Propensity for C-terminal domain swapping correlates with increased regional flexibility in the C-terminus of RNase A

Protein Science

Volumn 20, Issue 10, 2011, Pages 1735-1744

  Miller, Katherine H ^a,b   Marqusee, Susan ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Conformational flexibility; Domain swapping; Hydrogen exchange; Local fluctuations; RNase A

Indexed keywords

ACETIC ACID; DIMER; RIBONUCLEASE A;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DEUTERIUM HYDROGEN EXCHANGE; FREEZE DRYING; MUTATION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; WILD TYPE;

ANIMALS; CATTLE; MODELS, MOLECULAR; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PANCREAS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASE, PANCREATIC;

BOVINAE;

EID: 80053143458     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.708     Document Type: Article

References (31)

1. Bennett MJ, Sawaya MR, Eisenberg D (2006) Deposition diseases and 3D domain swapping. Structure 14: 811-824. (Pubitemid 43674098)
2. Schlunegger MP, Bennett MJ, Eisenberg D (1997) Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly. Adv Protein Chem 50:61-122. (Pubitemid 27449486)
3. Lopez-Alonso JP, Bruix M, Font J, Ribo M, Vilanova M, Jimenez MA, Santoro J, Gonzalez C, Laurents DV (2010) NMR spectroscopy reveals that RNase A is chiefly denatured in 40% acetic acid: implications for oligomer formation by 3D domain swapping. J Am Chem Soc 132:1621-1630.
4. Lopez-Alonso JP, Gotte G, Laurents DV (2009) Kinetic analysis provides insight into the mechanism of ribonuclease A oligomer formation. Arch Biochem Biophys 489:41-47.
5. Malevanets A, Sirota FL, Wodak SJ (2008) Mechanism and energy landscape of domain swapping in the B1 domain of protein G. J Mol Biol 382:223-235.
6. Esposito L, Daggett V (2005) Insight into ribonuclease A domain swapping by molecular dynamics unfolding simulations. Biochemistry 44:3358-3368. (Pubitemid 40322006)
7. Chahine J, Cheung MS (2005) Computational studies of the reversible domain swapping of p13suc1. Biophys J 89:2693-2700. (Pubitemid 41401059)
8. Ercole C, Lopez-Alonso JP, Font J, Ribo M, Vilanova M, Picone D, Laurents DV (2011) Crowding agents and osmolytes provide insight into the formation and dissociation of RNase A oligomers. Arch Biochem Biophys 506:123-129.
9. Rousseau F, Schymkowitz JW, Wilkinson HR, Itzhaki LS (2001) Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues. Proc Natl Acad Sci USA 98:5596-5601. (Pubitemid 32435687)
10. Picone D, Di Fiore A, Ercole C, Franzese M, Sica F, Tomaselli S, Mazzarella L (2005) The role of the hinge loop in domain swapping. The special case of bovine seminal ribonuclease. J Biol Chem 280:13771-13778. (Pubitemid 40517273)
11. Russo N, Antignani A, D'Alessio G (2000) In vitro evolution of a dimeric variant of human pancreatic ribonuclease. Biochemistry 39:3585-3591. (Pubitemid 30183839)
12. Richards FM, Vithayathil PJ (1959) The preparation of subtilisn-modified ribonuclease and the separation of the peptide and protein components. J Biol Chem 234: 1459-1465.
13. Beals JM, Haas E, Krausz S, Scheraga HA (1991) Conformational studies of a peptide corresponding to a region of the C-terminus of ribonuclease A: implications as a potential chain-folding initiation site. Biochemistry 30:7680-7692.
14. Wang A, Robertson AD, Bolen DW (1995) Effects of a naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemistry 34: 15096-15104.
15. Neira JL, Sevilla P, Menendez M, Bruix M, Rico M (1999) Hydrogen exchange in ribonuclease A and ribonuclease S: evidence for residual structure in the unfolded state under native conditions. J Mol Biol 285: 627-643. (Pubitemid 29041797)
16. Burgess AW, Weinstein LI, Gabel D, Scheraga HA (1975) Immobilized carboxypeptidase A as a probe for studying the thermally induced unfolding of bovine pancreatic ribonuclease. Biochemistry 14:197-200.
17. Miller KH, Karr JR, Marqusee S (2010) A hinge region cis-proline in ribonuclease A acts as a conformational gatekeeper for C-terminal domain swapping. J Mol Biol 400:567-578.
18. Liu Y, Gotte G, Libonati M, Eisenberg D (2001) A domain- swapped RNase A dimer with implications for amyloid formation. Nat Struct Biol 8:211-214. (Pubitemid 32180044)
19. Sambashivan S, Liu Y, Sawaya MR, Gingery M, Eisenberg D (2005) Amyloid-like fibrils of ribonuclease A with three-dimensional domain-swapped and nativelike structure. Nature 437:266-269. (Pubitemid 41294490)
20. Linderstrom-Lang K (1955) Deuterium exchange between peptides and water. Chem Soc Spec Publ 2:1-20.
21. Santoro MM, Bolen DW (1988) Unfolding free energy changes determined by the linear extrapolation method. I. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27:8063-8068.
22. Qu Y, Bolen DW (2003) Hydrogen exchange kinetics of RNase A and the urea:TMAO paradigm. Biochemistry 42:5837-5849. (Pubitemid 36582876)
23. Robertson AD, Baldwin RL (1991) Hydrogen exchange in thermally denatured ribonuclease A. Biochemistry 30:9907-9914.
24. Bai Y, Milne JS, Mayne L, Englander SW (1993) Primary structure effects on peptide group hydrogen exchange. Proteins 17:75-86. (Pubitemid 23261059)
25. Zhang Y-Z (1995) Protein and peptide structure and interactions studied by hydrogen exchange and NMR. Philadelphia: University of Pennsylvania.
26. Schultz DA, Friedman AM, White MA, Fox RO (2005) The crystal structure of the cis-proline to glycine variant (P114G) of ribonuclease A. Protein Sci 14:2862-2870.
27. Hvidt A, Nielsen SO (1966) Hydrogen exchange in proteins. Adv Protein Chem 21:287-386.
28. DelCardayre SB, Ribo M, Yokel EM, Quirk DJ, Rutter WJ, Raines RT (1995) Engineering ribonuclease A: production, purification and characterization of wildtype enzyme and mutants at Gln11. Protein Eng 8: 261-273.
29. Marley J, Lu M, Bracken C (2001) A method for efficient isotopic labeling of recombinant proteins. J Biomol NMR 20:71-75. (Pubitemid 32519656)
30. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293.
31. Keller RLJ (2004) The Computer Aided Resonance Tutorial, http://cara.nmr-software.org/downloads/.