adipose tissue; cortisol; elephant seal; epinephrine; leptin; lipolysis; PCB mobilization; precision-cut slices; Oceanography; Global and Planetary Change; Aquatic Science; Water Science and Technology; Environmental Science (miscellaneous); Ocean Engineering
Abstract :
[en] 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.
Research Center/Unit :
CART - Centre Interfacultaire d'Analyse des Résidus en Traces - ULiège
Disciplines :
Chemistry Aquatic sciences & oceanology
Author, co-author :
Pirard, Laura; Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Belgium
Khudyakov, Jane I.; Department of Biological Sciences, University of the Pacific, Stockton, United States
Crocker, Daniel E.; Department of Biology, Sonoma State University, Rohnert Park, United States
Van Hassel, Liesbeth; Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Belgium
Scholl, Georges ; Université de Liège - ULiège > Département de chimie (sciences) > Center for Analytical Research and Technology (CART)
Eppe, Gauthier ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)
Page, Melissa M.; Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Belgium
Rees, Jean-François; Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Belgium
Smith, Donald R.; Microbiology and Environmental Toxicology Department, University of California, Santa Cruz, United States
Debier, Cathy; Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Belgium
Language :
English
Title :
Cortisol and epinephrine alter the adipose functions and the mobilization of PCBs in adipose tissue slices from elephant seal
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. LP is a F.R.I.A. Grant Holder of the FNRS (Fonds de la Recherche Scientifique, Belgium). The scientific mission of LP was also funded by the FNRS. AcknowledgmentsThe author(s) declare financial support was received for the research, authorship, and/or publication of this article. LP is a F.R.I.A. Grant Holder of the FNRS (Fonds de la Recherche Scientifique, Belgium). The scientific mission of LP was also funded by the FNRS.
Andersen C. L. Jensen J. L. Ørntoft T. F. (2004). Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64 (15), 5245–5250. doi: 10.1158/0008-5472.CAN-04-0496
Ball H. C. Londraville R. L. Prokop J. W. George J. C. Suydam R. S. Vinyard C. et al. (2017). Beyond thermoregulation: metabolic function of cetacean blubber in migrating bowhead and beluga whales. J. Comp. Physiol. B: Biochem. Syst. Environ. Physiol. 187 (1), 235–252. doi: 10.1007/s00360-016-1029-6
Beltest (2000). Determination of polychlorinated biphenyls in animal feed, animal fat, egg and egg products, milk products and other foodstuffs (Beltest, Belgium: Beltest - Belac (Belgian Organisation for Accreditation)).
Bełtowski J. (2003). Adiponectin and resistin-new hormones of white adipose tissue. MedSciMonit 9 (2), 55–61.
Best N. J. Bradshaw C. J. A. Hindell M. A. Nichols P. D. (2003). Vertical stratification of fatty acids in the blubber of southern elephant seals (Mirounga leonina): Implications for diet analysis. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 134 (2), 253–263. doi: 10.1016/S1096-4959(02)00252-X
Blair H. B. Merchant N. D. Friedlaender A. S. Wiley D. N. Parks S. E. (2016). Evidence for ship noise impacts on humpback whale foraging behaviour. Biol. Lett. 12 (8), 20160005. doi: 10.1098/rsbl.2016.0005
Bligh E. G. Dyer W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37 (8), 911–917. doi: 10.1139/O59-099
Bourez S. Van den Daelen C. Le Lay S. Poupaert J. Larondelle Y. Thomé J. P. et al. (2013). The dynamics of accumulation of PCBs in cultured adipocytes vary with the cell lipid content and the lipophilicity of the congener. Toxicol. Lett. 216 (1), 40–46. doi: 10.1016/j.toxlet.2012.09.027
Carlini A. R. Márquez M. E. I. Ramdohr S. Bornemann H. Panarello H. O. Daneri G. A. (2001). Postweaning Duration and Body Composition Changes in Southern Elephant Seal (Mirounga leonina) Pups at King George Island. Physiol. Biochem. Zool. 74 (4), 531–540. doi: 10.1086/322168
Caron A. Lee S. Elmquist J. K. Gautron L. (2018). Leptin and brain–adipose crosstalks. Nat. Rev. Neurosci. 19 (3), 153–165. doi: 10.1038/nrn.2018.7
Chakrabarti P. Kandror K. V. (2009). FoxO1 controls insulin-dependent adipose triglyceride lipase (ATGL) expression and lipolysis in adipocytes. J. Biol. Chem. 284 (20), 13296–13300. doi: 10.1074/jbc.C800241200
Champagne C. D. Houser D. S. Costa D. P. Crocker D. E. (2012). The effects of handling and anesthetic agents on the stress response and carbohydrate metabolism in northern elephant seals. PloS One 7 (5), e38442. doi: 10.1371/JOURNAL.PONE.0038442
Champagne C. D. Kellar N. M. Trego M. L. Delehanty B. Boonstra R. Wasser S. K. et al. (2018). Comprehensive endocrine response to acute stress in the bottlenose dolphin from serum, blubber, and feces. Gen. Comp. Endocrinol. 266, 178–193. doi: 10.1016/j.ygcen.2018.05.015
Choe S. S. Huh J. Y. Hwang I. J. Kim J. I. Kim J. B. (2016). Adipose tissue remodeling: Its role in energy metabolism and metabolic disorders. Front. Endocrinol. 7 (4). doi: 10.3389/FENDO.2016.00030/BIBTEX
Clark L. S. Cowan D. F. Pfeiffer D. C. (2006). Morphological changes in the atlantic bottlenose dolphin (Tursiops truncatus) adrenal gland associated with chronic stress. J. Comp. Pathol. 135 (4), 208–216. doi: 10.1016/j.jcpa.2006.07.005
Coelho M. Oliveira T. Fernandes R. (2013). State of the art paper Biochemistry of adipose tissue: an endocrine organ. Arch. Med. Sci. 2 (2), 191–200. doi: 10.5114/aoms.2013.33181
Costantini D. Marasco V. Møller A. P. (2011). A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 181 (4), 447–456. doi: 10.1007/S00360-011-0566-2
Crocker D. E. Champagne C. D. Fowler M. A. Houser D. S. (2014). Adiposity and fat metabolism in lactating and fasting northern elephant seals. Adv. Nutr. 5 (1), 57–64. doi: 10.3945/an.113.004663
Crocker D. E. Khudyakov J. I. Champagne C. D. (2016). Oxidative stress in northern elephant seals: Integration of omics approaches with ecological and experimental studies. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 200, 94–103. doi: 10.1016/J.CBPA.2016.02.011
Dantzer B. Fletcher Q. E. Boonstra R. Sheriff M. J. (2014). Measures of physiological stress: A transparent or opaque window into the status, management and conservation of species? Conserv. Physiol. 2, 1. doi: 10.1093/conphys/cou023
Debier C. Crocker D. E. Houser D. S. Vanden Berghe M. Fowler M. Mignolet E. et al. (2012). Differential changes of fat-soluble vitamins and pollutants during lactation in northern elephant seal mother-pup pairs. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 162 (4), 323–330. doi: 10.1016/J.CBPA.2012.04.001
Debier C. Pirard L. Verhaegen M. Rzucidlo C. Tinant G. Dewulf C. et al. (2020). In vitro lipolysis and leptin production of elephant seal blubber using precision-cut adipose tissue slices. Front. Physiol. 11. doi: 10.3389/fphys.2020.615784
Debier C. Pomeroy P. P. Dupont C. Joiris C. Comblin V. Le Boulengé E. et al. (2003). Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar. Ecol. Prog. Ser. 247, 237–248. doi: 10.3354/meps247237
Deck C. A. Honeycutt J. L. Cheung E. Reynolds H. M. Borski R. J. (2017). Assessing the functional role of leptin in energy homeostasis and the stress response in vertebrates. Front. Endocrinol. 8. doi: 10.3389/fendo.2017.00063
de Oliveira C. Iwanaga-Carvalho C. Mota J. F. Oyama L. M. Ribeiro E. B. Oller Do Nascimento C. M. (2011). Effects of adrenal hormones on the expression of adiponectin and adiponectin receptors in adipose tissue, muscle and liver. Steroids. 76 (12), 1260–1267. doi: 10.1016/j.steroids.2011.06.004
Deyarmin J. S. McCormley M. C. Champagne C. D. Stephan A. P. Busqueta L. P. Crocker D. E. et al. (2019). Blubber transcriptome responses to repeated ACTH administration in a marine mammal. Sci. Rep. 9 (1), 2718. doi: 10.1038/s41598-019-39089-2
Duncan R. E. Ahmadian M. Jaworski K. Sarkadi-Nagy E. Sul H. S. (2007). Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 27, 79–101. doi: 10.1146/annurev.nutr.27.061406.093734
Elenkov I. J. Webster E. L. Torpy D. J. Chrousos G. P. (1999). Stress, corticotropin-releasing hormone, glucocorticoids, and the immune/inflammatory response: acute and chronic effects. Ann. N. Y. Acad. Sci. 876 (1), 1–13. doi: 10.1111/J.1749-6632.1999.TB07618.X
Erbe C. Marley S. A. Schoeman R. P. Smith J. N. Trigg L. E. Embling C. B. (2019). The effects of ship noise on marine mammals—A review. Front. Mar. Sci. 6. doi: 10.3389/fmars.2019.00606
Espinoza M. B. Aedo J. E. Zuloaga R. Valenzuela C. Molina A. Valdés J. A. (2017). Cortisol induces reactive oxygen species through a membrane glucocorticoid receptor in rainbow trout myotubes. J. Cell. Biochem. 118 (4), 718–725. doi: 10.1002/JCB.25676
Fair P. A. Becker P. R. (2000). Review of stress in marine mammals. J. Aquat. Ecosyst. Stress Recovery. 7 (4), 335–354. doi: 10.1023/A:1009968113079
Ferrante M. C. Amero P. Santoro A. Monnolo A. Simeoli R. Di Guida F. et al. (2014). Polychlorinated biphenyls (PCB 101, PCB 153 and PCB 180) alter leptin signaling and lipid metabolism in differentiated 3T3-L1 adipocytes. Toxicol. Appl. Pharmacol. 279 (3), 401–408. doi: 10.1016/j.taap.2014.06.016
Fowler M. A. Costa D. P. Crocker D. E. Shen W.-J. Kraemer F. B. (2015). Adipose triglyceride lipase, not hormone-sensitive lipase, is the primary lipolytic enzyme in fasting elephant seals (Mirounga angustirostris). Physiol. Biochem. Zool. 88 (3), 284–294. doi: 10.1086/680079
Fowler M. A. Debier C. Mignolet E. Linard C. Crocker D. E. Costa D. P. (2014). Fatty acid mobilization and comparison to milk fatty acid content in northern elephant seals. J. Comp. Physiol. Part B Biochem. Syst. Environ. Physiol. 184 (1), 125–135. doi: 10.1007/S00360-013-0787-7
Fried S. K. Ricci M. R. Russell C. D. Laferrère B. (2000). Regulation of leptin production in humans. J. Nutr. 130 (12), 3127–3131. doi: 10.1093/jn/130.12.3127s
Frühbeck G. Gómez-Ambrosi J. Muruzábal F. J. Burrell M. A. (2001). The adipocyte: A model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am. J. Physiol. Endocrinol. Metab. 280, E827–E847. doi: 10.1152/ajpendo.2001.280.6.E827
Gaidhu M. P. Anthony N. M. Patel P. Hawke T. J. Ceddia R. B. (2010). Dysregulation of lipolysis and lipid metabolism in visceral and subcutaneous adipocytes by high-fat diet: role of ATGL, HSL, and AMPK. Am. J. Physiol. Cell. Physiol. 298, C961–C971. doi: 10.1152/ajpcell.00547.2009
Gaidhu M. P. Fediuc S. Anthony N. M. So M. Mirpourian M. Perry R. L. S. et al. (2009). Prolonged AICAR-induced AMP-kinase activation promotes energy dissipation in white adipocytes: novel mechanisms integrating HSL and ATGL. J. Lipid Res. 50 (4), 704. doi: 10.1194/JLR.M800480-JLR200
Gregoraszczuk E. L. Ptak A. (2013). Endocrine-disrupting chemicals: some actions of POPs on female reproduction. Int. J. Endocrinol. doi: 10.1155/2013/828532
Hing S. Narayan E. J. Thompson R. C. A. Godfrey S. S. (2016). The relationship between physiological stress and wildlife disease: consequences for health and conservation. Wildl. Res. 43, 51–60. doi: 10.1071/WR15183
Hua C. Geng Y. Niu L. Chen Q. Cai L. Tao S. et al. (2018). Stimulating lipolysis in subcutaneous adipose tissues by chronic dexamethasone administration in goats. Livest. Sci. 214, 62–67. doi: 10.1016/j.livsci.2018.05.020
Jenssen B. M. (2006). Endocrine-disrupting chemicals and climate change: A worst-case combination for arctic marine mammals and seabirds? Environ. Health Perspect. 114 (SUPPL.1), 76–80. doi: 10.1289/EHP.8057
Kashiwabara L. Pirard L. Debier C. Crocker D. E. Khudyakov J. I. (2023). Effects of cortisol, epinephrine, and bisphenol contaminants on the transcriptional landscape of marine mammal blubber. Am. J. Physiol. Regul. Integr. Comp. Physiol. 325 (5), 504–522. doi: 10.1152/ajpregu.00165.2023
Kelesidis T. Kelesidis I. Chou S. Mantzoros C. S. (2010). Narrative review: the role of leptin in human physiology: emerging clinical applications. Ann. Intern. Med. 152 (2), 93. doi: 10.1059/0003-4819-152-2-201001190-00008
Kershaw J. L. Botting C. H. Brownlow A. Hall A. J. (2018).). Not just fat: investigating the proteome of cetacean blubber tissue. Conserv. Physiol. 6 (1). doi: 10.1093/CONPHYS/COY003
Kershaw J. L. Sherrill M. Davison N. J. Brownlow A. Hall A. J. (2017). Evaluating morphometric and metabolic markers of body condition in a small cetacean, the harbor porpoise (Phocoena phocoena). Ecol. Evol. 7 (10), 3494–3506. doi: 10.1002/ece3.2891
Khudyakov J. I. Abdollahi E. Ngo A. Sandhu G. Stephan A. Costa D. P. et al. (2019). Expression of obesity-related adipokine genes during fasting in a naturally obese marine mammal. Am. J. Physiol. Regul. Integr. Comp. Physiol. 317 (4), R521–R529. doi: 10.1152/ajpregu.00182.2019
Khudyakov J. I. Allen K. N. Crocker D. E. Trost N. S. Roberts A. H. Pirard L. et al. (2022). Comprehensive molecular and morphological resolution of blubber stratification in a deep-diving, fasting-adapted seal. Front. Physiol. 13. doi: 10.3389/FPHYS.2022.1057721/BIBTEX
Khudyakov J. I. Champagne C. D. Meneghetti L. M. Crocker D. E. (2017). Blubber transcriptome response to acute stress axis activation involves transient changes in adipogenesis and lipolysis in a fasting-adapted marine mammal. Sci. Rep. 7 (42110). doi: 10.1038/SREP42110
Kim J. M. Choi J. S. Kim Y. H. Jin S. H. Lim S. Jang H. J. et al. (2013). An activator of the cAMP/PKA/CREB pathway promotes osteogenesis from human mesenchymal stem cells. J. Cell. Physiol. 228 (3), 617–626. doi: 10.1002/JCP.24171
Klemm D. J. Leitner J. W. Watson P. Nesterova A. Reusch J. E. B. Goalstone M. L. et al. (2001). Insulin-induced Adipocyte Differentiation: activation of creb rescues adipogenesis from the arrest caused by inhibition of prenylation. J. Biol. Chem. 276 (30), 28430–28435. doi: 10.1074/JBC.M103382200
Lafontan M. Berlan M. (1993). Fat cell adrenergic receptors and the control of white and brown fat cell function. J. Lipid Res. 34, 1057–1091. doi: 10.1016/S0022-2275(20)37695-1
Lafontan M. Langin D. (2009). Lipolysis and lipid mobilization in human adipose tissue. Prog. Lipid Res. 48 (5), 275–297. doi: 10.1016/j.plipres.2009.05.001
Le Boeuf B. J. Crocker D. E. Costa D. P. Blackwell S. B. Webb P. M. Houser D. S. (2000). Foraging ecology of northern elephant seals. Ecol. Monogr. 70 (3), 353. doi: 10.2307/2657207
Louis C. Covaci A. Crocker D. E. Debier C. (2016). Lipophilicity of PCBs and fatty acids determines their mobilisation from blubber of weaned northern elephant seal pups. Sci. Total Environ. 541, 599–602. doi: 10.1016/J.SCITOTENV.2015.09.094
Louis C. Dirtu A. C. Stas M. Guiot Y. Malarvannan G. Das K. et al. (2014a). Mobilisation of lipophilic pollutants from blubber in northern elephant seal pups (Mirounga angustirostris) during the post-weaning fast. Environ. Res. 132, 438–448. doi: 10.1016/J.ENVRES.2014.04.016
Louis C. Perdaens L. Suciu S. Tavoni S. K. Crocker D. E. Debier C. (2015). Mobilisation of blubber fatty acids of northern elephant seal pups (Mirounga angustirostris) during the post-weaning fast. Comp. Biochem. Physiol. Part A: Mol. Integr. Physiol. 183, 78–86. doi: 10.1016/J.CBPA.2015.01.008
Louis C. Tinant G. Mignolet E. Thomé J. P. Debier C. (2014b). PCB-153 shows different dynamics of mobilisation from differentiated rat adipocytes during lipolysis in comparison with PCB-28 and PCB-118. PloS One 9 (9), e106495. doi: 10.1371/journal.pone.0106495
Louis C. Van den Daelen C. Tinant G. Bourez S. Thomé J. P. Donnay I. et al. (2014c). Efficient in vitro adipocyte model of long-term lipolysis: A tool to study the behavior of lipophilic compounds. In Vitro Cell. Dev. Biol. –Animal 50 (6), 507–518. doi: 10.1007/s11626-014-9733-6
Mashburn K. L. Atkinson S. (2008). Variability in leptin and adrenal response in juvenile Steller sea lions (Eumetopias jubatus) to adrenocorticotropic hormone (ACTH) in different seasons. Gen. Comp. Endocrinol. 155 (2), 352–358. doi: 10.1016/J.YGCEN.2007.05.030
McTernan P. G. Kusminski C. M. Kumar S. (2006). Resistin. Curr. Opin. Lipidol. 17 (2), 170–175. doi: 10.1097/01.MOL.0000217899.59820.9A
Mikkelsen L. Johnson M. Wisniewska D. M. van Neer A. Siebert U. Madsen P. T. et al. (2019). Long-term sound and movement recording tags to study natural behavior and reaction to ship noise of seals. Ecol. Evol. 9 (5), 2588–2601. doi: 10.1002/ece3.4923
Moriceau M. A. Cano-Sancho G. Kim M. J. Coumoul X. Emond C. Arrebola J. P. et al. (2023). Partitioning of persistent organic pollutants between adipose tissue and serum in human studies. Toxics. 11 (1), 41. doi: 10.3390/TOXICS11010041/S1
Noren D. P. Crocker D. E. Williams T. M. Costa D. P. (2003). Energy reserve utilization in northern elephant seal (Mirounga angustirostris) pups during the postweaning fast: size does matter. J. Comp. Physiol. B. Biochem. Syst. Environ. Physiol. 173 (5), 443–454. doi: 10.1007/S00360-003-0353-9
Nowacek D. P. Thorne L. H. Johnston D. W. Tyack P. L. (2007). Responses of cetaceans to anthropogenic noise. Mamm. Rev. 37 (2), 81–115. doi: 10.1111/j.1365-2907.2007.00104.x
Ortiz R. M. Wade C. E. Ortiz C. L. (2001). Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am. J. Physiol. – Regul. Integr. Comp. Physiol. 280, R790–R795. doi: 10.1152/AJPREGU.2001.280.3.R790
Peckett A. J. Wright D. C. Riddell M. C. (2011). The effects of glucocorticoids on adipose tissue lipid metabolism. Metab. Clin. Exp. 60 (11), 1500–1510. doi: 10.1016/J.METABOL.2011.06.012
Peterson S. H. Ackerman J. T. Holser R. R. McDonald B. I. Costa D. P. Crocker D. E. (2023). Mercury bioaccumulation and cortisol interact to influence endocrine and immune biomarkers in a free-ranging marine mammal. Environ. Sci. Technol. 57 (14), 5678–5692. doi: 10.1021/ACS.EST.2C08974/ASSET/IMAGES/LARGE/ES2C08974_0008.JPEG
Pujade Busqueta L. Crocker D. E. Champagne C. D. McCormley M. C. Deyarmin J. S. Houser D. S. et al. (2020). A blubber gene expression index for evaluating stress in marine mammals. Conserv. Physiol. 8 (1), coaa082. doi: 10.1093/conphys/coaa082
Rolland R. M. McLellan W. A. Moore M. J. Harms C. A. Burgess E. A. Hunt K. E. (2017). Fecal glucocorticoids and anthropogenic injury and mortality in North Atlantic right whales Eubalaena glacialis. Endanger. Species Res. 34, 417–429. doi: 10.3354/esr00866
Rolland R. M. Parks S. E. Hunt K. E. Castellote M. Corkeron P. J. Nowacek D. P. et al. (2012). Evidence that ship noise increases stress in right whales. Proc. R. Soc B: Biol. Sci. 279 (1737), 2363–2368. doi: 10.1098/rspb.2011.2429
Rzucidlo C. L. Sperou E. S. Holser R. R. Khudyakov J. I. Costa D. P. Crocker D. E. (2021). Changes in serum adipokines during natural extended fasts in female northern elephant seals. Gen. Comp. Endocrinol. 308, 113760. doi: 10.1016/J.YGCEN.2021.113760
Schnitzler J. G. Reckendorf A. Pinzone M. Autenrieth M. Tiedemann R. Covaci A. et al. (2019). Supporting evidence for PCB pollution threatening global killer whale population. Aquat. Toxicol. 206, 102–104. doi: 10.1016/j.aquatox.2018.11.008
Stimson R. H. Anderson A. J. Ramage L. E. Macfarlane D. P. de Beaux A. C. Mole D. J. et al. (2017). Acute physiological effects of glucocorticoids on fuel metabolism in humans are permissive but not direct. Diabetes Obes. Metab. 19 (6), 883–891. doi: 10.1111/dom.12899
Strandberg U. Käkelä A. Lydersen C. Kovacs K. M. Grahl-Nielsen O. Hyvärinen H. et al. (2008). Stratification, composition, and function of marine mammal blubber: The ecology of fatty acids in marine mammals. Physiol. Biochem. Zool. 81 (4), 473–485. doi: 10.1086/589108
Than A. Ye F. Xue R. Ong J. W. Poh C. L. Chen P. (2011). The crosstalks between adipokines and catecholamines. Mol. Cell. Endocrinol. 332 (1–2), 261–270. doi: 10.1016/j.mce.2010.11.002
Timmermans S. Souffriau J. Libert C. (2019). A general introduction to glucocorticoid biology. Front. Immunol. 10. doi: 10.3389/fimmu.2019.0154
Trumble S. J. Norman S. A. Crain D. D. Mansouri F. Winfield Z. C. Sabin R. et al. (2018). Baleen whale cortisol levels reveal a physiological response to 20th century whaling. Nat. Commun. 9, 4587. doi: 10.1038/s41467-018-07044-w
Tsubai T. Noda Y. Ito K. Nakao M. Seino Y. Oiso Y. et al. (2016). Insulin elevates leptin secretion and mRNA levels via cyclic AMP in 3T3-L1 adipocytes deprived of glucose. Heliyon 3, e00194. doi: 10.1016/J.HELIYON.2016.E00194
Vanden Berghe M. Mat A. Arriola A. Polain S. Stekke V. Thomé J. P. et al. (2010). Relationships between vitamin A and PCBs in grey seal mothers and pups during lactation. Environ. pollut. 158 (5), 1570–1575. doi: 10.1016/J.ENVPOL.2009.12.012
Vanden Berghe M. Weijs L. Habran S. Das K. Bugli C. Rees J. F. et al. (2012). Selective transfer of persistent organic pollutants and their metabolites in grey seals during lactation. Environ. Int. 46, 6–15. doi: 10.1016/J.ENVINT.2012.04.011
Vázquez-Medina J. P. Crocker D. E. Forman H. J. Ortiz R. M. (2010). Prolonged fasting does not increase oxidative damage or inflammation in postweaned northern elephant seal pups. J. Exp. Biol. 213, 2524–2530. doi: 10.1242/JEB.041335
Vázquez-Medina J. P. Zenteno-Savín T. Forman H. J. Crocker D. E. Ortiz R. M. (2011). Prolonged fasting increases glutathione biosynthesis in postweaned northern elephant seals. J. Exp. Biol. 214 (8), 1294. doi: 10.1242/JEB.054320
Viscarra J. A. Champagne C. D. Crocker D. E. Ortiz R. M. (2011a). 5′AMP-activated protein kinase activity is increased in adipose tissue of northern elephant seal pups during prolonged fasting-induced insulin resistance. J. Endocrinol. 209 (3), 317. doi: 10.1530/JOE-11-0017
Viscarra J. A. Ortiz R. M. (2013). Cellular mechanisms regulating fuel metabolism in mammals: role of adipose tissue and lipids during prolonged food deprivation. Metab. Clin. Exp. 62 (7), 889. doi: 10.1016/J.METABOL.2012.12.014
Viscarra J. A. Vázquez-Medina J. P. Crocker D. E. Ortiz R. M. (2011b). Glut4 is upregulated despite decreased insulin signaling during prolonged fasting in northern elephant seal pups. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 (1), 150–154. doi: 10.1152/ajpregu.00478.2010
Viscarra J. A. Vázquez-Medina J. P. Rodriguez R. Champagne C. D. Adams S. H. Crocker D. E. et al. (2012). Decreased expression of adipose CD36 and FATP1 are associated with increased plasma non-esterified fatty acids during prolonged fasting in northern elephant seal pups (Mirounga angustirostris). J. Exp. Biol. 215 (14), 2455–2464. doi: 10.1242/jeb.069070
Xu C. He J. Jiang H. Zu L. Zhai W. Pu S. et al. (2009). Direct effect of glucocorticoids on lipolysis in adipocytes. Mol. Endocrinol. 23 (8), 1161–1170. doi: 10.1210/me.2008-0464
Zhang Y. Zhou T. Feng S. Wang W. Liu H. Wang P. et al. (2021). The chronic effect of cortisol on orchestrating cerebral blood flow and brain functional connectivity: evidence from Cushing’s disease. Metab. Clin. Exp. 115, 154432. doi: 10.1016/J.METABOL.2020.154432
