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

Cellular and Molecular Biology Letters

Volumn 16, Issue 3, 2011, Pages 431-451

  Markus, Annett ^a   Yan, Xin ^a   Rolfs, Arndt ^a   Luo, Jiankai ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

ADAM; Brain development; Chicken; Gene expression; Protein

Indexed keywords

ADAM PROTEIN; ADAM10 ENDOPEPTIDASE; ADAM12 PROTEIN; ADAM17 PROTEIN; ADAM22 PROTEIN; ADAM23 PROTEIN; ADAM9 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BRAIN DEVELOPMENT; CHICKEN; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE EXPRESSION PROFILING; INCUBATION TIME; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROBLEM IDENTIFICATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 80052497044     PISSN: 14258153     EISSN: 16891392     Source Type: Journal    
DOI: 10.2478/s11658-011-0016-x     Document Type: Article

References (63)

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.
2. Black, R. A. and White, J. M. ADAMs: focus on the protease domain. Curr. Opin. Cell Biol. 10 (1998) 654-659.
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.
4. Edwards, D. R., Handsley, M. M. and Pennington, C. J. The ADAM metalloproteinases. Mol. Aspects. Med. 29 (2008) 258-289.
5. Seals, D. F. and Courtneidge, S. A. The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17 (2003) 7-30.
6. White, J. M. ADAMs: modulators of cell-cell and cell-matrix interactions. Curr. Opin. Cell Biol. 15 (2003) 598-606.
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.
8. Blobel, C. P. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 6 (2005) 32-43.
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.
10. Alfandari, D., McCusker, C. and Cousin, H. ADAM function in embryogenesis. Semin Cell Dev. Biol. 20 (2009) 153-163.
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.
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.
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.
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. Nature410 (2001) 174-179.
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.
16. Lin, J., Luo, J. and Redies, C. Differential expression of five members of the ADAM family in the developing chicken brain. Neuroscience157 (2008) 360-375.
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.
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.
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.
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.
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). Proteomics6 (2006) 1833-1847.
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.
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.
24. Hall, R. J. and Erickson, C. ADAM10: an active metalloprotease expressed during avian epithelial morphogenesis. Dev. Biol. 256 (2003) 146-159.
25. Yagami-Hiromasa, T., Sato, T., Kurisaki, T., Kamijo, K., Nabeshima, Y. and Fujisawa-Sehara, A. A metalloprotease-disintegrin participating in myoblast fusion. Nature377 (1995) 652-656.
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.
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. Biochemistry47 (2008) 9911-9919.
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.
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.
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.
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.
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.
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.
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.
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.
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.
37. Zamenhof, S., Stimulation of brain development in chick embryo by elevated temperature. Roux Arch. Dev. Biol. 180 (1976) 1-8.
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.
39. Pan, D. and Rubin, G. M. Kuzbanian controls proteolytic processing of Notch and mediated lateral inhibition during Drosophila and vertebrate neurogenesis. Cell90 (1997) 271-280.
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. USA93 (1996) 13233-13238.
41. Rooke, J., Pan, D., Xu, T. and Rubin, G. M. KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science273 (1996) 1227-1231.
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.
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.
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. USA102 (2005) 9182-9187.
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.
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.
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.
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.
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.
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.
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.
52. Black, R. A. Tumor necrosis factor-alpha converting enzyme. Int. J. Biochem. Cell Biol. 34 (2002) 1-5.
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.
54. Kenny, P. A. and Bissel, M. J. Targeting TACE-dependent EGFR-ligand shedding in breast cancer. J. Clinic. Invest. 117 (2007) 337-345.
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. Cell20 (2009) 1785-1794.
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.
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.
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.
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.
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. Science313 (2006) 1792-1795.
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.
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.
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. Gene325 (2004) 171-178.