Structure and Activity of Largazole, a Potent Antiproliferative Agent from the Floridian Marine Cyanobacterium Symploca sp.

Journal of the American Chemical Society
2008.0

Abstract

The identification of new pharmacophores is of paramount biomedical importance, and natural products have recently regained attention for this endeavor, closely tied to the exploitation of the marine environment which harbors unmatched biodiversity. Marine cyanobacteria are prolific producers of bioactive secondary metabolites, many of which are modified peptides or peptide-polyketide hybrids with promising antitumor activities (e.g., dolastatin 10, curacin A, apratoxin A). As a result of ongoing investigations to identify new drug leads from cyanobacteria in Florida, we report here the structure determination and preliminary biological characterization of largazole, a marine cyanobacterial metabolite from a Symploca sp. with a novel chemical scaffold and nanomolar antiproliferative activity. Symploca species were targeted because a Palauan Symploca sp. previously yielded the clinical trial compound dolastatin 10, despite being less investigated than Lyngbya spp. A sample of Symploca sp. collected from Key Largo, Florida Keys, was extracted with organic solvents, and the cytotoxic crude extract was subjected to bioassay-guided fractionation (solvent partition, silica gel chromatography, reversed-phase HPLC) to yield largazole (1) as a colorless, amorphous solid. The structure of largazole was elucidated using 1H and 13C NMR, HRESI/APCIMS (molecular formula C29H42N4O5S3), and two-dimensional NMR (COSY, HSQC, HMBC), revealing structural features including a 2-substituted thiazoline-4-methyl-4-carboxylic acid unit, a 2,4-disubstituted thiazole unit, a 7-substituted 3-hydroxyhept-4-enoic acid moiety (E-geometry double bond), and an n-octanoyl group connected via a thioester. The absolute configuration of largazole was established as 2S,7R,17S by generating optically active fragments (2-methylcysteic acid, valine, malic acid) through ozonolysis, oxidative workup, and acid hydrolysis, followed by chiral HPLC analysis against authentic standards. Largazole potently inhibited the growth of highly invasive transformed human mammary epithelial cells (MDA-MB-231, GI50 7.7 nM) and induced cytotoxicity at higher concentrations (LC50 117 nM). It showed remarkable selectivity for transformed cells (e.g., osteosarcoma U2OS, GI50 55 nM) over nontransformed cells (e.g., murine mammary NMuMG, GI50 122 nM; fibroblasts NIH3T3, GI50 480 nM), a selectivity unmatched by other tested natural product drugs (paclitaxel, actinomycin D, doxorubicin). Largazole also strongly inhibited the growth of colon (HT29, GI50/LC50 12 nM/22 nM) and neuroblastoma (IMR-32, GI50/LC50 16 nM/22 nM) cell lines. Largazole possesses unusual structural features: a substituted 4-methylthiazoline linearly fused to a thiazole (similar to didehydromirabazole), a thioester moiety (not previously reported in cyanobacteria), and an unprecedented 3-hydroxy-7-mercaptohept-4-enoic acid unit. Most significantly, its potent biological activity and selectivity for cancer cells warrant further investigation into its mode of action, cancer chemotherapeutic potential, and biosynthesis.

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