Effects of peripheral inflammation on the blood-spinal cord barrier

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Xanthos, Dimitris N ^a   Püngel, Isabella ^a   Wunderbaldinger, Gabriele ^a   Sandkühler, Jürgen ^a  

^a Medical University of Vienna   (Austria)

Author keywords

Blood spinal cord barrier; Capsaicin; Carrageenan; Female; Immunoglobulin; Inflammation; Lumbar; Occludin; Spinal cord

Indexed keywords

CAPSAICIN; CARRAGEENAN; EVANS BLUE; FLUORESCEIN SODIUM; FLUORESCENT DYE; IMMUNOGLOBULIN; OCCLUDIN; IMMUNOGLOBULIN G; MEMBRANE PROTEIN;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SPINAL CORD BARRIER; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; IMMUNOGLOBULIN PRODUCTION; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; LUMBAR SPINAL CORD; MALE; MESENCEPHALON; MYELITIS; NOCICEPTION; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; THORACIC SPINAL CORD; ANIMAL; CHEMICALLY INDUCED DISORDER; INFLAMMATION; METABOLISM; SPINAL CORD;

ANIMALS; CARRAGEENAN; FEMALE; IMMUNOGLOBULIN G; INFLAMMATION; MALE; MEMBRANE PROTEINS; RATS; SEX FACTORS; SPINAL CORD;

EID: 84862240368     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-44     Document Type: Article

References (72)

1. Bartanusz V, Jezova D, Alajajian B, Digicaylioglu M. The blood-spinal cord barrier: morphology and clinical implications. Ann Neurol 2011, 70:194-206. 10.1002/ana.22421, 21674586.
2. Choi YK, Kim K-W. Blood-neural barrier: its diversity and coordinated cell-to-cell communication. BMB Rep 2008, 41:345-352. 10.5483/BMBRep.2008.41.5.345, 18510863.
3. de Vries HE, Kuiper J, de Boer AG, Van Berkel TJ, Breimer DD. The blood-brain barrier in neuroinflammatory diseases. Pharmacol Rev 1997, 49:143-155.
4. Sharma HS. Pathophysiology of blood-spinal cord barrier in traumatic injury and repair. Curr Pharm Design 2005, 11:1353-1389.
5. Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H, et al. Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS ONE 2007, 2:e1205-e1205. 10.1371/journal.pone.0001205, 2075163, 18030339.
6. Morgan L, Shah B, Rivers LE, Barden L, Groom AJ, Chung R, et al. Inflammation and dephosphorylation of the tight junction protein occludin in an experimental model of multiple sclerosis. Neuroscience 2007, 147:664-673. 10.1016/j.neuroscience.2007.04.051, 17560040.
7. Gordh T, Chu H, Sharma HS. Spinal nerve lesion alters blood-spinal cord barrier function and activates astrocytes in the rat. Pain 2006, 124:211-221. 10.1016/j.pain.2006.05.020, 16806707.
8. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis 2010, 37:13-25. 10.1016/j.nbd.2009.07.030, 19664713.
9. Marchi N, Teng Q, Ghosh C, Fan Q, Nguyen MT, Desai NK, et al. Blood-brain barrier damage, but not parenchymal white blood cells, is a hallmark of seizure activity. Brain Res 2010, 1353:176-186. 2933328, 20599815.
10. Li Y-Q, Chen P, Haimovitz-Friedman A, Reilly RM, Wong CS. Endothelial apoptosis initiates acute blood-brain barrier disruption after ionizing radiation. Cancer Res 2003, 63:5950-5956.
11. Škultétyová I, Tokarev D, Ježová D. Stress-induced increase in blood-brain barrier permeability in control and monosodium glutamate-treated rats. Brain Res Bull 1998, 45:175-178. 10.1016/S0361-9230(97)00335-3, 9443836.
12. Sharma HS, Ali SF. Acute administration of 3,4-methylenedioxymethamphetamine induces profound hyperthermia, blood-brain barrier disruption, brain edema formation, and cell injury. Ann N Y Acad Sci 2008, 1139:242-258. 10.1196/annals.1432.052, 18991870.
13. Kiyatkin EA, Sharma HS. Permeability of the blood-brain barrier depends on brain temperature. Neuroscience 2009, 161:926-939. 10.1016/j.neuroscience.2009.04.004, 2694729, 19362131.
14. Stokely ME, Orr EL. Acute effects of calvarial damage on dural mast cells, pial vascular permeability, and cerebral cortical histamine levels in rats and mice. J Neurotrauma 2008, 25:52-61. 10.1089/neu.2007.0397, 18355158.
15. Strbian D, Karjalainen-Lindsberg M-L, Tatlisumak T, Lindsberg PJ. Cerebral mast cells regulate early ischemic brain swelling and neutrophil accumulation. J Cereb Blood Flow Metab 2006, 26:605-612. 10.1038/sj.jcbfm.9600228, 16163296.
16. Sayed BA, Christy AL, Walker ME, Brown MA. Meningeal mast cells affect early T cell central nervous system infiltration and blood-brain barrier integrity through TNF: a role for neutrophil recruitment?. J Immunol 2010, 184:6891-6900. 10.4049/jimmunol.1000126, 20488789.
17. Gillardon F, Vogel J, Hein S, Zimmermann M, Uhlmann E. Inhibition of carrageenan-induced spinal c-Fos activation by systemically administered c-fos antisense oligodeoxynucleotides may be facilitated by local opening of the blood-spinal cord barrier. J Neurosci Res 1997, 47:582-589. 10.1002/(SICI)1097-4547(19970315)47:6<582::AID-JNR3>3.0.CO;2-9, 9089206.
18. Lu P, Gonzales C, Chen Y, Adedoyin A, Hummel M, Kennedy JD, et al. CNS penetration of small molecules following local inflammation, widespread systemic inflammation or direct injury to the nervous system. Life Sci 2009, 85:450-456. 10.1016/j.lfs.2009.07.009, 19632245.
19. Echeverry S, Shi XQ, Rivest S, Zhang J. Peripheral nerve injury alters blood-spinal cord barrier functional and molecular integrity through a selective inflammatory pathway. J Neurosci 2011, 31:10819-10828. 10.1523/JNEUROSCI.1642-11.2011, 21795534.
20. Beggs S, Liu XJ, Kwan C, Salter MW. Peripheral nerve injury and TRPV1-expressing primary afferent C-fibers cause opening of the blood-brain barrier. Mol Pain 2010, 6:74-79. 10.1186/1744-8069-6-74, 2984489, 21044346.
21. Sharma HS, Patnaik R, Sharma A, Muresanu DF. F108 Cerebrolysim attenuates blood-spinal cord barrier disruption,astrocytic activation and neuronal damage in the rat spinal following formalin nociception. Eur J Pain 2012, 5:105.
22. Oztas B, Camurcu S, Kaya M. Influence of sex on the blood brain barrier permeability during bicuculline-induced seizures. Int J Neurosci 1992, 65:131-139. 10.3109/00207459209003284, 1341674.
23. Bake S, Friedman JA, Sohrabji F. Reproductive age-related changes in the blood brain barrier: expression of IgG and tight junction proteins. Microvasc Res 2009, 78:413-424. 10.1016/j.mvr.2009.06.009, 2784250, 19591848.
24. Sun D, Whitaker JN, Wilson DB. Regulatory T cells in experimental allergic encephalomyelitis. III. Comparison of disease resistance in Lewis and Fischer 344 rats. Eur J Immunol 1999, 29:1101-1106. 10.1002/(SICI)1521-4141(199904)29:04<1101::AID-IMMU1101>3.0.CO;2-#, 10229076.
25. McCaffrey G, Seelbach MJ, Staatz WD, Nametz N, Quigley C, Campos CR, et al. Occludin oligomeric assembly at tight junctions of the blood-brain barrier is disrupted by peripheral inflammatory hyperalgesia. J Neurochem 2008, 106:2395-2409. 10.1111/j.1471-4159.2008.05582.x, 2656385, 18647175.
26. Gordh T, Sharma HS. Chronic spinal nerve ligation induces microvascular permeability disturbances, astrocytic reaction, and structural changes in the rat spinal cord. Acta Neurochir Suppl 2006, 96:335-340. 10.1007/3-211-30714-1_70, 16671481.
27. Kaya M, Gurses C, Kalayci R, Ekizoglu O, Ahishali B, Orhan N, et al. Morphological and functional changes of blood-brain barrier in kindled rats with cortical dysplasia. Brain Res 2008, 1208:181-191.
28. Miller DS. Regulation of P-glycoprotein and other ABC drug transporters at the blood-brain barrier. Trends Pharmacol Sci 2010, 31:246-254. 10.1016/j.tips.2010.03.003, 2882496, 20417575.
29. Wilson EH, Weninger W, Hunter CA. Trafficking of immune cells in the central nervous system. J Clin Invest 2010, 120:1368-1379. 10.1172/JCI41911, 2860945, 20440079.
30. Zehendner CM, Librizzi L, de Curtis M, Kuhlmann CR, Luhmann HJ. Caspase-3 contributes to ZO-1 and Cl-5 tight-junction disruption in rapid anoxic neurovascular unit damage. PLoS ONE 2011, 6:e16760. 10.1371/journal.pone.0016760, 3043060, 21364989.
31. Hirase T, Staddon JM, Saitou M, Ando-Akatsuka Y, Itoh M, Furuse M, et al. Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 1997, 110:1603-1613.
32. Wong V, Gumbiner BM. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 1997, 136:399-409. 10.1083/jcb.136.2.399, 2134825, 9015310.
33. Bennett J, Basivireddy J, Kollar A, Biron KE, Reickmann P, Jefferies WA, et al. Blood-brain barrier disruption and enhanced vascular permeability in the multiple sclerosis model EAE. J Neuroimmunol 2010, 229:180-191. 10.1016/j.jneuroim.2010.08.011, 20832870.
34. Zhao Y, Liu X, Yu A, Zhou Y, Liu B. Diabetes-related alteration of occludin expression in rat blood-spinal cord barrier. Cell Biochem Biophys 2010, 58:141-145. 10.1007/s12013-010-9099-7, 20717745.
35. Huber JD, Hau VS, Borg L, Campos CR, Egleton RD, Davis TP. Blood-brain barrier tight junctions are altered during a 72-h exposure to l-carrageenan-induced inflammatory pain. Am J Physiol Heart Circ Physiol 2002, 283:H1531-H1537.
36. Sakakibara A, Furuse M, Saitou M, Ando-Akatsuka Y, Tsukita S. Possible involvement of phosphorylation of occludin in tight junction formation. J Cell Biol 1997, 137:1393-1401. 10.1083/jcb.137.6.1393, 2132539, 9182670.
37. Feldman GJ, Mullin JM, Ryan MP. Occludin: structure, function and regulation. Adv Drug Deliv Rev 2005, 57:883-917. 10.1016/j.addr.2005.01.009, 15820558.
38. Ge S, Pachter JS. Isolation and culture of microvascular endothelial cells from murine spinal cord. J Neuroimmunol 2006, 177:209-214. 10.1016/j.jneuroim.2006.05.012, 16806499.
39. Pan W, Banks WA, Kastin AJ. Permeability of the blood-brain and blood-spinal cord barriers to interferons. J Neuroimmunol 1997, 76:105-111. 10.1016/S0165-5728(97)00034-9, 9184639.
40. Prockop LD, Naidu KA, Binard JE, Ransohoff J. Selective permeability of [3H]-D-mannitol and [14C]-carboxyl-inulin across the blood-brain barrier and blood-spinal cord barrier in the rabbit. J Spinal Cord Med 1995, 18:221-226.
41. Trojano M, Defazio G, Ricchiuti F, De Salvia R, Livrea P. Serum IgG to brain microvascular endothelial cells in multiple sclerosis. J Neurol Sci 1996, 143:107-113. 10.1016/S0022-510X(96)00184-0, 8981306.
42. Fullerton SM, Shirman GA, Strittmatter WJ, Matthew WD. Impairment of the blood-nerve and blood-brain barriers in apolipoprotein e knockout mice. Exp Neurol 2001, 169:13-22. 10.1006/exnr.2001.7631, 11312553.
43. McKenzie AL, Hall JJ, Aihara N, Fukuda K, Noble LJ. Immunolocalization of endothelin in the traumatized spinal cord: relationship to blood-spinal cord barrier breakdown. J Neurotrauma 1995, 12:257-268. 10.1089/neu.1995.12.257, 7473800.
44. Nicaise C, Mitrecic D, Demetter P, De Decker R, Authelet M, Boom A, et al. Impaired blood-brain and blood-spinal cord barriers in mutant SOD1-linked ALS rat. Brain Res 2009, 1301:152-162.
45. Nesic O, Lee J, Ye Z, Unabia GC, Rafati D, Hulsebosch CE, et al. Acute and chronic changes in aquaporin 4 expression after spinal cord injury. Neuroscience 2006, 143:779-792. 10.1016/j.neuroscience.2006.08.079, 1894918, 17074445.
46. Sandkühler J. Spinal plasticity and pain. Wall and Melzack's Textbook of Pain 2012, Elsevier, Churchill Livingstone, Koltzenburg M, McMahon S, in the press.
47. Honda M, Nakagawa S, Hayashi K, Kitagawa N, Tsutsumi K, Nagata I, et al. Adrenomedullin improves the blood-brain barrier function through the expression of claudin-5. Cell Mol Neurobiol 2006, 26:109-118. 10.1007/s10571-006-9028-x, 16763778.
48. Huai-Yun H, Secrest DT, Mark KS, Carney D, Brandquist C, Elmquist WF, et al. Expression of multidrug resistance-associated protein (MRP) in brain microvessel endothelial cells. Biochem Biophys Res Commun 1998, 243:816-820. 10.1006/bbrc.1997.8132, 9500978.
49. Sun H, Johnson DR, Finch RA, Sartorelli AC, Miller DW, Elmquist WF. Transport of fluorescein in MDCKII-MRP1 transfected cells and mrp1-knockout mice. Biochem Biophys Res Commun 2001, 284:863-869. 10.1006/bbrc.2001.5062, 11409873.
50. Hawkins BT, Lundeen TF, Norwood KM, Brooks HL, Egleton RD. Increased blood-brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases. Diabetologia 2007, 50:202-211.
51. Hawkins BT, Ocheltree SM, Norwood KM, Egleton RD. Decreased blood-brain barrier permeability to fluorescein in streptozotocin-treated rats. Neurosci Lett 2007, 411:1-5. 10.1016/j.neulet.2006.09.010, 1785293, 17110033.
52. Costello AH, Hargreaves KM. Suppression of carrageenan-induced hyperalgesia, hyperthermia and edema by a bradykinin antagonist. Eur J Pharmacol 1989, 171:259-263. 10.1016/0014-2999(89)90118-0, 2482813.
53. Wolka AM, Huber JD, Davis TP. Pain and the blood-brain barrier: obstacles to drug delivery. Adv Drug Deliv Rev 2003, 55:987-1006. 10.1016/S0169-409X(03)00100-5, 12935941.
54. Sharma HS, Kiyatkin EA. Rapid morphological brain abnormalities during acute methamphetamine intoxication in the rat: an experimental study using light and electron microscopy. J Chem Neuroanat 2009, 37:18-32. 10.1016/j.jchemneu.2008.08.002, 2638124, 18773954.
55. Kiyatkin EA, Brown PL, Sharma HS. Brain edema and breakdown of the blood-brain barrier during methamphetamine intoxication: critical role of brain hyperthermia. Eur J Neurosci 2007, 26:1242-1253. 10.1111/j.1460-9568.2007.05741.x, 17767502.
56. Tall JM, Crisp T. Effects of gender and gonadal hormones on nociceptive responses to intraplantar carrageenan in the rat. Neurosci Lett 2004, 354:239-241. 10.1016/j.neulet.2003.09.081, 14700740.
57. Greenspan JD, Craft RM, LeResche L, Arendt-Nielsen L, Berkley KJ, Fillingim RB, et al. Studying sex and gender differences in pain and analgesia: a consensus report. Pain 2007, 132:S26-S45. 2823483, 17964077.
58. Seker FB, Akgul S, Oztas B. Lifelong consumption of sodium selenite: gender differences on blood-brain barrier permeability in convulsive, hypoglycemic rats. Biol Trace Elem Res 2008, 124:12-19. 10.1007/s12011-008-8101-3, 18305911.
59. Oztas B, Akgul S, Seker FB. Gender difference in the influence of antioxidants on the blood-brain barrier permeability during pentylenetetrazol-induced seizures in hyperthermic rat pups. Biol Trace Elem Res 2007, 118:77-83. 10.1007/s12011-007-0020-1, 17848733.
60. Minami T, Sakita Y, Ichida S, Dohi Y. Gender difference regarding selenium penetration into the mouse brain. Biol Trace Elem Res 2002, 89:85-93. 10.1385/BTER:89:1:85, 12413054.
61. Sirav B, Seyhan N. Effects of radiofrequency radiation exposure on blood-brain barrier permeability in male and female rats. Electromagn Biol Med 2011, 30:253-260. 10.3109/15368378.2011.600167, 22047463.
62. Brooks TA, Nametz N, Charles R, Davis TP. Diclofenac attenuates the regional effect of lambda-carrageenan on blood-brain barrier function and cytoarchitecture. J Pharmacol Exp Ther 2008, 325:665-673. 10.1124/jpet.107.135632, 18305016.
63. Campos CR, Ocheltree SM, Hom S, Egleton RD, Davis TP. Nociceptive inhibition prevents inflammatory pain induced changes in the blood-brain barrier. Brain Res 2008, 1221:6-13. 2583462, 18554577.
64. Bake S, Sohrabji F. 17b-estradiol differentially regulates blood-brain barrier permeability in young and aging female rats. Endocrinology 2004, 145:5471-5475. 10.1210/en.2004-0984, 15471968.
65. Huber JD, Witt KA, Hom S, Egleton RD, Mark KS, Davis TP. Inflammatory pain alters blood-brain barrier permeability and tight junctional protein expression. Am J Physiol Heart Circ Physiol 2001, 280:H1241-H1248.
66. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005, 57:173-185. 10.1124/pr.57.2.4, 15914466.
67. Lisi L, Navarra P, Cirocchi R, Sharp A, Stigliano E, Feinstein DL, et al. Rapamycin reduces clinical signs and neuropathic pain in a chronic model of experimental autoimmune encephalomyelitis. J Neuroimmunol 2012, 243:43-51. 10.1016/j.jneuroim.2011.12.018, 22264993.
68. Lin T, Li K, Zhang F-Y, Zhang Z-K, Light AR, Fu K-Y. Dissociation of spinal microglia morphological activation and peripheral inflammation in inflammatory pain models. J Neuroimmunol 2007, 192:40-48. 10.1016/j.jneuroim.2007.09.003, 2198900, 17919739.
69. Xanthos DN, Gaderer S, Drdla R, Nuro E, Abramova A, Ellmeier W, et al. Central nervous system mast cells in peripheral inflammatory nociception. Mol Pain 2011, 7:42-58. 10.1186/1744-8069-7-42, 3123586, 21639869.
70. Cahill CM, Dray A, Coderre TJ. Enhanced thermal antinociceptive potency and anti-allodynic effects of morphine following spinal administration of endotoxin. Brain Res 2003, 960:209-218. 10.1016/S0006-8993(02)03885-4, 12505674.
71. Nicolussi EM, Huck S, Lassmann H, Bradl M. The cholinergic anti-inflammatory system limits T cell infiltration into the neurodegenerative CNS, but cannot counteract complex CNS inflammation. Neurobiol Dis 2009, 35:24-31. 10.1016/j.nbd.2009.03.010, 19344760.
72. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63. 10.1016/0165-0270(94)90144-9, 7990513.