The Mechanism of Diarrhetic Shellfish Poisoning Toxin Production in Prorocentrum Spp.: Physiological and Molecular Perspectives

Overview

Journal Toxins (Basel)

Publisher MDPI

Specialty Toxicology

Date 2016 Sep 27

PMID 27669302

Citations 19

Authors

Thomas Chun-Hung Lee

Fiona Long-Yan Fong

Kin-Chung Ho

Fred Wang-Fat Lee

Affiliations

Soon will be listed here.

Abstract

Diarrhetic shellfish poisoning (DSP) is a gastrointestinal disorder caused by the consumption of seafood contaminated with okadaic acid (OA) and dinophysistoxins (DTXs). OA and DTXs are potent inhibitors of protein phosphatases 2A, 1B, and 2B, which may promote cancer in the human digestive system. Their expression in dinoflagellates is strongly affected by nutritional and environmental factors. Studies have indicated that the level of these biotoxins is inversely associated with the growth of dinoflagellates at low concentrations of nitrogen or phosphorus, or at extreme temperature. However, the presence of leucine or glycerophosphate enhances both growth and cellular toxin level. Moreover, the presence of ammonia and incubation in continuous darkness do not favor the toxin production. Currently, studies on the mechanism of this biotoxin production are scant. Full genome sequencing of dinoflagellates is challenging because of the massive genomic size; however, current advanced molecular and omics technologies may provide valuable insight into the biotoxin production mechanism and novel research perspectives on microalgae. This review presents a comprehensive analysis on the effects of various nutritional and physical factors on the OA and DTX production in the DSP toxin-producing Prorocentrum spp. Moreover, the applications of the current molecular technologies in the study on the mechanism of DSP toxin production are discussed.

Citing Articles

Marine Algal Toxins and Public Health: Insights from Shellfish and Fish, the Main Biological Vectors.

Yuan K, Li H, Yang W Mar Drugs. 2024; 22(11).

PMID: 39590790 PMC: 11595774. DOI: 10.3390/md22110510.

Molecular Phylogeny, Morphology, Growth and Toxicity of Three Benthic Dinoflagellates sp. 9, and Developing in Strait of Gibraltar, Southwestern Mediterranean.

Ibghi M, Rijal Leblad B, Lbachir El Kbiach M, Aboualaalaa H, Daoudi M, Masseret E Toxins (Basel). 2024; 16(1).

PMID: 38251265 PMC: 10819257. DOI: 10.3390/toxins16010049.

Transcriptomic Analysis of the Response of the Toxic Dinoflagellate to Phosphorous Limitation.

Wan X, Yao G, Wang K, Liu Y, Wang F, Jiang H Microorganisms. 2023; 11(9).

PMID: 37764060 PMC: 10535992. DOI: 10.3390/microorganisms11092216.

Acute Toxicity of the Dinoflagellate on Early Life Stages of Zebrafish ().

Yang X, Yan Z, Chen J, Wang D, Li K Toxics. 2023; 11(4).

PMID: 37112597 PMC: 10144361. DOI: 10.3390/toxics11040370.

Upregulation of Peridinin-Chlorophyll A-Binding Protein in a Toxic Strain of under Normal and Phosphate-Depleted Conditions.

Lee T, Lai K, Xu S, Lee F Int J Mol Sci. 2023; 24(2).

PMID: 36675250 PMC: 9864435. DOI: 10.3390/ijms24021735.

References

Berven G, Saetre F, Halvorsen K, Seglen P . Effects of the diarrhetic shellfish toxin, okadaic acid, on cytoskeletal elements, viability and functionality of rat liver and intestinal cells. Toxicon. 2000; 39(2-3):349-62. DOI: 10.1016/s0041-0101(00)00137-9. View

Snyder R, Gibbs P, Palacios A, Abiy L, Dickey R, Lopez J . Polyketide synthase genes from marine dinoflagellates. Mar Biotechnol (NY). 2003; 5(1):1-12. DOI: 10.1007/s10126-002-0077-y. View

Hwang D, Lu Y . Influence of environmental and nutritional factors on growth, toxicity, and toxin profile of dinoflagellate Alexandrium minutum. Toxicon. 2000; 38(11):1491-503. DOI: 10.1016/s0041-0101(00)00080-5. View

Lee T, Kwok O, Ho K, Lee F . Effects of different nitrate and phosphate concentrations on the growth and toxin production of an Alexandrium tamarense strain collected from Drake Passage. Mar Environ Res. 2012; 81:62-9. DOI: 10.1016/j.marenvres.2012.08.009. View

Okamoto O, Robertson D, Fagan T, Hastings J, Colepicolo P . Different regulatory mechanisms modulate the expression of a dinoflagellate iron-superoxide dismutase. J Biol Chem. 2001; 276(23):19989-93. DOI: 10.1074/jbc.M101169200. View

Lidie K, Ryan J, Barbier M, Van Dolah F . Gene expression in Florida red tide dinoflagellate Karenia brevis: analysis of an expressed sequence tag library and development of DNA microarray. Mar Biotechnol (NY). 2005; 7(5):481-93. DOI: 10.1007/s10126-004-4110-6. View

Boe R, Gjertsen B, Vintermyr O, Houge G, Lanotte M, Doskeland S . The protein phosphatase inhibitor okadaic acid induces morphological changes typical of apoptosis in mammalian cells. Exp Cell Res. 1991; 195(1):237-46. DOI: 10.1016/0014-4827(91)90523-w. View

Daranas A, Fernandez J, Norte M, Gavin J, Suarez-Gomez B, Souto M . Biosynthetic studies of the DSP toxin skeleton. Chem Rec. 2004; 4(1):1-9. DOI: 10.1002/tcr.10072. View

Souto M, Fernandez J, Norte M, Fernandez M, Martinez A . Influence of amino acids on okadaic acid production. Toxicon. 2000; 39(5):659-64. DOI: 10.1016/s0041-0101(00)00190-2. View

10.

Fujiki H, Suganuma M, Suguri H, Yoshizawa S, Takagi K, Uda N . Diarrhetic shellfish toxin, dinophysistoxin-1, is a potent tumor promoter on mouse skin. Jpn J Cancer Res. 1988; 79(10):1089-93. PMC: 5917631. DOI: 10.1111/j.1349-7006.1988.tb01531.x. View

11.

LAFAY B, Ruimy R, de Traubenberg C, Breittmayer V, Gauthier M, Christen R . Roseobacter algicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflagellate Prorocentrum lima. Int J Syst Bacteriol. 1995; 45(2):290-6. DOI: 10.1099/00207713-45-2-290. View

12.

Nuydens R, de Jong M, Van Den Kieboom G, Heers C, Dispersyn G, Cornelissen F . Okadaic acid-induced apoptosis in neuronal cells: evidence for an abortive mitotic attempt. J Neurochem. 1998; 70(3):1124-33. DOI: 10.1046/j.1471-4159.1998.70031124.x. View

13.

Hackett J, Scheetz T, Yoon H, Soares M, Bonaldo M, Casavant T . Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics. 2005; 6:80. PMC: 1173104. DOI: 10.1186/1471-2164-6-80. View

14.

Toulza E, Shin M, Blanc G, Audic S, Laabir M, Collos Y . Gene expression in proliferating cells of the dinoflagellate Alexandrium catenella (Dinophyceae). Appl Environ Microbiol. 2010; 76(13):4521-9. PMC: 2897438. DOI: 10.1128/AEM.02345-09. View

15.

Tillett D, Dittmann E, Erhard M, Von Dohren H, Borner T, Neilan B . Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem Biol. 2000; 7(10):753-64. DOI: 10.1016/s1074-5521(00)00021-1. View

16.

Garcia C, Truan D, Lagos M, Pablo Santelices J, Diaz J, Lagos N . Metabolic transformation of dinophysistoxin-3 into dinophysistoxin-1 causes human intoxication by consumption of O-acyl-derivatives dinophysistoxins contaminated shellfish. J Toxicol Sci. 2006; 30(4):287-96. DOI: 10.2131/jts.30.287. View

17.

Dominguez H, Paz B, Daranas A, Norte M, Franco J, Fernandez J . Dinoflagellate polyether within the yessotoxin, pectenotoxin and okadaic acid toxin groups: characterization, analysis and human health implications. Toxicon. 2009; 56(2):191-217. DOI: 10.1016/j.toxicon.2009.11.005. View

18.

Christiansen G, Fastner J, Erhard M, Borner T, Dittmann E . Microcystin biosynthesis in planktothrix: genes, evolution, and manipulation. J Bacteriol. 2003; 185(2):564-72. PMC: 145317. DOI: 10.1128/JB.185.2.564-572.2003. View

19.

Jaeckisch N, Yang I, Wohlrab S, Glockner G, Kroymann J, Vogel H . Comparative genomic and transcriptomic characterization of the toxigenic marine dinoflagellate Alexandrium ostenfeldii. PLoS One. 2011; 6(12):e28012. PMC: 3229502. DOI: 10.1371/journal.pone.0028012. View

20.

Cohen P, Holmes C, Tsukitani Y . Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem Sci. 1990; 15(3):98-102. DOI: 10.1016/0968-0004(90)90192-e. View