Ghrelin prevents disruption of the blood-brain barrier after traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 2, 2012, Pages 385-393

  Lopez, Nicole E ^a   Krzyzaniak, Michael J ^a   Blow, Chelsea ^a   Putnam, James ^a   Ortiz Pomales, Yan ^a   Hageny, Ann Marie ^a   Eliceiri, Brian ^a   Coimbra, Raul ^a   Bansal, Vishal ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

aquaporin 4; blood brain barrier; ghrelin; traumatic brain injury

Indexed keywords

AQUAPORIN 4; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; GHRELIN; PROTEIN S100B;

ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; DRUG EFFECT; IMMUNOBLOTTING; MALE; MEMBRANE DAMAGE; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SHAM PROCEDURE; TRAUMATIC BRAIN INJURY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN INJURIES; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; GHRELIN; MALE; MICE; MICE, INBRED BALB C;

EID: 84856450304     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.2053     Document Type: Article

References (49)

1. Adelson, P.D., Jenkins, L.W., Hamilton, R.L., Robichaud, P., Tran, M.P., and Kochanek, P.M. (2001). Histopathologic re-sponse of the immature rat to diffuse traumatic brain injury. J. Neurotrauma 18, 967-976. (Pubitemid 33000668)
2. Bansal, V., Ryu, S.Y., Blow, C., Costantini, T., Loomis, W., Eli-ceiri, B., Baird, A., Wolf, P., and Coimbra, R. (2010). The hormone ghrelin prevents traumatic brain injury induced in-testinal dysfunction. J. Neurotrauma.
3. Barzo, P., Marmarou, A., Fatouros, P., Corwin, F., and Dunbar, J. (1996). Magnetic resonance imaging-monitored acute blood-brain barrier changes in experimental traumatic brain injury. J. Neurosurg. 85, 1113-1121. (Pubitemid 26396568)
4. Bloch, O., Papadopoulos, M.C., Manley, G.T., and Verkman, A.S. (2005). Aquaporin-4 gene deletion in mice increases focal edema associated with staphylococcal brain abscess. J. Neu-rochem. 95, 254-262. (Pubitemid 41384443)
5. Davies, D.C. (2002). Blood-brain barrier breakdown in septic encephalopathy and brain tumours. J. Anat. 200, 639-646. (Pubitemid 34823055)
6. Dietrich, W.D., Truettner, J., Zhao, W., Alonso, O.F., Busto, R., and Ginsberg, M.D. (1999). Sequential changes in glial fi-brillary acidic protein and gene expression following para-sagittal fluid-percussion brain injury in rats. J. Neurotrauma 16, 567-581. (Pubitemid 29350516)
7. Donkin, J.J., and Vink, R. (2010). Mechanisms of cerebral edema in traumatic brain injury: therapeutic developments. Curr. Opin. Neurol. 23, 293-299.
8. Ersahin, M., Toklu, H.Z., Erzik, C., Cetinel, S., Akakin, D., Velioglu-Ogunc, A., Tetik, S., Ozdemir, Z.N., Sener, G., and Yegen, B.C. (2010). The anti-inflammatory and neuroprotec-tive effects of ghrelin in subarachnoid hemorrhage-induced oxidative brain damage in rats. J. Neurotrauma 27, 1143-1155.
9. Faul, M. (2010). Traumatic brain injury in the United States: Emergency department visits, hospitalizations and deaths 2002-2006. http: //www.cdc.gov/traumaticbraininjury/tbi-ed.html.
10. Fazzina, G., Amorini, A.M., Marmarou, C.R., Fukui, S., Okuno, K., Dunbar, J.G., Glisson, R., Marmarou, A., and Kleindienst, A. (2010). The protein kinase C activator phorbol myristate acetate decreases brain edema by aquaporin 4 downregulation after middle cerebral artery occlusion in the rat. J. Neuro-trauma 27, 453-461.
11. Finkelstein, E., Corso, P.S., and Miller, T.R (2006). The Incidence and Economic Burden of Injuries in the United States. Oxford University Press: Oxford, New York.
12. Habgood, M.D., Bye, N., Dziegielewska, K.M., Ek, C.J., Lane, M.A., Potter, A., Morganti-Kossmann, C., Saunders, N.R. (2007). Changes in blood-brain barrier permeability to large and small molecules following traumatic brain injury in mice. Eur. J. Neurosci. 25, 231-238. (Pubitemid 46096237)
13. Higashida, T., Kreipke, C.W., Rafols, J.A., Peng, C., Schafer, S., Schafer, P., Ding, J.Y., Dornbos, D., 3rd, Li, X., Guthikonda, M., Rossi, N.F., and Ding, Y. (2011). The role of hypoxia-inducible factor-1alpha, aquaporin-4, and matrix metallopro-teinase-9 in blood-brain barrier disruption and brain edema after traumatic brain injury. J. Neurosurg. 114, 92-101.
14. Hinson, S.R., McKeon, A., and Lennon, V.A. (2010). Neurologi-cal autoimmunity targeting aquaporin-4. Neuroscience 168, 1009-1018.
15. Huber, J.D., Campos, C.R., Mark, K.S., and Davis, T.P. (2006). Alterations in blood-brain barrier ICAM-1 expression and brain microglial activation after lambda-carrageenan-induced inflammatory pain. Am. J. Physiol. Heart Circ. Physiol. 290, H732-H740.
16. Iseri, S.O., Sener, G., Saglam, B., Ercan, F., Gedik, N., and Yegen, B.C. (2008). Ghrelin alleviates biliary obstruction-induced chronic hepatic injury in rats. Regulatory Peptides 146, 73-79.
17. Jacob, A., Hack, B., Chiang, E., Garcia, J.G., Quigg, R.J., and Alexander, J.J. (2010). C5a alters blood-brain barrier integrity in experimental lupus. FASEB J. 24, 1682-1688.
18. Kapural, M., Krizanac-Bengez, L., Barnett, G., Perl, J., Masaryk, T., Apollo, D., Rasmussen, P., Mayberg, M.R., and Janigro, D. (2002). Serum S-100beta as a possible marker of blood-brain barrier disruption. Brain Res. 940, 102-104. (Pubitemid 34521759)
19. Kojima, M., Hosoda, H., Date, Y., Nakazato, M., Matsuo, H., and Kangawa, K. (1999). Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402, 656-660. (Pubitemid 129516334)
20. Kwan, R.O., Cureton, E., Dozier, K., Curran, B., Sadjadi, J., and Victorino, G.P. (2010). Ghrelin decreases microvascular leak during inflammation. J. Trauma 68, 1186-1191.
21. Lee, J., Borboa, A.K., Chun, H.B., Baird, A., and Eliceiri, B.P. (2010a). Conditional deletion of the focal adhesion kinase FAK alters remodeling of the blood-brain barrier in glioma. Cancer Res. 70, 10131-10140.
22. Lee, J.Y., Chung, H., Yoo, Y.S., Oh YJ., Oh TH., Park S., Yune TY. (2010b). Inhibition of apoptotic cell death by ghrelin improves functional recovery after spinal cord injury. Endocrinology 151, 3815-3826.
23. Liu, Y., Wang, P.S., Xie, D., Liu, K., and Chen, L. (2006). Ghrelin reduces injury of hippocampal neurons in a rat model of ce-rebral ischemia/reperfusion. Chin. J. Physiol. 49, 244-250.
24. Manley, G.T., Fujimura, M., Ma, T., Noshita, N., Filiz, F., Bollen, A.W., Chan, P., and Verkman, A.S. (2000). Aquaporin-4 de-letion in mice reduces brain edema after acute water intoxi-cation and ischemic stroke. Nat. Med. 6, 159-163. (Pubitemid 30082359)
25. Marchi, N., Rasmussen, P., Kapural, M., Fazio, V., Kight, K., Mayberg, M.R., Kanner, A., Ayumar, B., Albensi, B., Cavaglia, M., and Janigro, D. (2003). Peripheral markers of brain dam-age and blood-brain barrier dysfunction. Restor. Neurol. Neurosci. 21, 109-121. (Pubitemid 37330252)
26. Marmarou, A. (2003). Pathophysiology of traumatic brain ede-ma: current concepts. Acta Neurochir. Suppl. 86, 7-10.
27. Miao, Y., Xia, Q., Hou, Z., Zheng, Y., Pan, H., and Zhu, S. (2007). Ghrelin protects cortical neuron against focal ischemia/re-perfusion in rats. Biochem. Biophys. Res. Comm. 359, 795-800. (Pubitemid 46899020)
28. Mrak, R.E., and Griffinbc, W.S. (2001). The role of activated astrocytes and of the neurotrophic cytokine S100B in the pathogenesis of Alzheimer's disease. Neurobiol. Aging 22, 915-922. (Pubitemid 34066559)
29. Nag, S., Manias, J.L., and Stewart, D.J. (2009). Pathology and new players in the pathogenesis of brain edema. Acta Neu-ropathol. 118, 197-217.
30. Narayan, R.K., Michel, M.E., Ansell, B., Baethmann, A., Biegon, A., Bracken, M.B., Bullock, M.R., Choi, S.C., Clifton, G.L., Contant, C.F., Coplin, W.M., Dietrich, W.D., Ghajar, J., Grady, S.M., Grossman, R.G., Hall, E.D., Heetderks, W., Hovda, D.A., Jallo, J., Katz, R.L., Knoller, N., Kochanek, P.M., Maas, A.I., Majde, J., Marion, D.W., Marmarou, A., Marshall, L.F., McIntosh, T.K., Miller, E., Mohberg, N., Muizelaar, J.P., Pitts, L.H., Quinn, P., Riesenfeld, G., Robertson, C.S., Strauss, K.I., Teasdale, G., Temkin, N., Tuma, R., Wade, C., Walker, M.D., Weinrichm M., Whyte, J., Wilberger, J., Young, A.B., and Yurkewicz, L. (2002). Clinical trials in head injury. J. Neuro-trauma 19, 503-557. (Pubitemid 34587299)
31. O'Connor, C.A., Cernakn, I., and Vink, R. (2006). The temporal profile of edema formation differs between male and female rats following diffuse traumatic brain injury. Acta Neurochir. Suppl. 96, 121-124.
32. Okuno, K., Taya, K., Marmarou, C.R., Ozisik, P., Fazzina, G., Kleindienst, A., Gulsen, S., and Marmarou, A. (2008). The modulation of aquaporin-4 by using PKC-activator (phorbol myristate acetate) and V1a receptor antagonist (SR49059) fol-lowing middle cerebral artery occlusion/reperfusion in the rat. Acta Neurochir. Suppl. 102, 431-436.
33. Papadopoulos, M.C., Manley, G.T., Krishna, S., and Verkman, A.S. (2004). Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 18, 1291-1293. (Pubitemid 39561580)
34. Papadopoulos, M.C., and Verkman, A.S. (2005). Aquaporin-4 gene disruption in mice reduces brain swelling and mor-tality in pneumococcal meningitis. J. Biol. Chem. 280, 13906-13912. (Pubitemid 40517291)
35. Patel, T.H., Sprague, S., Lai, Q., Jimenez, D.F., Barone, C.M., and Ding, Y. (2008). Blood brain barrier (BBB) dysfunction asso-ciated with increased expression of tissue and urokinase plasminogen activators following peripheral thermal injury. Neurosci. Lett. 444, 222-226.
36. Pelinka, L.E., Toegel, E., Mauritz, W., and Redl, H. (2003). Serum S 100B: a marker of brain damage in traumatic brain injury with and without multiple trauma. Shock 19, 195-200.
37. Qiu, W.C., Wang, Z.G., Lv, R., Wang, W.G., Han, X.D., Yan, J., Wang, Y., Zheng, Q., and Ai, K.X. (2008). Ghrelin improves delayed gastrointestinal transit in alloxan-induced diabetic mice. World J. Gastroenterol. 14, 2572-2577. (Pubitemid 352037749)
38. Qi, X., Inagaki, K., Sobel, R.A., and Mochly-Rosen, D. (2008). Sustained pharmacological inhibition of deltaPKC protects against hypertensive encephalopathy through prevention of blood-brain barrier breakdown in rats. J. Clin. Invest. 118, 173-182.
39. Saul, T.G., and Ducker, T.B. (1982). Effect of intracranial pressure monitoring and aggressive treatment on mortality in severe head injury. J. Neurosurg. 56, 498-503. (Pubitemid 12055036)
40. Schilling, L., and Wahl, M. (1999). Mediators of cerebral edema. Adv. Exp. Med. Biol. 474, 123-141. (Pubitemid 32206767)
41. Sehirli, O., Sener, E., Sener, G., Cetinel, S., Erzik, C., and Yegen, B.C. (2008). Ghrelin improves burn-induced multiple organ injury by depressing neutrophil infiltration and the release of pro-inflammatory cytokines. Peptides 29, 1231-1240.
42. Simard, M., Arcuino, G., Takano, T., Liu, Q.S., and Nedergaard, M. (2003). Signaling at the gliovascular interface. J. Neurosci. 23, 9254-9262. (Pubitemid 37243827)
43. Stahel, P.F., Shohami, E., Younis, F.M., Kariya, K., Oho, V.I., Lenzlinger, P.M., Grosjean, M.B., Eugster, H.P., Trentz, O., Kossman, T., Morganti-Kossman, M.C. (2000). Experimental closed head injury: analysis of neurological outcome blood-brain barrier dysfunction, intracranial neutrophil infiltration, and neuronal cell death in mice deficient in genes for proin-flammatory cytokines. J. Cereb. Blood Flow Metab. 20, 369-380. (Pubitemid 30108456)
44. Taya, K., Gulsen, S., Okuno, K., Prieto, R., Marmarou, C.R., and Marmarou, A. (2008). Modulation of AQP4 expression by the selective V1a receptor antagonist, SR49059, decreases trauma-induced brain edema. Acta Neurochir. Suppl. 102, 425-429.
45. Tsao, N., Hsu, H.P., Wu, C.M., Liu, C.C., and Lei, H.Y. (2001). Tumour necrosis factor-alpha causes an increase in blood-brain barrier permeability during sepsis. J. Med. Microbiol. 50, 812-821. (Pubitemid 32802844)
46. Unterberg, A.W., Stover, J., Kress, B., and Kiening, K.L. (2004). Edema and brain trauma. Neuroscience 129, 1021-1029. (Pubitemid 39556253)
47. Wren, A.M., Small, C.J., Ward, H.L., Murphy, K.G., Dakin, C.L., Taheri, S., Kennedy, A.R., Roberts, G.H., Morgan, D.G., Ghatei, M.A., and Bloom, S.R. (2000). The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology 141, 4325-4328.
48. Xu, J., Wang, S., Lin, Y., Cao, L., Wang, R., and Chi, Z. (2009). Ghrelin protects against cell death of hippocampal neurons in pilocarpine-induced seizures in rats. Neurosci. Lett. 453,58-61.
49. Zelenina, M. Regulation of brain aquaporins. (2010). Neurochem. Int. 57, 468-488.