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Cellular and Molecular Biology Letters

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Volume 16, Issue 3 (Sep 2011)

Quantitative and dynamic expression profile of premature and active forms of the regional ADAM proteins during chicken brain development

Annett Markus
  • University of Rostock
  • Email:
/ Xin Yan
  • University of Rostock
  • Email:
/ Arndt Rolfs
  • University of Rostock
  • Email:
/ Jiankai Luo
  • University of Rostock
  • Email:
Published Online: 2011-07-23 | DOI: https://doi.org/10.2478/s11658-011-0016-x

Abstract

The ADAM (A Disintegrin and Metalloprotease) family of transmembrane proteins plays important roles in embryogenesis and tissue formation based on their multiple functional domains. In the present study, for the first time, the expression patterns of the premature and the active forms of six members of the ADAM proteins — ADAM9, ADAM10, ADAM12, ADAM17, ADAM22 and ADAM23 — in distinct parts of the developing chicken brain were investigated by quantitative Western blot analysis from embryonic incubation day (E) 10 to E20. The results show that the premature and the active forms of various ADAM proteins are spatiotemporally regulated in different parts of the brain during development, suggesting that the ADAMs play a very important role during embryonic development.

Keywords: ADAM; Gene expression; Protein; Brain development; Chicken

  • [1] Wolfsberg, T.G., Straight, P.D., Gerena, R.L., Huovila, A.P., Primakoff, P., Myles, D.G. and White, J.M. ADAM, a widely distributed and developmentally regulated gene family encoding membrane proteins with a disintegrin and metalloprotease domain. Dev. Biol. 169 (1995) 378–383. http://dx.doi.org/10.1006/dbio.1995.1152CrossrefGoogle Scholar

  • [2] Black, R.A. and White, J.M. ADAMs: focus on the protease domain. Curr. Opin. Cell Biol. 10 (1998) 654–659. http://dx.doi.org/10.1016/S0955-0674(98)80042-2CrossrefGoogle Scholar

  • [3] Schlöndorff, J. and Blobel, C.P. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J. Cell Sci. 112 (1999) 3603–3617. Google Scholar

  • [4] Edwards, D.R., Handsley, M.M. and Pennington, C.J. The ADAM metalloproteinases. Mol. Aspects. Med. 29 (2008) 258–289. http://dx.doi.org/10.1016/j.mam.2008.08.001CrossrefGoogle Scholar

  • [5] Seals, D.F. and Courtneidge, S.A. The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17 (2003) 7–30. http://dx.doi.org/10.1101/gad.1039703CrossrefGoogle Scholar

  • [6] White, J.M. ADAMs: modulators of cell-cell and cell-matrix interactions. Curr. Opin. Cell Biol. 15 (2003) 598–606. http://dx.doi.org/10.1016/j.ceb.2003.08.001CrossrefGoogle Scholar

  • [7] Duffy, M.J., Lynn, D.J., Lloyd, A.T. and O’shea, C.M. The ADAMs family of proteins: from basic studies to potential clinical applications. Thromb. Haemost. 89 (2003) 622–631. Google Scholar

  • [8] Blobel, C.P. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 6 (2005) 32–43. http://dx.doi.org/10.1038/nrm1548CrossrefGoogle Scholar

  • [9] Yang, P., Baker, K.A. and Hagg, T. The ADAMs family: coordinators of nervous system development, plasticity and repair. Prog. Neurobiol. 79 (2006) 73–94. http://dx.doi.org/10.1016/j.pneurobio.2006.05.001CrossrefGoogle Scholar

  • [10] Alfandari, D., McCusker, C. and Cousin, H. ADAM function in embryogenesis. Semin Cell Dev. Biol. 20 (2009) 153–163. http://dx.doi.org/10.1016/j.semcdb.2008.09.006CrossrefGoogle Scholar

  • [11] Neuner, R., Cousin, H., McCusker, C., Coyne, M. and Alfandari, D. Xenopus ADAM19 is involved in neural, neural crest and muscle development. Mech. Dev. 126 (2009) 240–255. http://dx.doi.org/10.1016/j.mod.2008.10.010CrossrefGoogle Scholar

  • [12] Hartmann, D., de Strooper, B., Serneels, L., Craessaerts, K., Herreman, A., Annaert, W., Umans, L., Lübke, T., Illert, A.L., von Figura, K. and Saftig, P. The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for a-secretase activity in fibroblasts. Hum. Mol. Gen. 11 (2002) 2615–2624. http://dx.doi.org/10.1093/hmg/11.21.2615CrossrefGoogle Scholar

  • [13] Horiuchi, K., Zhou, H.-M., Kelly, K., Manova, K. and Blobel, C.P. Evaluation of the contributions of ADAMs 9, 12, 15, 17, and 19 to heart development and ectodomain shedding of neuregulins β1 and β2. Dev. Biol. 283 (2005) 459–471. http://dx.doi.org/10.1016/j.ydbio.2005.05.004CrossrefGoogle Scholar

  • [14] Leighton, P.A., Mitchell, K.J., Goodrich, L.V., Lu, X., Pinson, K., Scherz, P., Skarnes, W.C. and Tessier-Lavigne, M. Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410 (2001) 174–179. http://dx.doi.org/10.1038/35065539CrossrefGoogle Scholar

  • [15] Sagane, K., Hayakawa, K., Kai, J., Hirohashi, T., Takahashi, E., Miyamoto, N., Ino, M., Oki, T., Yamazaki, K. and Nagasu, T. Ataxia and peripheral nerve hypomyelination in ADAM22-deficient mice. BMC Neurosci. 6 (2005) 33. http://dx.doi.org/10.1186/1471-2202-6-33CrossrefGoogle Scholar

  • [16] Lin, J., Luo, J. and Redies, C. Differential expression of five members of the ADAM family in the developing chicken brain. Neuroscience 157 (2008) 360–375. http://dx.doi.org/10.1016/j.neuroscience.2008.08.053CrossrefGoogle Scholar

  • [17] Lin, J., Yan, X., Markus, A., Redies, C., Rolfs, A. and Luo, J. Expression of seven members of the ADAM family in developing chicken spinal cord. Dev. Dyn. 239 (2010) 1246–1254. http://dx.doi.org/10.1002/dvdy.22272CrossrefGoogle Scholar

  • [18] Muraguchi, T., Takegami, Y., Ohtsuka, T., Kitajima, S., Chandana, E.P., Omura, A., Miki, T., Takahashi, R., Matsumoto, N., Ludwig, A., Noda, M. and Takahashi, C. RECK modulates Notch signaling during cortical neurogenesis by regulating ADAM10 activity. Nat. Neurosci. 10 (2007) 838–845. http://dx.doi.org/10.1038/nn1922CrossrefGoogle Scholar

  • [19] Murase, S., Cho, C., White, J.M. and Horwitz, A.F. ADAM2 promotes migration of neuroblasts in the rostral migratory stream to the olfactory bulb. Eur. J Neurosci. 27 (2008) 1585–1595. http://dx.doi.org/10.1111/j.1460-9568.2008.06119.xCrossrefGoogle Scholar

  • [20] Chen, Y.Y., Hehr, C.L., Atkinson-Leadbeater, K., Hocking, J.C. and MCFarlane, S. Targeting of retinal axons requires the metalloprotease ADAM10. J. Neurosci. 27 (2007) 8448–8456. http://dx.doi.org/10.1523/JNEUROSCI.1841-07.2007CrossrefGoogle Scholar

  • [21] Hoffrogge, R., Mikkat, S., Scharf, C., Beyer, S., Christoph, H., Pahnke, J., Mix, E., Berth, M., Uhrmacher, A., Zubrzycki, I., Miljan, E., Völker, U. and Rolfs, A. 2-DE proteome analysis of a proliferating and differentiating human neuronal stem cell line (ReNcell VM). Proteomics 6 (2006) 1833–1847. http://dx.doi.org/10.1002/pmic.200500556CrossrefGoogle Scholar

  • [22] Peters, S., Mix, E., Bauer, P., Weinelt, S., Schubert, B., Knoblich, R., Böttcher, T., Strauss, U., Pahnke, J., Cattaneo, E., Wree, A. and Rolfs, A. Wnt-5a expression in the rat neuronal progenitor cell line ST14A. Exp. Brain Res. 158 (2004) 189–195. http://dx.doi.org/10.1007/s00221-004-1887-0CrossrefGoogle Scholar

  • [23] Hotoda, N., Koike, H., Sasagawa, N. and Ishiuraa, S. A secreted form of human ADAM9 has an α-secretase activity for APP. Biochem. Biophys. Res. Commun. 293 (2002) 800–805. http://dx.doi.org/10.1016/S0006-291X(02)00302-9CrossrefGoogle Scholar

  • [24] Hall, R.J. and Erickson, C. ADAM10: an active metalloprotease expressed during avian epithelial morphogenesis. Dev. Biol. 256 (2003) 146–159. http://dx.doi.org/10.1016/S0012-1606(02)00133-1CrossrefGoogle Scholar

  • [25] Yagami-Hiromasa, T., Sato, T., Kurisaki, T., Kamijo, K., Nabeshima, Y. and Fujisawa-Sehara, A. A metalloprotease-disintegrin participating in myoblast fusion. Nature 377 (1995) 652–656. http://dx.doi.org/10.1038/377652a0CrossrefGoogle Scholar

  • [26] Moss, M.L., Sklair-Tavron, L. and Nudelman, R. Drug insight: tumor necrosis factor-converting enzyme as a pharmaceutical target for rheumatoid arthritis. Nat. Clin. Pract. Rheumatol. 4 (2008) 300–309. http://dx.doi.org/10.1038/ncprheum0797CrossrefGoogle Scholar

  • [27] Gonzales, P.E., Galli, J.D. and Milla, M.E. Identification of key sequence determinants for the inhibitory function of the prodomain of TACE. Biochemistry 47 (2008) 9911–9919. http://dx.doi.org/10.1021/bi801049vCrossrefGoogle Scholar

  • [28] Milla, M.E., Leesnitzer, M.A., Moss, M.L., Clay, W.C., Carter, H.L., Miller, A.B., Su, J.L., Lambert, M.H., Willard, D.H., Sheeley, D.M., Kost, T.A., Burkhart, W., Moyer, M., Blackburn, R.K., Pahel, G.L., Mitchell, J.L., Hoffman, C.R. and Becherer, J.D. Specific sequence elements are required for the expression of functional tumor necrosis factor-alpha-converting enzyme (TACE). J. Biol. Chem. 274 (1999) 30563–30570. http://dx.doi.org/10.1074/jbc.274.43.30563CrossrefGoogle Scholar

  • [29] Hougaard, S., Loechel, F., Xu, X., Tajima, R., Albrechtsen, R. and Wewer, U.M. Trafficking of human ADAM 12-L: retention in the trans-Golgi network. Biochem. Biophys. Res. Commun. 275 (2000) 261–267. http://dx.doi.org/10.1006/bbrc.2000.3295CrossrefGoogle Scholar

  • [30] Li, X., Yan, Y., Huang, W., Yang, Y., Wang, H. and Chang, L. The regulation of TACE catalytic function by its prodomain. Mol. Biol. Rep. 36 (2009) 641–651. http://dx.doi.org/10.1007/s11033-008-9224-5CrossrefGoogle Scholar

  • [31] Asai, M., Hattori, C., Szabó, B., Sasagawa, N., Maruyama, K., Tanuma, S. and Ishiura, S. Putative function of ADAM9, ADAM10, and ADAM17 as APP alpha-secretase. Biochem. Biophys. Res. Commun. 301 (2003) 231–235. http://dx.doi.org/10.1016/S0006-291X(02)02999-6CrossrefGoogle Scholar

  • [32] Roghani, M., Becherer, J.D., Moss, M.L., Atherton, R.E., Erdjument-Bromage, H., Arribas, J., Blackburn, R.K., Weskamp, G., Tempst, P. and Blobel, C.P. Metalloprotease-disintegrin MDC9: intracellular maturation and catalytic activity. J. Biol. Chem. 274 (1999) 3531–3540. http://dx.doi.org/10.1074/jbc.274.6.3531CrossrefGoogle Scholar

  • [33] Schwettmann, L. and Tschesche, H. Cloning and expression in Pichia pastoris of metalloprotease domain of ADAM 9 catalytically active against fibronectin. Protein Expr. Purif. 21 (2001) 65–70. http://dx.doi.org/10.1006/prep.2000.1374CrossrefGoogle Scholar

  • [34] Izumi, Y., Hirata, M., Hasuwa, H., Iwamoto, R., Umata, T., Miyado, K., Tamai, Y., Kurisaki, T., Sehara-Fujisawa, A., Ohno, S. and Mekada, E. A metalloprotease-disintegrin, MDC9/meltrin-gamma/ADAM9 and PKCdelta are involved in TPA-induced ectodomain shedding of membraneanchored heparin-binding EGF-like growth factor, EMBO J. 17 (1998) 7260–7272. http://dx.doi.org/10.1093/emboj/17.24.7260CrossrefGoogle Scholar

  • [35] Weskamp G., Cai, H., Brodie, T.A., Higashyama, S., Manova, K., Ludwig, T. and Blobel, C.P. Mice lacking the metalloprotease-disintegrin MDC9 (ADAM9) have no evident major abnormalities during development or adult life. Mol. Cell Biol. 22 (2002) 1537–1544. http://dx.doi.org/10.1128/MCB.22.5.1537-1544.2002CrossrefGoogle Scholar

  • [36] Nath, D., Slocombe, P.M., Webster, A., Stephens, P.E., Docherty, A.J. and Murphy, G. Meltrin gamma (ADAM-9) mediates cellular adhesion through alpha(6)beta(1)integrin, leading to a marked induction of fibroblast cell motility. J. Cell Sci. 113 (2000) 2319–2328. Google Scholar

  • [37] Zamenhof, S., Stimulation of brain development in chick embryo by elevated temperature. Roux Arch. Dev. Biol. 180 (1976) 1–8. http://dx.doi.org/10.1007/BF00848881CrossrefGoogle Scholar

  • [38] Hatta, K., Takagi, S., Fujisawa, H. and Takeichi, M. Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev. Biol. 120 (1987) 215–227. http://dx.doi.org/10.1016/0012-1606(87)90119-9CrossrefGoogle Scholar

  • [39] Pan, D. and Rubin, G.M. Kuzbanian controls proteolytic processing of Notch and mediated lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90 (1997) 271–280. http://dx.doi.org/10.1016/S0092-8674(00)80335-9CrossrefGoogle Scholar

  • [40] Fambrough, D., Pan, D., Rubin, G.M. and Goodman, C. The cell surface metalloprotease/disintegrin Kuzbanian is required for axonal extension in Drosophila. Proc. Natl. Acad. Sci. USA 93 (1996) 13233–13238. http://dx.doi.org/10.1073/pnas.93.23.13233CrossrefGoogle Scholar

  • [41] Rooke, J., Pan, D., Xu, T. and Rubin, G.M. KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science 273 (1996) 1227–1231. http://dx.doi.org/10.1126/science.273.5279.1227CrossrefGoogle Scholar

  • [42] Yan, Y., Shirakabe, K. and Werb, Z. The metalloprotease Kuzbanian (ADAM10) mediates the transactivation of EGF receptor by G proteincoupled receptors. J. Cell Biol. 158 (2002) 221–226. http://dx.doi.org/10.1083/jcb.200112026CrossrefGoogle Scholar

  • [43] Sahin, U. and Blobel, C.P. Ectodomian shedding of the EGF-receptor ligand epigen is mediated by ADAM17. FEBS Lett. 581 (2007) 41–44. http://dx.doi.org/10.1016/j.febslet.2006.11.074CrossrefGoogle Scholar

  • [44] Maretzky, T., Reiss, K., Ludwig, A., Buchholz, J., Scholz, F., Proksch, E., de Strooper, B., Hartmann, D. and Saftig, P. ADAM10 mediates Ecadherin shedding and regulates epithelial cell-cell adhesion, migration, and betacatenin translocation. Proc. Natl. Acad. Sci. USA 102 (2005) 9182–9187. http://dx.doi.org/10.1073/pnas.0500918102CrossrefGoogle Scholar

  • [45] Maretzky, T., Scholz, F., Köten, B., Proksch, E., Saftig, P. and Reiss, K. ADAM10-mediated E-cadherin release is regulated by proinflammatory cytokines and modulates keratinocyte cohesion in eczematous dermatitis. J. Invest. Dermatol. 128 (2008) 1737–1746. http://dx.doi.org/10.1038/sj.jid.5701242CrossrefGoogle Scholar

  • [46] Reiss, K., Maretzky, T., Ludwig, A., Tousseyn, T., de Strooper, B., Hartmann, D. and Saftig, P. ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and β-catenin nuclear signalling. EMBO J. 24 (2005) 742–752. http://dx.doi.org/10.1038/sj.emboj.7600548CrossrefGoogle Scholar

  • [47] Reiss, K., Maretzky, T., Haas, I.-G., Schulte, M., Ludwig, A., Frank, M. and Saftig, P. Regulated ADAM10-dependent ectodomain shedding of gamma-protocadherin C3 modulated cell-cell adhesion. J. Biol. Chem. 281 (2006) 21735–21744. http://dx.doi.org/10.1074/jbc.M602663200Google Scholar

  • [48] Schulz, B., Pruessmeyer, J., Maretzky, T., Ludwig, A., Blobel, C.P., Saftig, P. and Reiss, K. ADAM10 regulates endothelial permeability and T-cell transmigration by proteolysis of vascular endothelial cadherin. Circ. Res. 102 (2008) 1192–1201. http://dx.doi.org/10.1161/CIRCRESAHA.107.169805CrossrefGoogle Scholar

  • [49] Bernstein, H.G., Keilhoff, G., Bukowska, A., Ziegeler, A., Funke, S., Dobrowolny, H., Kanakis, D., Bogerts, B. and Lendeckel, U. ADAM (a disintegrin and metallo-protease) 12 is expressed in rat and human brain and localized to oligodendrocytes. J. Neurosci. Res. 75 (2004) 353–360. http://dx.doi.org/10.1002/jnr.10858CrossrefGoogle Scholar

  • [50] Gilpin, B.J., Loechel, F., Mattei, M.G., Engvall, E., Albrechtsen, R. and Wewer, U.M. A novel, secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo. J. Biol. Chem. 273 (1998) 157–166. http://dx.doi.org/10.1074/jbc.273.1.157CrossrefGoogle Scholar

  • [51] Galliano, M.F., Huet, C., Frygelius, J., Polgren, A., Wewer, U.M. and Engvall, E. Binding of ADAM12, a marker of skeletal muscle regeneration, to the muscle-specific actin-binding protein, alpha-actinin-2, is required for myoblast fusion. J. Biol. Chem. 275 (2000) 13933–13939. http://dx.doi.org/10.1074/jbc.275.18.13933CrossrefGoogle Scholar

  • [52] Black, R.A. Tumor necrosis factor-alpha converting enzyme. Int. J. Biochem. Cell Biol. 34 (2002) 1–5. http://dx.doi.org/10.1016/S1357-2725(01)00097-8CrossrefGoogle Scholar

  • [53] Zheng, Y., Saftig, P., Hartmann, D. and Blobel, C.P. Evaluation of the contribution of different ADAMs to TNFα shedding and of the function of the TNFα ectodomain in ensuring selective stimulated shedding by the TNFα convertase (TACE/ADAM17). J. Biol. Chem. 279 (2004) 42898–42906. http://dx.doi.org/10.1074/jbc.M403193200CrossrefGoogle Scholar

  • [54] Kenny, P.A. and Bissel, M.J. Targeting TACE-dependent EGFR-ligand shedding in breast cancer. J. Clinic. Invest. 117 (2007) 337–345. http://dx.doi.org/10.1172/JCI29518CrossrefGoogle Scholar

  • [55] Le Gall, S.M., Bobe, P., Reiss, K., Horiuchi, K., Niu, X.-D., Lundell, D., Gibb, D.R., Conrad, D., Saftig, P. and Blobel, C.P. ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins as transforming growth factor α, L-selectin, and tumor necrosis factor. Mol. Biol. Cell 20 (2009) 1785–1794. http://dx.doi.org/10.1091/mbc.E08-11-1135CrossrefGoogle Scholar

  • [56] Shah, B.H. and Catt, K.J. TACE-dependent EGF receptor activation in angiotensin-II-induced kidney disease. Trends Pharm. Sci. 27 (2006) 235–237. http://dx.doi.org/10.1016/j.tips.2006.03.010CrossrefGoogle Scholar

  • [57] Lautrette, A., Li, S., Alili, R., Sunnarborg, S.W., Burtin, M., Lee, D.C., Friedlander, G. and Terzi, F. Angiotensin II and EGF receptor cross-talk in chronic kidney diseases: a new therapeutic approach. Nat. Med. 11 (2005) 867–874. http://dx.doi.org/10.1038/nm1275CrossrefGoogle Scholar

  • [58] Sternlicht, M.D. and Sunnarborg, S.W. The ADAM17-amphiregulin-EGFR axis in mammary development and cancer. J. Mam. Gland. Bio. Neopla. 13 (2008) 181–194. http://dx.doi.org/10.1007/s10911-008-9084-6CrossrefGoogle Scholar

  • [59] Sagane, K., Ohya, Y., Hasegawa, Y. and Tanaka, I. Metalloproteinaselike, disintegrin-like, cysteine-rich proteins MDC2 and MDC3: novel human cellular disintegrins highly expressed in the brain. Biochem. J. 334 (1998) 93–98. Google Scholar

  • [60] Fukata, Y., Adesnik, H., Iwanaga, T., Bredt, D.S., Nicoll, R.A. and Fukata, M. Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science 313 (2006) 1792–1795. http://dx.doi.org/10.1126/science.1129947CrossrefGoogle Scholar

  • [61] Zhu, P., Sang, Y., Xu, H., Zhao, J., Xu R., Sun, Y., Xu, T., Wang, X., Chen, L., Feng, H., Li, C. and Zhao, S. ADAM22 plays an important role in cell adhesion and spreading with the assistance of 14-3-3. Biochem. Biophys. Res. Commun. 331 (2005) 938–946. http://dx.doi.org/10.1016/j.bbrc.2005.03.229CrossrefGoogle Scholar

  • [62] Sun, Y.P., Wang, Y., Zhang, J., Tao, J., Wang, C., Jing, N., Wu, C., Deng, K.J. and Qiao, S. ADAM23 plays multiple roles in neuronal differentiation of P19 embryonal carcinoma cells. Neurochem. Res. 32 (2007) 1217–1223. http://dx.doi.org/10.1007/s11064-007-9293-1CrossrefGoogle Scholar

  • [63] Sun, Y.P., Deng, K.J., Wang, F., Zhang, J., Huang, X., Qiao, S. and Zhao, S. Two novel isoforms of Adam23 expressed in the developmental process of mouse and human brains. Gene 325 (2004) 171–178. http://dx.doi.org/10.1016/j.gene.2003.10.012CrossrefGoogle Scholar

About the article

Published Online: 2011-07-23

Published in Print: 2011-09-01


Citation Information: Cellular and Molecular Biology Letters, ISSN (Online) 1689-1392, DOI: https://doi.org/10.2478/s11658-011-0016-x.

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