Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-28T17:08:35.045Z Has data issue: false hasContentIssue false
  • English
  • Français

Use of vector formalism in the analysis of hydrophobic and electric driving forces in biological assemblies

Published online by Cambridge University Press:  11 April 2022

Angel Mozo-Villarías Open the ORCID record for Angel Mozo-Villarías [Opens in a new window] ,
Juan A. Cedano Open the ORCID record for Juan A. Cedano [Opens in a new window]  and
Enrique Querol Open the ORCID record for Enrique Querol [Opens in a new window]
Angel Mozo-Villarías*
Affiliation:
Institut de Biotecnologia i Biomedicina and Departament de Bioquímica i Biologia Molecular, Campus de Bellaterra, Universitat Autónoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
Juan A. Cedano
Affiliation:
Institut de Biotecnologia i Biomedicina and Departament de Bioquímica i Biologia Molecular, Campus de Bellaterra, Universitat Autónoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
Enrique Querol
Affiliation:
Institut de Biotecnologia i Biomedicina and Departament de Bioquímica i Biologia Molecular, Campus de Bellaterra, Universitat Autónoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
*
Author for correspondence: Angel Mozo-Villarías, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Hydrophobic forces are known to have a crucial part not only in the conformation of the three-dimensional structure of proteins, but also in the build-up of DNA–protein complexes. Electric forces also play an important role both in the tertiary as well in the quaternary structure of macromolecular associations. Sometimes both hydrophobic and electric interactions add up their strengths to accomplish these structures but in most cases they act in opposite directions. This fact, together with being overall interactions with different ranges, provides a nuanced equilibrium also modulated by the need to comply with steric hindrances and geometric frustration effects. This review focuses on the utility of using the hydrophobic and electrical dipole moment vectors to describe the interactions that give rise to the structures of biological macromolecules. Although different definitions of both electric dipole and hydrophobic moments have been described in the literature, results obtained in biological assemblies demonstrate the principle of the biological membrane model. According to this model, postulated by our group, biological macromolecules tend to associate by aligning their hydrophobic moments in a similar manner to phospholipids in a membrane. Examples of both closed and open structures are used to assess the predictability of our model. We seek agreement between our results with those described in the current literature. The review ends with possible future projections using this formalism.

Keywords

Biological membrane modelconsensus DNADNAelectric dipole momenthydrophobic energyhydrophobic interactionhydrophobic momentproteinsprotein self-assemblingtranscription systems
Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 55 , 2022 , e4
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, CG, Jürgens, MC, Shepherd, DA, Freund, SMV, Ashcroft, AE and Ferguson, N (2013) Thermodynamic origins of protein folding, allostery, and capsid formation in the human hepatitis B virus core protein. Proceedings of the National Academy of Sciences of the USA 110, E2782–E2791.CrossRefGoogle ScholarPubMed
Antosiewicz, J (1995) Computation of the dipole moments of proteins. Biophysical Journal 69, 1344–1354.CrossRefGoogle ScholarPubMed
Aoki, M, Yokota, T, Shigiura, I, Sasaki, C, Hasegawa, T, Okumura, C, Ishiguro, K, Kohno, T, Sugio, S and Matsuzaki, T (2004) Structural insight into nucleotide recognition in tau-protein kinase I/glycogen synthase. Acta Crystallographica D60, 439–446.Google Scholar
Barlow, DJ and Thornton, JM (1986) The distribution of charged groups in proteins. Biopolymers 25, 1717–1733.CrossRefGoogle ScholarPubMed
Boldina, G, Ivashchenko, A and Régnier, M (2009) Using profiles based on nucleotide hydrophobicity to define essential regions for splicing. International Journal of Biological Sciences 5, 13–19.CrossRefGoogle ScholarPubMed
Bui, PT and Hoang, TX (2021) Hydrophobic and electrostatic interactions modulate protein escape at the ribosomal exit tunnel. Biophysical Journal 120, 4798–4808.CrossRefGoogle ScholarPubMed
Chandler, D (2005) Interfaces and the driving force of hydrophobic assembly. Nature 437, 640–646.CrossRefGoogle ScholarPubMed
Chari, MA, Singh, SN, Yadav, S, Brems, DN and Kalonia, DSA (2012) Determination of the dipole moments of RNAse SA wild type and a basic mutant. Proteins 80, 1041–1052.Google Scholar
Cherry, MA, Higgins, SK, Melroy, H, Lee, HS and Pokorny, A (2014) Peptides with the same composition, hydrophobicity, and hydrophobic moment bind to phospholipid bilayers with different affinities. Journal of Physical Chemistry B 118, 12462–12470.CrossRefGoogle ScholarPubMed
Chothia, C (1976) The nature of the accessible and buried surfaces in proteins. Journal of Molecular Biology 105, 1–12.CrossRefGoogle ScholarPubMed
Collepardo-Guevara, R and Schlick, T (2014) Chromatin fiber polymorphism triggered by variations of DNA linker lengths. Proceedings of the National Academy of Sciences of the USA 111, 8061–8066.CrossRefGoogle ScholarPubMed
Dabán, JR and Bermúdez, A (1998) Interdigitated solenoid model for compact chromatin. Biochemistry 37, 4299–4304.CrossRefGoogle ScholarPubMed
Decherchi, S and Rocchia, W (2013) A general and robust ray-casting-based algorithm for triangulating surfaces at the nanoscale. PLoS ONE 8, e59744.CrossRefGoogle ScholarPubMed
Eisenberg, D, Weiss, RM, Terwilliger, TC and Wilcox, W (1982 a) Hydrophobic moments and protein structure. Faraday Symposia of the Chemical Society 17, 109–120.CrossRefGoogle Scholar
Eisenberg, D, Weiss, RM and Terwilliger, TC (1982 b) The helical hydrophobic moment: a measure of amphiphilicity of a helix. Nature 299, 371–374.Google ScholarPubMed
Eisenberg, D, Weiss, RM and Terwilliger, TC (1984) The hydrophobic moment detects periodicity in protein hydrophobicity. Proceedings of the National Academy of Sciences of the USA 81, 140–144.CrossRefGoogle ScholarPubMed
Felder, CE, Prilusky, J, Silman, I and Sussman, JL (2007) A server and database for dipole moments of proteins. Nucleic Acids Research 35, W512–W521.CrossRefGoogle ScholarPubMed
Feng, B, Sosa, R, Mårtensson, A, Jiang, K, Tong, A, Dorfman, K, Takahashi, M, Lincoln, P, Bustamante, C, Westerlund, F and Nordén, B (2019) Hydrophobic catalysis and a potential biological role of DNA unstacking induced by environment effects. Proceedings of the National Academy of Sciences of the USA 116, 17169–17174.CrossRefGoogle Scholar
Fitzpatrick, AWP, Falcon, B, He, S, Murzin, AG, Murshudov, G, Garringer, HJ, Crowther, RA, Ghetti, B, Goedert, M and Scheres, SHW (2017) Cryo-EM structures of tau filaments from Alzheimer's disease. Nature 547, 185–190.CrossRefGoogle ScholarPubMed
Franco-Serrano, L, Hernández, S, Calvo, A, Severi, MA, Ferragut, G, Pérz-Pons, JA, Piñol, J, Pich, O, Mozo-Villarías, A, Amela, I, Querol, E and Cedano, J (2017) MultitaskProtDB-II: an update of a database of multitasking/moonlighting proteins. Nucleic Acids Research. 46, D645–D648.CrossRefGoogle Scholar
Frederic, E and Houssier, C (1973) Electric Dichroism and Electric Birefringence. Oxford: Clarendon Press.Google Scholar
Gao, D, Remsing, RC and Weeks, JD (2002) Short solvent model for ion correlations and hydrophobic association. Proceedings of the National Academy of Sciences of the USA 117, 1293–1302.CrossRefGoogle Scholar
Grason, GM (2016) Perspective: geometrically frustrated assemblies. Journal of Chemical Physics 145, 110901.CrossRefGoogle Scholar
Hammer, MU, Anderson, TH, Chaimovich, A, Shell, AMS and Israelachvili, J (2010) The search for the hydrophobic force law. Faraday Discussions 146, 299–308.CrossRefGoogle ScholarPubMed
Hancock, SP, Stella, S, Cascio, D and Johnson, RC (2016) DNA sequence determinants controlling affinity, stability and shape of DNA complexes bound by the nucleoid protein Fis. PLoS ONE 11, e0150189.CrossRefGoogle ScholarPubMed
Hanson, RM, Prilusky, J, Renjian, Z, Nakane, T and Sussman, JL (2013) JSmol and the next generation web-based representation of 3D molecular structure as applied to Proteopedia. The Israel Journal of Chemistry 53, 207–216.Google Scholar
Hol, WG (1985) The role of the α-helix dipole in protein function and structure. Progress in Biophysics and Molecular Biology 45, 149–195.CrossRefGoogle ScholarPubMed
Honig, B and Nichols, A (1995) Classical electrostatics in biology and chemistry. Science 268, 1144–1149.CrossRefGoogle ScholarPubMed
Hummer, G (1999) Hydrophobic force field as a molecular alternative to surface-area models. Journal of the American Chemical Society 121, 6299–6305.CrossRefGoogle Scholar
Hummer, G, Garde, S, García, AE, Pohorille, A and Pratt, LR (1996) An information theory model of hydrophobic interactions. Proceedings of the National Academy of Sciences of the USA 93, 8951–8955.CrossRefGoogle ScholarPubMed
Isom, DG, Castañeda, CA, Cannon, BR, Velu, PD and García Moreno, B (2010) Charges in the hydrophobic interior of proteins. Proceedings of the National Academy of Sciences of the United States of America 107, 16096–16100.CrossRefGoogle ScholarPubMed
Israelachvili, JM (2011) Intermolecular and Surface Forces, 3rd Edn. Amsterdam: Academic Press.Google Scholar
Israelachvili, J and Pashley, R (1982) The hydrophobic interaction is long range, decaying exponentially with distance. Nature 300, 341–342.Google ScholarPubMed
Ivanova, MI, Sievers, SA, Sawaya, MR, Wall, JS and Eisenberg, D (2009) Molecular basis for insulin fibril assembly. Proceedings of the National Academy of Sciences of the USA 106, 18990–18995.CrossRefGoogle ScholarPubMed
Jackson, RM and Sternberg, MJE (1994) Application of scaled particle theory to model the hydrophobic effect: implications for molecular association and protein stability. Protein Engineering 7, 371–383.CrossRefGoogle ScholarPubMed
Janin, J (1979) Surface and inside volumes in globular proteins. Nature 277, 491–492.CrossRefGoogle ScholarPubMed
Kapcha, LH and Rossky, PJ (2014) A simple atomic-level hydrophobicity scale reveals protein interfacial structure. Journal of Molecular Biology 426, 484–498.CrossRefGoogle ScholarPubMed
Katen, SP, Tan, Z, Chitapu, SR, Finn, MG and Zlotnick, A (2013) Assembly-directed antivirals differentially bind quasiequivalent pockets to modify hepatitis B virus capsid tertiary and quaternary structure. Structure 21, 1406–1416.CrossRefGoogle ScholarPubMed
Kegel, WK and van der Schoot, P (2004) Competing hydrophobic and screened-Coulomb interactions in hepatitis B virus capsid assembly. Biophysical Journal 86, 3905–3913.CrossRefGoogle ScholarPubMed
Kobayasi, A, Asai, H and Oosawa, F (1964) Electric birefringence of actin. Biochimica et Biophysica Acta 88, 528–540.Google ScholarPubMed
Kooijman, M, Bloemendal, M, Traub, P, van Grondelle, R and van Amerongen, H (1997) Transient electric birefringence study of intermediate filament formation from vimentin and glial fibrillary acidic protein. Journal of Biological Chemistry 272, 22548–22555.CrossRefGoogle ScholarPubMed
Kronberg, B (2016) The hydrophobic effect. Current Opinion in Colloid & Interface Science 22, 14–22.CrossRefGoogle Scholar
Lenz, M and Witten, TA (2017) Geometrical frustration yields fibre formation in self-assembly. Nature Physics 13, 1100–1104.CrossRefGoogle Scholar
Lin, MS, Fawzi, NL and Head-Gordon, T (2007) Hydrophobic potential of mean force as a solvation function for protein structure prediction. Structure 15, 727–740.CrossRefGoogle ScholarPubMed
Lindman, B, Medronho, B, Alves, L, Norgren, M and Nordenskiöld, L (2021) Hydrophobic interactions control the self-assembly of DNA and cellulose. Quarterly Reviews of Biophysics 54, e3, 1–22.CrossRefGoogle ScholarPubMed
Liu, C, Liu, CC, Kanekiyo, T, Xu, H and Bu, G (2013) Alipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nature Reviews Neurology 9, 106–118.CrossRefGoogle Scholar
Lokareddy, R, Sankhala, RS, Roy, A, Afonine, PV, Motwani, T, Teschke, CM, Parent, KN and Cingolani, G (2017) Portal protein functions akin to a DNA-sensor that couples genome-packaging to icosahedral capsid maturation. Nature Communications 8, 14310.CrossRefGoogle ScholarPubMed
Lu, Y, Weers, BD and Stellwagen, NC (2003) Analysis of DNA bending by transient electric birefringence. Biopolymers 70, 270–288.CrossRefGoogle Scholar
Lu, JX, Qian, W, Yau, WM, Schwieters, CD, Meredith, SC and Tycko, R (2013) Molecular structure of β-amyloid fibrils in Alzheimer's disease brain tissue. Cell 154, 1257–1268.CrossRefGoogle ScholarPubMed
Makowski, M, Czaplewski, C, Liwo, A and Scheraga, HA (2010) Potential of mean force of association of large hydrophobic particles: toward the nanoscale limit. Journal of Physical Chemistry B 114, 993–1003.CrossRefGoogle ScholarPubMed
Mant, CT, Kovacs, JM, Kim, HM, Pollock, DD and Hodges, RS (2009) Intrinsic amino acid side-chain hydrophilicity/hydrophobicity coefficients determined by reversed-phase high-performance liquid chromatography of model peptides: comparison with other hydrophilicity/hydrophobicity scales. Peptide Science 92, 573–595.CrossRefGoogle ScholarPubMed
Meyer, E, Rosenberg, K and Israelachvili, J (2006) Recent progress in understanding hydrophobic interactions. Proceedings of the National Academy of Sciences of the USA 103, 15739–15746.CrossRefGoogle ScholarPubMed
Mozo-Villarías, A and Querol, E (2019) A protein self-assembly model guided by electrostatic and hydrophobic dipole moments. PLoS ONE 14, e0216253.CrossRefGoogle ScholarPubMed
Mozo-Villarías, A, Cedano, JA and Querol, E (2003) A simple electrostatic criterion for predicting the thermal stability of proteins. Protein Engineering 16, 279–286.CrossRefGoogle ScholarPubMed
Mozo-Villarías, A, Cedano, JA and Querol, E (2014) A model of protein association based on their hydrophobic and electric interactions. PLoS ONE 9, e110352.CrossRefGoogle Scholar
Mozo-Villarías, A, Cedano, JA and Querol, E (2016) Vector description of electric and hydrophobic interactions in protein homodimers. European Biophysics Journal with Biophysics Letters 45, 341–346.CrossRefGoogle ScholarPubMed
Mozo-Villarías, A, Cedano, JA and Querol, E (2017) Self-assembly of open protein systems: a comprehensive view based on the interactions between 3D hydrophobic and electric dipole moment vectors. Journal of Proteomics & Bioinformatics 10, 252–259.CrossRefGoogle Scholar
Mozo-Villarías, A, Cedano, JA and Querol, E (2021) The importance of hydrophobic interactions in the structure of transcription systems. European Biophysics Journal with Biophysics Letters 50, 951–961.CrossRefGoogle ScholarPubMed
Nozaki Y, and Tanford, (1971) The solubility of amino acids and two glycine peptides in aqueous ethanol and dioxane solutions. Establishment of a hydrophobicity scale. Journal of Biological Chemistry 246, 2211–2217.CrossRefGoogle ScholarPubMed
Orttung, WH (1977) Direct solution of the Poisson equation for biomolecules of arbitrary shape, polarizability density and charge distribution. Annals of the New York Academy of Sciences 303, 22–37.CrossRefGoogle Scholar
Palau, J, Mozo, A and Querol, E (1980) On the interaction of histone H4 peptides with DNA. Biochimie 62, 241–249.CrossRefGoogle ScholarPubMed
Palau, J, Mozo, A and Querol, E (1983) On the interaction of histone H1 and H1 peptides with DNA. Anales de Química 79:84–90.Google Scholar
Paravastu, AK, Leapman, RD, Yau, WM and Tycko, R (2008) Molecular structural basis for polymorphism in Alzheimer's β-amyloid fibrils. Proceedings of the National Academy of Sciences of the USA 105, 18349–18354.CrossRefGoogle ScholarPubMed
Patel, AJ, Varilly, P and Chandler, D (2010) Fluctuations of water near extended hydrophobic and hydrophilic surfaces. Journal of Physical Chemistry B 114, 1632–1637.CrossRefGoogle ScholarPubMed
Patel, AJ, Varilly, P, Jamadagni, SN, Hagan, MF, Chandler, D and Garde, S (2012) Sitting at the edge: how biomolecules use hydrophobicity to tune their interactions and function. Journal of Physical Chemistry B 116, 2498–2503.CrossRefGoogle ScholarPubMed
Peng, C, Liu, J, Zhao, D and Zhou, J (2014) Adsorption of hydrophobin on different self-assembled monolayers: the role of the hydrophobic dipole and the electric dipole. Langmuir 30, 11401–11411.CrossRefGoogle ScholarPubMed
Perutz, MF (1978) Electrostatic effects in proteins. Science 201, 1187–1191.CrossRefGoogle ScholarPubMed
Peters, C and Elofsson, A (2014) The hydrophobic moment and its use in the classification of amphiphilic structres. Proteins 82, 2190–2198.CrossRefGoogle Scholar
Petersen, DC and Cone, RA (1975) The electric dipole moment of rhodopsin solubilized in Triton X-100. Biophysical Journal 15, 1181–1200.CrossRefGoogle ScholarPubMed
Phoenix, D and Harris, F (2002) Why is the biological hydrophobicity scale more accurate than earlier experimental hydrophobicity scales?. Molecular Membrane Biology 19, 1–10.CrossRefGoogle Scholar
Prat Gay, G, Ruiz-Sanz, J, Neira, JL, Corrales, FJ, Otzen, DE, Ladurner, AG and Fersht, AR (1995) Conformational pathway of the polypeptide chain of chymotrypsin inhibitor-2 growing from its N terminus in vitro. Parallels with the protein folding pathway. Journal of Molecular Biology 254, 968–979.CrossRefGoogle ScholarPubMed
Rawat, N and Biswas, P (2012) Hydrophobic moments, shape, and packing in disordered proteins. Journal of Physical Chemistry B 116, 6326–6335.CrossRefGoogle ScholarPubMed
Reißer, S, Strandberg, E, Steinbrecher, T and Ulrich, AS (2014) 3D hydrophobic moment vectors as a tool to characterize the surface polarity of amphiphilic peptides. Biophysical Journal 106, 2385–2394.CrossRefGoogle ScholarPubMed
Sabaté, R, Esparagó, A, de Groot, NS, Valle-Delgado, JJ, Fernández-Busquets, X and Ventura, S (2010) The role of protein sequence and amino acid composition in amyloid formation: scrambling and backward reading of IAPP amyloid fibrils. Journal of Molecular Biology 404, 337–352.CrossRefGoogle ScholarPubMed
Sarkar, A and Kellogg, E (2010) Hydrophobicity – shake flasks, protein folding and drug discovery. Current Topics in Medicinal Chemistry 10, 67–83.CrossRefGoogle ScholarPubMed
Sengupta, D, Behera, RN, Smith, JC and Ullman, GM (2005) The α-helix dipole: screened out? Structure (London, England: 1993) 13, 849–855.CrossRefGoogle ScholarPubMed
Silverman, BD (2001) Hydrophobic moments of protein structures: spatially profiling the distribution. Proceedings of the National Academy of Sciences of the USA 98, 4996–5001.CrossRefGoogle ScholarPubMed
Silverman, BD (2003) Hydrophobic moments of tertiary protein structures. Proteins: Structure, Function, and Bioinformatics 53, 880–888.CrossRefGoogle ScholarPubMed
Stellwagen, NC (2002) The use of transient electric birefringence to characterize the conformation of DNA in solution, the mechanism of DNA gel electrophoresis, and the structure of agarose gels. Colloids and Surfaces A 209, 107–122.CrossRefGoogle Scholar
Takashima, S (1996) Measurement and computation of the dipole moment of globular proteins III: chymotrypsin. Biophysical Chemistry 58, 13–20.CrossRefGoogle ScholarPubMed
Takashima, S (2001) The structure and dipole moment of globular proteins in solution and crystalline states: use of NMR and X-ray databases for the numerical calculation of dipole moment. Biopolymers 58, 398–409.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Takashima, S and Yamaoka, K (1999) The electric dipole moment of DNA-binding HU protein calculated by the use of an NMR database. Biophysical Chemistry 80, 153–163.CrossRefGoogle ScholarPubMed
Takei, T, Watanabe, A and Amako, Y (1999) Permanent electric dipole moment and polarizability in stark modulation spectra of the ICl B–X transition. Journal of Chemical Physics 110, 10874–10881.CrossRefGoogle Scholar
Tanford, C (1980) The Hydrophobic Effect: Formation of Micelles and Biological Membranes, 2nd Edn. Somerset, NJ: Wiley & Sons.Google Scholar
Tasi, CF and Lee, KJ (2011) A comparative study of the second-order hydrophobic moments for globular proteins: the consensus scale of hydrophobicity and the CHARMM partial atomic charges. International Journal of Molecular Sciences 12, 8449–8465.Google Scholar
Tsodikov, OV and Biswas, T (2011) Structural and thermodynamic signatures of DNA recognition by Mycobacterium tuberculosis DnaA. Journal of Molecular Biology 410, 461–476.CrossRefGoogle ScholarPubMed
Vik, SB (2011) The transmembrane helices of the L, M and N subunits of complex I from E. coli can be assigned on the basis of conservation and hydrophobic moment analysis. FEBS Letters 585, 1180–1184.CrossRefGoogle Scholar
Vik, SB and Dao, NN (1992) Prediction of transmembrane topology of Fo proteins from Escherichia coli F1Fo ATP synthase using variational and hydrophobic moment analyses. Biochimica et Biophysica Acta 1140, 199–207.CrossRefGoogle Scholar
Von Heijne, G and Blomberg, C (1979) Trans-membrane translocation of proteins. The direct transfer model. European Journal of Biochemistry 97, 175–181.CrossRefGoogle ScholarPubMed
Wallace, J, Daman, OA, Harris, F and Phoenix, DA (2004) Investigation of hydrophobic moment and hydrophobicity properties for transmembrane α-helices. Theoretical Biology and Medical Modelling 1, 5.CrossRefGoogle ScholarPubMed
Wang, P, Naduthambi, D, Mosley, RT, Niu, C, Furman, PA, Otto, MJ and Sofia, MJ (2011) Phenylpropenamide derivatives: anti-hepatitis B virus activity of the Z isomer, SAR and the search for novel analogs. Bioorganic & Medicinal Chemistry Letters 21, 4642–4647.CrossRefGoogle Scholar
Washel, A and Russell, ST (1984) Calculations of electrostatic interactions in biological systems and in solutions. Quarterly Reviews of Biophysics 17, 283–422.CrossRefGoogle Scholar
White, SH and Wimley, WC (1999) Membrane protein folding and stability: physical principles. Annual Review of Biophysics and Biomolecular Structure 28, 319–365.CrossRefGoogle ScholarPubMed
Wimley, WC and White, SH (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Structural & Molecular Biology 3, 842–848.CrossRefGoogle ScholarPubMed
Wolfenden, R, Anderson, L, Cullis, PM and Southgate, CC (1981) Affinities of amino acid side chains for solvent water. Biochemistry 20, 849–855.CrossRefGoogle ScholarPubMed
Worch, R (2013) The helical hairpin structure of the influenza fusion peptide can be seen on a hydrophobic moment map. FEBS Letters 587, 2980–2983.CrossRefGoogle ScholarPubMed
Wynne, SA, Crowther, RA and Leslie, AGW (1999) The crystal structure of the human hepatitis B virus capsid. Molecular Cell 3, 771–780.CrossRefGoogle ScholarPubMed
Xiao, F, Chen, Z, Wei, Z and Tian, L (2020) Hydrophobic interaction: a promising driving force for the biomedical applications of nucleic acids. Advanced Science 7, 2001048.CrossRefGoogle ScholarPubMed
Zhang, Y, Wang, W, Chen, J, Zhang, K, Gao, F, Gao, B, Zhang, S, Dong, M, Basenbacher, F, Gong, W, Zhang, M, Sun, F and Feng, W (2013) Structural insights into the intrinsic self-assembly of Par-3 N-terminal domain. Structure 21, 997–1006.CrossRefGoogle ScholarPubMed
Zhao, G, Perilla, JR, Yefenyuy, EL, Meng, X, Chen, B, Ning, J, Ahn, J, Gronenborn, AM, Schulten, K, Aiken, C and Zhang, P (2013) Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497, 643–646.CrossRefGoogle ScholarPubMed
Zhu, G, Xu, Z and Yan, LT (2020) Entropy at bio–nano interfaces. Nano Letters 20, 5616–5624.CrossRefGoogle ScholarPubMed
Supplementary material: File

Mozo-Villarías et al. supplementary material

Mozo-Villarías et al. supplementary material

Download Mozo-Villarías et al. supplementary material(File)
File 817.6 KB