Nuclear receptors of the honey bee: annotation and expression in the adult brain

Abstract

The Drosophila genome encodes 18 canonical nuclear receptors. All of the Drosophila nuclear receptors are here shown to be present in the genome of the honey bee ( Apis mellifera ). Given that the time since divergence of the Drosophila and Apis lineages is measured in hundreds of millions of years, the identification of matched orthologous nuclear receptors in the two genomes reveals the fundamental set of nuclear receptors required to 'make' an endopterygote insect. The single novelty is the presence in the A. mellifera genome of a third insect gene similar to vertebrate photoreceptor-specific nuclear receptor (PNR). Phylogenetic analysis indicates that this novel gene, which we have named AmPNR -like, is a new member of the NR2 subfamily not found in the Drosophila or human genomes. This gene is expressed in the developing compound eye of the honey bee. Like their vertebrate counterparts, arthropod nuclear receptors play key roles in embryonic and postembryonic development. Keywords: Apis mellifera , photoreceptor cell specific nuclear receptor, seven-up, steroid hormone receptor, ultraspiracle. IntroductionNuclear receptors constitute a protein superfamily that can be recognized in metazoans as distantly related as jellyfish and humans by the presence of highly conserved Nterminal DNA-binding domains (DBD) with 2 C4 zinc fingers (Robinson-Rechavi & Laudet, 2003). Nuclear receptor superfamily members also contain a conserved C-terminal ligand-binding domain (LBD) that is less conserved than the defining DBD. The variable LBD region of nuclear receptor proteins contains a ligand-binding pocket and a dimerization domain, plus regions that interact with cofactors serving as transcriptional intermediary factors (Moras & Gronemeyer, 1998).Many nuclear receptors regulate transcription via transduction of signals from small, lipophilic molecules such as steroid hormones (Carson-Jurica et al ., 1990;Tsai & O'Malley, 1994). Other nuclear receptor family members, identified on the basis of DBD homology, do not (or did not when they were initially described) have known ligands. They are therefore referred to as orphan receptors (Giguere, 1999). Phylogenetic analysis demonstrates that the earliest members of the nuclear receptor family were the so-called orphans and that ligand-binding capacity was acquired later in animal evolution (Escriva et al ., 1997;Bertrand et al ., 2004).The 49 nuclear receptors identified in the human genome include receptors for the steroid hormones, thyroid

Nuclear receptor BgFTZ‐F1 regulates molting and the timing of ecdysteroid production during nymphal development in the hemimetabolous insect Blattella germanica

“…The role of FTZ-F1 in molting has also been demonstrated in the coleopteran Tribolium castaneum (Tan and Palli, 2008), whereas its role as a competence factor for 20E action has been reported during the previtellogenic-vitellogenic transition in the dipteran Aedes aegypti (Li et al, 2000;Zhu et al, 2003). FTZ-F1 orthologs have also been identified in other holometabolous insects, namely the lepidopterans Manduca sexta (Weller et al, 2001) and Bombyx mori (Sun et al, 1994), and the hymenopteran Apis mellifera (Velarde et al, 2006).…”

Activity-dependent gene expression in honey bee mushroom bodies in response to orientation flight

“…In situ hybridization was performed as previously described (Velarde et al, 2006). Whole brains were dissected in cold physiological saline (Fahrbach et al, 1995), frozen in OCT medium, and cut in 12μm frontal sections.…”

Steroid hormone (20-hydroxyecdysone) modulates the acquisition of aversive olfactory memories in pollen forager honeybees

“…In adult worker honeybees, genes for ecdysteroid signaling have been found to be highly expressed in this region of the brain (Paul et al 2005Velarde et al 2006Velarde et al , 2009Yamazaki et al 2006Yamazaki et al , 2011Takeuchi et al 2007), and marked changes in gene expression in mushroom body intrinsic neurons have been described in response to 20-E (Velarde et al 2009). Interestingly, Velarde et al (2009) also showed that juvenile hormone (JH) modulates the expression of ecdysteroidresponsive receptor genes in the mushroom bodies of adult honeybees, an observation that may be of relevance to findings in this study.…”

“…There is evidence that ecdysteroids also regulate the behavior of adult worker honeybees. Genes involved in ecdysteroid signaling are preferentially expressed in the mushroom bodies of the bee brain (e.g., Paul et al 2005Paul et al , 2006Velarde et al 2006Velarde et al , 2009Yamazaki et al 2006Yamazaki et al , 2011Takeuchi et al 2007), and intrinsic mushroom body neurons (Kenyon cells) of adult worker bees have been shown to respond to ecdysteroids with a predictable cascade of gene expression (Velarde et al 2009). Interestingly, a recent report shows that ecdysone is converted into 20-E not only in fat bodies, but also in the brain of the honeybee, suggesting that ecdysteroids may function as neurohormones in this insect (Yamazaki et al 2011).…”