Nanostructural and Nanomechanical Alterations of Photosensitized Lipid Membranes Due to Light Induced Formation of Reactive Oxygen Species

Overview

Journal Sci Rep

Specialty Science

Date 2025 Jan 2

PMID 39747172

Authors

Adam Zolcsak

Balint Kiss

Tamas Bozo

Judit Somkuti

Istvan Vona

Miklos Kellermayer

Levente Herenyi

Affiliations

Soon will be listed here.

Abstract

Photosensitization has a wide range of applications in vastly distant fields. Three key components must be present at the same time to trigger the related photodynamic effect: light, the photosensitizer (PS) and oxygen. Irradiating the sensitizer leads to the formation of reactive oxygen species (ROS). Since PSs are accumulated preferably in lipid membranes, the study of photoinduced damage to membrane lipids can greatly increase our understanding of the effect of ROS on membranes in pathological as well as therapeutic conditions. We aimed to characterize the topographical and nanomechanical changes in supported lipid bilayers (SLBs) evoked by light-induced ROS formation. SLBs were prepared on mica surfaces by deposition of liposomes containing unsaturated lipid components. Topographical changes of SLBs were imaged by atomic force microscopy (AFM), and ROS-induced nanomechanical alterations of the membranes were assessed by AFM force measurements. To shed light on chemical alterations of the membrane constituents, infrared spectra were recorded. In the AFM images of porphyrin-containing membranes nanoscopic, bilayer-spanning holes were detected after irradiation. The measured rupture forces increased as a result of irradiation. These phenomena did not occur in membranes lacking unsaturated lipid components, emphasizing their role in ROS-mediated disruption confirmed by infrared spectroscopy results.

References

Akimov S, Volynsky P, Galimzyanov T, Kuzmin P, Pavlov K, Batishchev O . Pore formation in lipid membrane I: Continuous reversible trajectory from intact bilayer through hydrophobic defect to transversal pore. Sci Rep. 2017; 7(1):12152. PMC: 5610326. DOI: 10.1038/s41598-017-12127-7. View

Kiss B, Bozo T, Mudra D, Tordai H, Herenyi L, Kellermayer M . Development, structure and mechanics of a synthetic outer membrane model. Nanoscale Adv. 2022; 3(3):755-766. PMC: 9418885. DOI: 10.1039/d0na00977f. View

Jurak M, Mroczka R, Lopucki R . Properties of Artificial Phospholipid Membranes Containing Lauryl Gallate or Cholesterol. J Membr Biol. 2018; 251(2):277-294. PMC: 5910520. DOI: 10.1007/s00232-018-0025-z. View

Veres D, Bocskei-Antal B, Voszka I, Modos K, Csik G, Kaposi A . Comparison of binding ability and location of two mesoporphyrin derivatives in liposomes explored with conventional and site-selective fluorescence spectroscopy. J Phys Chem B. 2012; 116(32):9644-52. DOI: 10.1021/jp304712n. View

Frentrup H, Allen M . Error in dynamic spring constant calibration of atomic force microscope probes due to nonuniform cantilevers. Nanotechnology. 2011; 22(29):295703. DOI: 10.1088/0957-4484/22/29/295703. View

Kurokawa H, Ito H, Matsui H . Porphylipoprotein Accumulation and Porphylipoprotein Photodynamic Therapy Effects Involving Cancer Cell-Specific Cytotoxicity. Int J Mol Sci. 2021; 22(14). PMC: 8305091. DOI: 10.3390/ijms22147306. View

Johnson G, Ellis E, Kim H, Muthukrishnan N, Snavely T, Pellois J . Photoinduced membrane damage of E. coli and S. aureus by the photosensitizer-antimicrobial peptide conjugate eosin-(KLAKLAK)2. PLoS One. 2014; 9(3):e91220. PMC: 3946741. DOI: 10.1371/journal.pone.0091220. View

Baumann R, Penketh P, Seow H, Shyam K, Sartorelli A . Generation of oxygen deficiency in cell culture using a two-enzyme system to evaluate agents targeting hypoxic tumor cells. Radiat Res. 2008; 170(5):651-60. PMC: 2667281. DOI: 10.1667/RR1431.1. View

Butt H, Franz V . Rupture of molecular thin films observed in atomic force microscopy. I. Theory. Phys Rev E Stat Nonlin Soft Matter Phys. 2002; 66(3 Pt 1):031601. DOI: 10.1103/PhysRevE.66.031601. View

10.

Attwood S, Choi Y, Leonenko Z . Preparation of DOPC and DPPC Supported Planar Lipid Bilayers for Atomic Force Microscopy and Atomic Force Spectroscopy. Int J Mol Sci. 2013; 14(2):3514-39. PMC: 3588056. DOI: 10.3390/ijms14023514. View

11.

Cunill-Semanat E, Salgado J . Spontaneous and Stress-Induced Pore Formation in Membranes: Theory, Experiments and Simulations. J Membr Biol. 2019; 252(4-5):241-260. DOI: 10.1007/s00232-019-00083-4. View

12.

Lindblom G, Oradd G . Lipid lateral diffusion and membrane heterogeneity. Biochim Biophys Acta. 2008; 1788(1):234-44. DOI: 10.1016/j.bbamem.2008.08.016. View

13.

Bacellar I, Oliveira M, Dantas L, Costa E, Junqueira H, Martins W . Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids. J Am Chem Soc. 2018; 140(30):9606-9615. DOI: 10.1021/jacs.8b05014. View

14.

Baptista M, Cadet J, Greer A, Thomas A . Photosensitization Reactions of Biomolecules: Definition, Targets and Mechanisms. Photochem Photobiol. 2021; 97(6):1456-1483. DOI: 10.1111/php.13470. View

15.

Oleszko A, Olsztynska-Janus S, Walski T, Grzeszczuk-Kuc K, Bujok J, Galecka K . Application of FTIR-ATR Spectroscopy to Determine the Extent of Lipid Peroxidation in Plasma during Haemodialysis. Biomed Res Int. 2015; 2015:245607. PMC: 4417580. DOI: 10.1155/2015/245607. View

16.

Sokolov V, Batishchev O, Akimov S, Galimzyanov T, Konstantinova A, Malingriaux E . Residence time of singlet oxygen in membranes. Sci Rep. 2018; 8(1):14000. PMC: 6143606. DOI: 10.1038/s41598-018-31901-9. View

17.

Maekawa T, Chin H, Nyu T, Sut T, Ferhan A, Hayashi T . Molecular diffusion and nano-mechanical properties of multi-phase supported lipid bilayers. Phys Chem Chem Phys. 2019; 21(30):16686-16693. DOI: 10.1039/c9cp02085c. View

18.

Herenyi L, Veres D, Bekasi S, Voszka I, Modos K, Csik G . Location of mesoporphyrin in liposomes determined by site-selective fluorescence spectroscopy. J Phys Chem B. 2009; 113(21):7716-24. DOI: 10.1021/jp9022184. View

19.

Kim J, Santos O, Park J . Selective photosensitizer delivery into plasma membrane for effective photodynamic therapy. J Control Release. 2014; 191:98-104. DOI: 10.1016/j.jconrel.2014.05.049. View

20.

Ytzhak S, Weitman H, Ehrenberg B . The effect of lipid composition on the permeability of fluorescent markers from photosensitized membranes. Photochem Photobiol. 2013; 89(3):619-24. DOI: 10.1111/php.12035. View