Greater inflammatory activity and blunted glucocorticoid signaling in monocytes of chronically stressed caregivers

Brain, Behavior, and Immunity

Volumn 41, Issue 1, 2014, Pages 191-199

  Miller, Gregory E ^a   Murphy, Michael L M ^a   Cashman, Rosemary ^b   Ma, Roy ^b   Ma, Jeffrey ^c,d   Arevalo, Jesusa M G ^c,d   Kobor, Michael S ^e,f   Cole, Steve W ^c,d  

^a NORTHWESTERN UNIVERSITY   (United States)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e BC CHILDREN S HOSPITAL   (Canada)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Cytokines; Depression; Genomics; Glucocorticoids; Inflammation; Stress

Indexed keywords

ANTINEOPLASTIC AGENT; C REACTIVE PROTEIN; CD14 ANTIGEN; CD16 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CXCL2 CHEMOKINE; CYCLOOXYGENASE 2; FRACTALKINE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; BIOLOGICAL MARKER;

ADRENAL CORTEX; ADRENERGIC SYSTEM; ADULT; ARTICLE; CANCER RADIOTHERAPY; CAREGIVER; CAREGIVER BURDEN; CELL POPULATION; CHRONIC STRESS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISTRESS SYNDROME; DNA RESPONSIVE ELEMENT; DOWN REGULATION; EX VIVO STUDY; FEMALE; FLOW CYTOMETRY; FOLLOW UP; GENE EXPRESSION; GLIOBLASTOMA; HORMONE SENSITIVITY; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MIDDLE AGED; MONOCYTE; OUTCOME ASSESSMENT; PERCEIVED STRESS SCALE; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; WAIST CIRCUMFERENCE; BLOOD; BRAIN TUMOR; CELL CULTURE; CHEMISTRY; CHRONIC DISEASE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; LEUKOCYTE; MENTAL STRESS; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; SALIVA; SECRETION (PROCESS);

ADULT; BIOMARKERS; BRAIN NEOPLASMS; C-REACTIVE PROTEIN; CAREGIVERS; CELLS, CULTURED; CHRONIC DISEASE; FEMALE; GENE EXPRESSION PROFILING; GLIOBLASTOMA; HUMANS; HYDROCORTISONE; INFLAMMATION; LEUKOCYTES; LIPOPOLYSACCHARIDES; MALE; MIDDLE AGED; MONOCYTES; RECEPTORS, GLUCOCORTICOID; SALIVA; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84924029983     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.05.016     Document Type: Article

References (53)

1. Auffray C., Sieweke M.H., Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 2009, 27:669-692.
2. Babyak M.A. What you see may not be what you get: a brief, nontechnical introduction to overfitting in regression-type models. Psychosom. Med. 2004, 66:411-421.
3. Biosciences B.D. Application Note: Detecting Intracellular Cytokines in Activated Monocytes 1999, Becton, Dickinson, and Company, Franklin Lakes, NJ.
4. Beck I.M., Vanden Berghe W., Vermeulen L., Yamamoto K.R., Haegeman G., De Bosscher K. Crosstalk in inflammation: the interplay of glucocorticoid receptor-based mechanisms and kinases and phosphatases. Endocr. Rev. 2009, 30:830-882.
5. Busillo J.M., Cidlowski J.A. The five Rs of glucocorticoid action during inflammation: ready, reinforce, repress, resolve, and restore. Trends Endocrinol. Metab. 2013, 24:109-119.
6. Centers for Disease Control National Health and Nutrition Examination Survey Questionnaire 2009, U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Hyattsville, MD.
7. Christakis N.A., Allison P.D. Mortality after the hospitalization of a spouse. N. Engl. J. Med. 2006, 354:719-730.
8. Cohen S., Janicki-Deverts D., Doyle W.J., Miller G.E., Frank E., Rabin B.S., Turner R.B. Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc. Natl. Acad. Sci. USA 2012, 109:5995-5999.
9. Cohen S., Janicki-Deverts D.L., Miller G.E. Psychological stress and disease. J. Am. Med. Assoc. 2007, 298:1685-1687.
10. Cohen S., Kamarck T.W., Mermelstein R. A global measure of perceived stress. J. Health Soc. Behav. 1983, 24:385-396.
11. Cole S.W., Hawkley L.C., Arevalo J.M., Sung C.S., Rose R.M., Cacioppo J.T. Social regulation of gene expression: inflammation and the human transcriptional response to loneliness. Genome Biol. 2007, 8:r89.
12. Cole S.W., Galic Z., Zack J.A. Controlling false-negative errors in microarray differential expression analysis: a PRIM approach. Bioinformatics 2003, 19:1808-1816.
13. Cole S.W., Hawkley L.C., Arevalo J.M., Cacioppo J.T. Transcript origin analysis identifies antigen-presenting cells as primary targets of socially regulated gene expression in leukocytes. Proc. Natl. Acad. Sci. USA 2011, 108:3080-3085.
14. Cole S.W., Yan W., Galic Z., Arevalo J., Zack J.A. Expression-based monitoring of transcription factor activity: the TELiS database. Bioinformatics 2005, 21:803-810.
15. Dupre M.E., George L.K., Liu G., Peterson E.D. The cumulative effect of unemployment on risks for acute myocardial infarction. Arch. Intern. Med. 2012, 172:1731-1737.
16. Fredrickson B.L., Grewen K.M., Coffey K.A., Algoe S.B., Firestine A.M., Arevalo J.M., Ma J., Cole S.W. A functional genomic perspective on human well-being. Proc. Natl. Acad. Sci. USA 2013, 110:13684-13689.
17. Fries E., Hesse J., Hellhammer J., Hellhammer D.H. A new view on hypocortisolism. Psychoneuroendocrinology 2005, 30:1010-1016.
18. Galliher-Beckley A.J., Cidlowski J.A. Emerging roles of glucocorticoid receptor phosphorylation in modulating glucocorticoid hormone action in health and disease. IUBMB Life 2009, 61:979-986.
19. Hanley J.A., Negassa A., Edwardes M.D., Forrester J.E. Statistical analysis of correlated data using generalized estimating equations: an orientation. Am. J. Epidemiol. 2003, 157:364-375.
20. Haroon E., Raison C.L., Miller A.H. Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 2012, 37:137-162.
21. Ingersoll M.A., Spanbroek R., Lottaz C., Gautier E.L., Frankenberger M., Hoffmann R., Lang R., Haniffa M., Collin M., Tacke F., Habenicht A.J., Ziegler-Heitbrock L., Randolph G.J. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 2010, 115:e10-9.
22. Irwin M.R., Cole S.W. Reciprocal regulation of the neural and innate immune systems. Nat. Rev. Immunol. 2011, 11:625-632.
23. Ji J., Zoller B., Sundquist K., Sundquist J. Increased risks of coronary heart disease and stroke among spousal caregivers of cancer patients. Circulation 2012, 125:1742-1747.
24. Klengel T., Mehta D., Anacker C., Rex-Haffner M., Pruessner J.C., Pariante C.M., Pace T.W., Mercer K.B., Mayberg H.S., Bradley B., Nemeroff C.B., Holsboer F., Heim C.M., Ressler K.J., Rein T., Binder E.B. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat. Neurosci. 2013, 16:33-41.
25. Libby P., Ridker P.M., Hansson G.K. Progress and challenges in translating the biology of atherosclerosis. Nature 2011, 473:317-325.
26. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 2009, 10:434-445.
27. Matthews K., Gump B.B. Chronic work stress and marital dissolution increase risk of posttrial mortality in men from the Multiple Risk Factor Intervention Trial. Arch. Intern. Med. 2002, 162:309-315.
28. Miller A.H. Inflammation versus glucocorticoids as purveyors of pathology during stress: have we reached the tipping point?. Biol. Psychiatry 2008, 64:263-265.
29. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65:732-741.
30. Miller G.E., Chen E., Sze J., Marin T., Arevalo J.M.G., Doll R., Ma R., Cole S.W. A genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-κB signaling. Biol. Psychiatry 2008, 64:266-272.
31. Miller G.E., Chen E., Fok A., Walker H., Lim A., Nicholls E.P., Cole S.W., Kobor M.S. Low early-life social class leaves a biological residue manifest by decreased glucocorticoid and increased pro-inflammatory signaling. Proc. Natl. Acad. Sci. USA 2009, 106:14716-14721.
32. Miller G.E., Chen E., Zhou E.S. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychol. Bull. 2007, 133:25-45.
33. Miller G.E., Cohen S., Herbert T.B. Pathways linking major depression and immunity in ambulatory female patients. Psychosom. Med. 1999, 61:850-860.
34. Miller G.E., Cohen S., Ritchey A.K. Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid resistance model. Health Psychol. 2002, 21:531-541.
35. Nathan C., Ding A. Nonresolving inflammation. Cell 2010, 140:871-882.
36. O'Donovan A., Sun B., Cole S., Rempel H., Lenoci M., Pulliam L., Neylan T. Transcriptional control of monocyte gene expression in post-traumatic stress disorder. Dis. Markers 2011, 30:123-132.
37. Pace T.W., Heim C.M. A short review on the psychoneuroimmunology of posttraumatic stress disorder: from risk factors to medical comorbidities. Brain Behav. Immun. 2011, 25:6-13.
38. Pace T.W., Hu F., Miller A.H. Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain Behav. Immun. 2007, 21:9-19.
39. Paffenbarger R.S., Blair S.N., Lee I., Hyde R.T. Measurement of physical activity to assess health effects in a free-living population. Med. Sci. Sports Exerc. 1993, 25:60-70.
40. Pariante C.M., Miller A.H. Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment. Biol. Psychiatry 2001, 49:391-404.
41. Powell N.D., Sloan E.K., Bailey M.T., Arevalo J.M.G., Miller G.E., Chen E., Kobor M.S., Reader B.F., Sheridan J.F., Cole S.W. Social stress up-regulates inflammatory gene expression in the leukocyte transcriptome via beta-adrenergic induction of myelopoiesis. Proc. Natl. Acad. Sci. USA 2013, 110:16574-16579.
42. Radloff L.S. The CES-D scale: a self-report depression scale for research in the general population. J. Appl. Psychol. Meas. 1977, 1:385-401.
43. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 2006, 27:24-31.
44. 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.
45. Rohleder N. Acute and chronic stress induced changes in sensitivity of peripheral inflammatory pathways to the signals of multiple stress systems - 2011 Curt Richter Award Winner. Psychoneuroendocrinology 2012, 37:307-316.
46. Rohleder N., Marin T.J., Ma R., Miller G.E. Biologic cost of caring for a cancer patient: dysregulation of pro- and anti-inflammatory signaling pathways. J. Clin. Oncol. 2009, 27:2909-2915.
47. Sauer J., Castren M., Hopfner U., Holsboer F., Stalla G.K., Arzt E. Inhibition of lipopolysaccharide-induced monocyte interleukin-1 receptor antagonist synthesis by cortisol: involvement of the mineralocorticoid receptor. J. Clin. Endocrinol. Metab. 1996, 81:73-79.
48. Schulz R., Mendelsohn A.B., Haley W.E., Mahoney D., Allen R.S., Zhang S., Thompson L., Belle S.H. End-of-life care and the effects of bereavement on family caregivers of persons with dementia. N. Engl. J. Med. 2003, 349:1936-1942.
49. Schulz R., Beach S.R. Caregiving as a risk factor for mortality. J. Am. Med. Assoc. 1999, 282:2215-2219.
50. Scrivo R., Vasile M., Bartosiewicz I., Valesini G. Inflammation as "common soil" of the multifactorial diseases. Autoimmun. Rev. 2011, 10:369-374.
51. Sternberg E.M. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat. Rev. Immunol. 2006, 6:318-328.
52. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352:987-996.
53. Woollard K.J., Geissmann F. Monocytes in atherosclerosis: subsets and functions. Nat. Rev. Cardiol. 2010, 7:77-86.