Autophagy-Associated Shrinkage of the Hepatopancreas in Fasting Male Macrobrachium rosenbergii Is Rescued by Neuropeptide F.

Sirorat Thongrod,Prasert Sobhon,Ciro Isidoro,Wilairat Kankuan,Suratchanee Phadngam,Chaitip Wanichanon,Tanapan Siangcham,Federica Morani

doi:10.3389/fphys.2018.00613

Abstract

Invertebrate neuropeptide F-I (NPF-I), much alike its mammalian homolog neuropeptide Y, influences several physiological processes, including circadian rhythms, cortical excitability, stress response, and food intake behavior. Given the role of autophagy in the metabolic stress response, we investigated the effect of NPF-1 on autophagy during fasting and feeding conditions in the hepatopancreas and muscle tissues of the male giant freshwater prawn Macrobrachium rosenbergii. Starvation up-regulated the expression of the autophagy marker LC3 in both tissues. Yet, based on the relative levels of the autophagosome-associated LC3-II isoform and of its precursor LC3-I, the hepatopancreas was more responsive than the muscle to starvation-induced autophagy. Injection of NPF-I inhibited the autophagosome formation in the hepatopancreas of fasting prawns. Relative to the body weight, the muscle weight was not affected, while that of the hepatopancreas decreased upon starvation and NPF-1 treatment could largely prevent such weight loss. Thus, the hepatopancreas is the reserve organ for the nutrient homeostasis during starvation and NPF-I plays a crucial role in the balancing of energy expenditure and energy intake during starvation by modulating autophagy.

Highlights

Neuropeptide F (NPF), a member of the FMRFamide-related peptide group, plays an important role in the regulation of foraging, feeding-related behavior, circadian rhythm, stress responses, aggression, and energy homeostasis (Nassel and Wegener, 2011), and is considered homologue to mammalian neuropeptide Y (NPY)
The loss of weight and size in the hepatopancreas of starved prawns was largely prevented by NPF: on average, the weight of the hepatopancreas in starved prawns was reduced only by 3.74% when injected with NPF (Figure 2A)
We have recently described the autophagy response to starvation in the ovary of the female giant freshwater prawn M. rosenbergii (Kankuan et al, 2017)

Summary

Introduction

Neuropeptide F (NPF), a member of the FMRFamide-related peptide group, plays an important role in the regulation of foraging, feeding-related behavior, circadian rhythm, stress responses, aggression, and energy homeostasis (Nassel and Wegener, 2011), and is considered homologue to mammalian NPY. Invertebrate NPF was identified first in the flatworm Moniezia expansa (Maule et al, 1991). In Drosophila, NPFs consist of two types, NPF and short NPF (sNPF), and both function in the regulation of food intake and increase of body size (Lee et al, 2004; Carlsson et al, 2013). Two crustacean isoforms of NPF, i.e., NPF-I and NPF-II, have been identified in the penaeid shrimps Litopenaeus vannamei and Marsupenaeus japonicus (Christie et al, 2011). The two isoforms were shown to be differentially expressed in the nervous, midgut and muscle tissues of both species.

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