Restraint stress-induced morphological changes at the blood-brain barrier in adult rats

Frontiers in Molecular Neuroscience

Volumn 8, Issue JAN2016, 2016, Pages

  Sántha, Petra ^a,d   Veszelka, Szilvia ^a   Hoyk, Zsófia ^a   Mészáros, Mária ^a   Walter, Fruzsina R ^a   Tóth, Andrea E ^a   Kiss, Lóránd ^a   Kincses, András ^a   Oláh, Zita ^b   Seprényi, György ^b   Rákhely, Gábor ^b   Dér, András ^a   Pákáski, Magdolna ^b   Kálmán, János ^b   Kittel, Ágnes ^c   Deli, Mária A ^a  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

^b UNIVERSITY OF SZEGED   (Hungary)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Blood brain barrier; Brain capillary ultra structure; Brain endothelial cell; GFAP; Glial endfeet; Glucose transporter 1; Restraint stress; Tight junction

Indexed keywords

CLAUDIN 5; GLUCOSE TRANSPORTER 1; OCCLUDIN;

ADULT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BODY WEIGHT; BRAIN CAPILLARY; BRAIN EDEMA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FRONTAL CORTEX; HIPPOCAMPUS; IMAGE ANALYSIS; IMMOBILIZATION STRESS; IMMUNOHISTOCHEMISTRY; MACROGLIA; MALE; NONHUMAN; RAT;

EID: 84957891779     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2015.00088     Document Type: Article

References (78)

1. Abbott, N. J. (2002). Astrocyte-endothelial interactions and blood-brain barrier permeability. J. Anat. 200, 629-638. doi: 10.1046/j.1469-7580.2002.00064.x
2. Abbott, N. J., Patabendige, A. A., Dolman, D. E., Yusof, S. R., and Begley, D. J. (2010). Structure and function of the blood-brain barrier. Neurobiol. Dis. 37, 13-25. doi: 10.1016/j.nbd.2009.07.030
3. Abbott, N. J., Rönnbäck, L., and Hansson, E. (2006). Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53. doi: 10.1038/nrn1824
4. Abdel-Rahman, A., Shetty, A. K., and Abou-Donia, M. B. (2002). Disruption of the blood-brain barrier and neuronal cell death in cingulate cortex, dentate gyrus, thalamus, and hypothalamus in a rat model of Gulf-War syndrome. Neurobiol. Dis. 10, 306-326. doi: 10.1006/nbdi.2002.0524
5. Argandofia, E. G., Bengoetxea, H., Bulnes, S., Rico-Barrio, I., Ortuzar, N., and Lafuente, J. V. (2012). Effect of intracortical vascular endothelial growth factor infusion and blockade during the critical period in the rat visual cortex. Brain Res. 1473, 141-154. doi: 10.1016/j.brainres.2012.07.008
6. Bechter, K. (2013). Updating the mild encephalitis hypothesis of schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 42, 71-91. doi: 10.1016/j.pnpbp.2012.06.019
7. Belova, I., and Jonsson, G. (1982). Blood-brain barrier permeability and immobilization stress. Acta Physiol. Scand. 116, 21-29. doi: 10.1111/j.1748-1716.1982.tb10594.x
8. Boado, R. J., and Pardridge, W. M. (2002). Glucose deprivation and hypoxia increase the expression of the GLUT-1 glucose transporter via a specific mRNA cis-acting regulatory element. J. Neurochem. 80, 552-554. doi:10.1046/j.0022-3042.2001.00756.x
9. Chen, Y., Andres, A. L., Frotscher, M., and Baram, T. Z. (2012). Tuning synaptic transmission in the hippocampus by stress: the CRH system. Front. Cell. Neurosci. 6:13. doi: 10.3389/fncel.2012.00013
10. Chiba, S., Numakawa, T., Ninomiya, M., Richards, M. C., Wakabayashi, C., and Kunugi, H. (2012). Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol. Biol. Psychiatry 39, 112-119. doi: 10.1016/j.pnpbp.2012.05.018
11. Chrousos, G. P. (2009). Stress and disorders of the stress system. Nat. Rev. Endocrinol. 5, 374-381. doi: 10.1038/nrendo.2009.106
12. Clausius, R. (1850). On the motive power of heat, and on the laws which can be deduced from it for the theory of heat. Annalen der Physick 155, 500-524. doi: 10.1002/andp.18501550403
13. Dalkara, T., andAlarcon-Martinez, L. (2015). Cerebral microvascular pericytes and neurogliovascular signaling in health and disease. Brain Res. 1623, 3-17. doi: 10.1016/j.brainres.2015.03.047
14. De Klerk, O. L., Bosker, F. J., Luurtsema, G., Nolte, I. M., Dierckx, R., Den Boer, J. A., et al. (2011). The role of p-glycoprotein in psychiatric disorders: a reliable guard of the brain? Cent. Nerv. Syst. Agents Med. Chem. 11, 197-209. doi: 10.2174/187152411798047744
15. Deli, M. A. (2005). “The role ofblood-brain barrier in neurodegenerative diseases" in Molecular Bases of Neurodegeneration, eds I. Di Liegro and G. Savettieri (Trivandrum: Research Signpost), 137-161.
16. Detka, J., Kurek, A., Basta-Kaim, A., Kubera, M., Lasoň, W., and Budziszewska, B. (2014). Elevated brain glucose and glycogen concentrations in an animal model ofdepression. Neuroendocrinology 100, 178-190. doi: 10.1159/000368607
17. Emsley, J. G., and Macklis, J. D. (2006). Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol. 2, 175-186. doi: 10.1017/S1740925X06000202
18. Erickson, M. A., and Banks, W. A. (2013). Blood-brain barrier dysfunction as a cause and consequence of Alzheimer's disease. J. Cereb. Blood Flow Metab. 33, 1500-1513. doi: 10.1038/jcbfm.2013.135
19. Errede, M., Girolamo, F., Ferrara, G., Strippoli, M., Morando, S., Boldrin, V., et al. (2012). Blood-brain barrier alterations in the cerebral cortex in experimental autoimmune encephalomyelitis. J. Neuropathol. Exp. Neurol. 71, 840-854. doi: 10.1097/NEN.0b013e31826ac110
20. Esposito, P., Chandler, N., Kandere, K., Basu, S., Jacobson, S., Connolly, R., et al. (2002). Corticotropin-releasing hormone and brain mast cells regulate blood- brain-barrier permeability induced by acute stress. J. Pharmacol. Exp. Ther. 303, 1061-1066. doi: 10.1124/jpet.102.038497
21. Ezan, P., André, P., Cisternino, S., Saubaméa, B., Boulay, A. C., Doutremer, S., et al. (2012). Deletion of astroglial connexins weakens the blood-brain barrier. J. Cereb. Blood Flow Metab. 32, 1457-1467. doi: 10.1038/jcbfm.2012.45
22. Farkas, A. S., Acsai, K., Nagy, N., Tóth, A., Fülöp, F., Seprényi, G., et al. (2008). Na(+)/Ca(2+) exchanger inhibition exerts a positive inotropic effect in the rat heart, but fails to influence the contractility of the rabbit heart. Br. J. Pharmacol. 154, 93-104. doi: 10.1038/bjp.2008.83
23. Filaretova, L., Morozova, O., Laszlo, F., Morschl, E., and Zelena, D. (2013). Does chronic stress enhance the risk of diseases? Endocr. Regul. 47, 177-188. doi:10.4149/endo_2013_04_177
24. Foti Cuzzola, V., Galuppo, M., Iori, R., De Nicola, G. R., Cassata, G., Giacoppo, S., et al. (2013). Beneficial effects of (RS)-glucoraphanin on the tight junction dysfunction in a mouse model of restraint stress. Life Sci. 93, 288-305. doi: 10.1016/j.lfs.2013.07.003
25. Gajkowska, B., Kosson, A., Sacharczuk, M., Kosson, P., and Lipkowski, A. W. (2011) Blood-brain barrier permeability differentiates Sadowski mouse lines of high and low stress-induced analgesia: electron microscopy analysis. Folia Neuropathol. 49, 311-318.
26. Gonzalez, R. C., Woods, R. E., and Eddins, S. L. (2003). Digital Image Processing Using MATLAB. New Jersey, NJ: Prentice Hall.
27. Grigoryan, G., Biella, G., Albani, D., Forloni, G., and Segal, M. (2014). Stress impairs synaptic plasticity in triple-transgenic Alzheimer's disease mice: rescue by ryanodine. Neurodegener. Dis. 13, 135-138. doi: 10.1159/000354231
28. Hanin, I. (1996). The Gulf War, stress and a leaky blood-brain barrier. Nat. Med. 2, 1307-1308. doi: 10.1038/nm1296-1307
29. Hartz, A. M., Bauer, B., Soldner, E. L., Wolf, A., Boy, S., Backhaus, R., et al. (2012) Amyloid-ß contributes to blood-brain barrier leakage in transgenic human amyloid precursor protein mice and in humans with cerebral amyloid angiopathy. Stroke 43, 514-523. doi: 10.1161/STROKEAHA.111.627562
30. Haseloff, R. F., Blasig, I. E., Bauer, H. C., and Bauer, H. (2005). In search of the astrocytic factor(s) modulating blood-brain barrier functions in brain capillary endothelial cells in vitro. Cell. Mol. Neurobiol. 25, 25-39. doi: 10.1007/s10571-004-1375-x
31. Hewett, J. A. (2009). Determinants of regional and local diversity within the astroglial lineage of the normal central nervous system. J. Neurochem. 110, 1717-1736. doi: 10.1111/j.1471-4159.2009.06288.x
32. Hooijmans, C. R., Graven, C., Dederen, P. J., Tanila, H., van Groen, T., and Kiliaan, A. J. (2007). Amyloid beta deposition is related to decreased glucose transporter-1 levels and hippocampal atrophy in brains of aged APP/PS1 mice. Brain Res. 1181, 93-103. doi: 10.1016/j.brainres.2007.08.063
33. Horwood, N., and Davies, D. C. (1994). Immunolabelling of hippocampal microvessel glucose transporter protein is reduced in Alzheimer's disease. Virchows Arch. 425, 69-72. doi: 10.1007/BF00193951
34. Hsu, S. M., Raine, L., and Fanger, H. (1981). The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics. Am. J. Clin. Pathol. 75,816-821.
35. Huang, R. R., Hu, W., Yin, Y. Y., Wang, Y. C., Li, W. P., and Li, W. Z. (2015). Chronic restraint stress promotes learning and memory impairment due to enhanced neuronal endoplasmic reticulum stress in the frontal cortex and hippocampus in male mice. Int. J. Mol. Med. 35, 553-559. doi: 10.3892/ijmm.2014.2026
36. Huber, J. D., Egleton, R. D., and Davis, T. P. (2001). Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci. 24, 719-725. doi: 10.1016/S0166-2236(00)02004-X
37. Imbe, H., Kimura, A., Donishi, T., and Kaneoke, Y. (2012). Chronic restraint stress decreases glial fibrillary acidic protein and glutamate transporter in the periaqueductal gray matter. Neuroscience 223, 209-218. doi: 10.1016/j.neuroscience.2012.08.007
38. Jaggi, A. S., Bhatia, N., Kumar, N., Singh, N., Anand, P., and Dhawan, R. (2011). A review on animal models for screening potential anti-stress agents. Neurol. Sci. 32, 993-1005. doi: 10.1007/s10072-011-0770-6
39. Jang, S., Suh, S. H., Yoo, H. S., Lee, Y. M., and Oh, S. (2008). Changes in iNOS, GFAP and NR1 expression in various brain regions and elevation of sphingosine-1-phosphate in serum after immobilized stress. Neurochem. Res. 33,842-851. doi: 10.1007/s11064-007-9523-6
40. Jeong, Y. H., Park, C. H., Yoo, J., Shin, K. Y., Ahn, S. M., Kim, H. S., et al. (2006). Chronic stress accelerates learning and memory impairments and increases amyloid deposition in APPV717I-CT100 transgenic mice, an Alzheimer's disease model. FASEB J. 20, 729-731. doi: 10.1096/fj.05-4265fje
41. Jiao, H., Wang, Z., Liu, Y., Wang, P., and Xue, Y. (2011). Specific role of tight junction proteins claudin-5, occludin, and ZO-1 of the blood-brain barrier in a focal cerebral ischemic insult. J. Mol. Neurosci. 44, 130-139. doi: 10.1007/s12031-011-9496-4
42. Kelly, S. D., Harrell, C. S., and Neigh, G. N. (2014). Chronic stress modulates regional cerebral glucose transporter expression in an age- specific and sexually-dimorphic manner. Physiol. Behav. 126, 39-49. doi: 10.1016/j.physbeh.2013.12.002
43. Kim, J. I., Lee, J. W., Lee, Y. A., Lee, D. H., Han, N. S., Choi, Y. K., et al. (2013). Sexual activity counteracts the suppressive effects of chronic stress on adult hippocampal neurogenesis and recognition memory. Brain Res. 1538, 26-40. doi: 10.1016/j.brainres.2013.09.007
44. Kim, J. J., and Diamond, D. M. (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3, 453-462. doi: 10.1038/nrn849
45. Kniesel, U., and Wolburg, H. (1993). Tight junction complexity in the retinal pigment epithelium of the chicken during development. Neurosci. Lett. 149, 71-74. doi: 10.1016/0304-3940(93)90350-T
46. Leybaert, L., De Bock, M., Van Moorhem, M., Decrock, E., and De Vuyst, E. (2007). Neurobarrier coupling in the brain: adjusting glucose entry with demand. J. Neurosci. Res. 85, 3213-3220. doi: 10.1002/jnr.21189
47. Lim, D. C., and Pack, A. I. (2014). Obstructive sleep apnea and cognitive impairment: addressing the blood-brain barrier. SleepMed. Rev. 18, 35-48. doi: 10.1016/j.smrv.2012.12.003
48. Maggio, N., Shavit-Stein, E., Dori, A., Blatt, I., and Chapman, J. (2013). Prolonged systemic inflammation persistently modifies synaptic plasticity in the hippocampus: modulation by the stress hormones. Front. Mol. Neurosci. 6:46. doi: 10.3389/fnmol.2013.00046
49. Meszaros, Z. S., Perl, A., and Faraone, S. V. (2012). Psychiatric symptoms in systemic lupus erythematosus: a systematic review. J. Clin. Psychiatry 73, 993-1001. doi: 10.4088/jcp.11r07425
50. Najjar, S., Pearlman, D. M., Devinsky, O., Najjar, A., and Zagzag, D. (2013). Neurovascular unit dysfunction with blood-brain barrier hyperpermeability contributes to major depressive disorder: a review of clinical and experimental evidence. J.Neuroinflammation. 10:142. doi: 10.1186/1742-2094-10-142
51. Neuwelt, E. A., Bauer, B., Fahlke, C., Fricker, G., Iadecola, C., Janigro, D., et al. (2011). Engaging neuroscience to advance translational research in brain barrierbiology. Nat. Rev.Neurosci. 12, 169-182. doi: 10.1038/nrn2995
52. Northrop, N. A., and Yamamoto, B. K. (2012). Persistent neuroinflammatory effects of serial exposure to stress and methamphetamine on the blood-brain barrier. J. Neuroimmune Pharmacol. 7, 951-968. doi: 10.1007/s11481-012-9391-y
53. Oberheim, N. A., Goldman, S. A., and Nedergaard, M. (2012). Heterogeneity of astrocytic form and function. MethodsMol Biol. 814, 23-45. doi:10.1007/978-1-61779-452-0_3
54. Pekny, M., Stanness, K. A., Eliasson, C., Betsholtz, C., and Janigro, D. (1998). Impaired induction of blood-brain barrier properties in aortic endothelial cells by astrocytes from GFAP-deficient mice. Glia. 22, 390-400.
55. Peppiatt, C. M., Howarth, C., Mobbs, P., and Attwell, D. (2006). Bidirectional control of CNS capillary diameter by pericytes. Nature 443, 700-704. doi: 10.1038/nature05193
56. Pitman, D. L., Ottenweller, J. E., and Natelson, B. H. (1988). Plasma corticosterone levels during repeated presentation of two intensities of restraint stress: chronic stress and habituation. Physiol. Behav. 43, 47-55. doi: 10.1016/0031-9384(88)90097-2
57. Radley, J. J., Rocher, A. B., Miller, M., Janssen, W. G., Liston, C., Hof, P. R., et al. (2006). Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb. Cortex 16, 313-320. doi: 10.1093/cercor/bhi104
58. Sántha, P., Pákáski, M., Fazekas, O. C., Fodor, E. K., Kálmán, S., Kálmán, J., et al. (2012). Restraint stress in rats alters gene transcription and protein translation in the hippocampus. Neurochem. Res. 37, 958-964. doi:10.1007/s11064-011-0688-7
59. Schoenfeld, T. J., and Gould, E. (2013). Differential effects of stress and glucocorticoids on adultneurogenesis. Curr. Top. Behav. Neurosci. 15,139-164. doi:10.1007/7854_2012_233
60. Shah, Z. A., Sharma, P., and Vohora, S. B. (2003). Ginkgo biloba normalises stress-elevated alterations in brain catecholamines, serotonin and plasma corticosterone levels. Eur. Neuropsychopharmacol. 13, 321-325. doi: 10.1016/S0924-977X(03)00005-1
61. Shannon, C. E. (1948). A mathematical theory of communication. Bell Syst. Tech. J. 27, 379-423,623-656.
62. Sharma, H. S., Cervós-Navarro, J., and Dey, P. K. (1991). Increased blood- brain barrier permeability following acute short-term swimming exercise in conscious normotensive young rats. Neurosci. Res. 10, 211-221. doi: 10.1016/0168-0102(91)90058-7
63. Sharma, H. S., and Dey, P. K. (1988). EEG changes following increased blood- brain barrier permeability under long-term immobilization stress in young rats. Neurosci. Res. 5, 224-239. doi: 10.1016/0168-0102(88)90051-X
64. Sharma, H. S., Sharma, A., Mössler, H., and Muresanu, D. F. (2012). Neuroprotective effects of cerebrolysin, a combination of different active fragments of neurotrophic factors and peptides on the whole body hyperthermia-induced neurotoxicity: modulatory roles of co-morbidity factors and nanoparticle intoxication. Int. Rev. Neurobiol. 102, 249-276. doi: 10.1016/B978-0-12-386986-9.00010-7
65. Skultétyová, I., Tokarev, D., and Jezová, D. (1998). Stress-induced increase in blood-brain barrier permeability in control and monosodium glutamate- treated rats. Brain Res. Bull. 45, 175-178. doi: 10.1016/S0361-9230(97)00335-3
66. Song, L., and Pachter, J. S. (2004). Monocyte chemoattractant protein-1 alters expression of tight junction-associated proteins in brain microvascular endothelial cells. Microvasc. Res. 67, 78-89. doi: 10.1016/j.mvr.2003.07.001
67. Unal-Cevik, I., Kilinc, M., Gursoy-Ozdemir, Y., Gurer, G., and Dalkara, T. (2004). Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res. 1015, 169-174. doi:10.1016/j.brainres.2004.04.032
68. Vandenhaute, E., Culot, M., Gosselet, F., Dehouck, L., Godfraind, C., Franck, M., et al. (2012). Brain pericytes from stress-susceptible pigs increase blood-brain barrierpermeability in vitro. FluidsBarriers CNS 9:11. doi: 10.1186/2045-8118-9-11
69. Virgintino, D., Errede, M., Robertson, D., Capobianco, C., Girolamo, F., Vimercati, A., et al. (2004). Immunolocalization of tight junction proteins in the adult and developing human brain. Histochem. Cell Biol. 122, 51-59. doi: 10.1007/s00418-04-0665-1
70. Willis, C. L. (2012). Imaging in vivo astrocyte/endothelial cell interactions at the blood-brain barrier. Methods Mol Biol. 814, 515-529. doi: 10.1007/978-1-61779-452-0_34
71. Willis, C. L., Meske, D. S., and Davis, T. P. (2010). Protein kinase C activation modulates reversible increase in cortical blood-brain barrier permeability and tight junction protein expression during hypoxia and posthypoxic reoxygenation. J. Cereb. Blood Flow Metab. 30, 1847-1859. doi: 10.1038/jcbfm.2010.119
72. Wilson, R. S., Arnold, S. E., Schneider, J. A., Kelly, J. F., Tang, Y., and Bennett, D. A. (2006). Chronic psychological distress and risk ofAlzheimer’s disease in old age. Neuroepidemiology 27, 143-153. doi: 10.1159/000095761
73. Wilson, R. S., Schneider, J. A., Boyle, P. A., Arnold, S. E., Tang, Y., and Bennett, D. A. (2007). Chronic distress and incidence of mild cognitive impairment. Neurology 68, 2085-2092. doi: 10.1212/01.wnl.0000264930.97061.82
74. Winkler, E. A., Nishida, Y., Sagare, A. P., Rege, S. V., Bell, R. D., Perlmutter, D., et al. (2015). GLUT1 reductions exacerbate Alzheimer’s disease vasculo- neuronal dysfunction and degeneration. Nat. Neurosci. 18, 521-530. doi: 10.1038/nn.3966
75. Yang, Y., and Rosenberg, G. A. (2011). MMP-mediated disruption of claudin-5 in the blood-brain barrier of rat brain after cerebral ischemia. Methods Mol. Biol. 762, 333-345. doi: 10.1007/978-1-61779-185-7_24
76. Zitman, F. M., and Richter-Levin, G. (2013). Age and sex-dependent differences in activity, plasticity and response to stress in the dentate gyrus. Neuroscience 249, 21-30. doi: 10.1016/j.neuroscience.2013.05.030
77. Zlokovic, B. V. (2008). The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57, 178-201. doi: 10.1016/j.neuron.2008.01.003
78. Zlokovic, B. V. (2011). Neurovascular pathways to neurodegeneration in Alzheimer’s disease and other disorders. Nat. Rev. Neurosci. 12, 723-738. doi: 10.1038/nrn3114