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Interaction mechanism of chitosan oligomers in pure water with cell membrane models studied by SFG vibrational spectroscopy

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Author(s):
Rimoli, Caio Vaz ; Pedro, Rafael de Oliveira ; Miranda, Paulo B.
Total Authors: 3
Document type: Journal article
Source: COLLOIDS AND SURFACES B-BIOINTERFACES; v. 219, p. 12-pg., 2022-09-02.
Abstract

Chitosan is a versatile and biocompatible cationic antimicrobial polymer obtained from sustainable sources that is effective against a wide range of microorganisms. Although it is soluble only at low pH, chitosan oligomers (ChitO) are soluble in pure water and thus more appropriate for antibacterial applications. Although there is a vast literature on chitosan's antimicrobial activity, the molecular details of its interaction with biomembranes remain unclear. Here we investigate these molecular interactions by resorting to phospholipid Langmuir films (zwitterionic DPPC and anionic DPPG) as simplified membrane models (for mammalian and bacterial mem-branes, respectively), and using SFG vibrational spectroscopy to probe lipid tail conformation, headgroup dy-namics and interfacial water orientation. For comparison, we also investigate the interactions of another simple cationic antimicrobial polyelectrolyte, poly(allylamine) hydrochloride - PAH. By forming the lipid films over the polyelectrolyte solutions, we found that both have only a very small interaction with DPPC, but PAH adsorption is able to invert the interfacial water orientation (membrane potential). This might explain why ChitO is compatible with mammalian cells, while PAH is toxic. In contrast, their interaction with DPPG films is much stronger, even more so for ChitO, with both insertion within the lipid film and interaction with the oppositely charged headgroups. Again, PAH adsorption inverts the membrane potential, while ChitO does not. Finally, ChitO interaction with DPPG is weaker if the antimicrobial is injected underneath a pre-assembled Langmuir film, and its interaction mode depends on the time interval between end of film compression and ChitO injection. These differences between ChitO and PAH effects on the model membranes highlight the importance of mo-lecular structure and intermolecular interactions for their bioactivity, and therefore this study may provide in-sights for the rational design of more effective antimicrobial molecules. (AU)

FAPESP's process: 18/02819-0 - Interaction of chitosans and surfactants with cell membrane models investigated by nonlinear vibrational spectroscopy
Grantee:Paulo Barbeitas Miranda
Support Opportunities: Regular Research Grants
FAPESP's process: 13/23100-0 - Investigating the molecular mechanism of action for antimicrobial polyelectrolytes on biomimetic Langmuir nanofilms using SFG spectroscopy
Grantee:Caio Vaz Rimoli
Support Opportunities: Scholarships in Brazil - Master
FAPESP's process: 14/01595-0 - Investigating interfaces in polymeric optoelectronic devices by SFG spectroscopy
Grantee:Roberto Mendonça Faria
Support Opportunities: Regular Research Grants
FAPESP's process: 17/03503-4 - Molecular interaction between chitosan and cell membrane models investigated by non-linear vibrational spectroscopy
Grantee:Rafael de Oliveira Pedro
Support Opportunities: Scholarships in Brazil - Post-Doctoral