Radiation-induced neuroinflammation and radiation somnolence syndrome

CNS and Neurological Disorders - Drug Targets

Volumn 11, Issue 7, 2012, Pages 937-949

  Ballesteros Zebadúa, Paola ^a,b   Chavarria, Anahi ^b   Celis, Miguel Angel ^a   Paz, Carlos ^a   Franco Pérez, Javier ^a  

^a NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Cytokines; Neuroinflammation; Radiation somnolence syndrome; Radiotherapy; Sleep; Whole brain irradiation

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOOXYGENASE 2; DEXAMETHASONE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLIAL FIBRILLARY ACIDIC PROTEIN; GROWTH HORMONE RELEASING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PENTOXIFYLLINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PREDNISONE; PROSTAGLANDIN E2; PROSTANOID; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; BLOOD BRAIN BARRIER; BRAIN INJURY; DRUG DOSE INCREASE; ELECTROENCEPHALOGRAPHY; GLIOSIS; HUMAN; IMMUNE RESPONSE; IONIZING RADIATION; IRRADIATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN EXPRESSION; RADIATION DOSE; RADIATION EXPOSURE; RADIATION INJURY; RADIATION SOMNOLENCE SYNDROME; RANDOMIZED CONTROLLED TRIAL (TOPIC); REM SLEEP; SLEEP; SOMNOLENCE;

ANIMALS; BRAIN; CELL ADHESION MOLECULES; CRANIAL IRRADIATION; CYTOKINES; DISORDERS OF EXCESSIVE SOMNOLENCE; GLIOSIS; HUMANS; NERVE TISSUE PROTEINS; NEURITIS; NEURONS; OXIDATIVE STRESS; PROSTAGLANDINS; RADIATION INJURIES;

EID: 84873166474     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/1871527311201070937     Document Type: Article

References (84)

1. Soussain, C.; Ricard, D.; Fike, J.R.; Mazeron, J.J.; Psimaras, D.; Delattre, J.Y. CNS complications of radiotherapy and chemotherapy. Lancet, 2009, 374(9701), 1639-1651.
2. Tofilon, P.; Fike, J. The radioresponse of the central nervous system: a dynamic process. Radiat. Res., 2000, 153(4), 357-370.
3. Douw, L.; Klein, M.; Fagel, S.S.; van den Heuvel, J.; Taphoorn M.J.; Aaronson, N.K.; Postma, T.J.; Vandertop, W.P.; Mooij, J.J.; Boerman, R.H.; Beute, G.N.; Sluimer, J.D.; Slotman, B.J.; Reijneveld, J.C.; Heimans, J.J. Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term followup. Lancet Neurol., 2009, 8(9), 810-818.
4. Ryan, J. Radiation somnolence syndrome. J. Pediatr. Oncol. Nurs., 2000, 17(1), 50-53.
5. Uzal, D.; Ozyar, M.; Hayran, F.; Zorlu, L.; Atahan, L.; Yetkin, S. Reduced incidence of the somnolence syndrome after prophylactic cranial irradiation in children with acute lymphoblastic leukemia. Radiother. Oncol., 1998, 48(1) 29-32.
6. Druckman, A. Shlafscuct als forge der roentgenbestralung beitragzur strahlenempfindliichkeit des gehunda. Strahlenther, 1929, 33(3) 382-384.
7. Freeman, J.E.; Johnston, P.G.; Voke, J.M. Somnolence after prophylactic cranial irradiation in children with acute lymphoblastic leukaemia. Br. Med. J., 1973, 4(5891), 523-525.
8. Littman, P.; Rosenstock, J.; Gale, G.; Krisch, R.E.; Meadows, A.; Sather, H.; Coccia, P.; DeCamargo, B. The somnolence syndrome in leukemic children following reduced daily dose fractions of cranial radiation. Int. J. Radiat. Oncol. Biol. Phys., 1984, 10(10), 1851-1853.
9. Mandell, L.R.; Walker, R.W.; Steinherz, P.; Fuks, Z. Reduced incidence of the somnolence syndrome in leukemic children with steroid coverage during prophylactic cranial radiation therapy. Cancer, 1989, 63(10), 1975-1978.
10. Garwicz, S.; Aronson, S.; Elmqvist, D.; Landberg, T. Postirradiation syndrome and EEG findings in children with acute lymphoblastic leukaemia. Acta Paediatr. Scand., 1975, 64(3), 399-403.
11. Faithfull, S.; Brada, M. Somnolence syndrome in adults following cranial irradiation for primary brain tumors. Clin. Oncol., 1998, 10(4), 250-254.
12. Kelsey, C.R.; Marks, L.B. Somnolence syndrome after focal radiation therapy to the pineal region: case report and review of the literature. J. Neurooncol., 2006, 78(2), 153-156.
13. Tamaroff, M. Salwen, R.; Miller, D.; Murphy, M.L.; Nit, Y. Neuropsychological sequelae in irradiated(1800 rads and 2400 rads) and non-irradiated children with acute lymphoblastic leukemia(ALL). Proc. Am. Soc. Clin. Oncol., 1985, 4(165), C644.
14. Waber, D.P.; Tarbell, N.J.; Fairclough, D.; Atmore, K.; Castro, R.; Isquith, P.; Lussier, F.; Romero, I.; Carpenter, P.J.; Schiller, M. Cognitive sequelae of treatment in childhood acute lymphoblastic leukemia: cranial radiation requires an accomplice. J. Clin. Oncol., 1995, 13(10), 2490-2496.
15. Ch'ien, L.T.; Aur, R.J.; Stagner, S.; Cavallo, K.; Wood, A.; Goff, J.; Pitner, S.; Hustu, H.O.; Seifert, M.J.; Simone, J.V. Long term neurological implications of somnolence syndrome in children with acute lymphocytic leukemia. Ann. Neurol., 1980, 8(3), 273-277.
16. Stickgold, R. Sleep-dependent memory consolidation. Nature, 2005, 437(7063), 1272-1278.
17. Rosen, G.M.; Bendel, A.E.; Neglia, J.P.; Moertel, C.L.; Mahowald, M. Sleep in children with neoplasms of the central nervous system: case review of 14 children. Pediatrics, 2003, 112(1), e46-e54.
18. Rogers, L.Q.; Courneya, K.S.; Robbins, K.T.; Rao, K.; Malone, J.; Seiz, A.; Reminger, S.; Markwell, S.J.; Burra, V. Factors associated with fatigue, sleep and cognitive function among patients with head and neck cancer. Head Neck, 2008, 30(10), 1310-1317.
19. Mehanna, H.M.; Morton, R.P. Does quality of life predict longterm survival in patients with head and neck cancer? Arch. Otolaryngol. Head Neck Surg., 2006, 132(1), 27-31.
20. Barani, I.J.; Benedict, S.H.; Lin, P.S. Implications for the conventional radiotherapy of central nervous system malignancies. Int. J. Radiat. Oncol. Biol. Phys., 2007, 68(2), 324-333.
21. Hall, E.J.; Giaccia, A.J. Radiobiology for the Radiologist. 6th ed.; Lippincott Williams & Wilkins: Philadelphia, 2006, pp. 5-30.
22. Kyrkanides, S.; Olschowka, J.A.; Williams, J.P.; Hansen, J.T.; O'Banion, M.K. TNF-alpha and IL-1beta mediate intercellular adhesion molecule-1 induction via microglia-astrocyte interaction in CNS radiation injury. J. Neuroimmunol., 1999, 95(1-2), 95-106.
23. Chiang, C.S.; Hong, J.H.; Stalder, A.; Sun, J.R.; Withers, H.R.; McBride, W.H. Delayed molecular responses to brain irradiation. Int. J. Radiat. Biol., 1997, 72(1), 45-53.
24. Chiang, C.S.; McBride, W.H. Radiation enhances tumor necrosis factor alpha production by murine brain cells. Brain Res., 1991, 566(1-2), 265-269.
25. Li, Y.Q.; Jay, V.; Wong, C.S. Oligodendrocytes in the adult rat spinal cord undergo radiation-induced apoptosis. Cancer Res., 1996, 56(23), 5417-5422.
26. Daigle, J.L.; Hong, J.H.; Chiang, C.S.; McBride, W.H. The role of tumor necrosis factor signaling pathways in the response of murine brain to irradiation. Cancer Res., 2001, 61(24), 8859-8865.
27. Nieder, C.; Andratschke, N.; Astner, S.T. Experimental concepts for toxicity prevention and tissue restoration after central nervous system irradiation. Radiat. Oncol., 2007, 2, 23.
28. Lee, W.H.; Sonntag, W.E.; Mitschelen, M.; Yan, H.; Lee, Y.W. Irradiation induces regionally specific alterations in proinflammatory environments in rat brain. Int. J. Radiat. Biol., 2010, 86(2), 132-144.
29. Gaber, M.W.; Sabek, O.M.; Fukatsu, K.; Wilcox, H.G.; Kiani, M.F.; Merchant, T.E. Differences in ICAM-1 and TNF-alpha expression between large single fraction and fractionated irradiation in mouse brain. Int. J. Radiat. Biol., 2003, 79(5), 359-366.
30. Hong, J.H.; Chiang, C.S.; Campbell, I.L.; Sun, J.R.; Withers, H.R.; McBride, W.H. Induction of acute phase gene expression by brain irradiation. Int. J. Radiat. Oncol. Biol. Phys., 1995, 33(3) 619-626.
31. Dinarello, C.A. Immunological and inflammatory functions of the Interleukin-1 family. Annu. Rev. Immunol., 2009, 27, 519-550.
32. Hwang, S.Y.; Jung, J.S.; Kim, T.H.; Lim, S.J.; Oh, E.S.; Kim, J.Y.; Ji, K.A.; Joe, E.H.; Cho, K.H.; Han, I.O. Ionizing radiation induces astrocyte gliosis through microglia activation. Neurobiol. Dis., 2006, 21(3), 457-467.
33. Lee, W.H.; Sonntag, W.E.; Lee, Y.W. Aging attenuates radiationinduced expression of pro-inflammatory mediators in rat brain. Neurosci. Lett., 2010, 476(2), 89-93.
34. Wilson, C.M.; Gaber, M. W; Sabek, O. M; Zawaski, J. A; Merchant, T.E. Radiation-induced astrogliosis and blood-brain barrier damage can be abrogated using anti-TNF treatment. Int. J. Radiat. Oncol. Biol. Phys., 2009, 74(3), 934-941.
35. Yuan, H.; Gaber, M.W.; McColgan, T.; Naimark, M.D.; Kiani, M.F.; Merchant, T.E. Radiation-induced permeability and leukocyte adhesion in the rat blood-brain barrier: modulation with anti-ICAM-1 antibodies. Brain Res., 2003, 969(1-2), 59-69.
36. Ramanan, S.; Zhao, W.; Riddle, D.R.; Robbins, M.E. Role of PPARs in radiation-induced brain Injury. PPAR Res., 2010, 234975, 1-12.
37. Ramanan, S.; Kooshki, M.; Zhao, W.; Hsu, F.C.; Robbins, M.E. PPARalpha ligands inhibit radiation-induced microglial inflammatory responses by negatively regulating NF-kB and AP-1 pathways. Free Radic. Biol. Med., 2008, 45(12), 1695-1704.
38. Travis, E.L. Organizational response of normal tissues to irradiation. Semin. Radiat. Oncol., 2001, 11(3), 184-196.
39. Panagiotakos, G.; Alshamy, G.; Chan, B.; Abrams, R.; Greenberg, E.; Saxena, A.; Bradbury, M.; Edgar, M.; Gutin, P.; Tavar, V. Long-term impact of radiation on the stem cell and oligodendrocyte precursors in the brain. PLoS One, 2007, 2(7), e588.
40. Fike, J.R.; Rosi, S.; Limoli, C.L. Neural precursor cells and CNS radiation sensitivity. Semin. Radiat. Oncol., 2009, 19(2), 122-132.
41. Kyrkanides, S.; Moore, A.H.; Olschowka, J.A.; Daeschner, J.C.; Williams, J.P.; Hansen, J.T.; Kerry ÓBanion, M. Cyclooxygenase-2 modulates brain inflammation-related gene expression in central nervous system radiation injury. Brain Res. Mol. Brain Res., 2002, 104(2), 159-169.
42. Roedel, F.; Kley, N.; Beuscher, H.U.; Hildebrandt, G.; Keilholz, L.; Kern, P.; Voll, R.; Herrmann, M.; Sauer, R. Anti-inflammatory effect of low-dose X-irradiation and the involvement of a TGFbeta1-induced down-regulation of leukocyte/endothelial cell adhesion. Int. J. Radiat. Biol., 2002, 78(8), 711-719.
43. Monje, M.L.; Mizumatsu, S.; Fike, J.R.; Palmer, T.D. Irradiation induces neural precursor-cell dysfunction. Nat. Med., 2002, 8(9), 955-962.
44. Rola, R.; Raber, J.; Rizk, A.; Otsuka, S.; VandenBerg, S.R.; Morhardt, D.R.; Fike, J.R. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol., 2004, 188(2), 316-330.
45. van der Maazen, R.W.; Kleiboer, B.J.; Verhagen, I.; van der Kogel, A.J. Irradiation in vitro discriminates between different O-2A progenitor cell subpopulations in the perinatal central nervous system of rats. Radiat. Res., 1991, 128(1), 64-72.
46. van der Maazen, R.W.; Kleiboer, B.J.; Verhagen, I.; van der Kogel, A.J. Repair capacity of adult rat glial progenitor cells determined by an in vitro clonogenic assay after in vitro or in vivo fractionated irradiation. Int. J. Radiat. Biol., 1993, 63(5), 661-666.
47. Ljubimova, N.V.; Levitman, M.K.; Plotnikova, E.D.; Eidus, L.K. Endothelial cell population dynamics in rat brain after local irradiation. Br. J. Radiol., 1991, 64(766), 934-940.
48. Azzam, E.I.; de Toledo, S.M.; Little, J.B. Direct evidence for the participation of gap junction-mediated intercellular communication in the transmission of damage signals from alpha-particle irradiated to nonirradiated cells. Proc. Nat. Acad. Sci. USA, 2001, 98(2), 473-478.
49. Azzam, E.I.; de Toledo, S.M.; Little, J.B. Expression of Connexin43 is highly sensitive to ionizing radiation and other environmental stresses. Cancer Res., 2003, 63(21), 7128-7135.
50. Tolliver, J.M.; Pellmar, T.C. Ionizing radiation alters neuronal excitability in hippocampal slices of the guinea pig. Radiat. Res., 1987, 112(3), 555-563.
51. Siegel, J.M. Sleep viewed as a state of adaptive inactivity. Nat. Rev. Neurosci., 2009, 10(10), 747-753.
52. Mignot, E. Why we sleep: the temporal organization of recovery. PLoS Biol., 2008, 6(4), e106.
53. Saper, C.B.; Scammel, T.E.; Lu, J. Hypothalamic regulation of sleep and circadian rhythms. Nature, 2005, 437(7063), 1257-1263.
54. Jones, B.E. From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol. Sci., 2005, 26(11), 578-586.
55. Morganti-Kossman, M.C.; Lenzlinger, P.M.; Hans, V.; Stahel, P.; Csuka, E.; Ammann, E.; Stocker, R.; Trentz, O.; Kossmann, T. Production of cytokines following brain injury: beneficial and deleterious for the damaged tissue. Mol. Psychiatry, 1997, 2(2), 133-136.
56. Krueger, J.M.; Fang, J.; Hansen, M.K.; Zhang, J.; Obál, F. Humoral regulation of sleep. News Physiol. Sci., 1998, 13, 189-194.
57. Krueger, J.M. The role of cytokines in sleep regulation. Curr. Pharm. Des., 2008, 14(32), 3408-3416.
58. Shoham, S.; Davenne, D.; Cady, A.B.; Dinarello, C.A.; Krueger, J.M. Recombinant tumor necrosis factor and interleukin 1 enhance slow-wave sleep. Am. J. Physiol., 1987, 253(1), R142-R149.
59. Krueger, J.M.; Obál, F.J.; Fang, J.; Kubota, T.; Taishi, P. The role of cytokines in physiological sleep regulation. Ann. NY Acad. Sci., 2001, 933, 211-221.
60. Fang, J.; Wang, Y.; Krueger, J.M. Effects of interleukin-1beta on sleep are mediated by the type I receptor. Am. J. Physiol., 1998, 274(3), R655-R660.
61. Krueger, J.M.; Majde, J.A. Humoral links between sleep and the immune system. Ann. NY Acad. Sci., 2003, 99, 9-20.
62. Marshall, L.; Born, J. Brain-immune interactions in sleep. Int. Rev. Neurobiol., 2002, 52, 93-131.
63. Fang, B.J.; Tonelli, L.H.; Soriano, J.J.; Postolache, T.T. Disturbed sleep: linking allergic rhinitis, mood and suicidal behavior. Front. Biosci., 2010, 2, 30-46.
64. Spiegel, K.; Sheridan, J.F.; Van Cauter, E. Effect of sleep deprivation on response to immunization. JAMA, 2002, 288(12), 1471-1472.
65. Moldofsky, H. Central nervous system and peripheral immune functions and the sleep wake system. J. Psychiatry Neurosci., 1994, 19(5), 368-374.
66. Krueger, J.M. Somnogenic activity of immune response modifiers. Trends Pharmacol. Sci., 1990, 11(3), 122-126.
67. Dinarello, C.A. Interleukin-1and its biologically related cytokines. Adv. Immunol., 1989, 44, 153-205.
68. Imeri, L.; Opp, M.R. How(and why) the immune system makes us sleep. Nat. Rev. Neurosci., 2009, 10(3), 199-210.
69. Churchill, L.; Rector, D.M.; Yasuda, K.; Fix, C.; Rojas, M.J.; Yasuda. T.; Krueger, J.M. Tumor necrosis factor alpha: activity dependent expression and promotion of cortical column sleep in rats. Neuroscience, 2008, 156(1), 71-80.
70. Hight, K.; Hallett, H.; Churchill, L.; De, A.; Boucher, A.; Krueger, J.M. Time of day differences in the number of cytokine-, neurotrophin-and NeuN-immunoreactive cells in the rat somatosensory or visual cortex. Brain Res., 2010, 1337, 32-40.
71. Beynon, A.L.; Coogan, A.N. Diurnal, age, and immune regulation of interleukin-1b and interleukin-1 type 1 receptor in the mouse suprachiasmatic nucleus. Chronobiol. Int., 2010, 27(8), 1546-1563.
72. Obal, F.; Krueger, J.M. Biochemical regulation of non-rapid-eyemovement sleep. Front. Biosci., 2003, 8, d520-550.
73. Chen, L.; Majde, J.A.; Krueger, J.M. Spontaneous sleep in mice with targeted disruptions of neuronal or inducible nitric oxide synthase genes. Brain Res., 2003, 973(2), 214-222.
74. McCann, S.M.; Kimura, M.; Karanth, S.; Yu, W.H.; Mastronardi, C.A.; Rettori, V. The mechanism of action of cytokines to control the release of hypothalamic and pituitary hormones in infection. Ann. N Y Acad. Sci., 2000, 917, 4-18.
75. Soria-Gómez, E.; Guzmán, K.; Pech-Rueda, O.; Montes-Rodríguez, C.J.; Cisneros, M.; Prospéro-García, O. Oleoylethanolamide affects food intake and sleep-waking cycle through a hypothalamic modulation. Pharmacol. Res., 2010, 61(5), 379-384.
76. Chikahisa, S.; Tominaga, K.; Kawai, T.; Kitaoka, K.; Oishi, K.; Ishida, N.; Rokutan, K.; Sei, H. Bezafibrate, a peroxisome proliferator-activated receptors agonist, decreases body temperature and enhances electroencephalogram delta-oscillation during sleep in mice. Endocrinology, 2008, 149(10), 5262-5271.
77. Terao, A.; Matsumura, H.; Yoneda, H.; Saito, M. Enhancement of slow-wave sleep by tumor necrosis factor-alpha is mediated by cyclooxygenase-2 in rats. Neuroreport, 1998, 9(17), 3791-3796.
78. Jirák, D.; Námstková, K.; Herynek, V.; Liscák, R.; Vymazal, J.; Mares, V.; Sykova, E.; Hajek, M. Lesion evolution after gamma knife irradiation observed by magnetic resonance imaging. Int. J. Radiat. Biol., 2007, 83(4), 237-244.
79. Scheckenbach, K.E.; Crespin, S.; Kwak, B.R.; Chanson, M. Connexin channel-dependent signaling pathways in inflammation. J. Vasc. Res., 2011, 48(2), 91-103.
80. Froger, N.; Orellana, J.A.; Calvo, C.F.; Amigou, E.; Kozoriz, M.G.; Naus, C.C.; Saez, J.C.; Giaume, C. Inhibition of cytokine-induced connexin43 hemichannel activity in astrocytes is neuroprotective. Mol. Cell Neurosci., 2010, 45(1), 37-46.
81. Franco-Perez, J.; Paz, C. Quinine, a selective gap junction blocker, decreases REM sleep in rats. Pharmacol. Biochem. Behav., 2009, 94(2), 250-254.
82. Junek, A.; Rusak, B.; Semba, K. Short-term sleep deprivation may alter the dynamics of hippocampal cell proliferation in adult rats. Neuroscience, 2010, 170(4), 1140-1152.
83. Merrill, J.E.; Ignarro, L.J.; Sherman, M.P.; Melinek, J.; Lane, T.E. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol., 1993, 151(4), 2132-2141.
84. Goldberg, S.L.; Tefferi, A.; Rummans, T.A.; Chen, M.G.; Solberg, L.A.; Noël, P. Post-irradiation somnolence syndrome in an adult patient following allogeneic bone marrow transplantation. Bone Marrow Transplant., 1992, 9(6), 499-501.