Synthesis and characterization of chemically fueled supramolecular materials driven by carbodiimide-based fuels

Fabian Schnitter, Alexander M. Bergmann, Benjamin Winkeljann, Jennifer Rodon Fores, Oliver Lieleg, Job Boekhoven

Published: 2021-06-29 DOI: 10.1038/s41596-021-00563-9

Extended

Extended Data Fig. 1 Cryo-TEM microscope micrograph.

The control micrograph of a 10 mM precursor 2 stock solution excludes preassembly of the inactivated precursor in the absence of EDC fuel.

Extended Data Fig. 2 EDC hydrolysis and Fmoc deprotection kinetics.

a , b , The addition of the quenching solution freezes the reaction cycle of Fmoc-E-OH ( 1 ) ( a ) and Fmoc-AAD-OH ( 2 ) ( b ). In the timescale of the HPLC analysis, the degradation of EDC and Fmoc deprotection does not falsify the concentration determination.

Source data

Extended Data Fig. 3 The absorbance of light as a measure for turbidity.

a , Usage of different sample containers affects the measurement quality as sedimentation in a 96-well plate wrongly extends the system’s lifetime. b , Regarding colloids formed by 1 , a cuvette is a better choice as sample container.

Source data

Supplementary information

Reporting Summary

Supplementary Video 1

Macroscopic property of reaction cycle shown by evolution of turbidity

Supplementary Video 2

Macroscopic property of reaction cycle shown by evolution of a hydrogel

Generation of mouse–human chimeric embryos

Genome-wide quantification of transcription factor binding at single-DNA-molecule resolution using methyl-transferase footprinting

Generation of CRISPR–Cas9-mediated genetic knockout human intestinal tissue–derived enteroid lines by lentivirus transduction and single-cell cloning

A puromycin-dependent activity-based sensing probe for histochemical staining of hydrogen peroxide in cells and animal tissues

References

Extended
Supplementary information

Stupp, S. I. et al. Supramolecular materials: self-organized nanostructures. Science 276, 384–389 (1997).
Amabilino, D. B., Smith, D. K. & Steed, J. W. Supramolecular materials. Chem. Soc. Rev. 46, 2404–2420 (2017).
Zhou, J., Li, J., Du, X. & Xu, B. Supramolecular biofunctional materials. Biomaterials 129, 1–27 (2017).
Kato, T., Uchida, J., Ichikawa, T. & Soberats, B. Functional liquid-crystalline polymers and supramolecular liquid crystals. Polym. J. 50, 149–166 (2017).
Hegmann, T., Qi, H. & Marx, V. M. Nanoparticles in liquid crystals: synthesis, self-assembly, defect formation and potential applications. J. Inorg. Organomet. Polym. Mater. 17, 483–508 (2007).
Greaves, T. L. & Drummond, C. J. Ionic liquids as amphiphile self-assembly media. Chem. Soc. Rev. 37, 1709–1726 (2008).
de Greef, T. F. & Meijer, E. W. Materials science: supramolecular polymers. Nature 453, 171–173 (2008).
Aida, T., Meijer, E. W. & Stupp, S. I. Functional supramolecular polymers. Science 335, 813–817 (2012).
Weingarten, A. S. et al. Self-assembling hydrogel scaffolds for photocatalytic hydrogen production. Nat. Chem. 6, 964–970 (2014).
Grimaldi, N. et al. Lipid-based nanovesicles for nanomedicine. Chem. Soc. Rev. 45, 6520–6545 (2016).
Webber, M. J. & Langer, R. Drug delivery by supramolecular design. Chem. Soc. Rev. 46, 6600–6620 (2017).
Kadler, K. E., Holmes, D. F., Trotter, J. A. & Chapman, J. A. Collagen fibril formation. Biochem. J. 316, 1–11 (1996).
Zhu, J. & Kaufman, L. J. Collagen I self-assembly: revealing the developing structures that generate turbidity. Biophys. J. 106, 1822–1831 (2014).
Prockop, D. J. & Kivirikko, K. I. Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64, 403–434 (1995).
Zhao, B., Hu, H., Mandal, S. K. & Haddon, R. C. A bone mimic based on the self-assembly of hydroxyapatite on chemically functionalized single-walled carbon nanotubes. Chem. Mater. 17, 3235–3241 (2005).
Amendola, V. & Meneghetti, M. Self-healing at the nanoscale. Nanoscale 1, 74–88 (2009).
Tantakitti, F. et al. Energy landscapes and functions of supramolecular systems. Nat. Mater. 15, 469–476 (2016).
Lancia, F., Ryabchun, A. & Katsonis, N. Life-like motion driven by artificial molecular machines. Nat. Rev. Chem. 3, 536–551 (2019).
Needleman, D. & Dogic, Z. Active matter at the interface between materials science and cell biology. Nat. Rev. Mater. 2 (2017).
Korn, E., Carlier, M. & Pantaloni, D. Actin polymerization and ATP hydrolysis. Science 238, 638–644 (1987).
Desai, A. & Mitchison, T. J. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83–117 (1997).
Kohler, S., Schaller, V. & Bausch, A. R. Structure formation in active networks. Nat. Mater. 10, 462–468 (2011).
Boekhoven, J. et al. Dissipative self-assembly of a molecular gelator by using a chemical fuel. Angew. Chem. Int. Ed. Engl. 49, 4825–4828 (2010).
Boekhoven, J., Hendriksen, W. E., Koper, G. J., Eelkema, R. & van Esch, J. H. Transient assembly of active materials fueled by a chemical reaction. Science 349, 1075–1079 (2015).
van Esch, J. H., Klajn, R. & Otto, S. Chemical systems out of equilibrium. Chem. Soc. Rev. 46, 5474–5475 (2017).
Saha, B., Chatterjee, A., Reja, A. & Das, D. Condensates of short peptides and ATP for the temporal regulation of cytochrome c activity. Chem. Commun. 55, 14194–14197 (2019).
Post, E. A. J. & Fletcher, S. P. Dissipative self-assembly, competition and inhibition in a self-reproducing protocell model. Chem. Sci. 11, 9434–9442 (2020).
Deng, J. & Walther, A. Pathway complexity in fuel-driven DNA nanostructures with autonomous reconfiguration of multiple dynamic steady states. J. Am. Chem. Soc. 142, 685–689 (2020).
Cardona, M. A. & Prins, L. J. ATP-fuelled self-assembly to regulate chemical reactivity in the time domain. Chem. Sci. 11, 1518–1522 (2020).
Hossain, M. M., Atkinson, J. L. & Hartley, C. S. Dissipative assembly of macrocycles comprising multiple transient bonds. Angew. Chem. Int. Ed. Engl. 59, 13807–13813 (2020).
Bal, S., Ghosh, C., Ghosh, T., Vijayaraghavan, R. K. & Das, D. Non-equilibrium polymerization of cross-beta amyloid peptides for temporal control of electronic properties. Angew. Chem. Int. Ed. Engl. 59, 13506–13510 (2020).
Ragazzon, G. & Prins, L. J. Energy consumption in chemical fuel-driven self-assembly. Nat. Nanotechnol. 13, 882–889 (2018).
Astumian, R. D. Kinetic asymmetry allows macromolecular catalysts to drive an information ratchet. Nat. Commun. 10, 3837 (2019).
Maiti, S., Fortunati, I., Ferrante, C., Scrimin, P. & Prins, L. J. Dissipative self-assembly of vesicular nanoreactors. Nat. Chem. 8, 725–731 (2016).
van Ravensteijn, B. G. P., Hendriksen, W. E., Eelkema, R., van Esch, J. H. & Kegel, W. K. Fuel-mediated transient clustering of colloidal building blocks. J. Am. Chem. Soc. 139, 9763–9766 (2017).
Dambenieks, A. K., Vu, P. H. Q. & Fyles, T. M. Dissipative assembly of a membrane transport system. Chem. Sci. 5, 3396–3403 (2014).
Ogden, W.A. & Guan, Z. Redox chemical-fueled dissipative self-assembly of active materials. ChemSystemsChem http://doi.org/10.1002/syst.201900030 (2019).
Leira-Iglesias, J., Sorrenti, A., Sato, A., Dunne, P. A. & Hermans, T. M. Supramolecular pathway selection of perylenediimides mediated by chemical fuels. Chem. Commun. 52, 9009–9012 (2016).
Tena-Solsona, M. et al. Non-equilibrium dissipative supramolecular materials with a tunable lifetime. Nat. Commun. 8, 15895 (2017).
Kariyawasam, L. S. & Hartley, C. S. Dissipative assembly of aqueous carboxylic acid anhydrides fueled by carbodiimides. J. Am. Chem. Soc. 139, 11949–11955 (2017).
Dai, K. et al. Regulating chemically fueled peptide assemblies by molecular design. J. Am. Chem. Soc. 142, 14142–14149 (2020).
Riess, B. et al. Dissipative assemblies that inhibit their deactivation. Soft Matter 14, 4852–4859 (2018).
Grotsch, R. K. et al. Dissipative self-assembly of photoluminescent silicon nanocrystals. Angew. Chem. Int. Ed. Engl. 57, 14608–14612 (2018).
Grotsch, R. K. et al. Pathway dependence in the fuel-driven dissipative self-assembly of nanoparticles. J. Am. Chem. Soc. 141, 9872–9878 (2019).
Tena-Solsona, M., Wanzke, C., Riess, B., Bausch, A. R. & Boekhoven, J. Self-selection of dissipative assemblies driven by primitive chemical reaction networks. Nat. Commun. 9, 2044 (2018).
Wanzke, C., Tena-Solsona, M., Rieß, B., Tebcharani, L. & Boekhoven, J. Active droplets in a hydrogel release drugs with a constant and tunable rate. Mater. Horiz. 7, 1397–1403 (2020).
Donau, C. et al. Active coacervate droplets as a model for membraneless organelles and protocells. Nat. Commun. 11, 5167 (2020).
Kriebisch, B. A. K. et al. Reciprocal coupling in chemically fueled assembly: a reaction cycle regulates self-assembly and vice versa. J. Am. Chem. Soc. 142, 20837–20844 (2020).
Panja, S., Dietrich, B. & Adams, D. J. Chemically fuelled self-regulating gel-to-gel transition. ChemSystemsChem http://doi.org/10.1002/syst.201900038 (2019).
Bal, S., Das, K., Ahmed, S. & Das, D. Chemically fueled dissipative self-assembly that exploits cooperative catalysis. Angew. Chem. Int. Ed. Engl. 58, 244–247 (2019).
Coin, I., Beyermann, M. & Bienert, M. Solid-phase peptide synthesis: from standard procedures to the synthesis of difficult sequences. Nat. Protoc. 2, 3247–3256 (2007).
Chung, B. K. W., White, C. J. & Yudin, A. K. Solid-phase synthesis, cyclization, and site-specific functionalization of aziridine-containing tetrapeptides. Nat. Protoc. 12, 1277–1287 (2017).
Murray, J. K. & Gellman, S. H. Parallel synthesis of peptide libraries using microwave irradiation. Nat. Protoc. 2, 624–631 (2007).
Sackett, D. L. & Wolff, J. Nile red as a polarity-sensitive fluorescent probe of hydrophobic protein surfaces. Anal. Biochem. 167, 228–234 (1987).
Stuart, M. C. A., van de Pas, J. C. & Engberts, J. B. F. N. The use of Nile Red to monitor the aggregation behavior in ternary surfactant-water-organic solvent systems. J. Phys. Org. Chem. 18, 929–934 (2005).
Schnitter, F. & Boekhoven, J. A method to quench carbodiimide-fueled self-assembly. ChemSystemsChem http://doi.org/10.1002/syst.202000037 (2020).
Draper, E. R. & Adams, D. J. Low-molecular-weight gels: the state of the art. Chem 3, 390–410 (2017).
Greenspan, P., Mayer, E. P. & Fowler, S. D. Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 100, 965–973 (1985).
Nakajima, N. & Ikada, Y. Mechanism of amide formation by carbodiimide for bioconjugation in aqueous media. Bioconjug. Chem. 6, 123–130 (1995).
Goodling, K., Johnson, K., Lefkowitz, L. & Williams, B. W. The modern student laboratory: luminescent characterization of sodium dodecyl sulfate micellar solution properties. J. Chem. Educ. 71, A8 (1994).
Brown, P. R. Effect of flow rates and the slope of the linear concentration gradient on peak areas in high pressure liquid chromatography. J. Chromatogr. A 57, 383–390 (1971).