A current viewpoint on structure and evolution of collagens. I. Fibrillar collagens

Journal of Evolutionary Biochemistry and Physiology

Volumn 48, Issue 2, 2012, Pages 127-139

  Ivanova, V P ^a   Krivchenko, A I ^a  

^a SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

Author keywords

evolution; extracellular matrix; fibrillar collagens; fibrillogenesis; multidomain proteins

Indexed keywords

EID: 84862023613     PISSN: 00220930     EISSN: None     Source Type: Journal    
DOI: 10.1134/S0022093012020016     Document Type: Review

References (78)

1. van der Rest, M. and Garrone, R., Collagen Family of Proteins, FASEB J., 1991, vol. 5, pp. 2814-2823.
2. Ricard-Blum, S. and Ruggiero, F., The Collagen Superfamily: from the Extracellular Matrix to the Cell Membrane, Pathol. Biol., 2005, vol. 53, pp. 430-442.
3. Fraser, R. D., MacRae, T. P., and Suzuki, E., Chain Conformation in the Collagen Molecule, J. Mol. Biol., 1979, vol. 129. pp. 463-481.
4. Shoulders, M. D. and Raines, R. T., Collagen Structure and Stability, Annu. Rev. Biochem., 2009, vol. 78, pp. 929-958.
5. Di Lullo, G. A., Sweeney, S. M., Korkko, J., Ala-Kokko, L., and San Antonio, J. D., Mapping the Ligand-Binding Sites and Disease-Associated Mutations on the Most Abundant Protein in the Human, Type I Collagen, J. Biol. Chem., 2002, vol. 277, pp. 4223-4231.
6. Rossert, J., Terraz, C., and Dupont, S., Regulation of Type I Collagen Genes Expression, Nephrol. Dial. Transplant. 2000, vol. 15, pp. 66-68.
7. van der Mark, K., Localization of Collagen Types in Tissues, Int. Rev. Connect. Tissue Res., 1981, vol. 9, pp. 265-324.
8. Birk, D. E., Type V Collagen: Heterotypic Type I/V Collagen Interactions in the Regulation of Fibril Assembly, Micron, 2001, vol. 32, pp. 223-237.
9. Gopalakrishnan, B., Wang, W. M., and Greenspan, D. S., Biosynthetic Processing of the Pro-αl(V) Pro-α2(V) / Pro-α3(V) Procollagen Heterotrimer, J. Biol. Chem., 2004, vol. 279, pp. 30 904-30 912.
10. Bowen, K. B., Reimers, A. P., Luman, S., Kronz, J. D., Fyffe, W. E., and Oxford, J. T., Immunohistochemical Localization of Collagen Type XI α1 and α2 Chains in Human Colon Tissue, J. Histochem. Cytochem., 2008, vol. 56, pp. 275-283.
11. Vuristo, M. M., Pihlajamaa, T., Vandenberg, P., Prockop, D. J., and Ala-Kokko, L., The Human COL11A2 Gene Structure Indicates That the Gene Has Not Evolved with the Genes for the Major Fibrillar Collagens, J. Biol. Chem., 1995, vol. 270, pp. 22 873-22 881.
12. Koch, M., Laub, F., Zhou, P., Hahn, R. A., Tanaka, S., Burgeson, R. E., Gerecke, D. R., Ramirez, F., and Gordon, M. K., Collagen XXIV, a Vertebrate Fibrillar Collagen with Structural Features of Invertebrate Collagens: Selective Expression in Developing Cornea and Bone, J. Biol. Chem., 2003, vol. 278, pp. 43 236-43 244.
13. Matsuo, N., Tanaka, S., Yoshioka, H., Koch, M., Gordon, M. K., and Ramirez, F., Collagen XXIV (Col24al) Gene Expression Is a Specific Marker of Osteoblast Differentiation and Bone Formation, Connect. Tissue Res., 2008, vol. 49, pp. 68-75.
14. Boot-Handford, R. P., Tuckwell, D. S., Plumb, D. A., Rock, C. F., and Poulsom, R., A Novel and Highly Conserved Collagen [pro(α) l(XXVII)], with a Unique Expression Pattern and Unusual Molecular Characteristics, Establishes a New Clade within the Vertebrate Fibrillar Collagen Family, J. Biol. Chem., 2003, vol. 278, pp. 31 067-31 077.
15. Hjorten, R., Hansen, U., Underwood, R. A., Telfer, H. E., Fernandes, R. J., Krakow, D., Sebald, E., Wachsmann-Hogiu, S., Bruckner, P., Jacquet, R., Landis, W. J., Byers, P. H., and Pace, J. M., Type XXVII Collagen at the Transition of Cartilage to Bone during Skeletogenesis, Bone, 2007, vol. 41, pp. 535-542.
16. Pace, J. M., Corrado, M., Missero, C., and Byers, P. H., Identification, Characterization and Expression Analysis of a New Fibrillar Collagen Gene, COL27A1, Matrix Biol., 2003, vol. 22, pp. 3-14.
17. Fallani, A., Kroll, B., Warner, L. R., Oxford, R. J., Irwin, K. M., Mercer, L. M., Shadle, S. E., and Oxford, J. T., Structural Model of the Amino Propeptide of Collagen XI α 1 Chain with Similarity to the LNS Domains, Protein Sci., 2005, vol. 14, pp. 1526-1537.
18. Hohenester, E. and Engel, J., Domain Structure and Organization in Extracellular Matrix Proteins, Matrix Biol., 2002, vol. 21, pp. 115-128.
19. Gordon, M. K. and Hahn, R. A., Collagens, Cell Tissue Res., 2010, vol. 339, pp. 247-257.
20. Soderhdll, C., Marenholz, I., Kerscher, T., Ruschendorf, F., Esparza-Gordillo, J., Worm, M., Gruber, C., Mayr, G., Albrecht, M., Rohde, K., Schulz, H., Wahn, U., Hubner, N., and Lee, Y.-A., Variants in a Novel Epidermal Collagen Gene (COL29A1) Are Associated with Atopic Dermatitis, PLOS Biol., 2007, vol. 5, p. 242.
21. Khoshnoodi, J., Pedchenko, V., and Hudson, B. G., Mammalian Collagen IV, Microsc. Res. Tech., 2008, vol. 71, pp. 367-370.
22. Sutmuller, M., Bruijn, J. A., and de Heer, E., Collagen Types VIII and X, Two Non-Fibrillar, Short-Chain Collagens. Structure Homologies, Functions and Involvement in Pathology, Histol. Histopathol., 1997, vol. 12, pp. 557-566.
23. Ansorge, H. L., Meng, X., Zhang, G., Veit, G., Sun, M., Klement, J. F., Beason, D. P., Soslowsky, L. J., Koch, M., and Birk, D. E., Type XV Collagen Regulates Fibrillogenesis: Premature Collagen Fibril Growth and Tissue Dysfunction in Null Mice, J. Biol. Chem., 2009, vol. 284, pp. 8427-8438.
24. Fitzgerald, J. and Bateman, J. F., A New FACIT of the Collagen Family: COL21A1, FEBS Lett., 2001, vol. 505, pp. 275-280.
25. Gregory, K. E., Keene, D. R., Tufa, S. F., Lunstrum, G. P., and Morris, N. P., Developmental Distribution of Collagen Type XII in Cartilage: Association with Articular Cartilage and the Growth Plate, J. Bone Miner. Res., 2001, vol. 16, pp. 2005-2016.
26. Käpylä, J., Jäälinoja, J., Tulla, M., Ylöstalo, J., Nissinen, L., Viitasalo, T., Vehviläinen, P., Marjomäki, V., Nykvist, P., Säämänen, A.-M., Farndale, R. W., Birk, D. E., Ala-Kokko, L., and Heino, J., The Fibril-Associated Collagen IX Provides a Novel Mechanism for Cell Adhesion to Cartilaginous Matrix, J. Biol. Chem., 2004, vol. 279, pp. 51 677-51 687.
27. Kassner, A., Tiedemann, K., Notbohm, H., Ludwig, T., Morgelin, M., Reinhardt, D. P., Chu, M. L., Bruckner, P., and Grässel, S., Molecular Structure and Interaction of Recombinant Human Type XVI Collagen, J. Mol. Biol., 2004, vol. 339, pp. 835-853.
28. Koch, M., Foley, J. E., Hahn, R., Zhou, P., Burgeson, R. E., Gerecke, D. R., and Gordon, M. K., αl(XX) Collagen, a New Member of the Collagen Subfamily, Fibril-Associated Collagens with Interrupted Triple Helices, J. Biol. Chem., 2001, vol. 276, pp. 23 120-23 126.
29. Koch, M., Schulze, J., Hansen, U., Ashwodt, T., Keen, D. R., Brunken, W. J., Burgeson, R. E., Bruckner, P., and Bruckner-Tuderman, L., A Novel Marker of Tissue Junctions, Collagen XXII, J. Biol. Chem., 2004, vol. 279, pp. 22 514-22 521.
30. Myers, J. C., Li, D., Bageris, A., Abraham, V., Dion, A. S., and Amenta, P. S., Biochemical and Immunohistochemical Characterization of Human Type XIX Defines a Novel Class of Basement Membrane Zone Collagens, Am. J. Pathol., 1997, vol. 151, pp. 1729-1740.
31. Sato, K., Yomogida, K., Wada, T., Yorihuzi, T., Nishimune, Y., Hosokawa, N., Nagata, K., Type XXVI Collagen, a New Member of the Collagen Family, Is Specifically Expressed in the Testis and Ovary, J. Biol. Chem., 2002, vol. 277, pp. 37 678-37 684.
32. Veit, G., Kobbe, B., Keen, D. R., Paulsson, M., Koch, M., and Wagener, R., Collagen XXVIII, a Novel von Willebrand Factor A Domain-Containing Protein with Many Imperfections in the Collagenous Domain, J. Biol. Chem., 2006, vol. 281, pp. 3494-3504.
33. Kivirikko, S., Li, K., Christiano, A. M., and Uitto, J., Cloning of Mouse Type VII Collagen Reveals Evolutionary Conservation of Functional Protein Domains and Genomic Organization, J. Invest. Dermatol., 1996, vol. 106, pp. 1300-1306.
34. Banyard, J., Bao, L., and Zetter, B. R., Type XXIII Collagen, a New Transmembrane Collagen Identified in Metastatic Tumor Cells, J. Biol. Chem., 2003, vol. 278, pp. 20 989-20 994.
35. Franzke, C. W., Bruckner-Tuderman, L., and Blobel, C. P., Shedding of Collagen XVII/BP 180 in Skin Depends on Both ADAM10 and ADAM9, J. Biol. Chem., 2009, vol. 284, pp. 23 386-23 396.
36. Amenta, P. S., Scivoletti, N. A., Newman, M. D., Sciancalepore, J. P., Li, D., and Myers, J. C., Proteoglycan-Collagen XV in Human Tissues Is Seen Linking Banded Collagen Fibers Subjacent to the Basement Membrane, J. Histochem. Cytochem., 2005, vol. 53, pp. 165-176.
37. Latvanlehto, A., Snellman, A., Tu, H., and Pihlajaniemi, T., Type XIII Collagen and Some Other Transmembrane Collagens Contain Two Separate Coiled-Coil Motifs, Which May Function as Independent Oligomerization Domains, J. Biol. Chem., 2003, vol. 278, pp. 37 590-37 599.
38. Marneros, A. G. and Olsen, B. R., Physiological Role of Collagen XVIII and Endostatin, FASEB J., 2005, vol. 19, pp. 716-728.
39. Tong, Y., Hu, Y., Scearce-Levie, K., Ptaček, L. J., and Fu, Y.-H., COL25A1 Triggers and Promotes Alzheimer's Disease-Like Pathology in vivo, Neurogenetics, 2010, vol. 11, pp. 41-52.
40. Exposito, J. Y., Cluzel, C., Garrone, R., and Lethias, C., Evolution of Collagens, The Anatom. Record, 2002, vol. 268, pp. 302-316.
41. Shah, N. K., Sharma, M., Kirkpatrick, A., Ramshaw, J. A., and Brodsky, B., Gly-Gly-Containing Triplets of Low Stability Adjacent to a Type III Collagen Epitope, Biochemistry, 1997, vol. 36, pp. 5878-5883.
42. Hulmes, D. J., Building Collagen Molecules, Fibrils and Suprafibrillar Structures, J. Struct. Biol., 2002, vol. 137, pp. 2-10.
43. Koivu, J., Disulfide Bonding as a Determinant of the Molecular Composition of Types I, II and III Procollagen, FEBS Lett., 1987, vol. 217, pp. 216-220.
44. Malone, J. P., Alvares, K., and Veis, A., Structure and Assembly of the Heterotrimeric and Homotrimeric C-Propeptides of Type I Collagen: Significance of the α2(I) Chain, Biochemistry, 2005, vol. 44, pp. 15 269-15 279.
45. Dion, A. S. and Myers, J. C., COOH-Terminal Propeptides of the Major Human Procollagenes. Structural, Functional and Genetic Comparisons, J. Mol. Biol., 1987, vol. 193, pp. 127-143.
46. Lees, J. F., Tasab, M., and Bulleid, N. J., Identification of the Molecular Recognition Sequence, Which Determines the Type-Specific Assembly of Procollagen, EMBO J., 1997, vol. 16, pp. 908-916.
47. Hulmes, D. J. and Miller, A., Molecular Packing in Collagen, Nature, 1981, vol. 293, pp. 234-239.
48. Silver, D., Miller, J., Harrison, R., and Prockop, D. J., Helical Model of Nucleation and Propagation to Account for the Growth of Type I Collagen Fibrils from Symmetrical Pointed Tips: a Special Example of Self-Assembly of Rod-Like Monomers, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 9860-9864.
49. Kuznetsova, N. and Leikin, S., Does the Triple Helical Domain of Type I Collagen Encode Molecular Recognition and Fiber Assembly while Telopeptides Serve as Catalytic Domains? Effect of Proteolytic Cleavage on Fibrillogenesis and on Collagen-Collagen Interaction in Fibers, J. Biol. Chem., 1999, vol. 274, pp. 36 083-36 088.
50. Comper, W. D. and Veis, A., The mechanism of Nucleation for in vitro Collagen Fibril Formation, Biopolymers, 1977, vol. 16, pp. 2113-2131.
51. Prockop, D. J. and Fertala, A., Inhibition of the Self-Assembly of Collagen I into Fibrils with Synthetic Peptides. Demonstration That Assembly is Driven by Specific Binding Sites on the Monomers, J. Biol. Chem., 1998, vol. 273, pp. 15 598-15 604.
52. Knott, L. and Bailey, A. J., Collagen Cross-Links in Mineralizing Tissues: a Review of Their Chemistry, Function, and Clinical Relevance, Bone, 1998, vol. 22, pp. 181-187.
53. Malone, J. P., George, A., and Veis, A., Type I Collagen N-Telopeptides Adopt an Ordered Structure when Docked to Their Helix Receptor during Fibrillogenesis, Proteins, 2004, vol. 54, pp. 206-215.
54. Jelinski, L. W., Sullivan, C. E., Batchelder, L. S., and Torchia, D. A., Deuterium Nuclear Magnetic Resonance of Specifically Labeled Native Collagen. Investigation of Protein Molecular Dynamics Using the Quadrapolar Echo Technique, Biophys. J., 1980, vol. 32, pp. 515-529.
55. Blaschke, U. K., Eikenberry, E. F., Hulmes, D. J., Galla, H.-J., and Bruckner, P., Collagen XI Nucleates Self-Assembly and Limits Lateral Growth of Cartilage Fibrils, J. Biol. Chem., 2000, vol. 275, pp. 10 370-10 378.
56. Holmes, D. F. and Kadler, K. E., The 10+4 Microfibril Structure of Thin Cartilage Fibrils, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 17 249-17 254.
57. Gregory, K. E., Oxford, J. T., Chen, Y., Gambee, J. E., Gygi, S. P., Aebersold, R., Neame, P. J., Mechling, D. E., Bachinger, H. P., and Morris, N. P., Structural Organization of Distinct Domains within the Non-Collagenous N-Terminal Region of Collagen Type XI, J. Biol. Chem., 2000, vol. 275, pp. 11 498-11 506.
58. Medeck, R. J., Sosa, S., Morris, N. P., and Oxford, J. T., BMP-1-Mediated Proteolytic Processing of Alternatively Spliced Isoforms of Collagen Type XI, Biochem. J., 2003, vol. 376, pp. 361-368.
59. Pihlajamaa, T., Lankinen, H., Ylöstalo, J., Valmu, L., Jäälinoja, J., Zaucke, F., Spitznagel, L., Gösling, S., Puustinen, A., Mörgelin, M., Peränen, J., Maurer, P., Ala-Kokko, L., and Kilpeläinen, I., Characterization of Recombinant Amino-Terminal NC4 Domain of Human Collagen IX: Interaction with Glycosaminoglycans and Cartilage Oligomeric Matrix Protein, J. Biol. Chem., 2004, vol. 279, pp. 24 265-24 273.
60. Meek, K. M. and Fullwood, N. J., Corneal and Scleral Collagens-a Microscopic's Perspective, Micron, 2001, vol. 32, pp. 261-272.
61. Kadler, K. E., Hill A., and Canty-Laird, E. G., Collagen Fibrillogenesis: Fibronectin, Integrins, and Minor Collagens as Organizers and Nucleators, Curr. Opin. Cell Biol., 2008, vol. 20, pp. 495-501.
62. 2-Terminal Domain, a Putative Regulator of Corneal Fibrillogenesis, J. Cell Biol., 1993, vol. 121, pp. 1181-1189.
63. Thom, J. R. and Morris, N. P., Biosynthesis and Proteolytic Processing of Type XI Collagen in Embryonic Chick Sterna, J. Biol. Chem., 1991, vol. 266, pp. 7262-7269.
64. Chanut-Delalande, H., Fichard, A., Bernocco, S., Garrone, R., Hulmes, D. J., and Ruggiero, F., Control of Heterotypic Fibril Formation by Collagen V is Determined by Chain Stoichiometry, J. Biol. Chem., 2001, vol. 276, pp. 24 352-24 359.
65. Plumb, D. A., Dhir, V., Mironov, A., Ferrara, L., Poulsom, R., Kadler, K. E., Thornton, D. J., Briggs, M. D., and Boot-Handford, R. P., Collagen XXVII Is Developmentally Regulated and Forms Thin Fibrillar Structures Distinct from Those of Classical Vertebrate Fibrillar Collagens, J. Biol. Chem., 2007, vol. 282, pp. 12 791-12 795.
66. Yamada, Y., Avvedimento, V. E., Mudryj, M., Ohkubo, H., Vogeli, G., Irani, M., Pastan, I., and de Crombrugghe, B., The Collagen Gene: Evidence for Its Evolutionary Assembly by Amplification of a DNA Segment Containing an Exon of 54 bp, Cell, 1980, vol. 22, pp. 887-892.
67. Ratner, V. A., External and Internal Factors and Limitations of Molecular Evolution, Sovremennye problemy teorii evolyutsii (Current Problems of Theory of Evolution), Tatarinov, L. P., Ed., Moscow, Nauka, 1993, pp. 60-80.
68. Exposito, J. Y., Cluzel, C., Lethias, C., and Garrone, R., Tracing the Evolution of Vertebrate Fibrillar Collagens from an Ancestral α Chain, Matrix Biol., 2000, vol. 19, pp. 275-279.
69. Takahara, K., Hoffman, G. G., and Greenspan, D. S., Complete Structural Organization of the Human α l(V) Collagen Gene (COL5A1): Divergence from the Conserved Organization of Other Characterized Fibrillar Collagen Genes, Genomics, 1995, vol. 29, pp. 588-597.
70. Vuoristo, M. M., Pihlajamaa, T., Vandenberg, P., Prockop, D. J., and Ala-Kokko, L., The Human COL11A2 Gene Structure Indicates That the Gene Has Not Evolved with the Genes for the Major Fibrillar Collagens, J. Biol. Chem., 1995, vol. 270, pp. 22 873-22 881.
71. Exposito, J. Y., Larroux, C., Cluzel, C., Valcourt, U., Lethias, C., and Degnan, B. M., Demosponge and Sea Anemone Fibrillar Collagen Diversity Reveals the Early Emergence of A/C Clades and the Maintenance of the Modular Structure of Type V/XI Collagens from Sponge to Human, J. Biol. Chem., 2008, vol. 283, pp. 28 226-28 235.
72. Boot-Handford, R. P. and Tuckwell, D. S., Fibrillar Collagen: the Key to Vertebrate Evolution? A Tale of Molecular Incest, Bioessays, 2003, vol. 25, pp. 142-151.
73. Aouacheria, A., Cluzel, C., Lethias, C., Gouy, M., Garrone, R., and Exposito, J. Y., Invertebrate Data Predict an Early Emergence of Vertebrate Fibrillar Collagen Clades and Anti-Incest Model, J. Biol. Chem., 2004, vol. 279, pp. 47 711-47 719.
74. Bailey, W. J., Kim, J., Wagner, G. P., and Ruddle, F. H., Phylogenetic Reconstruction of Vertebrate Hox Cluster Duplications, Mol. Biol. Evol., 1997, vol. 14, pp. 843-853.
75. Smith, N. G., Knight, R., and Hurst, L. D., Vertebrate Genome Evolution: a Slow Shuffle or a Big Bang?, Bioessays, 1999, vol. 21, pp. 697-703.
76. Gilbert, W., Why Genes in Pieces?, Nature, 1978, vol. 271, p. 501.
77. Long, M., Evolution of Novel Genes, Curr. Opin. Genet. Devol., 2001, vol. 11, pp. 673-680.
78. Bornberg-Bauer, E., Beaussart, F., Kummerfeld, S. K., Teichmann, S. A., and Weiner, J., The Evolution of Domain Arrangements in Proteins and Interaction Networks, Cell. Mol. Life Sci., 2005, vol. 62, pp. 435-445.