Dynamical insight into Caenorhabditis elegans eIF4E recognition specificity for mono-and trimethylated structures of mRNA 5′ cap

Journal of Molecular Modeling

Volumn 17, Issue 4, 2011, Pages 727-737

  Ruszczyńska Bartnik, Katarzyna ^a   MacIejczyk, MacIej ^a,c   Stolarski, Ryszard ^b  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b UNIVERSITY OF WARSAW   (Poland)

^c UNIVERSITY OF WARMIA AND MAZURY IN OLSZTYN   (Poland)

Author keywords

Caenorhabditis elegans; Cap recognition; eIF4E isoforms; Molecular dynamics; mRNA 5 cap

Indexed keywords

7 METHYLGUANOSINE; CARBOXYLIC ACID; GLUTAMIC ACID; GUANOSINE; INITIATION FACTOR 4E; N2,N2,7 TRIMETHYLGUANOSINE; UNCLASSIFIED DRUG; WATER;

5' UNTRANSLATED REGION; ARTICLE; ASCARIS SUUM; CAENORHABDITIS ELEGANS; CHEMICAL STRUCTURE; COMPLEX FORMATION; DISSOCIATION; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SCHISTOSOMA MANSONI; SIMULATION;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; EUKARYOTIC INITIATION FACTOR-4E; METHYLATION; MICE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RNA CAPS; RNA, MESSENGER; SEQUENCE ALIGNMENT;

ASCARIS SUUM; CAENORHABDITIS ELEGANS; EUKARYOTA; MAMMALIA; MURINAE; SCHISTOSOMA;

EID: 79955590425     PISSN: 16102940     EISSN: 09485023     Source Type: Journal    
DOI: 10.1007/s00894-010-0773-x     Document Type: Article

References (59)

1. B Joshi A Cameron R Jagus 2004 Characterisation of mammalian eIF4E-famili members Eur J Biochem 271 2189 2203 10.1111/j.1432-1033.2004.04149.x 1:CAS:528:DC%2BD2cXkvVChurw%3D (Pubitemid 38747988)
2. JD Lewis E Izaurralde 1997 The role of the cap structure in RNA processing and nuclear export Eur J Biochem 247 461 469 10.1111/j.1432-1033. 1997.00461.x 1:CAS:528:DyaK2sXlsVCntbY%3D (Pubitemid 27308622)
3. H Liu ND Rodgers X Jiao M Kiledijian 2002 The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphates EMBO J 21 4699 4708 10.1093/emboj/cdf448 1:CAS:528:DC%2BD38Xms1Knu7s%3D (Pubitemid 34984357)
4. U Kühn E Wahle 2004 Structure and function of poly(A) binding proteins Biochim Biophys Acta 1678 67 84 (Pubitemid 38626168)
5. J Martinez Y-G Ren A-C Thuresson U Hellman J Åström A Virtanen 2000 A 54-kDa fragment of the poly(A)-specific ribonuclease is oligomeric, processive, and cap-interacting poly(A)-specific 3′ exonuclease J Biol Chem 275 24222 24230 10.1074/jbc.M001705200 1:CAS:528:DC%2BD3cXls12ltrk%3D (Pubitemid 30624713)
6. KA Hudak JD Bauman NE Tumer 2002 Pokeweed antiviral protein binds to the cap structure of eukaryotic mRNA and depurinates the mRNA downstream of the cap RNA 8 1148 1159 10.1017/S1355838202026638 1:CAS:528:DC%2BD38XntlOhsrk%3D (Pubitemid 35024571)
7. C Fabrega S Hausmann V Shen S Shuman CD Lima 2004 Structure and mechanism of mRNA cap (Guanine-N7) methyltransferase Mol Cell 13 77 89 10.1016/S1097-2765(03)00522-7 1:CAS:528:DC%2BD2cXovFWjtA%3D%3D (Pubitemid 38117117)
8. X Wang TMT Hall 2001 Structural basis for recognition of AU-rich element RNA by the HuD protein Nat Struct Biol 8 141 145 10.1038/84131 1:CAS:528:DC%2BD3MXhtVShtbs%3D (Pubitemid 32116066)
9. AE Hodel PD Gershon X Shi S-M Wang FA Quiocho 1997 Specific protein recognition of an mRNA cap through its alkylated base Nat Struct Biol 4 350 354 10.1038/nsb0597-350 1:CAS:528:DyaK2sXivFWnt7k%3D
10. D Guilligay F Tarendeau P Resa-Infante R Coloma T Crepin P Sehr J Lewis RW Ruigrok J Ortin DJ Hart S Cusack 2008 The structural basis for cap binding by influenza virus polymerase subunit PB2 Nat Struct Mol Biol 15 500 506 10.1038/nsmb.1421 1:CAS:528:DC%2BD1cXlsFSltbs%3D (Pubitemid 351653591)
11. 7G-cap hypermethylation of small nuclear, small nucleolar and telomerase RNA by the dimethyltransferase TGS1 Nucleic Acids Res 37 3865 3877 10.1093/nar/gkp249 1:CAS:528:DC%2BD1MXovVektrw%3D
12. A Niedzwiecka J Marcotrigiano J Stepinski M Jankowska-Anyszka A Wyslouch-Cieszynska M Dadlez A-C Gingras P Mak E Darzynkiewicz N Sonenberg SK Burley R Stolarski 2002 Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5′ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins J Mol Biol 319 615 635 10.1016/S0022-2836(02)00328-5 1:CAS:528:DC%2BD38XkvVahsLc%3D (Pubitemid 34729439)
13. T Blumenthal 1998 Gene clusters and polycistronic transcription in eukaryotes BioEssays 20 480 487 10.1002/(SICI)1521-1878(199806)20:6<480::AID- BIES6>3.0.CO;2-Q 1:STN:280:DyaK1czmsVKitA%3D%3D (Pubitemid 28320610)
14. M Jankowska-Anyszka BJ Lamphear EJ Aamodt T Harrington E Darzynkiewicz R Stolarski RE Rhoads 1998 Multiple isoforms of eukaryotic protein syntesis initiation factor 4E in Caenorhabditis elegans can distinguish between mono-and trimethylated mRNA cap structures J Biol Chem 273 10538 10542 10.1074/jbc.273.17.10538 1:CAS:528:DyaK1cXivFKntbc%3D (Pubitemid 28227664)
15. BD Keiper BJ Lamphear AM Desphande M Jankowska-Anyszka EJ Aamodt T Blumenthal RE Rhoads 2000 Functional characterization of five eIF4E isoforms in Caenorhabditis elegans J Biol Chem 275 10590 10596 10.1074/jbc.275.14.10590 1:CAS:528:DC%2BD3cXisFWjtbY%3D (Pubitemid 30202125)
16. A Stachelska Z Wieczorek K Ruszczynska R Stolarski M Pietrzak BJ Lamphear RE Rhoads E Darzynkiewicz M Jankowska-Anyszka 2002 Interaction of three Caenorhabditis elegans isoforms of translation initiation factor eIF4E with mono-and trimethylated mRNA 5′ cap analogues Acta Biochim Pol 49 671 682 1:CAS:528:DC%2BD38Xps12isb4%3D (Pubitemid 135700593)
17. H Miyoshi DS Dwyer BD Keiper M Jankowska-Anyszka E Darzynkiewicz RE Rhoads 2002 Discrimination between mono-and trimethylated cap structures by two isoforms of Caenorhabditis elegans eIF4E EMBO J 21 4680 4690 10.1093/emboj/cdf473 1:CAS:528:DC%2BD38Xms1Kms7k%3D (Pubitemid 34984355)
18. W Liu R Zhao C McFarland J Kieft A Niedzwiecka M Jankowska-Anyszka J Stepinski E Darzynkiewicz DNM Jones RE Davis 2009 Structural insight into parasite eIF4E binding specificity for m7G and m2, 2, 7G mRNA cap J Biol Chem 284 31336 31349 10.1074/jbc.M109.049858 1:CAS:528:DC%2BD1MXhtlCjsr7E
19. S Lall CC Friedman M Jankowska-Anyszka J Stepinski Darzynkiewicz RE Davis 2004 Contribution of trans-splicing, 5′-leader length, cap-poly(A) synergism, and initiation factors to nematode translation in an Ascaris suum embryo cell-free system J Biol Chem 279 45573 45585 10.1074/jbc.M407475200 1:CAS:528:DC%2BD2cXovVCnsrc%3D (Pubitemid 39491544)
20. A Strasser A Dickmanns R Luehrmann R Ficner 2005 Structural basis for m(3)G-cap-mediated nuclear import of spliceosomal UsnRNPs by snurportin1 EMBO J 24 2235 2243 10.1038/sj.emboj.7600701 1:CAS:528:DC%2BD2MXlvVWqsb8%3D (Pubitemid 41032577)
21. C Mazza A Segref IW Mattaj S Cusack 2002 Large-scale induced fit recognition of an m7G pppG cap analogue by the human nuclear cap-binding complex EMBO J 21 5548 5557 10.1093/emboj/cdf538 1:CAS:528:DC%2BD38XnvF2qtbk%3D (Pubitemid 35231034)
22. G Calero K Wilson T Ly JR Rios-Steiner J Clardy RA Cerione 2002 Structural basis of m(7)GpppG binding to the nuclear cap-binding protein complex Nat Struct Biol 9 912 917 10.1038/nsb874 1:CAS:528:DC%2BD38XovVyitbk%3D (Pubitemid 35417059)
23. J Marcotrigiano AC Gingras N Sonenberg SK Burley 1997 Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP Cell 89 951 961 10.1016/S0092-8674(00)80280-9 1:CAS:528:DyaK2sXktFakt74%3D (Pubitemid 27513521)
24. K Tomoo X Shen K Okabe Y Nozoe S Fukuhara S Morino T Ishida T Taniguchi H Hasegawa A Terashima M Sasaki Y Katsuya K Kitamura H Miyoshi M Ishikawa K Miura 2002 Crystal structures of 7-methylguanosine 5′-triphosphate (m(7)GTP)-and P(1)-7-methylguanosine-P(3)-adenosine-5′, 5′-triphosphate (m(7)GpppA)-bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible region Biochem J 362 539 544 10.1042/0264-6021:3620539 1:CAS:528:DC%2BD2cXit1eq (Pubitemid 34242303)
25. K Tomoo X Shen K Okabe Y Nozoe S Fukuhara S Morino M Sasaki T Taniguchi H Miyagawa K Kitamura K Miura T Ishida 2003 Structural features of human initiation factor 4E, studied by X-ray crystal analysis,and molecular dynamics simulations J Mol Biol 328 365 383 10.1016/S0022-2836(03)00314-0 1:CAS:528:DC%2BD3sXislehtro%3D (Pubitemid 36407580)
26. M Gu C Fabrega SW Liu H Liu M Kiledjian CD Lima 2004 Insights into the structure, mechanism, and regulation of scavenger mRNA decapping activity Mol Cell 14 67 80 10.1016/S1097-2765(04)00180-7 1:CAS:528:DC%2BD2cXjvVaqtr4%3D (Pubitemid 38469910)
27. N Chen MA Walsh Y Liu R Parker H Song 2005 Crystal Structures of human DcpS in ligand-free and m7GDP-bound forms suggest a dynamic mechanism for scavenger mRNA decapping J Mol Biol 347 707 718 10.1016/j.jmb.2005.01.062 1:CAS:528:DC%2BD2MXitlCgur4%3D (Pubitemid 40357914)
28. P Fechter L Mingay J Sharps A Chambers E Fodor GG Brownlee 2003 Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding J Biol Chem 278 20381 20388 10.1074/jbc.M300130200 1:CAS:528:DC%2BD3sXktVejsLo%3D (Pubitemid 36799239)
29. Af Monzingo S Dhaliwal A Dutt-Chaudhuri A Lyon JH Sadow DW Hoffman JD Robertus KS Browning 2007 The structure of the translation initiation factor eIF4E from wheat reveals a novel disulfide bond Plant Physiol 143 1504 1518 10.1104/pp.106.093146 1:CAS:528:DC%2BD2sXksFWjt74%3D (Pubitemid 46849464)
30. 7GDP and interaction with 4E-binding protein Nat Struct Biol 4 717 724 10.1038/nsb0997-717 1:CAS:528:DyaK2sXmtl2qu7k%3D (Pubitemid 27382431)
31. Y Tao DL Farsetta M Nibert SC Harrison 2002 RNA Synthesis in a cage-structural studies of reovirus polymerase λ3 Cell 111 733 745 10.1016/S0092-8674(02)01110-8 1:CAS:528:DC%2BD38XptlGrur0%3D (Pubitemid 35452525)
32. CJ Brown CS Verma MD Walkinshaw DP Lane 2009 Crystallization of eIF4E complexed with eIF4GI peptide and grycerol reveals distinct structural differences around the cap-binding site Cell Cycle 8 1905 1911 10.4161/cc.8.12.8742 1:CAS:528:DC%2BD1MXhsVOhs73M
33. M Goette MC Stumpe R Ficner H Grubmüller 2009 Molecular determinants of snurportin 1 ligand afinity and structural response upon binding Biophys J 97 581 589 10.1016/j.bpj.2009.04.049 1:CAS:528:DC%2BD1MXpsFOmtr8%3D
34. MJ Brower EF Cohen RL Dunbrack 1997 Prediction of protein side-chains rotamers from backbone dependent rotamer library: a new homology modeling tool J Mol Biol 267 1268 1282 10.1006/jmbi.1997.0926 (Pubitemid 27192637)
35. JD Thompson DG Higgins TJ Gibson 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choise Nucleic Acids Res 22 4673 4680 10.1093/nar/22.22.4673 1:CAS:528:DyaK2MXitlSgu74%3D (Pubitemid 24354800)
36. A Sali TL Blundell 1993 Comparative protein modelling by satisfaction of spatial restraints J Mol Biol 234 779 815 10.1006/jmbi.1993.1626 1:CAS:528:DyaK2cXnt1ylug%3D%3D (Pubitemid 24007801)
37. Mann G, Yun RH, Nyland L, Prins J, Board J, Hermans J (2002) Sigma MD program and a generic interface applicable to multifunctional programs with complex, hierarchical command structure. In: Schlick T, Gan HH (eds) Computational methods for macromoleules: challenges and applications. Springer, Berlin, pp 129-145
38. AD Mac Kerell Jr D Bashford M Bellot, et al. 1998 All-atom empirical potential for molecular modeling and dynamics studies of ptoteins J Phys Chem 102 3586 3616 (Pubitemid 128576688)
39. W Jorgensen J Chandrasekar J Madura R Impey M Klein 1983 Comparison of simple potential function for simulating liquid water J Chem Phys 79 936 935 10.1063/1.445870
40. HJC Berendsen JCM Postma WE van Gunsteren A Di Nola JR Haak 1984 Molecular dynamics with coupling to an external bath J Chem Phys 81 3684 3690 10.1063/1.448118 1:CAS:528:DyaL2cXmtlGksbY%3D
41. JP Ryckaert G Cicciotti HJC Berebdsen 1977 Numerical integration of the Cartesian equations of mosion of a system with constraints: molecular dynamics of n-alkanes J Comput Phys 23 327 341 10.1016/0021-9991(77)90098-5 1:CAS:528:DyaE2sXktVGhsL4%3D
42. NE Tuckreman BJ Berne GJ Martyna 1992 Reversible multiple time scale molecular dynamics J Chem Phys 97 1990 2001 10.1063/1.463137
43. TA Darden DM York LG Pedersen 1993 Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems J Chem Phys 98 10089 10092 10.1063/1.464397 1:CAS:528:DyaK3sXks1Ohsr0%3D
44. T Schlick R Skeel A Brünger L Kale JA Board Jr J Hermans K Schulten 1999 Algorithmic challanges in computational molecular biophysics J Comput Phys 151 9 48 10.1006/jcph.1998.6182 1:CAS:528:DyaK1MXivFejt7o%3D
45. A Amadei ABM Linssen HJC Berendsen 1993 Essential dynamics of proteins Proteins Struct Funct Bioinf 17 412 425 10.1002/prot.340170408 1:CAS:528:DyaK2cXis1Ghsbc%3D (Pubitemid 23358549)
46. AE Mark WF van Gunsteren 1994 Decomposition of the free energy of a system in terms of specific interactions. Implications fot theoretical and experimental studies J Mol Biol 240 167 176 10.1006/jmbi.1994.1430 1:CAS:528:DyaK2cXlslegsbk%3D (Pubitemid 24221737)
47. S Boresch G Archontis M Karplus 1994 Free energy simulations: the meaning of the individual contributions from a component analysis Proteins Struct Funct Bioinf 20 25 33 10.1002/prot.340200105 1:CAS:528:DyaK2MXhtVant7k%3D (Pubitemid 24308147)
48. L Volpon MJ Osborne I Topisirovic N Siddiqui KL Borden 2006 Cap-free structure of eIF4E suggests a basis for conformational regulation by its ligands EMBO J 25 5138 5149 10.1038/sj.emboj.7601380 1:CAS:528:DC%2BD28XhtFChsrzI (Pubitemid 44658531)
49. I Rutkowska-Wlodarczyk J Stepinski M dadlez E Darzynkiewicz R Stolarski A Niedzwiecka 2008 Structural changes of eIF4E upon binding to the mRNA 5′ monomethylguanosine and trimethylguanosine cap Biochemistry 47 2710 2720 10.1021/bi701168z 1:CAS:528:DC%2BD1cXhtFantL4%3D (Pubitemid 351328821)
50. 7-alkylated cap derivatives J Mol Biol 372 7 15 10.1016/j.jmb.2007.06.033 1:CAS:528: DC%2BD2sXovFeqsrc%3D (Pubitemid 47241139)
51. E Blachut-Okrasinska E Bojarska A Niedzwiecka L Chlebicka E Darzynkiewicz R Stolarski J Stepinski JM Antosiewicz 2000 Stopped-flow and Brownian dynamic studies of electrostatic effects in the kinetics of binding of 7-methyl-GpppG to the protein eIF4E Eur Biophys J 29 487 498 10.1007/s002490000096 1:CAS:528:DC%2BD3cXosVOls7o%3D
52. A Niedzwiecka J Stepinski JM Antosiewicz E Darzynkiewicz R Stolarski 2007 Biophysical approach to studies of cap-eIF4E interaction by synthetic cap analogs Meth Enzymol 430 209 245 10.1016/S0076-6879(07)30009-8 1:CAS:528:DC%2BD1cXhsVeqtLY%3D
53. SV Slepenkov E Darzynkiewicz RE Rhoads 2006 Stopped-flow kinetic analysis of eIF4E and phosphorylated eIF4E binding to cap analogs and capped oligoribonucleotides J Biol Chem 281 14927 14938 10.1074/jbc.M601653200 1:CAS:528:DC%2BD28XkslGqtrg%3D (Pubitemid 43855197)
54. P Kuzmic 1996 Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV protease Anal Biochem 237 260 273 10.1006/abio.1996.0238 1:CAS:528:DyaK28XjtlOktL4%3D (Pubitemid 26177089)
55. J Zuberek J Jemielity A Jablonowska J Stepinski M Dadlez R Stolarski E darzynkiewicz 2004 Influence of electric charge variation at residues 209 and 159 on the interaction of eIF4E with the mRNA 5′ terminus Biochemistry 43 5370 5379 10.1021/bi030266t 1:CAS:528:DC%2BD2cXjtVyrt7c%3D (Pubitemid 38620929)
56. AE Hodel PD Gershon X Shi S-M Wang AA Quiocho 1997 Specific protein recognition of an mRNA cap through its alkylated base Nat Struct Biol 4 350 354 10.1038/nsb0597-350 1:CAS:528:DyaK2sXivFWnt7k%3D
57. P Fechter GG Brownlee 2005 Recognition of mRNA cap structures by viral and cellular proteins J Gen Virol 86 1239 1249 10.1099/vir.0.80755-0 1:CAS:528:DC%2BD2MXjvFSksbk%3D (Pubitemid 40613240)
58. R Worch M Jankowska-Anyszka A Niedzwiecka J Stepinski K Mazza E Darzynkiewicz S Cusack R Stolarski 2009 Diverse role of three tyrosines in binding of the RNA 5′ cap to the human nuclear cap binding complex J Mol Biol 385 618 627 10.1016/j.jmb.2008.10.092 1:CAS:528:DC%2BD1MXkt1Wnsw%3D%3D
59. R Worch R Stolarski 2008 Stacking efficienct and flexibility analysis of aromatic amino acids in cap-binding proteins Proteins Struct Funct Bioinf 71 2026 2037 10.1002/prot.21882 1:CAS:528:DC%2BD1cXmsVWltL0%3D (Pubitemid 351732953)