Does the Chemical Diversity of the Order Haplosclerida (Phylum Porifera: Class Demospongia) Fit with Current Taxonomic Classification?

Abstract

Sponges and their associated microbiota are well known to produce a large diversity of natural products, also called specialized metabolites. In addition to their potential use in the pharmaceutical industry, these rather species-specific compounds may help in the classification of some particular sponge groups. We review herein compounds isolated from haplosclerid sponges (Class Demospongia, Order Haplosclerida) in order to help in the revision of this large group of marine invertebrates. We focus only on 3-alkylpyridine derivatives and polyacetylenic compounds, as these two groups of natural products are characteristic of haplosclerid species and are highly diverse. A close collaboration between chemists and biologists is required in order to fully apply chemotaxonomical approaches, and whenever possible biological data should include morphological and molecular data and some insight into their microbial abundance.

Key words

sponges - Haplosclerida - alkaloids - polyacetylenic - chemotaxonomy

• References

• 1 Zhang F, Blasiak LC, Karolin JO, Powell RJ, Geddes CD, Hill RT. Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges. Proc Natl Acad Sci USA 2015; 112: 4381-4386
• 2 De Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, de Goeij AF, Admiraal W. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 2013; 342: 108-110
• 3 Genta-Jouve G, Thomas OP. Sponge chemical diversity: from biosynthetic pathways to ecological roles. Adv Mar Biol 2012; 62: 183-230
• 4 Cardenas P, Perez T, Boury-Esnault N. Sponge systematics facing new challenges. Adv Mar Biol 2012; 61: 79-209
• 5 Van Soest RM, Hooper JA. Order Haplosclerida Topsent, 1928. In: Hooper JA, Van Soest RM, Willenz P, editors Systema Porifera – A guide to the classification of sponges. New York: Springer US; 2002: 831-832
• 6 Fromont J, Kerr S, Kerr R, Riddle M, Murphy P. Chemotaxonomic relationships within, and comparisons between, the orders Haplosclerida and Petrosida (Porifera: Demospongiae) using sterol complements. Biochem Syst Ecol 1994; 22: 735-752
• 7 Andersen RJ, van Soest RWM, Kong F. 3-Alkylpiperidine alkaloids isolated from marine sponges in the order Haplosclerida. In: Pelletier SW, editor Alkaloids: chemical and biological perspectives. Oxford: Pergamon Press; 1996: 301-355
• 8 Redmond NE, Raleigh J, van Soest RWM, Kelly M, Travers SAA, Bradshaw B, Vartia S, Stephens KM, McCormack GP. Phylogenetic relationships of the marine Haplosclerida (Phylum Porifera) employing ribosomal (28 S rRNA) and mitochondrial cox1, nad1 gene sequence data. PLoS One 2011; 6: e24344
• 9 Van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K, de Voogd NJ, Alvarez de Glasby B, Hajdu E, Pisera AB, Manconi R, Schoenberg C, Janussen D, Tabachnick KR, Klautau M, Picton B, Kelly M, Vacelet J, Dohrmann M, Díaz MC, Cárdenas P. World Porifera database. Available at: http://www.marinespecies.org/porifera Accessed September 1, 2015
• 10 Tsukamoto S, Takahashi M, Matsunaga S, Fusetani N, Van Soest RW. Hachijodines A–G: seven new cytotoxic 3-alkylpyridine alkaloids from two marine sponges of the genera Xestospongia and Amphimedon . J Nat Prod 2000; 63: 682-684
• 11 Takekawa Y, Matsunaga S, van Soest RW, Fusetani N. Amphimedosides, 3-alkylpyridine glycosides from a marine sponge Amphimedon sp. J Nat Prod 2006; 69: 1503-1505
• 12 Hirano K, Kubota T, Tsuda M, Mikami Y, Kobayashi J. Pyrinodemins B–D, potent cytotoxic bis-pyridine alkaloids from marine sponge Amphimedon sp. Chem Pharm Bull (Tokyo) 2000; 48: 974-977
• 13 Tsuda M, Hirano K, Kubota T, Kobayashi J. Pyrinodemin A, a cytotoxic pyridine alkaloid with an isoxazolidine moiety from sponge Amphimedon sp. Tetrahedron Lett 1999; 40: 4819-4820
• 14 Kubota T, Kura K, Fromont J, Kobayashi J. Pyrinodemins G–I, new bis-3-alkylpyridine alkaloids from a marine sponge Amphimedon sp. Tetrahedron 2013; 69: 96-100
• 15 Kura K, Kubota T, Fromont J, Kobayashi J. Pyrinodemins E and F, new 3-alkylpyridine alkaloids from sponge Amphimedon sp. Bioorg Med Chem Lett 2011; 21: 267-270
• 16 Nishi T, Kubota T, Fromont J, Sasaki T, Kobayashi J. Nakinadines B–F: new pyridine alkaloids with a β-amino acid moiety from sponge Amphimedon sp. Tetrahedron 2008; 64: 3127-3132
• 17 Quiñoà E, Crews P. Niphatynes, methoxylamine pyridines from the marine sponge, Niphates sp. Tetrahedron Lett 1987; 28: 2467-2468
• 18 Kobayashi J, Zeng CM, Ishibashi M, Shigemori H, Sasaki T, Mikami Y. Niphatesines E–H, new pyridine alkaloids from the Okinawan marine sponge Niphates sp. J Chem Soc Perkin 1 1992; 11: 1291-1294
• 19 Kobayashi J, Murayama T, Kosuge S, Kanda F, Ishibashi M, Kobayashi H, Ohizumi Y, Ohta T, Nozoe S, Sasaki T. Niphatesines A–D, new antineoplastic pyridine alkaloids from the Okinawan marine sponge Niphates sp. J Chem Soc Perkin 1 1990; 12: 3301-3303
• 20 Kariya Y, Kubota T, Fromont J, Kobayashi J. Pyrinadines B–G, new bis-pyridine alkaloids with an azoxy moiety from sponge Cribrochalina sp. Bioorg Med Chem 2006; 14: 8415-8419
• 21 Kariya Y, Kubota T, Fromont J, Kobayashi J. Pyrinadine A, a novel pyridine alkaloid with an azoxy moiety from sponge Cribrochalina sp. Tetrahedron Lett 2006; 47: 997-998
• 22 Redmond NE, Morrow CC, Thacker RW, Diaz MC, Boury-Esnault N, Cárdenas P, Hajdu E, Lôbo-Hajdu G, Picton BE, Pomponi SA, Kayal E, Collins AG. Phylogeny and systematics of Demospongiae in light of new small-subunit ribosomal DNA (18 S) sequences. Integr Comp Biol 2013; 53: 388-415
• 23 Xu NJ, Sun X, Yan XJ. A new cyclostellettamine from sponge Amphimedon compressa . Chin Chem Lett 2007; 18: 947-950
• 24 Schmitz FJ, Hollenbeak KH, Campbell DC. Marine natural products: halitoxin, toxic complex of several marine sponges of the genus Haliclona . J Org Chem 1978; 43: 3916-3922
• 25 Thompson MN, Gallimore WA, Townsend MM, Chambers NA, Williams LA. Bioactivity of amphitoxin, the major constituent of the Jamaican sponge Amphimedon compressa . Chem Biodivers 2010; 7: 1904-1910
• 26 Albrizio S, Ciminiello P, Fattorusso E, Magno S, Pawlik JR. Amphitoxin, a new high molecular weight antifeedant pyridinium salt from the caribbean sponge Amphimedon compressa . J Nat Prod 1995; 58: 647-652
• 27 Talpir R, Rudi A, Ilan M, Kashman Y. Niphatoxin A and B; two new ichthyo- and cytotoxic tripyridine alkaloids from a marine sponge. Tetrahedron Lett 1992; 33: 3033-3034
• 28 De Oliveira JH, Grube A, Köck M, Berlinck RG, Macedo ML, Ferreira AG, Hajdu E. Ingenamine G and cyclostellettamines GI, K, and L from the new Brazilian species of marine sponge Pachychalina sp. J Nat Prod 2004; 67: 1685-1689
• 29 De Oliveira JH, Seleghim MH, Timm C, Grube A, Köck M, Nascimento GG, Martins ACT, Silva EG, de Souza AO, Minarini PR. Antimicrobial and antimycobacterial activity of cyclostellettamine alkaloids from sponge Pachychalina sp. Mar Drugs 2006; 4: 1-8
• 30 Laville R, Thomas OP, Berrue F, Reyes F, Amade P. Pachychalines A–C: novel 3-alkylpyridinium salts from the marine sponge Pachychalina sp. European J Org Chem 2008; 2008: 121-125
• 31 Buchanan MS, Carroll AR, Addepalli R, Avery VM, Hooper JNA, Quinn RJ. Niphatoxin C, a cytotoxic tripyridine alkaloid from Callyspongia sp. J Nat Prod 2007; 70: 2040-2041
• 32 Torres YR, Berlinck RG, Magalhães A, Schefer AB, Ferreira AG, Hajdu E, Muricy G. Arenosclerins A–C and haliclonacyclamine E, new tetracyclic alkaloids from a Brazilian endemic Haplosclerid sponge Arenosclera brasiliensis . J Nat Prod 2000; 63: 1098-1105
• 33 Torres YR, Berlinck RG, Nascimento GG, Fortier SC, Pessoa C, de Moraes MO. Antibacterial activity against resistant bacteria and cytotoxicity of four alkaloid toxins isolated from the marine sponge Arenosclera brasiliensis . Toxicon 2002; 40: 885-891
• 34 Thacker RW, Hill AL, Hill MS, Redmond NE, Collins AG, Morrow CC, Spicer L, Carmack CA, Zappe ME, Pohlmann D, Hall C, Diaz MC, Bangalore PV. Nearly complete 28 S rRNA gene sequences confirm new hypotheses of sponge evolution. Integr Comp Biol 2013; 53: 373-387
• 35 Schmidt G, Timm C, Koeck M. Haliclocyclin C, a new monomeric 3-alkyl pyridinium alkaloid from the arctic marine sponge Haliclona viscosa . Z Naturforsch B 2011; 66: 745-748
• 36 Timm C, Volk C, Sasse F, Köck M. The first cyclic monomeric 3-alkylpyridinium alkaloid from natural sources: identification, synthesis, and biological activity. Org Biomol Chem 2008; 6: 4036-4040
• 37 Schmidt G, Timm C, Grube A, Volk CA, Köck M. Viscosalines B(1,2) and E(1,2): challenging new 3-alkyl pyridinium alkaloids from the marine sponge Haliclona viscosa . Chemistry 2012; 18: 8180-8189
• 38 Volk CA, Köck M. Viscosamine: the first naturally occurring trimeric 3-alkyl pyridinium alkaloid. Org Lett 2003; 5: 3567-3569
• 39 Teruya T, Kobayashi K, Suenaga K, Kigoshi H. Cyclohaliclonamines A–E: dimeric, trimeric, tetrameric, pentameric, and hexameric 3-alkyl pyridinium alkaloids from a marine sponge Haliclona sp. J Nat Prod 2006; 69: 135-137
• 40 Casapullo A, Pinto OC, Marzocco S, Autore G, Riccio R. 3-Alkylpyridinium alkaloids from the pacific sponge Haliclona sp. J Nat Prod 2009; 72: 301-303
• 41 Lee Y, Jang KH, Jeon JE, Yang WY, Sim CJ, Oh KB, Shin J. Cyclic Bis-1, 3-dialkylpyridiniums from the sponge Haliclona sp. Mar Drugs 2012; 10: 2126-2137
• 42 Damodaran V, Ryan JL, Keyzers RA. Cyclic 3-alkyl pyridinium alkaloid monomers from a New Zealand Haliclona -++-. marine sponge. J Nat Prod 2013; 76: 1997-2001
• 43 Laville R, Genta-Jouve G, Urda C, Fernandez R, Thomas OP, Reyes F, Amade P. Njaoaminiums A, B, and C: cyclic 3-alkylpyridinium salts from the marine sponge Reniera sp. Molecules 2009; 14: 4716-4724
• 44 Laville R, Amade P, Thomas OP. 3-Alkylpyridinium salts from Haplosclerida marine sponges: isolation, structure elucidations, and biosynthetic considerations. Pure Appl Chem 2009; 81: 1033-1040
• 45 Baker BJ, Scheuer PJ, Shoolery JN. Papuamine, an antifungal pentacyclic alkaloid from a marine sponge, Haliclona sp. J Am Chem Soc 1988; 110: 965-966
• 46 Fahy E, Molinski TF, Harper MK, Sullivan BW, Faulkner DJ, Parkanyi L, Clardy J. Haliclonadiamine, an antimicrobial alkaloid from the sponge Haliclona sp. Tetrahedron Lett 1988; 29: 3427-3428
• 47 Kashman Y, Koren-Goldshlager G, Gravalos MDG, Schleyer M. Halitulin, a new cytotoxic alkaloid from the marine sponge Haliclona tulearensis . Tetrahedron Lett 1999; 40: 997-1000
• 48 Sorek H, Rudi A, Aknin M, Gaydou EM, Kashman Y. Isohalitulin and haliclorensins B and C, three marine alkaloids from Haliclona tulearensis . J Nat Prod 2010; 73: 456-458
• 49 Heinrich MR, Kashman Y, Spiteller P, Steglich W. Revision of the structure of haliclorensin to (S)-7-methyl-1,5-diazacyclotetradecane and confirmation of the new structure by synthesis. Tetrahedron 2001; 57: 9973-9978
• 50 Koren-Goldshlager G, Kashman Y, Schleyer M. Haliclorensin, a novel diamino alkaloid from the marine sponge Haliclona tulearensis . J Nat Prod 1998; 61: 282-284
• 51 Fusetani N, Yasumuro K, Matsunaga S, Hirota H. Haliclamines A and B, cytotoxic macrocyclic alkaloids from a sponge of the genus Haliclona . Tetrahedron Lett 1989; 30: 6891-6894
• 52 Schmidt G, Timm C, Kock M. New haliclamines E and F from the Arctic sponge Haliclona viscosa . Org Biomol Chem 2009; 7: 3061-3064
• 53 Volk CA, Lippert H, Lichte E, Köck M. Two new haliclamines from the Arctic sponge Haliclona viscosa . European J Org Chem 2004; 2004: 3154-3158
• 54 Cychon C, Schmidt G, Mordhorst T, Koeck M. Structure elucidation of submilligram quantities of natural products – application to haliclamines G and H from the Arctic marine sponge Haliclona viscosa . Z Naturforsch B 2012; 67: 944-950
• 55 Jaspars M, Pasupathy V, Crews P. A tetracyclic diamine alkaloid, halicyclamine A, from the marine sponge Haliclona sp. J Org Chem 1994; 59: 3253-3255
• 56 Arai M, Liu L, Fujimoto T, Setiawan A, Kobayashi M. DedA protein relates to action-mechanism of halicyclamine A, a marine spongean macrocyclic alkaloid, as an anti-dormant mycobacterial substance. Mar Drugs 2011; 9: 984-993
• 57 Arai M, Sobou M, Vilchéze C, Baughn A, Hashizume H, Pruksakorn P, Ishida S, Matsumoto M, Jacobs jr. WR, Kobayashi M. Halicyclamine A, a marine spongean alkaloid as a lead for anti-tuberculosis agent. Bioorg Med Chem 2008; 16: 6732-6736
• 58 Charan RD, Garson MJ, Brereton IM, Willis AC, Hooper JNA. Haliclonacyclamines A and B, cytotoxic alkaloids from the tropical marine sponge Haliclona sp. Tetrahedron 1996; 52: 9111-9120
• 59 Clark RJ, Field KL, Charan RD, Garson MJ, Brereton M, Willis AC. The haliclonacyclamines, cytotoxic tertiary alkaloids from the tropical marine sponge Haliclona sp. Tetrahedron 1998; 54: 8811-8826
• 60 Matsunaga S, Miyata Y, van Soest RW, Fusetani N. Tetradehydrohalicyclamine A and 22-Hydroxyhalicyclamine A, new cytotoxic bis-piperidine alkaloids from a marine sponge Amphimedon sp. J Nat Prod 2004; 67: 1758-1760
• 61 De Oliveira JH, Nascimento AM, Kossuga MH, Cavalcanti BC, Pessoa CO, Moraes MO, Macedo ML, Ferreira AG, Hajdu E, Pinheiro US. Cytotoxic alkylpiperidine alkaloids from the Brazilian marine sponge Pachychalina alcaloidifera . J Nat Prod 2007; 70: 538-543
• 62 Dewi AS, Hadi TA, Fajarningsih ND, Blanchfield JT, Bernhardt PV, Garson MJ. Acanthocyclamine A from the Indonesian marine sponge Acanthostrongylophora ingens . Aust J Chem 2014; 67: 1205-1210
• 63 Nakagawa M, Endo M, Tanaka N, Gen-Pei L. Structures of xestospongin A, B, C and D, novel vasodilative compounds from marine sponge, Xestospongia exigua . Tetrahedron Lett 1984; 25: 3227-3230
• 64 Kobayashi M, Kawazoe K, Kitagawa I. Araguspongines B, C, D, E, F, G, H, and J, new vasodilative bis-1-oxaquinolizidine alkaloids from an Okinawan marine sponge, Xestospongia sp. Chem Pharm Bull (Tokyo) 1989; 37: 1676-1678
• 65 Quirion JC, Sevenet T, Husson HP, Weniger B, Debitus C. Two new alkaloids from Xestospongia sp., a New Caledonian sponge. J Nat Prod 1992; 55: 1505-1508
• 66 Venkateswarlu Y, Reddy MVR, Rao JV. Bis-1-oxaquinolizidines from the sponge Haliclona exigua . J Nat Prod 1994; 57: 1283-1285
• 67 Liu H, Mishima Y, Fujiwara T, Nagai H, Kitazawa A, Mine Y, Kobayashi H, Yao X, Yamada J, Oda T. Isolation of araguspongine M, a new stereoisomer of an araguspongine/xestospongin alkaloid, and dopamine from the marine sponge Neopetrosia exigua collected in Palau. Mar Drugs 2004; 2: 154-163
• 68 Li Y, Qin S, Guo YW, Gu YC, van Soest RW. 9′-Epi-3β, 3′β-dimethylxestospongin C, a new macrocyclic diamine alkaloid from the Hainan sponge Neopetrosia exigua . Planta Med 2011; 77: 179-181
• 69 Wei X, Nieves K, Rodríguez AD. Neopetrosiamine A, biologically active bis-piperidine alkaloid from the Caribbean sea sponge Neopetrosia proxima . Bioorg Med Chem Lett 2010; 20: 5905-5908
• 70 Morinaka BI, Molinski TF. Xestoproxamines A–C from Neopetrosia proxima. Assignment of absolute stereostructure of bis-piperidine alkaloids by integrated degradation-CD analysis. J Nat Prod 2011; 74: 430-440
• 71 Braekman JC, Daloze D, Cimino G, Trivellone E. 2D-NMR study of petrosins: Revised structure for petrosin-A. Bull Soc Chim Belg 1988; 97: 519-524
• 72 Braekman JC, Daloze D, Defay N, Zimmermann D. Petrosin-A and -B, two new bis-quinolizidine alkaloids from the sponge Petrosia seriata . Bull Soc Chim Belg 1984; 93: 941-944
• 73 Defant A, Mancini I, Raspor L, Guella G, Turk T, Sepčić K. New structural insights into saraines A, B, and C, macrocyclic alkaloids from the mediterranean sponge Reniera (Haliclona) sarai . European J Org Chem 2011; 2011: 3761-3767
• 74 Cimino G, Stefano SD, Scognamiglio G, Sodano G, Trivellone E. Sarains: A new class of alkaloids from the marine sponge Reniera sarai . Bull Soc Chim Belg 1986; 95: 783-800
• 75 Caprioli V, Cimino G, de Giulio A, Madaio A, Scognamiglio G, Trivellone E. Selected biological activities of saraines. Comp Biochem Physiol B 1992; 103: 293-296
• 76 Jang KH, Kang GW, Jeon JE, Lim C, Lee HS, Sim CJ, Oh KB, Shin J. Haliclonin A, a new macrocyclic diamide from the sponge Haliclona sp. Org Lett 2009; 11: 1713-1716
• 77 Sorek H, Rudi A, Benayahu Y, Kashman Y. Njaoamines G and H, two new cytotoxic polycyclic alkaloids and a tetrahydroquinolone from the marine sponge Neopetrosia sp . Tetrahedron Lett 2007; 48: 7691-7694
• 78 Reyes F, Fernández R, Urda C, Francesch A, Bueno S, de Eguilior C, Cuevas C. Njaoamines A–F, new cytotoxic polycyclic alkaloids from the haplosclerid sponge Reniera sp. Tetrahedron 2007; 63: 2432-2438
• 79 Hwang BS, Oh JS, Jeong EJ, Sim CJ, Rho JR. Densanins A and B, new macrocyclic pyrrole alkaloids isolated from the marine sponge Haliclona densaspicula . Org Lett 2012; 14: 6154-6157
• 80 Cavalcanti BC, Sombra CML, de Oliveira JH, Berlinck RG, de Moraes MO, Pessoa C. Cytotoxicity and genotoxicity of ingenamine G isolated from the Brazilian marine sponge Pachychalina alcaloidifera . Comp Biochem Physiol C Toxicol Pharmacol 2008; 147: 409-415
• 81 Sakai R, Kohmoto S, Higa T, Jefford CW, Bernardinelli G. Manzamine B and C, two novel alkaloids from the sponge Haliclona sp. Tetrahedron Lett 1987; 28: 5493-5496
• 82 Sakai R, Higa T, Jefford CW, Bernardinelli G. Manzamine A, a novel antitumor alkaloid from a sponge. J Am Chem Soc 1986; 108: 6404-6405
• 83 Ashok P, Ganguly S, Murugesan S. Manzamine alkaloids: isolation, cytotoxicity, antimalarial activity and SAR studies. Drug Discov Today 2014; 19: 1781-1791
• 84 Kobayashi M, Chen YJ, Aoki S, In Y, Ishida T, Kitagawa I. Four new β-carboline alkaloids isolated from two Okinawan marine sponges of Xestospongia sp. and Haliclona sp. Tetrahedron 1995; 51: 3727-3736
• 85 Nakamura H, Deng S, Kobayashi J, Ohizumi Y, Tomotake Y, Matsuzaki T, Hirata Y. Keramamine-A and -B, novel antimicrobial alkaloids from the Okinawan marine sponge Pellina sp. Tetrahedron Lett 1987; 28: 621-624
• 86 Ichiba T, Sakai R, Kohmoto S, Saucy G, Higa T. New manzamine alkaloids from a sponge of the genus Xestospongia . Tetrahedron Lett 1988; 29: 3083-3086
• 87 Kobayashi J, Tsuda M, Kawasaki N, Sasaki T, Mikami Y. 6-Hydroxymanzamine A and 3, 4-dihydromanzamine A, new alkaloids from the Okinawan marine sponge Amphimedon sp. J Nat Prod 1994; 57: 1737-1740
• 88 Kobayashi J, Tsuda M, Kawasaki N, Matsumoto K, Adachi T. Keramaphidin B, a novel pentacyclic alkaloid from a marine sponge Amphimedon sp.: A plausible biogenetic precursor of manzamine alkaloids. Tetrahedron Lett 1994; 35: 4383-4386
• 89 Tsuda M, Kawasaki N, Kobayashi J. Keramaphidin C and keramamine C plausible biogenetic precursors of manzamine C from an Okinawan marine sponge. Tetrahedron Lett 1994; 35: 4387-4388
• 90 Tsuda M, Kawasaki N, Kobayashi J. Ircinols A and B, first antipodes of manzamine-related alkaloids from an Okinawan marine sponge. Tetrahedron 1994; 50: 7957-7960
• 91 Tsuda M, Inaba K, Kawasaki N, Honma K, Kobayashi J. Chiral resolution of (±)-keramaphidin B and isolation of manzamine L, a new β-carboline alkaloid from a sponge Amphimedon sp. Tetrahedron 1996; 52: 2319-2324
• 92 Watanabe D, Tsuda M, Kobayashi J. Three new manzamine congeners from Amphimedon sponge. J Nat Prod 1998; 61: 689-692
• 93 Takahashi Y, Kubota T, Fromont J, Kobayashi J. Zamamidines A and B, new manzamine alkaloids from the sponge Amphimedon species. Org Lett 2008; 11: 21-24
• 94 Kubota T, Kamijyo Y, Takahashi-Nakaguchi A, Fromont J, Gonoi T, Kobayashi J. Zamamiphidin A, a new manzamine related alkaloid from an Okinawan marine sponge Amphimedon sp. Org Lett 2013; 15: 610-612
• 95 Rao KV, Kasanah N, Wahyuono S, Tekwani BL, Schinazi RF, Hamann MT. Three new manzamine alkaloids from a common Indonesian sponge and their activity against infectious and tropical parasitic diseases. J Nat Prod 2004; 67: 1314-1318
• 96 Rao KV, Donia MS, Peng J, Garcia-Palomero E, Alonso D, Martinez A, Medina M, Franzblau SG, Tekwani BL, Khan SI. Manzamine B and E and ircinal A related alkaloids from an Indonesian Acanthostrongylophora sponge and their activity against infectious, tropical parasitic, and Alzheimerʼs diseases. J Nat Prod 2006; 69: 1034-1040
• 97 Wahba AE, Fromentin Y, Zou Y, Hamann MT. Acantholactone, a new manzamine related alkaloid with an unprecedented δ-lactone and ε-lactam ring system. Tetrahedron Lett 2012; 53: 6329-6331
• 98 El Sayed KA, Kelly M, Kara UAK, Ang KKH, Katsuyama I, Dunbar DC, Khan AA, Hamann MT. New manzamine alkaloids with potent activity against infectious diseases. J Am Chem Soc 2001; 123: 1804-1808
• 99 Samoylenko V, Khan SI, Jacob MR, Tekwani BL, Walker LA, Hufford CD, Muhammad I. Bioactive (+)-manzamine A and (+)-8-hydroxymanzamine A tertiary bases and salts from Acanthostrongylophora ingens and their preparations. Nat Prod Commun 2009; 4: 185-192
• 100 Furusato A, Kato H, Nehira T, Eguchi K, Kawabata T, Fujiwara Y, Losung F, Mangindaan RE, de Voogd NJ, Takeya M. Acanthomanzamines A–E with new manzamine frameworks from the marine sponge Acanthostrongylophora ingens . Org Lett 2014; 16: 3888-3891
• 101 El-Desoky AH, Kato H, Eguchi K, Kawabata T, Fujiwara Y, Losung F, Mangindaan RE, de Voogd NJ, Takeya M, Yokosawa H. Acantholactam and pre-neo-kauluamine, manzamine-related alkaloids from the Indonesian marine sponge Acanthostrongylophora ingens . J Nat Prod 2014; 77: 1536-1540
• 102 Rodríguez J, Crews P. Revised structure of xestocyclamine A and description of a new analogue. Tetrahedron Lett 1994; 35: 4719-4722
• 103 Rodriguez J, Peters BM, Kurz L, Schatzman RC, McCarley D, Lou L, Crews P. An alkaloid protein kinase C inhibitor, xestocyclamine A, from the marine sponge Xestospongia sp. J Am Chem Soc 1993; 115: 10436-10437
• 104 Kong F, Andersen RJ, Allen TM. Ingenamine, a novel pentacyclic alkaloid from the marine sponge Xestospongia ingens . Tetrahedron Lett 1994; 35: 1643-1646
• 105 Kong F, Andersen RJ, Allen TM. Ingamines A and B, new cytotoxic alkaloids from the marine sponge Xestospongia ingens . Tetrahedron 1994; 50: 6137-6144
• 106 Kong F, Andersen RJ, Allen TM. Madangamine A, a novel cytotoxic alkaloid from the marine sponge Xestospongia ingens . J Am Chem Soc 1994; 116: 6007-6008
• 107 Kong F, Andersen RJ. Ingenamine alkaloids isolated from the sponge Xestospongia ingens: Structures and absolute configurations. Tetrahedron 1995; 51: 2895-2906
• 108 Ichiba T, Corgiat JM, Scheuer PJ, Kelly-Borges M. 8-Hydroxymanzamine A, a β-carboline alkaloid from a sponge, Pachypellina sp. J Nat Prod 1994; 57: 168-170
• 109 Umeyama A, Nagano C, Arihara S. Three novel C21 polyacetylenes from the marine sponge Callyspongia sp. J Nat Prod 1997; 60: 131-133
• 110 Youssef DTA, Yoshida WY, Kelly M, Scheuer PJ. Polyacetylenes from a Red Sea sponge Callyspongia species. J Nat Prod 2000; 63: 1406-1410
• 111 Nakao Y, Uehara T, Matunaga S, Fusetani N, van Soest RWM. Callyspongynic acid, a polyacetylenic acid which inhibits α-glucosidase, from the marine sponge Callyspongia truncata . J Nat Prod 2002; 65: 922-924
• 112 Braekman JC, Daloze D, Devijver C, Dubut D, van Soest RWM. A new C-20 polyacetylene from the sponge Callyspongia pseudoreticulata . J Nat Prod 2003; 66: 871-872
• 113 Youssef DTA, van Soest RWM, Fusetani N. Callyspongamide A, a new cytotoxic polyacetylenic amide from the Red Sea sponge Callyspongia fistularis . J Nat Prod 2003; 66: 861-862
• 114 Youssef DT, van Soest RWM, Fusetani N. Callyspongenols A–C, new cytotoxic C22-polyacetylenic alcohols from a Red Sea sponge, Callyspongia species. J Nat Prod 2003; 66: 679-681
• 115 Umeyama A, Matsuoka N, Mine R, Nakata A, Arimoto E, Matsui M, Shoji N, Arihara S, Takei M, Hashimoto T. Polyacetylene diols with antiproliferative and driving Th1 polarization effects from the marine sponge Callyspongia sp. J Nat Med 2010; 64: 93-97
• 116 Rotem M, Kashman Y. New polyacetylenes from the sponge Siphonochalina sp. Tetrahedron Lett 1979; 20: 3193-3196
• 117 Tada H, Yasuda F. Siphonodiol, a new polyacetylenic metabolite from the sponge Siphonochalina truncate . Chem Lett 1984; 13: 779-780
• 118 Ayyad SE, Angawy R, Saqer EA, Badria FA. Cytotoxic polyacetylenes from the Red Sea sponge Siphonochalina siphonella . Z Naturforsch C 2014; 69: 117-123
• 119 Cimino G, de Stefano S. New acetylenic compounds from the sponge Reniera fulva . Tetrahedron Lett 1977; 18: 1325-1328
• 120 Ortega MJ, Zubía E, Carballo JL, Salvá J. Fulvinol, a new long-chain diacetylenic metabolite from the sponge Reniera fulva . J Nat Prod 1996; 59: 1069-1071
• 121 Nuzzo G, Ciavatta ML, Villani G, Manzo E, Zanfardino A, Varcamonti M, Gavagnin M. Fulvynes, antimicrobial polyoxygenated acetylenes from the Mediterranean sponge Haliclona fulva . Tetrahedron 2012; 68: 754-760
• 122 Williams DH, Faulkner DJ. Three new acetylenes from the Palauan sponge Haliclona sp. J Nat Prod 1996; 59: 1099-1101
• 123 Shin J, Seo Y, Cho KW, Rho JR, Paul VJ. Osirisynes A–F, highly oxygenated polyacetylenes from the sponge Haliclona osiris . Tetrahedron 1998; 54: 8711-8720
• 124 Chill L, Miroz A, Kashman Y. Haliclonyne, a new highly oxygenated polyacetylene from the marine sponge Haliclona species. J Nat Prod 2000; 63: 523-526
• 125 Aoki S, Matsui K, Tanaka K, Satari R, Kobayashi M. Lembehyne A, a novel neuritogenic polyacetylene, from a marine sponge of Haliclona sp. Tetrahedron 2000; 56: 9945-9948
• 126 Aoki S, Matsui K, Wei H, Murakami N, Kobayashi M. Structure-activity relationship of neuritogenic spongean acetylene alcohols, lembehynes. Tetrahedron 2002; 58: 5417-5422
• 127 Zhou GX, Molinski T. Long-chain acetylenic ketones from the Micronesian sponge Haliclona sp. Importance of the 1-yn-3-ol group for antitumor activity. Mar Drugs 2003; 1: 46-53
• 128 Aratake S, Trianto A, Hanif N, de Voogd N, Tanaka J. A new polyunsaturated brominated fatty acid from a Haliclona sponge. Mar Drugs 2009; 7: 523-527
• 129 Kobayashi M, Mahmud T, Tajima H, Wang W, Aoki S, Nakagawa S, Mayumi T, Kitagawa I. Marine natural products. XXXVI. Biologically active polyacetylenes, adociacetylenes A, B, C, and D, from an Okinawan marine sponge of Adocia sp. Chem Pharm Bull 1996; 44: 720-724
• 130 Wright AE, McConnell OJ, Kohmoto S, Lui MS, Thompson W, Snader KM. Duryne, a new cytotoxic agent from the marine sponge Cribrochalina dura . Tetrahedron Lett 1987; 28: 1377-1379
• 131 Gunasekera SP, Faircloth GT. New acetylenic alcohols from the sponge Cribrochalina vasculum . J Org Chem 1990; 55: 6223-6225
• 132 Aiello A, Fattorusso E, Menna M, Pansini M. Further bioactive acetylenic compounds from the caribbean sponge Cribrochalina vasculum . J Nat Prod 1992; 55: 1275-1280
• 133 Hallock YF, Cardellina JH, Balaschak MS, Alexander MR, Prather TR, Shoemaker RH, Boyd MR. Antitumor activity and stereochemistry of acetylenic alcohols from the sponge Cribrochalina vasculum . J Nat Prod 1995; 58: 1801-1807
• 134 Dai JR, Hallock YF, Cardellina JH, Boyd MR. Vasculyne, a new cytotoxic acetylenic alcohol from the marine sponge Cribrochalina vasculum . J Nat Prod 1996; 59: 88-89
• 135 Legrave N, Hamrouni-Buonomo S, Dufies M, Guérineau V, Vacelet J, Auberger P, Amade P, Mehiri M. Nepheliosyne B, a new polyacetylenic acid from the new caledonian marine sponge Niphates sp. Mar Drugs 2013; 11: 2282-2292
• 136 De Jesus RP, Faulkner DJ. Chlorinated acetylenes from the San Diego sponge Haliclona lunisimilis . J Nat Prod 2003; 66: 671-674
• 137 Castiello D, Cimino G, de Rosa S, de Stefano S, Sodano G. High molecular weight polyacetylenes from the nudibranch Peltodoris actromaculata and the sponge Petrosia ficiformis . Tetrahedron Lett 1980; 21: 5047-5050
• 138 Cimino G, Crispino A, de Rosa S, de Stefano S, Sodano G. Polyacetylenes from the sponge Petrosia ficiformis found in dark caves. Experientia 1981; 37: 924-926
• 139 Cimino G, de Giulio A, de Rosa S, de Stefano S, Sodano G. Further high molecular weight polyacetylenes from the sponge Petrosia ficiformis . J Nat Prod 1985; 48: 22-27
• 140 Cimino G, de Giulio A, de Rosa S, di Marzo V. High molecular weight polyacetylenes from Petrosia ficiformis: Further structural analysis and biological activity. Tetrahedron Lett 1989; 30: 3563-3566
• 141 Cimino G, de Giulio A, de Rosa S, di Marzo V. Minor bioactive polyacetylenes from Petrosia ficiformis . J Nat Prod 1990; 53: 345-353
• 142 Guo Y, Gavagnin M, Trivellone E, Cimino G. Absolute stereochemistry of petroformynes, high molecular polyacetylenes from the marine sponge Petrosia ficiformis . Tetrahedron 1994; 50: 13261-13268
• 143 Guo Y, Gavagnin M, Trivellone E, Cimino G. Further structural studies on the petroformynes. J Nat Prod 1995; 58: 712-722
• 144 Guo Y, Gavagnin M, Salierno C, Cimino G. Further petroformynes from both Atlantic and Mediterranean populations of the sponge Petrosia ficiformis . J Nat Prod 1998; 61: 333-337
• 145 Isaacs S, Kashman Y, Loya S, Hizi A, Loya Y. Petrosynol and petrosolic acid, two novel natural inhibitors of the reverse transcriptase of human immunodeficiency virus from Petrosia sp. Tetrahedron 1993; 49: 10435-10438
• 146 Guerriero A, Debitus C, Laurent D, dʼAmbrosio M, Pietra F. Aztèquynol A, the first clearly defined, C-branched polyacetylene and the analogue Aztèquynol B. Isolation from the tropical marine sponge Petrosia sp. Tetrahedron Lett 1998; 39: 6395-6398
• 147 Fusetani N, Shiragaki T, Matsunaga S, Hashimoto K. Bioactive marine metabolites XX. Petrosynol and petrosynone, antimicrobial C30 polyacetylenes from the marine sponge Petrosia sp.: Determination of the absolute configuration. Tetrahedron Lett 1987; 28: 4313-4314
• 148 Fusetani N, Li HY, Tamura K, Matsunaga S. Antifungal brominated C18 acetylenic acids from the marine sponge, Petrosia volcano Hoshino. Tetrahedron 1993; 49: 1203-1210
• 149 Li H-Y, Matsunaga S, Fusetani N. Corticatic acids A–C, antifungal acetylenic acids from the marine sponge, Petrosia corticata . J Nat Prod 1994; 57: 1464-1467
• 150 Nishimura S, Matsunaga S, Shibazaki M, Suzuki K, Harada N, Naoki H, Fusetani N. Corticatic acids D and E, polyacetylenic geranylgeranyltransferase type I inhibitors, from the marine sponge Petrosia corticata . J Nat Prod 2002; 65: 1353-1356
• 151 Shin J, Seo Y, Cho KW. Five new polyacetylenes from a ponge of the genus Petrosia . J Nat Prod 1998; 61: 1268-1273
• 152 Seo Y, Cho KW, Rho J-R, Shin J, Sim CJ. Petrocortynes and petrosiacetylenes, novel polyacetylenes from a sponge of the genus Petrosia . Tetrahedron 1998; 54: 447-462
• 153 Kim JS, Lim YJ, Im KS, Jung JH, Shim CJ, Lee CO, Hong J, Lee H. Cytotoxic polyacetylenes from the marine sponge Petrosia sp. J Nat Prod 1999; 62: 554-559
• 154 Lim YJ, Lee CO, Hong J, Kim DK, Im KS, Jung JH. Cytotoxic polyacetylenic alcohols from the marine sponge Petrosia species. J Nat Prod 2001; 64: 1565-1567
• 155 Lim YJ, Park HS, Im KS, Lee CO, Hong J, Lee MY, Kim DK, Jung JH. Additional cytotoxic polyacetylenes from the marine sponge Petrosia species. J Nat Prod 2001; 64: 46-53
• 156 Lee YJ, Yoo SJ, Kang JS, Yun J, Shin HJ, Lee JS, Lee HS. Cytotoxic petrosiacetylenes from the marine sponge Petrosia sp. Lipids 2013; 48: 87-91
• 157 Juan YS, Lee CC, Tsao CW, Lu MC, El-Shazly M, Shih HC, Chen YC, Wu YC, Su JH. Structure elucidation and cytotoxic evaluation of new polyacetylenes from a marine sponge Petrosia sp. Int J Mol Sci 2014; 15: 16511-16521
• 158 Watanabe K, Tsuda Y, Hamada M, Omori M, Mori G, Iguchi K, Naoki H, Fujita T, van Soest RW. Acetylenic strongylodiols from a Petrosia (Strongylophora) Okinawan marine sponge. J Nat Prod 2005; 68: 1001-1005
• 159 Watanabe K, Mori G, Iguchi K, Suzuki M, van Soest RW. Nine acetylenic alcohols isolated from the Okinawan marine sponge of the genus Petrosia (Strongylophora). Nat Prod Res 2007; 21: 710-720
• 160 Okamoto C, Nakao Y, Fujita T, Iwashita T, van Soest RWM, Fusetani N, Matsunaga S. Cytotoxic C47-polyacetylene carboxylic acids from a marine sponge Petrosia sp. J Nat Prod 2007; 70: 1816-1819
• 161 Ueoka R, Ise Y, Matsunaga S. Cytotoxic polyacetylenes related to petroformyne-1 from the marine sponge Petrosia sp. Tetrahedron 2009; 65: 5204-5208
• 162 Hitora Y, Takada K, Okada S, Matsunaga S. Miyakosynes A–F, cytotoxic methyl branched acetylenes from a marine sponge Petrosia sp. Tetrahedron 2011; 67: 4530-4534
• 163 Ohta S, Ogawa T, Ohta E, Ikeuchi T, Kamemura K, Ikegami S. Petroacetylene, a new polyacetylene from the marine sponge Petrosia solida that inhibits blastulation of starfish embryos. Nat Prod Res 2013; 27: 1842-1847
• 164 Horikawa K, Yagyu T, Yoshioka Y, Fujiwara T, Kanamoto A, Okamoto T, Ojika M. Petrosiols A–E, neurotrophic diyne tetraols isolated from the Okinawan sponge Petrosia strongylata . Tetrahedron 2013; 69: 101-106
• 165 Schmitz FJ, Gopichand Y. (7E,13ξ,15Z)-14,16-dibromo-7,13,15-hexadecatrien-5-ynoic acid. A novel dibromo acetylenic acid from the marine sponge Xestospongia muta . Tetrahedron Lett 1978; 19: 3637-3640
• 166 Quinn RJ, Tucker DJ. A brominated bisacetylenic acid from the marine sponge Xestospongia testudinaria . Tetrahedron Lett 1985; 26: 1671-1672
• 167 Quinn RJ, Tucker DJ. Further acetylenic acids from the marine sponge Xestospongia testudinaria . J Nat Prod 1991; 54: 290-294
• 168 Bourguet-Kondracki ML, Rakotoarisoa MT, Martin MT, Guyot M. Bioactive bromopolyacetylenes from the marine sponge Xestospongia testudinaria . Tetrahedron Lett 1992; 33: 225-226
• 169 Hirsh S, Carmely S, Kashman Y. Brominated unsaturated acids from the marine sponge Xestospongia sp. Tetrahedron 1987; 43: 3257-3261
• 170 Quiñoà E, Crews P. Melynes, polyacetylene constituents from a Vanuatu marine sponge. Tetrahedron Lett 1988; 29: 2037-2040
• 171 Kobayashi J, Naitoh K, Ishida K, Shigemori H, Ishibashi M. Nepheliosyne A, new C47 acetylenic acid from the okinawan marine sponge Xestospongia sp. J Nat Prod 1994; 57: 1300-1303
• 172 Brantley SE, Molinski TF, Preston CM, DeLong EF. Brominated acetylenic fatty acids from Xestospongia sp., a marine spongebacteria association. Tetrahedron 1995; 51: 7667-7672
• 173 Dai JR, Hallock YF, Cardellina JH, Gray GN, Boyd MR. Triangulynes A−H and triangulynic acid, new cytotoxic polyacetylenes from the marine sponge Pellina triangulata . J Nat Prod 1996; 59: 860-865
• 174 Fu X, Abbas SA, Schmitz FJ, Vidavsky I, Gross ML, Laney M, Schatzman RC, Cabuslay RD. New acetylenic metabolites from the marine sponge Pellina triangulata . Tetrahedron 1997; 53: 799-814
• 175 Matsunaga S, Okada Y, Fusetani N, van Soest RWM. An antimicrobial C14 acetylenic acid from a marine sponge Oceanapia species. J Nat Prod 2000; 63: 690-691
• 176 Erpenbeck D, van Soest RWM. Status and perspective of sponge chemosystematics. Mar Biotechnol 2007; 9: 2-19
• 177 Montalvo NF, Hill RT. Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl Environ Microbiol 2011; 77: 7207-7216
• 178 Trindade-Silva AE, Rua C, Silva GGZ, Dutilh BE, Moreira APB, Edwards RA, Hajdu E, Lobo-Hajdu G, Vasconcelos AT, Berlinck RGS, Thompson FL. Taxonomic and functional microbial signatures of the endemic marine sponge Arenosclera brasiliensis . PLoS One 2012; 7: e39905
• 179 Khan ST, Musarrat J, Alkhedhairy AA, Kazuo S. Diversity of bacteria and polyketide synthase associated with marine sponge Haliclona sp. Ann Microbiol 2014; 64: 199-207
• 180 Jasmin C, Anas A, Nair S. Bacterial diversity associated with Cinachyra cavernosa and Haliclona pigmentifera, cohabiting sponges in the Coral Reef Ecosystem of Gulf of Mannar, Southeast Coast of India. PLoS One 2015; 10: e0123222