Horm Metab Res 2024; 56(01): 65-77
DOI: 10.1055/a-2201-6641
Review

Sensitivity of the Neuroendocrine Stress Axis in Metabolic Diseases

Diana Cozma
1   Department of Medicine III, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
,
Panagiota Siatra
1   Department of Medicine III, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
,
Stefan R. Bornstein
1   Department of Medicine III, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
2   School of Cardiovascular and Metabolic Medicine and Sciences, Faculty of Life Sciences & Medicine, King’s College London, London, UK
3   Department of Endocrinology, Diabetology and Clinical Nutrition, University Hospital Zurich (USZ) and University of Zurich (UZH), Zurich, Switzerland
,
Charlotte Steenblock
1   Department of Medicine III, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
› Author Affiliations
Funding Information Deutsche Forschungsgemeinschaft (CRC/Transregio 205 “The Adrenal: Central Relay in Health and Disease”, project number 314061271; IRTG 2251 "Immunological and cellular strategies in metabolic disease", project number 288034826).

Abstract

Metabolic diseases are prevalent in modern society and have reached pandemic proportions. Metabolic diseases have systemic effects on the body and can lead to changes in the neuroendocrine stress axis, the critical regulator of the body’s stress response. These changes may be attributed to rising insulin levels and the release of adipokines and inflammatory cytokines by adipose tissue, which affect hormone production by the neuroendocrine stress axis. Chronic stress due to inflammation may exacerbate these effects. The increased sensitivity of the neuroendocrine stress axis may be responsible for the development of metabolic syndrome, providing a possible explanation for the high prevalence of severe comorbidities such as heart disease and stroke associated with metabolic disease. In this review, we address current knowledge of the neuroendocrine stress axis in response to metabolic disease and discuss its role in developing metabolic syndrome.



Publication History

Received: 06 June 2023

Accepted after revision: 18 October 2023

Article published online:
03 January 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Bose M, Oliván B, Laferrère B. Stress and obesity: the role of the hypothalamic-pituitary-adrenal axis in metabolic disease. Curr Opin Endocrinol Diabetes Obes 2009; 16: 340-346
  • 2 Ylli D, Sidhu S, Parikh T. et al. Endotext. Endocrine changes in obesity. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc.;. 2000 www.endotext.org
  • 3 Holzapfel C, Waldenberger M, Lorkowski S. et al. Genetics and epigenetics in personalized nutrition: evidence, expectations, and experiences. Mol Nutr Food Res 2022; 66: e2200077
  • 4 Berger I, Werdermann M, Bornstein SR. et al. The adrenal gland in stress – adaptation on a cellular level. J Steroid Biochem Mol Biol 2019; 190: 198-206
  • 5 Marcus Y, Shefer G, Stern N. Adipose tissue renin-angiotensin-aldosterone system (RAAS) and progression of insulin resistance. Mol Cell Endocrinol 2013; 378: 1-14
  • 6 Gupte M, Boustany-Kari CM, Bharadwaj K. et al. ACE2 is expressed in mouse adipocytes and regulated by a high-fat diet. Am J Physiol Regul Integr Comp Physiol 2008; 295: R781-R788
  • 7 Bechmann N, Berger I, Bornstein SR. et al. Adrenal medulla development and medullary-cortical interactions. Mol Cell Endocrinol 2021; 528: 111258
  • 8 Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med 1995; 332: 1351-1362
  • 9 Wang T, He C. Pro-inflammatory cytokines: The link between obesity and osteoarthritis. Cytokine Growth Factor Rev 2018; 44: 38-50
  • 10 Al-Hussaniy HA, Alburghaif AH, Naji MA. Leptin hormone and its effectiveness in reproduction, metabolism, immunity, diabetes, hopes and ambitions. J Med Life 2021; 14: 600-605
  • 11 de Git KCG, Peterse C, Beerens S. et al. Is leptin resistance the cause or the consequence of diet-induced obesity?. Int J Obes (Lond) 2018; 42: 1445-1457
  • 12 Stephens TW, Basinski M, Bristow PK. et al. The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature 1995; 377: 530-532
  • 13 McKibbin PE, Cotton SJ, McMillan S. et al. Altered neuropeptide Y concentrations in specific hypothalamic regions of obese (fa/fa) Zucker rats. Possible relationship to obesity and neuroendocrine disturbances. Diabetes 1991; 40: 1423-1429
  • 14 White DW, Tartaglia LA. Leptin and OB-R: body weight regulation by a cytokine receptor. Cytokine Growth Factor Rev 1996; 7: 303-309
  • 15 Proulx K, Clavel S, Nault G. et al. High neonatal leptin exposure enhances brain GR expression and feedback efficacy on the adrenocortical axis of developing rats. Endocrinology 2001; 142: 4607-4616
  • 16 Pralong FP, Roduit R, Waeber G. Leptin inhibits directly glucocorticoid secretion by normal human and rat adrenal gland. Endocrinology 1998; 139(10): 4264–4268. doi: 10.1210/endo.139.10.6254
  • 17 Huby A-C, Antonova G, Groenendyk J. et al. Adipocyte-derived hormone leptin is a direct regulator of aldosterone secretion, which promotes endothelial dysfunction and cardiac fibrosis. Circulation 2015; 132: 2134-2145
  • 18 Cabandugama PK, Gardner MJ, Sowers JR. The renin angiotensin aldosterone system in obesity and hypertension: roles in the cardiorenal metabolic syndrome. Med Clin North Am 2017; 101: 129-137
  • 19 Kantartzis K, Fritsche A, Tschritter O. et al. The association between plasma adiponectin and insulin sensitivity in humans depends on obesity. Obes Res 2005; 13: 1683-1691
  • 20 Kadowaki T, Yamauchi T, Kubota N. et al. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest 2006; 116: 1784-1792
  • 21 Gavrila A, Peng C-K, Chan JL. et al. Diurnal and ultradian dynamics of serum adiponectin in healthy men: comparison with leptin, circulating soluble leptin receptor, and cortisol patterns. J Clin Endocrinol Metab 2003; 88: 2838-2843
  • 22 Li P, Sun F, Cao H-M. et al. Expression of adiponectin receptors in mouse adrenal glands and the adrenocortical Y-1 cell line: Adiponectin regulates steroidogenesis. Biochem Biophys Res Commun 2009; 390: 1208-1213
  • 23 Duclos M, Gatta B, Corcuff JB. et al. Fat distribution in obese women is associated with subtle alterations of the hypothalamic-pituitary-adrenal axis activity and sensitivity to glucocorticoids. Clin Endocrinol 2001; 55: 447-454
  • 24 Ehrhart-Bornstein M, Lamounier-Zepter V, Schraven A. et al. Human adipocytes secrete mineralocorticoid-releasing factors. Proc Natl Acad Sci U S A 2003; 100: 14211-14216
  • 25 Schinner S, Willenberg HS, Krause D. et al. Adipocyte-derived products induce the transcription of the StAR promoter and stimulate aldosterone and cortisol secretion from adrenocortical cells through the Wnt-signaling pathway. Int J Obes (Lond) 2007; 31: 864-870
  • 26 Janssen JAMJL. New insights into the role of insulin and hypothalamic-pituitary-adrenal (HPA) axis in the metabolic syndrome. Int J Mol Sci 2022; 23: 8178
  • 27 Kim EM, Grace MK, Welch CC. et al. STZ-induced diabetes decreases and insulin normalizes POMC mRNA in arcuate nucleus and pituitary in rats. Am J Physiol 1999; 276: R1320-R1326
  • 28 Werdermann M, Berger I, Scriba LD. et al. Insulin and obesity transform hypothalamic-pituitary-adrenal axis stemness and function in a hyperactive state. Mol Metab 2021; 43: 101112
  • 29 Wang X, Li H. Chronic high-fat diet induces overeating and impairs synaptic transmission in feeding-related brain regions. Front Mol Neurosci 2022; 15: 1019446
  • 30 Waise TMZ, Toshinai K, Naznin F. et al. One-day high-fat diet induces inflammation in the nodose ganglion and hypothalamus of mice. Biochem Biophys Res Commun 2015; 464: 1157-1162
  • 31 Thaler JP, Yi C-X, Schur EA. et al. Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest 2012; 122: 153-162
  • 32 Papargyri P, Zapanti E, Salakos N. et al. Links between HPA axis and adipokines: clinical implications in paradigms of stress-related disorders. Expert Rev Endocrinol Metab 2018; 13: 317-332
  • 33 Kern PA, Ranganathan S, Li C. et al. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 2001; 280: E745-E751
  • 34 Faist E, Meakins JL, Schildberg FW. Host defense dysfunction in trauma, shock, and sepsis. Mechanisms and therapeutic approaches. Berlin, New York: Springer-Verlag; 1993
  • 35 Bernardini R, Kamilaris TC, Calogero AE. et al. Interactions between tumor necrosis factor-alpha, hypothalamic corticotropin-releasing hormone, and adrenocorticotropin secretion in the rat. Endocrinology 1990; 126: 2876-2881
  • 36 Milanski M, Degasperi G, Coope A. et al. Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: implications for the pathogenesis of obesity. J Neurosci 2009; 29: 359-370
  • 37 Mendes NF, Kim Y-B, Velloso LA. et al. Hypothalamic microglial activation in obesity: a mini-review. Front Neurosci 2018; 12: 846
  • 38 Tan BL, Norhaizan ME. Effect of high-fat diets on oxidative stress, cellular inflammatory response and cognitive function. Nutrients 2019; 11: 2579
  • 39 Benani A, Troy S, Carmona MC. et al. Role for mitochondrial reactive oxygen species in brain lipid sensing: redox regulation of food intake. Diabetes 2007; 56: 152-160
  • 40 Valdearcos M, Xu AW, Koliwad SK. Hypothalamic inflammation in the control of metabolic function. Annu Rev Physiol 2015; 77: 131-160
  • 41 Min L. Functional hypercorticolism, visceral obesity, and metabolic syndrome. Endocr Pract 2016; 22: 506-508
  • 42 Tartaglia LA. The leptin receptor. J Biol Chem 1997; 272: 6093-6096
  • 43 McDonald R, Kuhn K, Nguyen TB. et al. A randomized clinical trial demonstrating cell type specific effects of hyperlipidemia and hyperinsulinemia on pituitary function. PLoS One 2022; 17: e0268323
  • 44 Salvatori R. Growth hormone deficiency in patients with obesity. Endocrine 2015; 49: 304-306
  • 45 Hjelholt A, Høgild M, Bak AM. et al. Growth hormone and obesity. Endocrinol Metab Clin North America 2020; 49: 239-250
  • 46 Kopelman PG, Noonan K, Goulton R. et al. Impaired growth hormone response to growth hormone releasing factor and insulin-hypoglycaemia in obesity. Clin Endocrinol 1985; 23: 87-94
  • 47 Chiodini I, Adda G, Scillitani A. et al. Cortisol secretion in patients with type 2 diabetes: relationship with chronic complications. Diabetes Care 2007; 30: 83-88
  • 48 Fehrenbach U, Jadan A, Auer TA. et al. Obesity and pituitary gland volume – a correlation study using three-dimensional magnetic resonance imaging. Neuroradiol J 2020; 33: 400-409
  • 49 Bestetti GE, Abramo F, Guillaume-Gentil C. et al. Changes in the hypothalamo-pituitary-adrenal axis of genetically obese fa/fa rats: a structural, immunocytochemical, and morphometrical study. Endocrinology 1990; 126: 1880-1887
  • 50 Lochner RH, Delfin L, Nezami BG. et al. Severe obesity associated with pituitary corticotroph hyperplasia and neoplasia. Endocr Pract 2023; 29: 471-477
  • 51 Rucker P, Ikuta T. Pituitary gland functional connectivity and BMI. Front Neurosci 2019; 13: 120
  • 52 Perogamvros I, Ray DW, Trainer PJ. Regulation of cortisol bioavailability–effects on hormone measurement and action. Nat Rev Endocrinol 2012; 8: 717-727
  • 53 Rosmond. Stress-related cortisol secretion in men: Relationships with abdominal obesity and en-docrine metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab 1998; 83: 1853
  • 54 Rosmond R, Radulovic V, Holm G. A brief update of glucocorticoid receptor variants and obesity risk. Ann New York Acad Sci 2006; 1083: 153-164
  • 55 Prpić-Križevac I, Canecki-Varžić S, Bilić-Ćurčić I. Hyperactivity of the hypothalamic-pituitary-adrenal axis in patients with type 2 diabetes and relations with insulin resistance and chronic complications. Wien Klin Wochenschr 2012; 124: 403-411
  • 56 Champaneri S, Xu X, Carnethon MR. et al. Diurnal salivary cortisol is associated with body mass index and waist circumference: the Multiethnic Study of Atherosclerosis. Obesity (Silver Spring) 2013; 21: E56-E63
  • 57 Zoulikha M, Nacira Z, Therese G-S. et al. Effect of two hypercaloric diets on the hormonal and metabolic profile of the adrenal gland. Horm Mol Biol Clin Investig 2021; 42: 373-382
  • 58 Morgan SA, McCabe EL, Gathercole LL. et al. 11β-HSD1 is the major regulator of the tissue-specific effects of circulating glucocorticoid excess. Proc Natl Acad Sci U S A 2014; 111: E2482-E2491
  • 59 Masuzaki H, Paterson J, Shinyama H. et al. A transgenic model of visceral obesity and the metabolic syndrome. Science 2001; 294: 2166-2170
  • 60 Kupczyk D, Bilski R, Kozakiewicz M. et al. 11β-HSD as a new target in pharmacotherapy of metabolic diseases. Int J Mol Sci 2022; 23: 8984
  • 61 Liu F, Chen Y, Xie W. et al. Obesity might persistently increase adrenal gland volume: a preliminary study. Obes Surg 2020; 30: 3503-3507
  • 62 Carsin-Vu A, Oubaya N, Mulé S. et al. MDCT linear and volumetric analysis of adrenal glands: normative data and multiparametric assessment. Eur Radiol 2016; 26: 2494-2501
  • 63 Askani E, Rospleszcz S, Lorbeer R. et al. Association of MRI-based adrenal gland volume and impaired glucose metabolism in a population-based cohort study. Diabetes Metab Res Rev 2022; 38: e3528
  • 64 Muscogiuri G, De Martino MC, Negri M. et al. Adrenal mass: insight into pathogenesis and a common link with insulin resistance. Endocrinology 2017; 158: 1527-1532
  • 65 Erdal M, Altunkaynak Z, Kocaman A. et al. Investigation of the relationship between HMGB1 and obesity in the adrenal gland. Med Rec 2022; 242-250
  • 66 Medjerab M, Abdelali M, Khalkhal A. et al. Adrenal cortex disorders in a new model of obesity, Gerbillus gerbillus, exposed to a high carbohydrate diet. C R Biol 2019; 342: 35-44
  • 67 Swierczynska MM, Mateska I, Peitzsch M. et al. Changes in morphology and function of adrenal cortex in mice fed a high-fat diet. Int J Obes 2015; 39: 321-330
  • 68 Kinyua AW, Doan KV, Yang DJ. et al. Insulin regulates adrenal steroidogenesis by stabilizing SF-1 activity. Sci Rep 2018; 8: 5025
  • 69 Bjornsdottir HH, Rawshani A, Rawshani A. et al. A national observation study of cancer incidence and mortality risks in type 2 diabetes compared to the background population over time. Sci Rep 2020; 10: 17376
  • 70 Ling S, Brown K, Miksza JK. et al. Association of type 2 diabetes with cancer: a meta-analysis with bias analysis for unmeasured confounding in 151 cohorts comprising 32 million people. Diabetes Care 2020; 43: 2313-2322
  • 71 Sciacca L, Vigneri R, Tumminia A. et al. Clinical and molecular mechanisms favoring cancer initiation and progression in diabetic patients. Nutr Metab Cardiovasc Dis 2013; 23: 808-815
  • 72 Belfiore A, Malaguarnera R, Vella V. et al. Insulin receptor isoforms in physiology and disease: an updated view. Endocr Rev 2017; 38: 379-431
  • 73 Murphy VE, Smith R, Giles WB. et al. Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocr Rev 2006; 27: 141-169
  • 74 van der Veeken J, Oliveira S, Schiffelers RM. et al. Crosstalk between epidermal growth factor receptor- and insulin-like growth factor-1 receptor signaling: implications for cancer therapy. Curr Cancer Drug Targets 2009; 9: 748-760
  • 75 Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat Rev Cancer 2012; 12: 159-169
  • 76 Shahid RK, Ahmed S, Le D. et al. Diabetes and cancer: risk, challenges, management and outcomes. Cancers (Basel) 2021; 13: 5735
  • 77 Bornstein SR, Steenblock C, Chrousos GP. et al. Stress-inducible-stem cells: a new view on endocrine, metabolic and mental disease?. Mol Psychiatry 2019; 24: 2-9
  • 78 Huang L, Yu X, Keim S. et al. Maternal prepregnancy obesity and child neurodevelopment in the Collaborative Perinatal Project. Int J Epidemiol 2014; 43: 783-792
  • 79 Hinkle SN, Schieve LA, Stein AD. et al. Associations between maternal prepregnancy body mass index and child neurodevelopment at 2 years of age. In J Obes 2012; 36: 1312-1319
  • 80 Sun P, Knezovic A, Parlak M. et al. Long-term effects of intracerebroventricular streptozotocin treatment on adult neurogenesis in the rat hippocampus. Curr Alzheimer Res 2015; 12: 772-784
  • 81 Sun P, Ortega G, Tan Y. et al. Streptozotocin impairs proliferation and differentiation of adult hippocampal neural stem cells in vitro-correlation with alterations in the expression of proteins associated with the insulin system. Front Aging Neurosci 2018; 10: 145
  • 82 Chirivella L, Kirstein M, Ferrón SR. et al. Cyclin-dependent kinase 4 regulates adult neural stem cell proliferation and differentiation in response to insulin. Stem Cells 2017; 35: 2403-2416
  • 83 Soukup J, Česák T, Hornychová H. et al. Stem cell transcription factor Sox2 is expressed in a subset of folliculo-stellate cells of growth hormone-producing pituitary neuroendocrine tumours and its expression shows no association with tumour size or IGF1 levels: a clinicopathological study of 109 Cases. Endocr Pathol 2020; 31: 337-347
  • 84 Godoy-Matos AF, Vieira AR, Moreira RO. et al. The potential role of increased adrenal volume in the pathophysiology of obesity-related type 2 diabetes. J Endocrinol Invest 2006; 29: 159-163
  • 85 Neirijnck Y, Calvel P, Kilcoyne KR. et al. Insulin and IGF1 receptors are essential for the development and steroidogenic function of adult Leydig cells. FASEB J 2018; 32: 3321-3335
  • 86 Dringenberg T, Schwitalla M, Haase M. et al. Control of CYP11B2/CYP11B1 expression ratio and consequences for the zonation of the adrenal cortex. Horm Metab Res 2013; 45: 81-85
  • 87 Altieri B, Tirabassi G, Della Casa S. et al. Adrenocortical tumors and insulin resistance: What is the first step?. Int J Cancer 2016; 138: 2785-2794
  • 88 Haase M, Thiel A, Scholl UI. et al. Subcellular localization of fibroblast growth factor receptor type 2 and correlation with CTNNB1 genotype in adrenocortical carcinoma. BMC Res Notes 2020; 13: 282
  • 89 Angelousi A, Kyriakopoulos G, Nasiri-Ansari N. et al. The role of epithelial growth factors and insulin growth factors in the adrenal neoplasms. Ann Transl Med 2018; 6: 253
  • 90 Ribeiro TC, Latronico AC. Insulin-like growth factor system on adrenocortical tumorigenesis. Mol Cell Endocrinol 2012; 351: 96-100
  • 91 Almeida MQ, Fragoso MCVB, Lotfi CFP. et al. Expression of insulin-like growth factor-II and its receptor in pediatric and adult adrenocortical tumors. J Clin Endocrnol Metab 2008; 93: 3524-3531
  • 92 Altieri B, Colao A, Faggiano A. The role of insulin-like growth factor system in the adrenocortical tumors. Minerva Endocrinol 2019; 44: 43-57
  • 93 King P, Paul A, Laufer E. Shh signaling regulates adrenocortical development and identifies progenitors of steroidogenic lineages. Proc Natl Acad Sci U S A 2009; 106: 21185-21190
  • 94 Grabek A, Dolfi B, Klein B. et al. The adult adrenal cortex undergoes rapid tissue renewal in a sex-specific manner. Cell Stem Cell 2019; 25: 290-296.e2
  • 95 Finco I, Lerario AM, Hammer GD. Sonic hedgehog and WNT signaling promote adrenal gland regeneration in male mice. Endocrinology 2018; 159: 579-596
  • 96 Afrisham R, Paknejad M, Soliemanifar O. et al. The influence of psychological stress on the initiation and progression of diabetes and cancer. Int J Endocrinol Metab 2019; 17: e67400
  • 97 Karavanaki K, Tsoka E, Liacopoulou M. et al. Psychological stress as a factor potentially contributing to the pathogenesis of Type 1 diabetes mellitus. J Endocrinol Invest 2008; 31: 406-415
  • 98 Al-Majed HT, Jones PM, Persaud SJ. et al. ACTH stimulates insulin secretion from MIN6 cells and primary mouse and human islets of Langerhans. J Endocrinol 2004; 180: 155-166
  • 99 Bandyopadhyay GK, Mahata SK. Chromogranin A regulation of obesity and peripheral insulin sensitivity. Front Endocrinol 2017; 8: 20
  • 100 Johnston JL. A role for norepinephrine metabolism in energy balance and obesity: a review. Canad Inst Food Sci Technol J 1987; 20: 331-335
  • 101 Bönisch C, Irmler M, Brachthäuser L. et al. Dexamethasone treatment alters insulin, leptin, and adiponectin levels in male mice as observed in DIO but does not lead to alterations of metabolic phenotypes in the offspring. Mamm Genome 2016; 27: 17-28
  • 102 Antuna-Puente B, Feve B, Fellahi S. et al. Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab 2008; 34: 2-11
  • 103 Calcia MA, Bonsall DR, Bloomfield PS. et al. Stress and neuroinflammation: a systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology (Berl) 2016; 233: 1637-1650
  • 104 Dionysopoulou S, Charmandari E, Bargiota A. et al. The role of hypothalamic inflammation in diet-induced obesity and its association with cognitive and mood disorders. Nutrients 2021; 13: 498
  • 105 Jacka FN, Cherbuin N, Anstey KJ. et al. Western diet is associated with a smaller hippocampus: a longitudinal investigation. BMC Med 2015; 13: 215
  • 106 Mannan M, Mamun A, Doi S. et al. Prospective associations between depression and obesity for adolescent males and females – a systematic review and meta-analysis of longitudinal studies. PLoS One 2016; 11: e0157240
  • 107 Rosmond R. Role of stress in the pathogenesis of the metabolic syndrome. Psychoneuroendocrinology 2005; 30: 1-10
  • 108 Saklayen MG. The global rpidemic of the metabolic syndrome. Curr Hypertens Rep 2018; 20: 12
  • 109 Cryer PE. Minireview: glucagon in the pathogenesis of hypoglycemia and hyperglycemia in diabetes. Endocrinology 2012; 153: 1039-1048
  • 110 Gayen JR, Saberi M, Schenk S. et al. A novel pathway of insulin sensitivity in chromogranin A null mice: a crucial role for pancreastatin in glucose homeostasis. J Biol Chem 2009; 284: 28498-28509
  • 111 Verberne AJM, Korim WS, Sabetghadam A. et al. Adrenaline: insights into its metabolic roles in hypoglycaemia and diabetes. Br J Pharmacol 2016; 173: 1425-1437
  • 112 Rayner DV. The sympathetic nervous system in white adipose tissue regulation. Proc Nutr Soc 2001; 60: 357-364
  • 113 Muzzin P, Revelli JP, Kuhne F. et al. An adipose tissue-specific beta-adrenergic receptor. Molecular cloning and down-regulation in obesity. J Biol Chem 1991; 266: 24053-24058
  • 114 Ward KD, Sparrow D, Landsberg L. et al. The relationship of epinephrine excretion to serum lipid levels: the Normative Aging Study. Metabolism 1994; 43: 509-513
  • 115 Bandyopadhyay GK, Lu M, Avolio E. et al. Pancreastatin-dependent inflammatory signaling mediates obesity-induced insulin resistance. Diabetes 2015; 64: 104-116
  • 116 O’Connor DT, Cadman PE, Smiley C. et al. Pancreastatin: multiple actions on human intermediary metabolism in vivo, variation in disease, and naturally occurring functional genetic polymorphism. J Clin Endocrinol Metab 2005; 90: 5414-5425
  • 117 Achard V, Boullu-Ciocca S, Desbriere R. et al. Renin receptor expression in human adipose tissue. Am J Physiol Regul Integr Comp Physiol 2007; 292: R274-R282
  • 118 Achard V, Tassistro V, Boullu-Ciocca S. et al. Expression and nutritional regulation of the (pro)renin receptor in rat visceral adipose tissue. J Endocrinol Invest 2011; 34: 840-846
  • 119 Dinh Cat AN, Friederich-Persson M, White A. et al. Adipocytes, aldosterone and obesity-related hypertension. J Mol Endocrinol 2016; 57: F7-F21
  • 120 Rossi GP, Belfiore A, Bernini G. et al. Body mass index predicts plasma aldosterone concentrations in overweight-obese primary hypertensive patients. J Clin Endocrinol Metab 2008; 93: 2566-2571
  • 121 Kopp UC, DiBona GF. Interaction between epinephrine and renal nerves in control of renin secretion rate. Am J Physiol 1986; 250: F999-F1007
  • 122 Dupont AG, Brouwers S. Brain angiotensin peptides regulate sympathetic tone and blood pressure. J Hypertens 2010; 28: 1599-1610
  • 123 Gianotti L, Belcastro S, D’Agnano S. et al. The stress axis in obesity and diabetes mellitus: an update. Endocrines 2021; 2: 334-347
  • 124 Kuo T, McQueen A, Chen T-C. et al. Regulation of glucose homeostasis by glucocorticoids. Adv Exp Med Biol 2015; 872: 99-126
  • 125 Bechtold AG, Patel G, Hochhaus G. et al. Chronic blockade of hindbrain glucocorticoid receptors reduces blood pressure responses to novel stress and attenuates adaptation to repeated stress. Am J Physiol Regul Integr Comp Physiol 2009; 296: R1445-R1454
  • 126 Whitworth JA, Williamson PM, Mangos G. et al. Cardiovascular consequences of cortisol excess. Vasc Health Risk Manag 2005; 1: 291-299
  • 127 Crawford AA, Soderberg S, Kirschbaum C. et al. Morning plasma cortisol as a cardiovascular risk factor: findings from prospective cohort and Mendelian randomization studies. Eur J Endocrinol 2019; 181: 429-438
  • 128 Haddad C, Courand P-Y, Berge C. et al. Impact of cortisol on blood pressure and hypertension-mediated organ damage in hypertensive patients. J Hypertens 2021; 39: 1412-1420
  • 129 Whitworth JA, Saines D, Thatcher R. et al. Blood pressure and metabolic effects of ACTH in normotensive and hypertensive man. Clin Exp Hypertens A 1983; 5: 501-522
  • 130 Beaupere C, Liboz A, Fève B. et al. Molecular mechanisms of glucocorticoid-induced insulin resistance. Int J Mol Sci 2021; 22: 623
  • 131 Nicolaides NC, Kyratzi E, Lamprokostopoulou A. et al. Stress, the stress system and the role of glucocorticoids. Neuroimmunomodulation 2015; 22: 6-19
  • 132 Kyrou I, Chrousos GP, Tsigos C. Stress, visceral obesity, and metabolic complications. Ann New York Acad Sci 2006; 1083: 77-110
  • 133 Sominsky L, Spencer SJ. Eating behavior and stress: a pathway to obesity. Front Psychol 2014; 5: 434
  • 134 Tsai S-F, Hung H-C, Shih MM-C. et al. High-fat diet-induced increases in glucocorticoids contribute to the development of non-alcoholic fatty liver disease in mice. FASEB J 2022; 36: e22130
  • 135 Lambillotte C, Gilon P, Henquin JC. Direct glucocorticoid inhibition of insulin secretion. An in vitro study of dexamethasone effects in mouse islets. J Clin Invest 1997; 99: 414-423
  • 136 Ullrich S, Berchtold S, Ranta F. et al. Serum- and glucocorticoid-inducible kinase 1 (SGK1) mediates glucocorticoid-induced inhibition of insulin secretion. Diabetes 2005; 54: 1090-1099
  • 137 Gesina E, Tronche F, Herrera P. et al. Dissecting the role of glucocorticoids on pancreas development. Diabetes 2004; 53: 2322-2329
  • 138 Fine NHF, Doig CL, Elhassan YS. et al. Glucocorticoids reprogram β-cell signaling to preserve insulin secretion. Diabetes 2018; 67: 278-290