Blood-Brain Barrier Disruption Induced by Chronic Sleep Loss: Low-Grade Inflammation May Be the Link

Journal of Immunology Research

Volumn 2016, Issue , 2016, Pages

  Hurtado Alvarado, G ^a   Dominguez Salazar E ^a   Pavon, L ^b   Velazquez Moctezuma J ^a   Gomez Gonzalez B ^a  

^a DEPARTAMENTO DE QUÍMICA   (Mexico)

^b INSTITUTO NACIONAL DE PSIQUIATRÍA RAMÓN DE LA FUENTE MUÑIZ   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; SOMATOMEDIN C; TUMOR NECROSIS FACTOR; VASCULOTROPIN; ACUTE PHASE PROTEIN; AUTACOID; CYTOKINE;

BLOOD BRAIN BARRIER; ENDOTHELIUM CELL; EPITHELIUM CELL; HUMAN; INFLAMMATION; MEMBRANE DAMAGE; MICROFLORA; NEUROPHYSIOLOGY; NONHUMAN; REVIEW; SLEEP DISORDER; TIGHT JUNCTION; ANIMAL; BRAIN; COMPLICATION; IMMUNOLOGY; INTESTINE FLORA; NEURODEGENERATIVE DISEASES; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SECRETION (PROCESS); SLEEP DEPRIVATION;

ACUTE-PHASE PROTEINS; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CYTOKINES; ENDOTHELIAL CELLS; EPITHELIAL CELLS; GASTROINTESTINAL MICROBIOME; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; NEURODEGENERATIVE DISEASES; RATS; SLEEP DEPRIVATION;

EID: 84990946283     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2016/4576012     Document Type: Review

References (120)

1. J. M. Krueger, F. Obál Jr., and J. Fang, "Why we sleep: a theoretical view of sleep function, " Sleep Medicine Reviews, vol. 3, no. 2, pp. 119-129, 1999.
2. J. M. Siegel, "Do all animals sleep?" Trends in Neurosciences, vol. 31, no. 4, pp. 208-213, 2008.
3. D. F. Dinges, S. D. Douglas, S. Hamarman, L. Zaugg, and S. Kapoor, "Sleep deprivation and human immune function, " Advances in Neuroimmunology, vol. 5, no. 2, pp. 97-110, 1995.
4. D. J. Frey, M. Fleshner, and K. P. Wright Jr., "The effects of 40 hours of total sleep deprivation on inflammatory markers in healthy young adults, " Brain, Behavior, and Immunity, vol. 21, no. 8, pp. 1050-1057, 2007.
5. P. Meerlo, R. E. Mistlberger, B. L. Jacobs, H. C. Heller, and D. McGinty, "New neurons in the adult brain: The role of sleep and consequences of sleep loss, " Sleep Medicine Reviews, vol. 13, no. 3, pp. 187-194, 2009.
6. J. G. McCoy andR. E. Strecker, "The cognitive cost of sleep lost, " Neurobiology of Learning and Memory, vol. 96, no. 4, pp. 564-582, 2011.
7. B. Gómez-González, G. Hurtado-Alvarado, E. Esqueda-León, R. Santana-Miranda, J. Á. Rojas-Zamorano, and J. Velázquez-Moctezuma, "REM sleep loss and recovery regulates bloodbrain barrier function, " Current Neurovascular Research, vol. 10, no. 3, pp. 197-207, 2013.
8. J. He, H. Hsuchou, Y. He, A. J. Kastin, Y. Wang, and W. Pan, "Sleep restriction impairs blood-brain barrier function, " The Journal of Neuroscience, vol. 34, no. 44, pp. 14697-14706, 2014.
9. T. Porkka-Heiskanen, K.-M. Zitting, and H.-K. Wigren, "Sleep, its regulation and possible mechanisms of sleep disturbances, " Acta Physiologica, vol. 208, no. 4, pp. 311-328, 2013.
10. A. Zager, M. L. Andersen, F. S. Ruiz, I. B. Antunes, and S. Tufik, "Effects of acute and chronic sleep loss on immune modulation of rats, " American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 293, no. 1, pp. R504-R509, 2007.
11. F. S. Ruiz, M. L. Andersen, R. C. S. Martins, A. Zager, J. D. Lopes, and S. Tufik, "Immune alterations after selective rapid eye movement or total sleep deprivation in healthy male volunteers, " Innate Immunity, vol. 18, no. 1, pp. 44-54, 2012.
12. G. Hurtado-Alvarado, L. Pavón, S. A. Castillo-García et al., "Sleep loss as a factor to induce cellular and molecular inflammatory variations, " Clinical & Developmental Immunology, vol. 2013, Article ID 801341, 14 pages, 2013.
13. L. Ibrahim, W. Duncan, D. A. Luckenbaugh, P. Yuan, R. Machado-Vieira, and C. A. Zarate Jr., "Rapid antidepressant changes with sleep deprivation inmajor depressive disorder are associated with changes in vascular endothelial growth factor (VEGF): a pilot study, " Brain Research Bulletin, vol. 86, no. 1-2, pp. 129-133, 2011.
14. J. M. Mullin, N. Agostino, E. Rendon-Huerta, and J. J. Thornton, "Keynote review: epithelial and endothelial barriers in human disease, " Drug Discovery Today, vol. 10, no. 6, pp. 395-408, 2005.
15. T. Anothaisintawee, S. Reutrakul, E. Van Cauter, and A. Thakkinstian, "Sleep disturbances compared to traditional risk factors for diabetes development: systematic review and metaanalysis, " Sleep Medicine Reviews, vol. 30, pp. 11-24, 2016.
16. M. A. Gupta, F. C. Simpson, and A. K. Gupta, "Psoriasis and sleep disorders: a systematic review, " Sleep Medicine Reviews, vol. 29, pp. 63-75, 2016.
17. J. L. Dettoni, F. M. Consolim-Colombo, L. F. Drager et al., "Cardiovascular effects of partial sleep deprivation in healthy volunteers, " Journal ofApplied Physiology, vol. 113, no. 2, pp. 232-236, 2012.
18. B. R. Weil, M. L. Mestek, C. M. Westby et al., "Short sleep duration is associated with enhanced endothelin-1 vasoconstrictor tone, " Canadian Journal of Physiology and Pharmacology, vol. 88, no. 8, pp. 777-781, 2010.
19. E. L. Schiffrin, "Vascular endothelin in hypertension, " Vascular Pharmacology, vol. 43, no. 1, pp. 19-29, 2005.
20. M. Woods, J. A. Mitchell, E. G. Wood et al., "Endothelin-1 is induced by cytokines in human vascular smooth muscle cells: evidence for intracellular endothelin-converting enzyme, " Molecular Pharmacology, vol. 55, no. 5, pp. 902-909, 1999.
21. M. Kohansieh and A. N. Makaryus, "Sleep deficiency and deprivation leading to cardiovascular disease, " International Journal of Hypertension, vol. 2015, Article ID 615681, 5 pages, 2015.
22. B. Takase, T. Akima, A. Uehata, F. Ohsuzu, and A. Kurita, "Effect of chronic stress and sleep deprivation on both flow-mediated dilation in the brachial artery and the intracellular magnesium level in humans, " Clinical Cardiology, vol. 27, no. 4, pp. 223-227, 2004.
23. J. C. J. Liu, S. Verhulst, S. A. A. Massar, and M. W. L. Chee, "Sleep deprived and sweating it out: The effects of total sleep deprivation on skin conductance reactivity to psychosocial stress, " Sleep, vol. 38, no. 1, pp. 155-159, 2015.
24. A. Carreras, S. X. Zhang, E. Peris et al., "Chronic sleep fragmentation induces endothelial dysfunction and structural vascular changes in mice, " Sleep, vol. 37, no. 11, pp. 1817-1824, 2014.
25. F. Sauvet, G. Florence, P. Van Beers et al., "Total sleep deprivation alters endothelial function in rats: a nonsympathetic mechanism, " SLEEP, vol. 37, no. 3, pp. 465-473, 2014.
26. C. A. Everson and L. A. Toth, "Systemic bacterial invasion induced by sleep deprivation, "American Journal of Physiology-Regulatory Integrative and Comparative Physiology, vol. 278, no. 4, pp. R905-R916, 2000.
27. T. A. Alvarenga, C. Hirotsu, R. Mazaro-Costa, S. Tufik, and M. L. Andersen, "Impairment of male reproductive function after sleep deprivation, " Fertility and Sterility, vol. 103, no. 5, pp. 1355-1362. e1, 2015.
28. T. Deboer, A. Fontana, and I. Tobler, "Tumor necrosis factor (TNF) ligand and TNF receptor deficiency affects sleep and the sleep EEG, " Journal of Neurophysiology, vol. 88, no. 2, pp. 839-846, 2002.
29. S. Yehuda, B. Sredni, R. L. Carasso, and D. Kenigsbuch-Sredni, "REM sleep deprivation in rats results in inflammation and interleukin-17 elevation, " Journal of Interferon and Cytokine Research, vol. 29, no. 7, pp. 393-398, 2009.
30. M. Chennaoui, F. Sauvet, C. Drogou et al., "Effect of one night of sleep loss on changes in tumor necrosis factor alpha (TNF-α) levels in healthymen, " Cytokine, vol. 56, no. 2, pp. 318-324, 2011.
31. D. P. Venancio and D. Suchecki, "Prolonged REM sleep restriction induces metabolic syndrome-related changes: mediation by pro-inflammatory cytokines, " Brain, Behavior, and Immunity, vol. 47, pp. 109-117, 2015.
32. A. Wolkow, B. Aisbett, J. Reynolds, S. A. Ferguson, and L. C. Main, "Acute psychophysiological relationships between mood, inflammatory and cortisol changes in response to simulated physical firefighting work and sleep restriction, " Applied Psychophysiology and Biofeedback, vol. 41, no. 2, pp. 165-180, 2016.
33. V. Ramesh, D. Nair, S. X. L. Zhang et al., "Disrupted sleep without sleep curtailment induces sleepiness and cognitive dysfunction via the tumor necrosis factor-α pathway, " Journal of Neuroinflammation, vol. 9, article 91, 2012.
34. Q. Zhao, X. Xie, Y. Fan et al., "Phenotypic dysregulation of microglial activation in young offspring rats with maternal sleep deprivation-induced cognitive impairment, " Scientific Reports, vol. 5, article 9513, 2015.
35. M. R. Irwin, T. Witarama, M. Caudill, R. Olmstead, and E. C. Breen, "Sleep loss activates cellular inflammation and signal transducer and activator of transcription (STAT) family proteins in humans, " Brain, Behavior, and Immunity, vol. 47, pp. 86-92, 2015.
36. J. E. Dumaine and N. T. Ashley, "Acute sleep fragmentation induces tissue-specific changes in cytokine gene expression and increases serum corticosterone concentration, " American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 308, no. 12, pp. R1062-R1069, 2015.
37. E. M. de Oliveira, B. Visniauskas, S. Sandri et al., "Late effects of sleep restriction: potentiating weight gain and insulin resistance arising from a high-fat diet in mice, " Obesity, vol. 23, no. 2, pp. 391-398, 2015.
38. G. A. Rosenberg, E. Y. Estrada, J. E. Dencoff, and W. G. Stetler-Stevenson, "Tumor necrosis factor-β-induced gelatinase B causes delayed opening of the blood-brain barrier: an expanded therapeutic window, " Brain Research, vol. 703, no. 1-2, pp. 151-155, 1995.
39. K. S. Mark and D. W. Miller, "Increased permeability of primary cultured brain microvessel endothelial cellmonolayers following TNF-α exposure, " Life Sciences, vol. 64, no. 21, pp. 1941-1953, 1999.
40. J. Peng, F. He, C. Zhang, X. Deng, and F. Yin, "Protein kinase C-α signals P115RhoGEF phosphorylation and RhoA activation in TNF-β-induced mouse brain microvascular endothelial cell barrier dysfunction, " Journal of Neuroinflammation, vol. 8, article 28, 2011.
41. J. Matsumoto, F. Takata, T. Machida et al., "Tumor necrosis factor-β-stimulated brain pericytes possess a unique cytokine and chemokine release profile and enhance microglial activation, " Neuroscience Letters, vol. 578, pp. 133-138, 2014.
42. H. E. de Vries, M. C. M. Blom-Roosemalen, M. van Oosten et al., "The influence of cytokines on the integrity of the bloodbrain barrier in vitro, " Journal of Neuroimmunology, vol. 64, no. 1, pp. 37-43, 1996.
43. J. B. Dickstein, H. Moldofsky, and J. B. Hay, "Brain-blood permeability: TNF-alpha promotes escape of protein tracer from CSF to blood, " American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 279, no. 1, pp. R148-R151, 2000.
44. L. Xie, H. Kang, Q. Xu et al., "Sleep drives metabolite clearance from the adult brain, " Science, vol. 342, no. 6156, pp. 373-377, 2013.
45. M. R. Zielinski, Y. Kim, S. A. Karpova, R. W. McCarley, R. E. Strecker, and D. Gerashchenko, "Chronic sleep restriction elevates brain interleukin-1 beta and tumor necrosis factor-alpha and attenuates brain-derived neurotrophic factor expression, " Neuroscience Letters, vol. 580, pp. 27-31, 2014.
46. G. Farkas, J. Márton, Z. Nagy et al., "Experimental acute pancreatitis results in increased blood-brain barrier permeability in the rat: a potential role for tumor necrosis factor and interleukin 6, " Neuroscience Letters, vol. 242, no. 3, pp. 147-150, 1998.
47. C. Silwedel and C. Förster, "Differential susceptibility of cerebral and cerebellar murine brain microvascular endothelial cells to loss of barrier properties in response to inflammatory stimuli, " Journal of Neuroimmunology, vol. 179, no. 1-2, pp. 37-45, 2006.
48. D. L. Bornstein, "Leukocytic pyrogen: a major mediator of the acute phase reaction, " Annals of the New York Academy of Sciences, vol. 389, no. 1, pp. 323-337, 1982.
49. J. Hu, Z. Chen, C. P. Gorczynski et al., "Sleep-deprived mice show altered cytokine production manifest by perturbations in serum IL-1ra, TNFa, and IL-6 levels, " Brain, Behavior, and Immunity, vol. 17, no. 6, pp. 498-504, 2003.
50. W. M. A. vanLeeuwen, M. Lehto, P. Karisola et al., "Sleep restriction increases the risk of developing cardiovascular diseases by augmenting proinflammatory responses through IL-17 and CRP, " PLoS ONE, vol. 4, no. 2, Article ID e4589, 2009.
51. A. Ericsson, C. Liu, R. P. Hart, and P. E. Sawchenko, "Type 1 interleukin-1 receptor in the rat brain: distribution, regulation, and relationship to sites of IL-1-induced cellular activation, " Journal of Comparative Neurology, vol. 361, no. 4, pp. 681-698, 1995.
52. J. P. Konsman and A. Blomqvist, "Brain blood vessel distribution of interleukin-1 type 1 receptor corresponds to patterns of jun phosphor-ylation and cyclooxygenase-2 induction by inflammatory stimuli, " Society for Neuroscience, vol. 27, pp. 843-814, 2001.
53. J. P. Konsman, S. Vigues, L. Mackerlova, A. Bristow, and A. Blomqvist, "Rat brain vascular distribution of interleukin-1 type-1 receptor immunoreactivity: relationship to patterns of inducible cyclooxygenase expression by peripheral inflammatory stimuli, " Journal of Comparative Neurology, vol. 472, no. 1, pp. 113-129, 2004.
54. R. A. Skinner, R. M. Gibson, N. J. Rothwell, E. Pinteaux, and J. I. Penny, "Transport of interleukin-1 across cerebromicrovascular endothelial cells, " British Journal of Pharmacology, vol. 156, no. 7, pp. 1115-1123, 2009.
55. A.-M. Van Dam, H. E. De Vries, J. Kuiper et al., "Interleukin-1 receptors on rat brain endothelial cells: a role in neuroimmune interaction?" The FASEB Journal, vol. 10, no. 2, pp. 351-356, 1996.
56. S. Ching, H. Zhang, N. Belevych et al., "Endothelial-specific knockdown of interleukin-1 (IL-1) type 1 receptor differentially alters CNS responses to IL-1 depending on its route of administration, " The Journal of Neuroscience, vol. 27, no. 39, pp. 10476-10486, 2007.
57. N. Quan, L. He, and W. Lai, "Endothelial activation is an intermediate step for peripheral lipopolysaccharide induced activation of paraventricular nucleus, " Brain Research Bulletin, vol. 59, no. 6, pp. 447-452, 2003.
58. Y. Wang, S. Jin, Y. Sonobe et al., "Interleukin-1β induces bloodbrain barrier disruption by downregulating sonic hedgehog in astrocytes, " PLoS ONE, vol. 9, no. 10, Article IDe110024, 2014.
59. E. S. Wohleb, M. L. Hanke, A. W. Corona et al., "β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat, " The Journal of Neuroscience, vol. 31, no. 17, pp. 6277-6288, 2011.
60. E. S. Wohleb, J. M. Patterson, V. Sharma, N. Quan, J. P. Godbout, and J. F. Sheridan, "Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuated stress-induced neuroinflammation and prevented anxiety-like behavior, " The Journal of Neuroscience, vol. 34, no. 7, pp. 2583-2591, 2014.
61. M.-A. Lécuyer, H. Kebir, and A. Prat, "Glial influences on BBB functions and molecular players in immune cell trafficking, " Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, vol. 1862, no. 3, pp. 472-482, 2016.
62. L. Redwine, R. L. Hauger, J. C. Gillin, and M. Irwin, "Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in humans, "The Journal of Clinical Endocrinology & Metabolism, vol. 85, no. 10, pp. 3597-3603, 2000.
63. E. Späth-Schwalbe, K. Hansen, F. Schmidt et al., "Acute effects of recombinant human interleukin-6 on endocrine and central nervous sleep functions in healthy men, " Journal of Clinical Endocrinology and Metabolism, vol. 83, no. 5, pp. 1573-1579, 1998.
64. A. N. Vgontzas, M. Zoumakis, D. A. Papanicolaou et al., "Chronic insomnia is associated with a shift of interleukin-6 and tumor necrosis factor secretion fromnighttime to daytime, " Metabolism, vol. 51, no. 7, pp. 887-892, 2002.
65. M. Haack, E. Sanchez, and J. M. Mullington, "Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers, " Sleep, vol. 30, no. 9, pp. 1145-1152, 2007.
66. S. Abedelmalek, N. Souissi, H. Chtourou et al., "Effects of partial sleep deprivation on proinflammatory cytokines, growth hormone, and steroid hormone concentrations during repeated brief sprint interval exercise, " Chronobiology International, vol. 30, no. 4, pp. 502-509, 2013.
67. M. R. Irwin, M. Wang, C. O. Campomayor, A. Collado-Hidalgo, and S. Cole, "Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation, " Archives of Internal Medicine, vol. 166, no. 16, pp. 1756-1762, 2006.
68. J. Guess, J. B. Burch, K. Ogoussan et al., "Circadian disruption, Per3, and human cytokine secretion, " Integrative CancerTherapies, vol. 8, no. 4, pp. 329-336, 2009.
69. F. Sauvet, G. Leftheriotis, D. Gomez-Merino et al., "Effect of acute sleep deprivation on vascular function in healthy subjects, " Journal of AppliedPhysiology, vol. 108, no. 1, pp. 68-75, 2010.
70. L. Krizanac-Bengez, M. Kapural, F. Parkinson et al., "Effects of transient loss of shear stress on blood-brain barrier endothelium: role of nitric oxide and IL-6, " Brain Research, vol. 977, no. 2, pp. 239-246, 2003.
71. Q. Feng, Y. I. Wang, and Y. Yang, "Neuroprotective effect of interleukin-6 in a ratmodel of cerebral ischemia, " Experimental andTherapeutic Medicine, vol. 9, no. 5, pp. 1695-1701, 2015.
72. L. Vallières and S. Rivest, "Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1β, " Journal of Neurochemistry, vol. 69, no. 4, pp. 1668-1683, 1997.
73. D. Matusevicius, P. Kivisäkk, B. He et al., "Interleukin-17mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis, " Multiple Sclerosis, vol. 5, no. 2, pp. 101-104, 1999.
74. E. Lubberts, L. A. B. Joosten, B. Oppers et al., "IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis, " The Journal of Immunology, vol. 167, no. 2, pp. 1004-1013, 2001.
75. D. Yen, J. Cheung, H. Scheerens et al., "IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6, " The Journal of Clinical Investigation, vol. 116, no. 5, pp. 1310-1316, 2006.
76. C. K. Wong, C. Y. Ho, E. K. Li, and C. W. K. Lam, "Elevation of proinflammatory cytokine (IL-18, IL-17, IL-12) and Th2 cytokine (IL-4) concentrations in patients with systemic lupus erythematosus, " Lupus, vol. 9, no. 8, pp. 589-593, 2000.
77. Y. Chen, P. Yang, F. Li, and A. Kijlstra, "The effects of Th17 cytokines on the inflammatory mediator production and barrier function of ARPE-19 cells, " PLoS ONE, vol. 6, no. 3, Article ID e18139, 2011.
78. H. Kebir, K. Kreymborg, I. Ifergan et al., "Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation, " Nature Medicine, vol. 13, no. 10, pp. 1173-1175, 2007.
79. J. Huppert, D. Closhen, A. Croxford et al., "Cellularmechanisms of IL-17-induced blood-brain barrier disruption, " The FASEB Journal, vol. 24, no. 4, pp. 1023-1034, 2010.
80. A. J. Szalai and M. A. McCrory, "Varied biologic functions of c-reactive protein: lessons learned from transgenic mice, " Immunologic Research, vol. 26, no. 1-3, pp. 279-287, 2002.
81. H. K. Meier-Ewert, P. M. Ridker, N. Rifai et al., "Effect of sleep loss on C-Reactive protein, an inflammatory marker of cardiovascular risk, " Journal of the American College of Cardiology, vol. 43, no. 4, pp. 678-683, 2004.
82. S. R. Patel, X. Zhu, A. Storfer-Isser et al., "Sleep duration and biomarkers of inflammation, " Sleep, vol. 32, no. 2, pp. 200-204, 2009.
83. M. L. Okun, M. Coussons-Read, and M. Hall, "Disturbed sleep is associated with increased C-reactive protein in young women, " Brain, Behavior, and Immunity, vol. 23, no. 3, pp. 351-354, 2009.
84. J. V. Castell, M. J. Gómez-Lechón, M. David, R. Fabra, R. Trullenque, and P. C. Heinrich, "Acute-phase response of human hepatocytes: regulation of acute-phase protein synthesis by interleukin-6, " Hepatology, vol. 12, no. 5, pp. 1179-1186, 1990.
85. C. R. W. Kuhlmann, L. Librizzi, D. Closhen et al., "Mechanisms of C-reactive protein-induced blood-brain barrier disruption, " Stroke, vol. 40, no. 4, pp. 1458-1466, 2009.
86. D. Closhen, B. Bender, H. J. Luhmann, and C. R. W. Kuhlmann, "CRP-induced levels of oxidative stress are higher in brain than aortic endothelial cells, " Cytokine, vol. 50, no. 2, pp. 117-120, 2010.
87. C. Amos, I. A. Romero, C. Schültze et al., "Cross-linking of brain endothelial intercellular adhesion molecule (ICAM)-1 induces association of ICAM-1 with detergent-insoluble cytoskeletal fraction, " Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 21, no. 5, pp. 810-816, 2001.
88. B. Engelhardt, F. K. Conley, and E. C. Butcher, "Cell adhesion molecules on vessels during inflammation in the mouse central nervous system, " Journal of Neuroimmunology, vol. 51, no. 2, pp. 199-208, 1994.
89. B. Devaux, D. Scholz, A. Hirche, W. P. Klovekorn, and J. Schaper, "Upregulation of cell adhesion molecules and the presence of low grade inflammation in human chronic heart failure, " European Heart Journal, vol. 18, no. 3, pp. 470-479, 1997.
90. V. M. Pak, B. T. Keenan, N. Jackson et al., "Adhesion molecule increases in sleep apnea: beneficial effect of positive airway pressure and moderation by obesity, " International Journal of Obesity, vol. 39, no. 3, pp. 472-479, 2015.
91. L.-L. Meng, Y.-Z. Tang, C.-L. Ni et al., "Impact of inflammatory markers on the relationship between sleep quality and incident cardiovascular events in type 2 diabetes, " Journal ofDiabetes and its Complications, vol. 29, no. 7, pp. 882-886, 2015.
92. A. T. Argaw, B. T. Gurfein, Y. Zhang, A. Zameer, and G. R. John, "VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown, " Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 6, pp. 1977-1982, 2009.
93. P. Stiefel, M. A. Sánchez-Armengol, J. Villar, A. Vallejo-Vaz, R. Moreno-Luna, and F. Capote, "Obstructive sleep apnea syndrome, vascular pathology, endothelial function and endothelial cells and circulating microparticles, " Archives of Medical Research, vol. 44, no. 6, pp. 409-414, 2013.
94. D. C. Limand A. I. Pack, "Obstructive sleep apnea and cognitive impairment: addressing the blood-brain barrier, " SleepMedicine Reviews, vol. 18, no. 1, pp. 35-48, 2014.
95. L. Ibrahim, W. Duncan, D. A. Luckenbaugh, P. Yuan, R. Machado-Vieira, and C. A. Zarate, "Rapid antidepressant changes with sleep deprivation inmajor depressive disorder are associated with changes in vascular endothelial growth factor (VEGF): a pilot study, " Brain Research Bulletin, vol. 86, no. 1-2, pp. 129-133, 2011.
96. H. Chen, Z. Zhao, J. Zheng et al., "The effect of IGF-1 on symptoms of sleep deprivation in a rat model of inflammatory heart disease and metabolic syndrome, " Biochemical and Biophysical Research Communications, vol. 446, no. 4, pp. 843-849, 2014.
97. S. Bake, A. K. Okoreeh, R. C. Alaniz, and F. Sohrabji, "Insulin-Like Growth Factor (IGF)-I modulates endothelial bloodbrain barrier function in ischemic middle-aged female rats, " Endocrinology, vol. 157, no. 1, pp. 61-69, 2016.
98. A. J. Park, J. Collins, P. A. Blennerhassett et al., "Altered colonic function and microbiota profile in a mouse model of chronic depression, " Neurogastroenterology and Motility, vol. 25, no. 9, pp. 733-e575, 2013.
99. E. Patterson, P. M. Ryan, J. F. Cryan et al., "Gut microbiota, obesity and diabetes, " Postgraduate Medical Journal, vol. 92, no. 1087, pp. 286-300, 2016.
100. J. R. Kelly, P. J. Kennedy, J. F. Cryan, T. G. Dinan, G. Clarke, and N. P. Hyland, "Breaking down the barriers: The gut microbiome, intestinal permeability and stress-related psychiatric disorders, " Frontiers in Cellular Neuroscience, vol. 9, article 392, 2015.
101. V. Braniste, M. Al-Asmakh, C. Kowal et al., "The gut microbiota influences blood-brain barrier permeability in mice, " Science Translational Medicine, vol. 19, no. 6, pp. 1-24, 2014.
102. C. Korth, "A co-evolutionary theory of sleep, " Medical Hypotheses, vol. 45, no. 3, pp. 304-310, 1995.
103. K. D. Rochfort and P. M. Cummins, "Cytokine-mediated dysregulation of zonula occludens-1 properties in human brain microvascular endothelium, " Microvascular Research, vol. 100, pp. 48-53, 2015.
104. D. A. Antonetti, A. J. Barber, L. A. Hollinger, E. B. Wolpert, and T. W. Gardner, "Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occluden 1. A potential mechanism for vascular permeability in diabetic retinopathy and tumors, " The Journal of Biological Chemistry, vol. 274, no. 33, pp. 23463-23467, 1999.
105. M. A. Lopez-Ramirez, R. Fischer, C. C. Torres-Badillo et al., "Role of caspases in cytokine-induced barrier breakdown in human brain endothelial cells, "The Journal of Immunology, vol. 189, no. 6, pp. 3130-3139, 2012.
106. K. Wiggins-Dohlvik, M. Merriman, C. A. Shaji et al., "Tumor necrosis factor-α disruption of brain endothelial cell barrier is mediated through matrix metalloproteinase-9, " The American Journal of Surgery, vol. 208, no. 6, pp. 954-960, 2014.
107. W. Tian and T. R. Kyriakides, "Matrix metalloproteinase-9 deficiency leads to prolonged foreign body response in the brain associated with increased IL-1β levels and leakage of the bloodbrain barrier, " Matrix Biology, vol. 28, no. 3, pp. 148-159, 2009.
108. W. J. Trickler, W. G. Mayhan, and D. W. Miller, "Brainmicrovessel endothelial cell responses to tumor necrosis factor-alpha involve a nuclear factor kappa B (NF-B) signal transduction pathway, " Brain Research, vol. 1048, no. 1-2, pp. 24-31, 2005.
109. D. Engblom, M. Ek, S. Saha, A. Ericsson-Dahlstrand, P.-J. Jakobsson, and A. Blomqvist, "Prostaglandins as inflammatory messengers across the blood-brain barrier, " Journal ofMolecular Medicine, vol. 80, no. 1, pp. 5-15, 2002.
110. D. J. Jaworowicz Jr., P. J. Korytko, S. S. Lakhman, and K. M. K. Boje, "Nitric oxide and prostaglandin E2 formation parallels blood-brain barrier disruption in an experimental rat model of bacterial meningitis, " Brain Research Bulletin, vol. 46, no. 6, pp. 541-546, 1998.
111. A. Eskilsson, E. Mirrasekhian, S. Dufour, M. Schwaninger, D. Engblom, and A. Blomqvist, "Immune-induced fever is mediated by IL-6 receptors on brain endothelial cells coupled to stat3-dependent induction of brain endothelial prostaglandin synthesis, "TheJournal ofNeuroscience, vol. 34, no. 48, pp. 15957-15961, 2014.
112. N. Laflamme, S. Lacroix, and S. Rivest, "An essential role of interleukin-1beta in mediating NF-kappaB activity and COX-2 transcription in cells of the blood-brain barrier in response to a systemic and localized inflammation but not during endotoxemia, " The Journal of Neuroscience, vol. 19, no. 24, pp. 10923-10930, 1999.
113. S. Y. Eum, I. Andras, B. Hennig, and M. Toborek, "NADPH oxidase and lipid raft-associated redox signaling are required for PCB153-induced upregulation of cell adhesion molecules in human brain endothelial cells, " Toxicology and Applied Pharmacology, vol. 240, no. 2, pp. 299-305, 2009.
114. J. H. Mills, L. F. Thompson, C. Mueller et al., "CD73 is required for efficient entry of lymphocytes into the central nervous system during experimental autoimmune encephalomyelitis, " Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 27, pp. 9325-9330, 2008.
115. W. Pan and A. J. Kastin, "The blood-brain barrier: regulatory roles in wakefulness and sleep, " The Neuroscientist, 2016.
116. G. Hurtado-Alvarado, A. M. Cabañas-Morales, and B. Gómez-Gónzalez, "Pericytes: brain-immune interface modulators, " Frontiers in Integrative Neuroscience, vol. 7, article 80, 2014.
117. A. C. Reynolds and S. Banks, "Total sleep deprivation, chronic sleep restriction and sleep disruption, " Progress in Brain Research, vol. 185, pp. 91-103, 2010.
118. D. Suchecki and S. Tufik, "Social stability attenuates the stress in themodifiedmultiple platformmethod for paradoxical sleep deprivation in the rat, " Physiology & Behavior, vol. 68, no. 3, pp. 309-316, 2000.
119. A. Rechtschaffen, B. M. Bergmann, C. A. Everson, C. A. Kushida, and M. A. Gilliland, "Sleep deprivation in the rat: I. Conceptual issues, " Sleep, vol. 12, no. 1, pp. 1-4, 1989.
120. A. Rechtschaffen and B. M. Bergmann, "Sleep deprivation in the rat by the disk-over-watermethod, " Behavioural Brain Research, vol. 69, no. 1-2, pp. 55-63, 1995.