Protein Biocargo and Anti-Inflammatory Effect of Tomato Fruit-Derived Nanovesicles Separated by Density Gradient Ultracentrifugation and Loaded with Curcumin

Mammadova, Ramila; Maggio, Serena; Fiume, Immacolata; Bokka, Ramesh; Moubarak, Maneea; Gellén, Gabriella; Schlosser, Gitta; Adamo, Giorgia; Bongiovanni, Antonella; Trepiccione, Francesco; Guescini, Michele; Pocsfalvi, Gabriella

doi:10.3390/pharmaceutics15020333

Open AccessArticle

Protein Biocargo and Anti-Inflammatory Effect of Tomato Fruit-Derived Nanovesicles Separated by Density Gradient Ultracentrifugation and Loaded with Curcumin

by

Ramila Mammadova

^1,†,

Serena Maggio

^2,†,

Immacolata Fiume

¹

,

Ramesh Bokka

¹,

Maneea Moubarak

^1,‡

,

Gabriella Gellén

³

,

Gitta Schlosser

³,

Giorgia Adamo

⁴

,

Antonella Bongiovanni

⁴,

Francesco Trepiccione

⁵,

Michele Guescini

²

and

Gabriella Pocsfalvi

^1,*

¹

Extracellular Vesicles and Mass Spectrometry Laboratory, Institute of Biosciences and BioResources, National Research Council of Italy, 80131 Naples, Italy

²

Department of Biomolecular Sciences, University of Urbino Carlo Bo, 61029 Urbino, Italy

³

MTA-ELTE Lendület Ion Mobility Mass Spectrometry Research Group, Institute of Chemistry, ELTE Eötvös Loránd University, H-1117 Budapest, Hungary

⁴

Institute for Biomedical Research and Innovation, National Research Council of Italy, 90146 Palermo, Italy

⁵

Department of Translational Medical Sciences, University of Campania Luigi Vanvitelli, 80138 Naples, Italy

^*

Author to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

^‡

In Sabbatical Leave from Department of Horticulture, Faculty of Agriculture, University of Damanhour, Damanhour 22516, Egypt.

Pharmaceutics 2023, 15(2), 333; https://doi.org/10.3390/pharmaceutics15020333

Submission received: 25 December 2022 / Revised: 12 January 2023 / Accepted: 16 January 2023 / Published: 19 January 2023

(This article belongs to the Special Issue Nanotechnology and Natural Products: Plant Bioactive Compounds for Drug Delivery (Volume II))

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Abstract

Plant-derived nanovesicles (PDNVs) have become attractive alternatives to mammalian cell-derived extracellular vesicles (EVs) both as therapeutic approaches and drug-delivery vehicles. In this study, we isolated tomato fruit-derived NVs and separated them by the iodixanol density gradient ultracentrifugation (DGUC) into twelve fractions. Three visible bands were observed at densities 1.064 ± 0.007 g/mL, 1.103 ± 0.006 g/mL and 1.122 ± 0.012 g/mL. Crude tomato PDNVs and DGUC fractions were characterized by particle size-distribution, concentration, lipid and protein contents as well as protein composition using mass spectrometry-based proteomics. Cytotoxicity and anti-inflammatory activity of the DGUC fractions associated to these bands were assessed in the lipopolysaccharide (LPS)-stimulated human monocytic THP-1 cell culture. The middle and the low-density visible DGUC fractions of tomato PDNVs showed a significant reduction in LPS-induced inflammatory IL-1β cytokine mRNA production. Functional analysis of proteins identified in these fractions reveals the presence of 14-3-3 proteins, endoplasmic reticulum luminal binding proteins and GTP binding proteins associated to gene ontology (GO) term GO:0050794 and the regulation of several cellular processes including inflammation. The most abundant middle-density DGUC fraction was loaded with curcumin using direct loading, sonication and extrusion methods and anti-inflammatory activity was compared. The highest entrapment efficiency and drug loading capacity was obtained by direct loading. Curcumin loaded by sonication increased the basal anti-inflammatory activity of tomato PDNVs.

Keywords: tomato; plant-derived nanovesicles (PDNVs); anti-inflammatory activity; in vitro analysis; loading methods; proteomics; curcumin; protein functional analysis

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MDPI and ACS Style

Mammadova, R.; Maggio, S.; Fiume, I.; Bokka, R.; Moubarak, M.; Gellén, G.; Schlosser, G.; Adamo, G.; Bongiovanni, A.; Trepiccione, F.; et al. Protein Biocargo and Anti-Inflammatory Effect of Tomato Fruit-Derived Nanovesicles Separated by Density Gradient Ultracentrifugation and Loaded with Curcumin. Pharmaceutics 2023, 15, 333. https://doi.org/10.3390/pharmaceutics15020333

AMA Style

Mammadova R, Maggio S, Fiume I, Bokka R, Moubarak M, Gellén G, Schlosser G, Adamo G, Bongiovanni A, Trepiccione F, et al. Protein Biocargo and Anti-Inflammatory Effect of Tomato Fruit-Derived Nanovesicles Separated by Density Gradient Ultracentrifugation and Loaded with Curcumin. Pharmaceutics. 2023; 15(2):333. https://doi.org/10.3390/pharmaceutics15020333

Chicago/Turabian Style

Mammadova, Ramila, Serena Maggio, Immacolata Fiume, Ramesh Bokka, Maneea Moubarak, Gabriella Gellén, Gitta Schlosser, Giorgia Adamo, Antonella Bongiovanni, Francesco Trepiccione, and et al. 2023. "Protein Biocargo and Anti-Inflammatory Effect of Tomato Fruit-Derived Nanovesicles Separated by Density Gradient Ultracentrifugation and Loaded with Curcumin" Pharmaceutics 15, no. 2: 333. https://doi.org/10.3390/pharmaceutics15020333

APA Style

Mammadova, R., Maggio, S., Fiume, I., Bokka, R., Moubarak, M., Gellén, G., Schlosser, G., Adamo, G., Bongiovanni, A., Trepiccione, F., Guescini, M., & Pocsfalvi, G. (2023). Protein Biocargo and Anti-Inflammatory Effect of Tomato Fruit-Derived Nanovesicles Separated by Density Gradient Ultracentrifugation and Loaded with Curcumin. Pharmaceutics, 15(2), 333. https://doi.org/10.3390/pharmaceutics15020333

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Protein Biocargo and Anti-Inflammatory Effect of Tomato Fruit-Derived Nanovesicles Separated by Density Gradient Ultracentrifugation and Loaded with Curcumin

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