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Expression patterns of ADAMs in the developing chicken lens

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Abstract

In the present study the expression patterns of ADAM (a disintegrin and metalloprotease) genes in the chicken developing lens were analyzed. Using in situ hybridization, we found that seven members of the ADAM family including ADAM9, ADAM10, ADAM12, ADAM13, ADAM17, ADAM22, and ADAM23 are expressed in the developing embryonic lens. From embryonic incubation day (E) 2 to E3, most of the ADAMs investigated here are expressed in the lens placode and lens vesicle. From E5 to E7, all seven ADAMs, but predominantly ADAM9 and ADAM10, are throughly expressed in the central epithelium, as well as in the proliferating lens epithelium and the equatorial lens epithelium. From E9 to E14, expression of ADAM9, ADAM10, and ADAM17 decreases moderately in these regions. ADAM12 and ADAM13 are weakly expressed in the central epithelium and the lens epithelium, and are not detectable from E14 onward. ADAM22 and ADAM23 are expressed in the central epithelium, the lens epithelium and the equatorial lens epithelium at E5 and decrease gradually afterwards in the same regions. At E16, only weak ADAM9, ADAM10 and ADAM17 signals are found in the anterior lens epithelium. The changing spatiotemporal expression of the seven ADAMs suggests a regulatory role for these molecules during chicken lens development.

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References

  • Alfandari D, Cousin H, Gaultier A, Smith K, White JM, Darribère T, Desimone DW (2001) Xenopus ADAM 13 is a metalloprotease required for cranial neural crest-cell migration. Curr Biol 11:918–930

    Article  PubMed  CAS  Google Scholar 

  • Alfandari D, McCusker C, Cousin H (2009) ADAM function in embryogenesis. Semin Cell Dev Biol 20:153–163

    Article  PubMed  CAS  Google Scholar 

  • Ashery-Padan R, Marquardt T, Zhou X, Gruss P (2000) Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev 14:2701–2711

    Article  PubMed  CAS  Google Scholar 

  • Belecky-Adams TL, Adler R, Beebe DC (2002) Bone morphogenetic protein signaling and the initiation of lens fiber cell differentiation. Development 129:3795–3802

    PubMed  CAS  Google Scholar 

  • Bland CE, Kimberly P, Rand MD (2003) Notch-induced proteolysis and nuclear localization of the Delta ligand. J Biol Chem 278:13607–13610

    Article  PubMed  CAS  Google Scholar 

  • Blobel CP (2005) ADAMs: key components in EGFR signalling and development. Natl Rev Mol Cell Biol 6:32–43

    Article  CAS  Google Scholar 

  • Canau M, Certel K, Schatzberg D, Wagner DD, Hynes RO (2010) The lack of ADAM17 activity during embryonic development causes hemorrhage and impairs vessel formation. PLoS One 5:e13433

    Article  Google Scholar 

  • Chen YY, Hehr CL, Atkinson-Leadbeater K, Hocking JC, McFarlane S (2007) Targeting of retinal axons requires the metalloproteinase ADAM10. J Neurosci 27:8448–8456

    Article  PubMed  CAS  Google Scholar 

  • Chow RL, Roux GD, Roghani M, Palmer MA, Rifkin DB, Moscatelli DA, Lang RA (1995) FGF suppresses apoptosis and induces differentiation of fibre cells in the mouse lens. Development 121:4383–4393

    PubMed  CAS  Google Scholar 

  • de Iongh R, McAvoy JW (1993) Spatio-temporal distribution of acidic and basic FGF indicates a role for FGF in rat lens morphogenesis. Dev Dyn 198:190–202

    Article  PubMed  Google Scholar 

  • Donner AL, Lachke SA, Maas RL (2006) Lens induction in vertebrates: variations on a conserved theme of signalling events. Semin Cell Dev Biol 17:676–685

    Article  PubMed  CAS  Google Scholar 

  • Edwards DR, Handsley MM, Pennington CJ (2008) The ADAM metalloproteinases. Mol Aspects Med 29:258–289

    Article  PubMed  CAS  Google Scholar 

  • Fokina VM, Frolova EI (2006) Expression patterns of Wnt genes during development of an anterior part of the chicken eye. Dev Dyn 235:496–505

    Article  PubMed  CAS  Google Scholar 

  • Furuta Y, Hogan BL (1998) BMP4 is essential for lens induction in the mouse embryo. Genes Dev 12:3764–3775

    Article  PubMed  CAS  Google Scholar 

  • Goldsmith AP, Gossage SJ, ffrench-Constant C (2004) ADAM23 is a cell-surface glycoprotein expressed by central nervous system neurons. J Neurosci Res 78:647–658

    Article  PubMed  CAS  Google Scholar 

  • Gschwind A, Hart S, Fischer OM, Ullrich A (2003) TACE cleavage of proamphiregulin regulates GPCR-induced proliferation and motility of cancer cells. EMBO J 22:2411–2421

    Article  PubMed  CAS  Google Scholar 

  • Hall RJ, Erickson CA (2003) ADAM 10: an active metalloprotease expressed during avian epithelial morphogenesis. Dev Biol 256:146–159

    Article  PubMed  CAS  Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

    Article  Google Scholar 

  • Hartmann D, de Strooper B, Serneels L, Craessaerts K, Herreman A, Annaert W, Umans L, Lübke T, Lena Illert A, von Figura K, Saftig P (2002) The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts. Hum Mol Genet 11:2615–2624

    Article  PubMed  CAS  Google Scholar 

  • Itoh Y, Joh T, Tanida S, Sasaki M, Kataoka H, Itoh K, Oshima T, Ogasawara N, Togawa S, Wada T, Kubota H, Mori Y, Ohara H, Nomura T, Higashiyama S, Itoh M (2005) IL-8 promotes cell proliferation and migration through metalloproteinase-cleavage proHB-EGF in human colon carcinoma cells. Cytokine 29:275–282

    PubMed  CAS  Google Scholar 

  • Jorissen E, Prox J, Bernreuther C, Weber S, Schwanbeck R, Serneels L, Snellinx A, Craessaerts K, Thathiah A, Tesseur I, Bartsch U, Weskamp G, Blobel CP, Glatzel M, De Strooper B, Saftig P (2010) The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex. J Neurosci 30:4833–4844

    Article  PubMed  CAS  Google Scholar 

  • Kohutek ZA, diPierro CG, Redpath GT, Hussaini IM (2009) ADAM-10-mediated N-cadherin cleavage is protein kinase C-alpha dependent and promotes glioblastoma cell migration. J Neurosci 29:4605–4615

    Article  PubMed  CAS  Google Scholar 

  • Kondoh H (1999) Transcription factors for lens development assessed in vivo. Curr Opin Genet Dev 9:301–308

    Article  PubMed  CAS  Google Scholar 

  • LaVoie MJ, Selkoe DJ (2003) The Notch ligands, Jagged and Delta, are sequentially processed by alpha-secretase and presenilin/gamma-secretase and release signaling fragments. J Biol Chem 278:34427–34437

    Article  PubMed  CAS  Google Scholar 

  • Le AC, Musil LS (2001) FGF signaling in chick lens development. Dev Biol 233:394–411

    Article  PubMed  CAS  Google Scholar 

  • Leong L, Menko AS, Grunwald GB (2000) Differential expression of N- and B-cadherin during lens development. Invest Ophthalmol Vis Sci 41:3503–3510

    PubMed  CAS  Google Scholar 

  • Lewis SL, Farlie PG, Newgreen DF (2004) Isolation and embryonic expression of avian ADAM 12 and ADAM 19. Gene Expr Patterns 5:75–79

    Article  PubMed  CAS  Google Scholar 

  • Li HS, Yang JM, Jacobson RD, Pasko D, Sundin O (1994) Pax-6 is first expressed in a region of ectoderm anterior to the early neural plate: implications of stepwise determination of the lens. Dev Biol 162:181–194

    Article  PubMed  CAS  Google Scholar 

  • Lieber T, Kidd S, Young MW (2002) Kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev 16:209–221

    Article  PubMed  CAS  Google Scholar 

  • Lin J, Redies C, Luo J (2007) Regionalized expression of ADAM13 during chicken embryonic development. Dev Dyn 236:862–870

    Article  PubMed  CAS  Google Scholar 

  • Lin J, Luo J, Redies C (2008) Differential expression of five members of ADAM family in the developing chicken brain. Neuroscience 157:360–375

    Article  PubMed  CAS  Google Scholar 

  • Lin J, Yan X, Markus A, Redies C, Rolfs A, Luo J (2010) Expression of seven members of the ADAM family in developing chicken spinal cord. Dev Dyn 239:1246–1254

    Article  PubMed  CAS  Google Scholar 

  • Lovicu FJ, McAvoy JW (2005) Growth factor regulation of lens development. Dev Biol 280:1–14

    Article  PubMed  CAS  Google Scholar 

  • Luo J, Treubert-Zimmermann U, Redies C (2004) Cadherins guide migrating Purkinje cells to specific parasagittal domains during cerebellar development. Mol Cell Neurosci 25:138–152

    Article  PubMed  CAS  Google Scholar 

  • Marcinkiewicz M, Seidah NG (2000) Coordinated expression of beta-amyloid precursor protein and the putative beta-secretase BACE and alpha-secretase ADAM10 in mouse and human brain. J Neurochem 75:2133–2143

    Article  PubMed  CAS  Google Scholar 

  • Maretzky T, Reiss K, Ludwig A, Buchholz J, Scholz F, Proksch E, de Strooper B, Hartmann D, Saftig P (2005) ADAM10 mediates E-cadherin shedding and regulates epithelial cell–cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci USA 102:9182–9187

    Article  PubMed  CAS  Google Scholar 

  • McCusker C, Cousin H, Neuner R, Alfandari D (2009) Extracellular cleavage of cadherin-11 by ADAM metalloproteases is essential for Xenopus cranial neural crest cell migration. Mol Biol Cell 20:78–89

    Article  PubMed  CAS  Google Scholar 

  • Neuner R, Cousin H, McCusker C, Coyne M, Alfandari D (2009) Xenopus ADAM19 is involved in neural, neural crest and muscle development. Mech Dev 126:240–255

    Article  PubMed  CAS  Google Scholar 

  • Pontoriero GF, Smith AN, Miller LA, Radice GL, West-Mays JA, Lang RA (2009) Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev Biol 326:403–417

    Article  PubMed  CAS  Google Scholar 

  • Rowan S, Conley KW, Le TT, Donner AL, Maas RL, Brown NL (2008) Notch signaling regulates growth and differentiation in the mammalian lens. Dev Biol 321:111–122

    Article  PubMed  CAS  Google Scholar 

  • Schäfer B, Marg B, Gschwind A, Ullrich A (2004) Distinct ADAM metalloproteinases regulate G protein-coupled receptor-induced cell proliferation and survival. J Biol Chem 279:47929–47938

    Article  PubMed  Google Scholar 

  • Shi W, Chen H, Sun J, Buckley S, Zhao J, Anderson KD, Williams RG, Warburton D (2003) TACE is required for fetal murine cardiac development and modeling. Dev Biol 261:371–380

    Article  PubMed  CAS  Google Scholar 

  • Smith AN, Miller LA, Song N, Taketo MM, Lang RA (2005) The duality of beta-catenin function: a requirement in lens morphogenesis and signalling suppression of lens fate in periocular ectoderm. Dev Biol 285:477–489

    Article  PubMed  CAS  Google Scholar 

  • Tholozan FM, Quinlan RA (2007) Lens cells: more than meets the eye. Int J Biochem Cell Biol 39:1754–1759

    Article  PubMed  CAS  Google Scholar 

  • Watabe-Uchida M, Masuda A, Shimada N, Endo M, Shimamura K, Yasuda K, Sehara-Fujisawa A (2004) Novel metalloprotease-disintegrin, meltrin epsilon (ADAM35), expressed in epithelial tissues during chick embryogenesis. Dev Dyn 230:557–568

    Article  PubMed  CAS  Google Scholar 

  • Wei S, Xu G, Bridges LC, Williams P, White JM, DeSimone DW (2010) ADAM13 induces cranial neural crest by cleaving class B Ephrins and regulating Wnt signaling. Dev Cell 19:345–352

    Article  PubMed  Google Scholar 

  • Xu L, Overbeek PA, Reneker LW (2002) Systematic analysis of E-, N- and P-cadherin expression in mouse eye development. Exp Eye Res 74:753–760

    Article  PubMed  CAS  Google Scholar 

  • Yagami-Hiromasa T, Sato T, Kurisaki T, Kamijo K, Nabeshima Y, Fujisawa-Sehara A (1995) A metalloprotease-disintegrin participating in myoblast fusion. Nature 377:652–656

    Article  PubMed  CAS  Google Scholar 

  • Yan X, Lin J, Wang H, Markus A, Wree A, Rolfs A, Luo J (2010) Regional expression of the ADAMs in developing chicken cochlea. Dev Dyn 239:2256–2265

    Article  PubMed  CAS  Google Scholar 

  • Yan X, Lin J, Markus A, Rolfs A, Luo J (2011) Regional expression of ADAM19 during chicken embryonic development. Dev Growth Differ 53:333–346

    Article  PubMed  CAS  Google Scholar 

  • Yang P, Baker KA, Hagg T (2006) The ADAMs family: coordinators of nervous system development, plasticity and repair. Prog Neurobiol 79:73–94

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Chen H, Wang YL, Warburton D (2001) Abrogation of tumor necrosis factor-alpha converting enzyme inhibits embryonic lung morphogenesis in culture. Int J Dev Biol 45:623–631

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. E. Mix from Department of Neurology, University of Rostock for critical reading of this manuscript. This work was supported by a grant from the German Research Foundation (DFG; LU1455/1-1) and by a fund from the National Natural Science Foundation of China (31000475).

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Authors and Affiliations

  1. Albrecht-Kossel-Institute for Neuroregeneration, School of Medicine University of Rostock, Gehlsheimer Strasse 20, 18147, Rostock, Germany

    Xin Yan, Arndt Rolfs & Jiankai Luo

  2. Institute of Anatomy I, School of Medicine University of Jena, Teichgraben 7, 07743, Jena, Germany

    Juntang Lin

  3. Department of Life Science and Technology, Xinxiang Medical University, Xinxiang, 453003, China

    Juntang Lin

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  1. Xin Yan
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Correspondence to Jiankai Luo.

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Xin Yan and Juntang Lin contributed equally to this work and should be considered co-first authors.

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Yan, X., Lin, J., Rolfs, A. et al. Expression patterns of ADAMs in the developing chicken lens. J Mol Hist 43, 121–135 (2012). https://doi.org/10.1007/s10735-011-9389-4

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  • DOI: https://doi.org/10.1007/s10735-011-9389-4

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