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13 pages, 1771 KiB

Open AccessArticle

AAPH or Peroxynitrite-Induced Biorelevant Oxidation of Methyl Caffeate Yields a Potent Antitumor Metabolite

by Laura Fási, Ahmed Dhahir Latif, István Zupkó, Sándor Lévai, Miklós Dékány, Zoltán Béni, Árpád Könczöl, György Tibor Balogh and Attila Hunyadi

Biomolecules 2020, 10(11), 1537; https://doi.org/10.3390/biom10111537 - 11 Nov 2020

Cited by 6 | Viewed by 2207

Abstract

Hydroxycinnamic acids represent a versatile group of dietary plant antioxidants. Oxidation of methyl-p-coumarate (pcm) and methyl caffeate (cm) was previously found to yield potent antitumor metabolites. Here, we report the formation of potentially bioactive products of pcm [...] Read more.

Hydroxycinnamic acids represent a versatile group of dietary plant antioxidants. Oxidation of methyl-p-coumarate (pcm) and methyl caffeate (cm) was previously found to yield potent antitumor metabolites. Here, we report the formation of potentially bioactive products of pcm and cm oxidized with peroxynitrite (ONOO¯), a biologically relevant reactive nitrogen species (RNS), or with α,α′-azodiisobutyramidine dihydrochloride (AAPH) as a chemical model for reactive oxygen species (ROS). A continuous flow system was developed to achieve reproducible in situ ONOO¯ formation. Reaction mixtures were tested for their cytotoxic effect on HeLa, SiHa, MCF-7 and MDA-MB-231 cells. The reaction of pcm with ONOO¯ produced two fragments, an o-nitrophenol derivative, and a new chlorinated compound. Bioactivity-guided isolation from the reaction mixture of cm with AAPH produced two dimerization products, including a dihydrobenzofuran lignan that exerted strong antitumor activity in vitro, and has potent in vivo antimetastatic activity which was previously reported. This compound was also detected from the reaction between cm and ONOO¯. Our results demonstrate the ROS/RNS dependent formation of chemically stable metabolites, including a potent antitumor agent (5), from hydroxycinnamic acids. This suggests that diversity-oriented synthesis using ROS/RNS to obtain oxidized antioxidant metabolite mixtures may serve as a valid natural product-based drug discovery strategy. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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17 pages, 2319 KiB

Open AccessArticle

Unveiling the Mechanism of Action of 7α-acetoxy-6β-hydroxyroyleanone on an MRSA/VISA Strain: Membrane and Cell Wall Interactions

by Filipe Pereira, Teresa Figueiredo, Rodrigo F. M. de Almeida, Catarina A. C. Antunes, Catarina Garcia, Catarina P. Reis, Lia Ascensão, Rita G. Sobral and Patricia Rijo

Biomolecules 2020, 10(7), 983; https://doi.org/10.3390/biom10070983 - 30 Jun 2020

Cited by 4 | Viewed by 2872

Abstract

The number of cases of failure in the treatment of infections associated with resistant bacteria is on the rise, due to the decreasing efficacy of current antibiotics. Notably, 7α-Acetoxy-6β-hydroxyroyleanone (AHR), a diterpene isolated from different Plectranthus species, showed antibacterial activity, namely against Methicillin-resistant [...] Read more.

The number of cases of failure in the treatment of infections associated with resistant bacteria is on the rise, due to the decreasing efficacy of current antibiotics. Notably, 7α-Acetoxy-6β-hydroxyroyleanone (AHR), a diterpene isolated from different Plectranthus species, showed antibacterial activity, namely against Methicillin-resistant Staphylococcus aureus (MRSA) strains. The high antibacterial activity and low cytotoxicity render this natural compound an interesting alternative against resistant bacteria. The aim of this study is to understand the mechanism of action of AHR on MRSA, using the MRSA/Vancomycin-intermediate S. aureus (VISA) strain CIP 106760, and to study the AHR effect on lipid bilayers and on the cell wall. Although AHR interacted with lipid bilayers, it did not have a significant effect on membrane passive permeability. Alternatively, bacteria treated with this royleanone displayed cell wall disruption, without revealing cell lysis. In conclusion, the results gathered so far point to a yet undescribed mode of action that needs further investigation. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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20 pages, 4284 KiB

Open AccessArticle

The Antioxidant Peptide Salamandrin-I: First Bioactive Peptide Identified from Skin Secretion of Salamandra Genus (Salamandra salamandra)

by Alexandra Plácido, João Bueno, Eder A. Barbosa, Daniel C. Moreira, Jhones do Nascimento Dias, Wanessa Felix Cabral, Patrícia Albuquerque, Lucinda J. Bessa, Jaime Freitas, Selma A. S. Kuckelhaus, Filipe C. D. A. Lima, Augusto Batagin-Neto, Guilherme D. Brand, João B. Relvas, José Roberto S. A. Leite and Peter Eaton

Biomolecules 2020, 10(4), 512; https://doi.org/10.3390/biom10040512 - 27 Mar 2020

Cited by 20 | Viewed by 4516

Abstract

Amphibian skin is a multifunctional organ that plays key roles in defense, breathing, and water balance. In this study, skin secretion samples of the fire salamander (Salamandra salamandra) were separated using RP-HPLC and de novo sequenced using MALDI-TOF MS/MS. Next, we [...] Read more.

Amphibian skin is a multifunctional organ that plays key roles in defense, breathing, and water balance. In this study, skin secretion samples of the fire salamander (Salamandra salamandra) were separated using RP-HPLC and de novo sequenced using MALDI-TOF MS/MS. Next, we used an in silico platform to screen antioxidant molecules in the framework of density functional theory. One of the identified peptides, salamandrin-I, [M + H]⁺ = 1406.6 Da, was selected for solid-phase synthesis; it showed free radical scavenging activity against DPPH and ABTS radicals. Salamandrin-I did not show antimicrobial activity against Gram-positive and -negative bacteria. In vitro assays using human microglia and red blood cells showed that salamandrin-I has no cytotoxicity up to the concentration of 100 µM. In addition, in vivo toxicity tests on Galleria mellonella larvae resulted in no mortality at 20 and 40 mg/kg. Antioxidant peptides derived from natural sources are increasingly attracting interest. Among several applications, these peptides, such as salamandrin-I, can be used as templates in the design of novel antioxidant molecules that may contribute to devising strategies for more effective control of neurological disease. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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20 pages, 3204 KiB

Open AccessArticle

An Extract of Transgenic Senna obtusifolia L. hairy roots with Overexpression of PgSS1 Gene in Combination with Chemotherapeutic Agent Induces Apoptosis in the Leukemia Cell Line

by Tomasz Kowalczyk, Przemysław Sitarek, Monika Toma, Laurent Picot, Marzena Wielanek, Ewa Skała and Tomasz Śliwiński

Biomolecules 2020, 10(4), 510; https://doi.org/10.3390/biom10040510 - 27 Mar 2020

Cited by 15 | Viewed by 3719

Abstract

Many biologically-active plant-derived compounds have therapeutic or chemopreventive effects. The use of plant in vitro cultures in conjunction with modern genetic engineering techniques allows greater amounts of valuable secondary metabolites to be obtained without interfering with the natural environment. This work presents the [...] Read more.

Many biologically-active plant-derived compounds have therapeutic or chemopreventive effects. The use of plant in vitro cultures in conjunction with modern genetic engineering techniques allows greater amounts of valuable secondary metabolites to be obtained without interfering with the natural environment. This work presents the first findings concerning the acquisition of transgenic hairy roots of Senna obtusifolia overexpressing the gene encoding squalene synthase 1 from Panax ginseng (PgSS1) (SOPSS hairy loot lines) involved in terpenoid biosynthesis. Our results confirm that one of PgSS1-overexpressing hairy root line extracts (SOPSS2) possess a high cytotoxic effect against a human acute lymphoblastic leukemia (NALM6) cell line. Further analysis of the cell cycle, the expression of apoptosis-related genes (TP53, PUMA, NOXA, BAX) and the observed decrease in mitochondrial membrane potential also confirmed that the SOPSS2 hairy root extract displays the highest effects; similar results were also obtained for this extract combined with doxorubicin. The high cytotoxic activity, observed both alone or in combination with doxorubicin, may be due to the higher content of betulinic acid as determined by HPLC analysis. Our results suggest synergistic effects of tested extract (betulinic acid in greater amount) with doxorubicin which may be used in the future to develop new effective strategies of cancer chemosensitization. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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14 pages, 2374 KiB

Open AccessArticle

Melittin—A Natural Peptide from Bee Venom Which Induces Apoptosis in Human Leukaemia Cells

by Michal Ceremuga, Maksymilian Stela, Edyta Janik, Leslaw Gorniak, Ewelina Synowiec, Tomasz Sliwinski, Przemyslaw Sitarek, Joanna Saluk-Bijak and Michal Bijak

Biomolecules 2020, 10(2), 247; https://doi.org/10.3390/biom10020247 - 06 Feb 2020

Cited by 55 | Viewed by 9984

Abstract

Bee venom is a very complex mixture produced and secreted by the honeybee (Apis mellifera). Melittin is a major component of bee venom that accounts for about 52% of its dry mass. A vast number of studies have been dedicated to [...] Read more.

Bee venom is a very complex mixture produced and secreted by the honeybee (Apis mellifera). Melittin is a major component of bee venom that accounts for about 52% of its dry mass. A vast number of studies have been dedicated to the effects of melittin’s regulation of apoptosis and to the factors that induce apoptosis in various types of cancer such as breast, ovarian, prostate, lung. The latest evidence indicates its potential as a therapeutic agent in the treatment of leukaemia. The aim of our present study is to evaluate melittin’s ability to induce apoptosis in leukaemia cell lines of different origin acute lymphoblastic leukaemia (CCRF-CEM) and chronic myelogenous leukaemia (K-562). We demonstrated that melittin strongly reduced cell viability in both leukaemia cell lines but not in physiological peripheral blood mononuclear cells (PMBCs). Subsequent estimated parameters (mitochondrial membrane potential, Annexin V binding and Caspases 3/7 activity) clearly demonstrated that melittin induced apoptosis in leukaemia cells. This is a very important step for research into the development of new potential anti-leukaemia as well as anticancer therapies. Further analyses on the molecular level have been also planned (analysis of proapoptotic genes expression and DNA damages) for our next research project, which will also focus on melittin. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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15 pages, 2050 KiB

Open AccessArticle

Anticancer Activity of Rutin and Its Combination with Ionic Liquids on Renal Cells

by Rita Caparica, Ana Júlio, Maria Eduarda Machado Araújo, André Rolim Baby, Pedro Fonte, João Guilherme Costa and Tânia Santos de Almeida

Biomolecules 2020, 10(2), 233; https://doi.org/10.3390/biom10020233 - 04 Feb 2020

Cited by 86 | Viewed by 5859

Abstract

The renal cell carcinoma (RCC) is the most common type of kidney cancer. Identifying novel and more effective therapies, while minimizing toxicity, continues to be fundamental in curtailing RCC. Rutin, a bioflavonoid widely found in nature, has shown promising anticancer properties, but with [...] Read more.

The renal cell carcinoma (RCC) is the most common type of kidney cancer. Identifying novel and more effective therapies, while minimizing toxicity, continues to be fundamental in curtailing RCC. Rutin, a bioflavonoid widely found in nature, has shown promising anticancer properties, but with limited applicability due to its poor water solubility and pharmacokinetics. Thus, the potential anticancer effects of rutin toward a human renal cancer cell line (786-O), while considering its safety in Vero kidney cells, was assessed, as well as the applicability of ionic liquids (ILs) to improve drug delivery. Rutin (up to 50 µM) did not show relevant cytotoxic effects in Vero cells. However, in 786-O cells, a significant decrease in cell viability was already observed at 50 µM. Moreover, exposure to rutin caused a significant increase in the sub-G1 population of 786-O cells, reinforcing the possible anticancer activity of this biomolecule. Two choline-amino acid ILs, at non-toxic concentrations, enhanced rutin’s solubility/loading while allowing the maintenance of rutin’s anticancer effects. Globally, our findings suggest that rutin may have a beneficial impact against RCC and that its combination with ILs ensures that this poorly soluble drug is successfully incorporated into ILs–nanoparticles hybrid systems, allowing controlled drug delivery. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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13 pages, 2520 KiB

Open AccessCommunication

Insight the Biological Activities of Selected Abietane Diterpenes Isolated from Plectranthus spp.

by Przemysław Sitarek, Monika Toma, Epole Ntungwe, Tomasz Kowalczyk, Ewa Skała, Joanna Wieczfinska, Tomasz Śliwiński and Patricia Rijo

Biomolecules 2020, 10(2), 194; https://doi.org/10.3390/biom10020194 - 28 Jan 2020

Cited by 18 | Viewed by 3244

Abstract

Natural compounds isolated from plants are excellent starting points in drug design and have been widely studied as anticancer agents; they hence find use in a considerable proportion of anticancer drugs. The genus Plectranthus (Lamiaceae) comprises a large and widespread group of species [...] Read more.

Natural compounds isolated from plants are excellent starting points in drug design and have been widely studied as anticancer agents; they hence find use in a considerable proportion of anticancer drugs. The genus Plectranthus (Lamiaceae) comprises a large and widespread group of species with various applications in traditional medicine. Therefore, the aim of the present study was to determine the effectiveness of treatment with four abietane diterpenoids isolated from P. madagascariensis and P. ecklonii, 6,7-dehydroroyleanone, 7β,6β-dihydroxyroyleanone, 7α-acetoxy-6β-hydroxyroyleanone and parvifloron D, in initiating apoptosis in a glioma cell line. The pure compounds were found to exhibit anticancer effects in primary H7PX glioma cells line by inducing apoptosis G2/M cell cycle arrest and double-strand breaks, indicated by increased levels of phosphorylated H2A.X and decreasing mitochondrial membrane potential; they also influenced the expression of pro- and anti-apoptotic genes (Bax, Bcl-2, TP53, or Cas-3). Our findings indicate that these compounds may offer potential as beneficial antitumor drugs but further in vivo studies are needed. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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10 pages, 2456 KiB

Open AccessArticle

Anti-Migratory and Pro-Apoptotic Properties of Parvifloron D on Triple-Negative Breast Cancer Cells

by Nuno Saraiva, João G. Costa, Catarina Reis, Nuno Almeida, Patrícia Rijo and Ana Sofia Fernandes

Biomolecules 2020, 10(1), 158; https://doi.org/10.3390/biom10010158 - 19 Jan 2020

Cited by 11 | Viewed by 3013

Abstract

Medicinal plants are important sources of new bioactive compounds with potential anticancer activity. Parvifloron D (ParvD) is an abietane diterpenoid, isolated in high amounts from Plectranthus ecklonii Benth. Previous reports have suggested potential therapeutic properties for ParvD. ParvD has shown pro-apoptotic and cytotoxic [...] Read more.

Medicinal plants are important sources of new bioactive compounds with potential anticancer activity. Parvifloron D (ParvD) is an abietane diterpenoid, isolated in high amounts from Plectranthus ecklonii Benth. Previous reports have suggested potential therapeutic properties for ParvD. ParvD has shown pro-apoptotic and cytotoxic effects in leukemia and melanoma cell lines. However, to the best of our knowledge, there are no studies in triple-negative breast cancer (TNBC) models. TNBC is a breast cancer subtype characterized by an aggressive behavior with poor clinical outcomes and weak overall therapeutic responses to the current treatment options. This work aimed at evaluating the anticancer effect of ParvD in MDA-MB-231 cells, a model of human TNBC. To obtain sufficient amounts of purified ParvD the efficiency of several extraction methods was compared. ParvD (0.1–10 µM) decreased cell viability in a concentration-dependent manner. Treatment with ParvD (5 µM) significantly increased the percentage of apoptotic nuclei and exposure to 3 µM ParvD increased the sub-G1 population. Since altered cell adherence, migration, and invasion are determinant processes for the formation of metastases, the effect of ParvD on these cellular processes was tested. Although treatment with ParvD (1 µM) had no effect on cell-substrate attachment, ParvD (1 µM) significantly reduced cell chemotaxis and invasion. This is the first report describing the proapoptotic effect of ParvD in TNBC cells. Moreover, for the first time we have shown that ParvD reduces cell motility, unraveling potential anti-metastatic properties. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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11 pages, 1167 KiB

Open AccessArticle

An Overview on the Properties of Ximenia Oil Used as Cosmetic in Angola

by Gabriel Satoto, Ana Sofia Fernandes, Nuno Saraiva, Fernando Santos, Nuno Neng, José Manuel Nogueira, Tânia Santos de Almeida and Maria Eduarda Araujo

Biomolecules 2020, 10(1), 18; https://doi.org/10.3390/biom10010018 - 20 Dec 2019

Cited by 5 | Viewed by 3641

Abstract

Ximenia (Ximenia americana L.) is a shrub, or small tree, native from Africa and spread across different continents. In Angola, the seeds oil is used by local populations, to prevent sunburn, to smooth and hydrate the skin, and to give it a [...] Read more.

Ximenia (Ximenia americana L.) is a shrub, or small tree, native from Africa and spread across different continents. In Angola, the seeds oil is used by local populations, to prevent sunburn, to smooth and hydrate the skin, and to give it a pleasant color and elasticity, to prevent stretch marks, in pregnant woman, and also as hair conditioner. Herein, an oil sold in the region (LPO), and two others extracted in laboratory, from seeds collected in the same region, were investigated in terms of their composition, chemical properties, UV transmission. The three oils are similar although the LPO is more acidic, 0.48 mg KOH/g. GC-MS analysis indicated that the major components are the fatty acids, oleic (31.82%), nervonic (11.09%), ximenic (10.22%), and hexacosa-17,20,23-trienoic acids (14.59%). Long chain fatty acids, n ≥ 20, accounted for 51.1% of the total fatty acids. A thin film of the oil showed a reduction in transmittance from 200 to 300 nm. Viscosity studies of the LPO indicated that at normal temperature of skin, the oil can be spread over the skin as a thin film. At concentrations up to 10 µg/mL, the LPO is not toxic to human keratinocytes, suggesting the safety of this oil. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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16 pages, 2235 KiB

Open AccessEditor’s ChoiceArticle

Total Phenolic and Flavonoid Content and Biological Activities of Extracts and Isolated Compounds of Cytisus villosus Pourr.

by Farida Larit, Francisco León, Samira Benyahia and Stephen J. Cutler

Biomolecules 2019, 9(11), 732; https://doi.org/10.3390/biom9110732 - 13 Nov 2019

Cited by 15 | Viewed by 5717

Abstract

The aim of this study was to evaluate the total phenolic and flavonoid content, and the in vitro antioxidant, anti-inflammatory, antibacterial, antifungal, antimalarial, cytotoxicity, and antiprotozoal activities of the Algerian plant Cytisus villosus Pourr. (Syn. Cytisus triflorus L’Hérit.). Additionally, the radioligand displacement affinity [...] Read more.

The aim of this study was to evaluate the total phenolic and flavonoid content, and the in vitro antioxidant, anti-inflammatory, antibacterial, antifungal, antimalarial, cytotoxicity, and antiprotozoal activities of the Algerian plant Cytisus villosus Pourr. (Syn. Cytisus triflorus L’Hérit.). Additionally, the radioligand displacement affinity on opioid and cannabinoid receptors was assessed for the extracts and isolated pure compounds. The hydro alcoholic extract of the aerial part of C. villosus was partitioned with chloroform (CHCl₃), ethyl acetate (EtOAc), and n-butanol (n-BuOH). The phenolic content of the C. villosus extracts was evaluated using a modified Folin–Ciocalteau method. The total flavonoid content was measured spectrometrically using the aluminum chloride colorimetric assay. The known flavonoids genistein (1), chrysin (2), chrysin-7-O-β-d-glucopyranoside (3), and 2″-O-α-l-rhamnosylorientin (4) were isolated. The antioxidant activities of the extracts and isolated compounds were evaluated using 2,2-diphenyl-1-picrylhydrazyl (DDPH) and cellular antioxidant activity (CAA) assays. The plant extracts showed moderate antioxidant activity. EtOAc and n-BuOH extracts showed moderate anti-inflammatory activity through the inhibition of induced nitric oxide synthase (iNOS) with IC₅₀ values of 48 and 90 µg/mL, respectively. The isolated pure compounds 1 and 3 showed good inhibition of Inducible nitric oxide synthase (iNOS) with IC₅₀ values of 9 and 20 µg/mL, respectively. Compounds 1 and 2 exhibited lower inhibition of Nuclear Factor kappa-light-chain-enhancer of activated B cells (NF-κB) with IC₅₀ values of 28 and 38 µg/mL, respectively. Furthermore, the extracts and isolated pure compounds have been shown to exhibit low affinity for cannabinoid and opioid receptors. Finally, n-BuOH extract was a potent inhibitor of Trypanosoma brucei with IC₅₀ value of 7.99 µg/mL and IC₉₀ value of 12.61 µg/mL. The extracts and isolated compounds showed no antimicrobial, antimalarial nor antileishmanial activities. No cytotoxic effect was observed on cancer cell lines. The results highlight this species as a promising source of anti-inflammatory and antitrypanosomal agents. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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Review

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12 pages, 1398 KiB

Open AccessReview

Bioactive Compounds from Hermetia Illucens Larvae as Natural Ingredients for Cosmetic Application

by Cíntia Almeida, Patrícia Rijo and Catarina Rosado

Biomolecules 2020, 10(7), 976; https://doi.org/10.3390/biom10070976 - 29 Jun 2020

Cited by 33 | Viewed by 7018

Abstract

Due to the sustainable organic matter bioconversion process used as substrate for its development, the Hermetia illucens (Linnaeus) larvae biomass is considered a source of compounds with high aggregate value and quite a promising market. The materials that can be extracted from H. [...] Read more.

Due to the sustainable organic matter bioconversion process used as substrate for its development, the Hermetia illucens (Linnaeus) larvae biomass is considered a source of compounds with high aggregate value and quite a promising market. The materials that can be extracted from H. illucens larvae have opened the door to a diverse new field of ingredients, mainly for the feed and food industry, but also with potential applicability in cosmetics. In this review we succinctly describe the larval development and rearing cycle, the main compounds identified from different types of extractions, their bioactivities and focus on possible applications in cosmetic products. A search was made in the databases PubMed, ScienceDirect and Web of Science with the terms ‘Hermetia illucens’, ‘bioactives’, ‘biochemical composition’ and ‘cosmetics ingredients’, which included 71 articles published since 1994. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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20 pages, 1153 KiB

Open AccessReview

Zoopharmacology: A Way to Discover New Cancer Treatments

by Eva María Domínguez-Martín, Joana Tavares, Patrícia Ríjo and Ana María Díaz-Lanza

Biomolecules 2020, 10(6), 817; https://doi.org/10.3390/biom10060817 - 26 May 2020

Cited by 11 | Viewed by 4338

Abstract

Zoopharmacognosy is the multidisciplinary approach of the self-medication behavior of many kinds of animals. Recent studies showed the presence of antitumoral secondary metabolites in some of the plants employed by animals and their use for the same therapeutic purposes in humans. Other related [...] Read more.

Zoopharmacognosy is the multidisciplinary approach of the self-medication behavior of many kinds of animals. Recent studies showed the presence of antitumoral secondary metabolites in some of the plants employed by animals and their use for the same therapeutic purposes in humans. Other related and sometimes confused term is Zootherapy, which consists on the employment of animal parts and/or their by-products such as toxins, venoms, etc., to treat different human ailments. Therefore, the aim of this work is to provide a brief insight for the use of Zoopharmacology (comprising Zoopharmacognosy and Zootherapy) as new paths to discover drugs studying animal behavior and/or using compounds derived from animals. This work is focused on the approaches related to cancer, in order to propose a new promising line of research to overcome multidrug resistance (MDR). This novel subject will encourage the use of new alternative prospective ways to find new medicines. Full article

(This article belongs to the Special Issue Selected Papers from Bio.Natural Meeting 2019)

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