The proinflammatory RAGE/NF-κB pathway is involved in neuronal damage and reactive gliosis in a model of sleep apnea by intermittent hypoxia

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Angelo, Maria Florencia ^a   Aguirre, Alejandra ^a   Reyes, Rolando X Avilés ^a   Villarreal, Alejandro ^a   Lukin, Jerónimo ^a   Melendez, Matías ^b   Vanasco, Virginia ^d   Barker, Phil ^c   Alvarez, Silvia ^d   Epstein, Alberto ^b   Jerusalinsky, Diana ^a   Ramos, Alberto Javier ^a  

^a Facultad de Medicina   (Argentina)

^b UNIVERSITÉ LYON 1   (France)

^c MCGILL UNIVERSITY   (Canada)

^d University of Buenos Aires   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ADVANCED GLYCATION END PRODUCT RECEPTOR ANTIBODY; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NEUTRALIZING ANTIBODY; PROTEIN ANTIBODY; PROTEIN INHIBITOR; PROTEIN S100B; PROTEIN S100B ANTIBODY; UNCLASSIFIED DRUG; VIRUS VECTOR; IMMUNOGLOBULIN RECEPTOR;

ADULT; AMPLICON; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; GLIA CELL; GLIOSIS; HERPES SIMPLEX VIRUS; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; INTERMITTENT HYPOXIA; MALE; MOUSE; NERVE CELL DEGENERATION; NERVE CELL LESION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PROTEIN EXPRESSION; RAT; SLEEP DISORDERED BREATHING; TRANSCRIPTION INITIATION; ANIMAL; ANOXIA; DISEASE MODEL; METABOLISM; NERVE CELL; PATHOLOGY; WISTAR RAT;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ANIMALS; ANOXIA; DISEASE MODELS, ANIMAL; GLIOSIS; MALE; NEURONS; NF-KAPPA B; RATS; RATS, WISTAR; RECEPTORS, IMMUNOLOGIC; SLEEP APNEA SYNDROMES;

EID: 84907482268     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107901     Document Type: Article

References (62)

1. Decary A, Rouleau I, Montplaisir J (2000) Cognitive deficits associated with sleep apnea syndrome: a proposed neuropsychological test battery. Sleep 23: 369-381.
2. Engleman HM, Kingshott RN, Martin SE, Douglas NJ (2000) Cognitive function in the sleep apnea/hypopnea syndrome (SAHS). Sleep 23 Suppl 4: S102-8.
3. Gozal D, Kheirandish-Gozal L (2007) Neurocognitive and behavioral morbidity in children with sleep disorders. Curr Opin Pulm Med 13: 505-509.
4. Gozal D, Kheirandish-Gozal L (2008) Cardiovascular morbidity in obstructive sleep apnea: oxidative stress, inflammation, and much more. Am J Respir Crit Care Med 177: 369-375.
5. Roure N, Gomez S, Mediano O, Duran J, Pena Mde L, et al. (2008) Daytime sleepiness and polysomnography in obstructive sleep apnea patients. Sleep Med 9: 727-731.
6. Basner RC (2007) Continuous positive airway pressure for obstructive sleep apnea. N Engl J Med 356: 1751-1758.
7. Feuerstein C, Naegele B, Pepin JL, Levy P (1997) Frontal lobe-related cognitive functions in patients with sleep apnea syndrome before and after treatment. Acta Neurol Belg 97: 96-107.
8. Naegele B, Pepin JL, Levy P, Bonnet C, Pellat J, et al. (1998) Cognitive executive dysfunction in patients with obstructive sleep apnea syndrome (OSAS) after CPAP treatment. Sleep 21: 392-397.
9. Thomas RJ, Rosen BR, Stern CE, Weiss JW, Kwong KK (2005) Functional imaging of working memory in obstructive sleep-disordered breathing. J Appl Physiol (1985) 98: 2226-2234.
10. Zimmerman ME, Aloia MS (2006) A review of neuroimaging in obstructive sleep apnea. J Clin Sleep Med 2: 461-471.
11. Aviles-Reyes RX, Angelo MF, Villarreal A, Rios H, Lazarowski A, et al. (2010) Intermittent hypoxia during sleep induces reactive gliosis and limited neuronal death in rats: implications for sleep apnea. J Neurochem 112: 854-869.
12. Baronio D, Martinez D, Fiori CZ, Bambini-Junior V, Forgiarini LF, et al. (2013) Altered aquaporins in the brains of mice submitted to intermittent hypoxia model of sleep apnea. Respir Physiol Neurobiol 185: 217-221.
13. Gozal D, Daniel JM, Dohanich GP (2001) Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci 21: 2442-2450.
14. Gozal E, Gozal D, Pierce WM, Thongboonkerd V, Scherzer JA, et al. (2002) Proteomic analysis of CA1 and CA3 regions of rat hippocampus and differential susceptibility to intermittent hypoxia. J Neurochem 83: 331-45.
15. Row BW, Liu R, Xu W, Kheirandish L, Gozal D (2003) Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am J Respir Crit Care Med 167: 1548-1553.
16. Payne RS, Goldbart A, Gozal D, Schurr A (2004) Effect of intermittent hypoxia on long-term potentiation in rat hippocampal slices. Brain Res 1029: 195-199.
17. Sizonenko SV, Sirimanne E, Mayall Y, Gluckman PD, Inder T, et al. (2003) Selective cortical alteration after hypoxic-ischemic injury in the very immature rat brain. Pediatr Res 54: 263-269.
18. Hung MW, Tipoe GL, Poon AM, Reiter RJ, Fung ML (2008) Protective effect of melatonin against hippocampal injury of rats with intermittent hypoxia. J Pineal Res 44: 214-221.
19. Lavie L (2003) Obstructive sleep apnoea syndrome-an oxidative stress disorder. Sleep Med Rev 7: 35-51.
20. Fung SJ, Xi MC, Zhang JH, Sampogna S, Yamuy Jet al. (2007) Apnea promotes glutamate-induced excitotoxicity in hippocampal neurons. Brain Res 1179: 42-50.
21. Bravo Mde L, Serpero LD, Barcelo A, Barbe F, Agusti A, Gozal D. (2007) Inflammatory proteins in patients with obstructive sleep apnea with and without daytime sleepiness. Sleep Breath 11: 177-185.
22. Burckhardt IC, Gozal D, Dayyat E, Cheng Y, Li RC, et al. (2008) Green tea catechin polyphenols attenuate behavioral and oxidative responses to intermittent hypoxia. Am J Respir Crit Care Med 177: 1135-1141.
23. Ridet JL, Malhotra SK, Privat A, Gage FH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20: 570-577.
24. Maragakis NJ, Rothstein JD (2006) Mechanisms of Disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol 2: 679-689.
25. Stoll G, Jander S, Schroeter M (1998) Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56: 149-171.
26. Privat A (2003) Astrocytes as support for axonal regeneration in the central nervous system of mammals. Glia 43: 91-93.
27. Liberto CM, Albrecht PJ, Herx LM, Yong VW, Levison SW (2004) Pro-regenerative properties of cytokine-activated astrocytes. J Neurochem 89: 1092-1100.
28. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, et al. (2012) Genomic analysis of reactive astrogliosis. J Neurosci 32: 6391-6410.
29. Villarreal A, Aviles Reyes RX, Angelo MF, Reines AG, Ramos AJ (2011) S100B alters neuronal survival and dendrite extension via RAGE-mediated NF-kappaB signaling. J Neurochem 117: 321-332.
30. Ponath G, Schettler C, Kaestner F, Voigt B, Wentker D, et al. (2007) Autocrine S100B effects on astrocytes are mediated via RAGE. J Neuroimmunol 184: 214-222.
31. Ramos AJ, Villarreal A, Seoane R, Angelo MF, Aviles Reyes RX, et al. (2013) S100B is a damage associated molecular pattern protein (DAMP) that promotes reactive gliosis in a RAGE dependent manner PSM01.32. Journal of Neurochem, 125: 117.
32. da Silva LG, Mottin CC, Souza DO, Portela LV, Braga CW, et al. (2008) Serum S100B but not NSE levels are increased in morbidly obese individuals affected by obstructive sleep apnea-hypopnea syndrome. Obes Surg 18: 993-999.
33. Duru S, Hikmet Firat I, Colak N, Ginis Z, Delibasi T, et al. (2012) Serum S100B protein: a useful marker in obstructive sleep apnea syndrome. Neurol Neurochir Pol 46: 450-455.
34. Bhakar AL, Tannis LL, Zeindler C, Russo MP, Jobin C, et al. (2002) Constitutive nuclear factor-kappa B activity is required for central neuron survival. J Neurosci 22: 8466-8475.
35. Lee W, Parpura V (2012) Dissociated cell culture for testing effects of carbon nanotubes on neuronal growth. Methods Mol Biol 846: 261-276.
36. Shan X, Chi L, Ke Y, Luo C, Qian S, et al. (2007) Manganese superoxide dismutase protects mouse cortical neurons from chronic intermittent hypoxia-mediated oxidative damage. Neurobiol Dis 28: 206-215.
37. Paxinos G, Watson C (2007) The Rat Brain in Stereotaxic Coordinates, 6th Ed. San Diego: Elsevier.
38. Slipczuk L, Bekinschtein P, Katche C, Cammarota M, Izquierdo I, et al. (2009) BDNF activates mTOR to regulate GluR1 expression required for memory formation. PLoS One. 4: e6007.
39. Fraga CG, Leibovitz BE, Tappel AL (1988) Lipid peroxidation measured as thiobarbituric acid-reactive substances in tissue slices: characterization and comparison with homogenates and microsomes. Free Radic Biol Med 4: 155-161.
40. Ramos A, Ho WC, Forte S, Dickson K, Boutilier J, et al. (2007) Hypo-osmolar stress induces p75NTR expression by activating Sp1-dependent transcription. J Neurosci 27: 1498-1506.
41. Zaupa C, Revol-Guyot V, Epstein AL (2003) Improved packaging system for generation of high-level noncytotoxic HSV-1 amplicon vectors using Cre-loxP site-specific recombination to delete the packaging signals of defective helper genomes. Hum Gene Ther 14: 1049-1063.
42. Logvinoff C, Epstein AL (2001) A novel approach for herpes simplex virus type 1 amplicon vector production, using the Cre-loxP recombination system to remove helper virus. Hum Gene Ther 12: 161-167.
43. Krisky DM, Marconi PC, Oligino TJ, Rouse RJ, Fink DJ, et al. (1998) Development of herpes simplex virus replication-defective multigene vectors for combination gene therapy applications. Gene Ther 5: 1517-1530.
44. Machuca I, Jacquemont B, Epstein A (1986). Multiple adjacent or overlapping loci affecting the level of gC and cell fusion mapped by intratypic recombinants of HSV-1. Virology 150: 117-125.
45. Selmi C, Montano N, Furlan R, Keen CL, Gershwin ME (2007) Inflammation and oxidative stress in obstructive sleep apnea syndrome. Exp Biol Med (Maywood) 232: 1409-1413.
46. da Rosa DP, Forgiarini LF, Baronio D, Feijo CA, Martinez D, et al. (2012) Simulating sleep apnea by exposure to intermittent hypoxia induces inflammation in the lung and liver. Mediators Inflamm 2012: 879419.
47. Wang B, Yan B, Song D, Ye X, Liu SF (2013) Chronic intermittent hypoxia down-regulates endothelial nitric oxide synthase expression by an NF-kappaB-dependent mechanism. Sleep Med 14: 165-171.
48. Row BW (2007) Intermittent hypoxia and cognitive function: implications from chronic animal models. Adv Exp Med Biol 618: 51-67.
49. Parpura V, Haydon PG, Henderson E (1993) Three-dimensional imaging of living neurons and glia with the atomic force microscope. J Cell Sci 104 (Pt2): 427-432.
50. Foell D, Wittkowski H, Vogl T, Roth J (2007) S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol 81: 28-37.
51. Bernardini C, Lattanzi W, Businaro R, Leone S, Corvino V, et al. (2010) Transcritpional effects of S100B on neuroblastoma cells: perturbation of cholesterol homeostasis and interference on the cell cycle. Gene Expr 14: 345-359.
52. Braga CW, Martinez D, Wofchuk S, Portela LV, Souza DO (2006) S100B and NSE serum levels in obstructive sleep apnea syndrome. Sleep Med 7: 431-435.
53. Sonka K, Kelemen J, Kemlink D, Volna J, Pretl M, et al. (2007) Evening and morning plasma levels of protein S100B in patients with obstructive sleep apnea. Neuro Endocrinol Lett 28: 575-579.
54. Williams A, Scharf SM (2007) Obstructive sleep apnea, cardiovascular disease, and inflammation-is NF-kappaB the key? Sleep Breath 11: 69-76.
55. Krueger JM, Obal FJ, Fang J, Kubota T, Taishi P (2001) The role of cytokines in physiological sleep regulation. Ann N Y Acad Sci 933: 211-221.
56. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32: 638-647.
57. Vincent AM, Perrone L, Sullivan KA, Backus C, Sastry AM, et al. (2007) Receptor for advanced glycation end products activation injures primary sensory neurons via oxidative stress. Endocrinology 148: 548-558.
58. Inta I, Paxian S, Maegele I, Zhang W, Pizzi M, et al. (2006) Bim and Noxa are candidates to mediate the deleterious effect of the NF-kappa B subunit RelA in cerebral ischemia. J Neurosci 26: 12896-12903.
59. Bierhaus A, Stern DM, Nawroth PP (2006) RAGE in inflammation: a new therapeutic target? Curr Opin Investig Drugs 7: 985-991.
60. Wu KM, Lin CC, Chiu CH, Liaw SF (2010) Effect of treatment by nasal continuous positive airway pressure on serum high mobility group box-1 protein in obstructive sleep apnea. Chest 137: 303-309.
61. Brett J, Schmidt AM, Yan SD, Zou YS, Weidman E, et al. (1993) Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol 143: 1699-1712.
62. Okun E, Griffioen KJ, Mattson MP (2011) Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci 34: 269-281.