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Bioactive Nitrogenous Secondary Metabolites from the Marine Sponge Genus Haliclona

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Bioactive Nitrogenous Secondary Metabolites from the Marine Sponge Genus Haliclona marine drugs Review Bioactive Nitrogenous Secondary Metabolites from the Marine Sponge Genus Haliclona Jiaying Zhu, Yang Liu, Zijun Liu, Hao Wang and Huawei Zhang * School of Pharmaceutical Sciences, Zhejiang University of Technology, Hangzhou 310014, China; [email protected] (J.Z.); [email protected] (Y.L.); [email protected] (Z.L.); [email protected] (H.W.) * Correspondence: [email protected]; Tel.: +86-571-8832-0613 Received: 12 November 2019; Accepted: 2 December 2019; Published: 3 December 2019 Abstract: Marine sponge genus Haliclona, one of the most prolific sources of natural products, contains over 600 species but only a small part of them had been classified and chemically investigated. On the basis of extensive literature search, this review firstly summarizes 112 nitrogenous secondary metabolites from classified and unclassified Haliclona sponges as well as from their symbiotic microorganisms. Most of these substances have only been found in Haliclona sponges, and display diverse bioactive properties with potential applications in new drug discovery. Keywords: marine sponge; Haliclona; symbiotic microbe; secondary metabolite; alkaloid; bioactivity 1. Introduction The marine environment is the largest treasure trove of creatures, including plants, animals and microorganisms. People never stop conducting chemical studies of marine organisms owing to their potential capability to produce bioactive secondary metabolites that are potential sources of leads for new drug development. So far over 34,000 articles about marine-derived natural products research have been published [1]. Marine sponges, which are immemorial organisms, are widely distributed around the world and comprise over ten thousand species, most of which them live in the sea, while only one percent are freshwater sponges [2]. These creatures are a great source of natural products with a broad spectrum of biological properties. Numerous sponge-derived chemicals, especial alkaloid compounds, display pharmacological effects, such as didemnin B, cytarabine, trabectedin, vidarabine, etc. The marine sponge genus Haliclona belongs to the family Chalinidae, order Haplosclerida, class Demospongiae [3]. Its skeleton is made up of grids of single spines or a network of spongy fibrous branches without an epidermal skeleton [2]. The Haliclona genus consists of over 600 species distributed throughout the world [3]. However, only a few dozen specimens collected from the Pacific Ocean [4], north Indian Ocean [5], Atlantic Ocean [6], and Mediterranean Sea [7] have been chemically investigated. These studies suggest that Haliclona sponges are some of the most prolific producers of bioactive secondary metabolites. On the basis of a extensive literature search using SciFinder, this review firstly summarizes all nitrogenous substances from the marine sponge genus Haliclona and its symbiotic microbes. 2. Bioactive Alkaloids from Haliclona Genus As many as 103 alkaloid secondary metabolites have been isolated and characterized from Haliclona sponges since 1994. However, only 32 of them (compounds 1–32) were from seven classified Haliclona species including H. baeri, H. cymaeformis, H. densaspicula, H. exigua, H. koremella, H. nigra and H. tulearensis, and are respectively introduced in detail according to their biological sources. Other alkaloids (compounds 33–103) from unclassified Haliclona sponges are grouped into Mar. Drugs 2019, 17, 682; doi:10.3390/md17120682 www.mdpi.com/journal/marinedrugs Mar.Mar. Drugs Drugs 2019 2019, ,17 17, ,x x FOR FOR PEER PEER REVIEW REVIEW 22 ofof 1313 HaliclonaMar.Haliclona Drugs 2019 speciesspecies, 17, 682 includingincluding H.H. baeri,baeri, H.H. cymaeformis,cymaeformis, H.H. densaspicula,densaspicula, H.H. exigua,exigua, H.H. koremelkoremella,la, H.H. 2 nigranigra of 13 andand H.H. tulearensistulearensis,, andand areare respectivelyrespectively introducedintroduced inin detaildetail accordingaccording toto theirtheir biologicalbiological sourcessources.. OtherOther alkaloids alkaloids ( (compoundscompounds 3 333--101033)) from from unclassified unclassified Haliclona Haliclona sponge spongess are are grouped grouped into into three three types types three types on basis of their chemical structures, namely 3-alkylpyridine, amide and depsipeptide, onon basisbasis ofof theirtheir chemicalchemical structures,structures, namelynamely 33--alkylpyridine,alkylpyridine, amideamide andand depsipeptide,depsipeptide, andand and miscellaneous alkaloids. miscellaneousmiscellaneous alkaloidalkaloidss.. 2.1. Haliclona Baeri 2.1.2.1. HaliclonaHaliclona BaeriBaeri There is only one report on a chemical study of Haliclona baeri collected from the coast of Jongbrii ThereThere is is only only one one report report on on a a chemical chemical study study of of Haliclona Haliclona baeri baeri collected collected from from the the coast coast of of Jongbrii Jongbrii Province (Thailand) [8]. One new nitrogenated compound maleimide-5-oxime (1) along with one ProvinceProvince (Thailand)(Thailand) [8].[8]. OneOne newnew nitrogenatednitrogenated compoundcompound mamaleimideleimide--55--oximeoxime ((11)) alongalong withwith oneone benzoic derivative and two tetillapyrones was separated from this sponge (Figure1). The follow-up benzoicbenzoic derivativederivative andand twotwo tetillapyronestetillapyrones waswas separatedseparated fromfrom thisthis spongesponge ((FigureFigure 11)).. TheThe followfollow--upup bioassay tests suggested that compound 1 had weak cytotoxic activity against the human DAOY bbioassayioassay testtestss suggestsuggesteded thatthat compoundcompound 11 hadhad weakweak cytotoxiccytotoxic activityactivity againstagainst thethe humanhuman DAOYDAOY medulloblastoma cell line at 50 µg/mL [9]. medulloblastomamedulloblastoma cellcell lineline atat 5050 μμg/mLg/mL [9][9].. 11 FigureFigureFigure 1. 1 1.Chemical .Chemical Chemical structure structure structure of of of compound compound compound1 1from1 from fromHaliclona Haliclona Haliclona baeri baeri baeri. 2.2.2.2. Haliclona Haliclona CymaeformisCymaeformis FractionationFractionation of of the the ethanol ethanol extract extract of of HaliclonaHaliclona cymaeformis cymaeformis collectedcollected from from a a XuwenXuwen coral coral reefreef (Guangdong,(Guangdong(Guangdong,, China) China) using using silica silica gel gel column column chromatographychromatography led ledled to toto isolationisolation of ofof eleveneleven alkaloid alkaloids,alkaloids,s, includingincluding oneone indoleindole alkaloidalkaloid 2 2,,, sixsix nucleosidesnucleosidenucleosidess 3 3––88 and and four four sterols sterols (Figure(Figure2 2) )[2) [10]. [10].10]. SubsequentlySubsequently two two pairspairs ofof 6-oxypurine66--oxypurineoxypurine regioisomersregioisomers substitutedsubstituted atat thethe 77 oror 99 positionposition (compounds(compounds 99––1212)) werewere purifiedpurifiedpurified fromfrom thethe samesame specimensspecimenpecimen (Figure(Figure2 2))[2) 11[11].[11].]. 22 33 R R = = H H 55 R R = = H H 77 R R = = H H 4 R = CH3 6 R = CH3 8 R = CH3 4 R = CH3 6 R = CH3 8 R = CH3 99 1010 1111 1212 Figure 2. Chemical structures of compounds 2–12 from Haliclona cymaeformis. FigureFigure 2.2. Chemical structures of compounds 22––1212from fromHaliclona Haliclona cymaeformiscymaeformis.. 2.3.2.3. Haliclona Haliclona DensaspiculaDensaspicula TwoTwo novel novelnovel alkaloidsalkaloids withwith with sixsix six hexacyclichexacyclic hexacyclic diamines,diamines, diamines, densaninsdensanins densanins AA ((13 A13)) ( and13and) andBB ((1414 B)) (Figure(Figure (14) (Figure 3)3),, werewere3), werefoundfound found in in methanol methanol in methanol extract extract extract ofof the the of sponge sponge the sponge HaliclonaHaliclonaHaliclona densaspicula densaspicula densaspicula from from fromKeomun Keomun Keomun Island Island Island (Korea) (Korea) (Korea) and and their their and absolutetheirabsolute absolute chemicalchemical chemical structuresstructures structures werewere were determineddetermined determined byby by1D1D 1D andand and 2D2D 2D NMRNMR NMR spectralspectral spectral analysisanalysis analysis andand Mosher MosherMosher reactionreactions.reactionss.. Bio BiologicalBiologicallogical evaluation evaluationevaluation indicatedindicated that that compounds compounds 1313 and and 14 14 possess possess potent potent inhibitory inhibitory effects eeffectsffects on lipopolysaccharide-induced nitric oxide production in BV2 microglial cells with IC50 values of 1.05 onon lipopolysaccharide-inducedlipopolysaccharide-induced nitric nitric oxide oxide production production in in BV2 BV2 microglial microglial cells cells with with IC IC5050values values ofof 1.051.05 and 2.14 μM, respectively [4,12]. Mar.andand Drugs 2.142.14 µ2019μM,M,, respectively17respectively, x FOR PEER [ [4,12].4REVIEW,12]. 3 of 13 13 14 densaspicula. FigureFigure 3 3.. ChemicalChemical structures structures of of compounds compounds 1313––14 from Haliclona densaspicula. 2.4. Haliclona Exigua Chemical study of the sponge specimen Haliclona exigua collected from the coastal areas of India and Indonesia afforded nine alkaloid derivatives, including xestospongin D (15), araguspongins C-E (16–18), 3α-methylaraguspongine C (19), neopetrocyclamines A (20) and B (21), papuamine (22) and haliclonadiamine (23) (Figure 4) [5,13–17]. Compound 16 was the most common alkaloid from H. exigua and shown to have strong inhibitory activity against human lymphatic filarial parasite B, promastigote and intracellular amastigote forms of Leishmania donovani, and anti-fouling
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