Extent of structural asymmetry in homodimeric proteins: Prevalence and relevance

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Swapna, Lakshmipuram Seshadri ^a   Srikeerthana, Kuchi ^a,b   Srinivasan, Narayanaswamy ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HOMODIMER PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; DEPOLYMERIZATION; DIMERIZATION; GENETIC CONSERVATION; LIGAND BINDING; MACROMOLECULE; PROTEIN BINDING; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

DIMERIZATION; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEINS;

EID: 84861324339     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036688     Document Type: Article

References (77)

1. Goodsell DS, Olson AJ, (2000) Structural symmetry and protein function. Annu Rev Biophys Biomol Struct 29: 105-153.
2. Soding J, Lupas AN, (2003) More than the sum of their parts: on the evolution of proteins from peptides. Bioessays 25: 837-846.
3. Dobson CM, (2003) Protein folding and misfolding. Nature 426: 884-890.
4. Hayouka Z, Rosenbluh J, Levin A, Loya S, Lebendiker M, et al. (2007) Inhibiting HIV-1 integrase by shifting its oligomerization equilibrium. Proc Natl Acad Sci U S A 104: 8316-8321.
5. Wright CF, Teichmann SA, Clarke J, Dobson CM, (2005) The importance of sequence diversity in the aggregation and evolution of proteins. Nature 438: 878-881.
6. Blundell TL, Srinivasan N, (1996) Symmetry, stability, and dynamics of multidomain and multicomponent protein systems. Proc Natl Acad Sci U S A 93: 14243-14248.
7. Lukatsky DB, Shakhnovich BE, Mintseris J, Shakhnovich EI, (2007) Structural similarity enhances interaction propensity of proteins. J Mol Biol 365: 1596-1606.
8. Lukatsky DB, Zeldovich KB, Shakhnovich EI, (2006) Statistically enhanced self-attraction of random patterns. Phys Rev Lett 97: 178101.
9. Andre I, Strauss CE, Kaplan DB, Bradley P, Baker D, (2008) Emergence of symmetry in homooligomeric biological assemblies. Proc Natl Acad Sci U S A 105: 16148-16152.
10. Levy ED, Pereira-Leal JB, Chothia C, Teichmann SA, (2006) 3D complex: a structural classification of protein complexes. PLoS Comput Biol 2: e155.
11. Ispolatov I, Yuryev A, Mazo I, Maslov S, (2005) Binding properties and evolution of homodimers in protein-protein interaction networks. Nucleic Acids Res 33: 3629-3635.
12. Levy ED, Boeri Erba E, Robinson CV, Teichmann SA, (2008) Assembly reflects evolution of protein complexes. Nature 453: 1262-1265.
13. Dayhoff JE, Shoemaker BA, Bryant SH, Panchenko AR, (2010) Evolution of protein binding modes in homooligomers. J Mol Biol 395: 860-870.
14. Levy ED, (2007) PiQSi: protein quaternary structure investigation. Structure 15: 1364-1367.
15. Abraham AL, Pothier J, Rocha EP, (2009) Alternative to homo-oligomerisation: the creation of local symmetry in proteins by internal amplification. J Mol Biol 394: 522-534.
16. Pereira-Leal JB, Levy ED, Kamp C, Teichmann SA, (2007) Evolution of protein complexes by duplication of homomeric interactions. Genome Biol 8: R51.
17. Marianayagam NJ, Sunde M, Matthews JM, (2004) The power of two: protein dimerization in biology. Trends Biochem Sci 29: 618-625.
18. Holm L, Sander C, (1993) Protein structure comparison by alignment of distance matrices. Journal of molecular biology 233: 123-138.
19. Pednekar D, Durani S, (2010) Protein homomers in point-group assembly: symmetry making and breaking are specific and distinctive in their codes of chemical alphabet in side chains. Proteins 78: 3048-3055.
20. Vende P, Piron M, Castagne N, Poncet D, (2000) Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3′ end. J Virol 74: 7064-7071.
21. Deo RC, Groft CM, Rajashankar KR, Burley SK, (2002) Recognition of the rotavirus mRNA 3′ consensus by an asymmetric NSP3 homodimer. Cell 108: 71-81.
22. Piron M, Delaunay T, Grosclaude J, Poncet D, (1999) Identification of the RNA-binding, dimerization, and eIF4GI-binding domains of rotavirus nonstructural protein NSP3. J Virol 73: 5411-5421.
23. Jiang J, Ballinger CA, Wu Y, Dai Q, Cyr DM, et al. (2001) CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J Biol Chem 276: 42938-42944.
24. Murata S, Minami Y, Minami M, Chiba T, Tanaka K, (2001) CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2: 1133-1138.
25. Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, et al. (1999) Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 19: 4535-4545.
26. Nikolay R, Wiederkehr T, Rist W, Kramer G, Mayer MP, et al. (2004) Dimerization of the human E3 ligase CHIP via a coiled-coil domain is essential for its activity. J Biol Chem 279: 2673-2678.
27. Nagradova NK, (2001) Interdomain interactions in oligomeric enzymes: creation of asymmetry in homo-oligomers and role in metabolite channeling between active centers of hetero-oligomers. FEBS Lett 487: 327-332.
28. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, et al. (2005) Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 20: 525-538.
29. Lei M, Lu W, Meng W, Parrini MC, Eck MJ, et al. (2000) Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 102: 387-397.
30. Erickson HP, (1997) FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol 7: 362-367.
31. Leung AK, Lucile White E, Ross LJ, Reynolds RC, DeVito JA, et al. (2004) Structure of Mycobacterium tuberculosis FtsZ reveals unexpected, G protein-like conformational switches. J Mol Biol 342: 953-970.
32. Stricker J, Erickson HP, (2003) In vivo characterization of Escherichia coli ftsZ mutants: effects on Z-ring structure and function. J Bacteriol 185: 4796-4805.
33. Etienne-Manneville S, (2010) From signaling pathways to microtubule dynamics: the key players. Curr Opin Cell Biol 22: 104-111.
34. Lowe J, Li H, Downing KH, Nogales E, (2001) Refined structure of alpha beta-tubulin at 3.5 A resolution. J Mol Biol 313: 1045-1057.
35. Zhao Q, Khorasanizadeh S, Miyoshi Y, Lazar MA, Rastinejad F, (1998) Structural elements of an orphan nuclear receptor-DNA complex. Mol Cell 1: 849-861.
36. Perlmann T, Rangarajan PN, Umesono K, Evans RM, (1993) Determinants for selective RAR and TR recognition of direct repeat HREs. Genes Dev 7: 1411-1422.
37. Bouillon R, Okamura WH, Norman AW, (1995) Structure-function relationships in the vitamin D endocrine system. Endocr Rev 16: 200-257.
38. DeLuca HF, Zierold C, (1998) Mechanisms and functions of vitamin D. Nutr Rev 56: S4-10; discussion S 54-75.
39. Shaffer PL, Gewirth DT, (2002) Structural basis of VDR-DNA interactions on direct repeat response elements. Embo J 21: 2242-2252.
40. Zitomer RS, Sellers JW, McCarter DW, Hastings GA, Wick P, et al. (1987) Elements involved in oxygen regulation of the Saccharomyces cerevisiae CYC7 gene. Mol Cell Biol 7: 2212-2220.
41. Winkler H, Adam G, Mattes E, Schanz M, Hartig A, et al. (1988) Co-ordinate control of synthesis of mitochondrial and non-mitochondrial hemoproteins: a binding site for the HAP1 (CYP1) protein in the UAS region of the yeast catalase T gene (CTT1). Embo J 7: 1799-1804.
42. Lodi T, Guiard B, (1991) Complex transcriptional regulation of the Saccharomyces cerevisiae CYB2 gene encoding cytochrome b2: CYP1(HAP1) activator binds to the CYB2 upstream activation site UAS1-B2. Mol Cell Biol 11: 3762-3772.
43. Zhang L, Guarente L, (1996) The C6 zinc cluster dictates asymmetric binding by HAP1. Embo J 15: 4676-4681.
44. King DA, Zhang L, Guarente L, Marmorstein R, (1999) Structure of a HAP1-DNA complex reveals dramatically asymmetric DNA binding by a homodimeric protein. Nat Struct Biol 6: 64-71.
45. Ha N, Hellauer K, Turcotte B, (1996) Mutations in target DNA elements of yeast HAP1 modulate its transcriptional activity without affecting DNA binding. Nucleic Acids Res 24: 1453-1459.
46. Marmorstein R, Harrison SC, (1994) Crystal structure of a PPR1-DNA complex: DNA recognition by proteins containing a Zn2Cys6 binuclear cluster. Genes Dev 8: 2504-2512.
47. Swaminathan K, Flynn P, Reece RJ, Marmorstein R, (1997) Crystal structure of a PUT3-DNA complex reveals a novel mechanism for DNA recognition by a protein containing a Zn2Cys6 binuclear cluster. Nat Struct Biol 4: 751-759.
48. Marmorstein R, Carey M, Ptashne M, Harrison SC, (1992) DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356: 408-414.
49. Khare SD, Dokholyan NV, (2007) Molecular mechanisms of polypeptide aggregation in human diseases. Curr Protein Pept Sci 8: 573-579.
50. Wang HW, Nogales E, (2005) Nucleotide-dependent bending flexibility of tubulin regulates microtubule assembly. Nature 435: 911-915.
51. Lee SH, Dominguez R, (2010) Regulation of actin cytoskeleton dynamics in cells. Mol Cells 29: 311-325.
52. Birck C, Chen Y, Hulett FM, Samama JP, (2003) The crystal structure of the phosphorylation domain in PhoP reveals a functional tandem association mediated by an asymmetric interface. J Bacteriol 185: 254-261.
53. Zhao H, Msadek T, Zapf J, Madhusudan, Hoch JA, et al. (2002) DNA complexed structure of the key transcription factor initiating development in sporulating bacteria. Structure 10: 1041-1050.
54. Kanellopoulos PN, Tsernoglou D, van der Vliet PC, Tucker PA, (1996) Alternative arrangements of the protein chain are possible for the adenovirus single-stranded DNA binding protein. J Mol Biol 257: 1-8.
55. Tucker PA, Tsernoglou D, Tucker AD, Coenjaerts FE, Leenders H, et al. (1994) Crystal structure of the adenovirus DNA binding protein reveals a hook-on model for cooperative DNA binding. Embo J 13: 2994-3002.
56. Brown JH, (2010) How sequence directs bending in tropomyosin and other two-stranded alpha-helical coiled coils. Protein Sci 19: 1366-1375.
57. Renatus M, Stennicke HR, Scott FL, Liddington RC, Salvesen GS, (2001) Dimer formation drives the activation of the cell death protease caspase 9. Proc Natl Acad Sci U S A 98: 14250-14255.
58. Brown JH, Kim KH, Jun G, Greenfield NJ, Dominguez R, et al. (2001) Deciphering the design of the tropomyosin molecule. Proc Natl Acad Sci U S A 98: 8496-8501.
59. Madrazo J, Brown JH, Litvinovich S, Dominguez R, Yakovlev S, et al. (2001) Crystal structure of the central region of bovine fibrinogen (E5 fragment) at 1.4-A resolution. Proc Natl Acad Sci U S A 98: 11967-11972.
60. Brown JH, (2006) Breaking symmetry in protein dimers: designs and functions. Protein Sci 15: 1-13.
61. Harrison CJ, Hayer-Hartl M, Di Liberto M, Hartl F, Kuriyan J, (1997) Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276: 431-435.
62. Hu L, Benson ML, Smith RD, Lerner MG, Carlson HA, (2005) Binding MOAD (Mother Of All Databases). Proteins 60: 333-340.
63. Benson ML, Smith RD, Khazanov NA, Dimcheff B, Beaver J, et al. (2008) Binding MOAD, a high-quality protein-ligand database. Nucleic Acids Res 36: D674-678.
64. Murzin AG, Brenner SE, Hubbard T, Chothia C, (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247: 536-540.
65. Henrick K, Feng Z, Bluhm WF, Dimitropoulos D, Doreleijers JF, et al. (2008) Remediation of the protein data bank archive. Nucleic Acids Res 36: D426-433.
66. Keskin O, Tsai CJ, Wolfson H, Nussinov R, (2004) A new, structurally nonredundant, diverse data set of protein-protein interfaces and its implications. Protein Sci 13: 1043-1055.
67. Chothia C, (1975) Structural invariants in protein folding. Nature 254: 304-308.
68. Lee B, Richards FM, (1971) The interpretation of protein structures: estimation of static accessibility. J Mol Biol 55: 379-400.
69. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
70. Mayrose I, Graur D, Ben-Tal N, Pupko T, (2004) Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior. Mol Biol Evol 21: 1781-1791.
71. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38 (Suppl): W529-533.
72. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
73. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH, (2007) UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23: 1282-1288.
74. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
75. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, et al. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33: W299-302.
76. Yuan Z, Zhao J, Wang ZX, (2003) Flexibility analysis of enzyme active sites by crystallographic temperature factors. Protein Eng 16: 109-114.
77. Delano WL, (2002) The PyMoL Molecular Graphics System San Carlos, CA, USA DeLano Scientific.