Towards commercial production of sponge medicines

Marine Drugs

Volumn 7, Issue 4, 2009, Pages 787-802

  Koopmans, Marieke ^a   Martens, Dirk ^a   Wijffels, Rene H ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Bioactive metabolite; Biosynthetic pathway; Cell culture; Sponge culture; Sponge medicine

Indexed keywords

AEROPLYSININ 1; APLYSINIMINE; DIENONE; DITERPENE; FATTY ACID; HALICHONDRIN B; ISOXAZOLINE ALKALOID; NATURAL PRODUCT; SPONGE EXTRACT; STEVENSINE; UNCLASSIFIED DRUG;

APLYSINA AEROPHOBA; APOPTOSIS; ARTICLE; BIOMASS PRODUCTION; BIOSYNTHESIS; CELL CULTURE; DNA MODIFICATION; DNA REPLICATION; DRUG MANUFACTURE; DRUG SYNTHESIS; DYSIDEA AVARA; FATTY ACID METABOLISM; HALICLONA OCULATA; IN VITRO STUDY; METABOLITE; METABOLOME; METAGENOMICS; NONHUMAN; RHOPALOEIDES ODORABILE; SPONGE (PORIFERA); SYMBIONT;

EID: 75149173058     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md7040787     Document Type: Article

References (84)

1. Faulkner, D.J. Marine natural products. Nat. Prod. Rep. 2002, 19, 1-48.
2. Sipkema, D.; Franssen, M.C.R.; Osinga, R.; Tramper, J.; Wijffels, R.H. Marine sponges as pharmacy. Mar. Biotechnol. 2005, 7, 142-162.
3. Dumdei, E.J.; Blunt, J.W.; Munro, M.H.G.; Battershill, C.N.; Page, M.J. The Whys and Whats of Sponge Chemistry: Why Chemists Extract Sponges and What Problems Does This Cause? Watanabe, Y., Fusetani, N., Eds.; Springer-Verlag: Tokyo, Japan, 1998; pp. 353-364.
4. Sipkema, D.; Osinga, R.; Schatton, W.; Mendola, D.; Tramper, J.; Wijffels, R.H. Large-scale production of pharmaceuticals by marine sponges: Sea, cell, or synthesis? Biotechnol. Bioeng. 2005, 90, 201-222.
5. Hoover, C.A.; Slattery, M.; Marsh, A.G. A functional approach to transcriptome profiling: Linking gene expression patterns to metabolites that matter. Mar. Biotechnol. 2007, 9, 411-419.
6. Munro, M.H.G.; Blunt, J.W.; Lake, R.J.; Litaudon, M.; Battershill, C.N.; Page, M.J. From Seabed to Sickbed: What are the prospects? In Sponges in Time and Space: Biology, Chemistry, Paleontology; Soest, R.V.M.; van Kempen, T.M.G., Braekman, J.C., Eds.; Balkema: Rotterdam, The Netherland, 1994; pp. 473-484.
7. Wulff, J.L. Ecological interactions of marine sponges. Can. J. Zool. 2006, 84, 146-166.
8. Proksch, P. Defensive roles for secondary metabolites from marine sponges and sponge-feeding nudibranchs. Toxicon 1994, 32, 639-655.
9. Ruzicka, R.; Gleason, D.F. Latitudinal variation in spongivorous fishes and the effectiveness of sponge chemical defenses. Oecologia 2008, 154, 785-794.
10. Abdo, D.A.; Motti, C.A.; Battershill, C.N.; Harvey, E.S. Temperature and spatiotemporal variability of salicylihalamide A in the sponge Haliclona sp. J. Chem. Ecol. 2007, 33, 1635-1645.
11. Page, M.J.; Northcote, P.T.; Webb, V.L.; Mackey, S.; Handley, S.J. Aquaculture trials for the production of biologically active metabolites in the New Zealand sponge Mycale hentscheli (Demospongiae: Poecilosclerida). Aquaculture 2005, 250, 256-269.
12. Becerro, M.A.; Turon, X.; Uriz, M.J. Natural variation of toxicity in encrusting sponge Crambe crambe (Schidt) in relation to size and environment. J. Chem. Ecol. 1995, 21, 1931-1946.
13. Lopez-Legentil, S.; Bontemps-Subielos, N.; Turon, X.; Banaigs, B. Secondary metabolite and inorganic contents in Cystodytes sp. (Ascidiacea): Temporal patterns and association with reproduction and growth. Mar. Biol. 2007, 151, 293-299.
14. Turon, X.; Becerro, M.A.; Uriz, M.J.; Llopis, J. Small-scale association measures in epibenthic communities as a clue for allelochemical interactions. Oecologia 1996, 108, 351-360.
15. Thacker, R.W.; Becerro, M.A.; Lumbang, W.A.; Paul, V.J. Allelopathic interaction between sponges on a tropical reef. Ecology 1998, 79, 1740-1750.
16. Becerro, M.A.; Thacker, R.W.; Turon, X.; Uriz, M.J.; Paul, V.J. Biogeography of sponge chemical ecology: Comparisons of tropical an temperate defenses. Oecologia 2003, 135, 91-101.
17. Pawlik, J.R.; Chanas, B.; Toonen, R.J.; Fenical, W. Defenses of Caribean sponges against predatory reef fish. I. Chemical deterrence. Mar. Ecol. Prog. Ser. 1995, 127, 183-194.
18. Schupp, P.; Eder, C.; Pail, C.; Proksch, P. Distribition of secondary metabolites in the sponge Oceanapia sp. and its ecological implications. Mar. Biol. 1999, 135, 573-580.
19. Thoms, C.; Wolff, M.; Padmakumar, K.; Ebel, R.; Proksch, P. Chemical defense of Mediterranean sponges Aplysina cavernicola and Aplysina aerophoba. Z. Naturforsch 2004, 59c, 113-122.
20. Baldwin, I.T. The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 1988, 77, 378-381.
21. Thornton, R.G.; Kerr, R.G. Induction of pseuopterosin biosynthesis in the gorgonian Pseudopterogorgia elisabethae. J. Chem. Ecol. 2002, 28, 2083-2090.
22. Thompson, J.E.; Murphy, P.T.; Bergquist, P.R.; Evans, E.A. Environmetally induced variation in diterpene composition of the marine sponge Rhopaloeides odorabile. Biochem. Syst. Ecol. 1987, 15, 595-606.
23. Webster, N.S.; Xavier, J.R.; Freckelton, M.; Motti, C.A.; Cobb, R. Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ. Microbiol. 2008, 10, 3366-3376.
24. Duckworth, A.R.; Samples, G.A.; Wright, A.E.; Pomponi, S.A. In vitro culture of the tropical sponge Axinella corrugata (Demospongia): Effect of food cell concentration on growth, clearance rate and biosynthesis of stevensine. Mar. Biotechnol. 2003, 5, 519-527.
25. Thoms, C.; Ebel, R.; Proksch, P. Activated chemical defense in Aplysina sponges revisited. J. Chem. Ecol. 2006, 32, 97-123.
26. Ebel, R.; Brenzinger, M.; Kunze, A.; Gross, H.J.; Proksch, P. Wound activation of protoxins in marine sponge Aplysina aerophoba. J. Chem. Ecol. 1997, 23, 1451-1462.
27. Thoms, C.; Schupp, P.J. Activated chemical defense in marine sponges-a case study on Aplysinella rhax. J. Chem. Ecol. 2008, 34, 1242-1252.
28. Walters, K.D.; Pawlik, J.R. Is there a trade-off between wound-healing and chemical defenses among caribbean reef sponges? Integr. Comp. Biol. 2005, 45, 352-358.
29. Fortman, J.L.; Sherman, D.H. Utilizing the power of microbial genetics to bridge the gap between the promise and the application of matine natural products. ChemBioChem 2005, 6, 960-978.
30. Grozdanov, L.; Hentschel, U. An environmental genomics perspective on the diversity and function of marine sponge-associated microbiota. Curr. Opin. Microbiol. 2007, 10, 215-220.
31. Kennedy, J.; Marchesi, J.R.; Dobson, A.D.W. Marine metagenomics: Strategies for the discovery of novel enzymes with biotechnological applications from marine environments. Microb. Cell Factories 2008, 7, 27.
32. Hutchinson, C.R. Polyketide and non-ribosomal peptide synthases: Falling together by coming apart. Proc. Natl. Acad. Sci. USA 2003, 100, 3010-3012.
33. Piel, J.; Hui, D.; Wen, G.; Butzke, D.; Platzer, M.; Fusetani, N.; Matsunaga, S. Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc. Natl. Acad. Sci. USA 2004, 101, 16222-16227.
34. Blunt, J.W.; Copp, B.R.; Hu, W.P.; Munro, M.H.G.; Northcote, P.T.; Prinsep, M.R. Marine natural products. Nat. Prod. Rep. 2008, 26, 170-244.
35. Moco, S. Metabolomics technologies applied to the identification of compounds in plants. Wageningen University: Wageningen, The Netherland, 2007.
36. Hahn, S.; Stoilov, T.B.; Ha, T.B.T.; Readerstorff, D.; Doss, G.A.; Li, H.; Djerassi, C. Biosyntethic studies of marine lipids. 17. The course of chain elongation and desaturation in long-chain fatty acids. J. Am. Chem. Soc. 1988, 110, 8117-8124.
37. Raederstorff, D.; Shu, A.Y.L.; Thompson, J.E.; Djerassi, C. Biosyntethic studies of marine lipids. 11 1 Synthesis, biosynthesis, and absolute configuration of the internally branched demospongic acid 22-Methyl-5,9- octacosadienoic acid. J. Org. Chem. 1987, 52, 2337-2346.
38. Byrne, K.M.; Smith, S.K.; Ondeyka, J.G. Biosynthesis of nodulisporic acid a: Precursor studies. J. Am. Chem. Soc. 2002, 124, 7055-7060.
39. Sara, M.; Bavestrello, G.; Cattanea-vietti, R.; Cerrano, C. Endosymbiosis in sponges: Relevance for epigenesist and evolution. Symbiosis 1998, 25, 57-70.
40. Taylor, M.W.; Radax, R.; Steger, D.; Wagner, M. Sponge-associated microorganisms: Evolution, Ecology and Biotechnological potential. Microbiol. Mol. Biol. Rev. 2007, 71, 295-347.
41. Wijffels, R.H. Potential of sponges and microalgae for marine biotechnology. Trends Biotechnol. 2008, 26, 26-31.
42. Becerro, M.A.; Paul, V.J.; Starmer, J. Intracolonial variation in chemical defenses of the sponge Cacospongia sp. and its consequences on generalist fish predators and the specialist nudibranch predator Glossodoris pallida. Mar. Ecol. Prog. Ser. 1998, 168, 187-196.
43. Kubanek, J.; Whalen, K.E.; Engel, S.; Kelly, S.R.; Henkel, T.P.; Fenical, W.; Pawlik, J.R. Multiple defensive roles for triterpene glycosides from two Caribbean sponges. Oecologia 2002, 131, 125-136.
44. Unson, M.D.; Faulkner, D.J. Cyanobacterial symbiont biosynthesis of chlorinated metabolites from Dysidea herbacea (Porifera). Experientia 1993, 49, 349-353.
45. Garson, M.J.; Flowers, A.E.; Webb, R.I.; Charan, R.D.; McCaffrey, E.J. A sponge/dinoflagellate association in the haplosclerid sponge Haliclona sp.: Cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation. Cell Tissue Res. 1998, 293, 365-373.
46. Uriz, M.J.; Turon, X.; Galera, J.; Tur, J.M. New light on the cell location of avarol within the sponge Dysidea avara (Dendroceratida). Cell Tissue Res. 1996, 285, 519-527.
47. Pomponi, S.A.; Willoughby, R. Sponge Cell Culture for the Production of Bioactive Metabolites; van Soest, R., van Kempen, T.M.G., Braekman, J.C., Eds.; Balkema: Rotterdam, The Netherlands, 1994; pp. 395-400.
48. Lee, K.L.; Lee, J.H.; Lee, H.K. Microbial symbiosis in marine sponges. J. Microbiol. 2001, 39, 254-264.
49. Proksch, P.; Edrada, R.A.; Ebel, R. Drugs from the seas-current status and microbiological implications. Appl. Microbiol. Biotechnol. 2002, 59, 125-134.
50. Hill, R.T. Manzamine-producing actinomycetes. United States Patent Application 20050244938.
51. Sakai, R.; Yoshida, K.; Kimura, A.; Koike, K.; Jimbo, M.; Kobiyama, A.; Kamiya, H. Cellular origin of dysiherbaine, an excitory amino acid derived from a marine sponge. ChemBioChem 2008, 9, 543-551.
52. Holler, U.; Wright, A.D.; Matthee, G.F.; Konig, G.M.; Draeger, S.; Aust, H.J.; Schulz, B. Fungi from marine sponges: Diversity, biological activity and secondary metabolites. Mycol. Res. 2000, 104, 1354-1365.
53. Newman, D.J.; Hill, R.T. New drugs from marine microbes: The tide is turning. J.Ind.Microbiol.Biotechnol. 2006, 33, 539-544.
54. Muller, W.E.G.; Zahn, R.K.; Gasic, M.J.; Dogovi, N.; Maidhof, P.A.; Becker, C.; Diehl-Seifert, B.; Eich, E. Avarol, a cytostatically active compound from the marin sponge Dysidea avara. Comput. Biochem. Physiol. 1985, 80C, 47-52.
55. Dayton, P.K. Observations of growth, dispersal and population dynamics of some sponges in McMurdo Sound, Antarctica. Colloques Internationaux du C.N.R.S. 1979, 291, 271-282.
56. de Caralt, S.; Uriz, M.J.; Wijffels, R.H. Grazing, differential size-class dynamics and survival of the Mediterranean sponge Corticium candelabrum. Mar. Ecol. Prog. Ser. 2008, 360, 97-106
57. de Voogd, N. The mariculture potential of the indonesian reef-dweeling sponge Callyspongia (Euplacella) biru: Growth, survival and bioactive compounds. Aquaculture 2007, 262, 54-64.
58. Duckworth, A.R.; Pomponi, S.A. Relative importance of bacteria, microalgae and yeast for growth of the sponge Halichondria melanadocia (De Laubenfels, 1936): A laboratory study. J. Exp. Mar. Biol. Ecol. 2005, 323, 151-195.
59. Garrabou, J.; Zabala, M. Growth dynamics in four Mediterranean Demosponges. Estuarine Coastal Shelf Sci. 2001, 52, 293-303.
60. Koopmans, M.; Wijffels, R.H. Seasonal growth rate of the sponge Haliclona oculata (demospongiae: Haplosclerida). Mar. Biotechnol. 2008, 10, 502-510.
61. Barthel, D.; Theede, H. A new method for the culture of marine sponges and its application for experimental studies. Ophelia 1986, 25, 2, 75-82.
62. Belarbi, E.H.; Ramirez Dominguez, M.; Ceron Garcia, M.C.; Contreras Gomez, A.; Garcia Camacho, F.; Molina Grima, E. Cultivation of explants of the marine sponge Crambe crambe in closed systems. Biomol. Eng. 2003, 20, 333-337.
63. De Caralt, S.; Agell, G.; Uriz, M.J. Long-term culture of sponge explants: Conditions enhancing survival and growth, and assessment of bioactivity. Biomol. Eng. 2003, 20, 339-347.
64. Duckworth, A.R.; Battershill, C.N. Sponge aquaculture for the production of biolocigally active metabolites: The influence of farming protocols and environment. Aquaculture 2003, 221, 311-329.
65. Mendola, D. Aquaculture of three phyla of marine invertebrates to yield bioactive metabolites: Process developments and economics. Biomol. Eng. 2003, 20, 441-458.
66. Osinga, R.; Belarbi, E.H.; Molina Grima, E.; Tramper, J.; Wijffels, R.H. Progress towards a controlled culture of the marine sponge Pseadosuberites andrewsi in a bioreactor. J. Biotechnol. 2003, 100, 141-146.
67. Sipkema, D.; Yosef, N.A.M.; Adamczewski, M.; Osinga, R.; Mendola, D.; Tramper, J.; Wijffels, R.H. Hypothesized kinetic models for describing the growthof globular and encrusting demosponges. Mar. Biotechnol. 2005, 8, 40-51.
68. Hadas, E.; Shpigel, M.; Ilan, M. Sea ranching of the marine sponge Negombata magnifica (Demospongiae, Latrunculiidae) as a first step for latrunculin B mass production. Aquaculture 2005, 244, 159-169.
69. Osinga, R.; De Beukelaer, P.B.; Meijer, E.M.; Tramper, J.; Wijffels, R.H. Growth of the sponge Pseudosuberites (aff.) andrewsi in a closed system. J. Biotechnol. 1999, 70, 155-161.
70. Pomponi, S.A.; Willoughby, R.; Kaighn, M.E.; Wright, A.E. Development of techniques for in vitro production of bioactive natural products from marine sponges. In Invertebrate Cell Culture: Novel Directions and Biotechnology Applications; Maramorosch, K., Mitsuhashi, J., Eds.; Science Publishers: Enfield, NH, USA, 1997; pp. 231-237.
71. Thompson, J.E.; Barrow, K.D.; Faulkner, D.J. Localization of two brominated metabolites, aerothionen and homoaerothionin, in spherulous cells of the marine sponge Aplysina fistularis. Acta Zool. Stockholm 1983, 64, 199-210.
72. Muller, W.E.G.; Wimmer, W.; Schatton, W.; Bohm, M.; Batel, R.; Filic, Z. Initiation of an aquaculture of sponges for the sustainable production of bioactive metabolites in open systems: Example, Geodia cydonium. Mar. Biotechnol. 1999, 1, 569-579.
73. De Caralt, S.; Uriz, M.J.; Wijffels, R.H. Cell culture from sponges: Pluripotency and immortality. Trends Biotechnol. 2008, 25, 467-471.
74. Mendola, D. The importance of water flow for culture of Dysidea avara sponges Wageningen University, Wageningen, The Netherland, 2008.
75. Sipkema, D.; Van Wielink, R.; Van Lammeren, A.A.M.; Tramper, J.; Osinga, R.; Wijffels, R.H. Primmorphs from seven marine sponges: Formation and structure. J. Biotechnol. 2003, 100, 127-139.
76. Li, Z.; He, L.; Miao, X. Cultivable bacterial community from south China sea sponge as revealed by DGGE fingerprinting and 16S rDNA phylogenetic analysis. Curr. Microbiol. 2007, 55, 465-472.
77. Muscholl-Silberhorn, A.; Thiel, V.; Imhoff, J.F. Abundance and bioactivity of cultured sponge-associated bacteria from the Mediterranean Sea. Microb. Ecol. 2007, 55, 94-106.
78. Kaeberlein, T.; Lewis, K.; Epstein, S.S. Isolating " uncultivable" microorganisms in pure culture in a simulated natural environment. Science 2006, 296, 1127-1129.
79. Kennedy, J.; Baker, P.; Piper, C.; Cotter, P.D.; Walsh, M.; Mooij, M.J.; Bourke, M.B.; Rea, M.C.; O'Connor, P.M.; Ross, R.P.; Gill, C.; O'Gara, F.; Machesi, J.R.; Dobson, A.D.W. Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar. Biotechnol. 2009, 11, 384-396.
80. Piel, J. Bacterial symbionts: Prospects for the sustainable production of invertebrate-derived pharmaceuticals. Curr. Med. Chem. 2006, 13, 39-50.
81. Anthony, J.R.; Anthony, L.C.; Nowroozi, F.; Kwon, G.; Newman, J.D.; Keasling, J.D. Optimization of the mevalonate-based isoprenoid biosynthetic pathway in Escherichia coli for production of the anti-malarial drug presursor amorpha-4,11-diene. Metab. Eng. 2009, 11, 13-19.
82. Engels, B.; Dahm, P.; Jennewein, S. Metabolic engineering of taxadiene biosynthesis in yeast as a first step towards Taxol (Paclitaxel) production. Metab. Eng. 2008, 10, 201-206.
83. Ro, D.K.; Ouellet, M.; Paradise, E.M.; Burd, H.; Eng, D.; Paddon, C.J.; Newman, J.D.; Keasling, J.D. Induction of multiple pleiotropic drug resistance genes in yeast engineered to produce an increased level of anti-malarial drug precursor, artemisinic acid. BMC Biotechnol. 2008, 8, 83.
84. Chemler, J.A.; Koffas, M.A.G. Metabolic engineering for plant natural product biosynthesis in microbes. Curr. Opin. Biotechnol. 2008, 19, 597-605.