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Secondary and Supersecondary Structure of Proteins in Light of the Structure of Hydrophobic Cores

  • Mateusz Banach
  • Leszek Konieczny
  • Irena RotermanEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1958)

Abstract

The traditional classification of protein structures (with regard to their supersecondary and tertiary conformation) is based on an assessment of conformational similarities between various polypeptide chains and particularly on the presence of specific secondary structural motifs. Mutual relations between secondary folds determine the overall shape of the protein and may be used to assign proteins to specific families (such as the immunoglobulin-like family). An alternative means of conducting structural assessment focuses on the structure of the protein’s hydrophobic core. In this case, the protein is treated as a quasi-micelle, which exposes hydrophilic residues on its surface while internalizing hydrophobic residues. The accordance between the actual distribution of hydrophobicity in a protein and its corresponding theoretical (“idealized”) distribution can be determined quantitatively, which, in turn, enables comparative analysis of structures regarded as geometrically similar (as well as geometrically divergent structures which are nevertheless regarded as similar in the sense of the fuzzy oil drop model). In this scope, the protein may be compared to an “intelligent micelle,” where local disorder is often intentional and related to biological function—unlike traditional surfactant micelles which remain highly symmetrical throughout and do not carry any encoded information.

Key words

Tertiary structure Supersecondary structure Secondary structure Hydrophobicity Water environment Hydrophobic core Micelle 

Notes

Acknowledgments

The authors are indebted to Piotr Nowakowski and Anna Śmietańska for their editorial and technical help. This research was supported by Jagiellonian University Medical College grant no. K/ZDS/006363.

References

  1. 1.
    Sillitoe I, Lewis TE, Cuff AL, Das S, Ashford P, Dawson NL, Furnham N, Laskowski RA, Lee D, Lees J, Lehtinen S, Studer R, Thornton JM, Orengo CA (2015) CATH: comprehensive structural and functional annotations for genome sequences. Nucleic Acids Res 43:D376–D381.  https://doi.org/10.1093/nar/gku947CrossRefPubMedGoogle Scholar
  2. 2.
  3. 3.
    Fox NK, Brenner SE, Chandonia JM (2014) SCOPe: Structural Classification of Proteins—extended, integrating SCOP and ASTRAL data and classification of new structures. Nucleic Acids Res 42:D304–D309CrossRefGoogle Scholar
  4. 4.
  5. 5.
    Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44(Database Issue):D279–D285CrossRefGoogle Scholar
  6. 6.
  7. 7.
    Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242CrossRefGoogle Scholar
  8. 8.
  9. 9.
    Sternberg MJE (1996) Protein structure prediction—principles and approaches. In: Sternebrg MJE (ed) Protein structure prediction: a practical approach. IRL Press, OxfordGoogle Scholar
  10. 10.
    Roterman I, Banach M, Kalinowska B, Konieczny L (2016) Influence of the aqueous environment on protein structure—a plausible hypothesis concerning the mechanism of amyloidogenesis. Entropy 18(10):351CrossRefGoogle Scholar
  11. 11.
    Roterman I, Banach M, Konieczny L (2017) Application of the fuzzy oil drop model describes amyloid as a ribbonlike micelle. Entropy 19(4):167CrossRefGoogle Scholar
  12. 12.
    Kalinowska B, Banach M, Konieczny L, Roterman I (2015) Application of divergence entropy to characterize the structure of the hydrophobic core in DNA interacting proteins. Entropy 17(3):1477–1507CrossRefGoogle Scholar
  13. 13.
    Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132CrossRefGoogle Scholar
  14. 14.
    Konieczny L, Brylinski M, Roterman I (2006) Gauss function based model of hydrophobicity density in proteins. In Silico Biol 6:15–22PubMedGoogle Scholar
  15. 15.
    Kauzmann W (1959) Some factors in the interpretation of protein denaturation. Adv Protein Chem 14:1–63CrossRefGoogle Scholar
  16. 16.
    Levitt M (1976) A simplified representation of protein conformations for rapid simulation of protein folding. J Mol Biol 104:59–107CrossRefGoogle Scholar
  17. 17.
    Kullback S, Leibler RA (1951) On information and sufficiency. Ann Math Stat 22:79–86CrossRefGoogle Scholar
  18. 18.
    Dygut J, Kalinowska B, Banach M, Piwowar M, Konieczny L, Roterman I (2016) Structural interface forms and their involvement in stabilization of multidomain proteins or protein complexes. Int J Mol Sci 17(10):E1741CrossRefGoogle Scholar
  19. 19.
    Kalinowska B, Banach M, Wiśniowski Z, Konieczny L, Roterman I (2017) Is the hydrophobic core a universal structural element in proteins? J Mol Model 23(7):205CrossRefGoogle Scholar
  20. 20.
    Devlin TM (2011) Textbook of biochemistry with clinical correlations, vol 7. Wiley, New YorkGoogle Scholar
  21. 21.
    Han KD, Park SJ, Jang SB, Lee BJ (2008) Solution structure of conserved hypothetical protein HP0892 from Helicobacter pylori. Proteins 70(2):599–602CrossRefGoogle Scholar
  22. 22.
    Banach M, Konieczny L, Roterman I (2014) The fuzzy oil drop model, based on hydrophobicity density distribution, generalizes the influence of water environment on protein structure and function. J Theor Biol 359:6–17CrossRefGoogle Scholar
  23. 23.
    Fokkens J, Klebe G (2006) A simple protocol to estimate differences in protein binding affinity for enantiomers without prior resolution of racemates. Angew Chem Int Ed Engl 45(6):985–989CrossRefGoogle Scholar
  24. 24.
    Jones EY, Davis SJ, Williams AF, Harlos K, Stuart DI (1992) Crystal structure at 2.8 A resolution of a soluble form of the cell adhesion molecule CD2. Nature 360(6401):232–239CrossRefGoogle Scholar
  25. 25.
    Kister A (2015) Amino acid distribution rules predict protein fold: protein grammar for beta-strand sandwich-like structures. Biomolecules 5:41–59CrossRefGoogle Scholar
  26. 26.
    Fokas AS, Papatheodorou TS, Kister AE, Gelfand IM (2005) A geometric construction determines all permissible strand arrangements of sandwich proteins. PNAS 102(44):15851–15853CrossRefGoogle Scholar
  27. 27.
    Fokas AS, Gelfand IM, Kister AE (2004) Prediction of the structural motifs of sandwich proteins. PNAS 101(48):16780–16783CrossRefGoogle Scholar
  28. 28.
    McManus AM, Nielsen KJ, Marcus JP, Harrison SJ, Green JL, Manners JM, Craik DJ (1999) MiAMP1, a novel protein from Macadamia integrifolia adopts a Greek key beta-barrel fold unique amongst plant antimicrobial proteins. J Mol Biol 293(3):629–638CrossRefGoogle Scholar
  29. 29.
    Banach M, Kalinowska B, Konieczny L, Roterman I (2016) Role of disulfide bonds in stabilizing the conformation of selected enzymes—an approach based on divergence entropy applied to the structure of hydrophobic core in proteins. Entropy 18(3):67CrossRefGoogle Scholar
  30. 30.
    Fu Z, Wang M, Paschke R, Rao KS, Frerman FE, Kim JJ (2004) The crystal structure and mechanism of human glutaryl-CoA dehydrogenase. Biochemistry 43:9674–9684CrossRefGoogle Scholar
  31. 31.
    Banach M, Prudhomme N, Carpentier M, Duprat E, Papandreou N, Kalinowska B, Chomilier J, Roterman I (2015) Contribution to the prediction of the fold code: application to immunoglobulin and flavodoxin cases. PLoS One 10(4):e0125098CrossRefGoogle Scholar
  32. 32.
    Li W, Kinch LN, Karplus PA, Grishin NV (2015) ChSeq: a database of chameleon sequences. Protein Sci 24(7):1075–1086.  https://doi.org/10.1002/pro.2689CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Kalinowska B, Banach M, Konieczny L, Roterman I (2016) Chameleon sequences—sequence-to-structure relation in proteins. J Proteomics Bioinform 9:264–275Google Scholar
  34. 34.
    Gallego F, Sol D, Chornet JJC, Cavada BS. PDBGoogle Scholar
  35. 35.
    Doki S, Kato HE, Solcan N, Iwaki M, Koyama M, Hattori M, Iwase N, Tsukazaki T, Sugita Y, Kandori H, Newstead S, Ishitani R, Nureki O (2013) Structural basis for dynamic mechanism of proton-coupled symport by the peptide transporter POT. Proc Natl Acad Sci U S A 110(28):11343–11348CrossRefGoogle Scholar
  36. 36.
    Binkowski TA, Xu X, Edwards A, Savchenko A, Joachimiak A. Midwest Center for Structural Genomics (MCSG)—PDBGoogle Scholar
  37. 37.
    Joint Center for Structural Genomics (JCSG)—PDBGoogle Scholar
  38. 38.
    Krieg S, Huché F, Diederichs K, Izadi-Pruneyre N, Lecroisey A, Wandersman C, Delepelaire P, Welte W (2009) Heme uptake across the outer membrane as revealed by crystal structures of the receptor-hemophore complex. Proc Natl Acad Sci U S A 106(4):1045–1050CrossRefGoogle Scholar
  39. 39.
    Gopal B, Haire LF, Cox RA, Jo Colston M, Major S, Brannigan JA, Smerdon SJ, Dodson G (2000) The crystal structure of NusB from Mycobacterium tuberculosis. Nat Struct Biol 7(6):475–478CrossRefGoogle Scholar
  40. 40.
    Williams GJ, Breazeale SD, Raetz CR, Naismith JH (2005) Structure and function of both domains of ArnA, a dual function decarboxylase and a formyltransferase, involved in 4-amino-4-deoxy-L-arabinose biosynthesis. J Biol Chem 280(24):23000–23008CrossRefGoogle Scholar
  41. 41.
    Malashkevich VN, Xiang DF, Raushel FM, Almo SC, Burley SK. New York Sgx Research Center For Structural Genomics (Nysgxrc)—PDBGoogle Scholar
  42. 42.
    Benarroch D, Smith P, Shuman S (2008) Characterization of a trifunctional mimivirus mRNA capping enzyme and crystal structure of the RNA triphosphatase domain. Structure 16(4):501–512CrossRefGoogle Scholar
  43. 43.
    Khan MB, Sponder G, Sjöblom B, Svidová S, Schweyen RJ, Carugo O, Djinović-Carugo K (2013) Structural and functional characterization of the N-terminal domain of the yeast Mg2+ channel Mrs2. Acta Crystallogr D Biol Crystallogr 69(Pt 9):1653–1664CrossRefGoogle Scholar
  44. 44.
    Holyoak T, Zhang B, Deng J, Tang Q, Prasannan CB, Fenton AW (2013) Energetic coupling between an oxidizable cysteine and the phosphorylatable N-terminus of human liver pyruvate kinase. Biochemistry 52(3):466–476CrossRefGoogle Scholar
  45. 45.
    Leonetti MD, Yuan P, Hsiung Y, Mackinnon R (2012) Functional and structural analysis of the human SLO3 pH- and voltage-gated K+ channel. Proc Natl Acad Sci U S A 109(47):19274–19279CrossRefGoogle Scholar
  46. 46.
    Joint Center for Structural Genomics (JCSG). Crystal structure of ftsz-like protein of unknown function (zp_00109722.1) from nostoc punctiforme pcc 73102 at 1.22 a resolution—PDBGoogle Scholar
  47. 47.
    Nishino T, Komori K, Ishino Y, Morikawa K (2003) X-ray and biochemical anatomy of an archaeal XPF/Rad1/Mus81 family nuclease: similarity between its endonuclease domain and restriction enzymes. Structure 11(4):445–457CrossRefGoogle Scholar
  48. 48.
    Ebihara A, Okamoto A, Kousumi Y, Yamamoto H, Masui R, Ueyama N, Yokoyama S, Kuramitsu S (2005) Structure-based functional identification of a novel heme-binding protein from Thermus thermophilus HB8. J Struct Funct Genom 6(1):21–32CrossRefGoogle Scholar
  49. 49.
    Altun M, Walter TS, Kramer HB, Herr P, Iphöfer A, Boström J, David Y, Komsany A, Ternette N, Navon A, Stuart DI, Ren J, Kessler BM (2015) The human otubain2-ubiquitin structure provides insights into the cleavage specificity of poly-ubiquitin-linkages. PLoS One 10(1):e0115344CrossRefGoogle Scholar
  50. 50.
    Irving JA, Cabrita LD, Rossjohn J, Pike RN, Bottomley SP, Whisstock JC (2003) The 1.5 A crystal structure of a prokaryote serpin: controlling conformational change in a heated environment. Structure 11(4):387–397CrossRefGoogle Scholar
  51. 51.
    Mancusso R, Gregorio GG, Liu Q, Wang DN (2012) Structure and mechanism of a bacterial sodium-dependent dicarboxylate transporter. Nature 491(7425):622–626CrossRefGoogle Scholar
  52. 52.
    Ferguson AD, Welte W, Hofmann E, Lindner B, Holst O, Coulton JW, Diederichs K (2000) A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure 8(6):585–592CrossRefGoogle Scholar
  53. 53.
    Nagano S, Cupp-Vickery JR, Poulos TL (2005) Crystal structures of the ferrous dioxygen complex of wild-type cytochrome P450eryF and its mutants, A245S and A245T: investigation of the proton transfer system in P450eryF. J Biol Chem 280(23):22102–22107CrossRefGoogle Scholar
  54. 54.
    Craig TK, Abendroth J, Lorimer D, Burgin AB Jr, Segall A, Rohwer F. Crystal structure of a pentameric capsid protein isol from metagenomic phage sequences solved by iodide sad phasing—PDBGoogle Scholar
  55. 55.
    Iverson TM, Alber BE, Kisker C, Ferry JG, Rees DC (2000) A closer look at the active site of gamma-class carbonic anhydrases: high-resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila. Biochemistry 39(31):9222–9231CrossRefGoogle Scholar
  56. 56.
    Roterman I, Banach M, Konieczny L (2017) Propagation of fibrillar structural forms in proteins stopped by naturally occurring short polypeptide chain fragments. Pharmaceuticals (Basel) 10(4):89CrossRefGoogle Scholar
  57. 57.
    Roterman I, Banach M, Konieczny L (2018) Towards the design of anti-amyloid short peptide helices. Bioinformation 14(1):1–7CrossRefGoogle Scholar
  58. 58.
    Xiao Y, Ma B, McElheny D, Parthasarathy S, Long F, Hoshi M, Nussinov R, Ishii Y (2015) A beta (1–42) fibril structure illuminates self-recognition and replication of amyloid in Alzheimer’s disease. Nat Struct Mol Biol 22:499–505CrossRefGoogle Scholar
  59. 59.
    Chiti F, Dobson CM (2017) Protein misfolding, amyloid formation and human disease; a summary of progress over the last decade. Annu Rev Biochem 86:27–68CrossRefGoogle Scholar
  60. 60.
    Gremer L, Schölzel D, Schenk C, Reinartz E, Labahn J, Ravelli RBG, Tusche M, Lopez-Iglesias C, Hoyer W, Heise H, Willbold D, Schröder GF (2017) Fibril structure of amyloid-β(1–42) by cryo-electron microscopy. Science 358(6359):116–119CrossRefGoogle Scholar
  61. 61.
    Biedermann F, Nau WM, Schneider H-J (2014) The hydrophobic effect revisited—studies with supramolecular complexes imply high-energy water as a noncovalent driving force. Angew Chem 53:11158–11171CrossRefGoogle Scholar
  62. 62.
    Schutzius TM, Jung S, Maitra T, Graeber G, Köhme M, Poulikakos D (2015) Spontaneous droplet trampolining on rigid superhydrophobic surfaces. Nature 527(7576):82–85CrossRefGoogle Scholar
  63. 63.
    Kim KH, Späh A, Pathak H, Perakis F, Mariedahl D, Amann-Winkel K, Sellberg JA, Lee JH, Kim S, Park J, Nam KH, Katayama T, Nilsson A (2017) Maxima in the thermodynamic response and correlation functions of deeply supercooled water. Science 358(6370):1589–1593CrossRefGoogle Scholar
  64. 64.
    Konieczny L, Roterman I (2012) Conclusions. In: Roterman-Konieczna I (ed) Protein folding in silico. Elsevier, Oxford, pp 191–203CrossRefGoogle Scholar
  65. 65.
    Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223–230CrossRefGoogle Scholar
  66. 66.
    Kim W, Xiao J, Chaikof EL (2011) Recombinant amphiphilic protein micelles for drug delivery. Langmuir 27(23):14329–14334CrossRefGoogle Scholar
  67. 67.
    Kim W, Brady C, Chaikof EL (2012) Amphiphilic protein micelles for targeted in vivo imaging. Acta Biomater 8(7):2476–2482CrossRefGoogle Scholar
  68. 68.
    Schott H (1968) On the similarity between micelles of nonionic detergents and globular proteins. J Am Oil Chem Soc 45(11):823–824CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Mateusz Banach
    • 1
  • Leszek Konieczny
    • 2
  • Irena Roterman
    • 1
    Email author
  1. 1.Department of Bioinformatics and TelemedicineJagiellonian University, Medical CollegeKrakówPoland
  2. 2.Chair of Medical BiochemistryJagiellonian University, Medical CollegeKrakówPoland

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