Changes in serum adipokines during natural extended fasts in female northern elephant seals

Rzucidlo, Caroline L.; Sperou, Emily S.; Holser, Rachel R.; Khudyakov, Jane; Costa, Daniel P.; Crocker, Daniel E.

doi:10.1016/j.ygcen.2021.113760

Cited by 4 publications

(5 citation statements)

References 69 publications

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“…Consistent observations were made by transcriptomic analysis after repeated ACTH injections in juvenile NES during the same life history stage (Deyarmin et al, 2019). In other studies conducted on adult females during both breeding and molting seasons, decreasing circulating levels of adiponectin were associated with increased secretion of CORT (Rzucidlo et al, 2021). Conversely, a similar study related a positive correlation between circulating cortisol levels and ADIPOQ expression in late fasting female NES (Khudyakov et al, 2019).…”

Section: Figuresupporting

confidence: 81%

“…The results obtained in the present study suggest that both CORT and EPI regulate adiponectin expression in NES blubber, although their effects may vary depending on life history stage of individuals as suggested in correlative studies. In regards to resistin expression, we found that neither CORT nor EPI affected resistin expression in NES PCATS, consistent with no change in circulating resistin levels observed over fasting in adult NES (Rzucidlo et al, 2021).…”

Section: Figuresupporting

confidence: 79%

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Cortisol and epinephrine alter the adipose functions and the mobilization of PCBs in adipose tissue slices from elephant seal

Pirard,

Khudyakov,

Crocker

et al. 2023

Front. Mar. Sci.

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Marine mammals are exposed to increasing intensities of anthropogenic stressors such as acoustic disturbance and contaminants. Correlative studies have suggested concerning shifts in behavioral and physiological status of stress-exposed individuals, which could alter the health and survival of marine mammal populations. However, functional studies of the effects of multiple stressors on marine mammals are lacking. To fill in this gap, we recently developed an ex vivo approach of precision-cut adipose tissue slices (PCATS) to study the impact of stressors on the function of an essential endocrine organ: the adipose tissue. In the present study, we investigated the impact of hormones associated with the stress response on adipose tissue from northern elephant seals (Mirounga angustirostris). Blubber biopsies were collected from 17 weaned northern elephant seal pups, separated into inner and outer layers, dissected into PCATS, and cultured for 48 hours. To mimic prolonged and short-term exposure to physiological stress, PCATS were treated with 2 µM cortisol (CORT) for the entire 48 hours or 100 nM epinephrine (EPI) for the last 12 hours of culture, respectively. Hormones were applied individually or in combination. CORT and EPI exhibited an interacting, blubber layer-dependent, effect on adipose tissue biology, as quantified by gene expression in PCATS, and release of glycerol, free fatty acids, leptin and polychlorinated biphenyls into culture media. EPI stimulated a higher rate of lipolysis than CORT in PCATS from both blubber layers. The combination of CORT and EPI upregulated the expression of adipose triglyceride lipase in inner blubber PCATS and downregulated hormone-sensitive lipase in outer blubber-derived PCATS. Expression of the leptin gene and secretion of the leptin adipokine were both decreased by EPI, while addition of CORT attenuated this effect in inner blubber PCATS only. CORT also increased the expression of the antioxidant enzyme glutathione peroxidase 3 in PCATS from both blubber layers. Polychlorinated biphenyls exhibited selective and limited mobilization from PCATS treated with stress hormones, highlighting the lipophilic properties of these toxic compounds. This study showed that physiological stress can impact several essential functions of marine mammal blubber, such as lipolysis and adipokine production.

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Section: Figuresupporting

confidence: 81%

Section: Figuresupporting

confidence: 79%

Cortisol and epinephrine alter the adipose functions and the mobilization of PCBs in adipose tissue slices from elephant seal

Pirard,

Khudyakov,

Crocker

et al. 2023

Front. Mar. Sci.

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“…They maintain high rates of lipid oxidation and low rates of protein catabolism for its duration, which can last up to 4 months in breeding adult males (Champagne et al, 2012). Some of the endocrine and molecular mechanisms that regulate fasting metabolism in seals have been identified, including increases in corticosteroid and thyroid hormones, insulin resistance, alteration in adipokine signaling and expression of metabolic enzymes and transporters, and antioxidant defenses (Ensminger et al, 2021;Fowler et al, 2018;Rzucidlo et al, 2021). However, they have not been examined at the systems level in multiple tissues simultaneously.…”

Section: Discussionmentioning

confidence: 99%

“…Many features of NES fasting metabolism have been described, such as high rates of fatty acid oxidation and endogenous glucose production, insulin resistance, and alterations in circulating corticosteroid, thyroid and adipokine hormones that may facilitate lipid catabolism and glucose and protein sparing (Fowler et al, 2018;Martinez et al, 2017;Rzucidlo et al, 2021). Unique features of NES metabolism that distinguish them from humans and laboratory mammals include extremely high fasting metabolic rates, efficient protein sparing despite elevated cortisol levels, low ketoacid production, maintenance of elevated high-density lipoprotein (HDL) levels, and resistance to oxidative stress during fasting (Crocker et al, 2014a;Ensminger et al, 2021;Tift et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Changes in apolipoprotein abundance dominate proteome responses to prolonged fasting in elephant seals

Khudyakov

Holser

Vierra

et al. 2022

Journal of Experimental Biology

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Unlike many animals that reduce activity during fasting, northern elephant seals (NES) undergo prolonged fasting during energy-intensive life-history stages such as reproduction and molting, fueling fasting energy needs by mobilizing fat stores accrued during foraging. NES display several unique metabolic features such as high fasting metabolic rates, elevated blood lipid and high-density lipoprotein (HDL) cholesterol levels, efficient protein sparing and resistance to oxidative stress during fasting. However, the cellular mechanisms that regulate these adaptations are still not fully understood. To examine how metabolic coordination is achieved during prolonged fasting, we profiled changes in blubber, skeletal muscle and plasma proteomes of adult female NES over a 5 week fast associated with molting. We found that while blubber and muscle proteomes were remarkably stable over fasting, over 50 proteins changed in abundance in plasma, including those associated with lipid storage, mobilization, oxidation and transport. Apolipoproteins dominated the blubber, plasma and muscle proteome responses to fasting. APOA4, APOE and APOC3, which are associated with lipogenesis and triglyceride accumulation, decreased, while APOA1, APOA2 and APOM, which are associated with lipid mobilization and HDL function, increased over fasting. Our findings suggest that changes in apolipoprotein composition may underlie the maintenance of high HDL levels and, together with adipokines and hepatokines that facilitate lipid catabolism, may mediate the metabolic transitions between feeding and fasting in NES. Many of these proteins have not been previously studied in this species and provide intriguing hypotheses about metabolic regulation during prolonged fasting in mammals.

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“…In northern elephant seals, the secretion patterns of four adipokines at various stages of life history were scrutinized, and the results suggested that the expression and function of adipose-derived hormones in species that undergo natural significant changes in body fat percentage as part of their life history may differ in some respects from those in humans and model animals 66 . Since dolphins do not have a life history stage characterized by a marked increase or decrease in body fat accumulation observed in the elephant seal, it is unlikely that the same functional changes in adipokines occur in dolphins as in the seal.…”

Section: Limitationsmentioning

confidence: 99%

Comprehensive expression analysis of hormone-like substances in the subcutaneous adipose tissue of the common bottlenose dolphin Tursiops truncatus

Suzuki,

Funasaka,

Yoshimura

et al. 2024

Sci Rep

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Marine mammals possess a specific subcutaneous fat layer called blubber that not only insulates and stores energy but also secretes bioactive substances. However, our understanding of its role as a secretory organ in cetaceans is incomplete. To exhaustively explore the hormone-like substances produced in dolphin subcutaneous adipose tissue, we performed seasonal blubber biopsies from captive female common bottlenose dolphins (Tursiops truncatus; N = 8, n = 32) and analyzed gene expression via transcriptomics. Analysis of 186 hormone-like substances revealed the expression of 58 substances involved in regulating energy metabolism, tissue growth/differentiation, vascular regulation, immunity, and ion/mineral homeostasis. Adiponectin was the most abundantly expressed gene, followed by angiopoietin protein like 4 and insulin-like growth factor 2. To investigate the endocrine/secretory responses of subcutaneous adipose tissue to the surrounding temperature, we subsequently compared the mean expression levels of the genes during the colder and warmer seasons. In the colder season, molecules associated with appetite suppression, vasodilation, and tissue proliferation were relatively highly expressed. In contrast, warmer seasons enhanced the expression of substances involved in tissue remodeling, immunity, metabolism, and vasoconstriction. These findings suggest that dolphin blubber may function as an active secretory organ involved in the regulation of metabolism, appetite, and tissue reorganization in response to changes in the surrounding environment, providing a basis for elucidating the function of hormone-like substances in group-specific evolved subcutaneous adipose tissue.

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Changes in serum adipokines during natural extended fasts in female northern elephant seals

Cited by 4 publications

References 69 publications

Cortisol and epinephrine alter the adipose functions and the mobilization of PCBs in adipose tissue slices from elephant seal

Cortisol and epinephrine alter the adipose functions and the mobilization of PCBs in adipose tissue slices from elephant seal

Changes in apolipoprotein abundance dominate proteome responses to prolonged fasting in elephant seals

Comprehensive expression analysis of hormone-like substances in the subcutaneous adipose tissue of the common bottlenose dolphin Tursiops truncatus

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