Altered populations of natural killer cells, cytotoxic T lymphocytes, and regulatory T cells in major depressive disorder: Association with sleep disturbance

Brain, Behavior, and Immunity

Volumn 66, Issue , 2017, Pages 193-200

  Suzuki, Hideo ^a,b   Savitz, Jonathan ^a,c   Kent Teague, T ^d,e,f   Gandhapudi, Siva K ^g   Tan, Chibing ^d   Misaki, Masaya ^a   McKinney, Brett A ^h   Irwin, Michael R ⁱ   Drevets, Wayne C ^j   Bodurka, Jerzy ^a,k  

^a LAUREATE INSTITUTE FOR BRAIN RESEARCH   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF TULSA   (United States)

^d UNIVERSITY OF OKLAHOMA   (United States)

^e UNIVERSITY OF OKLAHOMA COLLEGE OF PHARMACY   (United States)

^f OKLAHOMA STATE UNIVERSITY   (United States)

^g UNIVERSITY OF KENTUCKY   (United States)

^h The University of Tulsa   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j JOHNSON AND JOHNSON   (United States)

^k USA   (United States)

more..

Author keywords

CD8+ cells; Depression; Flow cytometry; Natural killer cells; Regulatory T cells; Sleep

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR4; INTERLEUKIN 7 RECEPTOR;

ADULT; ARTICLE; CD8+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DISEASE ASSOCIATION; EFFECTOR CELL; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; MEMORY T LYMPHOCYTE; NATURAL KILLER CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SLEEP DISORDER; COMPLICATION; FLOW CYTOMETRY; IMMUNOLOGY; PHYSIOLOGY;

ADULT; DEPRESSIVE DISORDER, MAJOR; FEMALE; FLOW CYTOMETRY; HUMANS; KILLER CELLS, NATURAL; MALE; SLEEP WAKE DISORDERS; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY;

EID: 85021066782     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2017.06.011     Document Type: Article

References (77)

1. Axelsson, J., Rehman, J.U., Akerstedt, T., Ekman, R., Miller, G.E., Hoglund, C.O., Lekander, M., Effects of sustained sleep restriction on mitogen-stimulated cytokines, chemokines and T helper 1/T helper 2 balance in humans. PLoS One, 8, 2013, e82291.
2. Backhaus, J., Junghanns, K., Broocks, A., Riemann, D., Hohagen, F., Test-retest reliability and validity of the Pittsburgh Sleep Quality Index in primary insomnia. J. Psychosom. Res. 53 (2002), 737–740.
3. Baglioni, C., Battagliese, G., Feige, B., Spiegelhalder, K., Nissen, C., Voderholzer, U., Lombardo, C., Riemann, D., Insomnia as a predictor of depression: a meta-analytic evaluation of longitudinal epidemiological studies. J. Affect. Disord. 135 (2011), 10–19.
4. Blume, J., Douglas, S.D., Evans, D.L., Immune suppression and immune activation in depression. Brain Behav. Immun. 25 (2011), 221–229.
5. Buysse, D.J., Reynolds, C.F. 3rd, Monk, T.H., Berman, S.R., Kupfer, D.J., The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 28 (1989), 193–213.
6. Cho, H.J., Lavretsky, H., Olmstead, R., Levin, M.J., Oxman, M.N., Irwin, M.R., Sleep disturbance and depression recurrence in community-dwelling older adults: a prospective study. Am. J. Psychiatry 165 (2008), 1543–1550.
7. Cohen, H., Ziv, Y., Cardon, M., Kaplan, Z., Matar, M.A., Gidron, Y., Schwartz, M., Kipnis, J., Maladaptation to mental stress mitigated by the adaptive immune system via depletion of naturally occurring regulatory CD4+CD25+ cells. J. Neurobiol. 66 (2006), 552–563.
8. Cohen, S., Doyle, W.J., Alper, C.M., Janicki-Deverts, D., Turner, R.B., Sleep habits and susceptibility to the common cold. Arch. Intern. Med. 169 (2009), 62–67.
9. Cooper, M.A., Fehniger, T.A., Caligiuri, M.A., The biology of human natural killer-cell subsets. Trends Immunol. 22 (2001), 633–640.
10. Cosyns, P., Maes, M., Vandewoude, M., Stevens, W.J., De Clerck, L.S., Schotte, C., Impaired mitogen-induced lymphocyte responses and the hypothalamic-pituitary-adrenal axis in depressive disorders. J. Affect. Disord. 16 (1989), 41–48.
11. Cover, H., Irwin, M., Immunity and depression: insomnia, retardation, and reduction of natural killer cell activity. J. Behav. Med. 17 (1994), 217–223.
12. Darrow, S.M., Verhoeven, J.E., Revesz, D., Lindqvist, D., Penninx, B.W., Delucchi, K.L., Wolkowitz, O.M., Mathews, C.A., The association between psychiatric disorders and telomere length: a meta-analysis involving 14,827 persons. Psychosom. Med. 78 (2016), 776–787.
13. Dhabhar, F.S., Effects of stress on immune function: the good, the bad, and the beautiful. Immunol. Res. 58 (2014), 193–210.
14. Dhabhar, F.S., McEwen, B.S., Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav. Immun. 11 (1997), 286–306.
15. Evans, D.L., Ten Have, T.R., Douglas, S.D., Gettes, D.R., Morrison, M., Chiappini, M.S., Brinker-Spence, P., Job, C., Mercer, D.E., Wang, Y.L., Cruess, D., Dube, B., Dalen, E.A., Brown, T., Bauer, R., Petitto, J.M., Association of depression with viral load, CD8 T lymphocytes, and natural killer cells in women with HIV infection. Am. J. Psychiatry 159 (2002), 1752–1759.
16. First, M., Structured Clinical Interview for DSM-IV-TR Axis I Disorders – Non-Patient Edition (SCID-I/NP). 2010, Biometrics Research Department, New York State Psychiatric Institute, New York, NY.
17. Fondell, E., Axelsson, J., Franck, K., Ploner, A., Lekander, M., Balter, K., Gaines, H., Short natural sleep is associated with higher T cell and lower NK cell activities. Brain Behav. Immun. 25 (2011), 1367–1375.
18. Frank, M.G., Wieseler Frank, J.L., Hendricks, S.E., Burke, W.J., Johnson, D.R., Age at onset of major depressive disorder predicts reductions in NK cell number and activity. J. Affect. Disord. 71 (2002), 159–167.
19. Fu, B., Li, X., Sun, R., Tong, X., Ling, B., Tian, Z., Wei, H., Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), E231–240.
20. Glaser, R., Kiecolt-Glaser, J.K., Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol. 5 (2005), 243–251.
21. Gold, S.M., Kruger, S., Ziegler, K.J., Krieger, T., Schulz, K.H., Otte, C., Heesen, C., Endocrine and immune substrates of depressive symptoms and fatigue in multiple sclerosis patients with comorbid major depression. J. Neurol. Neurosurg. Psychiatry 82 (2011), 814–818.
22. Grosse, L., Carvalho, L.A., Birkenhager, T.K., Hoogendijk, W.J., Kushner, S.A., Drexhage, H.A., Bergink, V., Circulating cytotoxic T cells and natural killer cells as potential predictors for antidepressant response in melancholic depression. Restoration of T regulatory cell populations after antidepressant therapy. Psychopharmacology 233 (2016), 1679–1688.
23. Grosse, L., Hoogenboezem, T., Ambree, O., Bellingrath, S., Jorgens, S., de Wit, H.J., Wijkhuijs, A.M., Arolt, V., Drexhage, H.A., Deficiencies of the T and natural killer cell system in major depressive disorder: T regulatory cell defects are associated with inflammatory monocyte activation. Brain Behav. Immun. 54 (2016), 38–44.
24. Irwin, M.R., Human psychoneuroimmunology: 20 years of discovery. Brain Behav. Immun. 22 (2008), 129–139.
25. Irwin, M.R., Why sleep is important for health: a psychoneuroimmunology perspective. Annu. Rev. Psychol. 66 (2015), 143–172.
26. Irwin, M.R., Cole, S.W., Reciprocal regulation of the neural and innate immune systems. Nat. Rev. Immunol. 11 (2011), 625–632.
27. Irwin, M.R., Miller, A.H., Depressive disorders and immunity: 20 years of progress and discovery. Brain Behav. Immun. 21 (2007), 374–383.
28. Irwin, M., Mascovich, A., Gillin, J.C., Willoughby, R., Pike, J., Smith, T.L., Partial sleep deprivation reduces natural killer cell activity in humans. Psychosom. Med. 56 (1994), 493–498.
29. Irwin, M., McClintick, J., Costlow, C., Fortner, M., White, J., Gillin, J.C., Partial night sleep deprivation reduces natural killer and cellular immune responses in humans. Faseb J. 10 (1996), 643–653.
30. Irwin, M., Costlow, C., Williams, H., Artin, K.H., Chan, C.Y., Stinson, D.L., Levin, M.J., Hayward, A.R., Oxman, M.N., Cellular immunity to varicella-zoster virus in patients with major depression. J. Infect. Dis. 178:Suppl. 1 (1998), S104–108.
31. Irwin, M.R., Levin, M.J., Laudenslager, M.L., Olmstead, R., Lucko, A., Lang, N., Carrillo, C., Stanley, H.A., Caulfield, M.J., Weinberg, A., Chan, I.S., Clair, J., Smith, J.G., Marchese, R.D., Williams, H.M., Beck, D.J., McCook, P.T., Zhang, J.H., Johnson, G., Oxman, M.N., Varicella zoster virus-specific immune responses to a herpes zoster vaccine in elderly recipients with major depression and the impact of antidepressant medications. Clin. Infect. Dis. 56 (2013), 1085–1093.
32. Irwin, M.R., Olmstead, R., Carrillo, C., Sadeghi, N., Nicassio, P., Ganz, P.A., Bower, J.E., Tai Chi Chih compared with cognitive behavioral therapy for the treatment of insomnia in survivors of breast cancer: a randomized, partially blinded, noninferiority trial. J. Clin. Oncol., 2017 JCO2016710285.
33. Kiecolt-Glaser, J.K., Glaser, R., Gravenstein, S., Malarkey, W.B., Sheridan, J., Chronic stress alters the immune response to influenza virus vaccine in older adults. Proc. Natl. Acad. Sci. U.S.A. 93 (1996), 3043–3047.
34. Kim, J., Kim, A.R., Shin, E.C., Cytomegalovirus infection and memory T cell inflation. Immune Netw. 15 (2015), 186–190.
35. Kipnis, J., Cardon, M., Avidan, H., Lewitus, G.M., Mordechay, S., Rolls, A., Shani, Y., Schwartz, M., Dopamine, through the extracellular signal-regulated kinase pathway, downregulates CD4+CD25+ regulatory T-cell activity: implications for neurodegeneration. J. Neurosci. 24 (2004), 6133–6143.
36. Kipnis, J., Cohen, H., Cardon, M., Ziv, Y., Schwartz, M., T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc. Natl. Acad. Sci. U.S.A. 101 (2004), 8180–8185.
37. Koch, S., Larbi, A., Ozcelik, D., Solana, R., Gouttefangeas, C., Attig, S., Wikby, A., Strindhall, J., Franceschi, C., Pawelec, G., Cytomegalovirus infection: a driving force in human T cell immunosenescence. Ann. N.Y. Acad. Sci. 1114 (2007), 23–35.
38. Lang, A., Brien, J.D., Nikolich-Zugich, J., Inflation and long-term maintenance of CD8 T cells responding to a latent herpesvirus depend upon establishment of latency and presence of viral antigens. J. Immunol. 183 (2009), 8077–8087.
39. Lange, T., Dimitrov, S., Born, J., Effects of sleep and circadian rhythm on the human immune system. Ann. N.Y. Acad. Sci. 1193 (2010), 48–59.
40. Laroni, A., Gandhi, R., Beynon, V., Weiner, H.L., IL-27 imparts immunoregulatory function to human NK cell subsets. PLoS One, 6, 2011, e26173.
41. Lee, E., Cho, H.J., Olmstead, R., Levin, M.J., Oxman, M.N., Irwin, M.R., Persistent sleep disturbance: a risk factor for recurrent depression in community-dwelling older adults. Sleep 36 (2013), 1685–1691.
42. Leserman, J., Role of depression, stress, and trauma in HIV disease progression. Psychosom. Med. 70 (2008), 539–545.
43. Li, Y., Xiao, B., Qiu, W., Yang, L., Hu, B., Tian, X., Yang, H., Altered expression of CD4(+)CD25(+) regulatory T cells and its 5-HT(1a) receptor in patients with major depression disorder. J. Affect. Disord. 124 (2010), 68–75.
44. Maecker, H.T., McCoy, J.P., Nussenblatt, R., Standardizing immunophenotyping for the Human Immunology Project. Nat. Rev. Immunol. 12 (2012), 191–200.
45. Maes, M., Meltzer, H.Y., Stevens, W., Calabrese, J., Cosyns, P., Natural killer cell activity in major depression: relation to circulating natural killer cells, cellular indices of the immune response, and depressive phenomenology. Prog. Neuropsychopharmacol. Biol. Psychiatry 18 (1994), 717–730.
46. Mechawar, N., Savitz, J., Neuropathology of mood disorders: do we see the stigmata of inflammation?. Transl. Psychiatry, 6, 2016, e946.
47. Michel, T., Poli, A., Cuapio, A., Briquemont, B., Iserentant, G., Ollert, M., Zimmer, J., Human CD56 bright NK cells: an update. J. Immunol. 196 (2016), 2923–2931.
48. Miller, A.H., Depression and immunity: a role for T cells?. Brain Behav. Immun. 24 (2010), 1–8.
49. Miller, G.E., Cohen, S., Herbert, T.B., Pathways linking major depression and immunity in ambulatory female patients. Psychosom. Med. 61 (1999), 850–860.
50. Miller, G.E., Cohen, S., Pressman, S., Barkin, A., Rabin, B.S., Treanor, J.J., Psychological stress and antibody response to influenza vaccination: when is the critical period for stress, and how does it get inside the body?. Psychosom. Med. 66 (2004), 215–223.
51. Morandi, F., Horenstein, A.L., Chillemi, A., Quarona, V., Chiesa, S., Imperatori, A., Zanellato, S., Mortara, L., Gattorno, M., Pistoia, V., Malavasi, F., CD56brightCD16- NK cells produce adenosine through a CD38-mediated pathway and act as regulatory cells inhibiting autologous CD4+ T cell proliferation. J. Immunol. 195 (2015), 965–972.
52. Moretta, L., Ferlazzo, G., Bottino, C., Vitale, M., Pende, D., Mingari, M.C., Moretta, A., Effector and regulatory events during natural killer-dendritic cell interactions. Immunol. Rev. 214 (2006), 219–228.
53. O'Hara, G.A., Welten, S.P., Klenerman, P., Arens, R., Memory T cell inflation: understanding cause and effect. Trends Immunol. 33 (2012), 84–90.
54. Pavon, L., Sandoval-Lopez, G., Eugenia Hernandez, M., Loria, F., Estrada, I., Perez, M., Moreno, J., Avila, U., Leff, P., Anton, B., Heinze, G., Th2 cytokine response in major depressive disorder patients before treatment. J. Neuroimmunol. 172 (2006), 156–165.
55. Petrovsky, N., Harrison, L.C., Diurnal rhythmicity of human cytokine production: a dynamic disequilibrium in T helper cell type 1/T helper cell type 2 balance?. J. Immunol. 158 (1997), 5163–5168.
56. Prather, A.A., Hall, M., Fury, J.M., Ross, D.C., Muldoon, M.F., Cohen, S., Marsland, A.L., Sleep and antibody response to hepatitis B vaccination. Sleep 35 (2012), 1063–1069.
57. Prather, A.A., Janicki-Deverts, D., Hall, M.H., Cohen, S., Behaviorally assessed sleep and susceptibility to the common cold. Sleep 38 (2015), 1353–1359.
58. Prather, A.A., Janicki-Deverts, D., Adler, N.E., Hall, M., Cohen, S., Sleep habits and susceptibility to upper respiratory illness: the moderating role of subjective socioeconomic status. Ann. Behav. Med. 51 (2017), 137–146.
59. Redwine, L., Dang, J., Hall, M., Irwin, M., Disordered sleep, nocturnal cytokines, and immunity in alcoholics. Psychosom. Med. 65 (2003), 75–85.
60. Ronaldson, A., Gazali, A.M., Zalli, A., Kaiser, F., Thompson, S.J., Henderson, B., Steptoe, A., Carvalho, L., Increased percentages of regulatory T cells are associated with inflammatory and neuroendocrine responses to acute psychological stress and poorer health status in older men and women. Psychopharmacology 233 (2016), 1661–1668.
61. Sakami, S., Ishikawa, T., Kawakami, N., Haratani, T., Fukui, A., Kobayashi, F., Fujita, O., Araki, S., Kawamura, N., Coemergence of insomnia and a shift in the Th1/Th2 balance toward Th2 dominance. NeuroImmunomodulation 10 (2002), 337–343.
62. Sallusto, F., Geginat, J., Lanzavecchia, A., Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22 (2004), 745–763.
63. Saul, A.N., Oberyszyn, T.M., Daugherty, C., Kusewitt, D., Jones, S., Jewell, S., Malarkey, W.B., Lehman, A., Lemeshow, S., Dhabhar, F.S., Chronic stress and susceptibility to skin cancer. J. Natl. Cancer Inst. 97 (2005), 1760–1767.
64. Savitz, J.B., Drevets, W.C., Neuroreceptor imaging in depression. Neurobiol. Dis. 52 (2013), 49–65.
65. Savitz, J., Tan, C., Taylor, A., Drevets, W., Teague, K., Abnormalities in regulatory T cells and natural killer cells in major depressive disorder. J. Immunol., 190(43), 2013, 25.
66. Schepis, D., Gunnarsson, I., Eloranta, M.L., Lampa, J., Jacobson, S.H., Karre, K., Berg, L., Increased proportion of CD56bright natural killer cells in active and inactive systemic lupus erythematosus. Immunology 126 (2009), 140–146.
67. Schwartz, M., Kipnis, J., Autoimmunity on alert: naturally occurring regulatory CD4(+)CD25(+) T cells as part of the evolutionary compromise between a ‘need’ and a ‘risk’. Trends Immunol. 23 (2002), 530–534.
68. Schwartz, M., Kipnis, J., Protective autoimmunity and neuroprotection in inflammatory and noninflammatory neurodegenerative diseases. J. Neurol. Sci. 233 (2005), 163–166.
69. Segerstrom, S.C., Hardy, J.K., Evans, D.R., Greenberg, R.N., Vulnerability, distress, and immune response to vaccination in older adults. Brain Behav. Immun. 26 (2012), 747–753.
70. Sephton, S.E., Dhabhar, F.S., Keuroghlian, A.S., Giese-Davis, J., McEwen, B.S., Ionan, A.C., Spiegel, D., Depression, cortisol, and suppressed cell-mediated immunity in metastatic breast cancer. Brain Behav. Immun. 23 (2009), 1148–1155.
71. Snyder, C.M., Cho, K.S., Bonnett, E.L., van Dommelen, S., Shellam, G.R., Hill, A.B., Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29 (2008), 650–659.
72. Spiegel, K., Sheridan, J.F., Van Cauter, E., Effect of sleep deprivation on response to immunization. JAMA 288 (2002), 1471–1472.
73. Toben, C., Baune, B.T., An act of balance between adaptive and maladaptive immunity in depression: a role for T lymphocytes. J. Neuroimmune Pharmacol. 10 (2015), 595–609.
74. Vadasz, Z., Haj, T., Kessel, A., Toubi, E., Age-related autoimmunity. BMC Med., 11, 2013, 94.
75. Verhoeven, J.E., Revesz, D., Epel, E.S., Lin, J., Wolkowitz, O.M., Penninx, B.W., Major depressive disorder and accelerated cellular aging: results from a large psychiatric cohort study. Mol. Psychiatry 19 (2014), 895–901.
76. Williams, J.B., Kobak, K.A., Development and reliability of a structured interview guide for the Montgomery Asberg Depression Rating Scale (SIGMA). Br. J. Psychiatry 192 (2008), 52–58.
77. Zorrilla, E.P., Luborsky, L., McKay, J.R., Rosenthal, R., Houldin, A., Tax, A., McCorkle, R., Seligman, D.A., Schmidt, K., The relationship of depression and stressors to immunological assays: a meta-analytic review. Brain Behav. Immun. 15 (2001), 199–226.