Perturbing the folding energy landscape of the bacterial immunity protein Im7 by site-specific N-linked glycosylation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 52, 2010, Pages 22528-22533

  Chen, Mark M ^a   Bartlett, Alice I ^b   Nerenberg, Paul S ^c   Friel, Claire T ^b   Hackenberger, Christian P R ^a   Stultz, Collin M ^c   Radford, Sheena E ^b   Imperiali, Barbara ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHITOBIOSE; DISACCHARIDE; GLYCAN; IM7 PROTEIN; SOLVENT; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL IMMUNITY; CONTROLLED STUDY; MOLECULAR RECOGNITION; N LINKED GLYCOSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; THERMODYNAMICS;

AMINO ACID SEQUENCE; BINDING SITES; CARRIER PROTEINS; CIRCULAR DICHROISM; DISACCHARIDES; ESCHERICHIA COLI PROTEINS; GLYCOSYLATION; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; SPECTROMETRY, FLUORESCENCE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; THERMODYNAMICS;

BACTERIA (MICROORGANISMS);

EID: 78651099872     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1015356107     Document Type: Article

References (38)

1. Walsh CT, Garneau-Tsodikova S, Gatto GJ (2005) Protein posttranslational modifications: The chemistry of proteome diversifications. Angew Chem Int Ed Engl 44:7342-7372. (Pubitemid 41689988)
2. Abu-Qarn M, Eichler J, Sharon N (2008) Not just for eukarya anymore: Protein glycosylation in bacteria and archaea. Curr Opin Struct Biol 18:544-550.
3. Weerapana E, Imperiali B (2006) Asparagine-linked protein glycosylation: From eukaryotic to prokaryotic systems. Glycobiology 16:91R-101R.
4. Varki A (1993) Biological roles of oligosaccharides: All of the theories are correct. Glycobiology 3:97-130.
5. Mitra N, Sinha S, Ramya TNC, Surolia A (2006) N-linked oligosaccharides as outfitters for glycoprotein folding, form and function. Trends Biochem Sci 31:156-163.
6. Bosques CJ, Imperiali B (2003) The interplay of glycosylation and disulfide formation influences fibrillization in a prion protein fragment. Proc Natl Acad Sci USA 100:7593-7598.
7. Lederkremer GZ (2009) Glycoprotein folding, quality control and ER-associated degradation. Curr Opin Struct Biol 19:515-523.
8. Imberty A, Varrot A (2008) Microbial recognition of human cell surface glycoconjugates. Curr Opin Struct Biol 18:567-576.
9. Skropeta D (2009) The effect of individual N-glycans on enzyme activity. Bioorg Med Chem 17:2645-2653.
10. Hanson SR, et al. (2009) The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability. Proc Natl Acad Sci USA 106:3131-3136.
11. Shental-Bechor D, Levy Y (2008) Effect of glycosylation on protein folding: A close look at thermodynamic stabilization. Proc Natl Acad Sci USA 105:8256-8261.
12. Petrescu AJ, Milac AL, Petrescu SM, Dwek RA,Wormald MR (2004) Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology 14:103-114.
13. Shental-Bechor D, Levy Y (2009) Folding of glycoproteins: Toward understanding the biophysics of the glycosylation code. Curr Opin Struct Biol 19:524-533.
14. Sola RJ, Griebenow K (2009) Effects of glycosylation on the stability of protein pharmaceuticals. J Pharm Sci 98:1223-1245.
15. Buskas T, Ingale S, Boons GJ (2006) Glycopeptides as versatile tools for glycobiology. Glycobiology 16:113R-136R.
16. Imperiali B, Rickert KW (1995) Conformational implications of asparagine-linked glycosylation. Proc Natl Acad Sci USA 92:97-101.
17. O'Connor SE, Pohlmann J, Imperiali B, Saskiawan I, Yamamoto K (2001) Probing the effect of the outer saccharide residues of N-linked glycans on peptide conformation. J Am Chem Soc 123:6187-6188.
18. Payne RJ,Wong CH (2010) Advances in chemical ligation strategies for the synthesis of glycopeptides and glycoproteins. Chem Commun (Cambridge, UK) 46:21-43.
19. Friel CT, Smith DA, Vendruscolo M, Gsponer J, Radford SE (2009) The mechanism of folding of Im7 reveals competition between functional and kinetic evolutionary constraints. Nat Struct Mol Biol 16:318-324.
20. Friel CT, Capaldi AP, Radford SE (2003) Structural analysis of the rate-limiting transition states in the folding of Im7 and Im9: similarities and differences in the folding of homologous proteins. J Mol Biol 326:293-305.
21. Bartlett AI, Radford SE (2010) Desolvation and development of specific hydrophobic core packing during Im7 folding. J Mol Biol 396:1329-1345.
22. Hoffmann D, Florke H (1998) A structural role for glycosylation: lessons from the hp model. Folding Des 3:337-343.
23. Sugita Y, Okamoto Y (1999) Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 314:141-151.
24. Hackenberger CPR, Friel CT, Radford SE, Imperiali B (2005) Semisynthesis of a glycosylated Im7 analogue for protein folding studies. J Am Chem Soc 127:12882-12889.
25. Evans TC, Jr, Benner J, Xu MQ (1999) The in vitro ligation of bacterially expressed proteins using an intein from Methanobacterium thermoautotrophicum. J Biol Chem 274:3923-3926.
26. Spence GR, Capaldi AP, Radford SE (2004) Trapping the on-pathway folding intermediate of Im7 at equilibrium. J Mol Biol 341:215-226.
27. Capaldi AP, Kleanthous C, Radford SE (2002) Im7 folding mechanism: Misfolding on a path to the native state. Nat Struct Biol 9:209-216.
28. Petrescu A-J (2009) SAGS database. Structural Assessment of Glycosylation Sites http://sags.biochim.ro/.
29. Foit L, et al. (2009) Optimizing protein stability in vivo. Mol Cell 36:861-871.
30. O'Connor SE, Imperiali B (1998) A molecular basis for glycosylation-induced conformational switching. Chem Biol 5:427-437.
31. Imberty A, Perez S (1995) Stereochemistry of the N-glycosylation sites in glycoproteins. Protein Eng 8:699-709.
32. Dennis CA, et al. (1998) A structural comparison of the colicin immunity proteins Im7 and Im9 gives new insights into the molecular determinants of immunity-protein specificity. Biochem J 333(Pt 1):183-191.
33. Hackenberger CPR, O'Reilly MK, Imperiali B (2005) Improving glycopeptide synthesis: A convenient protocol for the preparation of beta-glycosylamines and the synthesis of glycopeptides. J Org Chem 70:3574-3578.
34. Brooks BR, et al. (2009) CHARMM: The biomolecular simulation program. J Comput Chem 30:1545-1614.
35. Chen J, Im W, Brooks CL, 3rd (2006) Balancing solvation and intramolecular interactions: Toward a consistent generalized Born force field. J Am Chem Soc 128:3728-3736.
36. MacKerell AD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586-3616.
37. Kuttel M, Brady JW, Naidoo KJ (2002) Carbohydrate solution simulations: Producing a force field with experimentally consistent primary alcohol rotational frequencies and populations. J Comput Chem 23:1236-1243.
38. Spiriti J, Bogani F, van der Vaart A, Ghirlanda G (2008) Modulation of protein stability by O-glycosylation in a designed Gc-MAF analog. Biophys Chem 134:157-167.