Single-molecule studies on polySUMO proteins reveal their mechanical flexibility

Biophysical Journal

Volumn 104, Issue 10, 2013, Pages 2273-2281

  Kotamarthi, Hema Chandra ^a   Sharma, Riddhi ^a   Koti Ainavarapu, Sri Rama ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

SUMO 1 PROTEIN; SUMO PROTEIN; SUMO1 PROTEIN, HUMAN; SUMO2 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; ENZYME STABILITY; HUMAN; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN UNFOLDING;

AMINO ACID SEQUENCE; ENZYME STABILITY; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN UNFOLDING; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMO-1 PROTEIN;

EID: 84878119770     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.04.008     Document Type: Article

References (56)

1. M. Rief, and M. Gautel H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 1997 1109 1112
2. M. Carrion-Vazquez, and A.F. Oberhauser J.M. Fernandez Mechanical and chemical unfolding of a single protein: a comparison Proc. Natl. Acad. Sci. USA 96 1999 3694 3699
3. M. Carrion-Vazquez, and A.F. Oberhauser J.M. Fernandez Mechanical design of proteins studied by single-molecule force spectroscopy and protein engineering Prog. Biophys. Mol. Biol. 74 2000 63 91
4. N. Crampton, and D.J. Brockwell Unravelling the design principles for single protein mechanical strength Curr. Opin. Struct. Biol. 20 2010 508 517
5. H. Li, and Y. Cao Protein mechanics: from single molecules to functional biomaterials Acc. Chem. Res. 43 2010 1331 1341
6. E.M. Puchner, and H.E. Gaub Force and function: probing proteins with AFM-based force spectroscopy Curr. Opin. Struct. Biol. 19 2009 605 614
7. A. Galera-Prat, and A. Gómez-Sicilia M. Carrión- Vázquez Understanding biology by stretching proteins: recent progress Curr. Opin. Struct. Biol. 20 2010 63 69
8. S.R. Ainavarapu, and A.P. Wiita J.M. Fernandez A single-molecule assay to directly identify solvent-accessible disulfide bonds and probe their effect on protein folding J. Am. Chem. Soc. 130 2008 436 437
9. T. Bornschlögl, and M. Rief Single-molecule protein unfolding and refolding using atomic force microscopy Methods Mol. Biol. 783 2011 233 250
10. V. Aggarwal, and S.R. Kulothungan S.R. Ainavarapu Ligand-modulated parallel mechanical unfolding pathways of maltose-binding proteins J. Biol. Chem. 286 2011 28056 28065
11. K. Eom, and P.C. Li G.J. Rodin Relationship between the mechanical properties and topology of cross-linked polymer molecules: parallel strands maximize the strength of model polymers and protein domains J. Phys. Chem. B 107 2003 8730 8733
12. T. Hoffmann, and L. Dougan Single molecule force spectroscopy using polyproteins Chem. Soc. Rev. 41 2012 4781 4796
13. D.J. Brockwell, and G.S. Beddard S.E. Radford Mechanically unfolding the small, topologically simple protein L Biophys. J. 89 2005 506 519
14. S.P. Ng, and R.W. Rounsevell J. Clarke Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation J. Mol. Biol. 350 2005 776 789
15. R.T. Hay SUMO: a history of modification Mol. Cell 18 2005 1 12
16. R. Geiss-Friedlander, and F. Melchior Concepts in sumoylation: a decade on Nat. Rev. Mol. Cell Biol. 8 2007 947 956
17. A.C. Vertegaal Uncovering ubiquitin and ubiquitin-like signaling networks Chem. Rev. 111 2011 7923 7940
18. M. Carrion-Vazquez, and H. Li J.M. Fernandez The mechanical stability of ubiquitin is linkage dependent Nat. Struct. Biol. 10 2003 738 743
19. S. Müller, and C. Hoege S. Jentsch SUMO, ubiquitin's mysterious cousin Nat. Rev. Mol. Cell Biol. 2 2001 202 210
20. F. Melchior SUMO - nonclassical ubiquitin Annu. Rev. Cell Dev. Biol. 16 2000 591 626
21. J. Song, and Z. Zhang Y. Chen Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation J. Biol. Chem. 280 2005 40122 40129
22. W.C. Huang, and T.P. Ko A.H. Wang Crystal structures of the human SUMO-2 protein at 1.6 A and 1.2 A resolution: implication on the functional differences of SUMO proteins Eur. J. Biochem. 271 2004 4114 4122
23. H. Ding, and Y. Xu Y. Shi Solution structure of human SUMO-3 C47S and its binding surface for Ubc9 Biochemistry 44 2005 2790 2799
24. P. Bayer, and A. Arndt J. Becker Structure determination of the small ubiquitin-related modifier SUMO-1 J. Mol. Biol. 280 1998 275 286
25. M.J. Sippl, and M. Wiederstein Detection of spatial correlations in protein structures and molecular complexes Structure 20 2012 718 728
26. M.J. Sippl, and M. Wiederstein A note on difficult structure alignment problems Bioinformatics 24 2008 426 427
27. A.C. Vertegaal SUMO chains: polymeric signals Biochem. Soc. Trans. 38 2010 46 49
28. A.C. Vertegaal Small ubiquitin-related modifiers in chains Biochem. Soc. Trans. 35 2007 1422 1423
29. I. Matic, and M. van Hagen A.C. Vertegaal In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy Mol. Cell. Proteomics 7 2008 132 144
30. E.L. Florin, and M. Rief H.E. Gaub Sensing specific molecular- interactions with the atomic-force microscope Biosens. Bioelectron. 10 1995 895 901
31. C. Bustamante, and J.F. Marko S. Smith Entropic elasticity of lambda-phage DNA Science 265 1994 1599 1600
32. A.F. Oberhauser, and P.E. Marszalek J.M. Fernandez The molecular elasticity of the extracellular matrix protein tenascin Nature 393 1998 181 185
33. M. Rief, J.M. Fernandez, and H.E. Gaub Elastically coupled two-level systems as a model for biopolymer extensibility Phys. Rev. Lett. 81 1998 4764 4767
34. G.I. Bell Models for the specific adhesion of cells to cells Science 200 1978 618 627
35. E. Evans, and K. Ritchie Dynamic strength of molecular adhesion bonds Biophys. J. 72 1997 1541 1555
36. C. Bustamante, and Y.R. Chemla D. Izhaky Mechanical processes in biochemistry Annu. Rev. Biochem. 73 2004 705 748
37. M.S. Li, and M. Kouza Dependence of protein mechanical unfolding pathways on pulling speeds J. Chem. Phys. 130 2009 145102-1 145102-7
38. H. Dietz, and F. Berkemeier M. Rief Anisotropic deformation response of single protein molecules Proc. Natl. Acad. Sci. USA 103 2006 12724 12728
39. O. Bieri, and J. Wirz T. Kiefhaber The speed limit for protein folding measured by triplet-triplet energy transfer Proc. Natl. Acad. Sci. USA 96 1999 9597 9601
40. C.L. Chyan, and F.C. Lin G. Yang Reversible mechanical unfolding of single ubiquitin molecules Biophys. J. 87 2004 3995 4006
41. P.E. Marszalek, and H. Lu J.M. Fernandez Mechanical unfolding intermediates in titin modules Nature 402 1999 100 103
42. Y. Cao, and C. Lam H. Li Nonmechanical protein can have significant mechanical stability Angew. Chem. Int. Ed. Engl. 45 2006 642 645
43. S.R. Ainavarapu, and L. Li J.M. Fernandez Ligand binding modulates the mechanical stability of dihydrofolate reductase Biophys. J. 89 2005 3337 3344
44. R.B. Best, and B. Li J. Clarke Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation Biophys. J. 81 2001 2344 2356
45. D. Sharma, and G. Feng H. Li Stabilization provided by neighboring strands is critical for the mechanical stability of proteins Biophys. J. 95 2008 3935 3942
46. H. Li, and J.M. Fernandez Mechanical design of the first proximal Ig domain of human cardiac titin revealed by single molecule force spectroscopy J. Mol. Biol. 334 2003 75 86
47. M. Gao, M. Wilmanns, and K. Schulten Steered molecular dynamics studies of titin I1 domain unfolding Biophys. J. 83 2002 3435 3445
48. O. Mayans, and J. Wuerges M. Wilmanns Structural evidence for a possible role of reversible disulphide bridge formation in the elasticity of the muscle protein titin Structure 9 2001 331 340
49. D.P. Sadler, and E. Petrik D.J. Brockwell Identification of a mechanical rheostat in the hydrophobic core of protein L J. Mol. Biol. 393 2009 237 248
50. C. Vehlow, and H. Stehr M. Lappe CMView: interactive contact map visualization and analysis Bioinformatics 27 2011 1573 1574
51. V. Sobolev, and A. Sorokine M. Edelman Automated analysis of interatomic contacts in proteins Bioinformatics 15 1999 327 332
52. M. Schlierf, H. Li, and J.M. Fernandez The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques Proc. Natl. Acad. Sci. USA 101 2004 7299 7304
53. M.C. Geoffroy, and R.T. Hay An additional role for SUMO in ubiquitin-mediated proteolysis Nat. Rev. Mol. Cell Biol. 10 2009 564 568
54. A.G. van der Veen, and H.L. Ploegh Ubiquitin-like proteins Annu. Rev. Biochem. 81 2012 323 357
55. P.G. Pedrioli, and B. Raught R. Aebersold Automated identification of SUMOylation sites using mass spectrometry and SUMmOn pattern recognition software Nat. Methods 3 2006 533 539
56. M.H. Tatham, and M.C. Geoffroy R.T. Hay RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation Nat. Cell Biol. 10 2008 538 546