In Silico Predicting the Presence of the S100B Motif in Edible Plants and Detecting Its Immunoreactive Materials: Perspectives for Functional Foods, Dietary Supplements and Phytotherapies
Abstract
:1. Introduction
2. Results
2.1. In Silico Molecular Investigations
2.2. A S100B Dimeric EF-Hand Organization in Plants
2.3. Immunodetection of S100B-like Material in Plant Extracts
3. Discussion
4. Materials and Methods
4.1. In Silico Molecular Investigations
4.1.1. Data Preparation
4.1.2. Molecular Modelling
4.2. In Field Investigations
4.2.1. Sample Preparation
4.2.2. Enzyme-Linked Immunosorbent Assay for S100B
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Donato, R.; Cannon, B.R.; Sorci, G.; Riuzzi, F.; Hsu, K.; Weber, D.J.; Geczy, C.L. Functions of S100 proteins. Curr. Mol. Med. 2013, 13, 24–57. [Google Scholar] [CrossRef] [PubMed]
- Santamaria-Kisiel, L.; Rintala-Dempsey, A.C.; Shaw, G.S. Calcium-dependent and -independent interactions of the S100 protein family. Biochem. J. 2006, 396, 201–214. [Google Scholar] [CrossRef] [PubMed]
- Xia, P.; Ji, X.; Yan, L.; Lian, S.; Chen, Z.; Luo, Y. Roles of S100A8, S100A9 and S100A12 in infection, inflammation and immunity. Immunology 2023, 171, 365–376. [Google Scholar] [CrossRef]
- Luan, S.; Wang, C. Calcium Signaling Mechanisms Across Kingdoms. Annu. Rev. Cell Dev. Biol. 2021, 37, 311–340. [Google Scholar] [CrossRef] [PubMed]
- Moore, B.W. A soluble protein characteristic of the nervous system. Biochem. Biophys. Res. Commun. 1965, 19, 739–744. [Google Scholar] [CrossRef]
- Michetti, F.; Di Sante, G.; Clementi, M.E.; Sampaolese, B.; Casalbore, P.; Volonté, C.; Romano Spica, V.; Parnigotto, P.P.; Di Liddo, R.; Amadio, S.; et al. Growing role of S100B protein as a putative therapeutic target for neurological- and nonneurological-disorders. Neurosci. Biobehav. Rev. 2021, 127, 446–458. [Google Scholar] [CrossRef]
- Michetti, F.; Clementi, M.E.; Di Liddo, R.; Valeriani, F.; Ria, F.; Rende, M.; Di Sante, G.; Romano Spica, V. The S100B Protein: A Multifaceted Pathogenic Factor More Than a Biomarker. Int. J. Mol. Sci. 2023, 24, 9605. [Google Scholar] [CrossRef] [PubMed]
- Michetti, F.; Di Sante, G.; Clementi, M.E.; Valeriani, F.; Mandarano, M.; Ria, F.; Di Liddo, R.; Rende, M.; Romano Spica, V. The Multifaceted S100B Protein: A Role in Obesity and Diabetes? Int. J. Mol. Sci. 2024, 25, 776. [Google Scholar] [CrossRef]
- Seguella, L.; Palenca, I.; Franzin, S.B.; Zilli, A.; Esposito, G. Mini-review: Interaction between intestinal microbes and enteric glia in health and disease. Neurosci. Lett. 2023, 806, 137221. [Google Scholar] [CrossRef]
- Langeh, U.; Singh, S. Targeting S100B Protein as a Surrogate Biomarker and its Role in Various Neurological Disorders. Curr. Neuropharmacol. 2021, 19, 265–277. [Google Scholar] [CrossRef]
- Clementi, M.E.; Sampaolese, B.; Di Sante, G.; Ria, F.; Di Liddo, R.; Romano Spica, V.; Michetti, F. S100B Expression Plays a Crucial Role in Cytotoxicity, Reactive Oxygen Species Generation and Nitric Oxide Synthase Activation Induced by Amyloid β-Protein in an Astrocytoma Cell Line. Int. J. Mol. Sci. 2023, 24, 5213. [Google Scholar] [CrossRef] [PubMed]
- Marenholz, I.; Heizmann, C.W.; Fritz, G. S100 proteins in mouse and man: From evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 2004, 322, 1111–1122. [Google Scholar] [CrossRef] [PubMed]
- Michetti, F.; D’Ambrosi, N.; Toesca, A.; Puglisi, M.A.; Serrano, A.; Marchese, E.; Corvino, V.; Geloso, M.C. The S100B story: From biomarker to active factor in neural injury. J. Neurochem. 2019, 148, 168–187. [Google Scholar] [CrossRef]
- Prez, K.D.; Fan, L. Structural Basis for S100B Interaction with its Target Proteins. J. Mol. Genet. Med. Int. J. Biomed. Res. 2018, 12, 366. [Google Scholar] [CrossRef]
- Freire, M.A.M.; Rocha, G.S.; Bittencourt, L.O.; Falcao, D.; Lima, R.R.; Cavalcanti, J.R.L.P. Cellular and Molecular Pathophysiology of Traumatic Brain Injury: What Have We Learned So Far? Biology 2023, 12, 1139. [Google Scholar] [CrossRef]
- Michetti, F.; Gazzolo, D. S100B protein in biological fluids: A tool for perinatal medicine. Clin. Chem. 2002, 48, 2097–2104. [Google Scholar] [CrossRef]
- Gazzolo, D.; Monego, G.; Corvino, V.; Bruschettini, M.; Bruschettini, P.; Zelano, G.; Michetti, F. Human milk contains S100B protein. Biochim. Biophys. Acta 2003, 1619, 209–212. [Google Scholar] [CrossRef] [PubMed]
- Peila, C.; Coscia, A.; Bertino, E.; Volti, G.L.; Galvano, F.; Visser, G.H.A.; Gazzolo, D. Holder pasteurization affects S100B concentrations in human milk. J. Matern. Fetal Neonatal Med. 2018, 31, 513–517. [Google Scholar] [CrossRef]
- Galvano, F.; Frigiola, A.; Gagliardi, L.; Ciotti, S.; Bognanno, M.; Iacopino, A.; Nigro, F.; Tina, G.L.; Cavallaro, D.; Mussap, M.; et al. S100B milk concentration in mammalian species. Front. Biosci. 2009, 1, 542–546. [Google Scholar] [CrossRef]
- Orsini, M.; Di Liddo, R.; Valeriani, F.; Mancin, M.; D’Incà, R.; Castagnetti, A.; Aceti, A.; Parnigotto, P.P.; Romano Spica, V.; Michetti, F. In Silico Evaluation of Putative S100B Interacting Proteins in Healthy and IBD Gut Microbiota. Cells 2020, 9, 1697. [Google Scholar] [CrossRef]
- Romano Spica, V.; Valeriani, F.; Orsini, M.; Clementi, M.E.; Seguella, L.; Gianfranceschi, G.; Di Liddo, R.; Di Sante, G.; Ubaldi, F.; Ria, F.; et al. S100B Affects Gut Microbiota Biodiversity. Int. J. Mol. Sci. 2023, 24, 2248. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Skolnick, J. TM-align: A protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 2005, 33, 2302–2309. [Google Scholar] [CrossRef] [PubMed]
- Zhang, D.; Kanthasamy, A.; Yang, Y.; Anantharam, V.; Kanthasamy, A. Protein kinase cδ negatively regulates tyrosine hydroxylase activity and dopamine synthesis by enhancing protein phosphatase-2a activity in dopaminergic neurons. J. Neurosci. 2007, 27, 5349–5362. [Google Scholar] [CrossRef]
- Gonzalez, L.L.; Garrie, K.; Turner, M.D. Role of S100 proteins in health and disease. Biochim. Biophys. Acta Mol. Cell Res. 2020, 1867, 118677. [Google Scholar] [CrossRef] [PubMed]
- Rose, R.J. Molecular Cell Biology of the Growth and Differentiation of Plant Cells; CRC Press: Boca Raton, FL, USA, 2016. [Google Scholar] [CrossRef]
- Siqueira, J.A.; Hardoim, P.; Ferreira, P.C.G.; Nunes-Nesi, A.; Hemerly, A.S. Unraveling Interfaces between Energy Metabolism and Cell Cycle in Plants. Trends Plant Sci. 2018, 23, 731–747. [Google Scholar] [CrossRef]
- Bentham, A.R.; De la Concepcion, J.C.; Mukhi, N.; Zdrzałek, R.; Draeger, M.; Gorenkin, D.; Hughes, R.K.; Banfield, M.J. A molecular roadmap to the plant immune system. J. Biol. Chem. 2020, 295, 14916–14935. [Google Scholar] [CrossRef]
- Zhang, W.J.; Zhou, Y.; Zhang, Y.; Su, Y.H.; Xu, T. Protein phosphorylation: A molecular switch in plant signaling. Cell Rep. 2023, 42, 112729. [Google Scholar] [CrossRef]
- Gazzolo, D.; Abella, R.; Marinoni, E.; di Iorio, R.; Li Volti, G.; Galvano, F.; Florio, P. New markers of neonatal neurology. J. Matern.-Fetal Neonatal Med. 2009, 22 (Suppl. S3), 57–61. [Google Scholar] [CrossRef]
- Jin, Z.; Na, J.; Lin, X.; Jiao, R.; Liu, X.; Huang, Y. Plant-derived exosome-like nanovesicles: A novel nanotool for disease therapy. Heliyon 2024, 10, e30630. [Google Scholar] [CrossRef]
- Maleš, I.; Dragović-Uzelac, V.; Jerković, I.; Zorić, Z.; Pedisić, S.; Repajić, M.; Garofulić, I.E.; Dobrinčić, A. Non-Volatile and Volatile Bioactives of Salvia officinalis L. Thymus serpyllum L. and Laurus nobilis L. Extracts with Potential Use in the Development of Functional Beverages. Antioxidants 2022, 11, 1140. [Google Scholar] [CrossRef]
- Maleš, I.; Pedisić, S.; Zorić, Z.; Elez-Garofulić, I.; Repajić, M.; You, L.; Vladimir-Knežević, S.; Butorac, D.; Dragović-Uzelac, V. The medicinal and aromatic plants as ingredients in functional beverage production. J. Funct. Foods 2022, 96, 105210. [Google Scholar] [CrossRef]
- Kompoura, V.; Karapantzou, I.; Mitropoulou, G.; Parisis, N.A.; Gkalpinos, V.K.; Anagnostou, V.A.; Tsiailanis, A.D.; Vasdekis, E.P.; Koutsaliaris, I.K.; Tsouka, A.N.; et al. Exploiting the beneficial effects of Salvia officinalis L. extracts in human health and assessing their activity as potent functional regulators of food microbiota. Food Chem. 2024, 441, 138175. [Google Scholar] [CrossRef] [PubMed]
- Lima, M.D.C.; do Nascimento, H.M.A.; da Silva, J.Y.P.; de Brito Alves, J.L.; de Souza, E.L. Evidence for the Beneficial Effects of Brazilian Native Fruits and Their By-Products on Human Intestinal Microbiota and Repercussions on Non-Communicable Chronic Diseases-A Review. Foods 2023, 12, 3491. [Google Scholar] [CrossRef]
- Alqurashi, R.M.; Alarifi, S.N.; Walton, G.E.; Costabile, A.F.; Rowland, I.R.; Commane, D.M. In vitro approaches to assess the effects of açai (Euterpe oleracea) digestion on polyphenol availability and the subsequent impact on the faecal microbiota. Food Chem. 2017, 234, 190–198. [Google Scholar] [CrossRef]
- Bester, A.; O’Brien, M.; Cotter, P.D.; Dam, S.; Civai, C. Shotgun Metagenomic Sequencing Revealed the Prebiotic Potential of a Fruit Juice Drink with Fermentable Fibres in Healthy Humans. Foods 2023, 12, 2480. [Google Scholar] [CrossRef]
- Jiang, H.; Dong, J.; Jiang, S.; Liang, Q.; Zhang, Y.; Liu, Z.; Ma, C.; Wang, J.; Kang, W. Effect of Durio zibethinus rind polysaccharide on functional constipation and intestinal microbiota in rats. Food Res. Int. 2020, 136, 109316. [Google Scholar] [CrossRef]
- Tan, X.-S.; Ma, J.-Y.; Feng, R.; Ma, C.; Chen, W.-J.; Sun, Y.-P.; Fu, J.; Huang, M.; He, C.-Y.; Shou, J.-W.; et al. Tissue distribution of berberine and its metabolites after oral administration in rats. PLoS ONE 2013, 8, e77969. [Google Scholar] [CrossRef] [PubMed]
- Ma, T.; Li, C.; Zhao, F.; Cao, J.; Zhang, X.; Shen, X. Effects of co-fermented collagen peptide-jackfruit juice on the immune response and gut microbiota in immunosuppressed mice. Food Chem. 2021, 365, 130487. [Google Scholar] [CrossRef]
- Zhumaliyeva, G.; Zhussupova, A.; Zhusupova, G.E.; Błońska-Sikora, E.; Cerreto, A.; Omirbekova, N.; Zhunusbayeva, Z.; Gemejiyeva, N.; Ramazanova, M.; Wrzosek, M.; et al. Natural Compounds of Salvia L. Genus and Molecular Mechanism of Their Biological Activity. Biomedicines 2023, 11, 3151. [Google Scholar] [CrossRef]
- UniProt’s Blastp Page. Available online: https://www.uniprot.org/blast (accessed on 2 July 2004).
- Chiara, M.; Gioiosa, S.; Chillemi, G.; D’Antonio, M.; Flati, T.; Picardi, E.; Zambelli, F.; Horner, D.S.; Pesole, G.; Castrignanò, T. CoVaCS: A consensus variant calling system. BMC Genom. 2018, 19, 120. [Google Scholar] [CrossRef]
- Kazutaka, K.; Kazuharu, M.; Kei-ichi, K.; Takashi, M. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002, 30, 3059–3066. [Google Scholar] [CrossRef]
- Capella-Gutiérrez, S.; Silla-Martínez, J.M.; Gabaldón, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25, 1972–1973. [Google Scholar] [CrossRef] [PubMed]
- Minh, B.Q.; Schmidt, H.A.; Chernomor, O.; Schrempf, D.; Woodhams, M.D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol. Biol. Evol. 2020, 37, 1530–1534. [Google Scholar] [CrossRef]
- Le, S.Q.; Gascuel, O. An Improved General Amino Acid Replacement Matrix. Mol. Biol. Evol. 2008, 25, 1307–1320. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. J. Mol. Evol. 1994, 39, 306–314. [Google Scholar] [CrossRef]
- NCBI Common Taxonomy Tree Web Page. Available online: https://www.ncbi.nlm.nih.gov/Taxonomy/CommonTree/wwwcmt.cgi (accessed on 2 July 2024).
- Castrignanò, T.; Gioiosa, S.; Flati, T.; Cestari, M.; Picardi, E.; Chiara, M.; Fratelli, M.; Amente, S.; Cirilli, M.; Tangaro, M.A.; et al. ELIXIR-IT HPC@CINECA: High performance computing resources for the bioinformatics community. BMC Bioinform. 2020, 21, 352. [Google Scholar] [CrossRef]
- Jumper, J.; Evans, R.; Pritzel, A.; Green, T.; Figurnov, M.; Ronneberger, O.; Tunyasuvunakool, K.; Bates, R.; Žídek, A.; Potapenko, A.; et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021, 596, 583–589. [Google Scholar] [CrossRef]
- Steinegger, M.; Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 2017, 35, 1026–1028. [Google Scholar] [CrossRef]
- Steinegger, M.; Meier, M.; Mirdita, M.; Vöhringer, H.; Haunsberger, S.J.; Söding, J. HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinform. 2019, 20, 473. [Google Scholar] [CrossRef]
- Ali, S.A.; Hassan, M.I.; Islam, A.; Ahmad, F. A review of methods available to estimate solvent-accessible surface areas of soluble proteins in the folded and unfolded states. Curr. Protein Pept. Sci. 2014, 15, 456–476. [Google Scholar] [CrossRef]
- Castrignanò, T.; De Meo, P.D.; Carrabino, D.; Orsini, M.; Floris, M.; Tramontano, A. The MEPS server for identifying protein conformational epitopes. BMC Bioinform. 2007, 8 (Suppl. S1), S6. [Google Scholar] [CrossRef] [PubMed]
Name File | Accession | Description | Organism | RMSD | TM-Align Score | SASA [Å2] | RMSD Conserved | TM-Align Score Conserved |
---|---|---|---|---|---|---|---|---|
S100B | P04271 | S100B | Homo Sapiens | 6504.42 | ||||
Adansonia digitata | Q6EIJ6 | Maturase K | Artocarpus heterophyllus | 3.67 | 0.41058 | 55,361.468 | 2.04 | 0.47283 |
Adiantum capillus-veneris | A0A9D4UGI1 | EF-hand domain-containing protein | Adiantum capillus-veneris | 2.46 | 0.55553 | 7227.491 | 2.32 | 0.74548 |
Ceratopteris richardii | A0A8T2T945 | EF-hand domain-containing protein | Ceratopteris richardii | 3.06 | 0.63275 | 12,912.797 | 2.36 | 0.73105 |
Cuscuta europaea | A0A9P0ZHW9 | EF-hand domain-containing protein | Cuscuta europaea | 3.8 | 0.61591 | 11,235.978 | 2.85 | 0.7075 |
Durio zibethinus | A0A6P6AZ13 | Probable calcium-binding protein | Durio zibethinus | 2.74 | 0.66936 | 11,374.781 | 2.63 | 0.71475 |
Gossypium klotzschianum | A0A7J8USE5 | EF-hand domain-containing protein | Gossypium klotzschianum | 2.43 | 0.62498 | 11,317.836 | 2.41 | 0.70399 |
Handroanthus impetiginosus | A0A2G9G7M9 | EF-hand domain-containing protein | Handroanthus impetiginosus | 3.07 | 0.61603 | 15,050.241 | 2.19 | 0.73368 |
Hibiscus syriacus | A0A6A3BQP9 | PfkB-like carbohydrate kinase family protein | Hibiscus syriacus | 2.82 | 0.61948 | 10,389.12 | 2.13 | 0.76271 |
Malus domestica | A0A498KP84 | EF-hand domain-containing protein | Malus domestica | 3.5 | 0.60179 | 37,161.187 | 2.81 | 0.63253 |
Musa acuminata | A0A804HRU8 | hypothetical protein | Musa acuminata subsp. malaccensis | 2.53 | 0.61628 | 5706.664 | 2.03 | 0.77669 |
Olea europaea | A0A8S0U3M0 | Probable calcium-binding CML18 | Olea europaea subsp. europaea | 2.51 | 0.63074 | 12,185.494 | 2.38 | 0.7467 |
Sample | Scientific Notation | S100B Presence |
---|---|---|
Açai (powder) | Euterpe oleracea, Von Martius, Arecaceae | + |
Banana (fresh) | Musa acuminata, Colla, Musaceae | − |
Banana (powder) | Musa acuminata, Colla, Musaceae | − |
Baobab (powder) | Adansonia, Linnaeus, Malvaceae | + |
Broccoli (fresh) | Brassica oleracea var. italica, Linnaeus, Brassicaceae | − |
Cabbage (fresh) | Brassica oleracea var. capitata, Brassicaceae | − |
Cocoa (powder) | Theobroma cacao, Linneo, Malvaceae | − |
Durian (fresh) | Durio zibethinus, Linnaeus, Malvaceae | + |
Durian (Freeze/dry) | Durio zibethinus, Linnaeus, Malvaceae | + |
Durian (powder) | Durio zibethinus, Linnaeus, Malvaceae | + |
Graviola (powder) | Annona muricata, Linnaeus, Annonaceae | + |
Jack fruit (lyophilized) | Artocarpus heterophyllus, Lamarck, Moraceae | + |
Kiwi (fresh) | Actinidia chinensis, Planch, Actinidiacee | − |
Kombucha(powder) | Camellia sinensis, Linnaeus, Theaceae | + |
Laurel (fresh) | Laurus nobilis, Linnaeus, Lauraceae | + |
Mela Annurca (cps) | Malus domestica, Borkhausen, Rosaceae | + |
Reishi Mushroom (powder) | Ganoderma lucidum, (Curtis) P. Karst. Ganodermataceae | − |
Sage (fresh) | Salvia officinalis, Linnaeus, Lamiaceae | + |
Salad (fresh) | Lactuca sativa, Linnaeus, Asteraceae | − |
Spinach (fresh) | Spinacia oleracea, Linnaeus, Amaranthaceae | − |
Spinach (powder) | Spinacia oleracea, Linnaeus, Amaranthaceae | − |
Sunflower (powder) | Helianthus annuus, Linnaeus, Asteraceae | − |
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Romano Spica, V.; Volpini, V.; Valeriani, F.; Carotenuto, G.; Arcieri, M.; Platania, S.; Castrignanò, T.; Clementi, M.E.; Michetti, F. In Silico Predicting the Presence of the S100B Motif in Edible Plants and Detecting Its Immunoreactive Materials: Perspectives for Functional Foods, Dietary Supplements and Phytotherapies. Int. J. Mol. Sci. 2024, 25, 9813. https://doi.org/10.3390/ijms25189813
Romano Spica V, Volpini V, Valeriani F, Carotenuto G, Arcieri M, Platania S, Castrignanò T, Clementi ME, Michetti F. In Silico Predicting the Presence of the S100B Motif in Edible Plants and Detecting Its Immunoreactive Materials: Perspectives for Functional Foods, Dietary Supplements and Phytotherapies. International Journal of Molecular Sciences. 2024; 25(18):9813. https://doi.org/10.3390/ijms25189813
Chicago/Turabian StyleRomano Spica, Vincenzo, Veronica Volpini, Federica Valeriani, Giovanni Carotenuto, Manuel Arcieri, Serena Platania, Tiziana Castrignanò, Maria Elisabetta Clementi, and Fabrizio Michetti. 2024. "In Silico Predicting the Presence of the S100B Motif in Edible Plants and Detecting Its Immunoreactive Materials: Perspectives for Functional Foods, Dietary Supplements and Phytotherapies" International Journal of Molecular Sciences 25, no. 18: 9813. https://doi.org/10.3390/ijms25189813