Cyclosporine Treatment in Traumatic Brain Injury: Operation Brain Trauma Therapy

Journal of Neurotrauma

Volumn 33, Issue 6, 2016, Pages 553-566

  Dixon, C Edward ^a   Bramlett, Helen M ^b,c   Dietrich, W Dalton ^b   Shear, Deborah A ^d   Yan, Hong Q ^a   Deng Bryant, Ying ^d   Mondello, Stefania ^e   Wang, Kevin K W ^f   Hayes, Ronald L ^f   Empey, Philip E ^g   Povlishock, John T ^h   Tortella, Frank C ^d   Kochanek, Patrick M ⁱ  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^e UNIVERSITY OF MESSINA   (Italy)

^f UNIVERSITY OF FLORIDA HEALTH   (United States)

^g UNIVERSITY OF PITTSBURGH   (United States)

^h VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

ⁱ UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

biomarker; calcineurin; controlled cortical impact; fluid percussion; neuroprotection; penetrating ballistic like brain injury; phosphatase; rat; therapy

Indexed keywords

CYCLOSPORIN A; GLIAL FIBRILLARY ACIDIC PROTEIN; UBIQUITIN C TERMINAL HYDROLASE L1; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CYCLOSPORIN; IMMUNOSUPPRESSIVE AGENT;

ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; DISEASE SEVERITY; LOW DRUG DOSE; MALE; MORRIS WATER MAZE TEST; MORTALITY; MOTOR COORDINATION; NEUROPROTECTION; NONHUMAN; RANDOMIZED CONTROLLED TRIAL (TOPIC); RAT; TRAUMATIC BRAIN INJURY; TREATMENT OUTCOME; ANIMAL; BLOOD; CONVALESCENCE; DISEASE MODEL; DRUG EFFECTS; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; BIOMARKERS; BRAIN INJURIES, TRAUMATIC; CYCLOSPORINE; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOSUPPRESSIVE AGENTS; MALE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; UBIQUITIN THIOLESTERASE;

EID: 84962224160     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2015.4122     Document Type: Article

References (38)

1. Okonkwo, D.O., and Povlishock, J.T. (1999). An intrathecal bolus of cyclosporin A before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J. Cereb. Blood Flow Metab. 19, 443-451.
2. Sullivan, P.G., Thompson, M.B., and Scheff, S.W. (1999). Cyclosporin A attenuates acute mitochondrial dysfunction following traumatic brain injury. Exp. Neurol. 160, 226-234.
3. Signoretti, S., Marmarou, A., Tavazzi, B., Dunbar, J., Amorini, A.M., Lazzarino, G., and Vagnozzi, R. (2004). The protective effect of cyclosporin A upon N-acetylaspartate and mitochondrial dysfunction following experimental diffuse traumatic brain injury. J. Neurotrauma 21, 1154-1167.
4. Alessandri, B., Rice, A.C., Levasseur, J., DeFord, M., Hamm, R.J., and Bullock, M.R. (2002). Cyclosporin A improves brain tissue oxygen consumption and learning/memory performance after lateral fluid percussion injury in rats. J. Neurotrauma 19, 829-841.
5. Buki, A., Okonkwo, D.O., and Povlishock, J.T. (1999). Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J. Neurotrauma 16, 511-521.
6. Suehiro, E., and Povlishock, J.T. (2001). Exacerbation of traumatically induced axonal injury by rapid posthypothermic rewarming and attenuation of axonal change by cyclosporin A. J. Neurosurg. 94, 493-498.
7. Okonkwo, D.O., Melon, D.E., Pellicane, A.J., Mutlu, L.K., Rubin, D.G., Stone, J.R., and Helm, G.A. (2003). Dose-response of cyclosporin A in attenuating traumatic axonal injury in rat. Neuroreport 14, 463-466.
8. Van Den Heuvel, C., Donkin, J.J., Finnie, J.W., Blumbergs, P.C., Kuchel, T., Koszyca, B., Manavis, J., Jones, N.R., Reilly, P.L., and Vink, R. (2004). Downregulation of amyloid precursor protein (APP) expression following post-traumatic cyclosporin-A administration. J. Neurotrauma 21, 1562-1572.
9. Scheff, S.W., and Sullivan, P.G. (1999). Cyclosporin A significantly ameliorates cortical damage following experimental traumatic brain injury in rodents. J. Neurotrauma 16, 783-792.
10. Sullivan, P.G., Thompson, M., and Scheff, S.W. (2000). Continuous infusion of cyclosporin A postinjury significantly ameliorates cortical damage following traumatic brain injury. Exp. Neurol. 161, 631-637.
11. Sullivan, P.G., Rabchevsky, A.G., Hicks, R.R., Gibson, T.R., Fletcher-Turner, A., Scheff, S.W. (2000). Dose-response curve and optimal dosing regimen of cyclosporin A after traumatic brain injury in rats. Neuroscience 101, 289-295.
12. Sullivan, P.G., Sebastian, A.H., and Hall, E.D. (2011). Therapeutic window analysis of the neuroprotective effects of cyclosporine A after traumatic brain injury. J. Neurotrauma 28, 311-318.
13. Mbye, L.H., Singh, I.N., Carrico, K.M., Saatman, K.E., and Hall, E.D. (2009). Comparative neuroprotective effects of cyclosporin A and NIM811, a nonimmunosuppressive cyclosporin A analog, following traumatic brain injury. J. Cereb. Blood Flow Metab. 29, 87-97.
14. Kilbaugh, T.J., Bhandare, S., Lorom, D.H., Saraswati, M., Robertson, C.L., and Margulies, S.S. (2011). Cyclosporin A preserves mitochondrial function after traumatic brain injury in the immature rat and piglet. J. Neurotrauma 28, 763-774.
15. Hansson, M.J., Persson, T., Friberg, H., Keep, M.F., Rees, A., Wieloch, T., and Elmer, E. (2003). Powerful cyclosporin inhibition of calcium-induced permeability transition in brain mitochondria. Brain Res. 960, 99-111.
16. Friberg, H., Ferrand-Drake, M., Bengtsson, F., Halestrap, A.P., and Wieloch, T. (1998). Cyclosporin A, but not FK 506, protects mitochondria and neurons against hypoglycemic damage and implicates the mitochondrial permeability transition in cell death. J. Neurosci. 18, 5151-5159.
17. Lemaire, M., Bruelisauer, A., Guntz, P., and Sato, H. (1996). Dosedependent brain penetration of SDZ PSC 833, a novel multidrug resistance-reversing cyclosporin, in rats. Cancer Chemother. Pharmacol. 38, 481-486.
18. Tanaka, C., Kawai, R., and Rowland, M. (1999). Physiologically based pharmacokinetics of cyclosporine A: reevaluation of dosenonlinear kinetics in rats. J. Pharmacokinet. Biopharm. 27, 597-623.
19. Shear, D.A., Dixon, C.E., Bramlett, H.M., Mondello, S., Dietrich, W.D., Deng-Bryant, Y., Schmid, K.E., Wang, K.K.W., Hayes, R.L., Povlishock, J.T., Kochanek, P.M., and Tortella, F.C. (2016). Nicotinamide treatment in traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 523-537.
20. Atkins, C.M., Truettner, J.S., Lotocki, G., Sanchez-Molano, J., Kang, Y., Alonso, O.F., Sick, T.J., Dietrich, W.D., and Bramlett, H.M. (2010). Post-traumatic seizure susceptibility is attenuated by hypothermia therapy. Eur. J. Neurosci. 32, 1912-1920.
21. Dixon, C.E., Lyeth, B.G., Povlishock, J.T., Findling, R.L., Hamm, R.J., Marmarou, A., Young, H.P., and Hayes, R.L. (1987). A fluid-percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119.
22. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghmai, A.A., and Hayes, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262.
23. Yan, H.Q., Yu, J., Kline, A.E., Letart, P., Jenkins, L.W., Marion, D.W., and Dixon, C.E. (2000). Evaluation of combined fibroblast growth factor-2 and moderate hypothermia therapy in traumatically brain injured rats. Brain Res. 887, 134-143.
24. Shear, D.A., Lu, X.C., Bombard, M.C., Pedersen, R., Chen, Z., Davis, A., and Tortella, F.C. (2010). Longitudinal characterization of motor and cognitive deficits in a model of penetrating ballistic-like brain injury. J. Neurotrauma 27, 1911-1923.
25. Mondello, S., Shear, D.A., Bramlett, H.M., Dixon, C.E., Schmid, K. E., Dietrich, W.D., Wang, K.K., Hayes, R. L., Glushakova, O., Catania, M., Richieri, S., Povlishock, J.T., Tortella, F.C., and Kochanek, P.M. (2015). Insight into pre-clinical models of traumatic brain injury using circulating brain damage biomarkers: Operation brain trauma therapy. J. Neurotrauma 33, 595-605.
26. Kochanek, P.M., Bramlett, H.M., Dixon, E.C., Shear, D.A., Dietrich, W.D., Schmid, K.E., Mondello, S.W., Wang, K.K., Hayes, R.L., Povilshock, J.T., and Tortella, F.C. (2015). Approach to modeling, therapy evaluation, drug selection, and biomarker assessments, for a multicenter pre-clinical drug screening consortium for acute therapies in severe traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 513-522.
27. Kochanek, P.M., Bramlett, H.M., Shear, D.A., Dixon, C.E., Dietrich, W.D., Schmid, K.E., Mondello, S., Wang, K.K., Hayes, R.L., Poloyac, S.M., Empey, P.E., Povlishock, J.T., Mountney, A., Browning, M., Deng-Bryant, Y., Yan, H.Q., Jackson, T.C., Catania, M., Anagli, J., Glushakova, O., and Tortella, F.C. (2015). Synthesis of findings, current investigations, and future directions: Operation brain trauma therapy. J. Neurotrauma 33, 606-614.
28. Blaya, M.O., Bramlett, H.M., Naidoo, J., Pieper, A.A., and Dietrich, W.D. (2014). Neuroprotective efficacy of a proneurogenic compound after traumatic brain injury. J. Neurotrauma, 31, 476-486.
29. Feeney, D.M., Gonzalez, A., and Law, W.A. (1982). Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science 217, 855-857.
30. Papa, L., Akinyi, L., Liu, M.C., Pineda, J.A., Tepas, J.J., 3rd, Oli, M.W., Zheng, W., Robinson, G., Robicsek, S.A., Gabrielli, A., Heaton, S.C., Hannay, H.J., Demery, J.A., Brophy, G.M., Layon, J., Robertson, C.S., Hayes, R.L., and Wang, K.K. (2010). Ubiquitin Cterminal hydrolase is a novel biomarker in humans for severe traumatic brain injury. Crit. Care Med. 38, 138-144.
31. Papa, L., Lewis, L.M., Falk, J.L., Zhang, Z., Silvestri, S., Giordano, P., Brophy, G.M., Demery, J.A., Dixit, N.K., Ferguson, I., Liu, M.C., Mo, J., Akinyi, L., Schmid, K., Mondello, S., Robertson, C.S., Tortella, F.C., Hayes, R.L., and Wang, K.K. (2012). Elevated levels of serum glial fibrillary acidic protein breakdown products in mild and moderate traumatic brain injury are associated with intracranial lesions and neurosurgical intervention. Ann. Emerg. Med. 59, 471-483.
32. Zhang, Z., Mondello, S., Kobeissy, F., Rubenstein, R., Streeter, J., Hayes, R.L., and Wang, K.K. (2011). Protein biomarkers for traumatic and ischemic brain injury: from bench to bedside. Transl. Stroke Res. 2, 455-462.
33. Zoltewicz, J.S., Mondello, S., Yang, B., Newsom, K.J., Kobeissy, F., Yao, C., Lu, X.C., Dave, J.R., Shear, D.A., Schmid, K., Rivera, V., Cram, T., Seaney, J., Zhang, Z., Wang, K.K., Hayes, R.L., and Tortella, F.C. (2013). Biomarkers track damage after graded injury severity in a rat model of penetrating brain injury. J. Neurotrauma 30, 1161-1169.
34. Aminmansour, B., Fard, S.A., Habibabadi, M.R., Moein, P., Norouzi, R., Naderan, M. (2014). The efficacy of cyclosporine-a on diffuse axonal injury after traumatic brain injury. Adv. Biomed. Res. 3, 35.
35. Readnower, R.D., Pandya, J.D., McEwen, M.L., Pauly, J.R., Springer, J.E., and Sullivan, P.G. (2011). Post-injury administration of the mitochondrial permeability transition pore inhibitor, NIM811, is neuroprotective and improves cognition after traumatic brain injury in rats. J. Neurotrauma 28, 1845-1853.
36. de Groen, P.C., Aksamit, A.J., Rakela, J., Forbes, G.S., and Krom, R.A. (1987). Central nervous system toxicity after liver transplantation. The role of cyclosporine and cholesterol. N. Engl. J. Med. 317, 861-866.
37. Windebank, A.J., Blexrud, M.D., and de Groen, P.C. (1994). Potential neurotoxicity of the solvent vehicle for cyclosporine. J. Pharmacol. Exp. Ther. 268, 1051-1056.
38. Hatton J, Rosbolt B, Empey P, Kryscio R, and Young B. (2008) Dosing and safety of cyclosporine in patients with severe brain injury. J Neurosurg. 109, 699-707.