Localization and Functional Characterization of a Novel Adipokinetic Hormone in the Mollusk, Aplysia californica

Johnson, Joshua I.; Kavanaugh, Scott I.; Nguyen, Cindy B.; Tsai, Pei‐San

doi:10.1371/journal.pone.0106014

Cited by 29 publications

(36 citation statements)

References 61 publications

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“…In insects, this topic has been addressed in the cricket Gryllus bimaculatus , and outside of the phylum Insecta in the mollusk Aplysia californica . AKH signaling reduces feeding in both crickets and mollusks . In contrast, we show here that the Drosophila AKH is an orexigenic peptide.…”

Section: Discussionmentioning

confidence: 66%

“…In comparison to the functions in energy mobilization, food intake‐related actions of AKH have been relatively understudied so far. In insects, this topic has been addressed in the cricket Gryllus bimaculatus , and outside of the phylum Insecta in the mollusk Aplysia californica . AKH signaling reduces feeding in both crickets and mollusks .…”

Section: Discussionmentioning

confidence: 99%

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The obesity‐related Adipokinetic hormone controls feeding and expression of neuropeptide regulators of Drosophila metabolism

Gáliková

Klepsatel

et al. 2016

Euro J Lipid Sci & Tech

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Homeostasis of circulating and storage energy reserves in mammals is dependent on the antagonistically acting insulin and glucagon signaling. In the model organism Drosophila melanogaster, this function is executed by the insulin‐like peptides and the glucagon‐like Adipokinetic hormone (AKH). Loss of Drosophila AKH results in the adulthood‐specific onset of obesity coupled with hypoglycemia. However, apart from the role of AKH in the lipid mobilization, the physiological and endocrine underpinnings of the AKH deficiency‐triggered obesity are unknown. Here, we investigate the role of AKH in feeding and metabolic rate control, and address the interactions of this hormone with other endocrine regulators of fly metabolism. Via in vivo gain‐ and loss‐of‐function analyses, we show that despite its anti‐obesity effects, AKH is an orexigenic peptide. Moreover, AKH also affects expression of orexigenic factors CCHamide‐2 and neuropeptide F. In addition, AKH regulates metabolic genes like Corazonin, Limostatin, and Insulin‐like peptides (Ilps) 2, 3, 5, and 6. Altogether, our work shows that the Drosophila AKH is a central regulator of energy homeostasis; next to its well‐known role in the control of energy expenditure, this hormone controls also food intake, and expression of other endocrine regulators of fly metabolism. Practical applications: Basic research of the neuroendocrine regulation of metabolism in the fruit fly D. melanogaster has potential applications in both human medicine and insect pest control. The evolutionary conservation of the key metabolic pathways, together with the unprecedented choice of transgenic tools turned the fruit fly into a useful model to study human diseases, including obesity and diabetes. Based on the evolutionary conservation of AKH and glucagon functions, our investigations might provide useful hints regarding the physiological actions, and endocrine interactions of human glucagon, too. In addition, insect neuropeptides are emerging as important targets for the parasite and pest control; understanding of their regulatory networks has thus potential implications also in the development of novel insecticides. Adipokinetic hormone (AKH) is an insect analog of the human hormone glucagon. Our investigations of the roles of this hormone in the model organism Drosophila melanogaster have shown that this anti‐obesity factor is a central regulator of fly metabolism, and controls crucial processes such as feeding, metabolic rate, storage of energy reserves, and expression of regulatory genes from the neuropeptide hormone family, including the fly homologs of human insulin.

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Section: Discussionmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

The obesity‐related Adipokinetic hormone controls feeding and expression of neuropeptide regulators of Drosophila metabolism

Gáliková

Klepsatel

et al. 2016

Euro J Lipid Sci & Tech

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“…qPCR primers for ac-akh were designed based on the previously published sequence (11). qPCR of ac-akh was carried out using FastStart Universal SYBR Green mix (Roche, Indianapolis, IN) and calculated using the 2 −ΔΔ CT method (26).…”

Section: Methodsmentioning

confidence: 99%

An Adipokinetic Hormone Acts as a Volume Regulator in the Intertidal Gastropod Mollusk, Aplysia californica

Martillotti

Tsai

2018

Front. Endocrinol.

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Adipokinetic hormone (AKH) is a multifunctional neuropeptide in the gonadotropin-releasing hormone superfamily. In insects, AKH acts to mobilize energy stores during times of high energetic demand, but has been shown to have other effects. In lophotrochozoans, the presence and function of AKH are less characterized. We have previously identified an AKH in an intertidal gastropod mollusk, the California sea hare (Aplysia californica), and named it ac-AKH. Our previous data showed ac-AKH induced an acute weight loss, suggesting a role in volume regulation. The overarching goals of this study were to test the role of ac-AKH as a volume regulator and examine the mechanism by which ac-AKH induced the acute weight loss. Our results showed that ac-AKH reduced body mass, in part, through the reduction of hemolymph volume without altering hemolymph osmolality or specific osmolytes. The effect of ac-AKH on volume loss was accentuated under a hyposaline condition. We further showed that ac-akh expression was inhibited during a hyposaline challenge, and that the administration of ac-AKH partially reversed the increase in body mass, but not hemolymph osmolality change, caused by the hyposaline challenge. These data collectively show that ac-AKH is a proximate regulator controlling the fluid volume, but not osmolality, in A. californica. Importantly, our results highlight the functional divergence of this structurally conserved neuropeptide in the molluscan lineage.

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“…Mollusca (Johnson, Kavanaugh, Nguyen, & Tsai, 2014), and the AKH peptide family is now considered part of the gonadotropin releasing hormone (GnRH) superfamily (Gäde, Šimek, & Marco, 2011b;Hauser & Grimmelikhuijzen, 2014;Roch, Busby, & Sherwood, 2011, 2014. The primary structural characteristics of the AKH family peptides is a chain length of 8-10 amino acids, at least two posttranslational modifications (one at the N-terminus as a pyroglutamate residue and one at the C-terminus as a carboxyamide), an aromatic amino acid such as phenylalanine or tyrosine at position 4, a branched amino acid such as serine or threonine at position 5, always the aromatic tryptophan at position 8, and a glycine residue at position 9 (Gäde et al, 1997b).…”

mentioning

confidence: 99%

The adipokinetic hormone of Mantodea in comparison to other Dictyoptera

GÄde

Marco

2017

Arch Insect Biochem Physiol

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Six species of the order Mantodea (praying mantises) are investigated for the presence and sequence of putative adipokinetic hormones (AKHs). The selected species span a wide evolutionary range of various families and subfamilies of the clade Mantodea. The corpora cardiaca of the different species are dissected, methanolic extracts prepared, peptides separated by liquid chromatography, and AKHs detected and sequenced by ion trap mass spectrometry. All six species investigated contain an octapeptide with the primary structure pGlu-Val-Asn-Phe-Thr-Pro-Asn-Trp amide, which is code-named Emppe-AKH and had been found earlier in three other species of Mantodea. Conspecific bioassays with the species Creoboter sp. (family Hymenopodidae) reveal an adipokinetic but not a hypertrehalosemic function of Emppe-AKH. Comparison with other members of the Dictyoptera (cockroaches, termites) show that Emppe-AKH is only found in certain termites, which have been recently placed into the Blattaria (cockroaches) as sister group to the family Cryptocercidae. Termites and cockroaches both show biodiversity in the sequence of AKHs, and some cockroach species even contain two AKHs. In contrast, all praying mantises-irrespective of their phylogenetic position-synthesize uniformly only one and the same octapeptide Emppe-AKH.

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Localization and Functional Characterization of a Novel Adipokinetic Hormone in the Mollusk, Aplysia californica

Cited by 29 publications

References 61 publications

The obesity‐related Adipokinetic hormone controls feeding and expression of neuropeptide regulators of Drosophila metabolism

The obesity‐related Adipokinetic hormone controls feeding and expression of neuropeptide regulators of Drosophila metabolism

An Adipokinetic Hormone Acts as a Volume Regulator in the Intertidal Gastropod Mollusk, Aplysia californica

The adipokinetic hormone of Mantodea in comparison to other Dictyoptera

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