Crystal structure of human collagen XVIII trimerization domain: A novel collagen trimerization Fold.

Collagens contain a unique triple-helical structure with a repeating sequence -G-X-Y-, where proline and hydroxyproline are major constituents in X and Y positions, respectively. Folding of the collagen triple helix requires trimerization domains. Once trimerized, collagen chains are correctly aligned and the folding of the triple helix proceeds in a zipper-like fashion. Here we report the isolation, characterization, and crystal structure of the trimerization domain of human type XVIII collagen, a member of the multiplexin family. This domain differs from all other known trimerization domains in other collagens and exhibits a high trimerization potential at picomolar concentrations. Strong chain association and high specificity of binding are needed for multiplexins, which are present at very low levels.

[1]  W. Halfter,et al.  Collagen XVIII Is a Basement Membrane Heparan Sulfate Proteoglycan* , 1998, The Journal of Biological Chemistry.

[2]  Y. Muragaki,et al.  Identification of a novel collagen chain represented by extensive interruptions in the triple-helical region. , 1993, Biochemical and biophysical research communications.

[3]  R J Read,et al.  Crystallography & NMR system: A new software suite for macromolecular structure determination. , 1998, Acta crystallographica. Section D, Biological crystallography.

[4]  A. Ooshima,et al.  Isolation and sequencing of cDNAs for proteins with multiple domains of Gly-Xaa-Yaa repeats identify a distinct family of collagenous proteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[5]  J. Weisel,et al.  The molecular structure of human tissue type XV presents a unique conformation among the collagens. , 2007, The Biochemical journal.

[6]  S. Sheriff,et al.  Human mannose-binding protein carbohydrate recognition domain trimerizes through a triple α-helical coiled-coil , 1994, Nature Structural Biology.

[7]  J. Ferretti,et al.  Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity , 1995, Infection and immunity.

[8]  C. Pace,et al.  Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding , 1995, Protein science : a publication of the Protein Society.

[9]  William Arbuthnot Sir Lane,et al.  Endostatin: An Endogenous Inhibitor of Angiogenesis and Tumor Growth , 1997, Cell.

[10]  Damien Ficheux,et al.  α-Helical Coiled-coil Oligomerization Domains Are Almost Ubiquitous in the Collagen Superfamily* , 2003, Journal of Biological Chemistry.

[11]  J. Myers,et al.  COOH-terminal propeptides of the major human procollagens. Structural, functional and genetic comparisons. , 1987, Journal of molecular biology.

[12]  J. Myers,et al.  Basement Membrane Zone Type XV Collagen Is a Disulfide-bonded Chondroitin Sulfate Proteoglycan in Human Tissues and Cultured Cells* , 2000, The Journal of Biological Chemistry.

[13]  W. Weis,et al.  Trimeric structure of a C-type mannose-binding protein. , 1994, Structure.

[14]  N. Bulleid,et al.  The role of cysteine residues in the folding and association of the COOH-terminal propeptide of types I and III procollagen. , 1994, The Journal of biological chemistry.

[15]  G. Garcı́a-Cardeña,et al.  Oligomerization-Dependent Regulation of Motility and Morphogenesis by the Collagen Xviii Nc1/Endostatin Domain , 2001, The Journal of cell biology.

[16]  The C-terminus of the P22 tailspike protein acts as an independent oligomerization domain for monomeric proteins. , 2009, The Biochemical journal.

[17]  R. Kammerer,et al.  Collagen stabilization at atomic level: crystal structure of designed (GlyProPro)10foldon. , 2003, Structure.

[18]  C. Pace.  Determination and analysis of urea and guanidine hydrochloride denaturation curves. , 1986, Methods in enzymology.

[19]  T. Pihlajaniemi,et al.  Primary structure of the alpha 1 chain of mouse type XVIII collagen, partial structure of the corresponding gene, and comparison of the alpha 1(XVIII) chain with its homologue, the alpha 1(XV) collagen chain. , 1994, The Journal of biological chemistry.

[20]  V. Sukhatme,et al.  Endostatin Induces Endothelial Cell Apoptosis* , 1999, The Journal of Biological Chemistry.

[21]  S. Grzesiek,et al.  Very fast folding and association of a trimerization domain from bacteriophage T4 fibritin. , 2004, Journal of molecular biology.

[22]  R. Timpl,et al.  Chain assembly intermediate in the biosynthesis of type III procollagen in chick embryo blood vessels. , 1981, The Journal of biological chemistry.

[23]  Kevin Cowtan,et al.  research papers Acta Crystallographica Section D Biological , 2005 .

[24]  Pace Cn,et al.  Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and beta-lactoglobulin. , 1974, The Journal of biological chemistry.

[25]  I Que,et al.  Endostatin inhibits VEGF‐induced endothelial cell migration and tumor growth independently of zinc binding , 1999, The EMBO journal.

[26]  L. Fessler,et al.  Protein assembly of procollagen and effects of hydroxylation. , 1974, The Journal of biological chemistry.

[27]  S. Steinbacher,et al.  Crystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer. , 1994, Science.

[28]  R. Timpl,et al.  Structure, function and tissue forms of the C‐terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin , 1998, The EMBO journal.

[29]  T. Pihlajaniemi,et al.  Alpha 1(XVIII), a collagen chain with frequent interruptions in the collagenous sequence, a distinct tissue distribution, and homology with type XV collagen. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Engel,et al.  Trimerization and Triple Helix Stabilization of the Collagen XIX NC2 Domain* , 2008, Journal of Biological Chemistry.

[31]  J. Engel,et al.  Collagen triple-helix formation in all-trans chains proceeds by a nucleation/growth mechanism with a purely entropic barrier. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Seckler,et al.  Structure of the Receptor-Binding Protein of Bacteriophage Det7: a Podoviral Tail Spike in a Myovirus , 2007, Journal of Virology.

[33]  B. Hudson,et al.  Crystal Structure of NC1 Domains , 2002, The Journal of Biological Chemistry.

[34]  Randy J Read,et al.  Electronic Reprint Biological Crystallography Phenix: Building New Software for Automated Crystallographic Structure Determination Biological Crystallography Phenix: Building New Software for Automated Crystallographic Structure Determination , 2022 .

[35]  T. Pihlajaniemi,et al.  Complete primary structure of two variant forms of human type XVIII collagen and tissue-specific differences in the expression of the corresponding transcripts. , 1998, Matrix biology : journal of the International Society for Matrix Biology.

[36]  P. Barlow,et al.  A parallel three stranded α‐helical bundle at the nucleation site of collagen triple‐helix formation , 1994, FEBS letters.

[37]  K. Kivirikko,et al.  Assembly of Stable Human Type I and III Collagen Molecules from Hydroxylated Recombinant Chains in the Yeast Pichia pastoris , 2003, Journal of Biological Chemistry.

[38]  J. Engel,et al.  Structure formation in the C terminus of type III collagen guides disulfide cross-linking. , 2004, Journal of molecular biology.

[39]  R. Kammerer,et al.  Stabilization of short collagen-like triple helices by protein engineering. , 2001, Journal of molecular biology.

[40]  J. Folkman,et al.  Antiangiogenesis in cancer therapy--endostatin and its mechanisms of action. , 2006, Experimental cell research.

[41]  B. Hudson,et al.  Molecular Recognition in the Assembly of Collagens: Terminal Noncollagenous Domains Are Key Recognition Modules in the Formation of Triple Helical Protomers* , 2006, Journal of Biological Chemistry.

[42]  Robert Huber,et al.  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 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[43]  D. Parry,et al.  Fifty years of coiled-coils and alpha-helical bundles: a close relationship between sequence and structure. , 2008, Journal of structural biology.

[44]  C. Renner,et al.  Natural and artificial cystine knots for assembly of homo- and heterotrimeric collagen models. , 2008, Antioxidants & redox signaling.

[45]  C. Pace,et al.  Urea and Guanidine Hydrochloride Denaturation of Ribonuclease , Lysozyme , & Zhymotrypsin , and @ Lactoglobulin * , 2003 .

[46]  D. Reinhardt,et al.  Properties of the Collagen Type XVII Ectodomain , 2001, The Journal of Biological Chemistry.

[47]  K. Doege,et al.  Folding of carboxyl domain and assembly of procollagen I. , 1986, The Journal of biological chemistry.

[48]  M. Billeter,et al.  MOLMOL: a program for display and analysis of macromolecular structures. , 1996, Journal of molecular graphics.

[49]  Yihai Cao.  Molecular mechanisms and therapeutic development of angiogenesis inhibitors. , 2008, Advances in cancer research.

[50]  T. Sasaki,et al.  Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity. , 2000, Journal of molecular biology.

[51]  V. Sukhatme,et al.  Endostatin: yeast production, mutants, and antitumor effect in renal cell carcinoma. , 1999, Cancer research.

[52]  O. Bogin,et al.  Insight into Schmid metaphyseal chondrodysplasia from the crystal structure of the collagen X NC1 domain trimer. , 2002, Structure.

[53]  K. Håkansson,et al.  Crystal structure of the trimeric alpha-helical coiled-coil and the three lectin domains of human lung surfactant protein D. , 1999, Structure.

[54]  M. Rossmann,et al.  The coiled-coil domain structure of the Sin Nombre virus nucleocapsid protein. , 2007, Journal of molecular biology.

[55]  A. Robinson,et al.  C‐terminal hydrophobic interactions play a critical role in oligomeric assembly of the P22 tailspike trimer , 2003, Protein science : a publication of the Protein Society.

[56]  J. Engel,et al.  Design and crystal structure of bacteriophage T4 mini-fibritin NCCF. , 2004, Journal of molecular biology.

[57]  J. Prieto,et al.  Enhanced antiangiogenic therapy with antibody‐collagen XVIII NC1 domain fusion proteins engineered to exploit matrix remodeling events , 2006, International journal of cancer.

[58]  Wayne A Hendrickson,et al.  [28] Phase determination from multiwavelength anomalous diffraction measurements. , 1997, Methods in enzymology.

[59]  K. Preissner,et al.  Isolation and characterization of the circulating form of human endostatin , 1997, FEBS letters.

[60]  K. Kar,et al.  Triple-helical peptides: an approach to collagen conformation, stability, and self-association. , 2008, Biopolymers.

[61]  Liisa Holm,et al.  Searching protein structure databases with DaliLite v.3 , 2008, Bioinform..

[62]  O. Bogin,et al.  Crystal structure of the collagen alpha1(VIII) NC1 trimer. , 2003, Matrix biology : journal of the International Society for Matrix Biology.

[63]  T. Pihlajaniemi,et al.  A short sequence in the N‐terminal region is required for the trimerization of type XIII collagen and is conserved in other collagenous transmembrane proteins , 2000, The EMBO journal.

[64]  T. Sasaki,et al.  Endostatin-induced tyrosine kinase signaling through the Shb adaptor protein regulates endothelial cell apoptosis. , 2000, Blood.

[65]  Collaborative Computational,et al.  The CCP4 suite: programs for protein crystallography. , 1994, Acta crystallographica. Section D, Biological crystallography.

[66]  David J. Scott,et al.  UltraScan - A Comprehensive Data Analysis Software Package for Analytical Ultracentrifugation Experiments , 2005 .