The NC1 dimer of human placental basement membrane collagen IV: does a covalent crosslink exist?
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Manuel E. Than
Abstract
Triple-helical collagen IV protomers associate through their N- and C-termini, forming a three-dimensional network that provides basement membranes with mechanical strength. Within this network, the C-terminal non-collagenous (NC1) domains form tight dimeric junctions. Crystallographic analyses of isolated NC1 domains show two trimeric cap-like structures interacting via a large interface. Previously, for NC1 from human placenta type-IV collagen we described covalent α1-α1 and α2-α2 crosslinks between Met93 and Lys211 of opposing α1(IV) and α2(IV) NC1-chains, which further stabilize this interface and explain the occurrence of reduction-insensitive NC1-chain dimers. However, their existence was recently questioned, and we therefore analyzed NC1-domain dimers in more detail by biochemical and protein crystallographic methods. Short-exposure diffraction data show a clear electron density cross-connecting the respective residues, which gradually disappears with prolonged crystal irradiation. Sequence analyses of isolated tryptic peptides derived from denatured NC1 monomers and dimers indicate that only the dimers, but not the monomers, yield these chemically labile cross-linked peptides. These data clearly demonstrate the presence of reduction-resistant, but chemically and radiation-sensitive covalent crosslinks between the side chains of Met93 and Lys211 in human placenta type-IV collagen.
References
Borza, D.B., Bondar, O., Ninomiya, Y., Sado, Y., Naito, I., Todd, P., and Hudson, B.G. (2001). The NC1 domain of collagen IV encodes a novel network composed of the α1, α2, α5, and α6 chains in smooth muscle basement membranes. J. Biol. Chem.276, 28532–28540.10.1074/jbc.M103690200Suche in Google Scholar
Boutaud, A., Borza, D.B., Bondar, O., Gunwar, S., Netzer, K.O., Singh, N., Ninomiya, Y, Sado, Y., Noelken, M.E., and Hudson, B.G. (2000). Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J. Biol. Chem.275, 30716–30724.10.1074/jbc.M004569200Suche in Google Scholar
Burmeister, W.P. (2000). Structural changes in a cryo-cooled protein crystal owing to radiation damage. Acta Crystallogr.D56, 328–341.10.1107/S0907444999016261Suche in Google Scholar
Collaborative Computational Project Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760–763.10.1107/S0907444994003112Suche in Google Scholar
Esnouf, R.M. (1999). Further additions to Molscript version 1.4, including reading and contouring of electron density maps. Acta Crystallogr.D55, 938–940.Suche in Google Scholar
Fowler, S.J., Jose, S., Zhang, X., Deutzmann, R., Sarras, M.P. Jr., and Boot-Handford, R.P. (2000). Characterization of Hydra type IV collagen. J. Biol. Chem.275, 39589–39599.10.1074/jbc.M005871200Suche in Google Scholar
Gunčar, G., Podobnik, M., Pungerčar, J., Štrukelj, B., Turk, V., and Turk, D. (1998). Crystal structure of porcine cathepsin H determined at 2.1 Å resolution: location of the mini-chain C-terminal carboxyl group defines cathepsin H aminopeptidase function. Structure15, 51–61.Suche in Google Scholar
Hudson, B.G., Reeders, S.T., and Tryggvason, K. (1993). Type IV collagen: structure, gene organization, and role in human diseases. J. Biol. Chem.268, 26033–26036.10.1016/S0021-9258(19)74270-7Suche in Google Scholar
Hudson, B.G., Tryggvason, K., Sundaramoorthy, M., and Neilson, E.G. (2003). Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N. Engl. J. Med.348, 2543–2555.10.1056/NEJMra022296Suche in Google Scholar PubMed
Kalluri, R. (2003). Basement membranes: structure, assembly and role in tumor angiogenesis. Nat. Rev. Cancer3, 422–433.10.1038/nrc1094Suche in Google Scholar PubMed
Kühn, K. (1994). Basement membrane (type IV) collagen. Matrix Biol.14, 439–445.Suche in Google Scholar
Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr.24, 946–950.10.1107/S0021889891004399Suche in Google Scholar
Mann, K., Gaill, F., and Timpl, R. (1992). Amino acid sequence and cell-adhesion activity of a fibril-forming collagen from the tube worm Riftia pachyptila living at deep sea hydrothermal vents. Eur. J. Biochem.210, 839–847.10.1111/j.1432-1033.1992.tb17487.xSuche in Google Scholar PubMed
Merrit, E.A. and Bacon, D.J. (1997). Raster3D: photorealistic molecular graphics. Methods Enzymol.277, 505–524.10.1016/S0076-6879(97)77028-9Suche in Google Scholar
Otwinowski, Z. and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillations mode. Methods Enzymol.276, 307–326.10.1016/S0076-6879(97)76066-XSuche in Google Scholar
Petitclerc, E., Boutaud, A., Prestayko, A., Xu, J., Sado, Y., Ninomiya, Y., Sarras, M.P. Jr, Hudson, B.G., and Brooks, P.C. (2000). New functions for non-collagenous domains of human collagen type IV. Novel integrin ligands inhibiting angiogenesis and tumor growth in vivo. J. Biol. Chem.275, 8051–8061.10.1074/jbc.275.11.8051Suche in Google Scholar
Ravelli, R.B.G. and McSweeney S.M. (2000). The ‘fingerprint’ that X-rays can leave on structures. Structure8, 315–328.10.1016/S0969-2126(00)00109-XSuche in Google Scholar
Ries, A., Engel, J., Lustig, A., and Kühn, K. (1995). The function of the NC1 domains in type IV collagen. J. Biol. Chem.270, 23790–23794.10.1074/jbc.270.40.23790Suche in Google Scholar PubMed
Siebold, B., Deutzmann, R., and Kühn, K. (1988). The arrangement of intra- and intermolecular disulfide bonds in the carboxyterminal, non-collagenous aggregation and cross-linking domain of basement-membrane type IV collagen. Eur. J. Biochem.176, 617–624.10.1111/j.1432-1033.1988.tb14321.xSuche in Google Scholar PubMed
Sundaramoorthy, M., Meiyappan, M., Todd, P., and Hudson, B.G. (2002). Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes. J. Biol. Chem.277, 31142–31153.10.1074/jbc.M201740200Suche in Google Scholar PubMed
Than, M.E., Henrich, S., Huber, R., Ries, A., Mann, K., Kühn, K., Timpl, R., Bourenkov, G.P., Bartunik, H.D., and Bode, W. (2002). The 1.9-Å crystal structure of the noncollagenous (NC1) domain of human placenta collagen IV shows stabilization via a novel type of covalent Met-Lys cross-link. Proc. Natl. Acad. Sci. USA99, 6607–6612.Suche in Google Scholar
Turk, D. (1992). Weiterentwicklung eines Programms für Molekülgraphik und Elektrondichte-Manipulation und seine Anwendung auf verschiedene Protein-Strukturaufklärungen. PhD thesis, Technische Universität München, Germany.Suche in Google Scholar
Vanacore, R.M., Shanmugasundararaj, S., Friedman, D.B., Bondar, O., Hudson, B.G., and Sundaramoorthy, M. (2004). The α1α2 network of collagen IV: reinforced stabilization of the noncollagenous domain-1 by noncovalent forces and the absence of Met-Lys crosslinks. J. Biol. Chem.279, 44723–44730.10.1074/jbc.M406344200Suche in Google Scholar PubMed
Weber, S., Engel, J., Wiedemann, H., Glanville, R.W., and Timpl, R. (1984). Subunit structure and assembly of globular domain of basement-membrane collagen type IV. Eur. J. Biochem.139, 401–410.10.1111/j.1432-1033.1984.tb08019.xSuche in Google Scholar PubMed
Yurchenco, P.D., Amenta, P.S., and Patton, B.L. (2004). Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol.22, 521–538.10.1016/j.matbio.2003.10.006Suche in Google Scholar PubMed
©2005 by Walter de Gruyter Berlin New York
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- Highlight: Molecular Machines
- Splicing of a rare class of introns by the U12-dependent spliceosome
- Proteasome-associated proteins: regulation of a proteolytic machine
- Novel insights into the mechanism of chaperone-assisted protein disaggregation
- Dynamic chromatin: concerted nucleosome remodelling and acetylation
- Efficient production of native actin upon translation in a bacterial lysate supplemented with the eukaryotic chaperonin TRiC
- The NC1 dimer of human placental basement membrane collagen IV: does a covalent crosslink exist?
- Intact growth factors are conserved in the extracellular matrix of ancient human bone and teeth: a storehouse for the study of human evolution in health and disease
- Differential accumulation of plastid preprotein translocon components during spruce (Picea abies L. Karst.) needle development
- Hypothyroidism induces expression of the peptide transporter PEPT2
- The precursor of secreted aspartic proteinase Sapp1p from Candida parapsilosis can be activated both autocatalytically and by a membrane-bound processing proteinase
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