Self-association of Streptococcus pyogenes collagen-like constructs into higher order structures

Protein Science

Volumn 18, Issue 6, 2009, Pages 1241-1251

  Yoshizumi, Ayumi ^a   Yu, Zhuoxin ^a   Silva, Teresita ^a   Thiagarajan, Geetha ^a   Ramshaw, John A M ^b   Inouye, Masayori ^a   Brodsky, Barbara ^a  

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

^b CSIRO   (Australia)

Author keywords

Cold shock vector; Collagen; Fibrils; Self association; Solubility; Streptococcus pyogenes

Indexed keywords

COLLAGEN; COLLAGEN FIBRIL;

ARTICLE; CIRCULAR DICHROISM; DIFFERENTIAL SCANNING CALORIMETRY; ELECTRON MICROSCOPY; ENTHALPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STABILITY; SOLUBILITY; STREPTOCOCCUS PYOGENES; TRIPLE HELIX;

CALORIMETRY, DIFFERENTIAL SCANNING; COLLAGEN; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; STREPTOCOCCUS PYOGENES; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PYOGENES;

EID: 66349116433     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.134     Document Type: Article

References (42)

1. Kielty CM, Grant ME, The Collagen family: structure, assembly and organization in the extracellular matrix. In: Royce PM, Steinmann B, Eds (2002) Connective tissue and its heritable disorders: molecular, genetic, and medical aspects, 2nd Ed., New York: Wiley-Liss, pp 159-222.
2. 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. (Pubitemid 43845965)
3. Exposito JY, Cluzel C, Garrone R, Lethias C (2002) Evolution of collagens. Anat Rec 268:302-316. (Pubitemid 35246848)
4. Rasmussen M, Jacobsson MB, Jorck L (2003) Genomebased identification and analysis of collagen-related structural motifs in bacterial and viral proteins. J Biol Chem 278:32313-32316. (Pubitemid 37048426)
5. Xu Y, Keene DR, Bujnicki JM, Höök M, Lukomski S (2002) Streptococcal Scl1 and Scl2 proteins form collagen-like triple helices. J Biol Chem 277:27312-27318. (Pubitemid 34951750)
6. Sylvestre P, Couture-Tosi E, Mock M (2002) A collagenlike surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol Microbiol 45:169-178.
7. Mohs A, Silva T, Yoshida T, Amin R, Lukomski S, Inouye M, Brodsky B (2007) Mechanism of stabilization of a bacterial collagen triple helix in the absence of hydroxyproline. J Biol Chem 282:29757-29765. (Pubitemid 350035254)
8. Boydston J, Chen P, Steichen C, Turnbough C (2005) Orientation within the exosporium and structural stability of the collagen-like glycoprotein BclA of Bacillus anthracis. J Bacteriol 187:5310-5317. (Pubitemid 41022950)
9. Karlström Å, Jacivsson K, Flock M, Folk JI, Guss B (2004) Identification of a novel collagen-like protein Scl C, in Streptococcus equi using signal sequence phage display Vet Microbiol 104:179-188.
10. Rasmussen M, Edén A, Björck L (2000) SclA, a novel collagen-like surface protein of Streptococcus pyogenes. Infect Immun 68:6370-6377.
11. Lukomski S, Nakashima K, Abdi I, Cipriano VJ, Ireland RM, Reid SD, Adams GG, Musser JM (2000) Identification and characterization of the scl gene encoding a group A Streptococcus extracellular protein virulence factor with similarity to human collagen. Infect Immun 68:6542-6553. (Pubitemid 32463352)
12. Whatmore AM (2001) Streptococcus pyogenes sclB encodes a putative hypervariable surface protein with a collagen-like repetitive structure. Microbiology 147:419-429. (Pubitemid 32156818)
13. Caswell CC, Lukomska E, Seo NS, Höök M, Lukomski S (2007) Scl1-dependent internalization of group A Streptococcus via direct interactions with the α2β(1) integrin enhances pathogen survival and re-emergence. Mol Microbiol 64:1319-1331.
14. Caswell CC, Barczyk M, Keene DR, Lukomska E, Gullberg DE, Lukomski S (2008) Identification of the first prokaryotic collagen sequence motif that mediates binding to human collagen receptors, integrins α2β1 and α11β1. J Biol Chem 283:36168-36175.
15. Humtsoe JO, Kim JK, Xu Y, Keene DR, Höök M, Lukomski S, Wary KK (2005) A streptococcal collagen-like protein interacts with the α2β1 integrin and induces intracellular signaling. J Biol Chem 280:13848-13857. (Pubitemid 40517283)
16. Han R, Zwiefka A, Caswell CC, Xu Y, Keene DR, Lukomska E, Zhao Z, Höök M, Lukomski S (2006) Assessment of prokaryotic collagen-like sequences derived from streptococcal Scl1 and Scl2 proteins as a source of recombinant GXY polymers. Appl Microbiol Biotechnol 72:109-115. (Pubitemid 44222429)
17. Hulmes DJ, Miller A, Parry DA, Piez KA, Woodhead-Galloway J (1973) Analysis of the primary structure of collagen for the origins of molecular packing. J Mol Biol 79:137-148.
18. Leikin S, Rau DC, Parsegian VA (1994) Direct measurement of forces between self-assembled proteins: temperature- dependent exponential forces between collagen triple helices. Proc Natl Acad Sci USA 91:276-280. (Pubitemid 24018687)
19. Qing G, Ma LC, Khorchid A, Swapna GV, Mal TK, Takayama MM, Xia B, Phadtare S, Ke H, Acton T, Montelione GT, Ikura M, Inouye M (2004) Cold-shock induced high-yield protein production in Escherichia coli. Nat Biotechnol 22:877-882. (Pubitemid 38886608)
20. Fletcher GC (1976) Dynamic light scattering from collagen solutions. I. Translational diffusion coefficient and aggregation effects Biopolymers 15:2201-2217.
21. Brodsky-Doyle B, Leonard KR, Reid KB (1976) Circular-dichroism and electron-microscopy studies of human subcomponent C1q before and after limited proteolysis by pepsin. Biochem J 159:279-286.
22. Feng Y, Melacini G, Taulane JP, Goodman M (1996) 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 1996;118:10351- 10358.
23. Privalov P (1982) Stability of proteins. Proteins which do not present a single cooperative system. Adv Protein Chem 35:1-104.
24. Bella J, Eaton M, Brodsky B, Berman HM (1994) Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution. Science 266:75-81. (Pubitemid 24985566)
25. Kramer RZ, Venugopal MG, Bella J, Mayville P, Brodsky B, Berman HM (2000) Staggered molecular packing in crystals of a collagen-like peptide with a single charged pair. J Mol. Biol 301:1191-1205.
26. Murray LW, Tanzer ML (1983) Characterization of a large fragment from annelid cuticle collagen and its relationship to the intact molecule. Coll Relat Res 3:445-458.
27. Kühn K (1982) Segment-long-spacing crystallites, a powerful tool in collagen research. Coll Relat Res 2:61-80.
28. Brodsky B, Eikenberry EF (1982) Characterization of fibrous forms of collagen. Methods Enzymol 82:127-174.
29. Olsen DR, Yang C, Bodo M, Chang R, Leigh S, Baez J, Carmichael D, Perälä M, Hämäläinen ER, Jarvinen M, Polarek J (2003) Recombinant collagen and gelatin for drug delivery. Adv Drug Deliv Rev 55:1547-1567. (Pubitemid 37412593)
30. Ruggiero F, Koch M (2008) Making recombinant extracellular matrix proteins. Methods 45:75-85.
31. Nokelainen M, Tu H, Vuorela A, Notbohm H, Kivirikko KI, Myllyharju J (2001) High-level production of human type I collagen in the yeast Pichia pastoris. Yeast 18:792-806. (Pubitemid 32633515)
32. Persikov A, Ramshaw J, Brodsky B (2005) Prediction of collagen stability from amino acid sequence. J Biol Chem 280:19343-19349. (Pubitemid 41379641)
33. Mallinger R, Schmut O (1988) Reaggregation behavior of different types of collagen in vitro: variations in the occurrence and structure of dimeric segment long-spacing collagen. J Ultrastruct Mol Struct Res 98:11-18. (Pubitemid 18138346)
34. 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 2006;281:33283-33290. (Pubitemid 46036711)
35. Steplewski A, Hintze V, Fertala A (2007) Molecular basis of organization of collagen fibrils. J Struct Biol 157:297-307. (Pubitemid 46127753)
36. Ito H, Steplewski A, Alabyeva T, Fertala A (2006) Testing the utility of rationally engineered recombinant collagenlike proteins for applications in tissue engineering. J Biomed Mater Res A 76:551-560.
37. Vitagliano L, Berisio R, Mazzarella L, Zagari A (2001) Structural bases of collagen stabilization induced by proline hydroxylation. Biopolymers 58:459-464. (Pubitemid 32303811)
38. 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.
39. Rele S, Song Y, Apkarian RP, Qu Z, Conticello VP, Chaikof EL (2007) D-periodic collagen-mimetic microfibers. J Am Chem Soc 129:14780-14787. (Pubitemid 350207893)
40. Perret S, Merle C, Bernocco S, Berland P, Garrone R, Hulmes DJS, Theisen M, Ruggiero F (2001) Unhydroxylated triple helical collagen I produced in transgenic plants provides new clues on the role of hydroxyproline in collagen folding and fibril formation. J Biol Chem 276:43693-43698. (Pubitemid 33651839)
41. Gill SC, von Hippel PH (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182:319-326. (Pubitemid 19277112)
42. Persikov AV, Xu Y, Brodsky B (2004) Equilibrium termal transition of collagen model peptides. Protein Sci 13:893-902. (Pubitemid 38429213)