Blunted glucocorticoid and mineralocorticoid sensitivity to stress in people with diabetes

Psychoneuroendocrinology

Volumn 51, Issue , 2015, Pages 209-218

  Carvalho, Livia A ^a   Urbanova, Livia ^a   Hamer, Mark ^a   Hackett, Ruth A ^a   Lazzarino, Antonio I ^a   Steptoe, Andrew ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Acute stress; Auto immune diseases; Cardiovascular; Corticosteroid sensitivity; Cytokines; HPA axis

Indexed keywords

ACETYLSALICYLIC ACID; ANTIHYPERTENSIVE AGENT; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; DEXAMETHASONE; HYDROCORTISONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INSULIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; METFORMIN; MONOCYTE CHEMOTACTIC PROTEIN 1; ORAL ANTIDIABETIC AGENT; PREDNISOLONE; GLUCOCORTICOID;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIASTOLIC BLOOD PRESSURE; FEMALE; HEART RATE; HORMONE SENSITIVITY; HUMAN; HYPERTENSION; MALE; MENTAL STRESS; NON INSULIN DEPENDENT DIABETES MELLITUS; PROTEIN BLOOD LEVEL; SALIVA LEVEL; SYSTOLIC BLOOD PRESSURE; AGED; BLOOD; BLOOD PRESSURE; CHEMISTRY; DRUG EFFECTS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MIDDLE AGED; PATHOPHYSIOLOGY; SALIVA;

AGED; BLOOD PRESSURE; CHEMOKINE CCL2; DEXAMETHASONE; DIABETES MELLITUS, TYPE 2; FEMALE; GLUCOCORTICOIDS; HEART RATE; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INTERLEUKIN-6; MALE; MIDDLE AGED; PITUITARY-ADRENAL SYSTEM; PREDNISOLONE; SALIVA; STRESS, PSYCHOLOGICAL;

EID: 84920593374     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.09.023     Document Type: Article

References (53)

1. Akash M.S., Rehman K., Chen S. An overview of valuable scientific models for diabetes mellitus. Curr. Diabetes Rev. 2013, 9:286-293.
2. Akash M.S., Rehman K., Chen S. Role of inflammatory mechanisms in pathogenesis of type 2 diabetes mellitus. J. Cell Biochem. 2013, 114:525-531.
3. Akash M.S., Rehman K., Sun H., Chen S. Interleukin-1 receptor antagonist improves normoglycemia and insulin sensitivity in diabetic Goto-Kakizaki-rats. Eur. J. Pharmacol. 2013, 701:87-95.
4. Akash M.S., Shen Q., Rehman K., Chen S. Interleukin-1 receptor antagonist: a new therapy for type 2 diabetes mellitus. J. Pharm. Sci. 2012, 101:1647-1658.
5. Bauer M.E., Papadopoulos A., Poon L., Perks P., Lightman S.L., Checkley S., Shanks N. Altered glucocorticoid immunoregulation in treatment resistant depression. Psychoneuroendocrinology 2003, 28:49-65.
6. Briet M., Schiffrin E.L. The role of aldosterone in the metabolic syndrome. Curr. Hypertens. Rep. 2011, 13:163-172.
7. Bruehl H., Rueger M., Dziobek I., Sweat V., Tirsi A., Javier E., Arentoft A., Wolf O.T., Convit A. Hypothalamic-pituitary-adrenal axis dysregulation and memory impairments in type 2 diabetes. J. Clin. Endocrinol. Metab. 2007, 92:2439-2445.
8. Cameron O.G., Kronfol Z., Greden J.F., Carroll B.J. Hypothalamic-pituitary-adrenocortical activity in patients with diabetes mellitus. Arch. Gen. Psychiatry 1984, 41:1090-1095.
9. Carvalho L.A., Garner B.A., Dew T., Fazakerley H., Pariante C.M. Antidepressants, but not antipsychotics, modulate GR function in human whole blood: an insight into molecular mechanisms. Eur. Neuropsychopharmacol. 2010, 20:379-387.
10. Carvalho L.A., Juruena M.F., Papadopoulos A.S., Poon L., Kerwin R., Cleare A.J., Pariante C.M. Clomipramine in vitro reduces glucocorticoid receptor function in healthy subjects but not in patients with major depression. Neuropsychopharmacology 2008, 33:3182-3189.
11. Chan O., Inouye K., Akirav E., Park E., Riddell M.C., Vranic M., Matthews S.G. Insulin alone increases hypothalamo-pituitary-adrenal activity, and diabetes lowers peak stress responses. Endocrinology 2005, 146:1382-1390.
12. Chan O., Inouye K., Riddell M.C., Vranic M., Matthews S.G. Diabetes and the hypothalamo-pituitary-adrenal (HPA) axis. Minerva Endocrinol. 2003, 28:87-102.
13. Chan O., Inouye K., Vranic M., Matthews S.G. Hyperactivation of the hypothalamo-pituitary-adrenocortical axis in streptozotocin-diabetes is associated with reduced stress responsiveness and decreased pituitary and adrenal sensitivity. Endocrinology 2002, 143:1761-1768.
14. Chida Y., Hamer M. An association of adverse psychosocial factors with diabetes mellitus: a meta-analytic review of longitudinal cohort studies. Diabetologia 2008, 51:2168-2178.
15. Chiodini I., Adda G., Scillitani A., Coletti F., Morelli V., Di L.S., Epaminonda P., Masserini B., Beck-Peccoz P., Orsi E., Ambrosi B., Arosio M. Cortisol secretion in patients with type 2 diabetes: relationship with chronic complications. Diabetes Care 2007, 30:83-88.
16. de Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19:269-301.
17. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 2004, 130:355-391.
18. Eickelberg O., Roth M., Lorx R., Bruce V., Rudiger J., Johnson M., Block L.H. Ligand-independent activation of the glucocorticoid receptor by beta2-adrenergic receptor agonists in primary human lung fibroblasts and vascular smooth muscle cells. J. Biol. Chem. 1999, 274:1005-1010.
19. Eriksson A.K., Ekbom A., Granath F., Hilding A., Efendic S., Ostenson C.G. Psychological distress and risk of pre-diabetes and type 2 diabetes in a prospective study of Swedish middle-aged men and women. Diabetic Med. 2008, 25:834-842.
20. Fernandez-Real J.M., Ricart W. Insulin resistance and inflammation in an evolutionary perspective: the contribution of cytokine genotype/phenotype to thriftiness. Diabetologia 1999, 42:1367-1374.
21. Fernandez-Real J.M., Vayreda M., Richart C., Gutierrez C., Broch M., Vendrell J., Ricart W. Circulating interleukin 6 levels, blood pressure, and insulin sensitivity in apparently healthy men and women. J. Clin. Endocrinol. Metab. 2001, 86:1154-1159.
22. Gruenewald T.L., Kemeny M.E., Aziz N., Fahey J.L. Acute threat to the social self: shame, social self-esteem, and cortisol activity. Psychosom. Med. 2004, 66:915-924.
23. Hackett R.A., Hamer M., Endrighi R., Brydon L., Steptoe A. Loneliness and stress-related inflammatory and neuroendocrine responses in older men and women. Psychoneuroendocrinology 2012, 37:1801-1809.
24. Haffner S.M., Lehto S., Ronnemaa T., Pyorala K., Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N. Engl. J. Med. 1998, 339:229-234.
25. Hamer M., O'Donnell K., Lahiri A., Steptoe A. Salivary cortisol responses to mental stress are associated with coronary artery calcification in healthy men and women. Eur. Heart J. 2010, 31:424-429.
26. Hudson J.I., Hudson M.S., Rothschild A.J., Vignati L., Schatzberg A.F., Melby J.C. Abnormal results of dexamethasone suppression tests in nondepressed patients with diabetes mellitus. Arch. Gen. Psychiatry 1984, 41:1086-1089.
27. Juruena M.F., Pariante C.M., Papadopoulos A.S., Poon L., Lightman S., Cleare A.J. Prednisolone suppression test in depression: prospective study of the role of HPA axis dysfunction in treatment resistance. Br. J. Psychiatry 2009, 194:342-349.
28. Kaye T.B., Rubin R.A., Goldfine A.B., Rajamani K., Kinsley B.T., Vischer U.M., Simonson D.C. Effect of glycemic control on the overnight dexamethasone suppression test in patients with diabetes mellitus. J. Clin. Endocrinol. Metab. 1992, 74:640-644.
29. Kern P.A., Ranganathan S., Li C., Wood L., Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 2001, 280:E745-E751.
30. Kraemer H.C., Giese-Davis J., Yutsis M., O'Hara R., Neri E., Gallagher-Thompson D., Taylor C.B., Spiegel D. Design decisions to optimize reliability of daytime cortisol slopes in an older population. Am. J. Geriatr. Psychiatry 2006, 14:325-333.
31. Lastra-Gonzalez G., Manrique-Acevedo C., Sowers J.R. The role of aldosterone in cardiovascular disease in people with diabetes and hypertension: an update. Curr. Diabetes Rep. 2008, 8:203-207.
32. Ljung T., Holm G., Friberg P., Andersson B., Bengtsson B.A., Svensson J., Dallman M., McEwen B., Bjorntorp P. The activity of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in relation to waist/hip circumference ratio in men. Obes. Res. 2000, 8:487-495.
33. Miller G.E., Rohleder N., Stetler C., Kirschbaum C. Clinical depression and regulation of the inflammatory response during acute stress. Psychosom. Med. 2005, 67:679-687.
34. Mukamal K.J., Nesto R.W., Cohen M.C., Muller J.E., Maclure M., Sherwood J.B., Mittleman M.A. Impact of diabetes on long-term survival after acute myocardial infarction: comparability of risk with prior myocardial infarction. Diabetes Care 2001, 24:1422-1427.
35. Nyberg S.T., Fransson E.I., Heikkila K., Ahola K., Alfredsson L., Bjorner J.B., Borritz M., Burr H., Dragano N., Goldberg M., Hamer M., Jokela M., Knutsson A., Koskenvuo M., Koskinen A., Kouvonen A., Leineweber C., Madsen I.E., Magnusson Hanson L.L., Marmot M.G., Nielsen M.L., Nordin M., Oksanen T., Pejtersen J.H., Pentti J., Rugulies R., Salo P., Siegrist J., Steptoe A., Suominen S., Theorell T., Vaananen A., Vahtera J., Virtanen M., Westerholm P.J., Westerlund H., Zins M., Batty G.D., Brunner E.J., Ferrie J.E., Singh-Manoux A., Kivimaki M. Job strain as a risk factor for type 2 diabetes: a pooled analysis of 124,808 men and women. Diabetes Care 2014, 37:2268-2275.
36. Pruessner M., Hellhammer D.H., Pruessner J.C., Lupien S.J. Self-reported depressive symptoms and stress levels in healthy young men: associations with the cortisol response to awakening. Psychosom. Med. 2003, 65:92-99.
37. Raison C.L., Miller A.H. When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am. J. Psychiatry 2003, 160:1554-1565.
38. Ray A., Huisman M.V., Tamsma J.T., van A.J., Bingen B.O., Broeders E.A., Hoogeveen E.S., van H.F., Kwee V.A., Laman B., Malgo F., Mohammadi M., Nijenhuis M., Rijkee M., van Tellingen M.M., Tromp M., Tummers Q., de V.L. The role of inflammation on atherosclerosis, intermediate and clinical cardiovascular endpoints in type 2 diabetes mellitus. Eur. J. Intern. Med. 2009, 20:253-260.
39. Reynolds R.M., Labad J., Strachan M.W., Braun A., Fowkes F.G., Lee A.J., Frier B.M., Seckl J.R., Walker B.R., Price J.F. Elevated fasting plasma cortisol is associated with ischemic heart disease and its risk factors in people with type 2 diabetes: the Edinburgh type 2 diabetes study. J. Clin. Endocrinol. Metab. 2010, 95:1602-1608.
40. Rohleder N., Wolf J.M., Kirschbaum C. Glucocorticoid sensitivity in humans-interindividual differences and acute stress effects. Stress 2003, 6:207-222.
41. Rotella F., Mannucci E. Depression as a risk factor for diabetes: a meta-analysis of longitudinal studies. J. Clin. Psychiatry 2013, 74:31-37.
42. Roy M., Collier B., Roy A. Hypothalamic-pituitary-adrenal axis dysregulation among diabetic outpatients. Psychiatry Res. 1990, 31:31-37.
43. Roy M.S., Roy A., Gallucci W.T., Collier B., Young K., Kamilaris T.C., Chrousos G.P. The ovine corticotropin-releasing hormone-stimulation test in type I diabetic patients and controls: suggestion of mild chronic hypercortisolism. Metabolism 1993, 42:696-700.
44. Rupprecht R., Reul J.M., van Steensel B., Spengler D., Soder M., Berning B., Holsboer F., Damm K. Pharmacological and functional characterization of human mineralocorticoid and glucocorticoid receptor ligands. Eur. J. Pharmacol. 1993, 247:145-154.
45. Steptoe A., Cropley M. Persistent high job demands and reactivity to mental stress predict future ambulatory blood pressure. J. Hypertens. 2000, 18:581-586.
46. Steptoe A., Feldman P.J., Kunz S., Owen N., Willemsen G., Marmot M. Stress responsivity and socioeconomic status: a mechanism for increased cardiovascular disease risk?. Eur. Heart J. 2002, 23:1757-1763.
47. Steptoe A., Hamer M., Chida Y. The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav. Immun. 2007, 21:901-912.
48. Steptoe A., Hackett R., Lazzarino A.I., Bostock S., La Marca R., Carvalho L.A., Hamer M. Disruption of Multisystem Responses to Stress in Type 2 Diabetes: Investigating the Dynamics of Allostatic Load. Proc. Natl. Acad. Sci. U.S.A 2014, [Epub ahead of print].
49. Steptoe A., Owen N., Kunz-Ebrecht S., Mohamed-Ali V. Inflammatory cytokines, socioeconomic status, and acute stress responsivity. Brain Behav. Immun. 2002, 16:774-784.
50. Steptoe A., Willemsen G., Owen N., Flower L., Mohamed-Ali V. Acute mental stress elicits delayed increases in circulating inflammatory cytokine levels. Clin. Sci. (Lond) 2001, 101:185-192.
51. Yehuda R., Yang R.K., Golier J.A., Grossman R.A., Bierer L.M., Tischler L. Effect of sertraline on glucocorticoid sensitivity of mononuclear leukocytes in post-traumatic stress disorder. Neuropsychopharmacology 2006, 31:189-196.
52. Yusuf S., Hawken S., Ounpuu S., Dans T., Avezum A., Lanas F., McQueen M., Budaj A., Pais P., Varigos J., Lisheng L. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 2004, 364:937-952.
53. Zalli A., Carvalho L.A., Lin J., Hamer M., Erusalimsky J.D., Blackburn E.H., Steptoe A. Shorter telomeres with high telomerase activity are associated with raised allostatic load and impoverished psychosocial resources. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:4519-4524.