Skip to main content
SpringerLink
Log in

Inferring and Using Protein Quaternary Structure Information from Crystallographic Data

  • Protocol
  • First Online:
Protein Complex Assembly

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1764))

Abstract

A precise knowledge of the quaternary structure of proteins is essential to illuminate both their function and their evolution. The major part of our knowledge on quaternary structure is inferred from X-ray crystallography data, but this inference process is hard and error-prone. The difficulty lies in discriminating fortuitous protein contacts, which make up the lattice of protein crystals, from biological protein contacts that exist in the native cellular environment. Here, we review methods devised to discriminate between both types of contacts and describe resources for downloading protein quaternary structure information and identifying high-confidence quaternary structures. The use of high-confidence datasets of quaternary structures will be critical for the analysis of structural, functional, and evolutionary properties of proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Turgay Y, Eibauer M, Goldman AE, Shimi T, Khayat M, Ben-Harush K, Dubrovsky-Gaupp A, Sapra KT, Goldman RD, Medalia O (2017) The molecular architecture of lamins in somatic cells. Nature 543(7644):261–264. https://doi.org/10.1038/nature21382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Levy ED, Teichmann S (2013) Structural, evolutionary, and assembly principles of protein oligomerization. Prog Mol Biol Transl Sci 117:25–51. https://doi.org/10.1016/B978-0-12-386931-9.00002-7

    Article  PubMed  CAS  Google Scholar 

  3. Marsh JA, Teichmann SA (2015) Structure, dynamics, assembly, and evolution of protein complexes. Annu Rev Biochem 84:551–575. https://doi.org/10.1146/annurev-biochem-060614-034142

    Article  PubMed  CAS  Google Scholar 

  4. Goodsell DS, Olson AJ (2000) Structural symmetry and protein function. Annu Rev Biophys Biomol Struct 29:105–153. https://doi.org/10.1146/annurev.biophys.29.1.105

    Article  PubMed  CAS  Google Scholar 

  5. Ali MH, Imperiali B (2005) Protein oligomerization: how and why. Bioorg Med Chem 13(17):5013–5020. https://doi.org/10.1016/j.bmc.2005.05.037

    Article  PubMed  CAS  Google Scholar 

  6. D’Alessio G (1999) Evolution of oligomeric proteins. The unusual case of a dimeric ribonuclease. Eur J Biochem 266(3):699–708

    Article  PubMed  Google Scholar 

  7. Pereira-Leal JB, Levy ED, Kamp C, Teichmann SA (2007) Evolution of protein complexes by duplication of homomeric interactions. Genome Biol 8(4):R51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ispolatov I, Yuryev A, Mazo I, Maslov S (2005) Binding properties and evolution of homodimers in protein-protein interaction networks. Nucleic Acids Res 33(11):3629–3635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Orlowski J, Kaczanowski S, Zielenkiewicz P (2007) Overrepresentation of interactions between homologous proteins in interactomes. FEBS Lett 581(1):52–56. https://doi.org/10.1016/j.febslet.2006.11.076

    Article  PubMed  CAS  Google Scholar 

  10. Levy ED, Pereira-Leal JB (2008) Evolution and dynamics of protein interactions and networks. Curr Opin Struct Biol 18(3):349–357. https://doi.org/10.1016/j.sbi.2008.03.003

    Article  PubMed  CAS  Google Scholar 

  11. Diss G, Gagnon-Arsenault I, Dion-Cote AM, Vignaud H, Ascencio DI, Berger CM, Landry CR (2017) Gene duplication can impart fragility, not robustness, in the yeast protein interaction network. Science 355(6325):630–634. https://doi.org/10.1126/science.aai7685

    Article  PubMed  CAS  Google Scholar 

  12. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, Andrews B, Tyers M, Boone C (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294(5550):2364–2368. https://doi.org/10.1126/science.1065810

    Article  PubMed  CAS  Google Scholar 

  13. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, Chan ET, Christie KR, Costanzo MC, Dwight SS, Engel SR, Fisk DG, Hirschman JE, Hitz BC, Karra K, Krieger CJ, Miyasato SR, Nash RS, Park J, Skrzypek MS, Simison M, Weng S, Wong ED (2012) Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res 40(Database issue):D700–D705. https://doi.org/10.1093/nar/gkr1029

    Article  PubMed  CAS  Google Scholar 

  14. Nooren IM, Thornton JM (2003) Diversity of protein-protein interactions. EMBO J 22(14):3486–3492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Griffin MD, Gerrard JA (2012) The relationship between oligomeric state and protein function. Adv Exp Med Biol 747:74–90. https://doi.org/10.1007/978-1-4614-3229-6_5

    Article  PubMed  CAS  Google Scholar 

  16. Matthews JM, Sunde M (2012) Dimers, oligomers, everywhere. Adv Exp Med Biol 747:1–18. https://doi.org/10.1007/978-1-4614-3229-6_1

    Article  PubMed  CAS  Google Scholar 

  17. Perica T, Marsh JA, Sousa FL, Natan E, Colwell LJ, Ahnert SE, Teichmann SA (2012) The emergence of protein complexes: quaternary structure, dynamics and allostery. Colworth Medal Lecture. Biochem Soc Trans 40(3):475–491. https://doi.org/10.1042/BST20120056

    Article  PubMed  CAS  Google Scholar 

  18. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88–118

    Article  CAS  PubMed  Google Scholar 

  19. Mattevi A, Valentini G, Rizzi M, Speranza ML, Bolognesi M, Coda A (1995) Crystal structure of Escherichia coli pyruvate kinase type I: molecular basis of the allosteric transition. Structure 3(7):729–741

    Article  CAS  PubMed  Google Scholar 

  20. Webb BA, Forouhar F, Szu FE, Seetharaman J, Tong L, Barber DL (2015) Structures of human phosphofructokinase-1 and atomic basis of cancer-associated mutations. Nature 523(7558):111–114. https://doi.org/10.1038/nature14405

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Ralser M, Heeren G, Breitenbach M, Lehrach H, Krobitsch S (2006) Triose phosphate isomerase deficiency is caused by altered dimerization—not catalytic inactivity—of the mutant enzymes. PLoS One 1:e30. https://doi.org/10.1371/journal.pone.0000030

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. White MF, Fothergill-Gilmore LA, Kelly SM, Price NC (1993) Dissociation of the tetrameric phosphoglycerate mutase from yeast by a mutation in the subunit contact region. Biochem J 295(Pt 3):743–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Mattevi A, Bolognesi M, Valentini G (1996) The allosteric regulation of pyruvate kinase. FEBS Lett 389(1):15–19

    Article  CAS  PubMed  Google Scholar 

  24. Marianayagam NJ, Sunde M, Matthews JM (2004) The power of two: protein dimerization in biology. Trends Biochem Sci 29(11):618–625. https://doi.org/10.1016/j.tibs.2004.09.006

    Article  PubMed  CAS  Google Scholar 

  25. Hashimoto K, Madej T, Bryant SH, Panchenko AR (2010) Functional states of homooligomers: insights from the evolution of glycosyltransferases. J Mol Biol 399(1):196–206. https://doi.org/10.1016/j.jmb.2010.03.059. S0022-2836(10)00334-7 [pii]

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Bergendahl LT, Marsh JA (2017) Functional determinants of protein assembly into homomeric complexes. Sci Rep 7(1):4932. https://doi.org/10.1038/s41598-017-05084-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Lemmon MA, Schlessinger J (1994) Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem Sci 19(11):459–463

    Article  CAS  PubMed  Google Scholar 

  28. Changeux JP, Edelstein SJ (2005) Allosteric mechanisms of signal transduction. Science 308(5727):1424–1428. https://doi.org/10.1126/science.1108595

    Article  PubMed  CAS  Google Scholar 

  29. Funnell AP, Crossley M (2012) Homo- and heterodimerization in transcriptional regulation. Adv Exp Med Biol 747:105–121.https://doi.org/10.1007/978-1-4614-3229-6_7

    Article  PubMed  CAS  Google Scholar 

  30. 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(25):14250–14255. https://doi.org/10.1073/pnas.231465798

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Chene P (2001) The role of tetramerization in p53 function. Oncogene 20(21):2611–2617. https://doi.org/10.1038/sj.onc.1204373

    Article  PubMed  CAS  Google Scholar 

  32. Chavez Zobel AT, Lambert H, Theriault JR, Landry J (2005) Structural instability caused by a mutation at a conserved arginine in the alpha-crystallin domain of Chinese hamster heat shock protein 27. Cell Stress Chaperones 10(2):157–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Heilmann M, Velanis CN, Cloix C, Smith BO, Christie JM, Jenkins GI (2016) Dimer/monomer status and in vivo function of salt-bridge mutants of the plant UV-B photoreceptor UVR8. Plant J 88(1):71–81. https://doi.org/10.1111/tpj.13260

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Perica T, Chothia C, Teichmann SA (2012) Evolution of oligomeric state through geometric coupling of protein interfaces. Proc Natl Acad Sci U S A 109(21):8127–8132. https://doi.org/10.1073/pnas.1120028109

    Article  PubMed  PubMed Central  Google Scholar 

  35. Perica T, Kondo Y, Tiwari SP, McLaughlin SH, Kemplen KR, Zhang X, Steward A, Reuter N, Clarke J, Teichmann SA (2014) Evolution of oligomeric state through allosteric pathways that mimic ligand binding. Science 346(6216):1254346. https://doi.org/10.1126/science.1254346

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Cohen-Khait R, Dym O, Hamer-Rogotner S, Schreiber G (2017) Promiscuous protein binding as a function of protein stability. Structure 25(12):1867–1874.e3. https://doi.org/10.1016/j.str.2017.11.002

    Article  PubMed  CAS  Google Scholar 

  37. Bershtein S, Mu W, Shakhnovich EI (2012) Soluble oligomerization provides a beneficial fitness effect on destabilizing mutations. Proc Natl Acad Sci U S A 109(13):4857–4862. https://doi.org/10.1073/pnas.1118157109

    Article  PubMed  PubMed Central  Google Scholar 

  38. Lynch M (2013) Evolutionary diversification of the multimeric states of proteins. Proc Natl Acad Sci U S A 110(30):E2821–E2828. https://doi.org/10.1073/pnas.1310980110

    Article  PubMed  PubMed Central  Google Scholar 

  39. Lukatsky DB, Zeldovich KB, Shakhnovich EI (2006) Statistically enhanced self-attraction of random patterns. Phys Rev Lett 97(17):178101. https://doi.org/10.1103/PhysRevLett.97.178101

    Article  PubMed  CAS  Google Scholar 

  40. Lukatsky DB, Shakhnovich BE, Mintseris J, Shakhnovich EI (2007) Structural similarity enhances interaction propensity of proteins. J Mol Biol 365(5):1596–1606

    Article  CAS  PubMed  Google Scholar 

  41. 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(42):16148–16152. https://doi.org/10.1073/pnas.0807576105

    Article  PubMed  PubMed Central  Google Scholar 

  42. Schulz GE (2010) The dominance of symmetry in the evolution of homo-oligomeric proteins. J Mol Biol 395(4):834–843. https://doi.org/10.1016/j.jmb.2009.10.044

    Article  PubMed  CAS  Google Scholar 

  43. Akiva E, Itzhaki Z, Margalit H (2008) Built-in loops allow versatility in domain-domain interactions: lessons from self-interacting domains. Proc Natl Acad Sci U S A 105(36):13292–13297. https://doi.org/10.1073/pnas.0801207105

    Article  PubMed  PubMed Central  Google Scholar 

  44. Hashimoto K, Panchenko AR (2010) Mechanisms of protein oligomerization, the critical role of insertions and deletions in maintaining different oligomeric states. Proc Natl Acad Sci U S A 107(47):20352–20357. https://doi.org/10.1073/pnas.1012999107

    Article  PubMed  PubMed Central  Google Scholar 

  45. Garcia-Seisdedos H, Empereur-Mot C, Elad N, Levy ED (2017) Proteins evolve on the edge of supramolecular self-assembly. Nature 548(7666):244–247. https://doi.org/10.1038/nature23320

    Article  PubMed  CAS  Google Scholar 

  46. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28(1):235–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Velankar S, van Ginkel G, Alhroub Y, Battle GM, Berrisford JM, Conroy MJ, Dana JM, Gore SP, Gutmanas A, Haslam P, Hendrickx PM, Lagerstedt I, Mir S, Fernandez Montecelo MA, Mukhopadhyay A, Oldfield TJ, Patwardhan A, Sanz-Garcia E, Sen S, Slowley RA, Wainwright ME, Deshpande MS, Iudin A, Sahni G, Salavert Torres J, Hirshberg M, Mak L, Nadzirin N, Armstrong DR, Clark AR, Smart OS, Korir PK, Kleywegt GJ (2016) PDBe: improved accessibility of macromolecular structure data from PDB and EMDB. Nucleic Acids Res 44(D1):D385–D395. https://doi.org/10.1093/nar/gkv1047

    Article  PubMed  CAS  Google Scholar 

  48. Zhang H, Kurisu G, Smith JL, Cramer WA (2003) A defined protein-detergent-lipid complex for crystallization of integral membrane proteins: the cytochrome b6f complex of oxygenic photosynthesis. Proc Natl Acad Sci U S A 100(9):5160–5163. https://doi.org/10.1073/pnas.0931431100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Janin J (1997) Specific versus non-specific contacts in protein crystals. Nat Struct Biol 4(12):973–974

    Article  CAS  PubMed  Google Scholar 

  50. Henrick K, Thornton JM (1998) PQS: a protein quaternary structure file server. Trends Biochem Sci 23(9):358–361

    Article  CAS  PubMed  Google Scholar 

  51. Chakrabarti P, Janin J (2002) Dissecting protein-protein recognition sites. Proteins 47(3):334–343

    Article  CAS  PubMed  Google Scholar 

  52. Levy ED (2010) A simple definition of structural regions in proteins and its use in analyzing interface evolution. J Mol Biol 403(4):660–670. S0022-2836(10)01016-8[pii]. https://doi.org/10.1016/j.jmb.2010.09.028

    Article  PubMed  CAS  Google Scholar 

  53. Scharer MA, Grutter MG, Capitani G (2010) CRK: an evolutionary approach for distinguishing biologically relevant interfaces from crystal contacts. Proteins 78(12):2707–2713. https://doi.org/10.1002/prot.22787

    Article  PubMed  CAS  Google Scholar 

  54. Duarte JM, Srebniak A, Scharer MA, Capitani G (2012) Protein interface classification by evolutionary analysis. BMC Bioinformatics 13:334. https://doi.org/10.1186/1471-2105-13-334

    Article  PubMed  PubMed Central  Google Scholar 

  55. Lee B, Richards FM (1971) The interpretation of protein structures: estimation of static accessibility. J Mol Biol 55(3):379–400

    Article  CAS  PubMed  Google Scholar 

  56. Chothia C, Janin J (1975) Principles of protein-protein recognition. Nature 256(5520):705–708

    Article  CAS  PubMed  Google Scholar 

  57. Georgy F (1907) Voronoi. Nouvelles applications des parametres continusa la théorie des formes quadratiques premier mémoire: sûr quelques propriétés des formes quadratiques positives parfaits. Journal für die reine und angewandte Mathematik 133:97–178

    Google Scholar 

  58. Poupon A (2004) Voronoi and Voronoi-related tessellations in studies of protein structure and interaction. Curr Opin Struct Biol 14(2):233–241. https://doi.org/10.1016/j.sbi.2004.03.010

    Article  PubMed  CAS  Google Scholar 

  59. Cazals F, Proust F, Bahadur RP, Janin J (2006) Revisiting the Voronoi description of protein-protein interfaces. Protein Sci 15(9):2082–2092. https://doi.org/10.1110/ps.062245906

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Bernauer J, Bahadur RP, Rodier F, Janin J, Poupon A (2008) DiMoVo: a Voronoi tessellation-based method for discriminating crystallographic and biological protein-protein interactions. Bioinformatics (Oxford, England) 24(5):652–658. https://doi.org/10.1093/bioinformatics/btn022

    Article  CAS  Google Scholar 

  61. Miller S, Lesk AM, Janin J, Chothia C (1987) The accessible surface area and stability of oligomeric proteins. Nature 328(6133):834–836. https://doi.org/10.1038/328834a0

    Article  PubMed  CAS  Google Scholar 

  62. Jones S, Thornton JM (1995) Protein-protein interactions: a review of protein dimer structures. Prog Biophys Mol Biol 63(1):31–65

    Article  CAS  PubMed  Google Scholar 

  63. Bahadur RP, Chakrabarti P, Rodier F, Janin J (2004) A dissection of specific and non-specific protein-protein interfaces. J Mol Biol 336(4):943–955

    Article  CAS  PubMed  Google Scholar 

  64. Janin J, Bahadur RP, Chakrabarti P (2008) Protein-protein interaction and quaternary structure. Q Rev Biophys 41(2):133–180. S0033583508004708 [pii]. https://doi.org/10.1017/S0033583508004708

    Article  PubMed  CAS  Google Scholar 

  65. Tsuchiya Y, Nakamura H, Kinoshita K (2008) Discrimination between biological interfaces and crystal-packing contacts. Adv Appl Bioinform Chem 1:99–113

    PubMed  PubMed Central  CAS  Google Scholar 

  66. Zhu H, Domingues FS, Sommer I, Lengauer T (2006) NOXclass: prediction of protein-protein interaction types. BMC Bioinformatics 7:27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Pal A, Chakrabarti P, Bahadur R, Rodier F, Janin J (2007) Peptide segments in protein-protein interfaces. J Biosci 32(1):101–111

    Article  CAS  PubMed  Google Scholar 

  68. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774–797

    Article  CAS  PubMed  Google Scholar 

  69. Liu Q, Li Z, Li J (2014) Use B-factor related features for accurate classification between protein binding interfaces and crystal packing contacts. BMC Bioinformatics 15(Suppl 16):S3. https://doi.org/10.1186/1471-2105-15-S16-S3

    Article  PubMed  PubMed Central  Google Scholar 

  70. Ponstingl H, Kabir T, Thornton JM (2003) Automatic inference of protein quaternary structure from crystals. J Appl Cryst 36(5):1116–1122

    Article  CAS  Google Scholar 

  71. Levy ED (2007) PiQSi: protein quaternary structure investigation. Structure 15(11):4

    Article  CAS  Google Scholar 

  72. Bahadur RP, Chakrabarti P, Rodier F, Janin J (2003) Dissecting subunit interfaces in homodimeric proteins. Proteins 53(3):708–719

    Article  CAS  PubMed  Google Scholar 

  73. Ponstingl H, Henrick K, Thornton JM (2000) Discriminating between homodimeric and monomeric proteins in the crystalline state. Proteins 41(1):47–57

    Article  CAS  PubMed  Google Scholar 

  74. Mitra P, Pal D (2011) Combining Bayes classification and point group symmetry under Boolean framework for enhanced protein quaternary structure inference. Structure 19(3):304–312. https://doi.org/10.1016/j.str.2011.01.009

    Article  PubMed  CAS  Google Scholar 

  75. Hwang H, Pierce B, Mintseris J, Janin J, Weng Z (2008) Protein-protein docking benchmark version 3.0. Proteins 73(3):705–709. https://doi.org/10.1002/prot.22106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Xu Q, Dunbrack RL Jr (2011) The protein common interface database (ProtCID)—a comprehensive database of interactions of homologous proteins in multiple crystal forms. Nucleic Acids Res 39(Database issue):D761–D770. https://doi.org/10.1093/nar/gkq1059

    Article  PubMed  CAS  Google Scholar 

  77. Bliven S, Lafita A, Parker A, Capitani G, Duarte JM (2017) Automated evaluation of quaternary structures from protein crystals. Acta Cryst Sec A A73:a117. https://doi.org/10.1101/224717

    Article  Google Scholar 

  78. Da Silva F, Desaphy J, Bret G, Rognan D (2015) IChemPIC: a random forest classifier of biological and crystallographic protein-protein interfaces. J Chem Inf Model 55(9):2005–2014. https://doi.org/10.1021/acs.jcim.5b00190

    Article  PubMed  CAS  Google Scholar 

  79. ENCODE Project Consortium, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SC, Sabo PJ, Sandstrom R, Shafer A, Vetrie D, Weaver M, Wilcox S, Yu M, Collins FS, Dekker J, Lieb JD, Tullius TD, Crawford GE, Sunyaev S, Noble WS, Dunham I, Denoeud F, Reymond A, Kapranov P, Rozowsky J, Zheng D, Castelo R, Frankish A, Harrow J, Ghosh S, Sandelin A, Hofacker IL, Baertsch R, Keefe D, Dike S, Cheng J, Hirsch HA, Sekinger EA, Lagarde J, Abril JF, Shahab A, Flamm C, Fried C, Hackermuller J, Hertel J, Lindemeyer M, Missal K, Tanzer A, Washietl S, Korbel J, Emanuelsson O, Pedersen JS, Holroyd N, Taylor R, Swarbreck D, Matthews N, Dickson MC, Thomas DJ, Weirauch MT, Gilbert J, Drenkow J, Bell I, Zhao X, Srinivasan KG, Sung WK, Ooi HS, Chiu KP, Foissac S, Alioto T, Brent M, Pachter L, Tress ML, Valencia A, Choo SW, Choo CY, Ucla C, Manzano C, Wyss C, Cheung E, Clark TG, Brown JB, Ganesh M, Patel S, Tammana H, Chrast J, Henrichsen CN, Kai C, Kawai J, Nagalakshmi U, Wu J, Lian Z, Lian J, Newburger P, Zhang X, Bickel P, Mattick JS, Carninci P, Hayashizaki Y, Weissman S, Hubbard T, Myers RM, Rogers J, Stadler PF, Lowe TM, Wei CL, Ruan Y, Struhl K, Gerstein M, Antonarakis SE, Fu Y, Green ED, Karaoz U, Siepel A, Taylor J, Liefer LA, Wetterstrand KA, Good PJ, Feingold EA, Guyer MS, Cooper GM, Asimenos G, Dewey CN, Hou M, Nikolaev S, Montoya-Burgos JI, Loytynoja A, Whelan S, Pardi F, Massingham T, Huang H, Zhang NR, Holmes I, Mullikin JC, Ureta-Vidal A, Paten B, Seringhaus M, Church D, Rosenbloom K, Kent WJ, Stone EA, NISC Comparative Sequencing Program; Baylor College of Medicine Human Genome Sequencing Center; Washington University Genome Sequencing Center; Broad Institute; Children’s Hospital Oakland Research Institute, Batzoglou S, Goldman N, Hardison RC, Haussler D, Miller W, Sidow A, Trinklein ND, Zhang ZD, Barrera L, Stuart R, King DC, Ameur A, Enroth S, Bieda MC, Kim J, Bhinge AA, Jiang N, Liu J, Yao F, Vega VB, Lee CW, Ng P, Shahab A, Yang A, Moqtaderi Z, Zhu Z, Xu X, Squazzo S, Oberley MJ, Inman D, Singer MA, Richmond TA, Munn KJ, Rada-Iglesias A, Wallerman O, Komorowski J, Fowler JC, Couttet P, Bruce AW, Dovey OM, Ellis PD, Langford CF, Nix DA, Euskirchen G, Hartman S, Urban AE, Kraus P, Van Calcar S, Heintzman N, Kim TH, Wang K, Qu C, Hon G, Luna R, Glass CK, Rosenfeld MG, Aldred SF, Cooper SJ, Halees A, Lin JM, Shulha HP, Zhang X, Xu M, Haidar JN, Yu Y, Ruan Y, Iyer VR, Green RD, Wadelius C, Farnham PJ, Ren B, Harte RA, Hinrichs AS, Trumbower H, Clawson H, Hillman-Jackson J, Zweig AS, Smith K, Thakkapallayil A, Barber G, Kuhn RM, Karolchik D, Armengol L, Bird CP, de Bakker PI, Kern AD, Lopez-Bigas N, Martin JD, Stranger BE, Woodroffe A, Davydov E, Dimas A, Eyras E, Hallgrimsdottir IB, Huppert J, Zody MC, Abecasis GR, Estivill X, Bouffard GG, Guan X, Hansen NF, Idol JR, Maduro VV, Maskeri B, McDowell JC, Park M, Thomas PJ, Young AC, Blakesley RW, Muzny DM, Sodergren E, Wheeler DA, Worley KC, Jiang H, Weinstock GM, Gibbs RA, Graves T, Fulton R, Mardis ER, Wilson RK, Clamp M, Cuff J, Gnerre S, Jaffe DB, Chang JL, Lindblad-Toh K, Lander ES, Koriabine M, Nefedov M, Osoegawa K, Yoshinaga Y, Zhu B, de Jong PJ (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447(7146):799–816. https://doi.org/10.1038/nature05874

    Article  CAS  Google Scholar 

  80. Beltrao P, Albanese V, Kenner LR, Swaney DL, Burlingame A, Villen J, Lim WA, Fraser JS, Frydman J, Krogan NJ (2012) Systematic functional prioritization of protein posttranslational modifications. Cell 150(2):413–425. https://doi.org/10.1016/j.cell.2012.05.036

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Valdar WS, Thornton JM (2001) Protein-protein interfaces: analysis of amino acid conservation in homodimers. Proteins 42(1):108–124

    Article  CAS  PubMed  Google Scholar 

  82. Caffrey DR, Somaroo S, Hughes JD, Mintseris J, Huang ES (2004) Are protein-protein interfaces more conserved in sequence than the rest of the protein surface? Protein Sci 13(1):190–202. https://doi.org/10.1110/ps.03323604

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Franzosa EA, Xia Y (2009) Structural determinants of protein evolution are context-sensitive at the residue level. Mol Biol Evol 26(10):2387–2395. https://doi.org/10.1093/molbev/msp146

    Article  PubMed  CAS  Google Scholar 

  84. Elcock AH, McCammon JA (2001) Identification of protein oligomerization states by analysis of interface conservation. Proc Natl Acad Sci U S A 98(6):2990–2994. https://doi.org/10.1073/pnas.061411798

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Guharoy M, Chakrabarti P (2005) Conservation and relative importance of residues across protein-protein interfaces. Proc Natl Acad Sci U S A 102(43):15447–15452. https://doi.org/10.1073/pnas.0505425102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. 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(Web Server issue):W529–W533. https://doi.org/10.1093/nar/gkq399

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Baskaran K, Duarte JM, Biyani N, Bliven S, Capitani G (2014) A PDB-wide, evolution-based assessment of protein-protein interfaces. BMC Struct Biol 14:22. https://doi.org/10.1186/s12900-014-0022-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Aloy P, Ceulemans H, Stark A, Russell RB (2003) The relationship between sequence and interaction divergence in proteins. J Mol Biol 332(5):989–998

    Article  CAS  PubMed  Google Scholar 

  89. Winter C, Henschel A, Kim WK, Schroeder M (2006) SCOPPI: a structural classification of protein-protein interfaces. Nucleic Acids Res 34(Database issue):D310–D314. https://doi.org/10.1093/nar/gkj099

    Article  PubMed  CAS  Google Scholar 

  90. Stein A, Ceol A, Aloy P (2011) 3did: identification and classification of domain-based interactions of known three-dimensional structure. Nucleic Acids Res 39(Database issue):D718–D723. https://doi.org/10.1093/nar/gkq962

    Article  PubMed  CAS  Google Scholar 

  91. Xu Q, Canutescu AA, Wang G, Shapovalov M, Obradovic Z, Dunbrack RL Jr (2008) Statistical analysis of interface similarity in crystals of homologous proteins. J Mol Biol 381(2):487–507. https://doi.org/10.1016/j.jmb.2008.06.002

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Faure G, Andreani J, Guerois R (2012) InterEvol database: exploring the structure and evolution of protein complex interfaces. Nucleic Acids Res 40(Database issue):D847–D856. https://doi.org/10.1093/nar/gkr845

    Article  PubMed  CAS  Google Scholar 

  93. Berman HM (2008) The Protein Data Bank: a historical perspective. Acta Crystallogr A 64(Pt 1):88–95. https://doi.org/10.1107/S0108767307035623

    Article  PubMed  CAS  Google Scholar 

  94. Velankar S, McNeil P, Mittard-Runte V, Suarez A, Barrell D, Apweiler R, Henrick K (2005) E-MSD: an integrated data resource for bioinformatics. Nucleic Acids Res 33(Database issue):D262–D265. https://doi.org/10.1093/nar/gki058

    Article  PubMed  CAS  Google Scholar 

  95. Berman H, Henrick K, Nakamura H (2003) Announcing the worldwide Protein Data Bank. Nat Struct Biol 10(12):980. https://doi.org/10.1038/nsb1203-980

    Article  PubMed  CAS  Google Scholar 

  96. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67(Pt 4):235–242. https://doi.org/10.1107/S0907444910045749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Levy ED, Pereira-Leal JB, Chothia C, Teichmann SA (2006) 3D complex: a structural classification of protein complexes. PLoS Comput Biol 2(11):e155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Dey S, Ritchie DW, Levy ED (2018) PDB-wide identification of biological assemblies from conserved quaternary structure geometry. Nat Methods 15(1):67–72. https://doi.org/10.1038/nmeth.4510

    Article  PubMed  CAS  Google Scholar 

  99. Ritchie DW, Ghoorah AW, Mavridis L, Venkatraman V (2012) Fast protein structure alignment using Gaussian overlap scoring of backbone peptide fragment similarity. Bioinformatics (Oxford, England) 28(24):3274–3281. https://doi.org/10.1093/bioinformatics/bts618

    Article  CAS  Google Scholar 

  100. Dessailly BH, Nair R, Jaroszewski L, Fajardo JE, Kouranov A, Lee D, Fiser A, Godzik A, Rost B, Orengo C (2009) PSI-2: structural genomics to cover protein domain family space. Structure 17(6):869–881. https://doi.org/10.1016/j.str.2009.03.015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Mosca R, Ceol A, Aloy P (2013) Interactome3D: adding structural details to protein networks. Nat Methods 10(1):47–53. https://doi.org/10.1038/nmeth.2289

    Article  PubMed  CAS  Google Scholar 

  102. Khafizov K, Madrid-Aliste C, Almo SC, Fiser A (2014) Trends in structural coverage of the protein universe and the impact of the Protein Structure Initiative. Proc Natl Acad Sci U S A 111(10):3733–3738. https://doi.org/10.1073/pnas.1321614111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ohad Medalia for providing the lamina meshwork image in Fig. 1 and William Cramer for providing the crystal photography in Fig. 2. We thank the PDBe team and in particular Sameer Velankar for the integration of QSbio into PDBe assembly pages. This work was supported by a VATAT fellowship to S. Dey, by the Israel Science Foundation and the I-CORE Program of the Planning and Budgeting Committee (grant nos. 1775/12 and 2179/14), by the Marie Curie CIG Program (project no. 711715), by the HFSP Career Development Award to E. D. Levy (award no. CDA00077/2015), and by a research grant from AM. Boucher. E.D. Levy is incumbent of the Recanati Career Development Chair of Cancer Research.

Author information

Authors and Affiliations

  1. Department of Structural Biology, Weizmann Institute of Science, Rehovot, Israel

    Sucharita Dey & Emmanuel D. Levy

Authors
  1. Sucharita Dey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emmanuel D. Levy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emmanuel D. Levy .

Editor information

Editors and Affiliations

  1. MRC Human Genetics Unit, Institute of Genetics & Molecular Medicine, University of Edinburgh, Edinburgh, United Kingdom

    Joseph A. Marsh

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Dey, S., Levy, E.D. (2018). Inferring and Using Protein Quaternary Structure Information from Crystallographic Data. In: Marsh, J. (eds) Protein Complex Assembly. Methods in Molecular Biology, vol 1764. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7759-8_23

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-7759-8_23

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-7758-1

  • Online ISBN: 978-1-4939-7759-8

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation