Supercoiled protein motifs: The collagen triple-helix and the α- helical coiled coil

Journal of Structural Biology

Volumn 122, Issue 1-2, 1998, Pages 17-29

  Beck, Konrad ^a   Brodsky, Barbara ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Coiled coils; Collagen; Extracellular matrix; Multidomain proteins; Peptides; Protein folding; Protein motifs; Protein structure; Sequence patterns; helix

Indexed keywords

ACETYLCHOLINESTERASE; CARBOHYDRATE BINDING PROTEIN; COLLAGEN; KERATIN; MEMBRANE PROTEIN; STRUCTURAL PROTEIN; TROPOMYOSIN;

ALPHA HELIX; AMINO ACID SEQUENCE; CRYSTAL STRUCTURE; EXTRACELLULAR MATRIX; LIGAND BINDING; MOLECULAR INTERACTION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; X RAY DIFFRACTION;

EID: 0031657823     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.1998.3965     Document Type: Article

References (83)

1. Astbury W. T. On the structure of biological fibres and the problem of muscle. Proc. R. Soc. B134:1947;303-328.
2. Biology of Invertebrate and Lower Vertebrate Collagens. 1985;Plenum Press, New York.
3. Balding S. D., Diaz L. A., Guidice G. J. A recombinant form of human BP180 ectodomain forms a collagen-like homotrimeric complex. Biochemistry. 36:1997;8821-8830.
4. Bamford J. K. H., Bamford D. H. Capsomer proteins of bacteriophage PRD1, a bacterial virus with a membrane. Virology. 177:1990;445-451.
5. Baum J., Brodsky B. Real-time NMR investigations of triple-helix folding and collagen folding diseases. Fold. Des. 2:1997;R53-R60.
6. Beck K., Dixon T. W., Engel J., Parry D. A. D. Ionic interactions in the coiled-coil domain of laminin determine the specificity of chain assembly. J. Mol. Biol. 231:1993;311-323.
7. Beck K., Boswell B. A., Ridgway C. C., Bächinger H. P. Triple helix formation of procollagen type I can occur at the rough endoplasmic reticulum membrane. J. Biol. Chem. 271:1996;21566-21573.
8. Beck K., Gambee J. E., Kamawal A., Bächinger H. P. A single amino acid can switch the oligomerization state of the α-helical coiled-coil of cartilage matrix protein. EMBO J. 16:1997;3767-3777.
9. Bella J., Eaton M., Brodsky B., Berman H. M. Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution. Science. 266:1994;75-81.
10. Bella J., Brodsky B., Berman H. M. Hydration structure of a collagen peptide. Structure. 3:1995;893-906.
11. Brown J. H., Cohen C., Parry D. A. D. Heptad breaks in α-helical coiled coils: Stutters and stammers. Proteins. 26:1996;134-145.
12. Chan V. C., Ramshaw J. A. M., Kirkpatrick A., Beck K., Brodsky B. Positional preferences of ionizable residues in Gly-X-Y triplets of the collagen triple-helix. J. Biol. Chem. 272:1997;31441-31446.
13. Celerin M., Ray J. M., Schisler N. J., Day A. W., Stetler-Stevenson W. G., Laudenbach D. E. Fungal fimbrae are composed of collagen. EMBO J. 15:1996;4445-4453.
14. Charalambous B. M., Keen J., McPherson M. J. Collagen-like sequences stabilize homotrimers of a bacterial hydrolase. EMBO J. 7:1988;2903-2909.
15. Cohen C. Design and function of fibrous proteins. Wolstenholme G. E. W., O'Connor M. CIBA Foundation Symposium: Principles of Biomolecular Organization. 1966;101-129 Churchill, London.
16. Cohen C., Bear R. S. Helical polypeptide chain configuration in collagen. J. Am. Chem. Soc. 75:1953;2783-2784.
17. Cohen C., Holmes K. C. X-ray diffraction evidence for α-helical coiled coils in native muscle. J. Mol. Biol. 6:1963;423-432.
18. Crick F. H. C. The packing of α-helices: Simple coiled-coils. Acta Crystallogr. 6:1953;689-697.
19. Deutzmann R., Aumailley M., Wiedemann H., Pysny W., Timpl R., Edgar D. Cell adhesion, spreading and neurite stimulation by laminin fragment E8 depends on maintenance of secondary and tertiary structure in its rod and globular domain. Eur. J. Biochem. 191:1990;513-522.
20. Doege K. J., Fessler J. H. Folding of carboxyl domain and assembly of procollagen I. J. Biol. Chem. 261:1986;8924-8934.
21. Drees B. L., Grotkopp E. K., Nelson H. C. M. The GCN4 leucine zipper can functionally substitute for the heat shock transcription factor's trimerization domain. J. Mol. Biol. 273:1997;61-74.
22. Elomaa O., Kangas M., Sahlberg C., Tuukkanen J., Sormunen R., Liakka A., Thesleff I., Kraal G., Tryggvason K. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell. 80:1995;603-609.
23. nn. Biopolymers. 16:1977;601-622.
24. Engel J., Prockop D. J. 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.
25. Ferguson B. M., Brockdorff N., Formstone E., Ngyuen T., Kronmiller J. E., Zonana J. Cloning ofTabby. Hum. Mol. Genet. 6:1997;1589-1594.
26. Fields G. B., Prockop D. J. Perspectives on synthesis and applications of triple-helical collagen model peptides. Biopolymers. 40:1996;345-357.
27. Fraser R. D. B., MacRae T. P. Conformation in Fibrous Proteins. 1973;Academic Press, New York.
28. Fraser R. D. B., MacRae T. P., Suzuki E. Chain conformation in the collagen molecule. J. Mol. Biol. 129:1979;463-481.
29. Goodman M., Feng Y., Melacini G., Taulane J. P. A template-inducedincipient. J. Am. Chem. Soc. 118:1996;5156-5157.
30. Harbury P. B., Zhang T., Kim P. S., Alber T. A switch between two-, three-, and four-stranded coiled-coils in GCN4 leucine zipper mutants. Science. 262:1993;1401-1407.
31. Harbury P. B., Kim P. S., Alber T. Crystal structure of an isoleucine-zipper trimer. Nature. 371:1994;80-83.
32. Hoppe H. J., Reid K. B. M. Collectins - soluble proteins containing collagenous regions and lectin domains - and their roles in innate immunity. Protein Sci. 3:1994;1143-1158.
33. Hoppe H. J., Barlow P. N., Reid K. B. M. A parallel three stranded α-helical bundle at the nucleation site of collagen triple-helix formation. FEBS Lett. 344:1994;191-195.
34. Hunter I., Schulthess T., Bruch M., Beck K., Engel J. Evidence for a specific mechanism of laminin assembly. Eur. J. Biochem. 188:1990;205-211.
35. Hurst H. C. Transcription factors 1: bZIP proteins. Protein Profile. 2:1995;101-168.
36. Ichijo H., Hellman U., Wernstedt C., Gonez L. J., Claesson-Welsh L., Heldin C.-H., Miyazono K. Molecular cloning and characterization of ficolin, a multimeric protein with fibrinogen- and collagen-like domains. J. Biol. Chem. 268:1993;14505-14513.
37. Kadler K. Extracellular Matrix 1: Fibril-forming collagens. Protein Profile. 2:1995;491-619.
38. Kammerer R. A. Alpha-helical coiled-coil oligomerization domains in extracellular proteins. Matrix Biol. 15:1997;555-565.
39. Kammerer R. A., Schulthess T., Landwehr R., Lustig A., Engel J. Tenascin-C hexabrachion assembly is a sequential two-step process initiated by coiled-coil α-helices. J. Biol. Chem. 1998.
40. Kielty C. M., Hopkinson I., Grant M. E. The collagen family: Structure, assembly, and organization in the extracellular matrix. Royce P. M., Steinmann B. Connective Tissue and Its Heritable Disorders. 1993;103-147 Wiley-Liss, New York.
41. Kodama T., Freeman M., Rohrer L., Zabrecky J., Matsudaira P., Krieger M. Type I macrophage scavenger receptor contains α-helical and collagen-like coiled coils. Nature. 343:1990;531-535.
42. Kohn W. D., Mant C. T., Hodges R. S. α-Helical protein assembly motifs. J. Biol. Chem. 272:1997;2583-2586.
43. Kondo N., Kondo J. Identification of novel blood proteins specific for mammalian hibernation. J. Biol. Chem. 267:1992;473-478.
44. Krejci E., Coussen F., Duval N., Chatel J.-M., Legay C., Puype M., Vandekerckhove J., Cartaud J., Bon S., Massoulié T. Primary structure of a collagenic tail peptide ofTorpedo. EMBO J. 10:1991;1285-1293.
45. Krieger M., Acton S., Ashkenas J., Pearson A., Penman M., Resnick D. Molecular flypaper, host defense, and atherosclerosis. Structure, binding properties, and functions of macrophage scavenger receptor. J. Biol. Chem. 268:1993;4569-4572.
46. Kuivaniemi K., Tromp G., Prockop D. J. Mutations in fibrillar collagens (types I, II, III, and XI), fibril-associated collagen (type IX), and network-forming collagen (type X) cause a spectrum of diseases of bone, cartilage and blood vessels. Hum. Mutat. 9:1997;300-315.
47. Lamberg A., Helaakoski T., Myllyharju J., Peltonen S., Notbohm H., Pihlajaniemi T., Kivirikko K. I. Characterization of human type III collagen expressed in a baculovirus system. J. Biol. Chem. 271:1996;11988-11995.
48. Lees J. F., Tasab M., Bulleid N. J. Identification of the molecular recognition sequence which determines the type-specific assembly of procollagen. EMBO J. 16:1997;908-916.
49. Li K., Tamai K., Tan E. M. L., Uitto J. Cloning of type XVII collagen. J. Biol. Chem. 268:1993;8825-8834.
50. Liu X., Siegel D. L., Fan P., Brodsky B., Baum J. Direct NMR measurement of the folding kinetics of a trimeric peptide. Biochemistry. 35:1996;4306-4313.
51. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science. 252:1991;1162-1164.
52. Lupas A. Coiled coils: New structures and new functions. Trends Biochem. Sci. 21:1996;375-382.
53. Lupas A. Predicting coiled-coil regions in proteins. Curr. Opin. Struct. Biol. 7:1997;388-393.
54. Maeda K., Okubo K., Shimomura I., Funahashi T., Matsuzawa Y., Matsubara K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (Adipose most abundant gene transcript 1). Biochem. Biophys. Res. Commun. 221:1996;286-289.
55. Malashkevich V. N., Kammerer R. A., Efimov V. P., Schulthess T., Engel J. The crystal structure of a five-stranded coiled coil in COMP: a prototype ion channel. Science. 274:1996;761-765.
56. Mayo K. H. NMR and x-ray studies of collagen model peptides. Biopolymers. 40:1996;359-370.
57. McBride O. W., Harrington W. F. Helix-coil transition in collagen. Evidence for a single-stranded triple helix. Biochemistry. 6:1967;1499-1514.
58. McBride D. J. Jr., Choe V., Shapiro J. R., Brodsky B. Altered collagen structure in mouse tail tendon lacking the α2(I) chain. J. Mol. Biol. 270:1997;275-284.
59. Miner J. H., Lewis R. M., Sanes J. R. Molecular cloning of a novel laminin chain, alpha 5, and widespread expression in adult mouse tissues. J. Biol. Chem. 270:1995;28523-28526.
60. Odgren P. R., Harvie L. W. Jr., Fey E. G. Phylogenetic occurrence of coiled-coil proteins: Implications for tissue structure in metazoavia. Proteins. 24:1996;467-484.
61. 10. J. Mol. Biol. 152:1981;427-443.
62. Ohashi T., Erickson H. P. Two oligomeric forms of plasma ficolin have differential Lectin activity. J. Biol. Chem. 272:1997;14220-14226.
63. Parry D. A. D. Coiled-coils in α-helix containing proteins. Analysis of the residue types within the heptad repeat and the use of these data in the prediction of coiled-coils in other proteins. Biosci. Rep. 2:1982;1017-1024.
64. Parry D. A. D., Dixon T. W., Cohen C. Analysis of the three α-helix motif in the spectrin superfamily of proteins. Biophys. J. 61:1992;858-867.
65. Pauling L., Corey R. B. The structure of fibrous proteins of the collagen-gelatin group. Proc. Natl. Acad. Sci. USA. 37:1951a;272-281.
66. Pauling L., Corey R. B. The structure of hair, muscle, and related proteins. Proc. Natl. Acad. Sci. USA. 37:1951b;261-271.
67. Pauling L., Corey R. B. Compound helical configurations of polypeptide chains: structure of proteins of the α-keratin type. Nature. 171:1953;59-61.
68. Privalov P. L. Stability of proteins. Proteins which do not present a single cooperative system. Adv. Prot. Chem. 35:1982;1-104.
69. Ramachandran G. N., Kartha G. Structure of collagen. Nature. 174:1954;269-270.
70. Ramachandran G. N., Kartha G. Structure of collagen. Nature. 176:1955;593-595.
71. Ramachandran G. N., Doyle B. B., Blout E. R. Single-chain triple-helical structure. Biopolymers. 6:1968;1771-1775.
72. Ramshaw J. A. M., Shah N. K., Brodsky B. Gly-X-Y tripeptide frequencies in collagen: A context for host-guest triple-helix peptides. J. Struct. Biol. 1998.
73. Resnick D., Chatterton J. E., Schwartz K., Slayter H., Krieger M. Structure of class A macrophage scavenger receptors. Electron microscopic study of flexible, multidomain, fibrous proteins and determination of the disulfide bond pattern of the scavenger receptor cysteine-rich domain. J. Biol. Chem. 271:1996;26924-26930.
74. Rich A., Crick F. H. C. The molecular structure of collagen. J. Mol. Biol. 3:1961;483-506.
75. Sherrif S., Chang C. Y., Ezekowitz R. A. B. Human mannose-binding protein carbohydrate recognition domain trimerizes through a triple α-helical coiled-coil. Nature Struct. Biol. 1:1994;789-794.
76. Sodek J., Hodges R. S., Smillie L. B., Jurasek L. Amino acid sequence of rabbit skeletal tropomyosin and its coiled-coil structure. Proc. Natl. Acad. Sci. USA. 69:1972;3800-3804.
77. Sosnick T. R., Jackson S., Wilk R. R., Englander S. W., DeGrado W. F. The role of helix formation in the folding of a fully α-helical coiled coil. Proteins. 24:1996;427-432.
78. Srivastava A. K., Pispa J., Hartung A. J., Du Y., Ezer S., Jenks T., Shimada T., Pekkanen M., Mikkola M. L., Ko M. S. H., Thesleff I., Kere J., Schlessinger D. The Tabby phenotype is caused by mutation in a mouse homologue of theEDA. Proc. Natl. Acad. Sci. USA. 94:1997;13069-13074.
79. Stern M., Stern R. A collagenous sequence in a prokaryotic hyaluronidase. Mol. Biol. Evol. 9:1992;1179-1180.
80. Weis W. I., Drickamer K. Trimeric structure of a C-type mannose-binding protein. Structure. 2:1994;1227-1240.
81. Whitby F. G., Kent H., Stewart F., Stewart M., Xie X., Hatch V., Cohen C., Phillips G. N. Jr. Structure of tropomyosin at 9 Ångstroms resolution. J. Mol. Biol. 227:1992;441-452.
82. Yan Y., Winograd E., Viel A., Cronin T., Harrison S. C., Branton D. Crystal structure of the repetitive segments of spectrin. Science. 262:1993;2027-2030.
83. Yang C. H., Lambie E. J., Snyder M. NuMA: An unusual long coiled-coil related protein in the mammalian nucleus. J. Cell Biol. 116:1992;1303-1317.