Molecular Genetic Analysis of Sexual Rejection: Roles of Octopamine and Its Receptor OAMB in<i>Drosophila</i>Courtship Conditioning

Zhou, Chuan; Huang, Hai; Kim, Susy M.; Lin, Hsuan-Wen; Meng, Xianglan; Han, Kuo; Chiang, Ann‐Shyn; Wang, Jing W.; Jiao, Renjie; Rao, Yi

doi:10.1523/jneurosci.0517-12.2012

Cited by 66 publications

(66 citation statements)

References 33 publications

(50 reference statements)

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“…Octopamine immunoreactivity is observed in the calyx and γ lobes (Sinakevitch and Strausfeld, 2006). While the αβ and α′β′ lobes are devoid of octopamine immunoreactivity, MARCM and GRASP analyses that allow high spatial resolution imaging reveal the octopamine neurons innervating the αβ lobes (Zhou et al, 2012). The calyx has OAMB-AS, but not OAMB-K3, immunoreactivity and this immunoreactivity is contributed by extrinsic, but not intrinsic, mushroom body neurons (J. Lim and K.-A.…”

Section: Discussionmentioning

confidence: 99%

Appetitive Learning Requires the Alpha1-Like Octopamine Receptor OAMB in theDrosophilaMushroom Body Neurons

et al. 2013

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Associative learning is a fundamental form of behavioral plasticity. Octopamine plays central roles in various learning types in invertebrates, however the target receptors and underlying mechanisms are poorly understood. Drosophila provides a powerful system to uncover the mechanisms for learning and memory. Here, we report that OAMB in the mushroom body neurons mediates the octopamine’s signal for appetitive olfactory learning. The octopamine receptor OAMB has two isoforms (OAMB-K3 and OAMB-AS), differing in the third cytoplasmic loop and downstream sequence. The activation of each OAMB isoform increases intracellular Ca2+ similar to the alpha1 adrenergic receptor, while OAMB-K3 additionally stimulates cAMP production. The oamb null mutants showed severely impaired learning in appetitive olfactory conditioning that tests flies’ capacity to learn and remember the odor associated with sugar reward. This deficit was also seen in the hypomorphic mutant with reduced OAMB expression in the mushroom bodies, the brain structure crucial for olfactory conditioning. Consistently, the oamb mutant’s learning phenotype was fully rescued by conditional expression of either OAMB isoform in the mushroom body αβ and γ neurons. These results indicate that the OAMB receptor is a key molecule mediating the octopamine’s signal for appetitive olfactory learning and its functional site is the mushroom body αβ and γ neurons. This study represents a critical step forward in understanding the cellular mechanism and neural circuit mediating reward learning and memory.

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Section: Discussionmentioning

confidence: 99%

Appetitive Learning Requires the Alpha1-Like Octopamine Receptor OAMB in theDrosophilaMushroom Body Neurons

et al. 2013

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“…Since octopamine is known to control aggression in Drosophila males (Baier et al 2002;Hoyer et al 2008;Zhou et al 2008Zhou et al , 2012Certel et al 2010;Erion et al 2012), to establish if TfAP-2 and Twz were required for octopamineregulated male behavior, we performed an aggression assay. To do this, Tdc2-GAL4, UAS-Tfap2 RNAi , UAS-Twz RNAi , and UASTfap2 OE were all crossed to w 1118 , and the heterozygous progeny were used as controls.…”

Section: Ap-2 and Twz Regulate Male Behaviormentioning

confidence: 99%

“…The behavioral decision to be aggressive is in part controlled by systems that also regulate metabolism, such as the monoamine system (Dierick and Greenspan 2007;Hoyer et al 2008;Zhou et al 2008;Alekseyenko et al 2010). In the fruit fly Drosophila melanogaster, it was determined that a major regulator of male aggressive and mating behavior is the noradrenaline analog, octopamine (Baier et al 2002;Hoyer et al 2008;Zhou et al 2008Zhou et al , 2012Certel et al 2010;Erion et al 2012). In addition, the monoamines dopamine and serotonin have been linked to the regulation of aggressive behavior (Lucki 1998;Baier et al 2002;Alekseyenko et al 2010Alekseyenko et al , 2013Belsare et al 2010).…”

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confidence: 99%

Regulation of Aggression by Obesity-Linked GenesTfAP-2andTwzThrough Octopamine Signaling inDrosophila

et al. 2014

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In Drosophila, the monoamine octopamine, through mechanisms that are not completely understood, regulates both aggression and mating behavior. Interestingly, our study demonstrates that the Drosophila obesity-linked homologs Transcription factor AP-2 (TfAP-2; TFAP2B in humans) and Tiwaz (Twz; KCTD15 in humans) interact to modify male behavior by controlling the expression of Tyramine b-hydroxylase and Vesicular monanime transporter, genes necessary for octopamine production and secretion. Furthermore, we reveal that octopamine in turn regulates aggression through the Drosophila cholecystokinin satiation hormone homolog Drosulfakinin (Dsk). Finally, we establish that TfAP-2 is expressed in octopaminergic neurons known to control aggressive behavior and that TfAP-2 requires functional Twz for its activity. We conclude that genetically manipulating the obesity-linked homologs TfAP-2 and Twz is sufficient to affect octopamine signaling, which in turn modulates Drosophila male behavior through the regulation of the satiation hormone Dsk.

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“…sNPF is expressed in the mushroom bodies and has been implicated in regulating IPCs (Nassel et al 2013) while it also acts as a neuromodulator in olfactory memory (Knapek et al 2013). Mushroom bodies also play important roles in courtship behavior and courtship learning or conditioning (Sakai and Kitamoto 2006;Keleman et al 2012;Zhou et al 2012). Finally, the expression of Nep1 in abdominal ganglia suggests a possible role in modulating sperm transfer and copulation duration that is regulated by corazonin expressed in the abdominal ganglia (Tayler et al 2012).…”

Section: Implications Of Neprilysins 1-5 Expression Patternsmentioning

confidence: 99%

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

et al. 2014

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Members of the M13 class of metalloproteases have been implicated in diseases and in reproductive fitness. Nevertheless, their physiological role remains poorly understood. To obtain a tractable model with which to analyze this protein family's function, we characterized the gene family in Drosophila melanogaster and focused on reproductive phenotypes. The D. melanogaster genome contains 24 M13 class protease homologs, some of which are orthologs of human proteases, including neprilysin. Many are expressed in the reproductive tracts of either sex. Using RNAi we individually targeted the five Nep genes most closely related to vertebrate neprilysin, Nep1-5, to investigate their roles in reproduction. A reduction in Nep1, Nep2, or Nep4 expression in females reduced egg laying. Nep1 and Nep2 are required in the CNS and the spermathecae for wild-type fecundity. Females that are null for Nep2 also show defects as hosts of sperm competition as well as an increased rate of depletion for stored sperm. Furthermore, eggs laid by Nep2 mutant females are fertilized normally, but arrest early in embryonic development. In the male, only Nep1 was required to induce normal patterns of female egg laying. Reduction in the expression of Nep2-5 in the male did not cause any dramatic effects on reproductive fitness, which suggests that these genes are either nonessential for male fertility or perform redundant functions. Our results suggest that, consistent with the functions of neprilysins in mammals, these proteins are also required for reproduction in Drosophila, opening up this model system for further functional analysis of this protein class and their substrates. P ROTEASES play key roles in diverse physiological systems. One such family of metalloproteases, the M13 class of neutral endopeptidases, consists mainly of membranebound zinc proteases that are involved in the processing of neuropeptides and peptide hormones (reviewed in Turner et al. 2000;Turner et al. 2001;Bland et al. 2008). In mammals, seven members of this family have been identified, of which neprilysin (NEP) and endothelin converting enzyme (ECE) are the best studied. These proteins have been implicated in various diseases including cardiovascular disease (Segura and Ruilope 2011;Wick et al. 2011), Alzheimer's disease (Mulder et al. 2012;Klein et al. 2013), inflammation and inflammatory disorders (Wong et al. 2011), and cancer (Smollich et al. 2007;Maguer-Satta et al. 2011).In addition to their role in disease, NEPs are essential for development and reproduction in mammals. The mammalian Neprilysin-2, called NL1 in mice, is highly expressed in the testis. NL1-deficient males sire fewer pups, even though spermatogenesis appears to be unaffected (Carpentier et al. 2004). In females, NEP expression in the uterus is modulated by estrogen treatment in rats (Pinto et al. 1999) and during the estrogen/progesterone cycle in humans (Head et al. 1993). In female rats and mice, controlled degradation of tachykinins, particularly substance-P, by NEP in the uterus ...

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Molecular Genetic Analysis of Sexual Rejection: Roles of Octopamine and Its Receptor OAMB inDrosophilaCourtship Conditioning

Cited by 66 publications

References 33 publications

Appetitive Learning Requires the Alpha1-Like Octopamine Receptor OAMB in theDrosophilaMushroom Body Neurons

Appetitive Learning Requires the Alpha1-Like Octopamine Receptor OAMB in theDrosophilaMushroom Body Neurons

Regulation of Aggression by Obesity-Linked GenesTfAP-2andTwzThrough Octopamine Signaling inDrosophila

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

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