Marine biomaterials: Biomimetic and pharmacological potential of cultivated Aplysina aerophoba marine demosponge

Björn Binnewerg; Mario Schubert; Alona Voronkina; Liubov Muzychka; Marcin Wysokowski; Iaroslav Petrenko; Mirko Djurović; Valentine Kovalchuk; Mikhail Tsurkan; Rajko Martinovic; Nicole Bechmann; Andriy Fursov; Viatcheslav N Ivanenko; Konstantin R Tabachnick; Oleg B Smolii; Yvonne Joseph; Marco Giovine; Stefan R Bornstein; Allison L Stelling; Antje Tunger; Marc Schmitz; Olga S Taniya; Igor S Kovalev; Grigory V Zyryanov; Kaomei Guan; Hermann Ehrlich

doi:10.1016/j.msec.2019.110566

Marine biomaterials: Biomimetic and pharmacological potential of cultivated Aplysina aerophoba marine demosponge

Mater Sci Eng C Mater Biol Appl. 2020 Apr:109:110566. doi: 10.1016/j.msec.2019.110566. Epub 2019 Dec 17.

Authors

Björn Binnewerg¹, Mario Schubert¹, Alona Voronkina², Liubov Muzychka³, Marcin Wysokowski⁴, Iaroslav Petrenko⁵, Mirko Djurović⁶, Valentine Kovalchuk⁷, Mikhail Tsurkan⁸, Rajko Martinovic⁶, Nicole Bechmann⁹, Andriy Fursov⁵, Viatcheslav N Ivanenko¹⁰, Konstantin R Tabachnick¹¹, Oleg B Smolii³, Yvonne Joseph⁵, Marco Giovine¹², Stefan R Bornstein¹³, Allison L Stelling¹⁴, Antje Tunger¹⁵, Marc Schmitz¹⁵, Olga S Taniya¹⁶, Igor S Kovalev¹⁷, Grigory V Zyryanov¹⁶, Kaomei Guan¹⁸, Hermann Ehrlich¹⁹

Affiliations

¹ Institute of Pharmacology and Toxicology, Technische Universität Dresden, Dresden 01307, Germany.
² Department of Pharmacy, National Pirogov Memorial Medical University, Vinnytsya 21018, Ukraine.
³ V.P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry, National Academy of Sciences of Ukraine, Kyiv 02094, Ukraine.
⁴ Institute of Chemical Technology and Engineering, Faculty of Chemical Technology, Poznan University of Technology, Poznan 60-965, Poland; Institute of Electronics and Sensor Materials, Technische Universität Bergakademie Freiberg, Freiberg 09599, Germany. Electronic address: Marcin.Wysokowski@put.poznan.pl.
⁵ Institute of Electronics and Sensor Materials, Technische Universität Bergakademie Freiberg, Freiberg 09599, Germany.
⁶ Institute of Marine Biology, University of Montenegro, Kotor 85330, Montenegro.
⁷ Department of Microbiology, National Pirogov Memorial Medical University, Vinnytsya 21018, Ukraine.
⁸ Leibniz Institute of Polymer Research Dresden, Dresden 01069, Germany.
⁹ Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Carl Gustav Carus, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Dresden 01307, Germany.
¹⁰ Department of Invertebrate Zoology, Biological Faculty, Lomonosov Moscow State University, Moscow 119992, Russia.
¹¹ P.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow 117997, Russia; International Institute of Biomineralogy GmbH, Freiberg 09599, Germany.
¹² Department of Sciences of Earth, Environment and Life, University of Genoa, Genova 16132, Italy.
¹³ Department of Internal Medicine III, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden 01307, Germany; Diabetes and Nutritional Sciences Division, King's College London, London WC2R 2LS, UK.
¹⁴ Duke University Medical Center, Department of Biochemistry, Durham, NC, USA.
¹⁵ National Center for Tumor Diseases, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden 01307, Germany; Institute of Immunology, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Dresden 01307, Germany.
¹⁶ Department of Organic and Biomolecular Chemistry, Chemical Engineering Institute, Ural Federal University named after the first President of Russia B. N. Yeltsin, Yekaterinburg 620002, Russia; Postovsky Institute of Organic Synthesis, Ural Branch of the Russian Academy of Sciences, Yekaterinburg 620219, Russia.
¹⁷ Department of Organic and Biomolecular Chemistry, Chemical Engineering Institute, Ural Federal University named after the first President of Russia B. N. Yeltsin, Yekaterinburg 620002, Russia.
¹⁸ Institute of Pharmacology and Toxicology, Technische Universität Dresden, Dresden 01307, Germany. Electronic address: Kaomei.Guan@tu-dresden.de.
¹⁹ Institute of Electronics and Sensor Materials, Technische Universität Bergakademie Freiberg, Freiberg 09599, Germany. Electronic address: Hermann.Ehrlich@esm.tu-freiberg.de.

PMID: 32228987
DOI: 10.1016/j.msec.2019.110566

Abstract

Marine demosponges of the Verongiida order are considered a gold-mine for bioinspired materials science and marine pharmacology. The aim of this work was to simultaneously isolate selected bromotyrosines and unique chitinous structures from A. aerophoba and to propose these molecules and biomaterials for possible application as antibacterial and antitumor compounds and as ready-to-use scaffolds for cultivation of cardiomyocytes, respectively. Among the extracted bromotyrosines, the attention has been focused on aeroplysinin-1 that showed interesting unexpected growth inhibition properties for some Gram-negative clinical multi-resistant bacterial strains, such as A. baumannii and K. pneumoniae, and on aeroplysinin-1 and on isofistularin-3 for their anti-tumorigenic activity. For both compounds, the effects are cell line dependent, with significant growth inhibition activity on the neuroblastoma cell line SH-SY5Y by aeroplysinin-1 and on breast cancer cell line MCF-7 by isofistularin-3. In this study, we also compared the cultivation of human induced pluripotent stem cell-derived cardiomyocytes (iPSC-CMs) on the A. aerophoba chitinous scaffolds, in comparison to chitin structures that were pre-coated with Geltrex™, an extracellular matrix mimetic which is used to enhance iPSC-CM adhesion. The iPSC-CMs on uncoated and pure chitin structures started contracting 24 h after seeding, with comparable behaviour observed on Geltrex-coated cell culture plates, confirming the biocompatibility of the sponge biomaterial with this cell type. The advantage of A. aerophoba is that this source organism does not need to be collected in large quantities to supply the necessary amount for further pre-clinical studies before chemical synthesis of the active compounds will be available. A preliminary analysis of marine sponge bioeconomy as a perspective direction for application of biomaterials and secondary bioactive metabolites has been finally performed for the first time.

Keywords: Aeroplysinin-1; Cardiomyocytes; Cell culture; Chitin; Marine biomaterials; Tissue engineering.

MeSH terms

Acetonitriles* / chemistry
Acetonitriles* / pharmacokinetics
Acetonitriles* / pharmacology
Alkaloids* / chemistry
Alkaloids* / pharmacokinetics
Alkaloids* / pharmacology
Animals
Aquatic Organisms / chemistry*
Biomimetic Materials* / chemistry
Biomimetic Materials* / pharmacokinetics
Biomimetic Materials* / pharmacology
Cell Line, Tumor
Cyclohexenes* / chemistry
Cyclohexenes* / pharmacokinetics
Cyclohexenes* / pharmacology
Delayed-Action Preparations / chemistry
Delayed-Action Preparations / pharmacokinetics
Humans
Induced Pluripotent Stem Cells / cytology
Induced Pluripotent Stem Cells / metabolism*
MCF-7 Cells
Myocytes, Cardiac / cytology
Myocytes, Cardiac / metabolism*
Porifera / chemistry*

Substances

Acetonitriles
Alkaloids
Cyclohexenes
Delayed-Action Preparations
isofistularin-3
aeroplysinin I