In Sickness and in Health: The Co-Regulation of Inflammation and Social Behavior

Neuropsychopharmacology

Volumn 42, Issue 1, 2017, Pages 242-253

  Eisenberger, Naomi I ^a   Moieni, Mona ^a   Inagaki, Tristen K ^b   Muscatell, Keely A ^c   Irwin, Michael R ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c University of North Carolina at Chapel Hill   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ENDOTOXIN; GLUCOCORTICOID;

ANTIINFLAMMATORY ACTIVITY; DEPRESSION; DISTRESS SYNDROME; EARLY LIFE STRESS; EXPOSURE; HUMAN; ILLNESS BEHAVIOR; IMMUNE SYSTEM; INFLAMMATION; LABORATORY TEST; LONELINESS; MENTAL HEALTH; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; REVIEW; RISK FACTOR; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; SOCIAL EXCLUSION; SOCIAL INTERACTION; SOCIAL ISOLATION; SOCIAL STRESS; ANIMAL; IMMUNOLOGY; MENTAL STRESS;

ANIMALS; HUMANS; INFLAMMATION; SOCIAL BEHAVIOR; SOCIAL ISOLATION; STRESS, PSYCHOLOGICAL;

EID: 84987624340     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2016.141     Document Type: Review

References (77)

1. Aschbacher K, Epel E, Wolkowitz OM, Prather AA, Puterman E, Dhabhar FS (2012).Maintenance of a positive outlook during acute stress protects against proinflammatoryreactivity and future depressive symptoms. Brain Behav Immun 26:346-352.
2. Avitsur R, Stark JL, Sheridan JF (2001). Social stress induces glucocorticoidresistance in subordinate animals. Horm Behav 39: 247-257.
3. Bilbo SD, Klein SL, DeVries AC, Nelson RJ (1999). Lipopolysaccharide facilitatespartner preference behaviors in female prairie voles. Physiol Behav 68: 151-156.
4. Bluthé RM, Dantzer R, Kelley KW (1992). Effects of interleukin-1 receptor antagoniston the behavioral effects of lipopolysaccharide in rat. Brain Res 573: 318-320.
5. Bluthé RM, Pawlowski M, Suarez S, Parnet P, Pittman Q, Kelley KW, et al. (1994).Synergy between tumor necrosis factor and interleukin-1 in the induction ofsickness behavior in mice. Psychoneuroendocrinology 19: 197-207.
6. Bonaccorso S, Metzer H, Maes M (2000). Psychological and behavioral effects ofinterferons. Curr Opin Psychiatry 13: 673-677.
7. Bowlby J (1969). Attachment. Attachment and Loss Vol. 1. Basic Books: New,York, NY.
8. Capuron L, Miller AH (2004). Cytokines and psychopathology: lessons fromInterferon-alpha. Biol Psychiatry 56: 819-824.
9. Carobrez SG, Gasparotto OC, Buwalda B, Bohus B (2002). Long-term consequencesof social stress on corticosterone and IL-1 levels in endotoxinchallengedrats. Physiol Behav 76: 99-105.
10. Carroll JE, Low CA, Prather AA, Cohen S, Fury JM, Ross DC, et al. (2011). Negativeaffective responses to a speech task predict changes in interleukin (IL)-6. BrainBehav Immun 25: 232-238.
11. Chiang JJ, Eisenberger NI, Seeman TE, Taylor SE (2012). Negative and competitivesocial interactions are related to heightened proinflammatory cytokine activity.Proc Natl Acad Sci 109: 1878-1882.
12. Cole SW (2006). The complexity of dynamic host networks. In: Complex SystemsScience In Biomedicine. Springer: US, 605-629.
13. Cole SW (2013). Social regulation of human gene expression: mechanisms andimplications for public health. Am. J. Public Health 103: S84-S92.
14. Cole SW (2014). Human social genomics. PLoS Genet 10: e1004601.
15. Cole SW, Hawkley LC, Arevalo JM, Sung CY, Rose RM, Cacioppo JT (2007).Social regulation of gene expression in human leukocytes. Genome Biol 8:R189.
16. Dantzer R (2001). Cytokine Induced sickness behavior: Mechanisms andimplications. Ann N Y Acad Sci 933: 222-234.
17. Dantzer R, Kelley KW (2007). Twenty years of research on cytokine-inducedsickness behavior. Brain Behav Immun 21: 153-160.
18. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008). Frominflammation to sickness and depression: when the immune system subjugatesthe brain. Nat Rev Neurosci 9: 46-57.
19. Dickerson SS, Gable SL, Irwin MR, Aziz N, Kemeny ME (2009). Social-evaluativethreat and proinflammatory cytokine regulation an experimental laboratoryinvestigation. Psychol Sci 20: 1237-1244.
20. Dickerson SS, Kemeny ME, Aziz N, Kim KH, Fahey JL (2004). Immunological effectsof induced shame and guilt. Psychosom Med 66: 124-131.
21. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, et al. (2010). A metaanalysisof cytokines in major depression. Biol Psychiatry 67: 446-457.
22. Eisenberger NI, Berkman ET, Inagaki TK, Rameson L, Mashal N, Irwin MR (2010a).Inflammation-induced anhedonia: Endotoxin reduces ventral striatum responsesto reward. Biol Psychiatry 68: 748-754.
23. Eisenberger NI, Cole SW (2012). Social neuroscience and health: neurophysiologicalmechanisms linking social ties with physical health. Nat Neurosci 15:669-674.
24. Eisenberger NI, Inagaki TK, Mashal NM, Irwin MR (2010b). Inflammation and socialexperience: an inflammatory challenge induces feelings of social disconnection inaddition to depressed mood. Brain Behav Immun 24: 558-563.
25. Eisenberger NI, Inagaki TK, Rameson L, Mashal NM, Irwin MR (2009). An fMRI studyof cytokine-induced depressed mood and social pain: the role of sex differences.Neuroimage 47: 881-890.
26. Eisenberger NI, Lieberman MD, Williams KD (2003). Does rejection hurt An fMRIstudy of social exclusion. Science 302: 290-292.
27. Ford ES, Loucks EB, Berkman LF (2006). Social integration and concentrations ofC-reactive protein among US adults. Ann Epidemiol 16: 78-84.
28. Fuligni AJ, Telzer EH, Bower J, Cole SW, Kiang L, Irwin MR (2009). A preliminarystudy of daily interpersonal stress and C-reactive protein levels amongadolescents from Latin American and European backgrounds. Psychosom Med71: 329-333.
29. Gibb J, Hayley S, Gandhi R, Poulter MO, Anisman H (2008). Synergistic and additiveactions of a psychosocial stressor and endotoxin challenge: circulating and braincytokines, plasma corticosterone and behavioral changes in mice. Brain BehavImmun 22: 573-589.
30. Goehler LE, Relton JK, Dripps D, Kiechle R, Tartaglia N, Maier SF, et al. (1997).Vagal paraganglia bind biotinylated interleukin-1 receptor antagonist: a possiblemechanism for immune-to-brain communication. Brain Res Bull 43: 357-364.
31. Hackett RA, Hamer M, Endrighi R, Brydon L, Steptoe A (2012). Loneliness andstress-related inflammatory and neuroendocrine responses in older menand women. Psychoneuroendocrinology 37: 1801-1809.
32. Hannestad J, DellaGioia N, Ortiz N, Pittman B, Bhagwagar Z (2011). Citalopramreduces endotoxin-induced fatigue. Brain Behav Immun 25: 256-259.
33. Hariri AR, Tessitore A, Mattay VS, Fera F, Weinberger DR (2002). The amygdalaresponse to emotional stimuli: a comparison of faces and scenes. Neuroimage17: 317-323.
34. Hart BL (1988). Biological basis of the behavior of sick animals. Neurosci BiobehavRev 12: 123-137.
35. Heffner KL, Waring ME, Roberts MB, Eaton CB, Gramling R (2011). Social isolation,C-reactive protein, and coronary heart disease mortality among communitydwellingadults. Social Sci Med 72: 1482-1488.
36. Heinrich LM, Gullone E (2006). The clinical significance of loneliness: aliterature review. Clin Psychol Rev 26: 695-718.
37. Hennessy MB, Deak T, Schiml PA (2014). Sociality and sickness: have cytokinesevolved to serve social functions beyond times of pathogen exposure BrainBehav Immun 37: 15-20.
38. Holt-Lunstad J, Smith TB, Layton JB (2010). Social relationships and mortality risk: ameta-analytic review. PLoS Med 7: e1000316.
39. Howren MB, Lamkin DM, Suls J (2009). Associations of depression with C-reactiveprotein, IL-1, and IL-6: A meta-analysis. Psychosom Med 71: 171-186.
40. Inagaki TK, Muscatell KA, Irwin MR, Cole S, Eisenberger NI (2012). Inflammationselectively enhances amygdala activity to socially threatening images. Neuroimage59: 3222-3226.
41. Inagaki TK, Muscatell KA, Moeini M, Dutcher J, Jevtic I, Irwin MR, et al. (2015). Therole of the ventral striatum in inflammatory-induced approach toward supportfigures. Brain Behav Immun 44: 247-252.
42. Irwin MR, Cole SW (2011). Reciprocal regulation of the neural and innate immunesystems. Nat Rev Immunol 11: 625-632.
43. Jaremka LM, Fagundes CP, Peng J, Bennett JM, Glaser R, Malarkey WB, et al.(2013). Loneliness promotes inflammation during acute stress. Psychol Sci 24:1089-1097.
44. Kelley KW, Bluthe RM, Dantzer R, Zhou JH, Shen WH, Johnson RW, et al. (2003).Cytokine-induced sickness behavior. Brain Behav Immun 17: S112-S118.
45. Maier SF, Watkins LR (1998). Cytokines for psychologists: Implications ofbidirectional immune-to-brain communication for understanding behavior, mood,and cognition. Psychol Rev 105: 83-107.
46. Miller AH, Maletic V, Raison CL (2009a). Inflammation and its discontents: the role ofcytokines in the pathophysiology of major depression. Biol Psychiatry 65:732-741.
47. Miller G, Rohleder N, Cole SW (2009b). Chronic interpersonal stress predictsactivation of pro-and anti-inflammatory signaling pathways six months later.Psychosom Med 71: 57-62.
48. Moieni M, Irwin MR, Jevtic I, Breen EC, Cho HJ, Arevalo JM, et al. (2015a).Trait sensitivity to social disconnection enhances pro-inflammatory responses to arandomized controlled trial of endotoxin. Psychoneuroendocrinology 62: 336-342.
49. Moieni M, Irwin MR, Jevtic I, Breen EC, Eisenberger NI (2015b). Inflammation impairssocial cognitive processing: a randomized controlled trial of endotoxin. BrainBehav Immun 48: 132-138.
50. Moieni M, Irwin MR, Jevtic I, Olmstead R, Breen EC, Eisenberger NI (2015c). Sexdifferences in depressive and socioemotional responses to an inflammatorychallenge: implications for sex differences in depression. Neuropsychopharmacology40: 1709-1716.
51. Monroe SM, Simons AD (1991). Diathesis-stress theories in the context of life stressresearch: implications for the depressive disorders. Psychol Bull 110: 406-425.
52. Moons WG, Eisenberger NI, Taylor SE (2010). Anger and fear responses to stresshave different biological profiles. Brain Behav Immun 24: 215-219.
53. Murphy ML, Slavich GM, Rohleder N, Miller GE (2013). Targeted rejection triggersdifferential pro-and anti-inflammatory gene expression in adolescents as afunction of social status. Clin Psychol Sci 1: 30-40.
54. Muscatell KA, Moieni M, Inagaki TK, Duthcher JM, Jevtic I, Breen EC, et al. (2016).Inflammation enhances neural sensitivity to negative and positive social feedback.Brain Behav Immun. (e-pub ahead of print).
55. Quan N, Avitsur R, Stark JL, He L, Shah M, Caligiuri M, et al. (2001). Social stressincreases the susceptibility to endotoxic shock. J. Neuroimmunol. 115: 36-45.
56. Quan N, Banks WA (2007). Brain-immune communication pathways. Brain BehavImmun 21: 727-735.
57. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC (1997). Pain affectencoded in human anterior cingulate but not somatosensory cortex. Science 277:968-971.
58. Raison CL, Capuron L, Miller AH (2006). Cytokines sing the blues: inflammation andthe pathogenesis of depression. Trends Immunol 27: 24-31.
59. Raison CL, Demetrashvili M, Capuron L, Miller AH (2005). Neuropsychiatric adverseeffects of Interferon-alpha: recognition and management. CNS Drugs 19: 105-123.
60. Raison CL, Miller AH (2011). Is depression an inflammatory disorder CurrPsychiatry Rep 13: 467-475.
61. Raison CL, Rutherford RE, Woolwine BJ, Shuo C, Schettler P, Drake DF, et al. (2013).A randomized controlled trial of the tumor necrosis factor antagonist infliximab fortreatment-resistant depression: the role of baseline inflammatory biomarkers.JAMA Psychiatry 70: 31-41.
62. Reichenberg A, Yirmiya R, Schuld A, Kraus T, Haack M, Morag A, et al. (2001).Cytokine-associated emotional and cognitive disturbances in humans. Arch GenPsychiatry 58: 445-452.
63. Schaller M, Miller GE, Gervais WM, Yager S, Chen E (2010). Mere visual perceptionof other people's disease symptoms facilitates a more aggressive immuneresponse. Psychological Sci 21: 649-652.
64. Schiepers OJG, Wichers MC, Maes M (2005). Cytokines and major depression.Prog Neuropsychopharmacol Biol Psychiatry 29: 201-217.
65. Schultze-Florey CR, Martínez-Maza O, Magpantay L, Breen EC, Irwin MR, Gündel Het al (2012). When grief makes you sick: bereavement induced systemicinflammation is a question of genotype. Brain Behav Immun 26: 1066-1071.
66. Shankar A, McMunn A, Banks J, Steptoe A (2011). Loneliness, social isolation, andbehavioral and biological health indicators in older adults. Health Psychology 30: 377.
67. Slavich GM, Cole SW (2013). The emerging field of human social genomics. ClinPsychological Sci 1: 331-348.
68. Slavich GM, Irwin MR (2014). From stress to inflammation and major depressivedisorder: a social signal transduction theory of depression. Psychol Bull 140: 774.
69. Slavich GM, Way BM, Eisenberger NI, Taylor SE (2010). Neural sensitivity to socialrejection is associated with inflammatory responses to social stress. Proc NatlAcad Sci 107: 14817-14822.
70. Sloan EK, Capitanio JP, Tarara RP, Mendoza SP, Mason WA, Cole SW (2007).Social stress enhances sympathetic innervation of primate lymph nodes:mechanisms and implications for viral pathogenesis. J Neurosci 27: 8857-8865.
71. Slopen N, Kubzansky LD, McLaughlin KA, Koenen KC (2013). Childhood adversityand inflammatory processes in youth: a prospective study. Psychoneuroendocrinology38: 188-200.
72. Steptoe A, Hamer M, Chida Y (2007). The effects of acute psychological stress oncirculating inflammatory factors in humans: a review and meta-analysis. BrainBehav Immun 21: 901-912.
73. Stevenson RJ, Hodgson D, Oaten MJ, Moussavi M, Langberg R, Case TI, et al.(2012). Disgust elevates core body temperature and up-regulates certain oralimmune markers. Brain Behav Immun 26: 1160-1168.
74. Willette AA, Lubach GR, Coe CL (2007). Environmental context differentially affectsbehavioral, leukocyte, cortisol, and interleukin-6 responses to low doses ofendotoxin in the rhesus monkey. Brain Behav Immun 21: 807-815.
75. Yamakawa K, Matsunaga M, Isowa T, Kimura K, Kasugai K, Yoneda M, et al. (2009).Transient responses of inflammatory cytokines in acute stress. Biol Psychol 82:25-32.
76. Yee JR, Prendergast BJ (2010). Sex-specific social regulation of inflammatoryresponses and sickness behaviors. Brain Behav Immun 24: 942-951.
77. Zhang WN, Chang SH, Guo LY, Zhang KL, Wang J (2013). The neural correlates ofreward-related processing in major depressive disorder: a meta-analysis offunctional magnetic resonance imaging studies. J Affect Disord 151: 531-539.