Molecular interactions of melatonin with lipid rafts
Vibrational and structural patterns of biomembranes in the presence of melatonin
Keywords:
lipid rafts, phospholipid membranes, melatonin, molecular interactions, structure, dynamics
Abstract
Biological membranes are composed of a lipid bilayer with a heterogeneous structure and complex dynamics, both of which can be modulated by the presence of melatonin. The lateral heterogeneities in lipid bilayers, also known as lipid rafts, have unique molecular interactions with melatonin, which we review here. Specifically, we discuss the molecular-level, physicochemical influences of melatonin on dynamics of lipid rafts and their structural properties, including melatonin’s propensity to preserve the structural integrity of lipid rafts at different length scales, as revealed through a range of experimental techniques and theoretical approaches.
References
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31. Lingwood D, Kaiser HJ, Levental I, Simons K (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. Trans. 37 (5): 955–960.
32. Kinnun JJ, Bolmatov D, Lavrentovich MO, Katsaras J (2020) Lateral heterogeneity and domain formation in cellular membranes. Chem. Phys. Lipids 232: 104976.
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36. Schick M (2012) Membrane heterogeneity: Manifestation of a curvature-induced microemulsion. Phys. Rev. E 85: 031902.
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40. Camley BA, Brown FLH (2010) Dynamic simulations of multicomponent lipid membranes over long length and time scales. Phys. Rev. Lett. 105: 148102.
41. Zhiliakov A, Wang Y, Quaini A, Olshanskii M, Majd S (2021) Experimental validation of a phase-field model to predict coarsening dynamics of lipid domains in multicomponent mem- branes. Biochim. Biophys. Acta Biomembranes. 1863: 183446.
42. Bolmatov D, Carillo JMY, Katsaras J, Lavrentovich MO (2020) Double membrane formation in heterogeneous vesicles. Soft Matter 16: 8806–8817.
43. Leibler S, Andelman D (1987) Ordered and curved meso-structures in membranes and amphiphilic films. J. Phys. France 48 (11): 2013–2018.
44. Allender DW, Schick M (2020) Recent experiments support a microemulsion origin of plasma membrane domains: Dependence of domain size on physical parameters. Membranes 10: 167.
45. Bolmatov D, et al. (2019) Deciphering melatonin-stabilized phase separation in phospholipid bilayers. Langmuir 35 (37): 12236–12245.
46. Bolmatov D, et al. (2020) Molecular picture of the transient nature of lipid rafts. Langmuir
36 (18):4887–4896.
47. Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc. Natl. Acad. Sci. U.S.A. 111 (22): 7898–7905.
48. Teng J, Loukin S, Anishkin A, Kung C (2015) The force-from-lipid (ffl) principle of mechanosensitivity, at large and in elements. Pflgers Arch. 467 (1): 27–37.
49. Reddy B, Bavi N, Lu A, Park Y, Perozo E (2019) Molecular basis of force-from-lipids gating in the mechanosensitive channel mscs. Elife 8: e50486.
50. Zhernenkov M, et al. (2016) Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations. Nat. Commun. 7: 11575.
51. Bolmatov D, Trachenko K (2011) Liquid heat capacity in the approach from the solid state: Anharmonic theory. Phys. Rev. B 84 (5): 054106.
52. Bolmatov D, Brazhkin V, Trachenko K (2012) The phonon theory of liquid thermodynamics.
Sci. Rep. 2: 421.
53. Bolmatov D, Zavyalov D, Zhernenkov M, Musaev ET, Cai YQ (2015) Unified phonon-based approach to the thermodynamics of solid, liquid and gas states. Ann. Phys. 363: 221–242.
54. Bolmatov D, Musaev ET, Trachenko K (2013) Symmetry breaking gives rise to energy spectra of three states of matter. Sci. Rep. 3 (1): 1–4.
55. Bolmatov D, Cai YQ, Zavyalov D, Zhernenkov M (2018) Crossover from picosecond collective to single particle dynamics defines the mechanism of lateral lipid diffusion. Biochim. Biophys. Acta Biomembranes. 1860 (11): 2446–2455.
56. Reiter RJ, Tan DX, Galano A (2014) Melatonin reduces lipid peroxidation and membrane viscosity. Front. Psychol. 5: 377.
57. Soloviov D, et al. (2020) Functional lipid pairs as building blocks of phase-separated mem- branes. Proc. Natl. Acad. Sci. U.S.A. 117: 4749–4757.
58. Bolmatov D, et al. (2018) Anomalous nanoscale optoacoustic phonon mixing in nematic meso- gens. J. Phys. Chem. Lett. 9 (10): 2546–2553.
59. S¸opu D, Kotakoski J, Albe K (2011) Finite-size effects in the phonon density of states of nanostructured germanium: A comparative study of nanoparticles, nanocrystals, nanoglasses, and bulk phases. Phys. Rev. B 83 (24): 245416.
60. Ouweneel AB, Thomas MJ, Sorci-Thomas MG (2020) The ins and outs of lipid rafts: functions in intracellular cholesterol homeostasis, microparticles, and cell membranes. J. Lipid Res. 61 (5): P676-686.
61. Hevia D, Sainz RM, Blanco D, Quirós I, Tan D-X, Rodríguez C, Mayo JC (2008) Melatonin uptake in prostate cancer cells: intracellular transport versus simple passive diffusion J. Pineal Res. 44 (3):247-2
2. Harayama T, Riezman H (2018) Understanding the diversity of membrane lipid composition.
Nat. Rev. Mol. Cell Biol. 19: 281–296.
3. Lu H, Marti J (2020) Cellular absorption of small molecules: free energy landscapes of mela- tonin binding at phospholipid membranes. Sci. Rep. 10 (1): 1–12.
4. Elisi GM, et al. (2020) Chiral recognition of flexible melatonin receptor ligands induced by conformational equilibria. Molecules 25 (18): 4057.
5. Hu Z, Marti J, Lu H (2021) Structure of benzothiadiazine at zwitterionic phospholipid cell membranes. J. Chem. Phys. 155 (15): 154303.
6. Banerjee A, Chattopadhyay A, Bandyopadhyay D (2021) Melatonin and biological membrane bilayers: a never ending amity. Melatonin Res. 4 (2): 232–252.
7. Lu H, Mart´ı J (2019) Binding and dynamics of melatonin at the interface of phosphatidylcholine-cholesterol membranes. PloS One 14 (11): e0224624.
8. Loh D, Reiter RJ (2021) Melatonin: regulation of biomolecular condensates in neurodegenerative disorders. Antioxidants 10 (9): 1483.
9. Martı J, Lu H (2021) Microscopic interactions of melatonin, serotonin and tryptophan with zwitterionic phospholipid membranes. Int. J. Mol. Sci. 22 (6): 2842.
10. Vona R, Iessi E, Matarrese P (2021) Role of cholesterol and lipid rafts in cancer signaling. a promising therapeutic opportunity? Front. Cell Dev. Biol. 9: 468.
11. Bolmatov D, Zav’yalov D, Carrillo JM, Katsaras J (2020) Fractal boundaries underpin the 2d melting of biomimetic rafts. Biochim. Biophys. Acta (BBA)-Biomembranes 1862 (8): 183249.
12. Allen JA, Halverson-Tamboli RA, Rasenick MM (2007) Lipid raft microdomains and neuro- transmitter signaling. Nat. Rev. Neurosci. 8 (2): 128–140.
13. Hicks DA, Nalivaeva NN, Turner AJ (2012) Lipid rafts and Alzheimer’s disease: protein-lipid interactions and perturbation of signaling. Front. Psychol. 3: 189.
14. Kurniawan J, Ventrici J, Kittleson G, Kuhl TL (2017) Interaction forces between lipid rafts.
Langmuir 33 (1): 382–387.
15. Bolmatov D, Kinnun JJ, Katsaras J, Lavrentovich MO (2020) Phonon-mediated lipid raft formation in biological membranes. Chem. Phys. Lipids 232: 104979.
16. Ghysels A, et al. (2019) Permeability of membranes in the liquid ordered and liquid disordered phases. Nat. Commun. 10 (1): 1–12.
17. Smith MD, et al. (2020) Solvent-induced membrane stress in biofuel production: molecular insights from small-angle scattering and all-atom molecular dynamics simulations. Green Chemistry 22 (23): 8278–8288.
18. Bradley RP, Radhakrishnan R (2016) Curvature–undulation coupling as a basis for curvature sensing and generation in bilayer membranes. Proc. Natl. Acad. Sci. U.S.A. 113 (35): E5117– E5124.
19. Drolle E, et al. (2013) Effect of melatonin and cholesterol on the structure of dopc and dppc membranes. Biochim. Biophys. Acta (BBA)-Biomembranes 1828 (9): 2247–2254.
20. Choi Y, et al. (2014) Melatonin directly interacts with cholesterol and alleviates cholesterol effects in dipalmitoylphosphatidylcholine monolayers. Soft Matter 10 (1): 206–213.
21. Dies H, Cheung B, Tang J, Rheinst¨adter MC (2015) The organization of melatonin in lipid membranes. Biochim. Biophys. Acta (BBA)-Biomembranes 1848 (4): 1032–1040.
22. Postila PA, R´og T (2020) A perspective: active role of lipids in neurotransmitter dynamics.
Mol. Neurobiol. 57 (2): 910–925.
23. Josey BP, Heinrich F, Silin V, L¨osche M (2020) Association of model neurotransmitters with lipid bilayer membranes. Biophys. J. 118 (5): 1044–1057.
24. Nanqin M, Robinson M, David JH, Leonenko Z (2020) Melatonin alters fluid phase coexistence in POPC/DPPC/cholesterol membranes. Biophys. J. 119 (12): 2391–2402.
25. Bessone CD, et al. (2020) Neuroprotective effect of melatonin loaded in ethylcellulose nanopar- ticles applied topically in a retinal degeneration model in rabbits. Exp. Eye Res. 200: 108222.
26. Murugova T, et al. (2020) Structural changes introduced by cholesterol and melatonin to the model membranes mimicking preclinical conformational diseases. Gen. Physiol. Biophys 39 (2): 101-114.
27. S´anchez AB, Clares B, Rodr´ıguez-Lagunas MJ, F´abrega MJ, Calpena AC (2020) Study of melatonin as preventive agent of gastrointestinal damage induced by sodium diclofenac. Cells 9 (1): 180.
28. Zhang D, et al. (2021) Unravelling melatonins varied antioxidizing protection of membrane lipids determined by its spatial distribution. J. Phys. Chem. Lett. 12 (31):7387–7393.
29. Kuˇcerka N, Nieh MP, Katsaras J (2011) Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochim. Biophys. Acta (BBA)-Biomembranes 1808 (11): 2761–2771.
30. Kocic G, et al. (2017) Antioxidative, membrane protective and antiapoptotic effects of mela- tonin, in silico study of physico-chemical profile and efficiency of nanoliposome delivery com- pared to betaine. RSC Adv. 7 (3): 1271–1281.
31. Lingwood D, Kaiser HJ, Levental I, Simons K (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. Trans. 37 (5): 955–960.
32. Kinnun JJ, Bolmatov D, Lavrentovich MO, Katsaras J (2020) Lateral heterogeneity and domain formation in cellular membranes. Chem. Phys. Lipids 232: 104976.
33. Elson EL, Fried E, Dolbow JE, Genin GM (2010) Phase separation in biological membranes: Integration of theory and experiment. Annu. Rev. Biophys. 39: 207–226.
34. de Almeida RFM, Fedorov A, Prieto M (2003) Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: Boundaries and composition of lipid rafts. Biophys. J. 85 (4): 2406– 2416.
35. Heberle FA, et al. (2013) Bilayer thickness mismatch controls domain size in model membranes.
J. Am. Chem. Soc. 135 (18): 6853–6859.
36. Schick M (2012) Membrane heterogeneity: Manifestation of a curvature-induced microemulsion. Phys. Rev. E 85: 031902.
37. Veatch SL, et al. (2008) Critical fluctuations in plasma membrane vesicles. ACS Chem. Biol.
3 (5): 287–293.
38. Levental I, Levental KR, Heberle FA (2002) Lipids rafts: Controversies resolved, mysteries remain. Trends Cell Biol. 30 (5): 341–353.
39. Guyer JE, Wheeler D, Warren JA (2009) FiPy: Partial differential equations with python. Comput. Sci. Eng. 11 (3): 6-15.
40. Camley BA, Brown FLH (2010) Dynamic simulations of multicomponent lipid membranes over long length and time scales. Phys. Rev. Lett. 105: 148102.
41. Zhiliakov A, Wang Y, Quaini A, Olshanskii M, Majd S (2021) Experimental validation of a phase-field model to predict coarsening dynamics of lipid domains in multicomponent mem- branes. Biochim. Biophys. Acta Biomembranes. 1863: 183446.
42. Bolmatov D, Carillo JMY, Katsaras J, Lavrentovich MO (2020) Double membrane formation in heterogeneous vesicles. Soft Matter 16: 8806–8817.
43. Leibler S, Andelman D (1987) Ordered and curved meso-structures in membranes and amphiphilic films. J. Phys. France 48 (11): 2013–2018.
44. Allender DW, Schick M (2020) Recent experiments support a microemulsion origin of plasma membrane domains: Dependence of domain size on physical parameters. Membranes 10: 167.
45. Bolmatov D, et al. (2019) Deciphering melatonin-stabilized phase separation in phospholipid bilayers. Langmuir 35 (37): 12236–12245.
46. Bolmatov D, et al. (2020) Molecular picture of the transient nature of lipid rafts. Langmuir
36 (18):4887–4896.
47. Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc. Natl. Acad. Sci. U.S.A. 111 (22): 7898–7905.
48. Teng J, Loukin S, Anishkin A, Kung C (2015) The force-from-lipid (ffl) principle of mechanosensitivity, at large and in elements. Pflgers Arch. 467 (1): 27–37.
49. Reddy B, Bavi N, Lu A, Park Y, Perozo E (2019) Molecular basis of force-from-lipids gating in the mechanosensitive channel mscs. Elife 8: e50486.
50. Zhernenkov M, et al. (2016) Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations. Nat. Commun. 7: 11575.
51. Bolmatov D, Trachenko K (2011) Liquid heat capacity in the approach from the solid state: Anharmonic theory. Phys. Rev. B 84 (5): 054106.
52. Bolmatov D, Brazhkin V, Trachenko K (2012) The phonon theory of liquid thermodynamics.
Sci. Rep. 2: 421.
53. Bolmatov D, Zavyalov D, Zhernenkov M, Musaev ET, Cai YQ (2015) Unified phonon-based approach to the thermodynamics of solid, liquid and gas states. Ann. Phys. 363: 221–242.
54. Bolmatov D, Musaev ET, Trachenko K (2013) Symmetry breaking gives rise to energy spectra of three states of matter. Sci. Rep. 3 (1): 1–4.
55. Bolmatov D, Cai YQ, Zavyalov D, Zhernenkov M (2018) Crossover from picosecond collective to single particle dynamics defines the mechanism of lateral lipid diffusion. Biochim. Biophys. Acta Biomembranes. 1860 (11): 2446–2455.
56. Reiter RJ, Tan DX, Galano A (2014) Melatonin reduces lipid peroxidation and membrane viscosity. Front. Psychol. 5: 377.
57. Soloviov D, et al. (2020) Functional lipid pairs as building blocks of phase-separated mem- branes. Proc. Natl. Acad. Sci. U.S.A. 117: 4749–4757.
58. Bolmatov D, et al. (2018) Anomalous nanoscale optoacoustic phonon mixing in nematic meso- gens. J. Phys. Chem. Lett. 9 (10): 2546–2553.
59. S¸opu D, Kotakoski J, Albe K (2011) Finite-size effects in the phonon density of states of nanostructured germanium: A comparative study of nanoparticles, nanocrystals, nanoglasses, and bulk phases. Phys. Rev. B 83 (24): 245416.
60. Ouweneel AB, Thomas MJ, Sorci-Thomas MG (2020) The ins and outs of lipid rafts: functions in intracellular cholesterol homeostasis, microparticles, and cell membranes. J. Lipid Res. 61 (5): P676-686.
61. Hevia D, Sainz RM, Blanco D, Quirós I, Tan D-X, Rodríguez C, Mayo JC (2008) Melatonin uptake in prostate cancer cells: intracellular transport versus simple passive diffusion J. Pineal Res. 44 (3):247-2
Published
2022-06-30
How to Cite
[1]
Bolmatov, D., Lavrentovich, M. and Reiter, R. 2022. Molecular interactions of melatonin with lipid rafts. Melatonin Research. 5, 2 (Jun. 2022), 101-113. DOI:https://doi.org/https://doi.org/10.32794/mr112500123.
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