Understanding the molecular machinery of genetics through 3D structures

Nature Reviews Genetics

Volumn 9, Issue 2, 2008, Pages 141-151

  Laskowski, Roman A ^a   Thornton, Janet M ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; CHROMATIN STRUCTURE; DNA SEQUENCE; EPIGENETICS; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE INSERTION; GENE MUTATION; GENETIC VARIABILITY; MOLECULAR GENETICS; PRIORITY JOURNAL; REVIEW; RNA SPLICING; THREE DIMENSIONAL IMAGING;

AMINO ACID SEQUENCE; ANIMALS; CHROMATIN; DATABASES, PROTEIN; EPIGENESIS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GENOMICS; HUMANS; IMAGING, THREE-DIMENSIONAL; MODELS, MOLECULAR; MOLECULAR BIOLOGY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; NUCLEIC ACID CONFORMATION; POINT MUTATION; PROTEINS; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 38349144394     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg2273     Document Type: Review

References (104)

1. Watson, J. D. & Crick, F. H. C. A structure for deoxyribose nucleic acid. Nature 171, 737-738 (1953).
2. Franklin, R. E. & Gosling, R. G. Molecular configuration in sodium thymonucleate. Nature 171, 740-741 (1953).
3. Kendrew, J. C. et al. Structure of myoglobin: a three-dimensional Fourier synthesis at 2Å resolution. Nature 185, 422-427 (1960).
4. Dutta, S. & Berman, H. M. Large macromolecular complexes in the Protein Data Bank: a status report. Structure 13, 381-388 (2005). An interesting Review of some of the large 3D structures that have been solved.
5. Adrian, M., Dubochet, J., Lepault, J. & McDowall, A. W. Cryo-electron microscopy of viruses. Nature 308, 32-36 (1984).
6. Grünewald, K. & Cyrklaff, M. Structure of complex viruses and virus-infected cells by electron cryo tomography. Curr. Opin. Microbiol. 9, 437-442 (2006).
7. Chothia, C. & Lesk, A. M. The relation between the divergence of sequence and structure in proteins. EMBO J. 5, 823-826 (1986). The first demonstration that protein 3D structure is better conserved than sequence is.
8. Rost, B. Twilight zone of protein sequence alignments. Protein Eng. 12, 85-94 (1999).
9. Pearl, F. M. G. et al. The CATH extended protein-family database: providing structural annotations for genome sequences. Prot. Sci. 11, 233-244 (2002).
10. Marsden, R. L. et al. Exploiting protein structure data to explore the evolution of protein function and biological complexity. Phil. Trans. Royal Soc. B-Biol. Sci. 361, 425-440 (2006).
11. Orengo, C. A., Sillitoe, I., Reeves, G. & Pearl, F. M. G. What can structural classifications reveal about protein evolution? J. Struct. Biol. 134, 145-165 (2001).
12. Lee, D., Grant, A., Buchan, D. & Orengo, C. A structural perspective on genome evolution. Curr. Opin. Struct. Biol. 13, 359-369 (2003).
13. Vogel, C., Bashton, M., Kerrison, N. D., Chothia, C. & Teichmann, S. A. Structure, function and evolution of multidomain proteins. Curr. Opin. Struct. Biol. 14, 208-216 (2004).
14. Ranea, J. A. G., Sillero, A. Thornton, J. M. & Orengo, C. A. Protein superfamily evolution and the last universal common ancestor (LUCA). J. Mol. Evol. 63, 513-525 (2006). These authors argue that the protein domains that are present across all kingdoms of life may have been present in the last universal common ancestor.
15. Martin, A. C. R. et al. Protein folds and functions. Structure 6, 875-884 (1998).
16. Matthews, B. W. Structural and genetic analysis of protein stability. Annu. Rev. Biochem. 62, 139-160 (1993).
17. Sinha, N. & Nussinov, R. Point mutations and sequence variability in proteins: redistributions of preexisting populations. Proc. Natl Acad. Sci. USA 98, 3139-3144 (2001).
18. Stenson, P. D. et al. Human Gene Mutation Database (HGMD): 2003 update. Hum. Mutat. 21, 577-581 (2003).
19. Wang, Z. & Moult, J. SNPs, protein structure, and disease. Hum. Mutat. 17, 263-270 (2001).
20. Steward, R. E., MacArthur, M. W, Laskowski, R. A. & Thornton, J. M. Molecular basis of inherited diseases: a structural perspctive. Trends Genet. 19, 505-513 (2003).
21. Ferrer-Costa, C., Orozco, M. & de la Cruz, X. Characterization of disease-associated single amino acid polymorphisms in terms of sequence and structure properties. J. Mol. Biol. 315, 771-786 (2002).
22. Yue, P. & Moult, J. Identification and analysis of deleterious human SNPs. J. Mol. Biol. 356, 1263-1274 (2006).
23. Yue, P., Li, Z. & Moult, J. Loss of protein structure stability as a major causative factor in monogenic disease. J. Mol. Biol. 353, 459-473 (2005).
24. Chang, Y.-F., Imam, J. S. & Wilkinson, M. F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76, 51-74 (2007).
25. Vogt, G. et al. Gain-of-glycosylation mutations. Curr. Opin. Genet. Dev. 17, 245-251 (2007).
26. Ng, P. C & Henikoff, S. Predicting the effect of amino acid substitutions on protein function. Annu. Rev. Genom. Human Genet. 7, 61-80 (2006).
27. Saunders, C. T. & Baker, D. Evaluation of structural and evolutionary contributions to deleterious mutation prediction. J. Mol. Biol. 322, 891-901 (2002).
28. Karchin, R. et al. LS-SNP: large-scale annotation of coding non-synonymous SNPs based on multiple information sources. Bioinformatics 21, 2814-2820 (2005).
29. Zvelebil, M. J., Barton, G. J., Taylor, W. R. & Sternberg, M. J. E. Prediction of protein secondary structure and active sites using the alignment of homologous sequences. J. Mol. Biol. 195, 957-961 (1987).
30. Poussu, E., Vihinen, M., Paulin, L. & Savilahti, H. Probing the α-complementing domain of E. coli β-galactosidase with use of an insertional pentapeptide mutagenesis strategy based on Mu in vitro DNA transposition. Proteins 54, 681-692 (2004).
31. Chen, R. Enzyme engineering: rational redesign versus directed evolution. Trends Biotechnol. 19, 13-14 (2001).
32. Getzoff, E. D. et al. Faster superoxide-dismutase mutants designed by enhancing electrostatic guidance. Nature 358, 347-351 (1992).
33. Xing, Y. & Lee, C. Alternative splicing and RNA selection pressure - evolutionary consequences for eukaryotic genomes. Nature Rev. Genet. 7, 499-509 (2006).
34. Black, D. L. Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 103, 367-370 (2000).
35. Johnson, J. M. et al. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302, 2141-2144 (2003).
36. Stamm, S. et al. Function of alternative splicing. Gene 344, 1-20 (2005). A nice Review of splice variants that are known to be associated with alternative functions.
37. Schmucker, D. et al. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101, 671-684 (2000).
38. Celetto, A. M. & Gravely, B. R. Alternative splicing of the Drosophila Dscam pre-mRNA is both temporally and spatially regulated. Genetics 159, 599-608 (2001).
39. Stetefeld, J. & Ruegg, M. A. Structural and functional diversity generated by alternative mRNA splicing. Trends Biochem. Sci. 30, 515-521 (2005).
40. Hymowitz, S. G. et al. The crystal structures of EDA-A1 and EDA-A2: splice variants with distinct receptor specificity. Structure 11, 1513-1520 (2003).
41. Walma, T. et al. A closed binding pocket and global destabilization modify the binding properties of an alternatively spliced form of the second PDZ domain of PTP-BL. Structure 12, 11-20 (2004).
42. 2A domain regulated by alternative splicing. Nature Struct. Mol. Biol. 11, 45-53 (2004).
43. Lewis, B. P., Green, R. E. & Brenner, S. E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl Acad. Sci. USA 100, 189-192 (2003).
44. Henikoff, S. et al. Gene families: the taxonomy of protein paralogs and chimeras. Science 278, 609-614 (1997).
45. Brodsky, G. et al. The human GARS-AIRS-GART gene encodes two proteins which are differentially expressed during human brain development and temporally overexpressed in cerebellum of individuals with Down syndrome. Hum. Mol. Genet. 6, 2043-2050 (1997).
46. Orban, T. I. & Olah, E. Emerging roles of BRCA1 alternative splicing. Mol. Pathol. 56, 191-197 (2003).
47. Kriventseva, E. V. et al. Increase of functional diversity by alternative splicing. Trends Genet. 19, 124-128 (2003).
48. Zavolan, M. & van Nimwegen, E. The types and prevalence of alternative splice forms. Curr. Opin. Struct. Biol. 16, 362-367 (2006).
49. Liu, M., Walch, H., Wu, S & Grigoriev, A. Significant expansion of exon-bordering protein domains during animal proteome evolution. Nucleic Acids Res. 33, 95-105 (2005). This paper demonstrates that protein domains with borders that coincide with exon borders seem to be more abundant than other domains, possibly as a result of exon shuffling and gene duplication.
50. Yura, K. et al. Alternative splicing in human transcriptome: functional and structural influence on proteins. Gene 380, 63-71 (2006).
51. Tress, M. L. et al. The implications of alternative splicing in the ENCODE protein complement. Proc. Natl Acad. Sci. USA 104, 5495-5500 (2007).
52. Romero, P. R. et al. Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc. Natl Acad. Sci. USA 103, 8390-8395 (2006).
53. Wang, P., Yan, B., Guo, J.-T., Hicks, C. & Xu, Y. Structural genomics analysis of alternative splicing and application to isoform structure modeling. Proc. Natl Acad. Sci. USA 102, 18920-18925 (2005).
54. Burlingame, R. W. et al. Crystallographic structure of the octameric histone core of the nucleosome at a resolution of 3.3Å. Science 228, 546-553 (1985).
55. Klug, A. et al. Crystallographic structure of the octamer histone core of the nucleosome. Science 229, 1109-1113 (1985).
56. Arents, G., Burlingame, R. W., Wang, B. C., Love, W. E. & Moudrianakis, E, N. The nucleosomal core histone octamer at 3.1 Å resolution: a tripartite protein assembly and a left-handed superhelix. Proc. Natl Acad. Sci. USA 88, 10148-10152 (1991).
57. Luger, K., Mäder, A. W., Richmond, R. K., Sargent D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 389, 251-260 (1997).
58. Luger, K. Structure and dynamic behaviour of nucleosomes. Curr. Opin. Genet. Dev. 13, 127-135 (2003).
59. Bhaumik, S. R., Smith, E. & Shilatifard, A. Covalent modifications of histones during development and disease pathogenesis. Nature Struct. Mol. Biol. 14, 1008-1016 (2007).
60. Turner, B. M. Cellular memory and the histone code. Cell 111, 285-291 (2002).
61. Taverna, S. D., Li, H., Ruthenburg, A. J., Allis, C. D. & Patel, D. J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nature Struct. Mol. Biol. 14, 1025-1040 (2007).
62. Latham, J. A. & Dent, S. Y. R. Cross-regulation of histone modifications. Nature Struct. Mol. Biol. 14, 1017-1024 (2007).
63. Rando, O. J. Global patterns of histone modifications. Curr. Opin. Genet. Dev. 17, 94-99 (2007).
64. Min, J., Zhang, Y. & Xu, R. M. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 17, 1823-1828 (2003).
65. Jacobs, S. A. & Khorasanizadeh, S. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295, 2080-2083 (2002).
66. Suto, R. K., Clarkson, M. J., Tremethick, D. J. & Luger, K. Crystal structure of a nucleosome core particle containing the variant histone H2A. Z. Nature Struct. Biol. 7, 1121-1124 (2000).
67. Couture, J.-F. & Trievel, R. C. Histone-modifying enzymes: encrypting an enigmatic epigenetic code. Curr. Opin. Struct. Biol. 16, 753-760 (2006).
68. Holbert, M. A. & Marmorstein, R. Structure and activity of enzymes that remove histone modifications. Curr. Opin. Struct. Biol. 15, 673-680 (2005).
69. Schalch, T., Duda, S., Sargent, D. F. & Richmond, T. J. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436, 138-141 (2005).
70. Groth, A., Rocha, W., Verreault, A. & Almouzni, G. Chromatin challenges during DNA replication and repair. Cell 128, 721-733 (2007).
71. Cairns, B. R. Chromatin remodeling: insights and intrigue from single-molecule studies. Nature Struct. Mol. Biol. 14, 989-996 (2007).
72. Greenbaum, J. A., Parker, S. C. J. & Tullius, T. D. Detection of DNA structural motifs in functional genomic elements. Genome Res. 17, 940-946 (2007).
73. Kornberg, R. D. & Lorch, Y. Chromatin rules. Nature Struct. Mol. Biol. 14, 986-988 (2007). An overview for a special edition of Nature Struct. Mol. Biol. (dated Nov 2007) devoted entirely to the structural organization and function of chromatin.
74. Luscombe, N. M., Austin, S. E., Berman, H. M. & Thornton, J. M. An overview of the structures of protein-DNA complexes. Genome Biol. 1, 1 (2000).
75. Matthews, B. W. Protein-DNA interaction. No code for recognition. Nature 335, 294-295 (1988).
76. Luscombe, N. M., Laskowski, R. A. & Thornton, J. M. Amino acid-base pair interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res. 29, 2860-2874 (2001).
77. Benos, P. V., Lapedes, A. S. & Stormo, G. D. Is there a code for protein-DNA recognition? Probab(ilistical)ly. BioEssays 24, 466-475 (2002).
78. Marmorstein, R. & Fitzgerald, M. X. Modulation of DNA-binding domains for sequence-specific DNA recognition. Gene 304, 1-12 (2003).
79. Ambros, V. The functions of animal microRNAs. Nature 431, 350-355 (2004).
80. MacRae, I. J. et al. Structural basis for double-stranded RNA processing by Dicer. Science 311, 195-198 (2006).
81. Serganov, A. & Patel, D. J. Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nature Rev. Genet. 8, 776-790 (2007).
82. Vitreschak, A. G., Rodionov, D. A., Mironov, A. A. & Gelfand, M. S. Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet. 20, 44-50 (2004).
83. Lanctôt, C., Cheutin, T., Cremer, M., Cavalli, G. & Cremer, T. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nature Rev. Genet. 8, 104-115 (2007).
84. Sexton, T., Schober, H., Fraser, P. & Gasser, S. M. Gene regulation through nuclear organization. Nature Struct. Mol. Biol. 14, 1049-1055 (2007).
85. Kulikova, T. et al. EMBL Nucleotide Sequence Database in 2006. Nucleic Acids Res. 35, D16-D20 (2007).
86. Brenner, S. E. A tour of structural genomics. Nature Rev. Genet. 2, 801-809 (2001).
87. Bateman, A. et al. The Pfam protein families database. Nucleic Acids Res. 32, D138-D141 (2004).
88. Chandonia, J. M. & Brenner, S. E. The impact of structural genomics: Expectations and outcomes. Science 311, 347-351 (2006).
89. Watson, J. D. et al. Towards fully automated structure-based function prediction in structural genomics: a case study. J. Mol. Biol. 367, 1511-22 (2007).
90. Bernstein, F. C. et al. The Protein Data Bank: a computer-based archival file of macromolecular structures. J. Mol. Biol. 112, 535-542 (1977).
91. Berman, H. M. et al. The Protein Data Bank. Nucleic Acids Res. 28, 235-242 (2000).
92. Berman, H. M., Henrick, K. & Nakamura, H. Announcing the worldwide Protein Data Bank. Nature Struct. Biol. 10, 980 (2003).
93. Laskowski, R. A., Chistyakov, V. V. & Thornton, J. M. PDBsum more: new summaries and analyses of the known 3D structures of proteins and nucleic acids. Nucleic Acids Res. 33, D266-D268 (2005).
94. Schwede, T., Kopp, J., Guex, N. & Peitsch, M. C. SWISS-MODEL: an automated protein-homology server. Nucleic Acids Res. 31, 3381-3385 (2003).
95. Pieper, U. et al. MODBASE: a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res. 32, D217-D222 (2004).
96. Dantzer, J, Moad, C. Heiland, R & Mooney S. MutDB services: interactive structural analysis of mutation data. Nucleic Acids Res. 33, W311-W314 (2005).
97. Berman, H. M. et al. The Nucleic Acid Database: a comprehensive relational database of three-dimensional structures of nucleic acids. Biophys. J. 63, 751-759 (1992).
98. Laskowski, R. A. in Structural Bioinformatics (eds Bourne, P. E. & Weissig, H.) 273-303 (John Wiley, New Jersey, 2003).
99. Kleywegt, G. J. & Jones, T. A. Phi-psi-chology: Ramachandran revisited. Structure 4, 1395-1400 (1996).
100. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007).
101. Rosenberg, J. M., Seeman, N. C., Kim, J. J. P., Suddath, F. L., Nicholas, H. B. & Rich, A. Double helix at atomic resolution. Nature 243, 150-154 (1973).
102. Day, R. O., Seeman, N. C., Rosenberg, J. M. & Rich, A. A crystalline fragment of the double helix: the structure of the dinucleoside phosphate guanylyl-3′, 5′-cytidine. Proc. Natl Acad. Sci. USA 70, 849-853 (1973). References 101 and 102 proved the Watson-Crick hydrogen-bonding hypothesis between complementary DNA bases.
103. Wing, R. et al. Crystal structure analysis of a complete turn of B-DNA. Nature 287, 755-758 (1980).
104. DeLano, W. L. The PyMOL Molecular Graphics System. (DeLano Scientific, San Carlos, USA, 2002).