International Journal of Molecular Sciences Article Successive Onset of Molecular, Cellular and Tissue-Specific Responses in Midgut Gland of Littorina littorea Exposed to Sub-Lethal Cadmium Concentrations Denis Benito 1,†, Michael Niederwanger 2,† ID , Urtzi Izagirre 1, Reinhard Dallinger 2,* and Manu Soto 1,* 1 CBET Research Group, Research Centre for Experimental Marine Biology and Biotechnology (PiE-UPV/EHU), University of the Basque Country UPV/EHU, Areatza Pasalekua, 48620 Plentzia-Bizkaia, Basque Country, Spain;
[email protected] (D.B.);
[email protected] (U.I.) 2 Institute of Zoology and Center of Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Technikerstraße 25, A-6020 Innsbruck, Austria;
[email protected] * Correspondence:
[email protected] (R.D.);
[email protected] (M.S.); Tel.: +43-512-507-51861 (R.D.); +34-946-015-512 (M.S.) † These authors contributed equally to this study. Received: 4 July 2017; Accepted: 18 August 2017; Published: 22 August 2017 Abstract: Cadmium (Cd) is one of the most harmful metals, being toxic to most animal species, including marine invertebrates. Among marine gastropods, the periwinkle (Littorina littorea) in particular can accumulate high amounts of Cd in its midgut gland. In this organ, the metal can elicit extensive cytological and tissue-specific alterations that may reach, depending on the intensity of Cd exposure, from reversible lesions to pathological cellular disruptions. At the same time, Littorina littorea expresses a Cd-specific metallothionein (MT) that, due to its molecular features, expectedly exerts a protective function against the adverse intracellular effects of this metal. The aim of the present study was, therefore, to assess the time course of MT induction in the periwinkle’s midgut gland on the one hand, and cellular and tissue-specific alterations in the digestive organ complex (midgut gland and digestive tract) on the other, upon exposure to sub-lethal Cd concentrations (0.25 and 1 mg Cd/L) over 21 days.