Biochemical properties of heterologously expressed and native adenylyl cyclases from the honeybee brain (Apis mellifera L.)

Fuss, Nadine; Mujagić, Samir; Erber, Joachim; Wachten, Sebastian; Baumann, Arnd

doi:10.1016/j.ibmb.2010.05.004

Cited by 4 publications

(3 citation statements)

References 49 publications

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“…In the honeybee, a first gene encoding an AC protein, AmAC3, was identified (Wachten et al 2006) and its biochemical and pharmacological properties were characterized in vitro (Fuss et al 2010). Moreover, recent studies indicate the presence of other ACs besides AmAC3 (Balfanz et al 2012).…”

Section: The Role Of Ac In L-ltm Formation In Honeybeesmentioning

confidence: 99%

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

et al. 2014

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Memory is a dynamic process that allows encoding, storage, and retrieval of information acquired through individual experience. In the honeybee Apis mellifera, olfactory conditioning of the proboscis extension response (PER) has shown that besides short-term memory (STM) and mid-term memory (MTM), two phases of long-term memory (LTM) are formed upon multiple-trial conditioning: an early phase (e-LTM) which depends on translation from already available mRNA, and a late phase (l-LTM) which requires de novo transcription and translation. Here we combined olfactory PER conditioning and neuropharmacological inhibition and studied the involvement of the NO-cGMP pathway, and of specific molecules, such as cyclic nucleotide-gated channels (CNG), calmodulin (CaM), adenylyl cyclase (AC), and Ca 2+ /calmodulin-dependent protein kinase (CaMKII), in the formation of olfactory LTM in bees. We show that in addition to NO-cGMP and cAMP-PKA, CNG channels, CaM, AC, and CaMKII also participate in the formation of a l-LTM (72-h post-conditioning) that is specific for the learned odor. Importantly, the same molecules are dispensable for olfactory learning and for the formation of both MTM (in the minute and hour range) and e-LTM (24-h post-conditioning), thus suggesting that the signaling pathways leading to l-LTM or e-LTM involve different molecular actors.

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Section: The Role Of Ac In L-ltm Formation In Honeybeesmentioning

confidence: 99%

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

et al. 2014

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“…In contrast to processes restricted to the AL, systemic inhibition of adenylyl cyclases (AC) blocks lLTM, whereas eLTM is left intact (Matsumoto et al 2014). This result suggests that different ACs are involved in the formation of eLTM and lLTM shortly after conditioning, a notion that is supported by the cloning and characterization of different AC genes from the honeybee brain (Wachten et al 2006;Fuss et al 2010;Balfanz et al 2012). So, in addition to PKA, other cAMP target proteins such as cyclic-nucleotide gated ion channels (CGN) and exchange proteins (EPAC), might play a role in eLTM and lLTM formation.…”

mentioning

confidence: 77%

Molecular mechanisms underlying formation of long-term reward memories and extinction memories in the honeybee (Apis mellifera)

Eisenhardt

2014

Learn. Mem.

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The honeybee (Apis mellifera) has long served as an invertebrate model organism for reward learning and memory research. Its capacity for learning and memory formation is rooted in the ecological need to efficiently collect nectar and pollen during summer to ensure survival of the hive during winter. Foraging bees learn to associate a flower's characteristic features with a reward in a way that resembles olfactory appetitive classical conditioning, a learning paradigm that is used to study mechanisms underlying learning and memory formation in the honeybee. Due to a plethora of studies on appetitive classical conditioning and phenomena related to it, the honeybee is one of the best characterized invertebrate model organisms from a learning psychological point of view. Moreover, classical conditioning and associated behavioral phenomena are surprisingly similar in honeybees and vertebrates, suggesting a convergence of underlying neuronal processes, including the molecular mechanisms that contribute to them. Here I review current thinking on the molecular mechanisms underlying long-term memory (LTM) formation in honeybees following classical conditioning and extinction, demonstrating that an in-depth analysis of the molecular mechanisms of classical conditioning in honeybees might add to our understanding of associative learning in honeybees and vertebrates. Reward memories in honeybeesThe honeybee (Apis mellifera) has long served as an invertebrate model organism for reward learning and memory research (Menzel 2012). Its value as a model organism in this area is rooted in its impressive capacity for learning and memory formation. Honeybees are social insects that exhibit a prounounced divison of labor. During the summer season a honeybee colony consists of a single, reproductive queen, a few hundred drones, and tens of thousands of sterile worker bees. Depending on their age, worker bees either work inside the hive and fulfill hive duties such as brood rearing, or forage outside the hive collecting nectar or pollen to nourish the queen, workers, and brood. During the winter, long-living worker bees stay inside the hive, clustering around the queen to keep her temperature constant and ensure her survival. Survival during the winter season is only possible when sufficient nectar and pollen has been collected during the summer and is stored in the hive (Seeley and Visscher 1985;Winston 1991;Seeley 1995. Honeybees visit one particular flower species during a foraging trip and collect nectar and pollen from the same food source as long as it is productive (Free 1963;Greggers and Menzel 1993;Greggers and Mauelshagen 1997;Gruter et al. 2011). Accordingly, honeybees learn the properties of a food source including its location and sensory characteristics such as odor, color, and shape (von Frisch 1967; for recent reviews, see Sandoz 2011; AvarguesWeber and Giurfa 2013;Hempel de Ibarra et al. 2014). They also learn the quantity or quality of the food source and the time of day at which it displays its highest total sugar c...

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“…The number of PKA substrates draws attention to the significance of AC, which operates in most cells, including insect cells, first discovered over 30 years ago [ 4 ]. They have been documented in a wide range of insect tissues, including prothoracic glands of the tobacco hornworm, Manduca sexta [ 5 ] and silkworm, Bombyx mori [ 6 ] and brains of Drosophila melanogaster and honey bees, Apis mellifera [ 7 ]. ACs act in a very wide array of cellular functions.…”

Section: Introductionmentioning

confidence: 99%

An adenylyl cyclase like-9 gene (NlAC9) influences growth and fecundity in the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae)

Huang

et al. 2017

PLoS ONE

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The cAMP/PKA intracellular signaling pathway is launched by adenylyl cyclase (AC) conversion of adenosine triphosphate (ATP) to 3', 5'-cyclic AMP (cAMP) and cAMP-dependent activation of PKA. Although this pathway is very well known in insect physiology, there is little to no information on it in some very small pest insects, such as the brown planthopper (BPH), Nilaparvata lugens Stål. BPH is a destructive pest responsible for tremendous crop losses in rice cropping systems. We are investigating the potentials of novel pest management technologies from RNA interference perspective. Based on analysis of transcriptomic data, the BPH AC like-9 gene (NlAC9) was up-regulated in post-mating females, which led us to pose the hypothesis that NlAC9 is a target gene that would lead to reduced BPH fitness and populations. Targeting NlAC9 led to substantially decreased soluble ovarian protein content, yeast-like symbiont abundance, and vitellogenin gene expression, accompanied with stunted ovarian development and body size. Eggs laid were decreased and oviposition period shortened. Taken together, our findings indicated that NlAC9 exerted pronounced effects on female fecundity, growth and longevity, which strongly supports our hypothesis.

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Biochemical properties of heterologously expressed and native adenylyl cyclases from the honeybee brain (Apis mellifera L.)

Cited by 4 publications

References 49 publications

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee

Molecular mechanisms underlying formation of long-term reward memories and extinction memories in the honeybee (Apis mellifera)

An adenylyl cyclase like-9 gene (NlAC9) influences growth and fecundity in the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae)

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