Solution structure of the symmetric coiled coil tetramer formed by the oligomerization domain of hnRNP C: Implications for biological function

Journal of Molecular Biology

Volumn 350, Issue 2, 2005, Pages 319-337

  Whitson, Stefanie R ^a   LeStourgeon, Wallace M ^a   Krezel, Andrzej M ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Coiled coil; hnRNP C; NMR; Symmetric oligomer; Tetramerization domain

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; MONOMER; TETRAMER;

ARTICLE; ELECTRICITY; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA BINDING; STOICHIOMETRY; STRUCTURE ANALYSIS;

EID: 20444371580     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.05.002     Document Type: Article

References (93)

1. J.G. McAfee, M. Huang, S. Soltaninassab, J.E. Rech, S. Iyengar, and W.M. LeStourgeon The packaging of pre-mRNA A.R. Krainer Eukaryotic mRNA Processing - Frontiers in Molecular Biology Series 1997 Oxford University Press New York 68 102
2. S.F. Barnett, D.L. Friedman, and W.M. LeStourgeon The C proteins of HeLa 40S nuclear ribonucleoprotein particles exist as anisotropic tetramers of (C1)3 C2 Mol. Cell Biol. 9 1989 492 498
3. B.M. Merrill, S.F. Barnett, W.M. LeStourgeon, and K.R. Williams Primary structure differences between proteins C1 and C2 of HeLa 40S nuclear ribonucleoprotein particles Nucl. Acids Res. 17 1989 8441 8449
4. G. Conway, J. Wooley, T. Bibring, and W.M. LeStourgeon Ribonucleoproteins package 700 nucleotides of pre-mRNA into a repeating array of regular particles Mol. Cell Biol. 8 1988 2884 2895
5. M. Huang, J.E. Rech, S.J. Northington, P.F. Flicker, A. Mayeda, A.R. Krainer, and W.M. LeStourgeon The C-protein tetramer binds 230 to 240 nucleotides of pre-mRNA and nucleates the assembly of 40S heterogeneous nuclear ribonucleoprotein particles Mol. Cell Biol. 14 1994 518 533
6. L. Shahied, E.H. Braswell, W.M. LeStourgeon, and A.M. Krezel An antiparallel four-helix bundle orients the high-affinity RNA binding sites in hnRNP C: a mechanism for RNA chaperonin activity J. Mol. Biol. 305 2001 817 828 10.1006/jmbi.2000.4331
7. M. Gorlach, M. Wittekind, R.A. Beckman, L. Mueller, and G. Dreyfuss Interaction of the RNA-binding domain of the hnRNP C proteins with RNA EMBO J. 11 1992 3289 3295
8. M. Gorlach, C.G. Burd, and G. Dreyfuss The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins J. Biol. Chem. 269 1994 23074 23078
9. L. Wan, J.K. Kim, V.W. Pollard, and G. Dreyfuss Mutational definition of RNA-binding and protein-protein interaction domains of heterogeneous nuclear RNP C1 J. Biol. Chem. 276 2001 7681 7688 10.1074/jbc.M010207200
10. J.G. McAfee, L. Shahied-Milam, S.R. Soltaninassab, and W.M. LeStourgeon A major determinant of hnRNP C protein binding to RNA is a novel bZIP-like RNA binding domain RNA 2 1996 1139 1152
11. L. Shahied-Milam, S.R. Soltaninassab, G.V. Iyer, and W.M. LeStourgeon The heterogeneous nuclear ribonucleoprotein C protein tetramer binds U1, U2, and U6 snRNAs through its high affinity RNA binding domain (the bZIP-like motif) J. Biol. Chem. 273 1998 21359 21367
12. J.H. Tan, Y. Kajiwara, L. Shahied, J. Li, J.G. McAfee, and W.M. LeStourgeon The bZIP-like motif of hnRNP C directs the nuclear accumulation of pre-mRNA and lethality in yeast J. Mol. Biol. 305 2001 829 838 10.1006/jmbi.2000.4332
13. J.R. Stone, J.L. Maki, and T. Collins Basal and hydrogen peroxide stimulated sites of phosphorylation in heterogeneous nuclear ribonucleoprotein C1/C2 Biochemistry 42 2003 1301 1308 10.1021/bi0268091
14. P.A. Fung, R. Labrecque, and T. Pederson RNA-dependent phosphorylation of a nuclear RNA binding protein Proc. Natl Acad. Sci. USA 94 1997 1064 1068
15. S.H. Mayrand, P. Dwen, and T. Pederson Serine/threonine phosphorylation regulates binding of C hnRNP proteins to pre-mRNA Proc. Natl Acad. Sci. USA 90 1993 7764 7768
16. P. Burkhard, J. Stetefeld, and S.V. Strelkov Coiled coils: a highly versatile protein folding motif Trends Cell Biol. 11 2001 82 88 10.1016/S0962-8924(00)01898-5
17. A. Lupas Coiled coils: new structures and new functions Trends Biochem. Sci. 21 1996 375 382 10.1016/0968-0004(96)10052-9
18. W.D. Kohn, C.T. Mant, and R.S. Hodges Alpha-helical protein assembly motifs J. Biol. Chem. 272 1997 2583 2586
19. A.D. McLachlan, and M. Stewart Tropomyosin coiled-coil interactions: evidence for an unstaggered structure J. Mol. Biol. 98 1975 293 304
20. D.L. Lee, P. Lavigne, and R.S. Hodges Are trigger sequences essential in the folding of two-stranded alpha-helical coiled-coils? J. Mol. Biol. 306 2001 539 553
21. K.T. O'Neil, and W.F. DeGrado A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids Science 250 1990 646 651
22. B.M. Huyghues-Despointes, and R.L. Baldwin Ion-pair and charged hydrogen-bond interactions between histidine and aspartate in a peptide helix Biochemistry 36 1997 1965 1970 10.1021/bi962546x
23. J.S. Smith, and J.M. Scholtz Energetics of polar side-chain interactions in helical peptides: salt effects on ion pairs and hydrogen bonds Biochemistry 37 1998 33 40 10.1021/bi972026h
24. P. Burkhard, R.A. Kammerer, M.O. Steinmetz, G.P. Bourenkov, and U. Aebi The coiled-coil trigger site of the rod domain of cortexillin I unveils a distinct network of interhelical and intrahelical salt bridges Struct. Fold. Des. 8 2000 223 230
25. J.Y. Su, R.S. Hodges, and C.M. Kay Effect of chain length on the formation and stability of synthetic alpha-helical coiled coils Biochemistry 33 1994 15501 15510
26. K.J. Lumb, C.M. Carr, and P.S. Kim Subdomain folding of the coiled coil leucine zipper from the bZIP transcriptional activator GCN4 Biochemistry 33 1994 7361 7367
27. S.Y. Lau, A.K. Taneja, and R.S. Hodges Synthesis of a model protein of defined secondary and quaternary structure. Effect of chain length on the stabilization and formation of two-stranded alpha-helical coiled-coils J. Biol. Chem. 259 1984 13253 13261
28. R. Fairman, H.G. Chao, L. Mueller, T.B. Lavoie, L. Shen, J. Novotny, and G.R. Matsueda Characterization of a new four-chain coiled-coil: influence of chain length on stability Protein Sci. 4 1995 1457 1469
29. K.M. Gernert, M.C. Surles, T.H. Labean, J.S. Richardson, and D.C. Richardson The Alacoil: a very tight, antiparallel coiled-coil of helices Protein Sci. 4 1995 2252 2260
30. O.D. Monera, N.E. Zhou, P. Lavigne, C.M. Kay, and R.S. Hodges Formation of parallel and antiparallel coiled-coils controlled by the relative positions of alanine residues in the hydrophobic core J. Biol. Chem. 271 1996 3995 4001
31. B. Lovejoy, S. Choe, D. Cascio, D.K. McRorie, W.F. DeGrado, and D. Eisenberg Crystal structure of a synthetic triple-stranded alpha-helical bundle Science 259 1993 1288 1293
32. P.B. Harbury, T. Zhang, P.S. Kim, and T. Alber A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants Science 262 1993 1401 1407
33. W.L. DeLano, and A.T. Brunger Helix packing in proteins: prediction and energetic analysis of dimeric, trimeric, and tetrameric GCN4 coiled coil structures Proteins 20 1994 105 123
34. B. Tripet, K. Wagschal, P. Lavigne, C.T. Mant, and R.S. Hodges Effects of side-chain characteristics on stability and oligomerization state of a de novo-designed model coiled-coil: 20 amino acid substitutions in position "d" J. Mol. Biol. 300 2000 377 402 10.1006/jmbi.2000.3866
35. K. Wagschal, B. Tripet, P. Lavigne, C. Mant, and R.S. Hodges The role of position a in determining the stability and oligomerization state of alpha-helical coiled coils: 20 amino acid stability coefficients in the hydrophobic core of proteins Protein Sci. 8 1999 2312 2329
36. A. Solan, K. Ratia, and R. Fairman Exploring the role of alanine in the structure of the Lac repressor tetramerization domain, a ferritin-like Alacoil J. Mol. Biol. 317 2002 601 612 10.1006/jmbi.2002.5427
37. S.A. Potekhin, V.N. Medvedkin, I.A. Kashparov, and S. Venyaminov Synthesis and properties of the peptide corresponding to the mutant form of the leucine zipper of the transcriptional activator GCN4 from yeast Protein Eng. 7 1994 1097 1101
38. S. Alberti, S. Oehler, B. von Wilcken-Bergmann, and B. Muller-Hill Genetic analysis of the leucine heptad repeats of Lac repressor: evidence for a 4-helical bundle EMBO J. 12 1993 3227 3236
39. O.D. Monera, C.M. Kay, and R.S. Hodges Electrostatic interactions control the parallel and antiparallel orientation of alpha-helical chains in two-stranded alpha-helical coiled-coils Biochemistry 33 1994 3862 3871
40. R.P. Sheridan, R.M. Levy, and F.R. Salemme Alpha-helix dipole model and electrostatic stabilization of 4-alpha-helical proteins Proc. Natl Acad. Sci. USA 79 1982 4545 4549
41. J.G. McAfee, S.R. Soltaninassab, M.E. Lindsay, and W.M. LeStourgeon Proteins C1 and C2 of heterogeneous nuclear ribonucleoprotein complexes bind RNA in a highly cooperative fashion: support for their contiguous deposition on pre-mRNA during transcription Biochemistry 35 1996 1212 1222 10.1021/bi951974k
42. J. Cavanagh, W.J. Fairbrother, A.G. Palmer, and N.J. Skelton Protein NMR spectroscopy 1996 Academic Press San Diego pp. 16-19
43. S. O'Donaghue, and M. Nilges Calculation of symmetric oligomer structures from NMR data M. Krishna L. Berliner Biological Magnetic Resonance: Structure, Computation and Dynamics in Protein NMR Vol. 17 1999 Kluwer Academic/Plenam Publishers New York 131 161
44. J.V. Staros N-hydroxysulfosuccinimide active esters: bis(N- hydroxysulfosuccinimide) esters of two dicarboxylic acids are hydrophilic, membrane-impermeant, protein cross-linkers Biochemistry 21 1982 3950 3955
45. D. Wishart, and B. Sykes Chemical shifts as a tool for structure determination Methods Enzymol. 239 1994 363 392
46. B. Tripet, and R.S. Hodges STABLECOIL: An algorithm designed to predict the location and relative stability of coiled-coils in native protein sequences M. Lebl R. Houghten Peptides: The Wave of the Future, Proceedings of the Second International/Seventeenth American Peptide Symposium 2001 Kluwer Academic Publishers New York 365 366
47. G. Bodenhausen, and D. Ruben Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy Chem. Phys. Letters 69 1980 185 189
48. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, and H. Weissig The Protein Data Bank Nucl. Acids Res 28 2000 235 242
49. A.M. Friedman, T.O. Fischmann, and T.A. Steitz Crystal structure of lac repressor core tetramer and its implications for DNA looping Science 268 1995 1721 1727
50. D.W. Banner, M. Kokkinidis, and D. Tsernoglou Structure of the ColE1 rop protein at 1.7 A resolution J. Mol. Biol. 196 1987 657 675
51. R.B. Sutton, D. Fasshauer, R. Jahn, and A.T. Brunger Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution Nature 395 1998 347 353 10.1038/26412
52. F.H.C. Crick The packing of α-helices: simple coiled coils Acta Crystallog. 6 1953 689 697
53. J. Walshaw, and D.N. Woolfson Socket: a program for identifying and analysing coiled-coil motifs within protein structures J. Mol. Biol. 307 2001 1427 1450 10.1006/jmbi.2001.4545
54. L. Lo Conte, C. Chothia, and J. Janin The atomic structure of protein-protein recognition sites J. Mol. Biol. 285 1999 2177 2198 10.1006/jmbi.1998.2439
55. D. Krylov, I. Mikhailenko, and C. Vinson A thermodynamic scale for leucine zipper stability and dimerization specificity: e and g interhelical interactions EMBO J. 13 1994 2849 2861
56. M. Eilers, A.B. Patel, W. Liu, and S.O. Smith Comparison of helix interactions in membrane and soluble alpha-bundle proteins Biophys. J. 82 2002 2720 2736
57. W.D. Kohn, C.M. Kay, and R.S. Hodges Orientation, positional, additivity, and oligomerization-state effects of interhelical ion pairs in alpha-helical coiled-coils J. Mol. Biol. 283 1998 993 1012 10.1006/jmbi.1998.2125
58. C.N. Pace Polar group burial contributes more to protein stability than nonpolar group burial Biochemistry 40 2001 310 313 10.1021/bi001574j
59. J.E. Rech, W.M. LeStourgeon, and P.F. Flicker Ultrastructural morphology of the hnRNP C protein tetramer J. Struct. Biol. 114 1995 77 83
60. D.G. Kneller, F.E. Cohen, and R. Langridge Improvements in protein secondary structure prediction by an enhanced neural network J. Mol. Biol. 214 1990 171 182
61. J. Garnier, J.-F. Gibrat, and B. Robson GOR secondary structure prediction method version IV Methods Enzymol. 266 1996 540 553
62. A.K. Das, N.R. Helps, P.T. Cohen, and D. Barford Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution EMBO J. 15 1996 6798 6809
63. F. Corpet, J. Gouzy, and D. Kahn The ProDom database of protein domain families Nucl. Acids Res. 26 1998 323 326
64. S. Nakielny, and G. Dreyfuss The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals J. Cell Biol. 134 1996 1365 1373
65. H. Siomi, and G. Dreyfuss RNA-binding proteins as regulators of gene expression Curr. Opin. Genet. Dev. 7 1997 345 353
66. M. Piotto, V. Saudek, and V. Sklenar Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions J. Biomol. NMR 2 1992 661 665
67. C. Bartels, T. Xia, M. Billeter, P. Güntert, and K. Wüthrich The program XEASY for computer-supported NMR spectral analysis of biological macromolecules J. Biomol. NMR 5 1995 1 10
68. J.L. Markley, A. Bax, Y. Arata, C.W. Hilbers, R. Kaptein, and B.D. Sykes Recommendations for the presentation of NMR structures of proteins and nucleic acids: IUPAC-IUBMB-IUPAB inter-union task group on the standardization of databases of protein and nucleic acid structures determined by NMR spectroscopy J. Biomol. NMR 12 1998 1 23
69. M. Bendall, D. Pegg, D. Doddrell, and J. Field Inverse DEPT sequence. Polarization transfer from a spin 1/2 nucleus to n spin 1/2 heteronuclei via correlated motion in the doubly rotating reference frame J. Magn. Reson. 51 1983 520 526
70. S. Grzesiek, and A. Bax Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR J. Am. Chem. Soc. 114 1992 6291 6293
71. S. Grzesiek, and A. Bax An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins J. Magn. Reson. 99 1992 201 207
72. A. Bax, and M. Ikura An efficient 3D NMR technique for correlating the proton and 15N backbone resonances with the alpha-carbon of the preceding residue in uniformly 15N/13C enriched proteins J. Biomol. NMR 1 1991 99 104
73. M. Sattler, J. Schleucher, and C. Griesinger Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients Prog. NMR Spectrosc. 34 1999 93 158
74. A. Kumar, R. Ernst, and K. Wüthrich A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules Biochem. Biophys. Res. Commun. 95 1980 1 6
75. D. Marion, L. Kay, S. Sparks, D. Torchia, and A. Bax Three-dimensional heteronuclear NMR of 15N labeled proteins J. Am. Chem. Soc. 111 1989 1515 1517
76. A. Bax, G. Clore, and A. Gronenborn 1H-1H correlation via isotropic mixing of 13C magnetization, a new three-dimensional approach for assigning 1H and 13C spectra of 13C enriched proteins J. Magn. Reson. 88 1990 425 431
77. L. Kay, G. Xu, A. Singer, D. Muhandiram, and J. Forman-Kay A gradient-enhanced HCCH-TOCSY experiment for recording side-chain 1H and 13C correlations in H2O samples of proteins J. Magn. Reson. B 101 1993 333 337
78. E. Zuiderweg, A. Petros, S. Fesik, and E. Olejniczak Four-dimensional [13C, 1H, 13C, 1H] HMQC-NOE-HMQC NMR spectroscopy: resolving tertiary NOE distance constraints in the spectra of larger proteins J. Am. Chem. Soc. 113 1991 370 372
79. G. Vuister, G. Clore, A. Gronenborn, R. Powers, D. Garrett, R. Tschudin, and A. Bax Increased resolution and improved spectral quality in four-dimensional 13C/13C-separated HMQC-NOESY-HMQC spectra using pulsed field gradients J. Magn. Reson. 101 1993 210 213
80. G. Vuister, A. Wang, and A. Bax Measurement of three-bond nitrogen-carbon J couplings in proteins uniformly enriched in 15N and 13C J. Am. Chem. Soc. 115 1993 5334 5335
81. N.A. Farrow, R. Muhandiram, A.U. Singer, S.M. Pascal, C.M. Kay, and G. Gish Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation Biochemistry 33 1994 5984 6003
82. P. Güntert, C. Mumenthaler, and K. Wüthrich Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273 1997 283 298
83. R.A. Laskowski, J.A. Rullmann, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486
84. D. Bashford, and D.A. Case Generalized Born models of macromolecular solvation effects Annu. Rev. Phys. Chem. 51 2000 129 152 10.1146/annurev. physchem.51.1.129
85. B. Xia, V. Tsui, D.A. Case, H.J. Dyson, and P.E. Wright Comparison of protein solution structures refined by molecular dynamics simulation in vacuum, with a generalized Born model, and with explicit water J. Biomol. NMR 22 2002 317 331
86. D.A. Pearlman, D.A. Case, J.W. Caldwell, W.R. Ross, T.E. Cheatham III, and S. DeBolt AMBER, a computer program for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to elucidate the structures and energies of molecules Comp. Phys. Commun. 91 1995 1 41
87. R. Koradi, M. Billeter, and K. Wüthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 29 32 see also pp. 51-5
88. A. Nicholls, K.A. Sharp, and B. Honig Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons Proteins 11 1991 281 296
89. M.S. Swanson, T.Y. Nakagawa, K. LeVan, and G. Dreyfuss Primary structure of human nuclear ribonucleoprotein particle C proteins: conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and pre-rRNA-binding proteins Mol. Cell Biol. 7 1987 1731 1739
90. W. Jiang, X. Guo, and V.P. Bhavanandan Four distinct regions in the auxiliary domain of heterogeneous nuclear ribonucleoprotein C-related proteins Biochim. Biophys. Acta 1399 1998 229 233
91. D.J. Williamson, S. Banik-Maiti, J. DeGregori, and H.E. Ruley hnRNP C is required for postimplantation mouse development but is dispensable for cell viability Mol. Cell Biol. 20 2000 4094 4105
92. F. Preugschat, and B. Wold Isolation and characterization of a Xenopus laevis C protein cDNA: structure and expression of a heterogeneous nuclear ribonucleoprotein core protein Proc. Natl Acad. Sci. USA 85 1988 9669 9673
93. E.J. Michaud, S.J. Bultman, L.J. Stubbs, and R.P. Woychik The embryonic lethality of homozygous lethal yellow mice (Ay/Ay) is associated with the disruption of a novel RNA-binding protein Genes Dev. 7 1993 1203 1213