Structural diversity of anti-pancreatic cancer capsimycins identified in mangrove-derived Streptomyces xiamenensis 318 and post-modification via a novel cytochrome P450 monooxygenase

Scientific Reports
2017.0

Abstract

<jats:title>Abstract</jats:title><jats:p>Polycyclic tetramate macrolactams (PTMs) were identified as distinct secondary metabolites of the mangrove-derived <jats:italic>Streptomyces xiamenensis</jats:italic> 318. Together with three known compounds—ikarugamycin (<jats:bold>1</jats:bold>), capsimycin (<jats:bold>2</jats:bold>) and capsimycin B (<jats:bold>3</jats:bold>)—two new compounds, capsimycin C (<jats:bold>4</jats:bold>) with <jats:italic>trans</jats:italic>-diols and capsimycin D (<jats:bold>5</jats:bold>) with <jats:italic>trans</jats:italic>-configurations at C-13/C-14, have been identified. The absolute configurations of the <jats:italic>tert/tert</jats:italic>-diols moiety was determined in <jats:bold>4</jats:bold> by NMR spectroscopic analysis, CD spectral comparisons and semi-synthetic method. The post-modification mechanism of the carbocyclic ring at C-14/C-13 of compound <jats:bold>1</jats:bold> in the biosynthesis of an important intermediate <jats:bold>3</jats:bold> was investigated. A putative cytochrome P450 superfamily gene, SXIM_40690 (<jats:italic>ikaD</jats:italic>), which was proximally localized to the ikarugamycin biosynthetic pathway, was characterized. <jats:italic>In vivo</jats:italic> gene inactivation and complementation experiment confirmed that IkaD catalysed the epoxide-ring formation reaction and further hydroxylation of ethyl side chain to form capsimycin G (<jats:bold>3′</jats:bold>). Binding affinities and kinetic parameters for the interactions between ikarugamycin (<jats:bold>1</jats:bold>) and capsimycin B (<jats:bold>3</jats:bold>) with IkaD were measured with Surface Plasmon Resonance. The intermediate compound <jats:bold>3′</jats:bold> was isolated and identified as 30-hydroxyl-capsimycin B. The caspimycins <jats:bold>2</jats:bold> and <jats:bold>3</jats:bold>, were transferred to methoxyl derivatives, <jats:bold>6</jats:bold> and <jats:bold>7</jats:bold>, under acidic and heating conditions. Compounds <jats:bold>1–3</jats:bold> exhibited anti-proliferative activities against pancreatic carcinoma with IC<jats:sub>50</jats:sub> values of 1.30–3.37 μM.

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