Dramatic morphological changes in liposomes induced by peptide nanofibers reversibly polymerized and depolymerized by the photoisomerization of spiropyran

Yingbing Liang; Shigesaburo Ogawa; Hiroshi Inaba; Kazunori Matsuura

doi:10.3389/fmolb.2023.1137885

Dramatic morphological changes in liposomes induced by peptide nanofibers reversibly polymerized and depolymerized by the photoisomerization of spiropyran

Front Mol Biosci. 2023 Mar 30:10:1137885. doi: 10.3389/fmolb.2023.1137885. eCollection 2023.

Authors

Yingbing Liang¹, Shigesaburo Ogawa¹, Hiroshi Inaba^{1

2}, Kazunori Matsuura^{1

2}

Affiliations

¹ Department of Chemistry and Biotechnology, Graduate School of Engineering Tottori University Koyama-Minami 4-101, Tottori, Japan.
² Centre for Research on Green Sustainable Chemistry Tottori University Koyama-Minami 4-101, Tottori, Japan.

Abstract

Cytoskeletons such as microtubules and actin filaments are natural protein assemblies, which dynamically control cellular morphology by reversible polymerization/depolymerization. Recently, the control of polymerization/depolymerization of fibrous protein/peptide assemblies by external stimuli has attracted significant attention. However, as far as we know, the creation of an "artificial cytoskeleton" that reversibly controls the polymerization/depolymerization of peptide nanofiber in giant unilamellar vesicles (GUVs) has not been reported. Here, we developed peptide nanofiber self-assembled from spiropyran (SP)-modified β-sheet-forming peptides, which can be reversibly polymerized/depolymerized by light. The reversible photoisomerization of the SP-modified peptide (FKFEC^SPKFE) to the merocyanine-peptide (FKFEC^MCKFE) by ultraviolet (UV) and visible light irradiation was confirmed by UV-visible spectroscopy. Confocal laser scanning microscopy with thioflavin T staining and transmission electron microscopy of the peptides showed that the SP-peptide formed β-sheet nanofibers, whereas the photoisomerization to the merocyanine-peptide almost completely dissociated the nanofibers. The merocyanine peptide was encapsulated in spherical GUVs comprising of phospholipids as artificial cell models. Interestingly, the morphology of GUV encapsulating the merocyanine-peptide dramatically changed into worm-like vesicles by the photoisomerization to the SP-modified peptide, and then reversibly changed into spherical GUV by the photoisomerization to the MC-modified peptide. These dynamic morphological changes in GUVs by light can be applied as components of a molecular robot with artificially controlled cellular functions.

Keywords: artificial cytoskeleton; liposome; merocyanine; peptide nanofiber; photoisomerization; polymerization/depolymerization; self-assembly; spiropyran.

Grants and funding

This research was supported by a Grant-in-Aid for Challenging Research (Exploratory) (JSPS KAKENHI Grant No. JP21K19008), Grant-in-Aid for Transformative Research Areas (A) “Molecular Cybernetics” (JSPS KAKENHI Grant number: JP20H05970), and ACT-X (Grant No. JPMJAX 2012) from the Japan Science and Technology Agency (JST).