Topics in Catalysis

, Volume 61, Issue 9–11, pp 1125–1138 | Cite as

Probing Molecular Basis for Constructing Interface Bionanostructures

  • Yuchen Lin
  • Jing Xu
  • Lanlan Yu
  • Yanlian Yang
  • Chen Wang
Original Paper


Understanding the interface of bionanostructures is crucial for novel biomedical applications. In this review, we endeavor to reflect the recent progress on molecular features of interfacial behavior of peptides and the molecular basis for tuning composition and distribution of amino acids at the interfaces. These progresses could help enrich the insights of protein-interface structures at the level of single amino acids.


Interface Bionanostructure Protein Peptide Scanning tunneling microscopy (STM) Amino acid 



The authors greatly acknowledge the financial support by the National Natural Science Foundation of China (Nos. 21673055, 21773042).


  1. 1.
    Stevens PS (1974) Patterns in nature, 1st edn. Little, BostonGoogle Scholar
  2. 2.
    Wainwright SA (1976) Mechanical design in organisms. Edward Arnold, LondonGoogle Scholar
  3. 3.
    Hernandez K, Fernandez-Lafuente R (2011) Control of protein immobilization: coupling immobilization and site-directed mutagenesis to improve biocatalyst or biosensor performance. Enzyme Microb Tech 48(2):107–122. CrossRefGoogle Scholar
  4. 4.
    Sassolas A, Blum LJ, Leca-Bouvier BD (2012) Immobilization strategies to develop enzymatic biosensors. Biotechnol Adv 30(3):489–511. CrossRefGoogle Scholar
  5. 5.
    Axup JY, Bajjuri KM, Ritland M, Hutchins BM, Kim CH, Kazane SA, Halder R, Forsyth JS, Santidrian AF, Stafin K, Lu YC, Tran H, Seller AJ, Biroce SL, Szydlik A, Pinkstaff JK, Tian F, Sinha SC, Felding-Habermann B, Smider VV, Schultz PG (2012) Synthesis of site-specific antibody–drug conjugates using unnatural amino acids. Proc Natl Acad Sci USA 109(40):16101–16106. CrossRefGoogle Scholar
  6. 6.
    Beck A, Goetsch L, Dumontet C, Corvaia N (2017) Strategies and challenges for the next generation of antibody drug conjugates. Nat Rev Drug Discov 16(5):315–337. CrossRefGoogle Scholar
  7. 7.
    Jiang W, Kim BYS, Rutka JT, Chan WCW (2008) Nanoparticle-mediated cellular response is size-dependent. Nat Nanotechnol 3(3):145–150. CrossRefGoogle Scholar
  8. 8.
    Nel AE, Madler L, Velegol D, Xia T, Hoek EMV, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009) Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 8(7):543–557. CrossRefGoogle Scholar
  9. 9.
    Brazeau P, Vale W, Burgus R, Ling N, Butcher M, Rivier J, Guillemin R (1973) Hypothalamic polypeptide that inhibits secretion of immunoreactive pituitary growth-hormone. Science 179(4068):77–79. CrossRefGoogle Scholar
  10. 10.
    Dimitriadis G, Mitrou P, Lambadiari V, Maratou E, Raptis SA (2011) Insulin effects in muscle and adipose tissue. Diabetes Res Clin Pract 93:S52–S59CrossRefGoogle Scholar
  11. 11.
    Harder J, Bartels J, Christophers E, Schroder JM (2001) Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 276(8):5707–5713. CrossRefGoogle Scholar
  12. 12.
    Rochet JC, Lansbury PT Jr (2000) Amyloid fibrillogenesis: themes and variations. Curr Opin Struct Biol 10(1):60–68CrossRefGoogle Scholar
  13. 13.
    Tan SY, Pepys MB (1994) Amyloidosis. Histopathology 25(5):403–414. CrossRefGoogle Scholar
  14. 14.
    Smith A (2003) Protein misfolding. Nature 426(6968):883–883. CrossRefGoogle Scholar
  15. 15.
    Xie JP, Zheng YG, Ying JY (2009) Protein-directed synthesis of highly fluorescent gold nanoclusters. J Am Chem Soc 131(3):888. CrossRefGoogle Scholar
  16. 16.
    Whaley SR, English DS, Hu EL, Barbara PF, Belcher AM (2000) Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 405(6787):665–668CrossRefGoogle Scholar
  17. 17.
    Hartgerink JD, Beniash E, Stupp SI (2001) Self-assembly and mineralization of peptide–amphiphile nanofibers. Science 294(5547):1684–1688CrossRefGoogle Scholar
  18. 18.
    Lee SW, Mao CB, Flynn CE, Belcher AM (2002) Ordering of quantum dots using genetically engineered viruses. Science 296(5569):892–895CrossRefGoogle Scholar
  19. 19.
    Scheibel T, Parthasarathy R, Sawicki G, Lin XM, Jaeger H, Lindquist SL (2003) Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition. Proc Natl Acad Sci USA 100(8):4527–4532CrossRefGoogle Scholar
  20. 20.
    Mao CB, Solis DJ, Reiss BD, Kottmann ST, Sweeney RY, Hayhurst A, Georgiou G, Iverson B, Belcher AM (2004) Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science 303(5655):213–217CrossRefGoogle Scholar
  21. 21.
    Nam KT, Kim DW, Yoo PJ, Chiang CY, Meethong N, Hammond PT, Chiang YM, Belcher AM (2006) Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 312(5775):885–888CrossRefGoogle Scholar
  22. 22.
    Jones S, Thornton JM (1996) Principles of protein–protein interactions. Proc Natl Acad Sci USA 93(1):13–20. CrossRefGoogle Scholar
  23. 23.
    Lo Conte L, Chothia C, Janin J (1999) The atomic structure of protein–protein recognition sites. J Mol Biol 285(5):2177–2198CrossRefGoogle Scholar
  24. 24.
    Keskin O, Gursoy A, Ma B, Nussinov R (2008) Principles of protein–protein interactions: what are the preferred ways for proteins to interact?. Chem Rev 108(4):1225–1244. CrossRefGoogle Scholar
  25. 25.
    Desmyter A, Transue TR, Ghahroudi MA, Thi MHD, Poortmans F, Hamers R, Muyldermans S, Wyns L (1996) Crystal structure of a camel single-domain V-H antibody fragment in complex with lysozyme. Nat Struct Biol 3(9):803–811. CrossRefGoogle Scholar
  26. 26.
    Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, Baker D (2003) Design of a novel globular protein fold with atomic-level accuracy. Science 302(5649):1364–1368. CrossRefGoogle Scholar
  27. 27.
    Strauch EM, Bernard SM, La D, Bohn AJ, Lee PS, Anderson CE, Nieusma T, Holstein CA, Garcia NK, Hooper KA, Ravichandran R, Nelson JW, Sheffler W, Bloom JD, Lee KK, Ward AB, Yager P, Fuller DH, Wilson IA, Baker D (2017) Computational design of trimeric influenza-neutralizing proteins targeting the hemagglutinin receptor binding site. Nat Biotechnol 35(7):667. CrossRefGoogle Scholar
  28. 28.
    Fallas JA, Ueda G, Sheffler W, Nguyen V, McNamara DE, Sankaran B, Pereira JH, Parmeggiani F, Brunette TJ, Cascio D, Yeates TR, Zwart P, Baker D (2017) Computational design of self-assembling cyclic protein homo-oligomers. Nat Chem 9(4):353–360. CrossRefGoogle Scholar
  29. 29.
    Bhardwaj G, Mulligan VK, Bahl CD, Gilmore JM, Harvey PJ, Cheneval O, Buchko GW, Pulavarti SVSRK., Kaas Q, Eletsky A, Huang PS, Johnsen WA, Greisen PJ, Rocklin GJ, Song YF, Linsky TW, Watkins A, Rettie SA, Xu XZ, Carter LP, Bonneau R, Olson JM, Coutsias E, Correnti CE, Szyperski T, Craik DJ, Baker D (2016) Accurate de novo design of hyperstable constrained peptides. Nature 538(7625):329. CrossRefGoogle Scholar
  30. 30.
    Schreiber G, Fleishman SJ (2013) Computational design of protein–protein interactions. Curr Opin Struc Biol 23(6):903–910. CrossRefGoogle Scholar
  31. 31.
    Lacerda SHD, Park JJ, Meuse C, Pristinski D, Becker ML, Karim A, Douglas JF (2010) Interaction of gold nanoparticles with common human blood proteins. ACS Nano 4(1):365–379. CrossRefGoogle Scholar
  32. 32.
    Engel MFM, van Mierlo CPM, Visser AJWG. (2002) Kinetic and structural characterization of adsorption-induced unfolding of bovine alpha-lactalbumin. J Biol Chem 277(13):10922–10930. CrossRefGoogle Scholar
  33. 33.
    Guinn EJ, Jagannathan B, Marqusee S (2015) Single-molecule chemo-mechanical unfolding reveals multiple transition state barriers in a small single-domain protein. Nat Commun. Google Scholar
  34. 34.
    Gershenson A, Gierasch LM, Pastore A, Radford SE (2014) Energy landscapes of functional proteins are inherently risky. Nat Chem Biol 10(11):884–891CrossRefGoogle Scholar
  35. 35.
    Sethuraman A, Vedantham G, Imoto T, Przybycien T, Belfort G (2004) Protein unfolding at interfaces: slow dynamics of alpha-helix to beta-sheet transition. Proteins 56(4):669–678. CrossRefGoogle Scholar
  36. 36.
    Cedervall T, Lynch I, Lindman S, Berggard T, Thulin E, Nilsson H, Dawson KA, Linse S (2007) Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci USA 104(7):2050–2055. CrossRefGoogle Scholar
  37. 37.
    Vaishanav SK, Chandraker K, Korram J, Nagwanshi R, Ghosh KK, Satnami ML (2016) Protein nanoparticle interaction: a spectrophotometric approach for adsorption kinetics and binding studies. J Mol Struct 1117:300–310. CrossRefGoogle Scholar
  38. 38.
    Milani S, Bombelli FB, Pitek AS, Dawson KA, Radler J (2012) Reversible versus irreversible binding of transferrin to polystyrene nanoparticles: soft and hard corona. ACS Nano 6(3):2532–2541. CrossRefGoogle Scholar
  39. 39.
    Roach P, Farrar D, Perry CC (2005) Interpretation of protein adsorption: surface-induced conformational changes. J Am Chem Soc 127(22):8168–8173. CrossRefGoogle Scholar
  40. 40.
    Lynch I, Salvati A, Dawson KA (2009) Protein–nanoparticle interactions what does the cell see?. Nat Nanotechnol 4(9):546–547CrossRefGoogle Scholar
  41. 41.
    Vroman L, Adams AL, Fischer GC, Munoz PC (1980) Interaction of high molecular-weight kininogen, factor-Xii, and fibrinogen in plasma at interfaces. Blood 55(1):156–159Google Scholar
  42. 42.
    Tenzer S, Docter D, Kuharev J, Musyanovych A, Fetz V, Hecht R, Schlenk F, Fischer D, Kiouptsi K, Reinhardt C, Landfester K, Schild H, Maskos M, Knauer SK, Stauber RH (2013) Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat Nanotechnol 8(10):772-U1000. CrossRefGoogle Scholar
  43. 43.
    Deng ZJ, Liang MT, Monteiro M, Toth I, Minchin RF (2011) Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation. Nat Nanotechnol 6(1):39–44. CrossRefGoogle Scholar
  44. 44.
    Fleischer CC, Payne CK (2014) Secondary structure of corona proteins determines the cell surface receptors used by nanoparticles. J Phys Chem B 118(49):14017–14026. CrossRefGoogle Scholar
  45. 45.
    Chakarova SD, Carlsson AE (2004) Model study of protein unfolding by interfaces. Phys Rev E. Google Scholar
  46. 46.
    Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorn I, Huang ZW, Fletterick RJ, Cohen FE, Prusiner SB (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 90(23):10962–10966. CrossRefGoogle Scholar
  47. 47.
    Surewicz WK, Mantsch HH, Chapman D (1993) Determination of protein secondary structure by Fourier-transform infrared-spectroscopy: a critical-assessment. Biochemistry 32(2):389–394. CrossRefGoogle Scholar
  48. 48.
    Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287(2):252–260. CrossRefGoogle Scholar
  49. 49.
    Jackson M, Mantsch HH (1995) The use and misuse of FTIR spectroscopy in the determination of protein-structure. Crit Rev Biochem Mol 30(2):95–120. CrossRefGoogle Scholar
  50. 50.
    Banuelos S, Muga A (1995) Binding of molten globule-like conformations to lipid bilayers: structure of native and partially folded alpha-lactalbumin bound to model membranes. J Biol Chem 270(50):29910–29915CrossRefGoogle Scholar
  51. 51.
    Lala AK, Kaul P, Ratnam PB (1995) Membrane–protein interaction and the molten globule state: interaction of alpha-lactalbumin with membranes. J Protein Chem 14(7):601–609. CrossRefGoogle Scholar
  52. 52.
    Dyson HJ, Wright PE (2004) Unfolded proteins and protein folding studied by NMR. Chem Rev 104(8):3607–3622. CrossRefGoogle Scholar
  53. 53.
    Halskau O, Froystein NA, Muga A, Martinez A (2002) The membrane-bound conformation of alpha-lactalbumin studied by NMR-monitored 1H exchange. J Mol Biol 321(1):99–110CrossRefGoogle Scholar
  54. 54.
    Engel MFM, Visser AJWG., van Mierlo CPM (2004) Conformation and orientation of a protein folding intermediate trapped by adsorption. Proc Natl Acad Sci USA 101(31):11316–11321. CrossRefGoogle Scholar
  55. 55.
    Keating CD, Kovaleski KM, Natan MJ (1998) Protein: colloid conjugates for surface enhanced Raman scattering: stability and control of protein orientation. J Phys Chem B 102(47):9404–9413. CrossRefGoogle Scholar
  56. 56.
    Yu QM, Golden G (2007) Probing the protein orientation on charged self-assembled monolayers on gold nanohole arrays by SERS. Langmuir 23(17):8659–8662. CrossRefGoogle Scholar
  57. 57.
    Kelly PM, Aberg C, Polo E, O’Connell A, Cookman J, Fallon J, Krpetic Z, Dawson KA (2015) Mapping protein binding sites on the biomolecular corona of nanoparticles. Nat Nanotechnol 10(5):472–479. CrossRefGoogle Scholar
  58. 58.
    Monopoli MP, Aberg C, Salvati A, Dawson KA (2012) Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol 7(12):779–786. CrossRefGoogle Scholar
  59. 59.
    Pisani C, Gaillard JC, Odorico M, Nyalosaso JL, Charnay C, Guari Y, Chopineau J, Devoisselle JM, Armengaud J, Prat O (2017) The timeline of corona formation around silica nanocarriers highlights the role of the protein interactome. Nanoscale 9(5):1840–1851. CrossRefGoogle Scholar
  60. 60.
    Schottler S, Becker G, Winzen S, Steinbach T, Mohr K, Landfester K, Mailander V, Wurm FR (2016) Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers. Nat Nanotechnol 11(4):372–377. CrossRefGoogle Scholar
  61. 61.
    Wan S, Kelly PM, Mahon E, Stockmann H, Rudd PM, Caruso F, Dawson KA, Yan Y, Monopoli MP (2015) The “Sweet” side of the protein corona: effects of glycosylation on nanoparticle-cell interactions. ACS Nano 9(2):2157–2166. CrossRefGoogle Scholar
  62. 62.
    Naik RR, Brott LL, Clarson SJ, Stone MO (2002) Silica-precipitating peptides isolated from a combinatorial phage display peptide library. J Nanosci Nanotechnol 2(1):95–100. CrossRefGoogle Scholar
  63. 63.
    Braun R, Sarikaya M, Schulten K (2002) Genetically engineered gold-binding polypeptides: structure prediction and molecular dynamics. J Biomat Sci Polym E 13(7):747–757. CrossRefGoogle Scholar
  64. 64.
    Sarikaya M, Tamerler C, Jen AKY, Schulten K, Baneyx F (2003) Molecular biomimetics: nanotechnology through biology. Nat Mater 2(9):577–585. CrossRefGoogle Scholar
  65. 65.
    Willett RL, Baldwin KW, West KW, Pfeiffer LN (2005) Differential adhesion of amino acids to inorganic surfaces. Proc Natl Acad Sci USA 102(22):7817–7822. CrossRefGoogle Scholar
  66. 66.
    Puddu V, Perry CC (2012) Peptide adsorption on silica nanoparticles: evidence of hydrophobic interactions. ACS Nano 6(7):6356–6363. CrossRefGoogle Scholar
  67. 67.
    Atanasoska LL, Buchholz JC, Somorjai GA (1978) Low-energy electron-diffraction study of surface-structures of adsorbed amino-acid monolayers and ordered films deposited on copper crystal surfaces. Surf Sci 72(1):189–207CrossRefGoogle Scholar
  68. 68.
    Zhao XY, Gai Z, Zhao RG, Yang WS (1999) Adsorption structures of glycine on Cu (001). Acta Phys Sin Chin Ed 48(1):94–101Google Scholar
  69. 69.
    Wang H, Zhao XY, Yang WS (2000) Adsorption of aspartic acid on Cu (001) studied by scanning tunneling microscopy. Acta Phys Sin Chin Ed 49(7):1316–1320Google Scholar
  70. 70.
    Wang H, Zhao XY, Zhao RG, Yang WS (2001) Adsorption of l-phenylalanine on Cu (001). Chin Phys Lett 18(3):445–448CrossRefGoogle Scholar
  71. 71.
    Yan H, Zhao XY, Zhao RG, Yang WS (2001) Adsorption of glycine on Cu (111) investigated by scanning tunneling microscopy. Acta Phys Sin Chin Ed 50(10):1964–1969Google Scholar
  72. 72.
    Kuhnle A, Linderoth TR, Hammer B, Besenbacher F (2002) Chiral recognition in dimerization of adsorbed cysteine observed by scanning tunnelling microscopy. Nature 415(6874):891–893. CrossRefGoogle Scholar
  73. 73.
    Lingenfelder M, Tomba G, Costantini G, Ciacchi LC, De Vita A, Kern K (2007) Tracking the chiral recognition of adsorbed dipeptides at the single-molecule level. Angew Chem Int Ed 46(24):4492–4495. CrossRefGoogle Scholar
  74. 74.
    Mao XB, Wang YB, Liu L, Niu L, Yang YL, Wang C (2009) Molecular-level evidence of the surface-induced transformation of peptide structures revealed by scanning tunneling microscopy. Langmuir 25(16):8849–8853. CrossRefGoogle Scholar
  75. 75.
    Tanaka H, Kawai T (2009) Partial sequencing of a single DNA molecule with a scanning tunnelling microscope. Nat Nanotechnol 4(8):518–522. CrossRefGoogle Scholar
  76. 76.
    Mao XB, Guo YY, Luo Y, Niu L, Liu L, Ma XJ, Wang HB, Yang YL, Wei GH, Wang C (2013) Sequence effects on peptide assembly characteristics observed by using scanning tunneling microscopy. J Am Chem Soc 135(6):2181–2187. CrossRefGoogle Scholar
  77. 77.
    Guo YY, Hou JF, Zhang XM, Yang YL, Wang C (2017) Stabilization effect of amino acid side chains in peptide assemblies on graphite studied by scanning tunneling microscopy. Chemphyschem 18(8):926–934. CrossRefGoogle Scholar
  78. 78.
    Xu B, Yin SX, Wang C, Zeng QD, Qiu XH, Bai CL (2001) Identification of hydrogen bond characterizations of isomeric 4Bpy and 2Bpy by STM. Surf Interface Anal 32(1):245–247. CrossRefGoogle Scholar
  79. 79.
    Westermark P, Engstrom U, Johnson KH, Westermark GT, Betsholtz C (1990) Islet amyloid polypeptide: pinpointing amino-acid-residues linked to amyloid fibril formation. Proc Natl Acad Sci USA 87(13):5036–5040CrossRefGoogle Scholar
  80. 80.
    Balbirnie M, Grothe R, Eisenberg DS (2001) An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated beta-sheet structure for amyloid. Proc Natl Acad Sci USA 98(5):2375–2380CrossRefGoogle Scholar
  81. 81.
    Gazit E (2005) Mechanisms of amyloid fibril self-assembly and inhibition. FEBS J 272(23):5971–5978CrossRefGoogle Scholar
  82. 82.
    Xu M, Zhu L, Liu JH, Yang YL, Wu JY, Wang C (2013) Characterization of beta-domains in C-terminal fragments of TDP-43 by scanning tunneling microscopy. J Struct Biol 181(1):11–16. CrossRefGoogle Scholar
  83. 83.
    Yu LL, Sun ZY, Yu Y, Qu FY, Yang YL, Li YM, Wang C (2016) Molecular evidence of glycosylation effect on the peptide assemblies identified with scanning tunneling microscopy. J Phys Chem C 120(12):6577–6582. CrossRefGoogle Scholar
  84. 84.
    Qu FY, Yu LL, Xie HY, Zheng YF, Xu J, Zou YM, Yang YL, Wang C (2017) Studies on composition and sequence effects in surface-mediated octapeptide assemblies by using scanning tunneling microscopy. J Phys Chem C 121(19):10364–10369. CrossRefGoogle Scholar
  85. 85.
    Wang CX, Mao XB, Yang AH, Niu L, Wang SN, Li DH, Guo YY, Wang YB, Yang YL, Wang C (2011) Determination of relative binding affinities of labeling molecules with amino acids by using scanning tunneling microscopy. Chem Commun 47(38):10638–10640. CrossRefGoogle Scholar
  86. 86.
    Mao XB, Wang CX, Ma XJ, Zhang M, Liu L, Zhang L, Niu L, Zeng QD, Yang YL, Wang C (2011) Molecular level studies on binding modes of labeling molecules with polyalanine peptides. Nanoscale 3(4):1592–1599. CrossRefGoogle Scholar
  87. 87.
    Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, Apostol MI, Thompson MJ, Balbirnie M, Wiltzius JJW, McFarlane HT, Madsen AO, Riekel C, Eisenberg D (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447(7143):453–457. CrossRefGoogle Scholar
  88. 88.
    Hilbich C, Kisterswoike B, Reed J, Masters CL, Beyreuther K (1992) Substitutions of hydrophobic amino-acids reduce the amyloidogenicity of Alzheimers-disease beta-A4 peptides. J Mol Biol 228(2):460–473. CrossRefGoogle Scholar
  89. 89.
    Kim HJ, Kim NC, Wang YD, Scarborough EA, Moore J, Diaz Z, MacLea KS, Freibaum B, Li SQ, Molliex A, Kanagaraj AP, Carter R, Boylan KB, Wojtas AM, Rademakers R, Pinkus JL, Greenberg SA, Trojanowski JQ, Traynor BJ, Smith BN, Topp S, Gkazi AS, Miller J, Shaw CE, Kottlors M, Kirschner J, Pestronk A, Li YR, Ford AF, Gitler AD, Benatar M, King OD, Kimonis VE, Ross ED, Weihl CC, Shorter J, Taylor JP (2013) Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495(7442):467. CrossRefGoogle Scholar
  90. 90.
    Molliex A, Temirov J, Lee J, Coughlin M, Kanagaraj AP, Kim HJ, Mittag T, Taylor JP (2015) Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163(1):123–133. CrossRefGoogle Scholar
  91. 91.
    Lee KH, Zhang PP, Kim HJ, Mitrea DM, Sarkar M, Freibaum BD, Cika J, Coughlin M, Messing J, Molliex A, Maxwell BA, Kim NC, Temirov J, Moore J, Kolaitis RM, Shaw TI, Bai B, Peng JM, Kriwacki RW, Taylor JP (2016) C9orf72 dipeptide repeats impair the assembly, dynamics, and function of membrane-less organelles. Cell 167(3):774. CrossRefGoogle Scholar
  92. 92.
    Ott W, Jobst MA, Bauer MS, Durner E, Milles LF, Nash MA, Gaub HE (2017) Elastin-like polypeptide linkers for single-molecule force spectroscopy. ACS Nano 11(6):6346–6354. CrossRefGoogle Scholar
  93. 93.
    Schwierz N, Horinek D, Liese S, Pirzer T, Balzer BN, Hugel T, Netz RR (2012) On the relationship between peptide adsorption resistance and surface contact angle: a combined experimental and simulation single-molecule study. J Am Chem Soc 134(48):19628–19638. CrossRefGoogle Scholar
  94. 94.
    Krysiak S, Liese S, Netz RR, Hugel T (2014) Peptide desorption kinetics from single molecule force spectroscopy studies. J Am Chem Soc 136(2):688–697. CrossRefGoogle Scholar
  95. 95.
    Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276(5315):1109–1112. CrossRefGoogle Scholar
  96. 96.
    Merkel R, Nassoy P, Leung A, Ritchie K, Evans E (1999) Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy. Nature 397(6714):50–53CrossRefGoogle Scholar
  97. 97.
    MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102(18):3586–3616CrossRefGoogle Scholar
  98. 98.
    Robison AD, Sun S, Poyton MF, Johnson GA, Pellois JP, Jungwirth P, Vazdar M, Cremer PS (2016) Polyarginine interacts more strongly and cooperatively than polylysine with phospholipid bilayers. J Phys Chem B 120(35):9287–9296. CrossRefGoogle Scholar
  99. 99.
    Seo J, Hoffmann W, Warnke S, Huang X, Gewinner S, Schollkopf W, Bowers MT, von Helden G, Pagel K (2017) An infrared spectroscopy approach to follow beta-sheet formation in peptide amyloid assemblies. Nat Chem 9(1):39–44. Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.CAS Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, CAS Key Laboratory of Standardization and Measurement for Nanotechnology, CAS Center for Excellence in Nanoscience, CAS Center for Excellence in Brain ScienceNational Center for Nanoscience and TechnologyBeijingPeople’s Republic of China
  2. 2.Sino-Danish CenterUniversity of Chinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.Department of ChemistryTsinghua UniversityBeijingPeople’s Republic of China
  4. 4.University of Chinese Academy of SciencesBeijingPeople’s Republic of China

Personalised recommendations