'Venus trapped, Mars transits': Cu and Fe redox chemistry, cellular topography and in situ ligand binding in terrestrial isopod hepatopancreas.

P Kille,D Hart,D Scarborough,K Powell,P Gunning,J F W Mosselmans,J M Charnock,I Mcdonald,A Hayes,A J Morgan

doi:10.1098/rsob.150270

Abstract

Woodlice efficiently sequester copper (Cu) in ‘cuprosomes' within hepatopancreatic ‘S' cells. Binuclear ‘B’ cells in the hepatopancreas form iron (Fe) deposits; these cells apparently undergo an apocrine secretory diurnal cycle linked to nocturnal feeding. Synchrotron-based µ-focus X-ray spectroscopy undertaken on thin sections was used to characterize the ligands binding Cu and Fe in S and B cells of Oniscus asellus (Isopoda). Main findings were: (i) morphometry confirmed a diurnal B-cell apocrine cycle; (ii) X-ray fluorescence (XRF) mapping indicated that Cu was co-distributed with sulfur (mainly in S cells), and Fe was co-distributed with phosphate (mainly in B cells); (iii) XRF mapping revealed an intimate morphological relationship between the basal regions of adjacent S and B cells; (iv) molecular modelling and Fourier transform analyses indicated that Cu in the reduced Cu+ state is mainly coordinated to thiol-rich ligands (Cu–S bond length 2.3 Å) in both cell types, while Fe in the oxidized Fe3+ state is predominantly oxygen coordinated (estimated Fe–O bond length of approx. 2 Å), with an outer shell of Fe scatterers at approximately 3.05 Å; and (v) no significant differences occur in Cu or Fe speciation at key nodes in the apocrine cycle. Findings imply that S and B cells form integrated unit-pairs; a functional role for secretions from these cellular units in the digestion of recalcitrant dietary components is hypothesized.

Highlights

30% of all proteins are considered to require a metal cofactor, usually a transition metal such as Cu, Fe, Mn or Zn [1]
2 A ), with an outer shell of Fe scatterers at approximately 3.05 A ; and (v) no significant differences occur in Cu or Fe speciation at key nodes in the apocrine cycle
Findings imply that S and B cells form integrated unit-pairs; a functional role for secretions from these cellular units in the digestion of recalcitrant dietary components is hypothesized

Summary

Introduction

30% of all proteins are considered to require a metal cofactor, usually a transition metal such as Cu, Fe, Mn or Zn [1]. Metal ions and proteins are functionally interdependent in other ways, including metal-mediated control of gene expression [2], direct [3] and indirect [4] metal ion involvement in intracellular signalling, and the roles of certain proteins as metallochaperones [5] and metallotransporters [6]. The requisite selectivity of these molecular events crucially depends on discriminatory metal sensors [7]. It is almost inevitable that imbalances in the homeostasis of these essential transition metals can lead to cytotoxicity and disease processes in both invertebrates and vertebrates because surpluses of redox-active species often induce reactive oxyradical generation [8].

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