Interruptions in the collagen repeating tripeptide pattern can promote supramolecular association

Protein Science

Volumn 19, Issue 5, 2010, Pages 1053-1064

  Hwang, Eileen S ^a   Thiagarajan, Geetha ^a   Parmar, Avanish S ^a   Brodsky, Barbara ^a  

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

Author keywords

Aggregation; Amyloid; Collagen; Peptide; Self assembly; Triple helix

Indexed keywords

ALANINE; COLLAGEN; GLYCINE; PROLINE; THIOFLAVINE;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; COLLAGEN DEGRADATION; DIFFERENTIAL SCANNING CALORIMETRY; GENETIC DISORDER; LIGAND BINDING; MISSENSE MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; TRIPLE HELIX;

AMINO ACID SEQUENCE; AMYLOID; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; COLLAGEN TYPE IV; HUMANS; LIGHT; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; OLIGOPEPTIDES; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; SCATTERING, RADIATION;

EID: 77951558891     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.383     Document Type: Article

References (54)

1. Ramachandran GN, Kartha G (1955) Structure of collagen. Nature 176:593-595.
2. Rich A, Crick FH (1961) The molecular structure of collagen. J Mol Biol 3:483-506.
3. Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78:929-958.
4. Kielty C, Grant M, The collagen family: structure, assembly and organization in the extracellular matrix. In: Royce PM, Steinmann BU, Eds. (2002) Connective tissue and its heritable disorders: molecular, genetic, and medical aspects. New York: Wiley-Liss, pp 159-222.
5. Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33-43.
6. Ricard-Blum S, Ruggiero F (2005) The collagen superfamily: from the extracellular matrix to the cell membrane. Pathol Biol (Paris) 53:430-442.
7. Veit G, Kobbe B, Keene DR, Paulsson M, Koch M, Wagener R (2006) Collagen XXVIII, a novel von Willebrand factor A domain-containing protein with many imperfections in the collagenous domain. J Biol Chem 281:3494-3504.
8. Boot-Handford RP, Tuckwell DS, Plumb DA, Rock CF, Poulsom R (2003) A novel and highly conserved collagen (proa1(XXVII)) with a unique expression pattern and unusual molecular characteristic establishes a new clade within the vertebrate fibrillar collagen family. J Biol Chem 278:31067-31077.
9. Koch M, Laub F, Zhou P, Hahn RA, Tanaka S, Burgeson RE, Gerecke DR, Ramirez F, Gordon MK (2003) Collagen XXIV, a vertebrate fibrillar collagen with structural features of invertebrate collagens: selective expression in developing cornea and bone. J Biol Chem 278:43236-43244.
10. Hudson BG, Tryggvason K, Sundaramoorthy M, Neilson EG (2003) Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N Engl J Med 348: 2543-2556.
11. Burgeson RE (1993) Type VII collagen, anchoring fibrils, and epidermolysis bullosa. J Invest Dermatol 101:252-255.
12. Brodsky B, Persikov AV (2005) Molecular structure of the collagen triple helix. Adv Protein Chem 70:301-339.
13. Jenkins CL, Raines RT (2002) Insights on the conformational stability of collagen. Nat Prod Rep 19:49-59.
14. Renner C, Sacca B, Moroder L (2004) Synthetic heterotrimeric collagen peptides as mimics of cell adhesion sites of the basement membrane. Biopolymers 76: 34-47.
15. Bella J, Liu J, Kramer R, Brodsky B, Berman HM (2006) Conformational effects of Gly-X-Gly interruptions in the collagen triple helix. J Mol Biol 362: 298-311.
16. Li Y, Brodsky B, Baum J (2007) NMR shows hydrophobic interactions replace glycine packing in the triple helix at a natural break in the (Gly-X-Y)n repeat. J Biol Chem 282:22699-22706.
17. Thiagarajan G, Li Y, Mohs A, Strafaci C, Popiel M, Baum J, Brodsky B (2008) Common interruptions in the repeating tripeptide sequence of non-fibrillar collagens: sequence analysis and structural studies on triple-helix peptide models. J Mol Biol 376:736-748.
18. Mohs A, Popiel M, Li Y, Baum J, Brodsky B (2006) Conformational features of a natural break in the type IV collagen Gly-X-Y repeat. J Biol Chem 281: 17197-17202.
19. Feng Y, Melacini G, Taulane JP, Goodman M (1996) Collagen-based structures containing the peptoid residue N-isobutylglycine (Nleu): synthesis and biophysical studies of Gly-Pro-Nleu sequences by circular dichroism, ultraviolet absorbance, and optical rotation. Biopolymers 39:859-872. (Pubitemid 126545738)
20. Persikov AV, Ramshaw JA, Brodsky B (2005) Prediction of collagen stability from amino acid sequence. J Biol Chem 280:19343-19349. (Pubitemid 41379641)
21. Persikov AV, Xu Y, Brodsky B (2004) Equilibrium thermal transitions of collagen model peptides. Protein Sci 13:893-902. (Pubitemid 38429213)
22. Miles AJ, Knutson JR, Skubitz AP, Furcht LT, McCarthy JB, Fields GB (1995) A peptide model of basement membrane collagen alpha 1 (IV) 531-543 binds the alpha 3 beta 1 integrin. J Biol Chem 270:29047-29050.
23. Berisio R, Vitagliano L, Mazzarella L, Zagari A (2000) Crystal structure of a collagen-like polypeptide with repeating sequence Pro-Hyp-Gly at 1.4 A resolution: implications for collagen hydration. Biopolymers 56: 8-13.
24. Kar K, Amin P, Bryan MA, Persikov AV, Mohs A, Wang YH, Brodsky B (2006) Self-association of collagen triple helic peptides into higher order structures. J Biol Chem 281:33283-33290. (Pubitemid 46036711)
25. Morimoto K, Kawabata K, Kunii S, Hamano K, Saito T, Tonomura B (2009) Characterization of type I collagen fibril formation using thioflavin T fluorescent dye. J Biochem 145:677-684.
26. West MW, Wang W, Patterson J, Mancias JD, Beasley JR, Hecht MH (1999) De novo amyloid proteins from designed combinatorial libraries. Proc Natl Acad Sci USA 96:11211-11216. (Pubitemid 29487360)
27. Welgus HG, Campbell EJ, Cury JD, Eisen AZ, Senior RM, Wilhelm SM, Goldberg GI (1990) Neutral metalloproteinases produced by human mononuclear phagocytes. Enzyme profile, regulation, and expression during cellular development. J Clin Invest 86: 1496-1502.
28. Fessler LI, Condic ML, Nelson RE, Fessler JH, Fristrom JW (1993) Site-specific cleavage of basement membrane collagen IV during Drosophila metamorphosis. Development 117:1061-1069.
29. Bella J, Eaton M, Brodsky B, Berman HM (1994) Crystal and molecular structure of a collagen-like peptide at 1.9 A resolution. Science 266:75-81. (Pubitemid 24985566)
30. Marini JC, Forlino A, Cabral WA, Barnes AM, San Antonio JD, Milgrom S, Hyland JC, Korkko J, Prockop DJ, De Paepe A, Coucke P, Symoens S, Glorieux FH, Roughley PJ, Lund AM, Kuurila-Svahn K, Hartikka H, Cohn DH, Krakow D, Mottes M, Schwarze U, Chen D, Yang K, Kuslich C, Troendle J, Dalgleish R, Byers PH (2007) Consortium for osteogenesis imperfecta mutations in the helical domain of type I collagen: regions rich in lethal mutations align with collagen binding sites for integrins and proteoglycans. Hum Mutat 28: 209-221. (Pubitemid 46309971)
31. Persikov AV, Pillitteri RJ, Amin P, Schwarze U, Byers PH, Brodsky B (2004) Stability related bias in residue replacing glycines within the collagen triple helix (Gly-Xaa-Yaa) in inherited connective tissue disorders. Hum Mutat 24:330-337. (Pubitemid 39336639)
32. Gaill F, Hamraoui L, Sicot FX, Timpl R (1994) Immunological properties and tissue localization of two different collagen types in annelid and vestimentifera species. Eur J Cell Biol 65:392-401.
33. Mann K, Gaill F, Timpl R (1992) Amino-acid sequence and cell-adhesion activity of a fibril-forming collagen from the tube worm Riftia pachyptila living at deep sea hydrothermal vents. Eur J Biochem 210:839-847. (Pubitemid 23015784)
34. Sicot FX, Mesnage M, Masselot M, Exposito JY, Garrone R, Deutsch J, Gaill F (2000) Molecular adaptation to an extreme environment: origin of the thermal stability of the pompeii worm collagen. J Mol Biol 302: 811-820.
35. Yoneda C, Hirayama Y, Nakaya M, Matsubara Y, Irie S, Hatae K, Watabe S (1999) The occurrence of two types of collagen proalpha-chain in the abalone Haliotis discus muscle. Eur J Biochem 261:714-721. (Pubitemid 29226069)
36. Bachinger HP, Doege KJ, Petschek JP, Fessler LI, Fessler JH (1982) Structural implications from an electronmicroscopic comparison of procollagen V with procollagen I, pC-collagen I, procollagen IV, and a Drosophila procollagen. J Biol Chem 257: 14590-14592.
37. Hofmann H, Voss T, Kuhn K, Engel J (1984) Localization of flexible sites in thread-like molecules from electron micrographs. Comparison of interstitial, basement membrane and intima collagens. J Mol Biol 172: 325-343.
38. Bachinger HP, Morris NP, Lunstrum GP, Keene DR, Rosenbaum LM, Compton LA, Burgeson RE (1990) The relationship of the biophysical and biochemical characteristics of type VII collagen to the function of anchoring fibrils. J Biol Chem 265: 10095-10101. (Pubitemid 20194369)
39. Kilchherr E, Hofmann H, Steigemann W, Engel J (1985) Structural model of the collagen-like region of C1q comprising the kink region and the fibre-like packing of the six triple helices. J Mol Biol 186:403-415. (Pubitemid 16175737)
40. Kar K, Wang YH, Brodsky B (2008) Sequence dependence of kinetics and morphology of collagen model peptide self-assembly into higher order structures. Protein Sci 17:1086-1095. (Pubitemid 351749214)
41. Cejas MA, Kinney WA, Chen C, Vinter JG, Almond HR, Jr, Balss KM, Maryanoff CA, Schmidt U, Breslav M, Mahan A, Lacy E, Maryanoff BE (2008) Thrombogenic collagen-mimetic peptides: self-assembly of triple helix-based fibrils driven by hydrophobic interactions. Proc Natl Acad Sci USA 105:8513-8518. (Pubitemid 351987711)
42. Yurchenco PD, Ruben GC (1987) Basement membrane structure in situ: evidence for lateral associations in the type IV collagen network. J Cell Biol 105:2559-2568.
43. Yurchenco PD, Ruben GC (1988) Type IV collagen lateral associations in the EHS tumor matrix. Comparison with amniotic and in vitro networks. Am J Pathol 132: 278-291.
44. Cheng JS, Dubal DB, Kim DH, Legleiter J, Cheng IH, Yu GQ, Tesseur I, Wyss-Coray T, Bonaldo P, Mucke L (2009) Collagen VI protects neurons against Abeta toxicity. Nat Neurosci 12:119-121.
45. Hashimoto T, Wakabayashi T, Watanabe A, Kowa H, Hosoda R, Nakamura A, Kanazawa I, Arai T, Takio K, Mann DM, Iwatsubo T (2002) CLAC: a novel Alzheimer amyloid plaque component derived from a transmembrane precursor, CLAC-P/collagen type XXV. EMBO J 21:1524-1534.
46. Osada Y, Hashimoto T, Nishimura A, Matsuo Y, Wakabayashi T, Iwatsubo T (2005) CLAC binds to amyloid beta peptides through the positively charged amino acid cluster within the collagenous domain 1 and inhibits formation of amyloid fibrils. J Biol Chem 280: 8596-8605. (Pubitemid 40349764)
47. Relini A, Canale C, De Stefano S, Rolandi R, Giorgetti S, Stoppini M, Rossi A, Fogolari F, Corazza A, Esposito G, Gliozzi A, Bellotti V (2006) Collagen plays an active role in the aggregation of beta2-microglobulin under physiopathological conditions of dialysis-related amyloidosis. J Biol Chem 281:16521-16529. (Pubitemid 43909603)
48. Soderberg L, Kakuyama H, Moller A, Ito A, Winblad B, Tjernberg LO, Naslund J (2005) Characterization of the Alzheimer's disease-associated CLAC protein and identification of an amyloid beta-peptide-binding site. J Biol Chem 280:1007-1015.
49. Kakuyama H, Soderberg L, Horigome K, Winblad B, Dahlqvist C, Naslund J, Tjernberg LO (2005) CLAC binds to aggregated Abeta and Abeta fragments, and attenuates fibril elongation. Biochemistry 44:15602-15609. (Pubitemid 41706145)
50. Schwarz U, Schuppan D, Oberbaumer I, Glanville RW, Deutzmann R, Timpl R, Kuhn K (1986) Structure of mouse type IV collagen. Amino-acid sequence of the Cterminal 511-residue-long triple-helical segment of the alpha 2(IV) chain and its comparison with the alpha 1(IV) chain. Eur J Biochem 157:49-56. (Pubitemid 16068229)
51. Consortium TU (2008) The Universal Protein Resource (UniProt). Nucleic Acids Res 36:D190-D195.
52. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J, Serrano L (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotechnol 22:1302-1306. (Pubitemid 39336784)
53. Linding R, Schymkowitz J, Rousseau F, Diella F, Serrano L (2004) A comparative study of the relationship between protein structure and beta-aggregation in globular and intrinsically disordered proteins. J Mol Biol 342:345-353. (Pubitemid 39094525)
54. Rousseau F, Schymkowitz J, Serrano L (2006) Protein aggregation and amyloidosis: confusion of the kinds? Curr Opin Struct Biol 16:118-126.