273
Views
1
CrossRef citations to date
0
Altmetric
Articles

Concentration-dependent cortisone adsorption and interaction with model lung surfactant monolayer

ORCID Icon, , & ORCID Icon
Pages 1627-1638 | Received 15 Feb 2022, Accepted 03 Aug 2022, Published online: 23 Aug 2022

References

  • Ingle DJ. The biologic properties of cortisone: a review. J. Clin. Endocrinol. 1950;10(10):1312–1354.
  • Daley-Yates PT. Inhaled corticosteroids: potency, dose equivalence and therapeutic index. Br J Clin Pharmacol. 2015;80(3):372–380.
  • Williams DM. Clinical pharmacology of corticosteroids. Respir Care. 2018;63(6):655–670.
  • Dougherty TF, Schneebell GL. Role of cortisone in regulation of inflammation. Proc Soc Exp Biol Med. 1950;75(3):854–859.
  • Yang R, Yu Y. Glucocorticoids are double-edged sword in the treatment of COVID-19 and cancers. Int J Biol Sci. 2021;17(6):1530–1537.
  • Lundberg IE, Grundtman C, Larsson E, et al. Corticosteroids—from an idea to clinical use. Best Pract Res Clin Rheumatol. 2004;18(1):7–19.
  • Raissy HH, Kelly HW, Harkins M, et al. Inhaled corticosteroids in lung diseases. Am J Respir Crit Care Med. 2013;187(8):798–803.
  • Barnes PJ. Inhaled corticosteroids. Pharmaceuticals. 2010;3(3):514–540.
  • Sin DD, Wu L, Anderson JA, et al. Inhaled corticosteroids and mortality in chronic obstructive pulmonary disease. Thorax. 2005;60(12):992–997.
  • Perez-Gil J, Weaver TE. Pulmonary surfactant pathophysiology: current models and open questions. Physiology. 2010;25(3):132–141.
  • Autilio C, Pérez-Gil J. Understanding the principle biophysics concepts of pulmonary surfactant in health and disease. Archiv Dis Childhood-Fetal Neonatal Ed. 2019;104(4):F443–F451.
  • Schurch S, Bachofen H, Goerke J, et al. A captive bubble method reproduces the in situ behavior of lung surfactant monolayers. J Appl Physiol. 1989;67(6):2389–2396.
  • Baoukina S, Mendez-Villuendas E, Tieleman DP. Molecular view of phase coexistence in lipid monolayers. J Am Chem Soc. 2012;134(42):17543–17553.
  • Duncan SL, Dalal IS, Larson RG. Molecular dynamics simulation of phase transitions in model lung surfactant monolayers. Biochim Biophys Acta (BBA)-Biomembranes. 2011;1808(10):2450–2465.
  • Goerke J. Pulmonary surfactant: functions and molecular composition. Biochim Biophys Acta (BBA)-Mol Basis Dis. 1998;1408(2-3):79–89.
  • Lopez-Rodriguez E, Pérez-Gil J. Structure-function relationships in pulmonary surfactant membranes: from biophysics to therapy. Biochim Biophys Acta (BBA)-Biomembranes. 2014;1838(6):1568–1585.
  • Parra E, Pérez-Gil J. Composition, structure and mechanical properties define performance of pulmonary surfactant membranes and films. Chem Phys Lipids. 2015;185:153–175.
  • Guagliardo R, Pérez-Gil J, De Smedt S, et al. Pulmonary surfactant and drug delivery: focusing on the role of surfactant proteins. J Controlled Release. 2018;291:116–126.
  • Daear W, Lai P, Anikovskiy M, et al. Differential interactions of gelatin nanoparticles with the major lipids of model lung surfactant: changes in the lateral membrane organization. J Phys Chem B. 2015;119(17):5356–5366.
  • Javanainen M, Lamberg A, Cwiklik L, et al. Atomistic model for nearly quantitative simulations of Langmuir monolayers. Langmuir. 2018;34(7):2565–2572.
  • Stachowicz-Kuśnierz A, Seidler T, Rogalska E, et al. Lung surfactant monolayer–a good natural barrier against dibenzo-p-dioxins. Chemosphere. 2020;240:124850(1)–124850(12).
  • Hu J, Li X, Li M, et al. Real-time monitoring of the effect of carbon nanoparticles on the surface behavior of DPPC/DPPG Langmuir monolayer. Colloids Surf B: Biointerfaces. 2020;190:110922(1)–110922(10).
  • Bykov A, Loglio G, Miller R, et al. Dynamic properties and relaxation processes in surface layer of pulmonary surfactant solutions. Colloids Surf A: Physicochem Eng Aspects. 2019;573:14–21.
  • Lee KYC. Collapse mechanisms of Langmuir monolayers. Annu Rev Phys Chem. 2008;59:771–791.
  • Wang YE, Zhang H, Fan Q, et al. Biophysical interaction between corticosteroids and natural surfactant preparation: implications for pulmonary drug delivery using surfactant as a carrier. Soft Matter. 2012;8(2):504–511.
  • Cimato A, Facorro G, Sarrasague MM. Developing an exogenous pulmonary surfactant-glucocorticoids association: effect of corticoid concentration on the biophysical properties of the surfactant. Respir Physiol Neurobiol. 2018;247:80–86.
  • Ravera F, Miller R, Zuo YY, et al. Methods and models to investigate the physico-chemical functionality of pulmonary surfactant. Curr Opin Colloid Interface Sci. 2021;55:101467(1)–101467(14).
  • Islam MZ, Hossain SI, Deplazes E, et al. The steroid mometasone alters protein containing lung surfactant monolayers in a concentration-dependent manner. J Mol Graph Modell. 2022;111:108084(1)–108084(11).
  • Palmer D, Schurch S, Belik J. Effect of budesonide and salbutamol on surfactant properties. J Appl Physiol. 2000;89(3):884–890.
  • Zhang H, Wang YE, Neal CR, et al. Differential effects of cholesterol and budesonide on biophysical properties of clinical surfactant. Pediatr Res. 2012;71(1):316–323.
  • Davies MJ, Brindley A, Chen X, et al. A quantitative assessment of inhaled drug particle–pulmonary surfactant interaction by atomic force microscopy. Colloids Surf B: Biointerfaces. 2009;73(1):97–102.
  • Hu J, Liu H, Xu P, et al. Investigation of drug for pulmonary administration–model pulmonary surfactant monolayer interactions using Langmuir–Blodgett monolayer and molecular dynamics simulation: a case study of ketoprofen. Langmuir. 2019;35(41):13452–13460.
  • Ortiz-Collazos S, Estrada-López ED, Pedreira AA, et al. Interaction of levofloxacin with lung surfactant at the air-water interface. Colloids Surf B: Biointerfaces. 2017;158:689–696.
  • Ortiz-Collazos S, Picciani PH, Oliveira Jr ON, et al. Influence of levofloxacin and clarithromycin on the structure of DPPC monolayers. Biochim Biophys Acta (BBA)-Biomembranes. 2019;1861(10):182994(1)–182994(10).
  • Lin X, Bai T, Zuo YY, et al. Promote potential applications of nanoparticles as respiratory drug carrier: insights from molecular dynamics simulations. Nanoscale. 2014;6(5):2759–2767.
  • Bai X, Li M, Hu G. Nanoparticle translocation across the lung surfactant film regulated by grafting polymers. Nanoscale. 2020;12(6):3931–3940.
  • Souza F, Souza L, Pimentel A. Permeation of beta-defensin-3 encapsulated with polyethylene glycol in lung surfactant models at air-water interface. Colloids Surf B: Biointerfaces. 2019;182:110357(1)–110357(10).
  • Vijayan R, Biggin PC. A steroid in a lipid bilayer: localization, orientation, and energetics. Biophys J. 2008;95(7):L45–L47.
  • Souza L, Nascimento J, Romeu A, et al. Penetration of antimicrobial peptides in a lung surfactant model. Colloids Surf B: Biointerfaces. 2018;167:345–353.
  • Islam MZ, Hossain SI, Deplazes E, et al. Molecular dynamics study of prednisolone concentration on cholesterol based lung surfactant monolayer. AIP Conf Proc. 2021;2324(1):060008(1)–060008(7).
  • Schneemilch M, Quirke N. Molecular dynamics of nanoparticle translocation at lipid interfaces. Mol Simul. 2010;36(11):831–835.
  • Chen P, Zhang Z, Gu N, et al. Effect of the surface charge density of nanoparticles on their translocation across pulmonary surfactant monolayer: a molecular dynamics simulation. Mol. Simul. 2018;44(2):85–93.
  • Alsop RJ, Khondker A, Hub JS, et al. The lipid bilayer provides a site for cortisone crystallization at high cortisone concentrations. Sci Rep. 2016;6(1):1–10.
  • Khondker A, Hub JS, Rheinstädter MC. Steroid–steroid interactions in biological membranes: cholesterol and cortisone. Chem Phys. Lipids. 2019;221:193–197.
  • Baoukina S, Monticelli L, Marrink SJ, et al. Pressure−area isotherm of a lipid monolayer from molecular dynamics simulations. Langmuir. 2007;23(25):12617–12623.
  • Melo M, Ingólfsson H, Marrink S. Parameters for Martini sterols and hopanoids based on a virtual-site description. J Chem Phys. 2015;143(24):243252(1)–243252(12).
  • Estrada-López ED, Murce E, Franca MP, et al. Prednisolone adsorption on lung surfactant models: insights on the formation of nanoaggregates, monolayer collapse and prednisolone spreading. RSC Adv. 2017;7(9):5272–5281.
  • Wassenaar TA, Ingólfsson HI, Böckmann RA, et al. Computational lipidomics with insane: a versatile tool for generating custom membranes for molecular simulations. J Chem Theory Comput. 2015;11(5):2144–2155.
  • Hossain SI, Gandhi NS, Hughes ZE, et al. Computational studies of lipid-wrapped gold nanoparticle transport through model lung surfactant monolayers. J Phys Chem B. 2021;125(5):1392–1401.
  • Gordon L, Lee K, Lipp M, et al. Conformational mapping of the N-terminal segment of surfactant protein B in lipid using 13C-enhanced Fourier transform infrared spectroscopy. J Peptide Res. 2000;55(4):330–347.
  • Johansson J, Szyperski T, Curstedt T, et al. The NMR structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich. alpha.-helix. Biochemistry. 1994;33(19):6015–6023.
  • Johansson J, Curstedt T. Synthetic surfactants with SP-B and SP-C analogues to enable worldwide treatment of neonatal respiratory distress syndrome and other lung diseases. J Intern Med. 2019;285(2):165–186.
  • Sarker M, Waring AJ, Walther FJ, et al. Structure of mini-B, a functional fragment of surfactant protein B, in detergent micelles. Biochemistry. 2007;46(39):11047–11056.
  • Biswas N, Shanmukh S, Waring AJ, et al. Structure and properties of phospholipid–peptide monolayers containing monomeric SP-B1–25: I. phases and morphology by epifluorescence microscopy. Biophys Chem. 2005;113(3):223–232.
  • Schram V, Hall SB. Thermodynamic effects of the hydrophobic surfactant proteins on the early adsorption of pulmonary surfactant. Biophys J. 2001;81(3):1536–1546.
  • Baumgart F, Ospina OL, Mingarro I, et al. Palmitoylation of pulmonary surfactant protein SP-C is critical for its functional cooperation with SP-B to sustain compression/expansion dynamics in cholesterol-containing surfactant films. Biophys J. 2010;99(10):3234–3243.
  • Ding J, Takamoto DY, Von Nahmen A, et al. Effects of lung surfactant proteins, SP-B and SP-C, and palmitic acid on monolayer stability. Biophys J. 2001;80(5):2262–2272.
  • Baoukina S, Tieleman DP. Computer simulations of lung surfactant. Biochim Biophys Acta (BBA)-Biomembranes. 2016;1858(10):2431–2440.
  • Hu Q, Bai X, Hu G, et al. Unveiling the molecular structure of pulmonary surfactant corona on nanoparticles. ACS Nano. 2017;11(7):6832–6842.
  • Monticelli L, Kandasamy SK, Periole X, et al. The MARTINI coarse-grained force field: extension to proteins. J Chem Theory Comput. 2008;4(5):819–834.
  • Abraham MJ, Murtola T, Schulz R, et al. GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX. 2015;1:19–25.
  • Cuendet MA, van Gunsteren WF. On the calculation of velocity-dependent properties in molecular dynamics simulations using the leapfrog integration algorithm. J Chem Phys. 2007;127(18):184102(1)–184102(8).
  • Bussi G, Donadio D, Parrinello M. Canonical sampling through velocity rescaling. J Chem Phys. 2007;126(1):014101(1)–014101(7).
  • Berendsen HJ, Postma Jv, van Gunsteren WF, et al. Molecular dynamics with coupling to an external bath. J Chem Phys. 1984;81(8):3684–3690.
  • Duncan SL, Larson RG. Comparing experimental and simulated pressure-area isotherms for DPPC. Biophys J. 2008;94(8):2965–2986.
  • Laing C, Baoukina S, Tieleman DP. Molecular dynamics study of the effect of cholesterol on the properties of lipid monolayers at low surface tensions. Phys Chem Chem Phys. 2009;11(12):1916–1922.
  • Allen MP, Tildesley DJ. Computer simulation of liquids. 2nd ed. Oxford University Press, United Kingdom; 1987.
  • Einstein A. On the movement of small particles suspended in a stationary liquid demanded by the molecular-kinetic theory of heart. Ann Phys. 1905;17:549–560.
  • Von Smoluchowski M. Zur kinetischen theorie der brownschen molekularbewegung und der suspensionen. Ann Phys. 1906;326(14):756–780.
  • Duncan SL, Larson RG. Folding of lipid monolayers containing lung surfactant proteins SP-B1–25 and SP-C studied via coarse-grained molecular dynamics simulations. Biochim Biophys Acta (BBA)-Biomembranes. 2010;1798(9):1632–1650.
  • Da Silva E, Vogel U, Hougaard KS, et al. An adverse outcome pathway for lung surfactant function inhibition leading to decreased lung function. Curr Res Toxicol. 2021;2:225–236.
  • Pérez-Gil J. Structure of pulmonary surfactant membranes and films: the role of proteins and lipid–protein interactions. Biochim Biophys Acta (BBA)-Biomembranes. 2008;1778(7-8):1676–1695.
  • Schürch D, Ospina OL, Cruz A, et al. Combined and independent action of proteins SP-B and SP-C in the surface behavior and mechanical stability of pulmonary surfactant films. Biophys J. 2010;99(10):3290–3299.
  • Islam MZ, Krajewska M, Hossain SI, et al. Concentration-dependent effect of the steroid drug prednisolone on a lung surfactant monolayer. Langmuir. 2022;38(14):4188–4199.
  • Crowley J, Withana M, Deplazes E. The interaction of steroids with phospholipid bilayers and membranes. Biophys. Rev. 2022;14:163–179.
  • Schlick T, Portillo-Ledesma S. Biomolecular modeling thrives in the age of technology. Nat Comput Sci. 2021;1(5):321–331.
  • Hollingsworth SA, Dror RO. Molecular dynamics simulation for all. Neuron. 2018;99(6):1129–1143.
  • Lbadaoui-Darvas M, Garberoglio G, Karadima KS, et al. Molecular simulations of interfacial systems: challenges, applications and future perspectives. Mol Simul. 2021;47(18):1569–1607.
  • Berendsen HJ. Molecular dynamics simulations: The limits and beyond. In: Deuflhard HJP, Leimkuhler B, Mark AE, Reich S, Skeel RD, editor. Computational molecular dynamics: challenges, methods, ideas. Berlin, Heidelberg: Springer; 1999. p. 3–36.
  • Mohammad-Aghaie D, Bresme F. Force-field dependence on the liquid-expanded to liquid-condensed transition in DPPC monolayers. Mol Simul. 2016;42(5):391–397.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.