Combination therapies for traumatic brain injury: Retrospective considerations

Journal of Neurotrauma

Volumn 33, Issue 1, 2016, Pages 101-112

  Margulies, Susan ^a   Anderson, Gail ^b   Atif, Fahim ^c   Badaut, Jerome ^d   Clark, Robert ^e   Empey, Philip ^f   Guseva, Maria ^g   Hoane, Michael ^h   Huh, Jimmy ⁱ   Pauly, Jim ^j   Raghupathi, Ramesh ^k   Scheff, Stephen ^j   Stein, Donald ^c   Tang, Huiling ^c   Hicks, Mona ^l  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITÉ DE BORDEAUX   (France)

^e UNIVERSITY OF PITTSBURGH   (United States)

^f UNIVERSITY OF PITTSBURGH   (United States)

^g Fresenius Kabi   (United States)

^h SOUTHERN ILLINOIS UNIVERSITY   (United States)

ⁱ CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^j UNIVERSITY OF KENTUCKY   (United States)

^k DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^l One Mind for Research   (United States)

more..

Author keywords

pharmacological interventions; preclinical therapeutic development; treatments

Indexed keywords

ACETYLCYSTEINE; AQUAPORIN 4; AQUAPORIN 4 INHIBITOR; CHOLINE; CREATINE; GLYPROMATE; MINOCYCLINE; PROBENECID; PROGESTERONE; PROTEIN INHIBITOR; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TRIPEPTIDE DERIVATIVE; UNCLASSIFIED DRUG; VITAMIN D;

ADULT; ARTICLE; DRUG SCREENING; DRUG THERAPY; ENZYME INHIBITION; EXPERIMENTAL DESIGN; HUMAN; MONOTHERAPY; NONHUMAN; OUTCOME ASSESSMENT; RETROSPECTIVE STUDY; TRAUMATIC BRAIN INJURY; ANIMAL; ANIMAL BEHAVIOR; BRAIN INJURIES; COMBINATION DRUG THERAPY; DISEASE MODEL; DRUG EFFECTS; MALE; MOUSE; PHYSIOLOGY; PROCEDURES; RAT;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN INJURIES; DISEASE MODELS, ANIMAL; DRUG THERAPY, COMBINATION; MALE; MICE; RATS;

EID: 84952949019     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2014.3855     Document Type: Article

References (107)

1. McAllister T.W. (2011). Neurobiological consequences of traumatic brain injury. Dialogues Clin. Neurosci. 13, 287-300.
2. Smith D.H, Hicks R, and Povlishock J.T. (2013). Therapy development for diffuse axonal injury. J. Neurotrauma. 30, 307-323.
3. Doppenberg E.M, Choi S.C, and Bullock R. (2004). Clinical trials in traumatic brain injury: Lessons for the future. J. Neurosurg. Anesthesiol. 16, 87-94.
4. Wright D.W, Yeatts S.D, Silbergleit R, Palesch Y.Y, Hertzberg V.S, Frankel M, Goldstein F.C, Caveney A.F, Howlett-Smith H, Bengelink E.M, Manley G.T, Merck L.H, Janis L.S, Barsan W.G, and NETT Investigators N. (2014). Very early administration of progesterone for acute traumatic brain injury. N. Engl. J. Med. 371, 2457-2466.
5. Skolnick B.E, Maas A.I, Narayan R.K, van der Hoop R.G, MacAllister T, Ward J.D, Nelson N.R, Stocchetti N, and SYNAPSE Trial. (2014). A clinical trial of progesterone for severe traumatic brain injury. N. Engl. J. Med. 371, 2467-2476.
6. Margulies S, and Hicks R. (2009). Combination therapies for traumatic brain injury: Prospective considerations. J. Neurotrauma. 26, 925-939.
7. Saatman K.E, Duhaime A.C, Bullock R, Maas A.I, Valadka A, Manley G.T, Workshop Scientific, Team and Advisory Panel Members. (2008). Classification of traumatic brain injury for targeted therapies. J. Neurotrauma. 25, 719-738.
8. Sidaros A, Skimminge A, Liptrot M.G, Sidaros K, Engberg A.W, Herning M, Paulson O.B, Jernigan T.L, and Rostrup E. (2009). Long-Term global and regional brain volume changes following severe traumatic brain injury: a longitudinal study with clinical correlates. Neuroimage. 44, 1-8.
9. Behan L.A, and Agha A. (2007). Endocrine consequences of adult traumatic brain injury. Horm. Res. 68, Suppl. 5, 18-21.
10. Deutsch E.R, Espinoza T.R, Atif F, Woodall E, Kaylor J, and Wright D.W. (2013). Progesterones role in neuroprotection, a review of the evidence. Brain Res. 1530, 82-105.
11. Cekic M, Cutler S.M, VanLandingham J.W, and Stein D.G. (2011). Vitamin D deficiency reduces the benefits of progesterone treatment after brain injury in aged rats. Neurobiol Aging. 32, 864-874.
12. Cekic M, Sayeed I, and Stein D.G. (2009). Combination treatment with progesterone and vitamin D hormone may be more effective than monotherapy for nervous system injury and disease. Front. Neuroendocrinol. 30, 158-172.
13. Norman A.W, Bouillon R, Whiting S.J, Vieth R, and Lips P. (2007). 13th Workshop consensus for vitamin D nutritional guidelines. J. Steroid Biochem. Mol. Biol. 103, 204-205.
14. Hua F, Reiss J.I, Tang H, Wang J, Fowler X, Sayeed I, and Stein D.G. (2012). Progesterone and low-dose vitamin D hormone treatment enhances sparing of memory following traumatic brain injury. Horm. Behav. 61, 642-651.
15. Aminmansour B, Nikbakht H, Ghorbani A, Rezvani M, Rahmani P, Torkashvand M, Nourian M, and Moradi M. (2012). ComParison of the administration of progesterone versus progesterone and vitamin D in improvement of outcomes in patients with traumatic brain injury: a randomized clinical trial with placebo group. Adv. Biomed. Res. 1, 58.
16. Atif F, Yousuf S, Sayeed I, Ishrat T, Hua F, and Stein D.G. (2013). Combination treatment with progesterone and vitamin D hormone is more effective than monotherapy in ischemic stroke: The role of BDNF/TrkB/Erk1/2 signaling in neuroprotection. Neuropharmacology. 67, 78-87.
17. Tang H, Hua F, Wang J, Sayeed I, Wang X, Chen Z, Yousuf S, Atif F, and Stein D.G. (2013). Progesterone and vitamin D: Improvement after traumatic brain injury in middle-Aged rats. Hormones and behavior. 64, 527-538.
18. Anderson G.D, Farin F.M, Bammler T.K, Beyer R.P, Swan A.A, Wilkerson H.W, Kantor E.D, and Hoane M.R. (2011). The effect of progesterone dose on gene expression after traumatic brain injury. J. Neurotrauma. 28, 1827-1843.
19. Peterson T.C, Hoane M.R, McConomy K.S, Farin F.M, Bammler T.K, MacDonald J.W, Kantor E.D, and Anderson G.D. (2015). A combination therapy of nicotinamide and progesterone improves functional recovery following traumatic brain injury. J. Neurotrauma. 32, 765-779.
20. Cutler S.M, Cekic, M, Miller D.M, Wali B, VanLandingham J.W, and Stein D.G. (2007). Progesterone improves acute recovery after traumatic brain injury in the aged rat. J. Neurotrauma. 24, 1475-1486.
21. Goss C.W, Hoffman S.W, and Stein D.G. (2003). Behavioral effects and anatomic correlates after brain injury: a progesterone dose-response study. Pharmacol. Biochem. Behav. 76, 231-242.
22. Wright D.W, Ritchie J.C, Mullins R.E, Kellermann A.L, and Denson D.D. (2005). Steady-state serum concentrations of progesterone following continuous intravenous infusion in patients with acute moderate to severe traumatic brain injury. J. Clin. Pharmacol. 45, 640-648.
23. Badaut J, Ashwal S, Adami A, Tone B, Recker R, Spagnoli D, Ternon B, and Obenaus A. (2011). Brain water mobility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J. Cereb. Blood Flow Metab. 31, 819-831.
24. Hirt L, Badaut J, Thevenet J, Granziera C, Regli L, Maurer F, Bonny C, and Bogousslavsky J. (2004). D-JNKI1, a cellpenetrating c-Jun-N-Terminal kinase inhibitor, protects against cell death in severe cerebral ischemia. Stroke. 35, 1738-1743.
25. Arima H, Yamamoto N, Sobue K, Umenishi F, Tada T, Katsuya H, and Asai K. (2003). Hyperosmolar mannitol simulates expression of aquaporins 4 and 9 through a p38 mitogen-Activated protein kinase-dependent pathway in rat astrocytes. J. Biol. Chem. 278, 44525-44534.
26. Armstead W.M, Kiessling J.W, Riley J, Cines D.B, and Higazi A.A. (2011). tPA contributes to impaired NMDA cerebrovasodilation after traumatic brain injury through activation of JNK MAPK. Neurol. Res. 33, 726-733.
27. Fukuda A.M, and Badaut J. (2012). Aquaporin 4: a player in cerebral edema and neuroinflammation. J. Neuroinflammation. 9, 279.
28. Michel-Monigadon D, Bonny C, and Hirt L. (2010). c-Jun Nterminal kinase pathway inhibition in intracerebral hemorrhage. Cerebrovasc. Dis. 29, 564-570.
29. Ortolano F, Colombo A, Zanier E.R, Sclip A, Longhi L, Perego C, Stocchetti N, Borsello T, and De Simoni M.G. (2009). c-Jun N-Terminal kinase pathway activation in human and experimental cerebral contusion. J. Neuropathol. Exp. Neurol. 68, 964-971.
30. Raghupathi R, Muir J.K, Fulp C.T, Pittman R.N, and McIntosh T.K. (2003). Acute activation of mitogen-Activated protein kinases following traumatic brain injury in the rat: implications for posttraumatic cell death. Exp. Neurol. 183, 438-448.
31. Saporito M.S, Brown E.R, Carswell S, DiCamillo A.M, Miller M.S, Murakata C, Neff N.T, Vaught J.L, and Haun F.A. (1998). Preservation of cholinergic activity and prevention of neuron death by CEP-1347/KT-7515 following excitotoxic injury of the nucleus basalis magnocellularis. Neuroscience. 86, 461-472.
32. Yatsushige H, Ostrowski R.P, Tsubokawa T, Colohan A, and Zhang J.H. (2007). Role of c-Jun N-Terminal kinase in early brain injury after subarachnoid hemorrhage. J. Neurosci. Res. 85, 1436-1448.
33. Fukuda A.M, and Badaut J. (2013). siRNA Treatment: A Swordin-The-Stone for acute brain injuries. Genes. 4, 435-456.
34. Bonny C, Oberson A, Negri S, Sauser C, and Schorderet D.F. (2001). Cell-permeable peptide inhibitors of JNK: novel blockers of beta-cell death. Diabetes. 50, 77-82.
35. Borsello T, Clarke P.G, Hirt L, Vercelli A, Repici M, Schorderet D.F, Bogousslavsky J, and Bonny C. (2003). A peptide inhibitor of c-Jun N-Terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med. 9, 1180-1186.
36. Wiegler K, Bonny C, Coquoz D, and Hirt L. (2008). The JNK inhibitor XG-102 protects from ischemic damage with delayed intravenous administration also in the presence of recombinant tissue plasminogen activator. Cerebrovasc. Dis. 26, 360-366.
37. Fukuda A.M, Adami A, Pop V, Bellone J.A, Coats J.S, Hartman R.E, Ashwal S, Obenaus A. and Badaut J. (2013). Posttraumatic reduction of edema with aquaporin-4 RNA interference improves acute and chronic functional recovery. J. Cereb. Blood Flow Metab. 33, 1621-1632.
38. Ajao D.O, Pop V, Kamper J.E, Adami A, Rudobeck E, Huang L, Vlkolinsky R, Hartman R.E, Ashwal S, Obenaus A, and Badaut J. (2012). Traumatic brain injury in young rats leads to progressive behavioral deficits coincident with altered tissue properties in adulthood. J. Neurotrauma. 29, 2060-2074.
39. Ajao D, Kamper J, Fukuda A.M, Pop V, Sorensen D.W, Toca V.B, Hartman R.E, Obenaus A, Ashwal S. and Badaut J. (2011). Inhibition of the JNK pathway improves long-Term neurobehavioral outcomes after juvenile traumatic brain injury. Society for Neuroscience Abstract Viewer and Itinerary Planner 41.
40. Fukuda A.M, Pop V, Spagnoli D, Ashwal S, Obenaus A. and Badaut J. (2012). Delayed increase of astrocytic aquaporin 4 after juvenile traumatic brain injury: Possible role in edema resolution? Neuroscience. 222, 366-378.
41. Kamper J.E, Pop V, Fukuda A.M, Ajao D.O, Hartman R.E, and Badaut J. (2013). Juvenile traumatic brain injury evolves into a chronic brain disorder: behavioral and histological changes over 6 months. Exp. Neurol. 250, 8-19.
42. Aldrich E.F, Eisenberg H.M, Saydjari C, Luerssen T.G, Foulkes M.A, Jane J.A, Marshall L.F, Marmarou A, and Young H.F. (1992). Diffuse brain swelling in severely head-injured children. A report from the NIH Traumatic Coma Data Bank. J. Neurosurg. 76, 450-454.
43. Zwienenberg M, and Muizelaar J.P. (1999). Severe pediatric head injury: The role of hyperemia revisited. J. Neurotrauma. 16, 937-943.
44. Anderson V, Catroppa C, Morse S, Haritou F, and Rosenfeld J. (2005). Functional plasticity or vulnerability after early brain injury? Pediatrics. 116, 1374-1382.
45. Levin H.S, Aldrich E.F, Saydjari C, Eisenberg H.M, Foulkes M.A, Bellefleur M, Luerssen T.G, Jane J.A, Marmarou A, Marshall L.F, et al. (1992). Severe head injury in children: experience of the Traumatic Coma Data Bank. Neurosurgery. 31, 435-444.
46. Potts M.B, Koh S.E, Whetstone W.D, Walker B.A, Yoneyama T, Claus C.P, Manvelyan H.M, and Noble-Haeusslein L.J. (2006). Traumatic injury to the immature brain: inflammation, oxidative injury, and iron-mediated damage as potential therapeutic targets. NeuroRx. 3, 143-153.
47. Armstead W.M. (2005). Age and cerebral circulation. Pathophysiology. 12, 5-15.
48. Prins M.L, and Hovda D.A. (2003). Developing experimental models to address traumatic brain injury in children. J. Neurotrauma. 20, 123-137.
49. Raghupathi R, and Huh J.W. (2007). Diffuse brain injury in the immature rat: evidence for an age-At-injury effect on cognitive function and histopathologic damage. J. Neurotrauma. 24, 1596-1608.
50. Huh J.W, Widing A.G, and Raghupathi R. (2008). Midline brain injury in the immature rat induces sustained cognitive deficits, bihemispheric axonal injury and neurodegeneration. Exp. Neurol. 213, 84-92.
51. Bye N, Habgood M.D, Callaway J.K, Malakooti N, Potter A, Kossmann T, and Morganti-Kossmann M.C. (2007). Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration. Exp. Neurol. 204, 220-233.
52. Sanchez Mejia R.O, Ona V.O, Li M, and Friedlander R.M. (2001). Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery. 48, 1393-1401.
53. Arvin K.L, Han B.H, Du Y, Lin S.Z, Paul S.M, and Holtzman D.M. (2002). Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann. Neurol. 52, 54-61.
54. Guan J, Thomas G.B, Lin H, Mathai S, Bachelor D.C, George S. and Gluckman P.D. (2004). Neuroprotective effects of the Nterminal tripeptide of insulin-like growth factor-1, glycine-prolineglutamate (GPE) following intravenous infusion in hypoxic-ischemic adult rats. Neuropharmacology. 47, 892-903.
55. Sizonenko S.V, Sirimanne E.S, Williams C.E, and Gluckman P.D. (2001). Neuroprotective effects of the N-Terminal tripeptide of IGF-1, glycine-proline-glutamate, in the immature rat brain after hypoxic-ischemic injury. Brain Res. 922, 42-50.
56. Sara V.R, Carlsson-Skwirut C, Drakenberg K, Giacobini M.B, Hakansson L, Mirmiran M, Nordberg A, Olson L, Reinecke M, , Stahlbom P.A, et al. (1993). The biological role of truncated insulin-like growth factor-1 and the tripeptide GPE in the central nervous system. Ann. N. Y. Acad. Sci. 692, 183-191.
57. Lu X.C, Chen R.W, Yao C, Wei H, Yang X, Liao Z, Dave J.R. and Tortella F.C. (2009). NNZ-2566, a glypromate analog, improves functional recovery and attenuates apoptosis and inflammation in a rat model of penetrating ballistic-Type brain injury. J. Neurotrauma. 26, 141-154.
58. Wei H.H, Lu X.C, Shear D.A, Waghray A, Yao C, Tortella F.C, and Dave J.R. (2009). NNZ-2566 treatment inhibits neuroinflammation and pro-inflammatory cytokine expression induced by experimental penetrating ballistic-like brain injury in rats. J. Neuroinflammation. 6, 19.
59. Dileonardi A.M, Huh J.W, and Raghupathi R. (2012). Differential effects of FK506 on structural and functional axonal deficits after diffuse brain injury in the immature rat. J. Neuropathol. Exp. Neurol. 71, 959-972.
60. Buller K.M, Carty M.L, Reinebrant H.E, and Wixey J.A. (2009). Minocycline: a neuroprotective agent for hypoxic-ischemic brain injury in the neonate? J. Neurosci. Res. 87, 599-608.
61. Plane J.M, Shen Y, Pleasure D.E, and Deng W. (2010). Prospects for minocycline neuroprotection. Arch. Neurol. 67, 1442-1448.
62. Reeves T.M, Phillips L.L, Lee N.N, and Povlishock J.T. (2007). Preferential neuroprotective effect of tacrolimus (FK506) on unmyelinated axons following traumatic brain injury. Brain Res. 1154, 225-236.
63. Marmarou C.R, and Povlishock J.T. (2006). Administration of the immunophilin ligand FK506 differentially attenuates neurofilament compaction and impaired axonal transport in injured axons following diffuse traumatic brain injury. Exp Neurol. 197, 353-362.
64. Singleton R.H, Stone J.R, Okonkwo D.O, Pellicane A.J, and Povlishock J.T. (2001). The immunophilin ligand FK506 attenuates axonal injury in an impact-Acceleration model of traumatic brain injury. J. Neurotrauma. 18, 607-614.
65. Staal J.A, Dickson T.C, Gasperini R, Liu Y, Foa L, and Vickers J.C. (2010). Initial calcium release from intracellular stores followed by calcium dysregulation is linked to secondary axotomy following transient axonal stretch injury. J. Neurochem. 112, 1147-1155.
66. DiLeonardi A.M, Huh J.W, and Raghupathi R. (2009). Impaired axonal transport and neurofilament compaction occur in separate populations of injured axons following diffuse brain injury in the immature rat. Brain Res. 1263, 174-182.
67. Setkowicz Z, Ciarach M, Guzik R, and Janeczko K. (2004). Different effects of neuroprotectants FK-506 and cyclosporin A on susceptibility to pilocarpine-induced seizures in rats with brain injured at different developmental stages. Epilepsy Res. 61, 63-72.
68. Wallimann, T, . and Hemmer W. (1994). Creatine kinase in nonmuscle tissues and cells. Mol. Cell Biochem. 133-134, 193-220.
69. Guerrero-Ontiveros M.L, and Wallimann T. (1998). Creatine supplementation in health and disease. Effects of chronic creatine ingestion in vivo: down-regulation of the expression of creatine transporter isoforms in skeletal muscle. Mol. Cell Biochem. 184, 427-437.
70. Brustovetsky N, Brustovetsky T, and Dubinsky J.M. (2001). On the mechanisms of neuroprotection by creatine and phosphocreatine. J. Neurochem. 76, 425-434.
71. Sullivan P.G, Geiger J.D, Mattson M.P, and Scheff S.W. (2000). Dietary supplement creatine protects against traumatic brain injury. Ann. Neurol. 48, 723-729.
72. Tarnopolsky M.A, and Beal M.F. (2001). Potential for creatine and other therapies targeting cellular energy dysfunction in neurological disorders. Ann. Neurol. 49, 561-574.
73. Scheff S.W, and Dhillon H.S. (2004). Creatine-enhanced diet alters levels of lactate and free fatty acids after experimental brain injury. Neurochem. Res. 29, 469-479.
74. Sanders L.M, and Zeisel S.H. (2007). Choline: dietary requirements and role in brain development. Nutr. Today. 42, 181-186.
75. Guseva M.V, Hopkins D.M, Scheff S.W, and Pauly J.R. (2008). Dietary choline supplementation improves behavioral, histological, and neurochemical outcomes in a rat model of traumatic brain injury. J. Neurotrauma. 25, 975-983.
76. Zafonte R.D, Bagiella E, Ansel B.M, Novack T.A, Friedewald W.T, Hesdorffer D.C, Timmons S.D, Jallo J, Eisenberg H, Hart T, Ricker J.H, Diaz-Arrastia R, Merchant R.E, Temkin N.R, Melton S, and Dikmen S.S. (2012). Effect of citicoline on functional and cognitive status among patients with traumatic brain injury: Citicoline Brain Injury Treatment Trial (COBRIT). JAMA. 308, 1993-2000.
77. Samuni Y, Goldstein S, Dean O.M, and Berk M. (2013). The chemistry and biological activities of N-Acetylcysteine. Biochim. Biophys. Acta. 1830, 4117-4129.
78. Heard K, and Green J. (2012). Acetylcysteine therapy for acetaminophen poisoning. Curr. Pharm. Biotechnol. 13, 1917-1923.
79. Xiong Y, Peterson P.L, and Lee C.P. (1999). Effect of Nacetylcysteine on mitochondrial function following traumatic brain injury in rats. J. Neurotrauma. 16, 1067-1082.
80. Abdel Baki S.G, Schwab B, Haber M, Fenton A.A, and Bergold P.J. (2010). Minocycline synergizes with N-Acetylcysteine and improves cognition and memory following traumatic brain injury in rats. PloS One 5, e12490.
81. Haber M, Abdel Baki S.G, Grinkina N.M, Irizarry R, Ershova A, Orsi S, Grill R.J, Dash, P, . and Bergold P.J. (2013). Minocycline plus N-Acetylcysteine synergize to modulate inflammation and prevent cognitive and memory deficits in a rat model of mild traumatic brain injury. Exp. Neurol. 249, 169-177.
82. Hoffer M.E, Balaban C, Slade M.D, Tsao J.W, and Hoffer B. (2013). Amelioration of acute sequelae of blast induced mild traumatic brain injury by N-Acetyl cysteine: a double-blind, placebo controlled study. PloS One 8, e54163.
83. Burnell J.M, and Kirby W.M. (1951). Effectiveness of a new compound, benemid, in elevating serum penicillin concentrations. J. Clin. Invest. 30, 697-700.
84. Hartz A.M, and Bauer B. (2011). ABC transporters in the CNS-An inventory. Curr. Pharm. Biotechnol. 12, 656-673.
85. Hammond C.L, Marchan R, Krance S.M, and Ballatori N. (2007). Glutathione export during apoptosis requires functional multidrug resistance-Associated proteins. J. Biol. Chem. 282, 14337-14347.
86. Silverman W.R, de Rivero Vaccari J.P, Locovei S, Qiu F, Carlsson S.K, Scemes E, Keane R.W, and Dahl G. (2009). The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 284, 18143-18151.
87. Karatas H, Erdener S.E, Gursoy-Ozdemir Y, Lule S, Eren-Kocak E, Sen Z.D, and Dalkara T. (2013). Spreading depression triggers headache by activating neuronal Panx1 channels. Science. 339, 1092-1095.
88. Bateman D.N, Dear J.W, Thanacoody H.K, Thomas S.H, Eddleston M, Sandilands E.A, Coyle J, Cooper J.G, Rodriguez A, Butcher I, Lewis S.C, Vliegenthart A.D, Veiraiah A, Webb D.J, and Gray A. (2014). Reduction of adverse effects from intravenous acetylcysteine treatment for paracetamol poisoning: a randomised controlled trial. Lancet. 383, 697-704.
89. Crawford I.L, Kennedy J.I, Lipton J.M. and Ojeda S.R. (1979). Effects of central administation of probenecid on fevers produced by leukocytic pyrogen and PGE2 in the rabbit. J. Physiol. 287, 519-533.
90. Empey P.E, de Mendizabal N.V, Bell M.J, Bies R.R, Anderson K.B, Kochanek P.M, Adelson P.D, and Poloyac S.M. (2013). Therapeutic hypothermia decreases phenytoin elimination in children with traumatic brain injury. Crit. Care Med. 41, 2379-2387.
91. Anderson G.D, Peterson T.C, Vonder Haar C, Kantor E.D, Farin F.M, Bammler T.K, Macdonald J.W, and Hoane M.R. (2013). ComParison of the effects of erythropoietin and anakinra on functional recovery and gene expression in a traumatic brain injury model. Front. Pharmacol. 4, 129.
92. Vonder Haar C, Anderson G.D, Elmore B.E, Moore L.H, Wright A.M, Kantor E.D, Farin F.M, Bammler T.K, MacDonald J.W, and Hoane M.R. (2014). ComParison of the effect of minocycline and simvastatin on functional recovery and gene expression in a rat traumatic brain injury model. J. Neurotrauma. 31, 961-975.
93. Anderson G.D, Peterson T.C, Farin F.M, Bammler T.K, Beyer R.P, Kantor E.D. and Hoane M.R. (2013). The effect of nicotinamide on gene expression in a traumatic brain injury model. Front. Neurosci. 7, 21.
94. Peterson T.C, Anderson G.D, Kantor E.D, and Hoane M.R. (2012). A comParison of the effects of nicotinamide and progesterone on functional recovery of cognitive behavior following cortical contusion injury in the rat. J. Neurotrauma. 29, 2823-2830.
95. Mahmood A, Goussev A, Kazmi H, Qu C, Lu D, and Chopp M. (2009). Long-Term benefits after treatment of traumatic brain injury with simvastatin in rats. Neurosurgery. 65, 187-192.
96. Li B, Mahmood A, Lu D, Wu H, Xiong Y, Qu C, and Chopp M. (2009). Simvastatin attenuates microglial cells and astrocyte activation and decreases interleukin-1beta level after traumatic brain injury. Neurosurgery. 65, 179-186.
97. Atif F, Sayeed I, Ishrat T. and Stein D.G. (2009). Progesterone with vitamin D affords better neuroprotection against excitotoxicity in cultured cortical neurons than progesterone alone. Mol. Med. 15, 328-336.
98. Temkin N.R, Anderson G.D, Winn H.R, Ellenbogen R.G, Britz G.W, Schuster J, Lucas T, Newell D.W, Mansfield P.N, Machamer J.E, Barber J, and Dikmen S.S. (2007). Magnesium sulfate for neuroprotection after traumatic brain injury: a randomised controlled trial. Lancet Neurol. 6, 29-38.
99. Temkin N.R, Dikmen S.S, Anderson G.D, Wilensky A.J, Holmes M.D, Cohen W, Newell D.W, Nelson P, Awan A, and Winn H.R. (1999). Valproate therapy for prevention of posttraumatic seizures: a randomized trial. J. Neurosurg. 91, 593-600.
100. Temkin N.R, Dikmen S.S, Wilensky A.J, Keihm J, Chabal S, and Winn H.R. (1990). A randomized, double-blind study of phenytoin for the prevention of post-Traumatic seizures. N. Engl. J. Med. 323, 497-502.
101. Chow S.C. (2014). Adaptive clinical trial design. Annu. Rev. Med. 65, 405-415.
102. Cruchaga C, Kauwe J.S, Harari O, Jin S.C, Cai Y, Karch C.M, Benitez B.A, Jeng A.T, Skorupa T, Carrell D, Bertelsen S, Bailey M, McKean D, Shulman J.M, De Jager P.L, Chibnik L, Bennett D.A, Arnold S.E, Harold D, Sims R, Gerrish A, Williams J, Van Deerlin V.M, Lee V.M, Shaw L.M, Trojanowski J.Q, Haines J.L, Mayeux R, Pericak-Vance M.A, Farrer L.A, Schellenberg G.D, Peskind E.R, Galasko D, Fagan A.M, Holtzman D.M, Morris J.C. (2013). GWAS of cerebrospinal fluid tau levels identifies risk variants for Alzheimers disease. Neuron. 78, 256-268.
103. Yeatts S.D. (2013). Novel methodologic approaches to phase I, II, and III trials. Stroke 44, S116-S118.
104. Gagne J.J, Thompson L, O'Keefe K, and Kesselheim A.S. (2014). Innovative research methods for studying treatments for rare diseases: methodological review. BMJ 349, g6802.
105. Bazarian J.J, Blyth B, Mookerjee S, He H, and McDermott M.P. (2010). Sex differences in outcome after mild traumatic brain injury. J. Neurotrauma. 27, 527-539.
106. Diaz-Arrastia R, Kochanek P.M, Bergold P, Kenney K, Marx C.E, Grimes C.J, Loh L.T, Adam L.T, Oskvig D, Curley K.C, and Salzer W. (2014). Pharmacotherapy of traumatic brain injury: state of the science and the road forward: report of the Department of Defense Neurotrauma Pharmacology Workgroup. J. Neurotrauma. 31, 135-158.
107. Marklund N, and Hillered L. (2011). Animal modelling of traumatic brain injury in preclinical drug development: where do we go from here? Br. J. Pharmacol. 164, 1207-1229