Dataset Information

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

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.

SUBMITTER: Khudyakov JI

PROVIDER: S-EPMC5301240 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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

Khudyakov J I JI Champagne C D CD Meneghetti L M LM Crocker D E DE

Scientific reports 20170210

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 measureme ...[more]

PMID: 28186107

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Project description:Blubber is a modified subcutaneous adipose tissue in marine mammals that provides energy storage, thermoregulation, hydrodynamic locomotion, and buoyancy. Blubber displays vertical stratification by lipid content, fatty acid composition, and vascularization, leading to the assumption that deeper blubber layers are metabolically active, while superficial layers are mainly structural and thermoregulatory. However, few studies have examined functional stratification of marine mammal blubber directly, especially in pinnipeds. We characterized morphological and transcriptional differences across blubber layers in the northern elephant seal, a deep-diving and fasting-adapted phocid. We collected blubber from seals early in their fasting period and divided blubber cores into three similarly sized portions. We hypothesized that the innermost blubber portion would have higher 1) heterogeneity in adipocyte size, 2) microvascular density, and 3) expression of genes associated with metabolism and hormone signaling than outer blubber. We found that adipocyte area and variance increased from outermost (skin-adjacent) to innermost (muscle-adjacent) blubber layers, suggesting that inner blubber has a higher capacity for lipid storage and turnover than outer blubber. Inner blubber had a higher proportion of CD144+ endothelial cells, suggesting higher microvascular density. In contrast, outer blubber had a higher proportion of CD4+ immune cells than inner blubber, suggesting higher capacity for response to tissue injury. Transcriptome analysis identified 61 genes that were differentially expressed between inner and outer blubber layers, many of which have not been studied previously in marine mammals. Based on known functions of these genes in other mammals, we suggest that inner blubber has potentially higher 1) adipogenic capacity, 2) cellular diversity, and 3) metabolic and neuroendocrine signaling activity, while outer blubber may have higher 1) extracellular matrix synthesis activity and 2) responsiveness to pathogens and cell stressors. We further characterized expression of nine genes of interest identified by transcriptomics and two adipokines with higher precision across blubber layers using targeted assays. Our study provides functional insights into stratification of blubber in marine mammals and a molecular key, including CD144, CD4, HMGCS2, GABRG2, HCAR2, and COL1A2, for distinguishing blubber layers for physiological and functional studies in seals.

Project description:Evaluating the impacts of anthropogenic disturbance on free-ranging marine mammal populations, many of which are in decline, requires robust diagnostic markers of physiological stress and health. However, circulating levels of canonical 'stress hormones' such as glucocorticoids, which are commonly used to evaluate animal health, do not capture the complexity of species-specific responses and cannot be easily measured in large, fully aquatic marine mammals. Alternatively, expression of stress-responsive genes in hormone target tissues such as blubber, the specialized subcutaneous adipose tissue that can be manually or remotely sampled from many marine mammals, may be a more informative and sensitive indicator of recent (within 24 h) exposure to stressors. We previously identified genes that were upregulated in the inner blubber of juvenile northern elephant seals during experimental stimulation of the hypothalamic-pituitary-adrenal axis. In this study, we measured baseline expression levels of a subset of these genes in inner blubber of unmanipulated juvenile elephant seals of varying physiological states and correlated them with other stress markers (body condition index, corticosteroid and thyroid hormone levels). Expression of 10 genes, including those associated with lipid metabolism (ACSL1, HMGCS2, CDO1), redox homeostasis (GPX3), adipokine signaling (ADIPOQ), lipid droplet formation (PLIN1, CIDEA) and adipogenesis (DKK1, AZGP1, TGFBI), was described by three principal components and was associated with cortisol and thyroid hormone levels. Significantly, baseline gene expression levels were predictive of circulating hormone levels, suggesting that these markers may be potential indicators of exposure to stressors in marine mammal species that are inaccessible for blood sampling. A similar approach may be used to identify species-specific stress markers in other tissues that can be sampled by remote biopsy dart from free-ranging marine mammals, such as outer blubber and skin.

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Dataset Information

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

Publications

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

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