Structures and folding pathways of topologically knotted proteins

Journal of Physics Condensed Matter

Volumn 23, Issue 3, 2011, Pages

  Virnau, Peter ^a   Mallam, Anna ^b,c   Jackson, Sophie ^b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTATIONAL STUDIES; FOLDING PATHWAY; INTRICATE STRUCTURES;

PROTEIN FOLDING;

TOPOLOGY;

PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; COMPUTER GRAPHICS; COMPUTER SIMULATION; HUMAN; PROTEIN CONFORMATION; PROTEIN DATABASE; PROTEIN FOLDING; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; COMPUTER GRAPHICS; COMPUTER SIMULATION; DATABASES, PROTEIN; HUMANS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS;

EID: 78651511523     PISSN: 09538984     EISSN: 1361648X     Source Type: Journal    
DOI: 10.1088/0953-8984/23/3/033101     Document Type: Review

References (120)

1. Mansfield M L 1994 Are there knots in proteins? Nat. Struct. Biol. 1 213-4
2. Mansfield M L 1997 Fit to be tied Nat. Struct. Biol. 4 166-7
3. Taylor W R 2000 A deeply knotted protein structure and how it might fold Nature 406 916-9
4. Virnau P, Mirny L A and Kardar M 2006 Intricate knots in proteins: function and evolution PLoS Comput. Biol. 2 1074-9
5. Lua R C and Grosberg A Y 2006 Statistics of knots, geometry of conformations, and evolution of proteins PLoS Comput. Biol. 2 e45
6. Yeates T O, Norcross T S and King N P 2007 Knotted and topologically complex proteins as models for studying folding and stability Curr. Opin. Chem. Biol. 11 595-603
7. Potestio R, Micheletti C and Orland H 2010 Knotted versus unknotted proteins: evidence of knot-promoting loops PLOS Comput. Biol. 6 e1000864
8. Taylor W R and Lin K 2003 Protein knots: a tangled problem Nature 421 25
9. Takusagawa F and Kamitori S 1996 A real knot in protein J. Am. Chem. Soc. 118 8945-6
10. Bryant T N, Watson H C and Wendell P L 1974 Structure of yeast phosphoglycerate kinase Nature 247 14-7
11. Khatib F, Weirauch M T and Rohl C A 2006 Rapid knot detection and application to protein structure prediction Bioinformatics 22 e252-9
12. Berman H M et al 2000 The protein data bank Nucleic Acids Res. 28 235-42
13. Bölinger D et al 2010 A Stevedore's protein knot PLOS Comput. Biol. 6 e1000731
14. King N P, Yeates E O and Yeates T O 2007 Identification of rare slipknots in proteins and their implications for stability and folding J. Mol. Biol. 373 153-66
15. Taylor W R 2007 Protein knots and fold complexity: some new twists Comput. Biol. Chem. 31 151-62
16. Cemazar M, Gruber C W and Craik D J 2008 Oxidative folding of cyclic cystine knot proteins Antioxid. Redox. Signal. 10 103-11
17. Craik D J 2009 Circling the enemy: cyclic proteins in plant defence Trends Plant Sci. 14 328-35
18. Kolmar H 2008 Alternative binding proteins: biological activity and therapeutic potential of cystine-knot miniproteins FEBS J. 275 2684-90
19. Mcdonald N Q and Hendrickson W A 1993 A structural superfamily of growth-factors containing a cystine knot motif Cell 73 421-4
20. Liang C Z and Mislow K 1994 Knots in proteins J. Am. Chem. Soc. 116 11189-90
21. Craik D J, Daly N L and Waine C 2001 The cystine knot motif in toxins and implications for drug design Toxicon 39 43-60
22. Craik D J, Cemazar M and Daly N L 2007 The chemistry and biology of cyclotides Curr. Opin. Drug Discov. Devel. 10 176-84
23. Mallam A L and Jackson S E 2005 Folding studies on a knotted protein J. Mol. Biol. 346 1409-21
24. Mallam A L and Jackson S E 2006 Probing nature's knots: the folding pathway of a knotted homodimeric protein J. Mol. Biol. 359 1420-36
25. Mallam A L and Jackson S E 2007 A comparison of the folding of two knotted proteins: YbeA and YibK J. Mol. Biol. 366 650-65
26. Mallam A L and Jackson S E 2007 The dimerization of an alpha/beta-knotted protein is essential for structure and function Structure 15 111-22
27. Mallam A L, Morris E R and Jackson S E 2008 Exploring knotting mechanisms in protein folding Proc. Natl Acad. Sci. USA 105 18740-5
28. Mallam A L et al 2008 Knotted fusion proteins reveal unexpected possibilities in protein folding Mol. Cell. 30 642-8
29. Mallam A L and Jackson S E 2008 Use of protein engineering techniques to elucidate protein folding pathways Prog. Mol. Biol. Transl. Sci. 84 57-113
30. Andersson F I et al 2009 Untangling the folding mechanism of the 52-knotted protein UCH-L3 FEBS J. 276 2625-35
31. Adams C C 2004 The Knot Book: An Elementary Introduction to the Mathematical Theory of Knots vol xiii (Providence, RI: American Mathematical Society) p 306
32. Kolesov G et al 2007 Protein knot server: detection of knots in protein structures Nucleic Acids Res. 35 W425-8 2Web Server issue
33. Hoste J, Thistlethwaite M and Weeks J 1998 The first 1, 701, 936 knots Math. Intell. 20 33-48
34. Virnau P 2010 Detection and visualization of physical knots in macromolecules Phys. Proced. 6 117-25
35. Koniaris K and Muthukumar M 1991 Self-entanglement in ring polymers J. Chem. Phys. 95 2873-81
36. Millett K, Dobay A and Stasiak A 2005 Linear random knots and their scaling behavior Macromolecules 38 601-6
37. Biou V et al 1997 The crystal structure of plant acetohydroxy acid isomeroreductase complexed with NADPH, two magnesium ions and a herbicidal transition state analog determined at 1.65 angstrom resolution EMBO J. 16 3405-15
38. Johnston S C et al 1997 Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 A resolution EMBO J. 16 3787-96
39. Shi D S et al 2002 Crystal structure of a transcarbamylase-like protein from the anaerobic bacterium Bacteroides fragilis at 2.0 angstrom resolution J. Mol. Biol. 320 899-908
40. Schmidberger J W et al 2008 The crystal structure of Dehl reveals a new alpha-haloacid dehalogenase fold and active-site mechanism J. Mol. Biol. 378 284-94
41. Wagner J R et al 2005 A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome Nature 438 325-31
42. Murzin A G et al 1995 Scop-a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 536-40
43. Krissinel E and Henrick K 2004 Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D 60 2256-68
44. Lai Y L et al 2007 pKNOT: the protein KNOT web server Nucleic Acids Res. 35 W420-4 (Web Server issue)
45. Yeates T private communication
46. Richardson J S 1977 Beta-sheet topology and relatedness of proteins Nature 268 495-500
47. Takusagawa F et al 1996 Crystal structure of S-adenosylmethionine synthetase J. Biol. Chem. 271 136-47
48. Takusagawa F, Kamitori S and Markham G D 1996 Structure and function of S-adenosylmethionine synthetase: crystal structures of S-adenosylmethionine synthetase with ADP, BrADP, and PPi at 28 angstroms resolution Biochemistry 35 2586-96
49. Nureki O et al 2002 An enzyme with a deep trefoil knot for the active-site architecture Acta Crystallogr. D 58 1129-37
50. Michel G et al 2002 The structure of the RlmB 23S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot Structure 10 1303-15
51. Shi D S et al 2005 Crystal structure of N-acetylornithine transcarbamylase from xanthomonas campestris-a novel enzyme in a new arginine biosynthetic pathway found in several eubacteria J. Biol. Chem. 280 14366-9
52. Shi D S et al 2007 A single mutation in the active site swaps the substrate specificity of N-acetyl-L-ornithine transcarbamylase and N-succinyl-L-ornithine transcarbamylase Protein Sci. 16 1689-99
53. Villeret V et al 1998 The crystal structure of pyrococcus furiosus ornithine carbamoyltransferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures Proc. Natl Acad. Sci. USA 95 2801-6
54. van Roon A M et al 2008 Solution structure of the U2 snRNP protein Rds3p reveals a knotted zinc-finger motif Proc. Natl Acad. Sci. USA 105 9621-6
55. Andreeva A and Murzin A G 2010 Structural classification of proteins and structural genomics: new insights into protein folding and evolution Acta Crystallogr. F 66 1190-7
56. Kumarevel T S et al 2010 Crystal Structure of a Hypothetical Protein (MJ0366) in preparation
57. Lu J et al 2009 Agrobacterium tumefaciens VirC2 enhances T-DNA transfer and virulence through its C-terminal ribbon-helix-helix DNA-binding fold Proc. Natl Acad. Sci. USA 106 9643-8
58. Leung E W W and Guddat L W 2009 Conformational changes in a plant ketol-acid reductoisomerase upon Mg2+and NADPH binding as revealed by two crystal structures J. Mol. Biol. 389 167-82
59. Wagner J R et al 2007 High resolution structure of deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution J. Biol. Chem. 282 12298-309
60. Johnston S C et al 1999 Structural basis for the specificity of ubiquitin C-terminal hydrolases EMBO J. 18 3877-87
61. Misaghi S et al 2005 Structure of the ubiquitin hydrolase UCH-L3 complexed with a suicide substrate J. Biol. Chem. 280 1512-20
62. Das C et al 2006 Structural basis for conformational plasticity of the Parkinson's disease-associated ubiquitin hydrolase UCH-L1 Proc. Natl Acad. Sci. USA 103 4675-80
63. Nishio K et al 2009 Crystal structure of the deubiquitinating enzyme UCH37 (human UCH-L5) catalytic domain Biochem. Biophys. Res. Commun. 390 855-60
64. Ashley C W 1944 The Ashley Book of Knots (Garden City, NY: Doubleday) p 620
65. King N P, Jacobitz A W, Sawaya M R, Goldschmidt L and Yeates T O 2010 Structure and folding of a designed knotted protein Proc. Natl Acad. Sci. USA at press
66. Onuchic J N and Wolynes P G 2004 Theory of protein folding Curr. Opin. Struct. Biol. 14 70-5
67. Daggett V and Fersht A 2003 The present view of the mechanism of protein folding Nat. Rev. Mol. Cell Biol. 4 497-502
68. Wallin S, Zeldovich K B and Shakhnovich E I 2007 The folding mechanics of a knotted protein J. Mol. Biol. 368 884-93
69. Sulkowska J I, Sulkowski P and Onuchic J 2009 Dodging the crisis of folding proteins with knots Proc. Natl Acad. Sci. USA 106 3119-24
70. Mallam A L 2009 How does a knotted protein fold? FEBS J. 276 365-75
71. Bateman A et al 2004 The Pfam protein families database Nucleic Acids Res. 32 D138-41 Database issue
72. Chiang P K et al 1996 S-Adenosylmethionine and methylation FASEB J. 10 471-80
73. Ahn H J et al 2003 Crystal structure of tRNA (m1G37) methyltransferase: insights into tRNA recognition EMBO J. 22 2593-603
74. Elkins P A et al 2003 Insights into catalysis by a knotted TrmD tRNA methyltransferase J. Mol. Biol. 333 931-49
75. Forouhar F et al 2003 Functional assignment based on structural analysis: crystal structure of the yggJ protein (HI0303) of Haemophilus influenzae reveals an RNA methyltransferase with a deep trefoil knot Proteins: Struct. Funct. Genet. 53 329-32
76. Lim K et al 2003 Structure of the YibK methyltransferase from Haemophilus influenzae (HI0766): a cofactor bound at a site formed by a knot Proteins: Struct. Funct. Genet. 51 56-67
77. Nureki O et al 2004 Deep knot structure for construction of active site and cofactor binding site of tRNA modification enzyme Structure 12 593-602
78. Zarembinski T I et al 2003 Deep trefoil knot implicated in RNA binding found in an archaebacterial protein Proteins: Struct. Funct. Genet. 50 177-83
79. Tkaczuk K L et al 2007 Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases BMC Bioinform. 8 73
80. Jaenicke R and Lilie H 2000 Folding and association of oligomeric and multimeric proteins Adv. Protein Chem. 53 329-401
81. Mallam A L, Rogers J M and Jackson S E 2010 Experimental detection of knotted conformations in denatured proteins Proc. Natl Acad. Sci. USA 107 8189-94
82. Borgia A, Williams P M and Clarke J 2008 Single-molecule studies of protein folding Annu. Rev. Biochem. 77 101-25
83. Dzubiella J 2009 Sequence-specific size, structure, and stability of tight protein knots Biophys. J. 96 831-9
84. Huang L and Makarov D E 2008 Translocation of a knotted polypeptide through a pore J. Chem. Phys. 129 121107
85. Saito R et al 2004 Structure of bovine carbonic anhydrase II at 1.95 A resolution Acta Crystallogr. D 60 792-5
86. Alam M T et al 2002 The importance of being knotted: effects of the C-terminal knot structure on enzymatic and mechanical properties of bovine carbonic anhydrase II FEBS Lett. 519 35-40
87. Wang T, Arakawa H and Ikai A 2001 Force measurement and inhibitor binding assay of monomer and engineered dimer of bovine carbonic anhydrase B Biochem. Biophys. Res. Commun. 285 9-14
88. Sulkowska J I et al 2008 Tightening of knots in proteins Phys. Rev. Lett. 100 058106
89. Bornschlogl T et al 2009 Tightening the knot in phytochrome by single-molecule atomic force microscopy Biophys. J. 96 1508-14
90. Andersson F I, Werrell E F, McMorran L, Crone W J K, Das C, Hsu S-T D and Jackson S E 2010 The effect of Parkinson's disease associated mutations on the deubiquitinating enzyme UCH-L1 J. Mol. Biol. submitted
91. Schmid F X 1993 Prolyl isomerase-enzymatic catalysis of slow protein-folding reactions Annu. Rev. Biophys. Biomol. Struct. 22 123-43
92. Cao Z et al 2005 Bovine mitochondrial peroxiredoxin III forms a two-ring catenane Structure 13 1661-4
93. Boutz D R et al 2007 Discovery of a thermophilic protein complex stabilized by topologically interlinked chains J. Mol. Biol. 368 1332-44
94. Duff A P et al 2003 the crystal structure of pichia pastoris lysyl oxidase Biochemistry 42 15148-57
95. Helgstrand C et al 2003 The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 Å resolution J. Mol. Biol. 334 885-99
96. Bayro M J et al 2003 Structure of antibacterial peptide microcin J25: a 21-residue lariat protoknot J. Am. Chem. Soc. 125 12382-3
97. Blankenship J W and Dawson P E 2003 Thermodynamics of a designed protein catenane J. Mol. Biol. 327 537-48
98. Yan L Z and Dawson P E 2001 Design and synthesis of a protein catenane Angew. Chem. Int. Edn 40 3625-7
99. Blankenship J W and Dawson P E 2007 Threading a peptide through a peptide: protein loops, rotaxanes, and knots Protein Sci. 16 1249-56
100. Faisca P F N et al 2010 The folding of knotted proteins: insights from lattice simulations Phys. Biol. 7 016009
101. Weisstein E W, Unknotting number From Mathworld-A Wolfram Web Resource
102. Flammini A, Maritan A and Stasiak A 2004 Simulations of action of DNA topoisomerases to investigate boundaries and shapes of spaces of knots Biophys. J. 87 2968-75
103. Flammini A and Stasiak A 2007 Natural classification of knots Proc. R. Soc. A 463 569-82
104. Ohta S et al 2004 Origin of mechanical strength of bovine carbonic anhydrase studied by molecular dynamics simulation Biophys. J. 87 4007-20
105. Sulkowska J I, Sulkowski P and Onuchic J N 2009 Jamming proteins with slipknots and their free energy landscape Phys. Rev. Lett. 103 268103
106. Sulkowska J I et al 2008 Stabilizing effect of knots on proteins Proc. Natl Acad. Sci. USA 105 19714-9
107. Taketomi H, Ueda Y and Go N 1975 Studies on protein folding, unfolding and fluctuations by computer-simulation. 1. Effect of specific amino-acid sequence represented by specific inter-unit interactions Int. J. Peptide Protein Res. 7 445-59
108. Clementi C, Jennings P A and Onuchic J N 2000 How native-state topology affects the folding of dihydrofolate reductase and interleukin-1 beta Proc. Natl Acad. Sci. USA 97 5871-6
109. Clementi C, Nymeyer H and Onuchic J N 2000 Topological and energetic factors: what determines the structural details of the transition state ensemble and 'en-route' intermediates for protein folding? An investigation for small globular proteins J. Mol. Biol. 298 937-53
110. Kaya H and Chan H S 2003 Solvation effects and driving forces for protein thermodynamic and kinetic cooperativity: how adequate is native-centric topological modeling? J. Mol. Biol. 326 911-31
111. Knott M and Chan H S 2006 Criteria for downhill protein folding: calorimetry, chevron plot, kinetic relaxation, and single-molecule radius of gyration in chain models with subdued degrees of cooperativity Proteins-Struct. Funct. Bioinform. 65 373-91
112. Levy Y, Wolynes P G and Onuchic J N 2004 Protein topology determines binding mechanism Proc. Natl Acad. Sci. USA 101 511-6
113. Wallin S and Chan H S 2006 Conformational entropic barriers in topology-dependent protein folding: perspectives from a simple native-centric polymer model J. Phys.: Condens. Matter 18 S307-28
114. Noel J K, Sulkowska J I and Onuchic J N 2010 Slipknotting upon native-like loop formation in a trefoil knot protein Proc. Natl Acad. Sci. USA 107 15403-8
115. Whitford P C et al 2009 An all-atom structure-based potential for proteins: bridging minimal models with all-atom empirical forcefields Proteins-Struct. Funct. Bioinform. 75 430-41
116. Grosberg A and Nechaev S 1993 Polymer topology Adv. Polym. Sci. 106 1-29
117. Mansfield M L 1994 Knots in hamilton cycles Macromolecules 27 5924-6
118. Lua R, Borovinskiy A L and Grosberg A Y 2004 Fractal and statistical properties of large compact polymers: a computational study Polymer 45 717-31
119. Virnau P, Kantor Y and Kardar M 2005 Knots in globule and coil phases of a model polyethylene J. Am. Chem. Soc. 127 15102-6
120. Grosberg A Y, Nechaev S K and Shakhnovich E I 1988 The role of topological constraints in the kinetics of collapse of macromolecules J. Physique 49 2095-100