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Entangled proteins: knots, slipknots, links, and lassos. (English) Zbl 1425.82044

Gupta, Sanju (ed.) et al., The role of topology in materials. Springer Series in Solid-State Sciences 189. Cham: Springer. 201-226 (2018).
Summary: In recent years the studies of entangled proteins have grown into the whole new, interdisciplinary and rapidly developing field of research. Here we present various types of entangled proteins studied within this field, which form knots, slipknots, links, and lassos. We discuss their geometric features and indicate what biological and physical role the entanglement plays. We also discuss mathematical tools necessary to analyze such structures and present databases and servers assembling information about entangled proteins: KnotProt, LinkProt, and LassoProt.
For the entire collection see [Zbl 1421.82001].

MSC:

82D60 Statistical mechanics of polymers
92D20 Protein sequences, DNA sequences
57M25 Knots and links in the \(3\)-sphere (MSC2010)
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[1] C.D. Allen, M.Y. Chen, A.Y. Trick, D.T. Le, A.L. Ferguson, A.J. Link, Thermal unthreading of the lasso peptides astexin-2 and astexin-3. ACS Chem. Biol. (2016) · doi:10.1021/acschembio.6b00588
[2] F.I. Andersson, D.G. Pina, A.L. Mallam, G. Blaser, S.E. Jackson, Untangling the folding mechanism of the 52-knotted protein uch-l3. FEBS J. 276(9), 2625-2635 (2009) · doi:10.1111/j.1742-4658.2009.06990.x
[3] B.T. Andrews, D.T. Capraro, J.I. Sulkowska, J.N. Onuchic, P.A. Jennings, Hysteresis as a marker for complex, overlapping landscapes in proteins. J. Phys. Chem. Lett. 4(1), 180-188 (2012) · doi:10.1021/jz301893w
[4] S.A. Beccara, T. Škrbić, R. Covino, C. Micheletti, P. Faccioli, Folding pathways of a knotted protein with a realistic atomistic force field. PLoS Comput. Biol. 9(3), e1003002 (2013)
[5] D. Bölinger, J.I. Sułkowska, H.-P. Hsu, L.A. Mirny, M. Kardar, J.N. Onuchic, P. Virnau, A Stevedore’s protein knot. PLoS Comput. Biol. 6(4), e1000731-e1000731 (2010) · doi:10.1371/journal.pcbi.1000731
[6] T. Bornschlögl, D.M. Anstrom, E. Mey, J. Dzubiella, M. Rief, K.T. Forest, Tightening the knot in phytochrome by single-molecule atomic force microscopy. Biophys. J. 96(4), 1508-1514 (2009) · doi:10.1016/j.bpj.2008.11.012
[7] T. Christian, R. Sakaguchi, A.P. Perlinska, G. Lahoud, T. Ito, E.A. Taylor, S. Yokoyama, J.I. Sulkowska, Y-M. Hou, Methyl transfer by substrate signaling from a knotted protein fold. Nat. Struct. Mol. Biol. (2016)
[8] M. Chwastyk, M. Cieplak, Cotranslational folding of deeply knotted proteins. J. Phys. Condens. Matter 27(35), 354105 (2015) · doi:10.1088/0953-8984/27/35/354105
[9] D.J. Craik, N.L. Daly, T. Bond, C. Waine, Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol. 294(5), 1327-1336 (1999) · doi:10.1006/jmbi.1999.3383
[10] D.J. Craik, M. Čemažar, C.K.L. Wang, N.L. Daly, The cyclotide family of circular miniproteins: nature’s combinatorial peptide template. Pept. Sci. 84(3), 250-266 (2006) · doi:10.1002/bip.20451
[11] P. Dabrowski-Tumanski, J.I. Sulkowska, Topological knots and links in proteins. Proc. Natl. Acad. Sci. 114(13), 3415-3420 (2017) · doi:10.1073/pnas.1615862114
[12] P. Dabrowski-Tumanski, A.I. Jarmolinska, J.I. Sulkowska, Prediction of the optimal set of contacts to fold the smallest knotted protein. J. Phys. Condens. Matter 27(35), 354109 (2015) · doi:10.1088/0953-8984/27/35/354109
[13] P. Dabrowski-Tumanski, W. Niemyska, P. Pasznik, J.I. Sulkowska, Lassoprot: server to analyze biopolymers with lassos. Nucleic Acids Res. 44(W1), W383-W389, 2016 · doi:10.1093/nar/gkw308
[14] P. Dabrowski-Tumanski, A. Stasiak, J.I. Sulkowska, In search of functional advantages of knots in proteins. PloS one, 11(11), e0165986 (2016) · doi:10.1371/journal.pone.0165986
[15] P. Dabrowski-Tumanski, A.I. Jarmolinska, W. Niemyska, E.J. Rawdon, K.C. Millett, J.I. Sulkowska, Linkprot: a database collecting information about biological links. Nucleic Acids Res. 45(D1), D243 (2017) · doi:10.1093/nar/gkw976
[16] N.L. Daly, D.J. Craik. Bioactive cystine knot proteins. Curr. Opin. Chem. Biol. 15(3), 362-368 (2011) · doi:10.1016/j.cbpa.2011.02.008
[17] L.-O. Essen, J. Mailliet, J. Hughes, The structure of a complete phytochrome sensory module in the Pr ground state. Proc. Natl. Acad. Sci. 105(38), 14709-14714 (2008) · doi:10.1073/pnas.0806477105
[18] B. Ewing, K.C. Millett, Computational algorithms and the complexity of link polynomials. Prog. Knot Theory Relat. Top. 56, 51-68 (1997) · Zbl 0930.57007
[19] P.F.N. Faísca, Knotted proteins: a tangled tale of structural biology. Comput. Struct. Biotechnol. J. 13, 459-468 (2015) · doi:10.1016/j.csbj.2015.08.003
[20] P.F.N. Faísca, R.D.M. Travasso, T. Charters, A. Nunes, M. Cieplak, The folding of knotted proteins: insights from lattice simulations. Phys. Biol. 7(1), 016009 (2010) · doi:10.1088/1478-3975/7/1/016009
[21] P. Freyd, D. Yetter, J. Hoste, W.B.R. Lickorish, K. Millett, A. Ocneanu, A new polynomial invariant of knots and links. Bull. Am. Math. Soc. 12(2), 239-246 (1985) · Zbl 0572.57002 · doi:10.1090/S0273-0979-1985-15361-3
[22] E. Haglund, J.I. Sułkowska, Z. He, G-S. Feng, P.A. Jennings, J.N. Onuchic, The unique cysteine knot regulates the pleotropic hormone leptin. PloS one 7(9), e45654 (2012) · doi:10.1371/journal.pone.0045654
[23] E. Haglund, J.I. Sulkowska, J.K. Noel, H. Lammert, J.N. Onuchic, P.A. Jennings, Pierced lasso bundles are a new class of knot-like motifs. PLoS Comput. Biol. 10(6), e1003613 (2014) · doi:10.1371/journal.pcbi.1003613
[24] E. Haglund, A. Pilko, R. Wollman, P.A. Jennings, J.N. Onuchic, Pierced lasso topology controls function in leptin. J. Phys. Chem. B 121(4), 706-718 (2017) · doi:10.1021/acs.jpcb.6b11506
[25] C. He, G.Z. Genchev, H. Lu, H. Li, Mechanically untying a protein slipknot: multiple pathways revealed by force spectroscopy and steered molecular dynamics simulations. J. Am. Chem. Soc. 134(25), 10428-10435 (2012) · doi:10.1021/ja3003205
[26] C. He, G. Lamour, A. Xiao, J. Gsponer, H. Li, Mechanically tightening a protein slipknot into a trefoil knot. J. Am. Chem. Soc. 136(34), 11946-11955 (2014) · doi:10.1021/ja503997h
[27] Y.M. Hou, R. Matsubara, R. Takase, I. Masuda, J.I. Sulkowska. TrmD: a methyl transferase for tRNA methylation with m1G37. The Enzymes (2017) · doi:10.1016/bs.enz.2017.03.003
[28] S.E. Jackson, A. Suma, C. Micheletti, How to fold intricately: using theory and experiments to unravel the properties of knotted proteins. Curr. Opin. Struct. Biol. 42, 6-14 (2017)
[29] M. Jamroz, W. Niemyska, E.J. Rawdon, A. Stasiak, K.C. Millett, P. Sułkowski, J.I. Sulkowska, Knotprot: a database of proteins with knots and slipknots. Nucleic Acids Res. 43(D1), D306-D314 (2015) · doi:10.1093/nar/gku1059
[30] A.I. Jarmolinska, A.P. Perlinska, R. Runkel, B. Trefz, P. Virnau, J.I. Sulkowska, Proteins? knotty problems (2017) (under review)
[31] N.P. King, A.W. Jacobitz, M.R. Sawaya, L. Goldschmidt, T.O. Yeates, Structure and folding of a designed knotted protein. Proc. Natl. Acad. Sci. 107(48), 20732-20737 (2010) · doi:10.1073/pnas.1007602107
[32] N.P. King, E.O. Yeates, T.O. Yeates, Identification of rare slipknots in proteins and their implications for stability and folding. J. Mol. Biol. 373(1), 153-166 (2007) · doi:10.1016/j.jmb.2007.07.042
[33] G. Kolesov, P. Virnau, M. Kardar, L.A. Mirny, Protein knot server: detection of knots in protein structures. Nucleic Acids Res. 35, W425-8 (2007) · doi:10.1093/nar/gkm312
[34] K. Koniaris, M. Muthukumar, Self-entanglement in ring polymers. J. Chem. Phys. 95(4), 2873-2881 (1991) · doi:10.1063/1.460889
[35] Y.-L. Lai, S.-C. Yen, Y. Sung-Huan, J.-K. Hwang, pknot: the protein knot web server. Nucleic Acids Res. 35(2), W420-W424 (2007) · doi:10.1093/nar/gkm304
[36] Y.-T.C. Lee, C-Y. Chang, S.-Y. Chen, Y.-R. Pan, M.-R. Ho, S.T.D. Hsu, Entropic stabilization of a deubiquitinase provides conformational plasticity and slow unfolding kinetics beneficial for functioning on the proteasome. Sci. Rep. 7, 45174 (2017) · doi:10.1038/srep45174
[37] W. Li, T. Terakawa, W. Wang, S. Takada, Energy landscape and multiroute folding of topologically complex proteins adenylate kinase and 2ouf-knot. Proc. Natl. Acad. Sci. 109(44), 17789-17794 (2012) · doi:10.1073/pnas.1201807109
[38] S.-C. Lou, S. Wetzel, H. Zhang, E.W. Crone, Y.-T. Lee, S.E. Jackson, S.-T.D. Hsu, The knotted protein UCh-L1 exhibits partially unfolded forms under native conditions that share common structural features with its kinetic folding intermediates. J. Mol. Biol. 428(11), 2507-2520 (2016) · doi:10.1016/j.jmb.2016.04.002
[39] R.C. Lua, Pyknot, a pymol tool for the discovery and analysis of knots in proteins. Bioinformatics 28(15), 2069-2071 (2012) · doi:10.1093/bioinformatics/bts299
[40] A.L. Mallam, S.E. Jackson, Knot formation in newly translated proteins is spontaneous and accelerated by chaperonins. Nat. Chem. Biol. 8(2), 147-153 (2012) · doi:10.1038/nchembio.742
[41] A.L. Mallam, J.M. Rogers, S.E. Jackson, Experimental detection of knotted conformations in denatured proteins. Proc. Natl. Acad. Sci. 107(18), 8189-8194 (2010) · doi:10.1073/pnas.0912161107
[42] M.L. Mansfield, Are there knots in proteins? Nat. Struct. Mol. Biol. 1(4), 213-214 (1994) · doi:10.1038/nsb0494-213
[43] K.C. Millett, E.J. Rawdon, A. Stasiak, J.I. Sułkowska, Identifying knots in proteins. Biochem. Soc. Trans. 41(2), 533-537 (2013) · doi:10.1042/BST20120339
[44] S. Najafi, R. Potestio, Folding of small knotted proteins: insights from a mean field coarse-grained model. J. Chem. Phys. 143(24):12B606_1 (2015)
[45] W. Niemyska, P. Dabrowski-Tumanski, M. Kadlof, E. Haglund, P. Sułkowski, J.I. Sulkowska, Complex lasso: new entangled motifs in proteins. Sci. Rep. 6, 36895 (2016)
[46] W. Niemyska, A.M. Gierut, P. Sulkowski, P. Dabrowski-Tumanski, J.I. Sulkowska, Pylasso a pymol plugin to identify lassos (2017) (under review)
[47] S. Niewieczerzal, J.I. Sulkowska, Knotting and unknotting proteins in the chaperonin cage: effects of the excluded volume. PloS one 12(5), e0176744 (2017) · doi:10.1371/journal.pone.0176744
[48] J.K. Noel, J.I. Sułkowska, J.N. Onuchic, Slipknotting upon native-like loop formation in a trefoil knot protein. Proc. Natl. Acad. Sci. 107(35), 15403-15408 (2010) · doi:10.1073/pnas.1009522107
[49] J.K. Noel, J.N. Onuchic, J.I. Sulkowska, Knotting a protein in explicit solvent. J. Phys. Chem. Lett. 4(21), 3570-3573 (2013) · doi:10.1021/jz401842f
[50] J.H. Przytycki, P. Traczyk, Invariants of links of conway type. Kobe J. Math. 4, 115-139 (1988) · Zbl 0655.57002
[51] M. Rief, H. Grubmüller, Force spectroscopy of single biomolecules. Chem. Phys. Chem. 3(3), 255-261 (2002) · doi:10.1002/1439-7641(20020315)3:3<255::AID-CPHC255>3.0.CO;2-M
[52] K.J. Rosengren, R.J. Clark, N.L. Daly, U. Göransson, A. Jones, D.J. Craik, Microcin j25 has a threaded sidechain-to-backbone ring structure and not a head-to-tail cyclized backbone. J. Am. Chem. Soc. 125(41), 12464-12474 (2003) · doi:10.1021/ja0367703
[53] T.C. Sayre, T.M. Lee, N.P. King, T.O. Yeates, Protein stabilization in a highly knotted protein polymer. Protein Eng. Des. Select. 24(8), 627-630 (2011) · doi:10.1093/protein/gzr024
[54] E. Shakhnovich, Protein folding: to knot or not to knot? Nat. Mater. 10(2), 84-86 (2011) · doi:10.1038/nmat2953
[55] T. Škrbić, C. Micheletti, P. Faccioli, The role of non-native interactions in the folding of knotted proteins. PLoS Comput. Biol. 8(6), e1002504 (2012) · doi:10.1371/journal.pcbi.1002504
[56] M.A. Soler, A. Nunes, P.F.N. Faísca, Effects of knot type in the folding of topologically complex lattice proteins. J. Chem. Phys. 141(2), 07B607_1 (2014)
[57] M.A. Soler, A. Rey, P.F.N. Faísca, Steric confinement and enhanced local flexibility assist knotting in simple models of protein folding. Phys. Chem. Chem. Phys. 18(38), 26391-26403 (2016) · doi:10.1039/C6CP05086G
[58] M. Sotomayor, K. Schulten, Single-molecule experiments in vitro and in silico. Science 316(5828), 1144-1148 (2007) · doi:10.1126/science.1137591
[59] J.I. Sułkowska, M. Cieplak, Mechanical stretching of proteins—a theoretical survey of the protein data bank. J. Phys. Condens. Matter 19(28), 283201 (2007)
[60] J.I. Sułkowska, M. Cieplak, Selection of optimal variants of gō-like models of proteins through studies of stretching. Biophys. J. 95(7), 3174-3191 (2008) · doi:10.1529/biophysj.107.127233
[61] J.I. Sułkowska, P. Sułkowski, P. Szymczak, M. Cieplak, Stabilizing effect of knots on proteins. Proc. Natl. Acad. Sci. 105(50), 19714-19719 (2008) · doi:10.1073/pnas.0805468105
[62] J.I. Sułkowska, P. Sułkowski, P. Szymczak, M. Cieplak, Tightening of knots in proteins. Phys. Rev. Lett. 100(5), 058106 (2008)
[63] J.I. Sułkowska, P. Sułkowski, J.N. Onuchic, Jamming proteins with slipknots and their free energy landscape. Phys. Rev. Lett. 103(26), 268103 (2009) · Zbl 1202.92030
[64] J.I. Sułkowska, P. Sułkowski, J. Onuchic, Dodging the crisis of folding proteins with knots. Proc. Natl. Acad. Sci. 106(9), 3119-3124 (2009) · Zbl 1202.92030 · doi:10.1073/pnas.0811147106
[65] J.I. Sułkowska, P. Sułkowski, P. Szymczak, M. Cieplak, Untying knots in proteins. J. Am. Chem. Soc. 132(40), 13954-13956 (2010) · doi:10.1021/ja102441z
[66] J.I. Sułkowska, J.K. Noel, J.N. Onuchic, Energy landscape of knotted protein folding. Proc. Natl. Acad. Sci. 109(44), 17783-17788 (2012) · doi:10.1073/pnas.1201804109
[67] J.I. Sułkowska, E.J. Rawdon, K.C. Millett, J.N. Onuchic, A. Stasiak, Conservation of complex knotting and slipknotting patterns in proteins. Proc. Natl. Acad. Sci. 109(26), E1715-E1723 (2012) · doi:10.1073/pnas.1205918109
[68] J.I. Sułkowska, J.K. Noel, C.A. Ramírez-Sarmiento, E.J. Rawdon, K.C. Millett, J.N. Onuchic, Knotting pathways in proteins. Biochem. Soc. Trans. 41(2), 523-527 (2013) · doi:10.1042/BST20120342
[69] P. Szymczak, Tight knots in proteins: can they block the mitochondrial pores? Biochem. Soc. Trans. 41(2), 620-624 (2013) · doi:10.1042/BST20120261
[70] P. Szymczak, Periodic forces trigger knot untying during translocation of knotted proteins. Sci. Rep. 6 (2016)
[71] W.R. Taylor, A deeply knotted protein structure and how it might fold. Nature 406(6798), 916-919 (2000) · doi:10.1038/35022623
[72] K.L. Tkaczuk, S. Dunin-Horkawicz, E. Purta, J.M. Bujnicki, Structural and evolutionary bioinformatics of the spout superfamily of methyltransferases. BMC Bioinform. 8(1), 73 (2007) · doi:10.1186/1471-2105-8-73
[73] L. Tubiana, E. Orlandini, C. Micheletti, Probing the entanglement and locating knots in ring polymers: a comparative study of different arc closure schemes. Prog. Theor. Phys. Suppl. 191, 192-204 (2011) · doi:10.1143/PTPS.191.192
[74] I. Tuszynska, J.M. Bujnicki, Predicting atomic details of the unfolding pathway for yibk, a knotted protein from the spout superfamily. J. Biomol. Struct. Dyn. 27(4), 511-520 (2010) · doi:10.1080/07391102.2010.10507335
[75] E. Uehara, T. Deguchi, Statistical and hydrodynamic properties of topological polymers for various graphs showing enhanced short-range correlation. J. Chem. Phys. 145(16), 164905 (2016) · doi:10.1063/1.4965828
[76] P. Virnau, L.A. Mirny, M. Kardar, Intricate knots in proteins: function and evolution. PLoS Comput. Biol. 2(9), e122 (2006)
[77] P. Virnau, A. Mallam, S. Jackson, Structures and folding pathways of topologically knotted proteins. J. Phys. Condens. Matter 23(3), 033101 (2010) · doi:10.1088/0953-8984/23/3/033101
[78] J.R. Wagner, J.S. Brunzelle, K.T. Forest, R.D. Vierstra, A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438(7066), 325-331 (2005) · doi:10.1038/nature04118
[79] S. Wallin, K.B. Zeldovich, E.I. Shakhnovich, The folding mechanics of a knotted protein. J. Mol. Biol. 368(3), 884-893 (2007) · doi:10.1016/j.jmb.2007.02.035
[80] I. Wang, S.-Y. Chen, S.-T.D. Hsu, Unraveling the folding mechanism of the smallest knotted protein, mj0366. J. Phys. Chem. B 119(12), 4359-4370 (2015) · doi:10.1021/jp511029s
[81] I. Wang, S.-Y. Chen, S.-T.D. Hsu, Folding analysis of the most complex stevedore’s protein knot. Sci. Rep. 6 (2016)
[82] M. Wojciechowski, À. Gómez-Sicilia, M. Carrión-Vázquez, M. Cieplak, Unfolding knots by proteasome-like systems: simulations of the behaviour of folded and neurotoxic proteins. Mol. Biosyst. 12(9), 2700-2712 (2016) · doi:10.1039/C6MB00214E
[83] Y. Zhao, S. Niewieczerzal, P. Dabrowski-Tumanski, J.I. Sulkowska, The exclusive effects of chaperonin on the behavior of the 52 knotted proteins (under review)
[84] F. Ziegler, N.C. Lim, S.S. Mandal, B. Pelz, W.-P. Ng, M. Schlierf, S.E. Jackson, M. Rief, Knotting and
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