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Article

PaOctβ2R: Identification and Functional Characterization of an Octopamine Receptor Activating Adenylyl Cyclase Activity in the American Cockroach Periplaneta americana

by
Wolfgang Blenau
1,†,
Anna-Sophie Bremer
2,†,
Yannik Schwietz
3,
Daniel Friedrich
4,
Lapo Ragionieri
5,
Reinhard Predel
5,
Sabine Balfanz
2 and
Arnd Baumann
2,*
1
Institute of Biochemistry, Leipzig University, 04103 Leipzig, Germany
2
Institute of Biological Information Processing, IBI-1, Research Center Jülich, 52428 Jülich, Germany
3
Department of Biology, Philipps University of Marburg, 35037 Marburg, Germany
4
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
5
Institute of Zoology, University of Cologne, 50923 Cologne, Germany
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to the work.
Int. J. Mol. Sci. 2022, 23(3), 1677; https://doi.org/10.3390/ijms23031677
Submission received: 7 January 2022 / Revised: 28 January 2022 / Accepted: 28 January 2022 / Published: 31 January 2022
(This article belongs to the Collection State-of-the-Art Molecular Neurobiology in Germany)
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Abstract

Biogenic amines constitute an important group of neuroactive substances that control and modulate various neural circuits. These small organic compounds engage members of the guanine nucleotide-binding protein coupled receptor (GPCR) superfamily to evoke specific cellular responses. In addition to dopamine- and 5-hydroxytryptamine (serotonin) receptors, arthropods express receptors that are activated exclusively by tyramine and octopamine. These phenolamines functionally substitute the noradrenergic system of vertebrates Octopamine receptors that are the focus of this study are classified as either α- or β-adrenergic-like. Knowledge on these receptors is scarce for the American cockroach (Periplaneta americana). So far, only an α–adrenergic-like octopamine receptor that primarily causes Ca2+ release from intracellular stores has been studied from the cockroach (PaOctα1R). Here we succeeded in cloning a gene from cockroach brain tissue that encodes a β-adrenergic-like receptor and leads to cAMP production upon activation. Notably, the receptor is 100-fold more selective for octopamine than for tyramine. A series of synthetic antagonists selectively block receptor activity with epinastine being the most potent. Bioinformatics allowed us to identify a total of 19 receptor sequences that build the framework of the biogenic amine receptor clade in the American cockroach. Phylogenetic analyses using these sequences and receptor sequences from model organisms showed that the newly cloned gene is an β2-adrenergic-like octopamine receptor. The functional characterization of PaOctβ2R and the bioinformatics data uncovered that the monoaminergic receptor family in the hemimetabolic P. americana is similarly complex as in holometabolic model insects like Drosophila melanogaster and the honeybee, Apis mellifera. Thus, investigating these receptors in detail may contribute to a better understanding of monoaminergic signaling in insect behavior and physiology.
Keywords: biogenic amines; cellular signaling; cockroach; gene annotation; gene family; GPCR; second messenger biogenic amines; cellular signaling; cockroach; gene annotation; gene family; GPCR; second messenger

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MDPI and ACS Style

Blenau, W.; Bremer, A.-S.; Schwietz, Y.; Friedrich, D.; Ragionieri, L.; Predel, R.; Balfanz, S.; Baumann, A. PaOctβ2R: Identification and Functional Characterization of an Octopamine Receptor Activating Adenylyl Cyclase Activity in the American Cockroach Periplaneta americana. Int. J. Mol. Sci. 2022, 23, 1677. https://doi.org/10.3390/ijms23031677

AMA Style

Blenau W, Bremer A-S, Schwietz Y, Friedrich D, Ragionieri L, Predel R, Balfanz S, Baumann A. PaOctβ2R: Identification and Functional Characterization of an Octopamine Receptor Activating Adenylyl Cyclase Activity in the American Cockroach Periplaneta americana. International Journal of Molecular Sciences. 2022; 23(3):1677. https://doi.org/10.3390/ijms23031677

Chicago/Turabian Style

Blenau, Wolfgang, Anna-Sophie Bremer, Yannik Schwietz, Daniel Friedrich, Lapo Ragionieri, Reinhard Predel, Sabine Balfanz, and Arnd Baumann. 2022. "PaOctβ2R: Identification and Functional Characterization of an Octopamine Receptor Activating Adenylyl Cyclase Activity in the American Cockroach Periplaneta americana" International Journal of Molecular Sciences 23, no. 3: 1677. https://doi.org/10.3390/ijms23031677

APA Style

Blenau, W., Bremer, A.-S., Schwietz, Y., Friedrich, D., Ragionieri, L., Predel, R., Balfanz, S., & Baumann, A. (2022). PaOctβ2R: Identification and Functional Characterization of an Octopamine Receptor Activating Adenylyl Cyclase Activity in the American Cockroach Periplaneta americana. International Journal of Molecular Sciences, 23(3), 1677. https://doi.org/10.3390/ijms23031677

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