Psychosocial stress induces hyperphagia and exacerbates diet-induced insulin resistance and the manifestations of the Metabolic Syndrome

Psychoneuroendocrinology

Volumn 38, Issue 12, 2013, Pages 2933-2942

  Sanghez, Valentina ^a,b   Razzoli, Maria ^a   Carobbio, Stefania ^c   Campbell, Mark ^c   McCallum, Jacob ^a   Cero, Cheryl ^a   Ceresini, Graziano ^b   Cabassi, Aderville ^b   Govoni, Paolo ^b   Franceschini, Paolo ^b   de Santis, Valentina ^b   Gurney, Allison ^a   Ninkovic, Ivana ^a   Parmigiani, Stefano ^b   Palanza, Paola ^b   Vidal Puig, Antonio ^c   Bartolomucci, Alessandro ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF PARMA   (Italy)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Adiponectin; Dominance; Glucose tolerance test; Hyperphagia; Laptin; Social stress; Subiordination; Type 2 diabetes

Indexed keywords

ADIPONECTIN; CARBON DIOXIDE; LEPTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; DYSLIPIDEMIA; GLUCOSE TOLERANCE TEST; HYPERLEPTINEMIA; HYPERPHAGIA; HYPOADIPONECTINEMIA; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; LIPID DIET; LUNG GAS EXCHANGE; MALE; MENTAL STRESS; METABOLIC SYNDROME X; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RISK FACTOR; SOCIAL INTERACTION; SOCIAL STATUS; WEIGHT GAIN;

ADIPONECTIN; DOMINANCE; GLUCOSE TOLERANCE TEST; HYPERPHAGIA; LAPTIN; SOCIAL STRESS; SUBIORDINATION; TYPE 2 DIABETES;

ADIPONECTIN; ANIMALS; CALORIMETRY, INDIRECT; DIABETES MELLITUS, TYPE 2; DIET; DIET, HIGH-FAT; ENERGY INTAKE; ENERGY METABOLISM; GLUCOSE TOLERANCE TEST; HYPERPHAGIA; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; LEPTIN; MALE; METABOLIC SYNDROME X; MICE; RISK FACTORS; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; STRESS, PSYCHOLOGICAL;

EID: 84888298689     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2013.07.022     Document Type: Article

References (59)

1. Aldinger K.A., Sokoloff G., Rosenberg D.M., Palmer A.A., Millen K.J. Genetic variation and population substructure in outbred CD-1 mice: implications for genome-wide association studies. PLoS ONE 2009, 4:e4729.
2. Bartolomucci A., Palanza P., Gaspani L., Limiroli E., Panerai A.E., et al. Social status in mice: behavioral, endocrine and immune changes are context dependent. Physiol. Behav. 2001, 73:401-410.
3. Bartolomucci A., Pederzani T., Sacerdote P., Panerai A.E., Parmigiani S., Palanza P. Behavioral and physiological characterization of male mice under chronic psychosocial stress. Psychoneuroendocrinology 2004, 29:899-910.
4. Bartolomucci A. Social stress, immune functions and disease in rodents. Front. Neuroendocrinol. 2007, 28:28-49.
5. Bartolomucci A., Cabassi A., Govoni P., Ceresini G., Cero C., et al. Metabolic consequences and vulnerability to diet-induced obesity in male mice under chronic social stress. PLoS ONE 2009, 4:e4331.
6. Bartolomucci A., Carola V., Pascucci T., Puglisi-Allegra S., Cabib S., et al. Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice. Dis. Model Mech. 2010, 3:459-470.
7. Bartolomucci A., Palanza P., Sacerdote P., Panerai A.E., Sgoifo A., et al. Social factors and individual vulnerability to chronic stress exposure. Neurosci. Biobehav. Rev. 2005, 29:67-81.
8. Bjorntorp P., Rosmond R. The metabolic syndrome - a neuroendocrine disorder?. Br. J. Nutr. 2000, 83(Suppl. 1):S49-S57.
9. Brüning J.C., Winnay J., Bonner-Weir S., Taylor S.I., Accili D., Kahn C.R. Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 1997, 88:561-572.
10. Brunner E. Biology and health inequality. PLoS Biol. 2007, 5(11):e267.
11. Cannon W.B. Bodily Changes in Pain, Hunger, Fear and Rage: An Account of Recent Researches into the Function of Emotional Excitement 1929, D. Appleton and Company.
12. Chandola T., Brunner E., Marmot M. Chronic stress at work and the metabolic syndrome: prospective study. Br. Med. J. 2006, 332:521-525.
13. Chaouloff F. Social stress models in depression research: what do they tell us?. Cell Tissue Res. 2013, (in press).
14. Chuang J.C., Cui H., Mason B.L., Mahgoub M., Bookout A.L., et al. Chronic social defeat stress disrupts regulation of lipid synthesis. J. Lipid Res. 2010, 51:1344-1353.
15. Chuang J.C., Krishnan V., Yu H.G., Mason B., Cui H., et al. A beta3-adrenergic-leptin-melanocortin circuit regulates behavioral and metabolic changes induced by chronic stress. Biol. Psychiatry 2010, 67:1075-1082.
16. Chuang J.C., Perello M., Sakata I., Osborne-Lawrence S., Savitt J.M., et al. Ghrelin mediates stress-induced food-reward behavior in mice. J. Clin. Invest. 2011, 121:2684-2692.
17. Dadomo H., Sanghez V., Di Cristo L., Lori A., Ceresini G., et al. Vulnerability to chronic subordination stress-induced depression-like disorders in adult 129SvEv male mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 2011, 35:1461-1471.
18. Dallman M.F. Stress-induced obesity and the emotional nervous system. Trends Endocrinol. Metab. 2010, 21:159-165.
19. Dallman M.F., Strack A.M., Akana S.F., Bradbury M.J., Hanson E.S., et al. Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front. Neuroendocrinol. 1993, 14:303-347.
20. Dubreucq S., Kambire S., Conforzi M., Metna-Laurent M., Cannich A., Soria-Gomez E., Richard E., Marsicano G., Chaouloff F. Cannabinoid type 1 receptors located on single-minded 1-expressing neurons control emotional behaviors. Neuroscience 2012, 204:230-244.
21. Finger B.C., Dinan T.G., Cryan J.F. The temporal impact of chronic intermittent psychosocial stress on high-fat diet-induced alterations in body weight. Psychoneuroendocrinology 2012, 37:729-741.
22. Finger B.C., Dinan T.G., Cryan J.F. High-fat diet selectively protects against the effects of chronic social stress in the mouse. Neuroscience 2011, 192:351-360.
23. Fisher J.P., Young C.N., Fadel P.J. Central sympathetic overactivity: maladies and mechanisms. Auton. Neurosci. 2009, 148:5-15.
24. Foster M.T., Solomon M.B., Huhman K.L., Bartness T.J. Social defeat increases food intake, body mass, and adiposity in Syrian hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290(5):R1284-R1293.
25. Gesquiere L.R., Learn N.H., Simao M.C., Onyango P.O., Alberts S.C., Altmann J. Life at the top: rank and stress in wild male baboons. Science 2012, 333(6040):357-360.
26. Kahn C.R. Insulin action, diabetogenes, and the cause of type II diabetes. Diabetes 1994, 43:1066-1084.
27. Koolhaas J.M., Bartolomucci A., Buwalda B., de Boer S.F., Flügge G., et al. Stress revisited: a critical evaluation of the stress concept. Neurosci. Biobehav. Rev. 2011, 35:1291-1301.
28. Kuo L.E., Kitlinska J.B., Tilan J.U., Li L., Baker S.B., et al. Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome. Nat. Med. 2007, 13(7):803-811.
29. Kyrou I., Chrousos G.P., Tsigos C. Stress, visceral obesity, and metabolic complications. Ann. N.Y. Acad. Sci. 2006, 1083:77-110.
30. Leiter E.H. Selecting the "right" mouse model for metabolic syndrome and type 2 diabetes research. Methods Mol. Biol. 2009, 560:1-17.
31. Lewis G.F., Carpentier A., Adeli K., Giacca A. Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr. Rev. 2002, 23:201-229.
32. Mackenbach J.P., Kunst A.E., Cavelaars A.E., Groenhof F., Geurts J.J., et al. Socioeconomic inequalities in morbidity and mortality in Western Europe. Lancet 1997, 349:1655-1659.
33. Martin B.C., Warram J.H., Krolewski A.S., Bergman R.N., Soeldner J.S., Kahn C.R. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. Lancet 1992, 340:925-929.
34. McEwen B.S. Protective and damaging effects of stress mediators. N. Engl. J. Med. 1998, 338:171-179.
35. McEwen B.S., Mirsky A.E. How socioeconomic status may "get under the skin" and affect the heart. Eur. Heart J. 2002, 23:1727-1728.
36. Moles A., Bartolomucci A., Garbugino L., Conti R., Caprioli A., et al. Psychosocial stress affects energy balance in mice: modulation by social status. Psychoneuroendocrinology 2006, 31:623-633.
37. Mooy J.M., De Vries H., Grootenhuis P.A., Bouter L.M., Heine R.J. Major stressful life events in relation to prevalence of undetected type 2 diabetes. The Hoorn Study. Diab. Care 2000, 23:197-201.
38. Patterson Z.R., Khazall R., Mackay H., Anisman H., Abizaid A. Central ghrelin signaling mediates the metabolic response of C57BL/6 male mice to chronic social defeat stress. Endocrinology 2013, 154(3):1080-1091.
39. Räikkönen K., Matthews K.A., Kuller L.H. Depressive symptoms and stressful life events predict metabolic syndrome among middle-aged women. Diab. Care 2007, 30:872-877.
40. Razzoli M., Cero C., Bartolomucci A. How does stress affect energy balance? Recent advances in physiology and neurobehavioral genetics. Phenotyping Behaviour and Cognition. Towards a Cutting-edge Neurobehavioural Genetics 2013, Wiley Book Seried, (in press). V. Tucci (Ed.).
41. Razzoli M., Carboni L., Andreoli M., Michielin F., Ballottari A., Arban R. Strain-specific outcomes of repeated social defeat and chronic fluoxetine treatment in the mouse. Pharmacol. Biochem. Behav. 2011, 97:566-576.
42. Sapolsky R.M. The influence of social hierarchy on primate health. Science 2005, 308:648-652.
43. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
44. Schmidt M.V., Czisch M., Sterlemann V., Reinel C., Sämann P., Müller M.B. Chronic social stress during adolescence in mice alters fat distribution in late life: prevention by antidepressant treatment. Stress 2009, 12:89-94.
45. Scott K.A., Melhorn S.J., Sakai R.R. Effects of chronic social stress on obesity. Curr. Obes. Rep. 2012, 1:16-25.
46. Shively C.A., Register T.C., Clarkson T.B. Social stress, visceral obesity, and coronary artery atherosclerosis in female primates. Obesity 2009, 17:1513-1520. (Silver Spring).
47. Shonkoff J.P., Boyce W.T., McEwen B.S. Neuroscience, molecular biology, and the childhood roots of health disparities: building a new framework for health promotion and disease prevention. J. Am. Med. Assoc. 2009, 301:2252-2259.
48. Shpilberg Y., Beaudry J.L., D'Souza A., Campbell J.E., Peckett A., Riddell M.C. A rodent model of rapid-onset diabetes induced by glucocorticoids and high-fat feeding. Dis. Model Mech. 2012, 5:671-680.
49. Singh-Manoux A., Marmot M.G., Adler N.E. Does subjective social status predict health and change in health status better than objective status?. Psychosom. Med. 2005, 67:855-861.
50. Singewald G.M., Nguyen N.K., Neumann I.D., Singewald N., Reber S.O. Effect of chronic psychosocial stress-induced by subordinate colony (CSC) housing on brain neuronal activity patterns in mice. Stress 2009, 12:58-69.
51. Stumvoll M., Goldstein B.J., van Haeften T.W. Type 2 diabetes: principles of pathogenesis and therapy. Lancet 2005, 365:1333-1346.
52. Sun B., Purcell R.H., Terrillion C.E., Yan J., Moran T.H., Tamashiro K.L. Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes 2012, 61:2833-2841.
53. Surwit R.S. Of mice and men: behavioral medicine in the study of type II diabetes. Ann. Behav. Med. 1993, 15:227-235.
54. Tamashiro K.L., Nguyen M.M., Ostrander M.M., Gardner S.R., Ma L.Y., et al. Social stress and recovery: implications for body weight and body composition. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R1864-R1874.
55. Taniguchi C.M., Emanuelli B., Kahn C.R. Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 2006, 7:85-96.
56. Tesfaye N., Seaquist E.R. Neuroendocrine responses to hypoglycemia. Ann. N. Y. Acad. Sci. 2010, 1212:12-28.
57. Ulrich-Lai Y.M., Arnhold M.M., Engeland W.C. Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:R1128-R1135.
58. Wilcox R.R. New Statistical Procedures for the Social Sciences: Modern Solutions to the Basic Problems 1987, Erlbaum, Hillsdale, NJ.
59. Wilson M.E., Fisher J., Fischer A., Lee V., Harris R.B., Bartness T.J. Quantifying food intake in socially housed monkeys: social status effects on caloric consumption. Physiol. Behav. 2008, 94:586-594.