Blubber transcriptome response to acute stress axis activation involves transient changes in adipogenesis and lipolysis in a fasting-adapted marine mammal

J I Khudyakov,D E Crocker,C D Champagne,L M Meneghetti

doi:10.1038/srep42110

Abstract

Stress can compromise an animal’s ability to conserve metabolic stores and participate in energy-demanding activities that are critical for fitness. Understanding how wild animals, especially those already experiencing physiological extremes (e.g. fasting), regulate stress responses is critical for evaluating the impacts of anthropogenic disturbance on physiology and fitness, key challenges for conservation. However, studies of stress in wildlife are often limited to baseline endocrine measurements and few have investigated stress effects in fasting-adapted species. We examined downstream molecular consequences of hypothalamic-pituitary-adrenal (HPA) axis activation by exogenous adrenocorticotropic hormone (ACTH) in blubber of northern elephant seals due to the ease of blubber sampling and its key role in metabolic regulation in marine mammals. We report the first phocid blubber transcriptome produced by RNAseq, containing over 140,000 annotated transcripts, including metabolic and adipocytokine genes of interest. The acute response of blubber to stress axis activation, measured 2 hours after ACTH administration, involved highly specific, transient (lasting <24 hours) induction of gene networks that promote lipolysis and adipogenesis in mammalian adipocytes. Differentially expressed genes included key adipogenesis factors which can be used as blubber-specific markers of acute stress in marine mammals of concern for which sampling of other tissues is not possible.

Highlights

To sources of anthropogenic disturbance that may cause stress and have adverse physiological impacts
We recently used an RNA sequencing (RNAseq) approach to identify genes differentially expressed in skeletal muscle of free-ranging elephant seals in response to acute corticosteroid elevation induced by administration of exogenous ACTH16,17
Acute corticosteroid elevation in juvenile northern elephant seals was induced by administration of exogenous ACTH (exACTH), which has been shown to rapidly increase circulating cortisol, aldosterone, glucose, and free fatty acids in juveniles and adults of this species[16,19,20]

Summary

Introduction

To sources of anthropogenic disturbance that may cause stress and have adverse physiological impacts. While gene expression changes can supplement hormone measurements as markers of stress, few studies have examined the downstream molecular effects of acute HPA axis activation in wild animals. We produced the first phocid blubber transcriptome containing 140,672 annotated transcripts, which include many metabolic genes of interest, and identified key regulators of adipogenesis and lipid homeostasis as markers of acute HPA axis activation in blubber. These data represent a valuable addition to the conservation physiologist’s toolset for evaluating stress states in free-ranging marine mammal species of concern from which blubber, but not blood samples, are possible to obtain (e.g. cetaceans)

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