Sostdc1 is Expressed in All Major Compartments of Developing and Adult Mammalian Eyes

Overview

Journal Graefes Arch Clin Exp Ophthalmol

Specialty Ophthalmology

Date 2019 Sep 19

PMID 31529323

Citations 2

Authors

Maud Valensi

Gabrielle Goldman

Dominique Marchant

Loic Van Den Berghe

Laurent Jonet

Alejandra Daruich

Matthieu P Robert

Eric Krejci

Christophe Klein

Frederic Mascarelli

Claudine Versaux-Botteri

Alexandre Moulin

Marc Putterman

Fabien Guimiot

Thierry Molina

Benoit Terris

Dominique Bremond-Gignac

Francine Behar-Cohen

Marc M Abitbol

Affiliations

Soon will be listed here.

Abstract

Purpose: This study was conducted in order to study Sostdc1 expression in rat and human developing and adult eyes.

Methods: Using the yeast signal sequence trap screening method, we identified the Sostdc1 cDNA encoding a protein secreted by the adult rat retinal pigment epithelium. We determined by in situ hybridization, RT-PCR, immunohistochemistry, and western blot analysis Sostdc1 gene and protein expression in developing and postnatal rat ocular tissue sections. We also investigated Sostdc1 immunohistolocalization in developing and adult human ocular tissues.

Results: We demonstrated a prominent Sostdc1 gene expression in the developing rat central nervous system (CNS) and eyes at early developmental stages from E10.5 days postconception (dpc) to E13 dpc. Specific Sostdc1 immunostaining was also detected in most adult cells of rat ocular tissue sections. We also identified the rat ocular embryonic compartments characterized by a specific Sostdc1 immunohistostaining and specific Pax6, Sox2, Otx2, and Vsx2 immunohistostaining from embryonic stages E10.5 to E13 dpc. Furthermore, we determined the localization of SOSTDC1 immunoreactivity in ocular tissue sections of developing and adult human eyes. Indeed, we detected SOSTDC1 immunostaining in developing and adult human retinal pigment epithelium (RPE) and neural retina (NR) as well as in several developing and adult human ocular compartments, including the walls of choroidal and scleral vessels. Of utmost importance, we observed a strong SOSTDC1 expression in a pathological ocular specimen of type 2 Peters' anomaly complicated by retinal neovascularization as well in the walls ofother pathological extra-ocular vessels. CONCLUSION: As rat Sostdc1 and human SOSTDC1 are dual antagonists of the Wnt/β-catenin and BMP signaling pathways, these results underscore the potential crucial roles of these pathways and their antagonists, such as Sostdc1 and SOSTDC1, in developing and adult mammalian normal eyes as well as in syndromic and nonsyndromic congenital eye diseases.

Citing Articles

Role of HDAC5 Epigenetics in Chronic Craniofacial Neuropathic Pain.

Hui S, Westlund K Int J Mol Sci. 2024; 25(13).

PMID: 38999998 PMC: 11241576. DOI: 10.3390/ijms25136889.

Toll-Like Receptor 7 Is Required for Lacrimal Gland Autoimmunity and Type 1 Diabetes Development in Male Nonobese Diabetic Mice.

Debreceni I, Chimenti M, Serreze D, Geurts A, Chen Y, Lieberman S Int J Mol Sci. 2020; 21(24).

PMID: 33322152 PMC: 7764018. DOI: 10.3390/ijms21249478.

References

De Almeida I, Oliveira N, Randall R, Hill C, McCoy J, Stern C . Calreticulin is a secreted BMP antagonist, expressed in Hensen's node during neural induction. Dev Biol. 2016; 421(2):161-170. PMC: 5231319. DOI: 10.1016/j.ydbio.2016.12.001. View

Fujimura N . WNT/β-Catenin Signaling in Vertebrate Eye Development. Front Cell Dev Biol. 2016; 4:138. PMC: 5127792. DOI: 10.3389/fcell.2016.00138. View

Klein R, Gu Q, Goddard A, Rosenthal A . Selection for genes encoding secreted proteins and receptors. Proc Natl Acad Sci U S A. 1996; 93(14):7108-13. PMC: 38944. DOI: 10.1073/pnas.93.14.7108. View

van Bezooijen R, DeRuiter M, Vilain N, Monteiro R, Visser A, van der Wee-Pals L . SOST expression is restricted to the great arteries during embryonic and neonatal cardiovascular development. Dev Dyn. 2006; 236(2):606-12. DOI: 10.1002/dvdy.21054. View

Vecino E, Acera A . Development and programed cell death in the mammalian eye. Int J Dev Biol. 2015; 59(1-3):63-71. DOI: 10.1387/ijdb.150070ev. View

St-Onge L, Sosa-Pineda B, Chowdhury K, Mansouri A, Gruss P . Pax6 is required for differentiation of glucagon-producing alpha-cells in mouse pancreas. Nature. 1997; 387(6631):406-9. DOI: 10.1038/387406a0. View

Ahn Y, Sanderson B, Klein O, Krumlauf R . Inhibition of Wnt signaling by Wise (Sostdc1) and negative feedback from Shh controls tooth number and patterning. Development. 2010; 137(19):3221-31. PMC: 6512258. DOI: 10.1242/dev.054668. View

Matsushima D, Heavner W, Pevny L . Combinatorial regulation of optic cup progenitor cell fate by SOX2 and PAX6. Development. 2011; 138(3):443-54. PMC: 3014633. DOI: 10.1242/dev.055178. View

Liu L, Wu S, Yang Y, Cai J, Zhu X, Wu J . SOSTDC1 is down-regulated in non-small cell lung cancer and contributes to cancer cell proliferation. Cell Biosci. 2016; 6:24. PMC: 4832458. DOI: 10.1186/s13578-016-0091-9. View

10.

Adams D, Karolak M, Robertson E, Oxburgh L . Control of kidney, eye and limb expression of Bmp7 by an enhancer element highly conserved between species. Dev Biol. 2007; 311(2):679-90. PMC: 2394512. DOI: 10.1016/j.ydbio.2007.08.036. View

11.

Lehmann G, Benedicto I, Philp N, Rodriguez-Boulan E . Plasma membrane protein polarity and trafficking in RPE cells: past, present and future. Exp Eye Res. 2014; 126:5-15. PMC: 4502961. DOI: 10.1016/j.exer.2014.04.021. View

12.

Chassaing N, Davis E, McKnight K, Niederriter A, Causse A, David V . Targeted resequencing identifies PTCH1 as a major contributor to ocular developmental anomalies and extends the SOX2 regulatory network. Genome Res. 2016; 26(4):474-85. PMC: 4817771. DOI: 10.1101/gr.196048.115. View

13.

Faber S, Robinson M, Makarenkova H, Lang R . Bmp signaling is required for development of primary lens fiber cells. Development. 2002; 129(15):3727-37. DOI: 10.1242/dev.129.15.3727. View

14.

Raviv S, Bharti K, Rencus-Lazar S, Cohen-Tayar Y, Schyr R, Evantal N . PAX6 regulates melanogenesis in the retinal pigmented epithelium through feed-forward regulatory interactions with MITF. PLoS Genet. 2014; 10(5):e1004360. PMC: 4038462. DOI: 10.1371/journal.pgen.1004360. View

15.

Tashiro K, Tada H, Heilker R, Shirozu M, Nakano T, Honjo T . Signal sequence trap: a cloning strategy for secreted proteins and type I membrane proteins. Science. 1993; 261(5121):600-3. DOI: 10.1126/science.8342023. View

16.

Rainger J, van Beusekom E, Ramsay J, McKie L, Al-Gazali L, Pallotta R . Loss of the BMP antagonist, SMOC-1, causes Ophthalmo-acromelic (Waardenburg Anophthalmia) syndrome in humans and mice. PLoS Genet. 2011; 7(7):e1002114. PMC: 3131273. DOI: 10.1371/journal.pgen.1002114. View

17.

Steinfeld J, Steinfeld I, Bausch A, Coronato N, Hampel M, Depner H . BMP-induced reprogramming of the neural retina into retinal pigment epithelium requires Wnt signalling. Biol Open. 2017; 6(7):979-992. PMC: 5550904. DOI: 10.1242/bio.018739. View

18.

Asai-Coakwell M, French C, Berry K, Ye M, Koss R, Somerville M . GDF6, a novel locus for a spectrum of ocular developmental anomalies. Am J Hum Genet. 2007; 80(2):306-15. PMC: 1785352. DOI: 10.1086/511280. View

19.

Jacobs K, Collins-Racie L, Colbert M, Duckett M, Kelleher K, Kriz R . A genetic selection for isolating cDNAs encoding secreted proteins. Gene. 1997; 198(1-2):289-96. DOI: 10.1016/s0378-1119(97)00330-2. View

20.

Beleggia F, Li Y, Fan J, Elcioglu N, Toker E, Wieland T . CRIM1 haploinsufficiency causes defects in eye development in human and mouse. Hum Mol Genet. 2015; 24(8):2267-73. PMC: 4380072. DOI: 10.1093/hmg/ddu744. View