The crucial role of trimerization domains in collagen folding

International Journal of Biochemistry and Cell Biology

Volumn 44, Issue 1, 2012, Pages 21-32

  Boudko, Sergei P ^a,b   Engel, Jürgen ^c   Bächinger, Hans Peter ^a,b  

^a SHRINERS HOSPITAL FOR CHILDREN   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Chain selection; Collagen triple helix; Protein folding; Protein structure; Trimerization domain

Indexed keywords

BIOMATERIAL; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 15; COLLAGEN TYPE 18; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGEN TYPE 8;

DNA HELIX; HUMAN; MUTATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; TRIMERIZATION;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; COLLAGEN; COLLAGEN TYPE IV; COLLAGEN TYPE VIII; COLLAGEN TYPE X; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY;

EID: 83555174430     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2011.09.009     Document Type: Review

References (122)

1. B.D. Ackley, J.R. Crew, H. Elamaa, T. Pihlajaniemi, C.J. Kuo, and J.M. Kramer The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance J Cell Biol 152 2001 1219 1232 (Pubitemid 34280179)
2. N.N. Ahmad, J. Dimascio, R.G. Knowlton, and W.S. Tasman Stickler syndrome. A mutation in the nonhelical 3′ end of type II procollagen gene Arch Ophthalmol 113 1995 1454 1457
3. P.S. Amenta, N.A. Scivoletti, M.D. Newman, J.P. Sciancalepore, D. Li, and J.C. Myers Proteoglycan-collagen XV in human tissues is seen linking banded collagen fibers subjacent to the basement membrane J Histochem Cytochem 53 2005 165 176 (Pubitemid 40194460)
4. H.P. Bächinger, P. Bruckner, R. Timpl, and J. Engel The role of cis-trans isomerization of peptide bonds in the coil ↔ triple helix conversion of collagen Eur J Biochem 90 1978 605 613
5. C. Baldock, M.J. Sherratt, C.A. Shuttleworth, and C.M. Kielty The supramolecular organization of collagen VI microfibrils J Mol Biol 330 2003 297 307 (Pubitemid 36773703)
6. S.G. Ball, C. Baldock, C.M. Kielty, and C.A. Shuttleworth The role of the C1 and C2 a-domains in type VI collagen assembly J Biol Chem 276 2001 7422 7430
7. J.E. Banham, C.R. Timmel, R.J. Abbott, S.M. Lea, and G. Jeschke The characterization of weak protein-protein interactions: evidence from DEER for the trimerization of a von Willebrand Factor A domain in solution Angew Chem Int Ed Engl 45 2006 1058 1061 (Pubitemid 44104885)
8. J.F. Bateman, S.R. Lamande, H.H. Dahl, D. Chan, T. Mascara, and W.G. Cole A frameshift mutation results in a truncated nonfunctional carboxyl-terminal pro alpha 1(I) propeptide of type I collagen in osteogenesis imperfecta J Biol Chem 264 1989 10960 10964 (Pubitemid 19168819)
9. J.F. Bateman, R. Wilson, S. Freddi, S.R. Lamande, and R. Savarirayan Mutations of COL10A1 in Schmid metaphyseal chondrodysplasia Hum Mutat 25 2005 525 534 (Pubitemid 40780986)
10. A.A. Bhattacharya, M.L. Lupher Jr., D.E. Staunton, and R.C. Liddington Crystal structure of the A domain from complement factor B reveals an integrin-like open conformation Structure (Camb) 12 2004 371 378 (Pubitemid 38353058)
11. O. Bogin, M. Kvansakul, E. Rom, J. Singer, A. Yayon, and E. Hohenester Insight into Schmid metaphyseal chondrodysplasia from the crystal structure of the collagen X NC1 domain trimer Structure (Camb) 10 2002 165 173 (Pubitemid 34164595)
12. S. Boudko, S. Frank, R.A. Kammerer, J. Stetefeld, T. Schulthess, and R. Landwehr Nucleation and propagation of the collagen triple helix in single-chain and trimerized peptides: transition from third to first order kinetics J Mol Biol 317 2002 459 470 (Pubitemid 34722183)
13. S.P. Boudko, J. Engel, and H.P. Bächinger Trimerization and triple helix stabilization of the collagen XIX NC2 domain J Biol Chem 283 2008 34345 34351
14. S.P. Boudko, T. Sasaki, J. Engel, T.F. Lerch, J. Nix, and M.S. Chapman Crystal structure of human collagen XVIII trimerization domain: a novel collagen trimerization fold J Mol Biol 392 2009 787 802
15. S.P. Boudko, K.D. Zientek, J. Vance, J.L. Hacker, J. Engel, and H.P. Bächinger The NC2 domain of collagen IX provides chain selection and heterotrimerization J Biol Chem 285 2010 23721 23731
16. A. Boutaud, D.B. Borza, O. Bondar, S. Gunwar, K.O. Netzer, and N. Singh 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 2000 30716 30724
17. L. Bruckner-Tuderman, O. Nilssen, D.R. Zimmermann, M.T. Dours-Zimmermann, D.U. Kalinke, and T. Gedde-Dahl Jr. Immunohistochemical and mutation analyses demonstrate that procollagen VII is processed to collagen VII through removal of the NC-2 domain J Cell Biol 131 1995 551 559
18. P. Bruckner, H.P. Bächinger, R. Timpl, and J. Engel Three conformationally distinct domains in the amino-terminal segment of type III procollagen and its rapid triple helix ↔ coil transition Eur J Biochem 90 1978 595 603
19. P. Bruckner, and D.J. Prockop Proteolytic enzymes as probes for the triple-helical conformation of procollagen Anal Biochem 110 1981 360 368
20. N.J. Bulleid, J.A. Dalley, and J.F. Lees The C-propeptide domain of procollagen can be replaced with a transmembrane domain without affecting trimer formation or collagen triple helix folding during biosynthesis EMBO J 16 1997 6694 6701 (Pubitemid 27503482)
21. T.M. Carland, and L. Gerwick The C1q domain containing proteins: where do they come from and what do they do? Dev Comp Immunol 34 2010 785 790
22. M. Chen, D.R. Keene, F.K. Costa, S.H. Tahk, and D.T. Woodley The carboxyl terminus of type VII collagen mediates antiparallel dimer formation and constitutes a new antigenic epitope for epidermolysis Bullosa acquisita autoantibodies J Biol Chem 276 2001 21649 21655
23. M. Chen, E.A. O'Toole, M. Muellenhoff, E. Medina, N. Kasahara, and D.T. Woodley Development and characterization of a recombinant truncated type VII collagen "minigene". Implication for gene therapy of dystrophic epidermolysis bullosa J Biol Chem 275 2000 24429 24435 (Pubitemid 30626534)
24. S.D. Chessler, G.A. Wallis, and P.H. Byers Mutations in the carboxyl-terminal propeptide of the pro alpha 1(I) chain of type I collagen result in defective chain association and produce lethal osteogenesis imperfecta J Biol Chem 268 1993 18218 18225 (Pubitemid 23260346)
25. C.N. David, S. Özbek, P. Adamczyk, S. Meier, B. Pauly, and J. Chapman Evolution of complex structures: minicollagens shape the cnidarian nematocyst Trends Genet 24 2008 431 438
26. J.M. Davis, B.A. Boswell, and H.P. Bächinger Thermal stability and folding of type IV procollagen and effect of peptidyl-prolyl cis-trans-isomerase on the folding of the triple helix J Biol Chem 264 1989 8956 8962 (Pubitemid 19151624)
27. A. De Paepe, L. Nuytinck, I. Hausser, I. Anton-Lamprecht, and J.M. Naeyaert Mutations in the COL5A1 gene are causal in the Ehlers-Danlos syndromes I and II Am J Hum Genet 60 1997 547 554 (Pubitemid 27097602)
28. R. Dölz, J. Engel, and K. Kühn Folding of collagen IV Eur J Biochem 178 1988 357 366
29. V.P. Efimov, I.V. Nepluev, B.N. Sobolev, T.G. Zurabishvili, T. Schulthess, and A. Lustig Fibritin encoded by bacteriophage T4 gene wac has a parallel triple-stranded alpha-helical coiled-coil structure J Mol Biol 242 1994 470 486 (Pubitemid 24327210)
30. J. Engel, H. Furthmayr, E. Odermatt, H. von der Mark, M. Aumailley, and R. Fleischmajer Structure and macromolecular organization of type VI collagen Ann N Y Acad Sci 460 1985 25 37 (Pubitemid 16074807)
31. J. Engel, and D.J. Prockop The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper Annu Rev Biophys Biophys Chem 20 1991 137 152
32. U. Engel, O. Pertz, C. Fauser, J. Engel, C.N. David, and T.W. Holstein A switch in disulfide linkage during minicollagen assembly in Hydra nematocysts EMBO J 20 2001 3063 3073 (Pubitemid 32611994)
33. J.Y. Exposito, M. van der Rest, and R. Garrone The complete intron/exon structure of Ephydatia mulleri fibrillar collagen gene suggests a mechanism for the evolution of an ancestral gene module J Mol Evol 37 1993 254 259 (Pubitemid 23249703)
34. J. Fitzgerald, C. Rich, F.H. Zhou, and U. Hansen Three novel collagen VI chains, alpha4(VI), alpha5(VI), and alpha6(VI) J Biol Chem 283 2008 20170 20180
35. S. Frank, S. Boudko, K. Mizuno, T. Schulthess, J. Engel, and H.P. Bächinger Collagen triple helix formation can be nucleated at either end J Biol Chem 278 2003 7747 7750 (Pubitemid 36800506)
36. S. Frank, R.A. Kammerer, D. Mechling, T. Schulthess, R. Landwehr, and J. Bann Stabilization of short collagen-like triple helices by protein engineering J Mol Biol 308 2001 1081 1089 (Pubitemid 32574378)
37. C. Gaboriaud, J. Juanhuix, A. Gruez, M. Lacroix, C. Darnault, and D. Pignol The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties J Biol Chem 278 2003 46974 46982 (Pubitemid 37452280)
38. S.K. Gara, P. Grumati, A. Urciuolo, P. Bonaldo, B. Kobbe, and M. Koch Three novel collagen VI chains with high homology to the alpha3 chain J Biol Chem 283 2008 10658 10670
39. G.J. Gibson, and M.H. Flint Type X collagen synthesis by chick sternal cartilage and its relationship to endochondral development J Cell Biol 101 1985 277 284 (Pubitemid 15061277)
40. R. Golbik, J.A. Eble, A. Ries, and K. Kühn The spatial orientation of the essential amino acid residues arginine and aspartate within the alpha1beta1 integrin recognition site of collagen IV has been resolved using fluorescence resonance energy transfer J Mol Biol 297 2000 501 509
41. W.T. Grant, G.J. Wang, and G. Balian Type X collagen synthesis during endochondral ossification in fracture repair J Biol Chem 262 1987 9844 9849
42. N.S. Greenhill, B.M. Ruger, Q. Hasan, and P.F. Davis The alpha1(VIII) and alpha2(VIII) collagen chains form two distinct homotrimeric proteins in vivo Matrix Biol 19 2000 19 28 (Pubitemid 30109392)
43. C. Grond-Ginsbach, F. Wigger, M. Morcher, F. von Pein, A. Grau, and I. Hausser Sequence analysis of the COL5A2 gene in patients with spontaneous cervical artery dissections Neurology 58 2002 1103 1105 (Pubitemid 34298555)
44. W. Halfter, S. Dong, B. Schurer, and G.J. Cole Collagen XVIII is a basement membrane heparan sulfate proteoglycan J Biol Chem 273 1998 25404 25412 (Pubitemid 28443308)
45. C.P. Hayward, J.A. Hassell, G.A. Denomme, R.A. Rachubinski, C. Brown, and J.G. Kelton The cDNA sequence of human endothelial cell multimerin. A unique protein with RGDS, coiled-coil, and epidermal growth factor-like domains and a carboxyl terminus similar to the globular domain of complement C1q and collagens type VIII and X J Biol Chem 270 1995 18246 18251
46. C.P. Hayward, and J.G. Kelton Multimerin Curr Opin Hematol 2 1995 339 344
47. H. Hofmann, T. Voss, K. Kühn, and J. Engel Localization of flexible sites in thread-like molecules from electron micrographs. Comparison of interstitial, basement membrane and intima collagens J Mol Biol 172 1984 325 343
48. R.V. Iozzo The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins J Biol Chem 274 1999 18843 18846 (Pubitemid 29314072)
49. J. Khoshnoodi, K. Sigmundsson, J.P. Cartailler, O. Bondar, M. Sundaramoorthy, and B.G. Hudson Mechanism of chain selection in the assembly of collagen IV: a prominent role for the alpha2 chain J Biol Chem 281 2006 6058 6069 (Pubitemid 43847707)
50. C.M. Kielty, A.P. Kwan, D.F. Holmes, S.L. Schor, and M.E. Grant Type X collagen, a product of hypertrophic chondrocytes Biochem J 227 1985 545 554 (Pubitemid 15067729)
51. U. Kishore, and K.B. Reid Modular organization of proteins containing C1q-like globular domain Immunopharmacology 42 1999 15 21 (Pubitemid 29322283)
52. K. Kühn Basement membrane (type IV) collagen Matrix Biol 14 1995 439 445
53. C.J. Kuo, K.R. LaMontagne Jr., G. Garcia-Cardena, B.D. Ackley, D. Kalman, and S. Park Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain J Cell Biol 152 2001 1233 1246 (Pubitemid 34280180)
54. M. Kvansakul, O. Bogin, E. Hohenester, and A. Yayon Crystal structure of the collagen alpha1(VIII) NC1 trimer Matrix Biol 22 2003 145 152 (Pubitemid 36627472)
55. A.P. Kwan, C.E. Cummings, J.A. Chapman, and M.E. Grant Macromolecular organization of chicken type X collagen in vitro J Cell Biol 114 1991 597 604 (Pubitemid 21909827)
56. U. Labermeier, T.A. Demlow, and M.C. Kenney Identification of collagens isolated from bovine Descemet's membrane Exp Eye Res 37 1983 225 237 (Pubitemid 13005102)
57. L. Labourdette, and M. van der Rest Analysis of the role of the COL1 domain and its adjacent cysteine-containing sequence in the chain assembly of type IX collagen FEBS Lett 320 1993 211 214 (Pubitemid 23105111)
58. S.R. Lamande, S.D. Chessler, S.B. Golub, P.H. Byers, D. Chan, and W.G. Cole Endoplasmic reticulum-mediated quality control of type I collagen production by cells from osteogenesis imperfecta patients with mutations in the pro alpha 1 (I) chain carboxyl-terminal propeptide which impair subunit assembly J Biol Chem 270 1995 8642 8649
59. S.R. Lamande, M. Mörgelin, N.E. Adams, C. Selan, and J.M. Allen The C5 domain of the collagen VI alpha3(VI) chain is critical for extracellular microfibril formation and is present in the extracellular matrix of cultured cells J Biol Chem 281 2006 16607 16614
60. S.R. Lamande, M. Mörgelin, C. Selan, G.J. Jobsis, F. Baas, and J.F. Bateman Kinked collagen VI tetramers and reduced microfibril formation as a result of Bethlem myopathy and introduced triple helical glycine mutations J Biol Chem 277 2002 1949 1956 (Pubitemid 34968773)
61. A. Lesage, F. Penin, C. Geourjon, D. Marion, and M. van der Rest Trimeric assembly and three-dimensional structure model of the FACIT collagen COL1-NC1 junction from CD and NMR analysis Biochemistry 35 1996 9647 9660 (Pubitemid 26302977)
62. A.V. Letarov, Y.Y. Londer, S.P. Boudko, and V.V. Mesyanzhinov The carboxy-terminal domain initiates trimerization of bacteriophage T4 fibritin Biochemistry (Mosc) 64 1999 817 823 (Pubitemid 129583364)
63. A.N. Lupas, and M. Gruber The structure of alpha-helical coiled coils Adv Protein Chem 70 2005 37 78
64. J.P. Malone, K. Alvares, and A. Veis Structure and assembly of the heterotrimeric and homotrimeric C-propeptides of type I collagen: significance of the alpha2(I) chain Biochemistry 44 2005 15269 15279 (Pubitemid 41681461)
65. A.G. Marneros, and B.R. Olsen Physiological role of collagen XVIII and endostatin FASEB J 19 2005 716 728 (Pubitemid 40617376)
66. M. Mazzorana, S. Cogne, D. Goldschmidt, and E. Aubert-Foucher Collagenous sequence governs the trimeric assembly of collagen XII J Biol Chem 276 2001 27989 27998
67. M. Mazzorana, H. Gruffat, A. Sergeant, and M. van der Rest Mechanisms of collagen trimer formation. Construction and expression of a recombinant minigene in HeLa cells reveals a direct effect of prolyl hydroxylation on chain assembly of type XII collagen J Biol Chem 268 1993 3029 3032 (Pubitemid 23070919)
68. A. McAlinden, T.A. Smith, L.J. Sandell, D. Ficheux, D.A. Parry, and D.J. Hulmes Alpha-helical coiled-coil oligomerization domains are almost ubiquitous in the collagen superfamily J Biol Chem 278 2003 42200 42207 (Pubitemid 37310486)
69. D.E. Mechling, J.E. Gambee, N.P. Morris, L.Y. Sakai, D.R. Keene, and R. Mayne Type IX collagen NC1 domain peptides can trimerize in vitro without forming a triple helix J Biol Chem 271 1996 13781 13785 (Pubitemid 26185422)
70. S. Meier, P.R. Jensen, P. Adamczyk, H.P. Bächinger, T.W. Holstein, and J. Engel Sequence-structure and structure-function analysis in cysteine-rich domains forming the ultrastable nematocyst wall J Mol Biol 368 2007 718 728 (Pubitemid 46527611)
71. A.G. Milbradt, C. Boulegue, L. Moroder, and C. Renner The two cysteine-rich head domains of minicollagen from Hydra nematocysts differ in their cystine framework and overall fold despite an identical cysteine sequence pattern J Mol Biol 354 2005 591 600 (Pubitemid 41628278)
72. A.L. Mitchell, U. Schwarze, J.F. Jennings, and P.H. Byers Molecular mechanisms of classical Ehlers-Danlos syndrome (EDS) Hum Mutat 30 2009 995 1002
73. K. Mizuno, S.P. Boudko, J. Engel, and H.P. Bächinger Kinetic hysteresis in collagen folding Biophys J 98 2010 3004 3014
74. E. Moutevelis, and D.N. Woolfson A periodic table of coiled-coil protein structures J Mol Biol 385 2009 726 732
75. Y. Muragaki, O. Jacenko, S. Apte, M.G. Mattei, Y. Ninomiya, and B.R. Olsen The alpha 2(VIII) collagen gene. A novel member of the short chain collagen family located on the human chromosome 1 J Biol Chem 266 1991 7721 7727 (Pubitemid 21906424)
76. J.C. Myers, S. Kivirikko, M.K. Gordon, A.S. Dion, and T. Pihlajaniemi Identification of a previously unknown human collagen chain, alpha 1(XV), characterized by extensive interruptions in the triple-helical region Proc Natl Acad Sci U S A 89 1992 10144 10148
77. J. Myllyharju, and K.I. Kivirikko Collagens, modifying enzymes and their mutations in humans, flies and worms Trends Genet 20 2004 33 43 (Pubitemid 38032818)
78. J. Myllyharju, A. Lamberg, H. Notbohm, P.P. Fietzek, T. Pihlajaniemi, and K.I. Kivirikko Expression of wild-type and modified proalpha chains of human type I procollagen in insect cells leads to the formation of stable [alpha1(I)]2alpha2(I) collagen heterotrimers and [alpha1(I)]3 homotrimers but not [alpha2(I)]3 homotrimers J Biol Chem 272 1997 21824 21830 (Pubitemid 27382798)
79. Y. Ninomiya, M. Gordon, M. van der Rest, T. Schmid, T. Linsenmayer, and B.R. Olsen The developmentally regulated type X collagen gene contains a long open reading frame without introns J Biol Chem 261 1986 5041 5050 (Pubitemid 17204300)
80. J.P. Orgel, T.C. Irving, A. Miller, and T.J. Wess Microfibrillar structure of type I collagen in situ Proc Natl Acad Sci U S A 103 2006 9001 9005 (Pubitemid 43902523)
81. S. Özbek, O. Pertz, M. Schwager, A. Lustig, T. Holstein, and J. Engel Structure/function relationships in the minicollagen of Hydra nematocysts J Biol Chem 277 2002 49200 49204 (Pubitemid 36014348)
82. S. Özbek, E. Pokidysheva, M. Schwager, T. Schulthess, N. Tariq, and D. Barth The glycoprotein NOWA and minicollagens are part of a disulfide-linked polymer that forms the cnidarian nematocyst wall J Biol Chem 279 2004 52016 52023 (Pubitemid 39656572)
83. J.M. Pace, C.D. Kuslich, M.C. Willing, and P.H. Byers Disruption of one intra-chain disulphide bond in the carboxyl-terminal propeptide of the proalpha1(I) chain of type I procollagen permits slow assembly and secretion of overmodified, but stable procollagen trimers and results in mild osteogenesis imperfecta J Med Genet 38 2001 443 449 (Pubitemid 32661205)
84. J.M. Pace, M. Wiese, A.S. Drenguis, N. Kuznetsova, S. Leikin, and U. Schwarze Defective C-propeptides of the proalpha2(I) chain of type I procollagen impede molecular assembly and result in osteogenesis imperfecta J Biol Chem 283 2008 16061 16067
85. O. Pakkanen, E.R. Hamalainen, K.I. Kivirikko, and J. Myllyharju Assembly of stable human type I and III collagen molecules from hydroxylated recombinant chains in the yeast Pichia pastoris. Effect of an engineered C-terminal oligomerization domain foldon J Biol Chem 278 2003 32478 32483 (Pubitemid 37048447)
86. K. Papanikolopoulou, M.J. van Raaij, and A. Mitraki Creation of hybrid nanorods from sequences of natural trimeric fibrous proteins using the fibritin trimerization motif Methods Mol Biol 474 2008 15 33
87. M.J. Pickup, and M.S. Pollanen Traumatic subarachnoid hemorrhage and the COL3A1 gene: emergence of a potential causal link Forensic Sci Med Pathol 7 2011 192 197
88. T. Pihlajaniemi, and M. Rehn Two new collagen subgroups: membrane-associated collagens and types XV and XVII Prog Nucleic Acid Res Mol Biol 50 1995 225 262
89. E. Pokidysheva, A.G. Milbradt, S. Meier, C. Renner, D. Haussinger, and H.P. Bächinger The structure of the Cys-rich terminal domain of Hydra minicollagen, which is involved in disulfide networks of the nematocyst wall J Biol Chem 279 2004 30395 30401 (Pubitemid 38937967)
90. F.M. Pope, S. Holden, D.J.P. Ferguson, P. Sawle, M. Nesbitt, and R. Pollitt Abstracts of the British Human Genetics Conference 2010 University of Warwick, 6-8 September 2010 J Med Genet 47 Suppl. 1 2010 20
91. S. Raman, G. Machaidze, A. Lustig, U. Aebi, and P. Burkhard Structure-based design of peptides that self-assemble into regular polyhedral nanoparticles Nanomedicine 2 2006 95 102 (Pubitemid 43956613)
92. M. Rehn, E. Hintikka, and T. Pihlajaniemi 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 J Biol Chem 269 1994 13929 13935
93. M. Rehn, and T. Pihlajaniemi Alpha 1(XVIII), a collagen chain with frequent interruptions in the collagenous sequence, a distinct tissue distribution, and homology with type XV collagen Proc Natl Acad Sci U S A 91 1994 4234 4238
94. S. Ricard-Blum, and F. Ruggiero The collagen superfamily: from the extracellular matrix to the cell membrane Pathol Biol (Paris) 53 2005 430 442 (Pubitemid 41112079)
95. J. Risteli, H.P. Bächinger, J. Engel, H. Furthmayr, and R. Timpl 7-S collagen: characterization of an unusual basement membrane structure Eur J Biochem 108 1980 239 250 (Pubitemid 11246090)
96. S. Réty, S. Salamitou, I. Garcia-Verdugo, D.J. Hulmes, F. Le Hégarat, and R. Chaby The crystal structure of the Bacillus anthracis spore surface protein BclA shows remarkable similarity to mammalian proteins J Biol Chem 280 2005 43073 43078 (Pubitemid 43049273)
97. L.Y. Sakai, D.R. Keene, N.P. Morris, and R.E. Burgeson Type VII collagen is a major structural component of anchoring fibrils J Cell Biol 103 1986 1577 1586 (Pubitemid 17174180)
98. V.J. Sanchez-Arevalo Lobo, A.M. Cuesta, L. Sanz, M. Compte, P. Garcia, and J. Prieto Enhanced antiangiogenic therapy with antibody-collagen XVIII NC1 domain fusion proteins engineered to exploit matrix remodeling events Int J Cancer 119 2006 455 462
99. T. Sasaki, N. Fukai, K. Mann, W. Göhring, B.R. Olsen, and R. Timpl Structure, function and tissue forms of the C-terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin EMBO J 17 1998 4249 4256 (Pubitemid 28362615)
100. T. Sasaki, H. Larsson, D. Tisi, L. Claesson-Welsh, E. Hohenester, and R. Timpl Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity J Mol Biol 301 2000 1179 1190
101. T.M. Schmid, and T.F. Linsenmayer A short chain (pro)collagen from aged endochondral chondrocytes. Biochemical characterization J Biol Chem 258 1983 9504 9509 (Pubitemid 13035600)
102. U. Schwarze, W.I. Schievink, E. Petty, M.R. Jaff, D. Babovic-Vuksanovic, and K.J. Cherry Haploinsufficiency for one COL3A1 allele of type III procollagen results in a phenotype similar to the vascular form of Ehlers-Danlos syndrome, Ehlers-Danlos syndrome type IV Am J Hum Genet 69 2001 989 1001 (Pubitemid 33015814)
103. L. Shapiro, and P.E. Scherer The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor Curr Biol 8 1998 335 338 (Pubitemid 28159119)
104. C.A. Shuttleworth Type VIII collagen Int J Biochem Cell Biol 29 1997 1145 1148 (Pubitemid 27522554)
105. S. Stephan, M.J. Sherratt, N. Hodson, C.A. Shuttleworth, and C.M. Kielty Expression and supramolecular assembly of recombinant alpha1(viii) and alpha2(viii) collagen homotrimers J Biol Chem 279 2004 21469 21477 (Pubitemid 38656557)
106. J. Stetefeld, S. Frank, M. Jenny, T. Schulthess, R.A. Kammerer, and S. Boudko Collagen stabilization at atomic level. Crystal structure of designed (GlyProPro)(10)foldon Structure (Camb) 11 2003 339 346 (Pubitemid 36287696)
107. M. Sundaramoorthy, M. Meiyappan, P. Todd, and B.G. Hudson Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes J Biol Chem 277 2002 31142 31153 (Pubitemid 34970820)
108. Y. Tao, S.V. Strelkov, V.V. Mesyanzhinov, and M.G. Rossmann Structure of bacteriophage T4 fibritin: a segmented coiled coil and the role of the C-terminal domain Structure (Camb) 5 1997 789 798 (Pubitemid 27307347)
109. M.E. Than, S. Henrich, R. Huber, A. Ries, K. Mann, and K. Kühn The 1.9- 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 U S A 99 2002 6607 6612 (Pubitemid 34526180)
110. R. Timpl, H. Wiedemann, V. van Delden, H. Furthmayr, and K. Kühn A network model for the organization of type IV collagen molecules in basement membranes Eur J Biochem 120 1981 203 211 (Pubitemid 12221838)
111. J. Uitto, and A.M. Christiano Molecular basis for the dystrophic forms of epidermolysis bullosa: mutations in the type VII collagen gene Arch Dermatol Res 287 1994 16 22
112. R. Vanacore, A.J. Ham, M. Voehler, C.R. Sanders, T.P. Conrads, and T.D. Veenstra A sulfilimine bond identified in collagen IV Science 325 2009 1230 1234
113. R.M. Vanacore, D.B. Friedman, A.J. Ham, M. Sundaramoorthy, and B.G. Hudson Identification of S-hydroxylysyl-methionine as the covalent cross-link of the noncollagenous (NC1) hexamer of the alpha1alpha1alpha2 collagen IV network: a role for the post-translational modification of lysine 211 to hydroxylysine 211 in hexamer assembly J Biol Chem 280 2005 29300 29310 (Pubitemid 41161385)
114. G. Verdone, A. Corazza, S.A. Colebrooke, D. Cicero, T. Eliseo, and J. Boyd NMR-based homology model for the solution structure of the C-terminal globular domain of EMILIN1 J Biomol NMR 43 2009 79 96
115. G. Verdone, R. Doliana, A. Corazza, S.A. Colebrooke, P. Spessotto, and S. Bot The solution structure of EMILIN1 globular C1q domain reveals a disordered insertion necessary for interaction with the alpha4beta1 integrin J Biol Chem 283 2008 18947 18956
116. K. von der Mark, T. Kirsch, A. Nerlich, A. Kuss, G. Weseloh, and K. Gluckert Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy Arthritis Rheum 35 1992 806 811
117. S. Weber, R. Dölz, R. Timpl, J.H. Fessler, and J. Engel Reductive cleavage and reformation of the interchain and intrachain disulfide bonds in the globular hexameric domain NC1 involved in network assembly of basement membrane collagen (type IV) Eur J Biochem 175 1988 229 236
118. R. Wilson, S. Freddi, D. Chan, K.S. Cheah, and J.F. Bateman Misfolding of collagen X chains harboring Schmid metaphyseal chondrodysplasia mutations results in aberrant disulfide bond formation, intracellular retention, and activation of the unfolded protein response J Biol Chem 280 2005 15544 15552 (Pubitemid 40616670)
119. J.A. Wirz, S.P. Boudko, T.F. Lerch, M.S. Chapman, and H.P. Bächinger Crystal structure of the human collagen XV trimerization domain: a potent trimerizing unit common to multiplexin collagens Matrix Biol 30 2011 9 15
120. D.N. Woolfson Building fibrous biomaterials from alpha-helical and collagen-like coiled-coil peptides Biopolymers 94 2010 118 127
121. P.D. Yurchenco, and J.C. Schittny Molecular architecture of basement membranes FASEB J 4 1990 1577 1590
122. Y. Zhang, and Q. Chen The noncollagenous domain 1 of type X collagen. A novel motif for trimer and higher order multimer formation without a triple helix J Biol Chem 274 1999 22409 22413