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Lobophorin K, a New Natural Product with Cytotoxic Activity Produced by Streptomyces Sp. M-207 Associated with the Deep-Sea Coral Lophelia Pertusa

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Lobophorin K, a New Natural Product with Cytotoxic Activity Produced by Streptomyces Sp. M-207 Associated with the Deep-Sea Coral Lophelia Pertusa marine drugs Article Lobophorin K, a New Natural Product with Cytotoxic Activity Produced by Streptomyces sp. M-207 Associated with the Deep-Sea Coral Lophelia pertusa Alfredo F. Braña 1, Aida Sarmiento-Vizcaíno 1, Miguel Osset 1, Ignacio Pérez-Victoria 2, Jesús Martín 2, Nuria de Pedro 2, Mercedes de la Cruz 2, Caridad Díaz 2, Francisca Vicente 2, Fernando Reyes 2,*, Luis A. García 3 and Gloria Blanco 1,* 1 Departamento de Biología Funcional, Área de Microbiología, Instituto Universitario de Oncología del Principado de Asturias, Universidad de Oviedo, 33006 Oviedo, Spain; [email protected] (A.F.B.); [email protected] (A.S.-V.); [email protected] (M.O.) 2 Fundación MEDINA, Centro de Excelencia en Investigación de Medicamentos Innovadores en Andalucía, Avda. del Conocimiento 3, Parque Tecnológico de Ciencias de la Salud, E-18016 Granada, Spain; [email protected] (I.P.-V.); [email protected] (J.M.); [email protected] (N.d.P.); [email protected] (M.d.l.C.); [email protected] (C.D.); [email protected] (F.V.) 3 Departamento de Ingeniería Química y Tecnología del Medio Ambiente, Área de Ingeniería Química, Universidad de Oviedo, 33006 Oviedo, Spain; [email protected] * Correspondences: [email protected] (F.R.); [email protected] (G.B.); Tel.: +34-958-993-965 (F.R.); +34-985-103-205 (G.B.) Academic Editors: Dong-Chan Oh and Sang-Jip Nam Received: 24 February 2017; Accepted: 15 May 2017; Published: 19 May 2017 Abstract: The present article describes the isolation of a new natural product of the lobophorin family, designated as lobophorin K (1), from cultures of the marine actinobacteria Streptomyces sp. M-207, previously isolated from the cold-water coral Lophelia pertusa collected at 1800 m depth during an expedition to the submarine Avilés Canyon. Its structure was determined using a combination of spectroscopic techniques, mainly ESI-TOF MS and 1D and 2D NMR. This new natural product displayed cytotoxic activity against two human tumor cell lines, such as pancreatic carcinoma (MiaPaca-2) and breast adenocarcinoma (MCF-7). Lobophorin K also displayed moderate and selective antibiotic activity against pathogenic Gram-positive bacteria such as Staphylococcus aureus. Keywords: lobophorins; spirotetronate antibiotic; Streptomyces; antitumor; Cantabrian Sea-derived actinobacteria 1. Introduction Lobophorins are natural products of marine origin with pharmacological interest due to their diverse biological activities. Structurally, they are members of the spirotetronate family first reported as anti-inflammatory compounds, such as lobophorins A and B [1]. Antibiotic activities were subsequently reported for other members of the family, such as lobophorins E and F [2], lobophorin G[3], and lobophorins H and I [4,5]. Unfortunately, due to an overlapping in the publication dates, the two last references add some confusion to the nomenclature of the lobophorin family, as the names lobophorin H and I were assigned twice to new compounds whose structures are not coincident, isolated independently by both research groups. The compound named lobophorin I in the Lin paper [5] has the same structure as lobophorin H in the Pan article [4], and the compound whose name was assigned as lobophorin H in the Lin paper would represent a new natural product whose name should be perhaps be reassigned as lobophorin I* in order to not add more confusion to the Mar. Drugs 2017, 15, 144; doi:10.3390/md15050144 www.mdpi.com/journal/marinedrugs Mar. Drugs 2017,, 15,, 144 2 of 8 the nomenclature of these molecules, taking into account the publication date of both articles. Very nomenclaturerecently, three of additional these molecules, members taking of the into lobophorin account the family—namely publication date oflobophorins both articles. CR1, Very CR2, recently, and threeCR3 were additional isolated members from cultures of the lobophorin of Streptomyces family—namely sp. strain 7790N4 lobophorins [6]. Finally, CR1, CR2, the andisolation CR3 were of a isolatedcompound from named cultures lobophorin of Streptomyces J from a sp.culture strain of the 7790N4 deep [ sea6].‐ Finally,derived theStreptomyces isolation sp. of astrain compound 12A35 namedhas also lobophorin been reported J from [7]. a In culture addition of the to their deep antimicrobial sea-derived Streptomyces activities, somesp. strain lobophorins 12A35 has also also display been reportedcytototoxic [7 ].activity In addition against to different their antimicrobial tumor cell activities,lines, such some as lobophorins lobophorins C alsoand displayD against cytototoxic liver and activitybreast tumor against cell different lines [8], tumor lobophorin cell lines, F such against as lobophorins SNC, breast, C and and D lung against tumor liver cell and lines breast [2], tumor and celllobophorins lines [8], lobophorinCR1 and CR2 F against against SNC, oral cancer breast, cell and lines lung [6]. tumor cell lines [2], and lobophorins CR1 and CR2 againstPrevious oral research cancer cellin the lines Cantabrian [6]. Sea (Biscay Bay), Northeast Atlantic, has revealed that bioactivePrevious actinobacteria, research in mainly the Cantabrian Streptomyces Sea species, (Biscay are Bay), associated Northeast to corals Atlantic, and other has revealedinvertebrates that bioactiveliving up to actinobacteria, 4700 m depth mainly in the submarineStreptomyces Avilésspecies, Canyon are associated [9–11]. Recently, to corals actinobacteria and other invertebrates displaying livinga wide up repertoire to 4700 m of depth chemically in the diverse submarine secondary Avilés Canyon metabolites [9–11 with]. Recently, different actinobacteria antibiotic or displayingantitumor aactivities wide repertoire have been of isolated chemically from diverse coral reef secondary ecosystems metabolites from the with Avilés different Canyon antibiotic [12]. We or report antitumor here activitiesthe finding have of beena new isolated natural from product, coral reeflobophorin ecosystems K, obtained from the Avilfromé sStreptomyces Canyon [12]. sp. We M report‐207, hereisolated the findingfrom the of cold a new‐water natural coral product, Lophelia lobophorin pertusa collected K, obtained at 1800 from mStreptomyces depth in sp.this M-207, submarine isolated canyon. from theFollowing cold-water our LC coral‐UVLophelia‐MS and pertusa LC‐HRMScollected chemical at 1800 dereplication m depth in approaches this submarine for marine canyon. natural Following products our LC-UV-MS[13], it was anddetermined LC-HRMS that chemical the extract dereplication obtained approachesfrom fermentation for marine broths natural of this products strain [ 13contained], it was determinedlobophorins thatA and the B, extract together obtained with a new from member fermentation of the lobophorin broths of this family. strain After contained targeted lobophorins isolation, we A andhave B, shown together that with this a new new compound, member of thelobophorin lobophorin K, displays family. After cytotoxic targeted activities isolation, against we havetwo human shown thattumor this cell new lines, compound, particularly lobophorin pancreatic K, carcinoma displays cytotoxic and breast activities adenocarcinoma against two and human it also tumor presents cell lines,moderate particularly and selective pancreatic antibiotic carcinoma activity and against breast pathogenic adenocarcinoma Gram‐positive and it also bacteria presents such moderate as S. aureus and. selective antibiotic activity against pathogenic Gram-positive bacteria such as S. aureus. 2. Results 2. Results 2.1. Taxonomy and Phylogenetic Analysis of the Strain M‐207 2.1. Taxonomy and Phylogenetic Analysis of the Strain M-207 The 16S rDNA of producing strain M‐207 was amplified by polymerase chain reaction (PCR) The 16S rDNA of producing strain M-207 was amplified by polymerase chain reaction (PCR) and and sequenced [12]. After Basic Logic Alignment Search Tool (BLAST) sequence comparison strain sequenced [12]. After Basic Logic Alignment Search Tool (BLAST) sequence comparison strain M-207 M‐207 showed 99.89% (920/921) identities to Streptomyces carnosus NBRC 13025T, Streptomyces showed 99.89% (920/921) identities to Streptomyces carnosus NBRC 13025T, Streptomyces olivaceus NRRL olivaceus NRRL B‐3009T, and Stresptomyces pactum NBRC 13433T. The phylogenetic tree generated by B-3009T, and Stresptomyces pactum NBRC 13433T. The phylogenetic tree generated by a neighbor-joining a neighbor‐joining method based on 16S rDNA sequence clearly revealed the evolutionary method based on 16S rDNA sequence clearly revealed the evolutionary relationship of the strain M-207 relationship of the strain M‐207 with these three known Streptomyces species (Figure 1). So, in the with these three known Streptomyces species (Figure1). So, in the absence of further taxonomic analysis absence of further taxonomic analysis the strain was designated as Streptomyces sp. M‐207. the strain was designated as Streptomyces sp. M-207. Figure 1. Neighbor-joiningNeighbor‐joining treetree based based on on 16 16 S S rDNA rDNA sequence sequence of of strain strain M-207 M‐207 and and the the closest closest strains strains of theof the genus genusStreptomyces Streptomyces. 2.2. Structure Determination Compound 1 had a molecular formula of C61H92N2O20 according to the protonated ion at m/z 1173.6322 observed in its ESI‐TOF spectrum (calc. for C61H93N2O20+, 1173.6316, ∆ 0.5 ppm). Signals Mar. Drugs 2017, 15, 144 3 of 8 2.2. Structure
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