Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model Membranes

Phase separation is essential for membrane function, and alterations in phase coexistence by membrane-interacting molecules, such as nicotine, can impair membrane stability. With the increasing use of e-cigarettes, concerns have arisen about the impact of nicotine on pulmonary surfactants. Here, we...

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Main Authors: Fadi S. S. Magalhães, Ernanni D. Vieira, Mariana R. B. Batista, Antonio J. Costa-Filho, Luis G. M. Basso
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Membranes
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Online Access:https://www.mdpi.com/2077-0375/14/12/267
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author Fadi S. S. Magalhães
Ernanni D. Vieira
Mariana R. B. Batista
Antonio J. Costa-Filho
Luis G. M. Basso
author_facet Fadi S. S. Magalhães
Ernanni D. Vieira
Mariana R. B. Batista
Antonio J. Costa-Filho
Luis G. M. Basso
author_sort Fadi S. S. Magalhães
collection DOAJ
description Phase separation is essential for membrane function, and alterations in phase coexistence by membrane-interacting molecules, such as nicotine, can impair membrane stability. With the increasing use of e-cigarettes, concerns have arisen about the impact of nicotine on pulmonary surfactants. Here, we used differential scanning calorimetry (DSC), molecular dynamics (MD) simulations, and electron spin resonance (ESR) to examine nicotine’s effect on the phase coexistence of two surfactant models: pure DPPC and a DPPC/POPC/POPG mixture. Our DSC analysis revealed that nicotine interacts with both membranes, increasing enthalpy and entropy change during the phase transition. ESR revealed that nicotine affects membrane fluidity and packing of DPPC more effectively than the ternary mixture, especially near the surface. MD simulations showed that neutral nicotine resides in the mid-plane, while protonated nicotine remains near the surface. Nicotine binding to the membranes is dynamic, switching between bound and unbound states. Analysis via ESR/van’t Hoff method revealed changes in the thermodynamics of phase coexistence, yielding distinct non-linear behavior. Nicotine altered the temperature dependence of the free energy, modifying the thermodynamic driving forces and the balance of non-covalent lipid interactions. These findings provide new insights into how nicotine influences pulmonary surfactant model membranes, with potential implications for surfactant function.
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spelling doaj-art-ad7a5c8a9cfd43958b874936e9a1af3b2025-08-20T02:43:43ZengMDPI AGMembranes2077-03752024-12-01141226710.3390/membranes14120267Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model MembranesFadi S. S. Magalhães0Ernanni D. Vieira1Mariana R. B. Batista2Antonio J. Costa-Filho3Luis G. M. Basso4Laboratório de Ciências Físicas, Centro de Ciência e Tecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, Campos dos Goytacazes 28013-602, RJ, BrazilLaboratório de Física Biológica, Instituto de Física, Universidade Federal de Goiás, Avenida Esperança s/n, Campus Samambaia, Goiânia 74690-900, GO, BrazilSchool of Life Sciences, Gibbet Hill Campus, University of Warwick, Coventry CV4 7Al, UKLaboratório de Biofísica Molecular, Departamento de Física, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto 14040-901, SP, BrazilLaboratório de Ciências Físicas, Centro de Ciência e Tecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, Campos dos Goytacazes 28013-602, RJ, BrazilPhase separation is essential for membrane function, and alterations in phase coexistence by membrane-interacting molecules, such as nicotine, can impair membrane stability. With the increasing use of e-cigarettes, concerns have arisen about the impact of nicotine on pulmonary surfactants. Here, we used differential scanning calorimetry (DSC), molecular dynamics (MD) simulations, and electron spin resonance (ESR) to examine nicotine’s effect on the phase coexistence of two surfactant models: pure DPPC and a DPPC/POPC/POPG mixture. Our DSC analysis revealed that nicotine interacts with both membranes, increasing enthalpy and entropy change during the phase transition. ESR revealed that nicotine affects membrane fluidity and packing of DPPC more effectively than the ternary mixture, especially near the surface. MD simulations showed that neutral nicotine resides in the mid-plane, while protonated nicotine remains near the surface. Nicotine binding to the membranes is dynamic, switching between bound and unbound states. Analysis via ESR/van’t Hoff method revealed changes in the thermodynamics of phase coexistence, yielding distinct non-linear behavior. Nicotine altered the temperature dependence of the free energy, modifying the thermodynamic driving forces and the balance of non-covalent lipid interactions. These findings provide new insights into how nicotine influences pulmonary surfactant model membranes, with potential implications for surfactant function.https://www.mdpi.com/2077-0375/14/12/267nicotinepulmonary surfactantphase coexistenceESRDSCvan’t Hoff
spellingShingle Fadi S. S. Magalhães
Ernanni D. Vieira
Mariana R. B. Batista
Antonio J. Costa-Filho
Luis G. M. Basso
Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model Membranes
Membranes
nicotine
pulmonary surfactant
phase coexistence
ESR
DSC
van’t Hoff
title Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model Membranes
title_full Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model Membranes
title_fullStr Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model Membranes
title_full_unstemmed Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model Membranes
title_short Effects of Nicotine on the Thermodynamics and Phase Coexistence of Pulmonary Surfactant Model Membranes
title_sort effects of nicotine on the thermodynamics and phase coexistence of pulmonary surfactant model membranes
topic nicotine
pulmonary surfactant
phase coexistence
ESR
DSC
van’t Hoff
url https://www.mdpi.com/2077-0375/14/12/267
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