Proteomics reveals selective regulation of proteins in response to memory‐related serotonin stimulation in Aplysia californica ganglia

Abstract

The marine mollusk Aplysia californica (Aplysia) is a powerful model for learning and memory due to its minimalistic nervous system. Key proteins, identified to be regulated by the neurotransmitter serotonin in Aplysia, have been successfully translated to mammalian models of learning and memory. Based upon a recently published large-scale analysis of Aplysia proteomic data, the current study investigated the regulation of protein levels 24 and 48 h after treatment with serotonin in Aplysia ganglia using a 2-D gel electrophoresis approach. Protein spots were quantified and protein-level changes of selected proteins were verified by Western blotting. Among those were Rab GDP dissociation inhibitor alpha (RabGDIα), synaptotagmin-1 and deleted in azoospermia-associated protein (DAZAP-1) in cerebral ganglia, calreticulin, RabGDIα, DAZAP-1, heterogeneous nuclear ribonucleoprotein F (hnRNPF), RACK-1 and actin-depolymerizing factor (ADF) in pleural ganglia and DAZAP-1, hnRNPF and ADF in pedal ganglia. Protein identity of the majority of spots was confirmed by a gel-based mass spectrometrical method (FT-MS). Taken together, protein-level changes induced by the learning-related neurotransmitter serotonin in Aplysia ganglia are described and a role for the abovementioned proteins in synaptic plasticity is proposed.

Transcriptional correlates of memory maintenance following long-term sensitization of Aplysia californica

“…These graphs show the most-represented terms across gene ontology levels (multilevel); the numbers in parenthesis represent a scoring/weighting system used by Blast2Go (Conesa et al 2005) to weight the representation of gene ontology terms. The complexity of response we observed here was not captured in previous proteomic screens, which identified only a handful of changes in protein expression 1 d after LTS training (Castellucci et al 1988) or serotonin exposure (Barzilai et al 1989;Monje et al 2012). It is possible that the transcriptional changes we observed do not always yield alterations in protein expression.…”

“…Despite this, there is a strong concor-dance between our results and these previous screens. For example, our list overlaps with at least 5 of the 19 proteins identified by Monje et al (2012): calponin, calreticulin, glutathione S-transferase, a heterogeneous nuclear riboprotein, and tubulin. 1 Monje et al (2012) identified regulated proteins with the accession number of the closest matching protein in any species making precise matching to Aplysia transcripts somewhat provisional.…”

“…These same two proteins were reconfirmed as persistently regulated in VC sensory neurons in a second screen that used serotonin exposure to mimic the induction of LTS memory (Barzilai et al 1989). Finally, a third screen was recently conducted examining changes in protein expression 1 and 2 d after serotonin exposure in cultured Aplysia ganglia; this identified 18 up-regulated and 1 down-regulated proteins 1 d after exposure in the pleural ganglia (Monje et al 2012).…”

A proteomic analysis of contextual fear conditioned rats reveals dynamic modifications in neuron and oligodendrocyte protein expression in the dentate gyrus

“…Previous studies have already explored memory processes through the prism of proteomics. Both invertebrate (Crow & Xue‐Bian, ; Monje et al ., ) and vertebrate models (Henninger et al ., ; Li et al ., ; Monopoli et al ., ; Kähne et al ., ; Hong et al ., ; Rao‐Ruiz et al ., ; Smidak et al ., ) were investigated. Smidak et al .…”

Characterization of the rapid transcriptional response to long-term sensitization training in Aplysia californica

“…Many others have examined changes in transcription or protein expression at different time points after 5-HT exposure in whole animals, ganglia, or cultured neurons (e.g. Barzilai, Kennedy, Sweatt, & Kandel, 1989; Monje et al, 2011). In a previous analysis of a small set of transcripts, however, we have shown that 5-HT and behavioral training do not always produce similar patterns of transcriptional change in Aplysia californica (Bonnick et al, 2012).…”