Diversity and evolution of the thyroglobulin type-1 domain superfamily

Molecular Biology and Evolution

Volumn 23, Issue 4, 2006, Pages 744-755

  Novinec, Marko ^a   Kordiš, Dušan ^a   Turk, Vito ^a   Lenarčič, Brigita ^a,b  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Evolution; Metazoa; Protein module; Thyroglobulin type 1 domain

Indexed keywords

CALCIUM; CYSTEINE; ENTACTIN; ENZYME INHIBITOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN; SOMATOMEDIN BINDING PROTEIN; THYROGLOBULIN; THYROTROPIN;

AMINO ACID SEQUENCE; ARTICLE; CALCIUM BINDING; CONTROLLED STUDY; DATA BASE; EVOLUTION; EXPRESSED SEQUENCE TAG; GENE DUPLICATION; GENOME; HUMAN; INTERVERTEBRAL DISK HERNIA; METAZOON; NONHUMAN; PHYLOGENY; PROTEIN EXPRESSION; PROTEIN STRUCTURE; UROCHORDATA; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENETIC VARIATION; HUMANS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PROTEIN STRUCTURE, TERTIARY; THYROGLOBULIN; VARIATION (GENETICS);

ANIMALIA; INVERTEBRATA; METAZOA; UROCHORDATA; VERTEBRATA;

EID: 33644889933     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msj082     Document Type: Article

References (51)

1. Bevec, T., V. Stoka, G. Pungerčič, I. Dolenc, and V. Turk. 1996. Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. J. Exp. Med. 183:1331-1338.
2. Bocock, J. P., C. J. Edgell, H. S. Marr, and A. H. Erickson. 2003. Human proteoglycan testican-1 inhibits the lysosomal cysteine protease cathepsin L. Eur. J. Biochem. 270:4008-4015.
3. Burge, C., and S. Karlin. 1997. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268:78-94.
4. Chiva, C., P. Barthe, A. Codina et al. (14 co-authors). 2003. Synthesis and NMR structure of p41icf, a potent inhibitor of human cathepsin L. J. Am. Chem. Soc. 125:1508-1517.
5. Erickson, A. C., and J. R. Couchman. 2000. Still more complexity in mammalian basement membranes. J. Histochem. Cytochem. 48:1291-1306.
6. Felsenstein, J. 1989. PHYLIP - phylogeny inference package (version 3.2). Cladistics 5:164-166.
7. Fowlkes, J. L., K. M. Thrailkill, C. George-Nascimento, C. K. Rosenberg, and D. M. Serra. 1997. Heparin-binding, highly basic regions within the thyroglobulin type-1 repeat of insulin-like growth factor (IGF)-binding proteins (IGFBPs) -3, -5, and -6 inhibit IGFBP-4 degradation. Endocrinology 138:2280-2285.
8. Galeša, K., R. Pain, M. A. Jongsma, V. Turk, and B. Lenarčič. 2003. Structural characterization of thyroglobulin type-1 domains of equistatin. FEBS Lett. 539:120-124.
9. Galtier, N., M. Gouy, and C. Gautier. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:543-548.
10. Grasberger, B. L., G. M. Clore, and A. M. Gronenborn. 1994. High-resolution structure of Ascaris trypsin inhibitor in solution: direct evidence for a pH-induced conformational transition in the reactive site. Structure 2:669-678.
11. Guillemot, J. C., M. Naspetti, F. Malergue, P. Montcourrier, F. Galland, and P. Naquet. 2001. Ep-CAM transfection in thymic epithelial cell lines triggers the formation of dynamic actin-rich protrusions involved in the organization of epithelial cell layers. Histochem. Cell Biol. 116:371-378.
12. Gunčar, G., G. Pungerčič, I. Klemenčič , V. Turk, and D. Turk. 1999. Crystal structure of MHC class II-associated p41 Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J. 18: 793-803.
13. Hazkani-Covo, E., E. Y. Levanon, G. Rotman, D. Graur, and A. Novik. 2004. Evolution of multicellularity in Metazoa: comparative analysis of the subcellular localization of proteins in Saccharomyces, Drosophila and Caenorhabditis. Cell Biol. Int. 28:171-178.
14. Headey, S. J., D. W. Keizer, S. Yao, G. Brasier, P. Kantharidis, L. A. Bach, and R. S. Norton. 2004. C-terminal domain of insulin-like growth factor (IGF) binding protein-6: structure and interaction with IGF-II. Mol. Endocrinol. 18:2740-2750.
15. Hennighausen, L. G., and A. E. Sippel. 1982. Mouse whey acidic protein is a novel member of the family of 'four-disulfide core' proteins. Nucleic Acids Res. 10:2677-2684.
16. Hwa, V., Y. Oh, and R. G. Rosenfeld. 1999a. Insulin-like growth factor binding proteins: a proposed superfamily. Acta Paediatr. Suppl. 88:37-45.
17. _. 1999b. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 20:761-787.
18. Kortschak, R. D., G. Samuel, R. Saint, and D. J. Miller. 2003. EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol. 13:2190-2195.
19. Lamas, L., P. C. Anderson, J. W. Fox, and J. T. Dunn. 1989. Consensus sequences for early iodination and hormonogenesis in human thyroglobulin. J. Biol. Chem. 264:13541-13545.
20. Laskowski, M. Jr. 1986. Protein inhibitors of serine proteinases - mechanism and classification. Adv. Exp. Med. Biol. 199:1-17.
21. Lee, M., and H. T. Cheung. 1996. Isolation and characterization of Caenorhabditis elegans extracellular matrix. Biochem. Biophys. Res. Commun. 221:503-509.
22. Lenarčič, B., and T. Bevec. 1998. Thyropins - new structurally related proteinase inhibitors. Biol. Chem. 379:105-111.
23. Lenarčič, B., G. Krishnan, R. Borukhovich, B. Ruck, V. Turk, and E. Moczydlowski. 2000. Saxiphilin, a saxitoxin-binding protein with two thyroglobulin type 1 domains, is an inhibitor of papain-like cysteine proteinases. J. Biol. Chem. 275:15572-15577.
24. Lenarčič, B., and V. Turk. 1999. Thyroglobulin type-1 domains in equistatin inhibit both papain-like cysteine proteinases and cathepsin D. J. Biol. Chem. 274:563-566.
25. Li, Y., and E. Moczydlowski. 1991. Purification and partial sequencing of saxiphilin, a saxitoxin-binding protein from the bullfrog, reveals homology to transferrin. J. Biol. Chem. 266:15481-15487.
26. Litvinov, S. V., M. Balzar, M. J. Winter, H. A. Bakker, I. H. Briaire-de Bruijn, F. Prins, G. J. Fleuren, and S. O. Warnaar. 1997. Epithelial cell adhesion molecule (Ep-CAM) modulates cell-cell interactions mediated by classic cadherins. J. Cell. Biol. 139:1337-1348.
27. Mahar, J., G. L. Lukacs, Y. Li, S. Hall, and E. Moczydlowski. 1991. Pharmacological and biochemical properties of saxiphilin, a soluble saxitoxin-binding protein from the bullfrog (Rana catesbeiana). Toxicon 29:53-71.
28. Marr, H. S., and C. J. Edgell. 2003. Testican-1 inhibits attachment of Neuro-2a cells. Matrix Biol. 22:259-266.
29. Meh, P., M. Pavšič, V. Turk, A. Baici, and B. Lenarčič. 2005. Dual concentration-dependent activity of thyroglobulin type-1 domain of testican: specific inhibitor and substrate of cathepsin L. Biol. Chem. 386:75-83.
30. Mercken, L., M. J. Simons, S. Swillens, M. Massaer, and G. Vassart. 1985. Primary structure of bovine thyroglobulin deduced from the sequence of its 8,431-base complementary DNA. Nature 316:647-651.
31. Molina, F., M. Bouanani, B. Pau, and C. Granier. 1996. Characterization of the type-1 repeat from thyroglobulin, a cysteine-rich module found in proteins from different families. Eur. J. Biochem. 240:125-133.
32. Murzin, A. G., S. E. Brenner, T. Hubbard, and C. Chothia. 1995. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247: 536-540.
33. Nakada, M., H. Miyamori, J. Yamashita, and H. Sato. 2003. Testican 2 abrogates inhibition of membrane-type matrix metalloproteinases by other testican family proteins. Cancer Res. 63:3364-3369.
34. Nakada, M., A. Yamada, T. Takino, H. Miyamori, T. Takahashi, J. Yamashita, and H. Sato. 2001. Suppression of membrane-type 1 matrix metalloproteinase (MMP)-mediated MMP-2 activation and tumor invasion by testican 3 and its splicing variant gene product, N-Tes. Cancer Res. 61:8896-8902.
35. Nakae, H., M. Sugano, Y. Ishimori, T. Endo, and T. Obinata. 1993. Ascidian entactin/nidogen. Implication of evolution by shuffling two kinds of cysteine-rich motifs. Eur. J. Biochem. 213:11-19.
36. Parma, J., D. Christophe, V. Pohl, and G. Vassart. 1987. Structural organization of the 5′ region of the thyroglobulin gene. Evidence for intron loss and "exonization" during evolution. J. Mol. Biol. 196:769-779.
37. Patthy, L. 2003. Modular assembly of genes and the evolution of new functions. Genetica 118:217-231.
38. Pungerčič, G., I. Dolenc, M. Dolinar, T. Bevec, S. Jenko, S. Kolarič, and V. Turk. 2002. Individual recombinant thyroglobulin type-1 domains are substrates for lysosomal cysteine proteinases. Biol. Chem. 383:1809-1812.
39. Raible, F., and D. Arendt. 2004. Metazoan evolution: some animals are more equal than others. Curr. Biol. 14:R106-R108.
40. Rawlings, N. D., D. P. Tolle, and A. J. Barrett. 2004. Evolutionary families of peptidase inhibitors. Biochem. J. 378:705-716.
41. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
42. Schnepp, A., P. Komp Lindgren, H. Hulsmann, S. Kroger, M. Paulsson, and U. Hartmann. 2005. Mouse testican-2. Expression, glycosylation, and effects on neurite outgrowth. J. Biol. Chem. 280:11274-11280.
43. Stumptner-Cuvelette, P., and P. Benaroch. 2002. Multiple roles of the invariant chain in MHC class II function. Biochim. Biophys. Acta 1542:1-13.
44. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
45. Upton, Z., S. J. Chan, D. F. Steiner, J. C. Wallace, and F. J. Ballard. 1993. Evolution of insulin-like growth factor binding proteins. Growth Regul. 3:29-32.
46. Vannahme, C., S. Gosling, M. Paulsson, P. Maurer, and U. Hartmann. 2003. Characterization of SMOC-2, a modular extracellular calcium-binding protein. Biochem. J. 373:805-814.
47. Vannahme, C., N. Smyth, N. Miosge, S. Gosling, C. Frie, M. Paulsson, P. Maurer, and U. Hartmann. 2002. Characterization of SMOC-1, a novel modular calcium-binding protein in basement membranes. J. Biol. Chem. 277:37977-37986.
48. Veerassamy, S., A. Smith, and E. R. Tillier. 2003. A transition probability model for amino acid substitutions from blocks. J. Comput. Biol. 10:997-1010.
49. Vogel, C., M. Bashton, N. D. Kerrison, C. Chothia, and S. A. Teichmann. 2004a. Structure, function and evolution of multidomain proteins. Curr. Opin. Struct. Biol. 14:208-216.
50. Vogel, C., C. Berzuini, M. Bashton, J. Gough, and S. A. Teichmann. 2004b. Supra-domains: evolutionary units larger than single protein domains. J. Mol. Biol. 336:809-823.
51. Yamashita, M., and S. Konagaya. 1996. A novel cysteine protease inhibitor of the egg of chum salmon, containing a cysteine-rich thyroglobulin-like motif. J. Biol. Chem. 271: 1282-1284.