Natural and artificial cystine knots for assembly of homo- and heterotrimeric collagen models

Antioxidants and Redox Signaling

Volumn 10, Issue 1, 2008, Pages 113-125

  Boulègue, Cyril ^a   Musiol, Hans Jürgen ^a   Götz, Marion G ^b   Renner, Christian ^a,c   Moroder, Luis ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b WHITMAN COLLEGE   (United States)

^c Deutsche Forschungsgemeinschaft   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANCHORING FIBRIL COLLAGEN; BEADED FILAMENT; COLLAGEN; COLLAGEN TYPE 10; COLLAGEN TYPE 14; COLLAGEN TYPE 19; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGEN TYPE 9; FIBRIL ASSOCIATED COLLAGENS WITH INTERRUPTED TRIPLE HELICES; FIBRILLAR COLLAGEN; MEMBRANE ASSOCIATED COLLAGENS WITH INTERRUPTED TRIPLE HELICES; MULTIPLEXIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CHEMICAL REACTION; COLLAGENOUS DOMAIN; CYSTINE KNOT MOTIF; HETEROTRIMERIC COLLAGEN; HOMOTRIMERIC COLLAGEN; MOLECULAR MODEL; MOLECULE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; BIOPOLYMERS; COLLAGEN; CYSTINE; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 36149000230     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2007.1868     Document Type: Review

References (116)

1. Areida SK, Reinhardt DP, Müller PK, Fietzek PP, Köwitz J, Marinkovich MP, and Notbohm H. Properties of the collagen type XVII ectodomain. Evidence for N- to C-terminal triple helix folding. J Biol Chem 276:1594-1601, 2001.
2. Bächinger HP and Engel J. The thermodynamics and kinetics of collagen folding. In: Protein Folding Handbook, edited by Buchner, J, and Kiefhaber, T. Weinheim, Germany: Wiley-VCH, 2005, Vol. 2, pp. 1059-1110.
3. Bächinger HP, Bruckner P, Timpl R, and Engel J. Role of cis-trans isomerization of peptide bonds in coil ↔ triple helix conversion of collagen. Eur J Biochem 90: 605-613, 1978.
4. Bächinger HP, Bruckner P, Timpl R, Prockop DJ, and Engel J. Folding mechanism of the triple helix in type-III collagen and type-III pN-collagen. Role of disulfide bridges and peptide-bond isomerization. Eur J Biochem 106: 619-632, 1980.
5. Bächinger HP, Fessler LI, Timpl R, and Fessler JH. Chain assembly intermediate in the biosynthesis of type-III procollagen in chick-embryo blood-vessels. J Biol Chem 256: 3193-3199, 1981.
6. Bachmann A, Kiefhaber T, Boudko S, Engel J, and Bächinger HP. Collagen triple-helix formation in all-trans chains proceeds by a nucleation/growth mechanism with a purely entropic barrier. Proc Natl Acad Sci USA 102: 13897-13902, 2005.
7. n model trimers with N- and C-terminal collagen type III cystine knots. Chem Eur J 9: 3703-3714, 2003.
8. 5 model trimers with an artificial cystine knot. Chem Eur J 9: 3692-3702, 2003.
9. Barth L, Sinner EK, Cadamur SA. Renner C, Oesterhelt D, and Moroder L. Homotrimeric collagen peptides as model systems for cell adhesion studies. In: Peptides for Youth, edited by Escher E, Lubell WD, and Del Valle S. American Peptide Society, in press.
10. Beck K, Boswell BA, Ridgway CC, B-hinger HP. Triple helix formation of procollagen type I can occur at the rough endoplasmic reticulum membrane. J Biol Chem 271: 21566-21573, 1996.
11. Beier G and Engel J. Renaturation of soluble collagen - Products formed at different temperatures. Biochemistry 5: 2744-2755, 1966.
12. Berg RA and Prockop DJ. Purification of carbon-14-labeled protocollagen and its hydroxylation by prolyl-hydroxylase. Biochemistry 12: 3395-3401, 1973.
13. Boudko S, Frank S, Kammerer RA, Stetefeld J, Schulthess T, Landwehr R, Lustig A, B-hinger HP, and Engel J. 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: 459-470, 2002.
14. Boudko SP and Engel J. Structure formation in the C-terminus of type III collagen guides disulfide cross-linking. J Mol Biol 335: 1289-1297, 2004.
15. Boulègue C, Milbradt AG, Renner C, and Moroder L. Single proline residues can dictate the oxidative folding pathways of cysteine-rich peptides. J Mol Biol 358: 846-856, 2006
16. Brodsky B and Persikov AV. Molecular structure of the collagen triple helix. Adv Prot Chem 70: 301-339, 2005.
17. Brown FR, Blout ER, Corato AD, and Lorenzi GP. Synthesis and structural studies of two collagen analogs: poly-(L-Prolyl-LSeryl-Glycyl) and poly-(L-Prolyl-L-Alanyl-Glycyl). J Mol Biol 63: 85-99, 1972.
18. Bruckner P, Bächinger HP, Timpl R, and Engel J. Three Conformationally distinct domains in amino-terminal segment of type-III procollagen and its rapid triple helix ( coil transition. Eur J Biochem 90: 595-603, 1978.
19. Bruckner P and Eikenberry EF. Formation of the triple helix of type-I procollagen in cellulo - Temperature-dependent kinetics support a model based on cis-trans isomerization of peptide bonds. Eur J Biochem 140: 391-395, 1984.
20. Bruckner P, Eikenberry EF, and Prockop DJ. Formation of the triple helix of type-I procollagen in cellulo - A kinetic model based on cis-trans isomerization of peptide-bonds. Eur J Biochem 118: 607-613, 1981.
21. t and their characterization with circular-dichroism and ultracentrifugation. Helv Chim Acta 58: 1276-1287, 1975.
22. Buevich AV and Baum J. Residue-specific real-time NMR diffusion experiments define the association states of proteins during folding. J Am Chem Soc 124: 7156-7162, 2002.
23. Bulleid NJ, Dalley JA, and Lees JF. 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: 6694-6701, 1997.
24. Cai WB, Kwok SW, Taulane JP, and Goodman M. Metal-assisted assembly and stabilization of collagen-like triple helices. J Am Chem Soc 126: 15030-15031, 2004.
25. Camacho CJ and Thirumalai D. Theoretical predictions of folding pathways by using the proximity rule, with applications to bovine pancreatic trypsin-inhibitor. Proc Natl Acad Sci USA 92: 1277-1281, 1995.
26. Capasso S, Mattia C, Mazzarella L, and Puliti R. Structure of a cis-peptide unit - Molecular-conformation of cyclic disulfide L-cysteinyl-L-cysteine. Acta Crystallogr B 33: 2080-2083, 1977.
27. Carugo O, Čemažar M, Zahariev S, Hudáky I, Gápári Z, Perczel A, and Pongor S. Vicinal disulfide turns. Protein Engineer 16: 637-639, 2003.
28. Čemažar M, Zahariev S, Lopez JJ, Carugo O, Jones JA, Hore PJ, and Pongor S. Oxidative folding intermediates with nonnative disulfide bridges between adjacent cysteine residues. Proc Natl Acad Sci USA 100: 5754-5759, 2003.
29. Chandrasekaran R and Balasubramamian R. Stereochemical studies of cyclic peptides. 4. Energy calculations of cyclic disulphide cysteinylcysteine. Biochim Biophys Acta 188:1-9, 1969.
30. Chopra RK and Ananthanarayanan VS. Conformational implications of enzymatic proline hydroxylation in collagen. Proc Natl Acad Sci USA 79: 7180-7184, 1982.
31. Chou PY and Fasman GD. Empirical predictions of protein conformation. Annu Rev Biochem 47: 251-276, 1978.
32. Creighton CJ, Reynolds CH, Lee DHS, Leo GC, and Reitz AB. Conformational analysis of the eight-membered ring of the oxidized cysteinyl-cysteine unit implicated in nicotinic acetylcholine receptor ligand recognition. J Am Chem Soc 123: 12664-12669, 2001.
33. Engel J and Bächinger HP. Structure, stability and folding of the collagen triple helix. Top Curr Chem 247: 7-33, 2005.
34. n. Biopolymers 16: 601-622, 1977.
35. Engel J and Prockop DJ. The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper. Annu Rev Biophys Biophys Chem 20: 137-152, 1991.
36. Feng YB, Melacini G, Taulane JP, and Goodman M. Acetyl-terminated and template-assembled collagen-based polypeptides composed of Gly-Pro-Hyp sequences. 2. Synthesis and conformational analysis by circular dichroism, ultraviolet absorbance, and optical rotation. J Am Chem Soc 118: 10351-10358, 1996.
37. Fessler LI, Timpl R, and Fessler JH. Assembly and processing of procollagen type-III in chick-embryo blood-vessels. J Biol Chem 256: 2531-2537, 1981.
38. Fields CG, Grab B, Lauer JL, and Fields GB. Purification and analysis of synthetic, triple-helical minicollagens by reversed-phase high-performance liquid-chromatography. Anal Biochem 231: 57-64, 1995.
39. Fields CG, Grab B, Lauer JL, Miles AJ, Yu YC, and Fields GB. Solid-phase synthesis of triple-helical collagen-model peptides. Lett Pept Sci 3: 3-16, 1996.
40. Fields CG, Lovdahl CM, Miles AJ, Hagen VLM, and Fields GB. Solid-phase synthesis and stability of triple-helical peptides incorporating native collagen sequences. Biopolymers 33: 1695-1707, 1993.
41. Fields GB and Prockop DJ. Perspectives on the synthesis and application of triple-helical, collagen-model peptides. Biopolymers 40: 345-357, 1996.
42. Fiori S, Saccà B, and Moroder L. Structural properties of a collagenous heterotrimer that mimics the collagenase cleavage site of collagen type I. J Mol Biol 319: 1235-1242, 2002.
43. Frank S, Boudko S, Mizuno K, Schulthess T, Engel J, and Bächinger HP. Collagen triple helix formation can be nucleated at either end. J Biol Chem 278: 7747-7750, 2003.
44. Frank S, Kammerer RA, Mechling D, Schulthess T, Landwehr R, Bann J, Guo Y, Lustig A, Bächinger HP, and Engel J. Stabilization of short collagen-like triple helices by protein engineering. J Mol Biol 308: 1081-1089, 2001.
45. Gauba V and Hartgerink JD. Self-assembled heterotrimeric collagen triple helices directed through electrostatic interactions. J Am Chem Soc 129: 2683-2690, 2007.
46. Glanville RW, Allmann H, and Fietzek PP. Cysteine residues mark C-terminal triple-helical-non-triple-helical junction in type III collagen. Hoppe-Seylers Z Physiol Chem 357: 1663-1665, 1976.
47. Goodman M, Bhumralkar M, Jefferson EA, Kwak J, and Locardi E. Collagen mimetics. Biopolymers 47: 127-142, 1998.
48. Goodman M, Feng YB, Melacini G, and Taulane JP. A template-induced incipient collagen-like triple-helical structure. J Am Chem Soc 118: 5156-5157, 1996.
49. Goodman M, Melacini G, and Feng YB. Collagen-like triple helices incorporating peptoid residues. J Am Chem Soc 118: 10928-10929, 1996.
50. Grab B, Miles AJ, Furcht LT, and Fields GB. Promotion of fibroblast adhesion by triple-helical peptide models of type I collagen-derived sequences. J Biol Chem 271: 12234-12240, 1996.
51. Greiche Y and Heidemann E. Collagen model peptides with antiparallel structure. Biopolymers 18: 2359-2361, 1979.
52. Harrington WF and Rao NV. Collagen structure in solution. I. Kinetics of helix regeneration in single-chain gelatins. Biochemistry 9: 3714-3724, 1970.
53. Heidemann E and Roth W. Synthesis and investigation of collagen model peptides. Adv Polym Sci 43: 143-203, 1982.
54. Hojo H, Akamatsu Y, Yamauchi K, Kinoshita M, Miki S, and Nakamura Y. Synthesis and structural characterization of triplehelical peptides which mimic the ligand binding site of the human macrophage scavenger receptor. Tetrahedron 53: 14263-14274, 1997.
55. Holmes TC. Novel peptide-based biomaterial scaffolds for tissue engineering. Trends Biotech 20: 16-21, 2002.
56. Horng JC, Hawk AJ, Zhao Q, Benedict ES, Burke SD, and Raines RT. Macrocyclic scaffold for the collagen triple helix. Org Lett 8: 4735-4738, 2006.
57. Khoshnoodi J, Cartailler JP, Alvares K, Veis A, and Hudson BG. Molecular recognition in the assembly of collagens - Terminal noncollagenous domains are key recognition modules in the formation of triple helical protomers. J Biol Chem 281: 38117-38121, 2006.
58. Kielthy CM and Grant ME. The collagen family. Structure assembly and organisation in the extracellular matrix. In: Connective Tissue and its Heritable Disorders, Molecular, Genetic and Medical Aspects, 2nd edition, edited by Royce PM and Steinmann B. New York: Wiley-Liss; 2002, pp. 159-222.
59. Kinberger GA, Cai WB, and Goodman M. Collagen mimetic dendrimers. J Am Chem Soc 124: 15162-15163, 2002.
60. Koide T. Triple helical collagen-like peptides. Engineering and applications in matrix biology. Connect Tiss Res 46: 131-141, 2005.
61. Koide T, Asada S, Takahara Y, Nishikawa Y, Nagata K, and Kitagawa K. Specific recognition of the collagen triple helix by chaperone HSP47. Minimal structural requirement and spatial molecular orientation. J Biol Chem 281: 3432-3438, 2006.
62. Koide T, Homma DL, Asada S, and Kitagawa K. Self-complementary peptides for the formation of collagen-like triple helical supramolecules. Bioorg Med Chem Lett 15: 5230-5233, 2005.
63. Koide T and Nagata K. Collagen biosynthesis. Top Curr Chem 247: 85-114, 2005.
64. Koide T, Nishikawa Y, Asada S, Yamazaki CM, Takahara Y, Homma DL, Otaka A, Ohtani K, Wakamiya N, Nagata K, and Kitagawa K. Specific recognition of the collagen triple helix by chaperone HSP47. II. The HSP47-binding structural motif in collagens and related proteins. J Biol Chem 281: 11177-11185, 2006.
65. Koide T, Nishikawa Y, and Takahara Y. Synthesis of heterotrimeric collagen models containing Arg residues in Y-positions and analysis of their conformational stability. Bioorg Med Chem Lett 14: 125-128, 2004.
66. Koide T, Yuguchi M, Kawakita M, and Konno H. Metal-assisted stabilization and probing of collagenous triple helices. J Am Chem Soc 124: 9388-9389, 2002.
67. Koivu J and Myllylä R. Interchain disulfide bond formation in type-I and type-II procollagen - Evidence for a protein disulfide isomerase catalyzing bond formation. J Biol Chem 262: 6159-6164, 1987.
68. Kotch FW and Raines RT. Self-assembly of synthetic collagen triple helices. Proc Natl Acad Sci USA 103: 3028-3033, 2006.
69. Kwak J, De Capua A, Locardi E, and Goodman M. TREN (tris(2-aminoethyl) amine) - An effective scaffold for the assembly of triple helical collagen mimetic structures. J Am Chem Soc 124: 14085-14091, 2002.
70. Labourdette L and van der Rest M. 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: 211-214, 1993.
71. Lesage A, Penin F, Geourjon C, Marion D, van der Rest M. Trimeric assembly and three-dimensional structure model of the FACIT collagen COL1-NC1 junction from CD and NMR analysis. Biochemistry 35: 9647-9660, 1996.
72. Letarov AV, Londer YY, Boudko SP, and Mesyanzhinov VV. The carboxy-terminal domain initiates trimerization of bacteriophage T4 fibritin. Biochem (Mosc) 64: 817-823, 1999.
73. Lunstrum GP, McDonough AM, Marinkovich MP, Keene DR, Morris NP, and Burgeson RE. Identification and partial-purification of a large, variant form of type-XII collagen. J Biol Chem 267: 20087-20092, 1992.
74. Mann K, Mechling DE, B-hinger HP, Eckerskorn C, Gaill F, and Timpl R. Glycosylated threonine but not 4-hydroxyproline dominates the triple helix stabilizing positions in the sequence of a hydrothermal vent worm cuticle collagen. J Mol Biol 261: 255-266, 1996.
75. Mazzorana M, Cogne S, Goldschmidt D, and Aubert-Foucher E. Collagenous sequence governs the trimeric assembly of collagen XII. J Biol Chem 276: 27989-27998, 2001.
76. Mazzorana M, Giry-Lozinguez C, and van der Rest M. Trimeric assembly of collagen-XII. Effect of deletion of the C-terminal part of the molecule. Matrix Biol 14: 583-588, 1995.
77. Mazzorana M, Gruffat H, Sergeant A, and van der Rest M. 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: 3029-3032, 1993.
78. Mazzorana M, Snellman A, Kivirikko KI, van der Rest M, and Pihlajaniemi T: Involvement of prolyl-4-hydroxylase in the assembly of trimeric minicollagen XII - Study in a baculovirus expression system. J Biol Chem 271: 29003-29008, 1996.
79. McAlinden A, Crouch EC, Bann JG, Zhang PN, and Sandell LJ. Trimerization of the amino propeptide of type IIA procollagen using a 14-amino acid sequence derived from the coiled-coil neck domain of surfactant protein D. J Biol Chem 277: 41274-41281, 2002.
80. 15GPCCG forms pH-dependent covalently linked triple helical trimers. J Biol Chem 275: 14532-14536, 2000.
81. Mechling DE, Gambee JE, Morris NP, Sakai LY, Keene DR, Mayne R, and Bächinger HP. Type IX collagen NC1 domain peptides can trimerize in vitro without forming a triple helix. J Biol Chem 271: 13781-13785, 1996.
82. Moroder L, Fiori S, Friedrich R, and Ottl J. Collagen mimics. Synthesis and properties of disulfide-bridged trimeric collagen peptides. In: Synthetic Macromolecules with Higher Structural Order, edited by Khan IM. ACS Symposium Series, vol. 812. Washington, DC: ACS, 2002, pp. 103-116.
83. Moroder L, Musiol HJ, Götz M, and Renner C. Synthesis of single-and multiple-stranded cystine-rich peptides. Biopolymers 80: 85-97, 2005.
84. Müller JCD, Ottl J, and Moroder L. Heterotrimeric collagen peptides as fluorogenic collagenase substrates - Synthesis, conformational properties, and enzymatic digestion. Biochemistry 39: 5111-5116, 2000.
85. Myllyharju J and Kivirikko KI. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20: 33-43, 2004.
86. Myllylä R, Kuuttisavolainen ER, and Kivirikko KI. Role of ascorbate in prolyl hydroxylase reaction. Biochem Biophys Res Comm 83: 441-448, 1978.
87. Ninomiya Y and Olsen BR. Synthesis and characterization of cDNA encoding a cartilage-specific short collagen. Proc Natl Acad Sci USA 81: 3014-3018, 1984.
88. Olsen BR. Collagen biosynthesis. In: Cell Biology of the Extracellular Matrix, edited by Hay ED. New York: Plenum Press, 1991, pp. 177-220.
89. Ottl J, Battistuta R, Pieper M, Tschesche H, Bode W, Kühn K, and Moroder L. Design and synthesis of heterotrimeric collagen peptides with a built-in cystine-knot. Models for collagen catabolism by matrix- metalloproteases. FEBS Lett 398: 31-36, 1996.
90. Ottl J, Gabriel D, Murphy G, Knauper V, Tominaga Y, Nagase H, Kröger M, Tschesche H, Bode W, and Moroder L. Recognition and catabolism of synthetic heterotrimeric collagen peptides by matrix metalloproteinases. Chem Biol 7: 119-132, 2000.
91. Ottl J and Moroder L. Disulfide-bridged heterotrimeric collagen peptides containing the collagenase cleavage site of collagen type I. Synthesis and conformational properties. J Am Chem Soc 121: 653-661, 1999.
92. Park C and Raines RT. Adjacent cysteine residues as a redox switch. Protein Engineer 14: 939-942, 2001.
93. Persikov AV, Ramshaw JAM, Kirkpatrick A, and Brodsky B. Amino acid propensities for the collagen triple-helix. Biochemistry 39: 14960-14967, 2000.
94. Persikov AV, Ramshaw JAM, Kirkpatrick A, and Brodsky B. Peptide investigations of pairwise interactions in the collagen triplehelix. J Mol Biol 316: 385-394, 2002.
95. Privalov PL. Stability of proteins. Proteins which do not present a single cooperative system. Adv Prot Chem 35: 1-104, 1982.
96. Prockop DJ and Kivirikko KI. Collagens. Molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64: 403-434, 1995.
97. Roth W and Heidemann E. Triple helix-coil transition of covalently bridged collagen-like peptides. Biopolymers 19: 1909-1917, 1980.
98. Roth W, Heppenheimer K, and Heidemann ER. Structure of collagen-like homopolytripeptides and heteropolytripeptides. IV. Polytripeptides by repetitive peptide-synthesis and bridging of oligopeptides. Macromol Chem Phys 180: 905-917, 1979.
99. Rump ET, Rijkers DTS, Hilbers HW, de Groot PG, and Liskamp RMJ. Cyclotriveratrylene (CTV) as a new chiral triacid scaffold capable of inducing triple helix formation of collagen peptides containing either a native sequence or Pro-Hyp-Gly repeats. Chem Eur J 8: 4613-4621, 2002.
100. Saccà B, Barth D, Musiol HJ, and Moroder L. Conformation-dependent side reactions in interstrand-disulfide bridging of trimeric collagenous peptides by regioselective cysteine chemistry. J Pept Sci 8: 205-210, 2002.
101. Saccà B, Fiori S, and Moroder L. Studies of the local conformational properties of the cell-adhesion domain of collagen type IV in synthetic heterotrimeric peptides. Biochemistry 42: 3429-3436, 2003.
102. Saccà B and Moroder L. Synthesis of heterotrimeric collagen peptides containing the a1b1 integrin recognition site of collagen type IV. J Pept Sci 8: 192-204, 2002.
103. Saccà B, Renner C, and Moroder L. The chain register in heterotrimeric collagen peptides affects triple helix stability and folding kinetics. J Mol Biol 324: 309-318, 2002.
104. Saccà B, Sinner EK, Kaiser J, Lübken C, Eble JA, and Moroder L. Binding and docking of synthetic heterotrimeric collagen type IV peptides with a1b1 integrin. ChemBioChem 3: 904-907, 2002.
105. n of defined molecular weights. Evidence for stabilization of collagen triple helix by hydroxyproline. Biochim Biophys Acta 303: 198-202, 1973.
106. Slatter DA, Foley LA, Peachey AR, Nietlispach D, and Farndale RW. Rapid synthesis of a register-specific heterotrimeric type I collagen helix encompassing the integrin a2b1 binding site. J Mol Biol 359: 289-298, 2006.
107. Snellman A, Keränen MR, Hägg PO, Lamberg A, Hiltunen JK, Kivirikko KI, and Pihlajaniemi T. Type XIII collagen forms homotrimers with three triple helical collagenous domains and its association into disulfide-bonded trimers is enhanced by prolyl 4-hydroxylase. J Biol Chem 275: 8936-8944, 2000.
108. Snellman A, Tu HM, Väisänen T, Kvist AP, Huhtala P, and Pihlajaniemi T. 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. EMBO J 19: 5051-5059, 2000.
109. 10 foldon. Structure 11: 339-346, 2003.
110. Tanaka T, Wada Y, Nakamura H, Doi T, Imanishi T, and Kodama T. A synthetic model of collagen structure taken from bovine macrophage scavenger receptor. FEBS Lett 334: 272-276, 1993.
111. Tao YZ, Strelkov SV, Mesyanzhinov VV, and Rossmann MG. Structure of bacteriophage T4 fibritin - A segmented coiled coil and the role of the C-terminal domain. Structure 5: 789-798, 1997.
112. Wang XH, Connor M, Smith R, Maciejewski MW, Howden MEH, Nicholson GM, Christie MJ, and King GF. Discovery and characterization of a family of insecticidal neurotoxins with a rare vicinal disulfide bridge. Nature Struct Biol 7: 505-513, 2000.
113. Welker E, Wedemeyer WJ, Narayan M, and Scheraga HA. Coupling of conformational folding and disulfide-bond reactions in oxidative folding of proteins. Biochemistry 40: 9059-9064, 2001.
114. Woolfson DN and Ryadnov MG. Peptide-based fibrous biomaterials - Some things old, new and borrowed. Curr Opin Chem Biol 10: 559-567, 2006.
115. Xia ZX, He YN, Dai WW, White SA, Boyd GD, and Mathews FS. Detailed active site configuration of a new crystal form of methanol dehydrogenase from Methylophilus W3A1 at 1.9 Ä resolution. Biochemistry 38: 1214-1220, 1999.
116. Yang W, Chan VC, Kirkpatrick A, Ramshaw JAM, and Brodsky B. Gly-Pro-Arg confers stability similar to Gly-Pro-Hyp in the collagen triple-helix of host-guest peptides. J Biol Chem 272: 28837-28840, 1997.