Sleep-deprivation reduces NK cell number and function mediated by β-adrenergic signalling

Psychoneuroendocrinology

Volumn 57, Issue , 2015, Pages 134-143

  De Lorenzo, Beatriz H P ^a,b   de Oliveira Marchioro, Laís ^a   Greco, Carollina Ribeiro ^a   Suchecki, Deborah ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b Centro Universitario Sao Camilo   (Brazil)

Author keywords

Cytotoxicity; Murine melanoma; NK cells; Sleep deprivation; Stress; 2 Adrenergic receptor

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CORTICOSTERONE; DEXAMETHASONE; PROPRANOLOL; BETA ADRENERGIC RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; CYTOTOXICITY; IN VITRO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MALE; MELANOMA CELL; MOUSE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REM SLEEP DEPRIVATION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; DISEASE MODEL; EXPERIMENTAL MELANOMA; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; SLEEP DEPRIVATION;

ANIMALS; DISEASE MODELS, ANIMAL; KILLER CELLS, NATURAL; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; RECEPTORS, ADRENERGIC, BETA; SLEEP DEPRIVATION; STRESS, PHYSIOLOGICAL;

EID: 84929333997     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.04.006     Document Type: Article

References (87)

1. Ananias R.Z., Rodrigues E.G., Braga E.G., Squaiella C.C., Mussalem J.S., Longhini A.L., Travassos L.R., Longo-Maugéri I.M. Modulatory effect of killed Propionibacterium acnes and its purified soluble polysaccharide on peritoneal exudate cells from C57Bl/6 mice: major NKT cell recruitment and increased cytotoxicity. Scand. J. Immunol. 2007, 65:538-548.
2. Avitsur R., Maayan R., Weizman A. Neonatal stress modulates sickness behavior: role for proinflammatory cytokines. J. Neuroimmunol. 2013, 257:59-66.
3. Barnes P.J. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin. Sci. (Lond.) 1998, 94:557-572.
4. Ben-Eliyahu S., Page G.G., Yirmiya R., Shakhar G. Evidence that stress and surgical interventions promote tumour development by suppressing natural killer cell activity. Int. J. Cancer 1999, 80:880-888.
5. Benschop R.J., Rodriguez-Feuerhahn M., Schedlowski M. Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav. Immun. 1996, 10:77-91.
6. Bollinger T., Bollinger A., Skrum L., Dimitrov S., Lange T., Solbach W. Sleep-dependent activity of T cells and regulatory T cells. Clin. Exp. Immunol. 2009, 155:231-238.
7. Born J., Lange T., Hansen K., Mölle M., Fehm H.L. Effects of sleep and circadian rhythm on human circulating immune cells. J. Immunol. 1997, 158:4454-4464.
8. Bush K.A., Krukowski K., Eddy J.L., Janusek L.W., Mathews H.L. Glucocorticoid receptor mediated suppression of natural killer cell activity: identification of associated deacetylase and corepressor molecules. Cell. Immunol. 2012, 275:80-89.
9. Campos-Rodríguez R., Godínez-Victoria M., Abarca-Rojano E., Pacheco-Yépez J., Reyna-Garfias H., Barbosa-Cabrera R.E., Drago-Serrano M.E. Stress modulates intestinal secretory immunoglobulin A. Front. Integr. Neurosci. 2013, 7:86.
10. Cermakian N., Lange T., Golombek D., Sarkar D., Nakao A., Shibata S., Mazzoccoli G. Crosstalk between the circadian clock circuitry and the immune system. Chronobiol. Int. 2013, 30:870-888.
11. Chen D., Rothenberg E.V. Interleukin 2 transcription factors as molecular targets of cAMP inhibition: delayed inhibition kinetics and combinatorial transcription roles. J. Exp. Med. 1994, 179:931-942.
12. Dhabhar F.S., Malarkey W.B., Neri E., McEwen B.S. Stress-induced redistribution of immune cells - from barracks to boulevards to battlefields: a tale of three hormones - Curt Richter Award winner. Psychoneuroendocrinology 2012, 37:1345-1368.
13. Dimitrov S., Lange T., Born J. Selective mobilization of cytotoxic leukocytes by epinephrine. J. Immunol. 2010, 184:503-511.
14. Elenkov I.J., Chrousos G.P. Stress system - organization, physiology and immunoregulation. Neuroimmunomodulation 2006, 13:257-267.
15. Fadda P., Fratta W. Stress-induced sleep deprivation modifies corticotropin releasing factor (CRF) levels and CRF binding in rat brain and pituitary. Pharmacol. Res. 1997, 35:443-446.
16. Fondell E., Axelsson J., Franck K., Ploner A., Lekander M., Bälter K., Gaines H. Short natural sleep is associated with higher T cell and lower NK cell activities. Brain Behav. Immun. 2011, 25:1367-1375.
17. Foster R.G., Kreitzman L. The rhythms of life - what your body clock means to you. Exp. Physiol. 2013, 99(4):599-606.
18. Frank M.G., Miguel Z.D., Watkins L.R., Maier S.F. Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav. Immun. 2010, 24:19-30.
19. Galvão M.e.O., Sinigaglia-Coimbra R., Kawakami S.E., Tufik S., Suchecki D. Paradoxical sleep deprivation activates hypothalamic nuclei that regulate food intake and stress response. Psychoneuroendocrinology 2009, 34:1176-1183.
20. Gandhi A.K., Kang J., Capone L., Parton A., Wu L., Zhang L.H., Mendy D., Lopez-Girona A., Tran T., Sapinoso L., Fang W., Xu S., Hampton G., Bartlett J.B., Schafer P. Dexamethasone synergizes with lenalidomide to inhibit multiple myeloma tumour growth, but reduces lenalidomide-induced immunomodulation of T and NK cell function. Curr. Cancer Drug Targets 2010, 10:155-167.
21. Gapstur S.M., Diver W.R., Stevens V.L., Carter B.D., Teras L.R., Jacobs E.J. Work schedule, sleep duration, insomnia, and risk of fatal prostate cancer. Am. J. Prev. Med. 2014, 46:S26-S33.
22. Glac W., Borman A., Badtke P., Stojek W., Orlikowska A., Tokarski J. Amphetamine enhances natural killer cytotoxic activity via beta-adrenergic mechanism. J. Physiol. Pharmacol. 2006, 57(Suppl. 11):125-132.
23. Glasner A., Avraham R., Rosenne E., Benish M., Zmora O., Shemer S., Meiboom H., Ben-Eliyahu S. Improving survival rates in two models of spontaneous postoperative metastasis in mice by combined administration of a beta-adrenergic antagonist and a cyclooxygenase-2 inhibitor. J. Immunol. 2010, 184:2449-2457.
24. Goldfarb Y., Benish M., Rosenne E., Melamed R., Levi B., Glasner A., Ben-Eliyahu S. CpG-C oligodeoxynucleotides limit the deleterious effects of beta-adrenoceptor stimulation on NK cytotoxicity and metastatic dissemination. J. Immunother. 2009, 32:280-291.
25. Goldfarb Y., Sorski L., Benish M., Levi B., Melamed R., Ben-Eliyahu S. Improving postoperative immune status and resistance to cancer metastasis: a combined perioperative approach of immunostimulation and prevention of excessive surgical stress responses. Ann. Surg. 2011, 253:798-810.
26. Gotlieb N., Rosenne E., Matzner P., Shaashua L., Sorski L., Ben-Eliyahu S. The misleading nature of in vitro and ex vivo findings in studying the impact of stress hormones on NK cell cytotoxicity. Brain Behav. Immun. 2015, 45:277-286.
27. Goujon E., Parnet P., Laye S., Combe C., Kelley K.W., Dantzer R. Stress downregulates lipopolysaccharide-induced expression of proinflammatory cytokines in the spleen, pituitary, and brain of mice. Brain Behav. Immun. 1995, 9:292-303.
28. Grundy A., Richardson H., Burstyn I., Lohrisch C., Sengupta S.K., Lai A.S., Lee D., Spinelli J.J., Aronson K.J. Increased risk of breast cancer associated with long-term shift work in Canada. Occup. Environ. Med. 2013, 70(12):831-838.
29. Guariniello L.D., Vicari P., Lee K.S., de Oliveira A.C., Tufik S. Bone marrow and peripheral white blood cells number is affected by sleep deprivation in a murine experimental model. J. Cell. Physiol. 2012, 227:361-366.
30. Guo W., Li P., Zhao G., Fan H., Hu Y., Hou Y. Glucocorticoid receptor mediates the effect of progesterone on uterine natural killer cells. Am. J. Reprod. Immunol. 2012, 67:463-473.
31. Haack M., Schuld A., Kraus T., Pollmächer T. Effects of sleep on endotoxin-induced host responses in healthy men. Psychosom. Med. 2001, 63:568-578.
32. Hahm B.J., Jo B., Dhabhar F.S., Palesh O., Aldridge-Gerry A., Bajestan S.N., Neri E., Nouriani B., Spiegel D., Zeitzer J.M. Bedtime misalignment and progression of breast cancer. Chronobiol. Int. 2013, 31(2):214-221.
33. Hakim F., Wang Y., Zhang S.X., Zheng J., Yolcu E.S., Carreras A., Khalyfa A., Shirwan H., Almendros I., Gozal D. Fragmented sleep accelerates tumour growth and progression through recruitment of tumour-associated macrophages and TLR4 signaling. Cancer Res. 2014, 74:1329-1337.
34. Hasegawa H., Yamashita K., Otubo D., Fujii S., Kamigaki T., Kuroda D., Kakeji Y. Allogeneic DCG promote lung NK cell activation and antitumour effect after invariant NKT cell activation. Anticancer Res. 2014, 34:3411-3417.
35. Hirotsu C., Rydlewski M., Araújo M.S., Tufik S., Andersen M.L. Sleep loss and cytokines levels in an experimental model of psoriasis. PLoS ONE 2012, 7:e51183.
36. Hoevenaar-Blom M.P., Spijkerman A.M., Kromhout D., van den Berg J.F., Verschuren W.M. Sleep duration and sleep quality in relation to 12-year cardiovascular disease incidence: the MORGEN study. Sleep 2011, 34:1487-1492.
37. Hou N., Zhang X., Zhao L., Zhao X., Li Z., Song T., Huang C. A novel chronic stress-induced shift in the Th1 to Th2 response promotes colon cancer growth. Biochem. Biophys. Res. Commun. 2013, 439:471-476.
38. Inbar S., Neeman E., Avraham R., Benish M., Rosenne E., Ben-Eliyahu S. Do stress responses promote leukemia progression? An animal study suggesting a role for epinephrine and prostaglandin-E2 through reduced NK activity. PLoS ONE 2011, 6:e19246.
39. 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. 1994, 56:493-498.
40. 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. 1996, 10:643-653.
41. Kim H.R., Moon S., Lee H.K., Kang J.L., Oh S., Seoh J.Y. Immune dysregulation in chronic stress: a quantitative and functional assessment of regulatory T cells. Neuroimmunomodulation 2012, 19:187-194.
42. Koban M., Le W.W., Hoffman G.E. Changes in hypothalamic corticotropin-releasing hormone, neuropeptide Y, and proopiomelanocortin gene expression during chronic rapid eye movement sleep deprivation of rats. Endocrinology 2006, 147:421-431.
43. Krukowski K., Eddy J., Kosik K.L., Konley T., Janusek L.W., Mathews H.L. Glucocorticoid dysregulation of natural killer cell function through epigenetic modification. Brain Behav. Immun. 2011, 25:239-249.
44. Lange T., Perras B., Fehm H.L., Born J. Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom. Med. 2003, 65:831-835.
45. Lehrer S., Green S., Ramanathan L., Rosenzweig K.E. Insufficient sleep associated with increased breast cancer mortality. Sleep Med. 2013, 14:469.
46. Leposavić G., Pilipović I., Radojević K., Pesić V., Perisić M., Kosec D. Catecholamines as immunomodulators: a role for adrenoceptor-mediated mechanisms in fine tuning of T-cell development. Auton. Neurosci. 2008, 144:1-12.
47. Leproult R., Copinschi G., Buxton O., Van Cauter E. Sleep loss results in an elevation of cortisol levels the next evening. Sleep 1997, 20:865-870.
48. Levi B., Benish M., Goldfarb Y., Sorski L., Melamed R., Rosenne E., Ben-Eliyahu S. Continuous stress disrupts immunostimulatory effects of IL-12. Brain Behav. Immun. 2011, 25:727-735.
49. Liu L., Fiorentino L., Natarajan L., Parker B.A., Mills P.J., Sadler G.R., Dimsdale J.E., Rissling M., He F., Ancoli-Israel S. Pre-treatment symptom cluster in breast cancer patients is associated with worse sleep, fatigue and depression during chemotherapy. Psychooncology 2009, 18:187-194.
50. Machado R.B., Tufik S., Suchecki D. Chronic stress during paradoxical sleep deprivation increases paradoxical sleep rebound: association with prolactin plasma levels and brain serotonin content. Psychoneuroendocrinology 2008, 33:1211-1224.
51. Maragno-Correa J.M., Patti C.L., Zanin K.A., Wuo-Silva R., Ruiz F.S., Zager A., Sá-Nunes A., Tufik S., Andersen M.L., Frussa-Filho R. Sleep deprivation increases mortality in female mice bearing Ehrlich ascitic tumour. Neuroimmunomodulation 2013, 20:134-140.
52. Marchetti B., Morale M.C., Paradis P., Bouvier M. Characterization, expression, and hormonal control of a thymic beta 2-adrenergic receptor. Am. J. Physiol. 1994, 267:E718-E731.
53. Melamed R., Rosenne E., Shakhar K., Schwartz Y., Abudarham N., Ben-Eliyahu S. Marginating pulmonary-NK activity and resistance to experimental tumour metastasis: suppression by surgery and the prophylactic use of a beta-adrenergic antagonist and a prostaglandin synthesis inhibitor. Brain Behav. Immun. 2005, 19:114-126.
54. Meron G., Tishler Y., Shaashua L., Rosenne E., Levi B., Melamed R., Gotlieb N., Matzner P., Sorski L., Ben-Eliyahu S. PGE2 suppresses NK activity in vivo directly and through adrenal hormones: effects that cannot be reflected by ex vivo assessment of NK cytotoxicity. Brain Behav. Immun. 2013, 28:128-138.
55. Mhatre S., Madkaikar M., Ghosh K., Desai M., Pujari V., Gupta M. Rapid flow cytometry based cytotoxicity assay for evaluation of NK cell function. Indian J. Exp. Biol. 2014, 52:983-988.
56. Molina P.E. Neurobiology of the stress response: contribution of the sympathetic nervous system to the neuroimmune axis in traumatic injury. Shock 2005, 24:3-10.
57. Munck A., Guyre P.M., Holbrook N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 1984, 5:25-44.
58. Ochoa-Cortes F., Guerrero-Alba R., Valdez-Morales E.E., Spreadbury I., Barajas-Lopez C., Castro M., Bertrand J., Cenac N., Vergnolle N., Vanner S.J. Chronic stress mediators act synergistically on colonic nociceptive mouse dorsal root ganglia neurons to increase excitability. Neurogastroenterol. Motil. 2014, 26:334-345.
59. Omne-Pontén M., Holmberg L., Burns T., Adami H.O., Bergström R. Determinants of the psycho-social outcome after operation for breast cancer Results of a prospective comparative interview study following mastectomy and breast conservation. Eur. J. Cancer 1992, 28A:1062-1067.
60. Oztürk L., Pelin Z., Karadeniz D., Kaynak H., Cakar L., Gözükirmizi E. Effects of 48hours sleep deprivation on human immune profile. Sleep Res. Online 1999, 2:107-111.
61. Palesh O., Peppone L., Innominato P.F., Janelsins M., Jeong M., Sprod L., Savard J., Rotatori M., Kesler S., Telli M., Mustian K. Prevalence, putative mechanisms, and current management of sleep problems during chemotherapy for cancer. Nat. Sci. Sleep 2012, 4:151-162.
62. Petrov M.E., Kim Y., Lauderdale D., Lewis C.E., Reis J.P., Carnethon M.R., Knutson K., Glasser S.J. Longitudinal associations between objective sleep and lipids: the CARDIA Study. Sleep 2013, 36:1587-1595.
63. Pilipović I., Radojević K., Perišić M., Leposavić G. Glucocorticoid-catecholamine interplay within the composite thymopoietic regulatory network. Ann. N. Y. Acad. Sci. 2012, 1261:34-41.
64. Redwine L., Hauger R.L., Gillin J.C., Irwin M. Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in humans. J. Clin. Endocrinol. Metab. 2000, 85:3597-3603.
65. Rosenne E., Sorski L., Shaashua L., Neeman E., Matzner P., Levi B., Ben-Eliyahu S. In vivo suppression of NK cell cytotoxicity by stress and surgery: glucocorticoids have a minor role compared to catecholamines and prostaglandins. Brain Behav. Immun. 2013, 37:207-219.
66. Ruiz F.S., Andersen M.L., Zager A., Martins R.C., Tufik S. Sleep deprivation reduces the lymphocyte count in a non-obese mouse model of type 1 diabetes mellitus. Braz. J. Med. Biol. Res. 2007, 40:633-637.
67. Sadegh L., Chen P.W., Brown J.R., Han Z., Niederkorn J.Y. NKT cells act through third party bone marrow-derived cells to suppress NK cell activity in the liver and exacerbate hepatic melanoma metastases. Int. J. Cancer 2015, 10.1002/ijc.29480.
68. Sanders V.M. The beta2-adrenergic receptor on T and B lymphocytes: do we understand it yet?. Brain Behav. Immun. 2012, 26:195-200.
69. Shakhar G., Ben-Eliyahu S. In vivo beta-adrenergic stimulation suppresses natural killer activity and compromises resistance to tumour metastasis in rats. J. Immunol. 1998, 160:3251-3258.
70. Smith J.W., Steiner A.L., Newberry W.M., Parker C.W. Cyclic adenosine 3',5'-monophosphate in human lymphocytes Alterations after phytohemagglutinin stimulation. J. Clin. Invest. 1971, 50:432-441.
71. Spiegel K., Leproult R., Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet 1999, 354:1435-1439.
72. Suchecki D., Lobo L.L., Hipólide D.C., Tufik S. Increased ACTH and corticosterone secretion induced by different methods of paradoxical sleep deprivation. J. Sleep Res. 1998, 7:276-281.
73. Suchecki D., Tiba P.A., Tufik S. Paradoxical sleep deprivation facilitates subsequent corticosterone response to a mild stressor in rats. Neurosci. Lett. 2002, 320:45-48.
74. Suchecki D., Tufik S. Social stability attenuates the stress in the modified multiple platform method for paradoxical sleep deprivation in the rat. Physiol. Behav. 2000, 68:309-316.
75. Tarr A.J., Powell N.D., Reader B.F., Bhave N.S., Roloson A.L., Carson W.E., Sheridan J.F. β-Adrenergic receptor mediated increases in activation and function of natural killer cells following repeated social disruption. Brain Behav. Immun. 2012, 26:1226-1238.
76. Thrivikraman K.V., Su Y., Plotsky P.M. Patterns of Fos-immunoreactivity in the CNS induced by repeated hemorrhage in conscious rats: correlations with pituitary-adrenal axis activity. Stress 1997, 2:145-158.
77. Van Onselen C., Paul S.M., Lee K., Dunn L., Aouizerat B.E., West C., Dodd M., Cooper B., Miaskowski C. Trajectories of sleep disturbance and daytime sleepiness in women before and after surgery for breast cancer. J. Pain Symptom Manage. 2013, 45:244-260.
78. Velazquez-Moctezuma J., Dominguez-Salazar E., Cortes-Barberena E., Najera-Medina O., Retana-Marquez S., Rodriguez-Aguilera E., Jiménez-Anguiano A., Cortes-Martinez L., Ortiz-Muñiz R. Differential effects of rapid eye movement sleep deprivation and immobilization stress on blood lymphocyte subsets in rats. Neuroimmunomodulation 2004, 11:261-267.
79. Vizler C., Nagy T., Kusz E., Glavinas H., Duda E. Flow cytometric cytotoxicity assay for measuring mammalian and avian NK cell activity. Cytometry 2002, 47:158-162.
80. Wan Mahmood W.A., Draman Yusoff M.S., Behan L.A., Di Perna A., Kyaw Tun T., McDermott J., Sreenan S. Association between sleep disruption and levels of lipids in Caucasians with type 2 diabetes. Int. J. Endocrinol. 2013, 10.1155/2013/341506.
81. Wang X., Ouyang Y., Wang Z., Zhao G., Liu L., Bi Y. Obstructive sleep apnea and risk of cardiovascular disease and all-cause mortality: a meta-analysis of prospective cohort studies. Int. J. Cardiol. 2013, 169(3):207-214.
82. Wengström Y., Häggmark C., Strander H., Forsberg C. Perceived symptoms and quality of life in women with breast cancer receiving radiation therapy. Eur. J. Oncol. Nurs. 2000, 4:78-88. discussion 89-90.
83. Xiang L., Marshall G.D. Glucocorticoid receptor BclI polymorphism associates with immunomodulatory response to stress hormone in human peripheral blood mononuclear cells. Int. J. Immunogenet. 2013, 40:222-229.
84. Xiao J., Huang H.W., Peng Y.P., Bao J.Y., Huang Y., Qiu Y.H. Modulation of natural killer cell function by alpha-adrenoreceptor-coupled signalling. Neuro Endocrinol. Lett. 2010, 31:635-644.
85. Yehuda S., Sredni B., Carasso R.L., Kenigsbuch-Sredni D. REM sleep deprivation in rats results in inflammation and interleukin-17 elevation. J. Interferon Cytokine Res. 2009, 29:393-398.
86. Zager A., Andersen M.L., Ruiz F.S., Antunes I.B., Tufik S. Effects of acute and chronic sleep loss on immune modulation of rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R504-R509.
87. Zager A., Ruiz F.S., Tufik S., Andersen M.L. Immune outcomes of paradoxical sleep deprivation on cellular distribution in naive and lipopolysaccharide-stimulated mice. Neuroimmunomodulation 2012, 19:79-87.