be listed here.

Abstract

ADAM10 and ADAM17 are two closely related members of the ADAM (a disintegrin and metalloprotease) family of membrane-bound sheddases, which proteolytically cleave surface membrane proteins. Both ADAM10 and ADAM17 have been implicated in the proteolytic cleavage of NOTCH receptors and as such regulators of NOTCH signaling. During retinal development, NOTCH signaling facilitates retinal neurogenesis by maintaining progenitor cells in a proliferative state and by mediating retinal cell fates. However, the roles of ADAM10 and ADAM17 in the retina are not well defined. In this study, we set out to clarify the roles of ADAM10 and ADAM17 during early retinal development. The retinal phenotype of conditionally abated Adam17 retinae (Adam17 CKO) did not differ from the controls whereas conditionally ablated Adam10 retinae (Adam10 CKO) exhibited abnormal morphogenesis characterized by the formation of rosettes and a loss of retinal laminae phenotypically similar to morphological abnormalities identified in mice with retinal NOTCH signaling deficiency. Additionally, Adam10 CKO retinae exhibited abnormal neurogenesis characterized by fewer proliferating progenitor cells and greater differentiation of early photoreceptors and retinal ganglion cells. Moreover, constitutive activation of the NOTCH1-intracellular domain (N1-ICD) rescued Adam10 CKO abnormal neurogenesis, as well as abnormal retinal morphology by maintaining retinal cells in the progenitor state. Collectively these findings provide in vivo genetic evidence that ADAM10, and not ADAM17, is indispensable for proper retinal development as a regulator of NOTCH signaling.

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References

Jorissen E, Prox J, Bernreuther C, Weber S, Schwanbeck R, Serneels L . The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex. J Neurosci. 2010; 30(14):4833-44. PMC: 2921981. DOI: 10.1523/JNEUROSCI.5221-09.2010. View

Hartmann D, De Strooper B, Serneels L, Craessaerts K, Herreman A, Annaert W . The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts. Hum Mol Genet. 2002; 11(21):2615-24. DOI: 10.1093/hmg/11.21.2615. View

Peschon J, Slack J, Reddy P, Stocking K, Sunnarborg S, Lee D . An essential role for ectodomain shedding in mammalian development. Science. 1998; 282(5392):1281-4. DOI: 10.1126/science.282.5392.1281. View

Yaron O, Farhy C, Marquardt T, Applebury M, Ashery-Padan R . Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development. 2006; 133(7):1367-78. DOI: 10.1242/dev.02311. View

Toonen J, Liang L, Sidjanin D . Waved with open eyelids 2 (woe2) is a novel spontaneous mouse mutation in the protein phosphatase 1, regulatory (inhibitor) subunit 13 like (Ppp1r13l) gene. BMC Genet. 2012; 13:76. PMC: 3469352. DOI: 10.1186/1471-2156-13-76. View

Parry D, Toomes C, Bida L, Danciger M, Towns K, McKibbin M . Loss of the metalloprotease ADAM9 leads to cone-rod dystrophy in humans and retinal degeneration in mice. Am J Hum Genet. 2009; 84(5):683-91. PMC: 2681008. DOI: 10.1016/j.ajhg.2009.04.005. View

Young R . Cell differentiation in the retina of the mouse. Anat Rec. 1985; 212(2):199-205. DOI: 10.1002/ar.1092120215. View

Ohsawa R, Kageyama R . Regulation of retinal cell fate specification by multiple transcription factors. Brain Res. 2007; 1192:90-8. DOI: 10.1016/j.brainres.2007.04.014. View

Fu X, Sun H, Klein W, Mu X . Beta-catenin is essential for lamination but not neurogenesis in mouse retinal development. Dev Biol. 2006; 299(2):424-37. PMC: 3385515. DOI: 10.1016/j.ydbio.2006.08.015. View

10.

Maurer K, Riesenberg A, Brown N . Notch signaling differentially regulates Atoh7 and Neurog2 in the distal mouse retina. Development. 2014; 141(16):3243-54. PMC: 4197552. DOI: 10.1242/dev.106245. View

11.

Erdmann B, Kirsch F, Rathjen F, More M . N-cadherin is essential for retinal lamination in the zebrafish. Dev Dyn. 2003; 226(3):570-7. DOI: 10.1002/dvdy.10266. View

12.

Lieber T, Kidd S, Young M . kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev. 2002; 16(2):209-21. PMC: 155326. DOI: 10.1101/gad.942302. View

13.

Jarriault S, Greenwald I . Evidence for functional redundancy between C. elegans ADAM proteins SUP-17/Kuzbanian and ADM-4/TACE. Dev Biol. 2005; 287(1):1-10. PMC: 1805470. DOI: 10.1016/j.ydbio.2005.08.014. View

14.

Zheng M, Shi M, Pei Z, Gao F, Han H, Ding Y . The transcription factor RBP-J is essential for retinal cell differentiation and lamination. Mol Brain. 2009; 2:38. PMC: 2804697. DOI: 10.1186/1756-6606-2-38. View

15.

Cepko C, Austin C, Yang X, Alexiades M, Ezzeddine D . Cell fate determination in the vertebrate retina. Proc Natl Acad Sci U S A. 1996; 93(2):589-95. PMC: 40096. DOI: 10.1073/pnas.93.2.589. View

16.

Sel S, Kalinski T, Enssen I, Kaiser M, Nass N, Trau S . Expression analysis of ADAM17 during mouse eye development. Ann Anat. 2011; 194(4):334-8. DOI: 10.1016/j.aanat.2011.10.008. View

17.

Esteve P, Sandonis A, Cardozo M, Malapeira J, Ibanez C, Crespo I . SFRPs act as negative modulators of ADAM10 to regulate retinal neurogenesis. Nat Neurosci. 2011; 14(5):562-9. DOI: 10.1038/nn.2794. View

18.

van Tetering G, van Diest P, Verlaan I, van der Wall E, Kopan R, Vooijs M . Metalloprotease ADAM10 is required for Notch1 site 2 cleavage. J Biol Chem. 2009; 284(45):31018-27. PMC: 2781502. DOI: 10.1074/jbc.M109.006775. View

19.

Malicki J, Jo H, Pujic Z . Zebrafish N-cadherin, encoded by the glass onion locus, plays an essential role in retinal patterning. Dev Biol. 2003; 259(1):95-108. DOI: 10.1016/s0012-1606(03)00181-7. View

20.

Hassemer E, Le Gall S, Liegel R, McNally M, Chang B, Zeiss C . The waved with open eyelids (woe) locus is a hypomorphic mouse mutation in Adam17. Genetics. 2010; 185(1):245-55. PMC: 2870960. DOI: 10.1534/genetics.109.113167. View