Weight loss by calorie restriction versus bariatric surgery differentially regulates the hypothalamo-pituitary-adrenocortical axis in male rats

Stress

Volumn 17, Issue 6, 2014, Pages 484-493

  Grayson, Bernadette E ^a   Hakala Finch, Andrew P ^a   Kekulawala, Melani ^a   Laub, Holly ^a   Egan, Ann E ^a   Ressler, Ilana B ^a   Woods, Stephen C ^a   Herman, James P ^a   Seeley, Randy J ^a   Benoit, Stephen C ^a   Ulrich Lai, Yvonne M ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Adrenocorticotropic hormone; Corticosterone; Corticotropin releasing hormone; Pair feeding; Roux en Y gastric bypass; Vertical sleeve gastrectomy

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; MESSENGER RNA; VASOPRESSIN; VASOPRESSIN DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BARIATRIC SURGERY; BEHAVIOR MODIFICATION; CALORIC RESTRICTION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENVIRONMENTAL STRESS; GENE EXPRESSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INTERMETHOD COMPARISON; MALE; NONHUMAN; OBESITY; RAT; ROUX Y ANASTOMOSIS; SLEEVE GASTRECTOMY; WEIGHT REDUCTION; ANIMAL; BLOOD; COMPARATIVE STUDY; DIET THERAPY; DISEASE MODEL; GASTRECTOMY; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LIPID DIET; LONG EVANS RAT; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; STOMACH BYPASS; TIME;

ANIMALS; CALORIC RESTRICTION; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; GASTRECTOMY; GASTRIC BYPASS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; OBESITY; PITUITARY-ADRENAL SYSTEM; RATS, LONG-EVANS; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TIME FACTORS; VASOPRESSINS; WEIGHT LOSS;

EID: 84910001121     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2014.967677     Document Type: Article

References (47)

1. Bevilacqua M, Dominguez LJ, Righini V, Vago T, Foschi D, Corsi F, Trabucchi E, et al. (2010). Acute parathyroid hormone increase by oral peptones administration after roux-en-Y gastric bypass surgery in obese subjects: role of phosphate in the rapid control of parathyroid hormone release. Surgery 147:655-61.
2. Bhatnagar S, Dallman M. (1998). Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84:1025-39.
3. Bornstein SR, Engeland WC, Ehrhart-Bornstein M, Herman JP. (2008). Dissociation of ACTH and glucocorticoids. Trends Endocrinol Metab 19:175-80.
4. Campfield LA, Smith FJ. (1986). Functional coupling between transient declines in blood glucose and feeding behavior: temporal relationships. Brain Res Bull 17:427-33.
5. Cerqueira JJ, Pego JM, Taipa R, Bessa JM, Almeida OF, Sousa N. (2005). Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 25:7792-800.
6. Chambers AP, Jessen L, Ryan KK, Sisley S, Wilson-Perez HE, Stefater MA, Gaitonde SG, et al. (2011). Weight-independent changes in blood glucose homeostasis after gastric bypass or vertical sleeve gastrectomy in rats. Gastroenterology 141:950-8.
7. Dallman MF. (2010). Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab 21:159-65.
8. Dimitrijevic M, Stanojevic S, Kustrimovic N, Leposavic G. (2012). Endpoint effector stress mediators in neuroimmune interactions: their role in immune system homeostasis and autoimmune pathology. Immunol Res 52:64-80.
9. Elenkov IJ, Chrousos GP. (2002). Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann N Y Acad Sci 966:290-303.
10. Engeland WC, Miller P, Gann DS. (1989). Dissociation between changes in plasma bioactive and immunoreactive adrenocorticotropin after hemorrhage in awake dogs. Endocrinology 124:2978-85.
11. Figueiredo HF, Bruestle A, Bodie B, Dolgas CM, Herman JP. (2003). The medial prefrontal cortex differentially regulates stress-induced cfos expression in the forebrain depending on type of stressor. Eur J Neurosci 18:2357-64.
12. Flak JN, Jankord R, Solomon MB, Krause EG, Herman JP. (2011). Opposing effects of chronic stress and weight restriction on cardiovascular, neuroendocrine and metabolic function. Physiol Behav 104: 228-34.
13. Francis LA, Granger DA, Susman EJ. (2013). Adrenocortical regulation, eating in the absence of hunger and BMI in young children. Appetite 64:32-8.
14. Goodwin GM, Fairburn CG, Keenan JC, Cowen PJ. (1988). The effects of dieting and weight loss upon the stimulation of thyrotropin (TSH) by thyrotropin-releasing hormone (TRH) and suppression of cortisol secretion by dexamethasone in men and women. J Affect Disord 14: 137-44.
15. Grayson BE, Fitzgerald MF, Hakala-Finch AP, Ferris VM, Begg DP, Tong J, Woods SC, et al (2014). Improvements in hippocampal-dependent memory and microglial infiltration with calorie restriction and gastric bypass surgery, but not with vertical sleeve gastrectomy. Int J Obes (Lond) 38:349-56.
16. Green PK, Wilkinson CW, Woods SC. (1992). Intraventricular corticosterone increases the rate of body weight gain in underweight adrenalectomized rats. Endocrinology 130:269-75.
17. Heiderstadt KM, McLaughlin RM, Wright DC, Walker SE, Gomez-Sanchez CE. (2000). The effect of chronic food and water restriction on open-field behaviour and serum corticosterone levels in rats. Lab Anim 34:20-8.
18. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai YM, Ostrander MM, Choi DC, Cullinan WE. (2003). Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151-80.
19. Herman JP, Watson SJ. (1995). Stress regulation of mineralocorticoid receptor heteronuclear RNA in rat hippocampus. Brain Res 677: 243-9.
20. Honma K, Honma S, Hirai T, Katsuno Y, Hiroshige T. (1986). Food ingestion is more important to plasma corticosterone dynamics than water intake in rats under restricted daily feeding. Physiol Behav 37: 791-5.
21. Kamara K, Eskay R, Castonguay T. (1998). High-fat diets and stress responsivity. Physiol Behav 64:1-6.
22. Lu Q, Tao F, Hou F, Zhang Z, Sun Y, Xu Y, Xu S, et al. (2014). Cortisol reactivity, delay discounting and percent body fat in Chinese urban young adolescents. Appetite 72:13-20.
23. McEwen BS. (2001). Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 933:265-77.
24. Mitchell DR, Lyles KW. (1990). Glucocorticoid-induced osteoporosis: mechanisms for bone loss; evaluation of strategies for prevention. J Gerontol 45:M153-8.
25. Pankevich DE, Teegarden SL, Hedin AD, Jensen CL, Bale TL. (2010). Caloric restriction experience reprograms stress and orexigenic pathways and promotes binge eating. J Neurosci 30:16399-407.
26. Patschan D, Loddenkemper K, Buttgereit F. (2001). Molecular mechanisms of glucocorticoid-induced osteoporosis. Bone 29:498-505.
27. Pories WJ, Swanson MS, MacDonald KG, Long SB, Morris PG, Brown BM, Barakat HA, et al. (1995). Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg 222:339-50.
28. Roslin MS, Dudiy Y, Brownlee A, Weiskopf J, Shah P. (2014). Response to glucose tolerance testing and solid high carbohydrate challenge: comparison between Roux-en-Y gastric bypass, vertical sleeve gastrectomy, and duodenal switch. Surg Endosc 28:91-9.
29. Ruiz-Tovar J, Oller I, Galindo I, Llavero C, Arroyo A, Calero A, Diez M, et al. (2013). Change in levels of C-reactive protein (CRP) and serum cortisol in morbidly obese patients after laparoscopic sleeve gastrectomy. Obes Surg 23:764-9.
30. Sapolsky RM, Krey LC, McEwen BS. (1985). Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 5:1222-7.
31. Schwabe L, Wolf OT. (2009). Stress prompts habit behavior in humans. J Neurosci 29:7191-8.
32. Sharma S, Fernandes MF, Fulton S. (2013). Adaptations in brain reward circuitry underlie palatable food cravings and anxiety induced by high-fat diet withdrawal. Int J Obes (Lond) 37:1183-91.
33. Soares JM, Sampaio A, Ferreira LM, Santos NC, Marques F, Palha JA, Cerqueira JJ, et al. (2012). Stress-induced changes in human decision-making are reversible. Transl Psychiatry 2:131-8.
34. Stefater MA, Perez-Tilve D, Chambers AP, Wilson-Perez HE, Sandoval DA, Berger J, Toure M, et al. (2010). Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology 138:2426-36.
35. Stefater MA, Wilson-Perez HE, Chambers AP, Sandoval DA, Seeley RJ. (2012). All bariatric surgeries are not created equal: insights from mechanistic comparisons. Endocr Rev 33:595-622.
36. Tafet GE, Bernardini R. (2003). Psychoneuroendocrinological links between chronic stress and depression. Prog Neuropsychopharmacol Biol Psychiatry 27:893-903.
37. Tannenbaum BM, Brindley DN, Tannenbaum GS, Dallman MF, McArthur MD, Meaney MJ. (1997). High-fat feeding alters both basal and stress-induced hypothalamic-pituitary-adrenal activity in the rat. Am J Physiol 273:E1168-77.
38. Tomiyama AJ, Mann T, Vinas D, Hunger JM, Dejager J, Taylor SE. (2010). Low calorie dieting increases cortisol. Psychosom Med 72: 357-64.
39. Ulrich-Lai YM, Engeland WC. (2002). Adrenal splanchnic innervation modulates adrenal cortical responses to dehydration stress in rats. Neuroendocrinology 76:79-92.
40. Ulrich-Lai YM, Figueiredo HF, Ostrander MM, Choi DC, Engeland WC, Herman JP. (2006a). Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. Am J Physiol Endocrinol Metab 291:E965-73.
41. Ulrich-Lai YM, Herman JP. (2009). Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397-409.
42. Ulrich-Lai YM, Ryan KK. (2014). Neuroendocrine circuits governing energy balance and stress regulation: functional overlap and therapeutic implications. Cell Metab 19:910-25.
43. Ulrich-Lai YM, Ostrander MM, Thomas IM, Packard BA, Furay AR, Dolgas CM, Van Hooren DC, et al. (2007). Daily limited access to sweetened drink attenuates hypothalamic-pituitary-adrenocortical axis stress responses. Endocrinology 148:1823-34.
44. Ulrich-Lai YM, Xie W, Meij JT, Dolgas CM, Yu L, Herman JP. (2006b). Limbic and HPA axis function in an animal model of chronic neuropathic pain. Physiol Behav 88:67-76.
45. Vahl TP, Ulrich-Lai YM, Ostrander MM, Dolgas CM, Elfers EE, Seeley RJ, D'Alessio DA, et al. (2005). Comparative analysis of ACTH and corticosterone sampling methods in rats. Am J Physiol Endocrinol Metab 289:E823-8.
46. Wing RR, Lang W, Wadden TA, Safford M, Knowler WC, Bertoni AG, Hill JO, et al. (2011). Benefits of modest weight loss in improving cardiovascular risk factors in overweight and obese individuals with type 2 diabetes. Diabetes Care 34:1481-6.
47. Witbracht MG, Laugero KD, Van Loan MD, Adams SH, Keim NL. (2012). Performance on the Iowa Gambling Task is related to magnitude of weight loss and salivary cortisol in a diet-induced weight loss intervention in overweight women. Physiol Behav 106: 291-7.