Chicken cognin interactome and the memory of filial imprinting

Abstract

Visual imprinting is a learning process whereby young animals come to prefer a visual stimulus after exposure to it (training). The intermediate medial mesopallium in the domestic chick forebrain is critical for visual imprinting and contributes to molecular regulation of memory formation. Criteria used to infer that a change following training is learning-related have been formulated and published. Cognin (protein disulphide isomerase) is one of several identified plasma membrane and mitochondrial proteins that are upregulated in a learning-related way 24 hours after training. Since virtually nothing is known about the cognin interactome, we have used immunoaffinity chromatography and mass spectrometry to identify proteins that interact with cognin in the cytoplasmic and plasma membrane-mitochondrial fractions. As the learning-related upregulation of cognin has been shown to occur in the plasma membrane-mitochondrial fraction and not in the cytoplasmic fraction, we studied the effect of training on three cognin-interacting partners in the plasma membrane-mitochondrial fraction: the b5 subunit of mitochondrial ATP synthase and the alpha-2 and alpha-3 subunits of sodium-potassium ATPase. Learning-related upregulation was found in the left intermediate medial mesopallium 24 hours after training for the b5 subunit of mitochondrial ATP synthase and the alpha-2 subunit of sodium-potassium ATPase. The hemispheric asymmetry revealed here is consistent with the predominance of many other learning-related effects in the left intermediate medial mesopallium. The alpha-2 subunit of sodium-potassium ATPase is mainly expressed in astrocytes, supporting a role for these glial cells in memory.

Src and Memory: A Study of Filial Imprinting and Predispositions in the Domestic Chick

“…Evidence from ablation experiments indicates that both the left and the right IMM have a storage function but that, in addition, the right IMM is necessary for subsequent storage without the IMM, in an, as yet, unidentified region termed S' (Cipolla-Neto et al, 1982 ); as shown in Solomonia et al ( 2000 ) and Tiunova et al ( 2019 ) for possible candidate regions for S'. Learning-related biochemical changes are usually more strongly expressed in the left IMM than in the right IMM, especially 24 h after imprinting (Solomonia and McCabe, 2015 ; see also Margvelani et al, 2018a ; Chitadze et al, 2020 ). The present study provides additional evidence of hemispheric asymmetry.…”

“…Several proteins are changed in a learning-related manner following imprinting (reviewed in Solomonia and McCabe, 2015 ). The affected proteins include, among others, cell adhesion molecules, neurotransmitter receptors, protein kinases and their substrates, transcription factors, mitochondrial and membrane proteins, vesicle recycling components, and translation factors (McCabe and Horn, 1988 , 1994 ; Sheu et al, 1993 ; Solomonia et al, 1997 , 1998 , 2000 , 2003 , 2005 , 2008 , 2011 , 2013 ; Meparishvili et al, 2015 ; Margvelani et al, 2018a , b ; Chitadze et al, 2020 ). Further results indicate that neurotransmitter release in the IMM is modulated with memory after imprinting (McCabe et al, 2001 ; Meredith et al, 2004 ).…”

“…Several proteins are changed in a learning-related manner following imprinting (reviewed in Solomonia and McCabe, 2015). The affected proteins include, among others, cell adhesion molecules, neurotransmitter receptors, protein kinases and their substrates, transcription factors, mitochondrial and membrane proteins, vesicle recycling components, and translation factors Horn, 1988, 1994;Sheu et al, 1993;Solomonia et al, 1997Solomonia et al, , 1998Solomonia et al, , 2000Solomonia et al, , 2003Solomonia et al, , 2005Solomonia et al, , 2008Solomonia et al, , 2011Solomonia et al, , 2013Meparishvili et al, 2015;Margvelani et al, 2018a,b;Chitadze et al, 2020).…”

Filial imprinting in domestic chicks; cytoplasmic polyadenylation element binding protein 3, predispositions and learning

“…Autoradiographs were calibrated with protein standards from the P2 mitochondrial-membrane fraction of IMMs of untrained chicks. Four standards (15,30,45, and 60 μg of total protein) were applied to each gel. For regression analysis, the optical density of each band from each sample was divided by the optical density which, from the calibration of the same autoradiograph, corresponded to 30 μg of total protein in the standard [16].…”

“…A series of learning-related molecular changes has been, thus, identified in the IMM, changes that are involved in a progression from transient/labile to trophic synaptic modifications, culminating in stable recognition memory [7–16]. These changes occur in proteins involved in cell adhesion, neurotransmitter release, cytoskeletal organization, oxidative phosphorylation, mitochondrial dynamics, local protein synthesis, and others [7–16].…”