5-hydroxytryptamine1A (5-HT1A) receptor agonists: A decade of empirical evidence supports their use as an efficacious therapeutic strategy for brain trauma

Brain Research

Volumn 1640, Issue , 2016, Pages 5-14

  Cheng, Jeffrey P ^a,b   Leary, Jacob B ^a,b   Sembhi, Aerin ^a   Edwards, Clarice M ^a,b   Bondi, Corina O ^a,b,c   Kline, Anthony E ^a,b,c  

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

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

5 HT1A receptor agonists; Behavioral outcome; Controlled cortical impact; Functional recovery; Hippocampus; Learning and memory; Morris water maze; Serotonin1A; Traumatic brain injury

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; BUSPIRONE; REPINOTAN; SEROTONIN 1A AGONIST; NEUROPROTECTIVE AGENT; SEROTONIN 1 AGONIST; SEROTONIN 1A RECEPTOR;

ACQUIRED BRAIN INJURY; ACUTE DRUG ADMINISTRATION; CHRONIC DRUG ADMINISTRATION; CONSENSUS; DRUG EFFICACY; ENVIRONMENTAL ENRICHMENT; HISTOPATHOLOGY; HUMAN; PRIORITY JOURNAL; REVIEW; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURIES, TRAUMATIC; METABOLISM; PATHOLOGY; PSYCHOLOGY;

ANIMALS; BRAIN INJURIES, TRAUMATIC; HUMANS; NEUROPROTECTIVE AGENTS; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN 5-HT1 RECEPTOR AGONISTS;

EID: 84949476237     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.11.026     Document Type: Review

References (76)

1. Alessandri, B., Tsuchida, E., Bullock, R.M., The neuroprotective effect of a new serotonin receptor agonist, BAY x3702, upon focal ischemic brain damage caused by acute subdural hematoma in the rat. Brain Res. 845 (1999), 232–235.
2. Anderson, V.A., Catroppa, C., Morse, S., Haritou, F., Rosenfeld, J., Outcome from mild head injury in young children: a prospective study. J. Clin. Exp. Neuropsychol. 23 (2001), 705–716.
3. 1A receptors in the rat hippocampus and cortex. Drug Dev. Res. 26 (1992), 275–286.
4. Babikian, T., Asarnow, R., Neurocognitive outcomes and recovery after pediatric TBI: meta-analytic review of the literature. Neuropyschology 23 (2009), 283–296.
5. Bales, J.W., Wagner, A.K., Kline, A.E., Dixon, C.E., Persistent cognitive dysfunction after traumatic brain injury: a dopamine hypothesis. Neurosci. Biobehav. Rev. 33 (2009), 981–1003.
6. Barnes, N.M., Sharp, T., A review of central 5-HT receptors and their function. Neuropharmacology 38 (1999), 1083–1152.
7. Bayir, H., Clark, R.S., Kochanek, P.M., Promising strategies to minimize secondary brain injury after head trauma. Crit. Care Med. 31 (2003), S112–S117.
8. Bondi, C.O., Klitsch, K.C., Leary, J.B., Kline, A.E., Environmental enrichment as a viable neurorehabilitation strategy for experimental traumatic brain injury. J. Neurotrauma 31 (2014), 873–888.
9. Bondi, C.O., Semple, B.D., Noble-Haeusslein, L.J., Osier, N.D., Carlson, S.W., Dixon, C.E., Giza, C.C., Kline, A.E., Found in translation: understanding the biology and behavior of traumatic brain injury. Neurosci. Biobehav. Rev., 2014, 10.1016/j.neubiorev.2014.12.004.
10. Bramlett, H.M., Green, E.J., Dietrich, W.D., Busto, R., Globus, M.Y., Ginsberg, M.D., Posttraumatic brain hypothermia provides protection from sensorimotor and cognitive behavioral deficits. J. Neurotrauma 12 (1995), 289–298.
11. Cheng, J.P., Aslam, H.A., Hoffman, A.N., Zafonte, R.D., Kline, A.E., The neurobehavioral benefit conferred by a single systemic administration of 8-OH-DPAT after brain trauma is confined to a narrow therapeutic window. Neurosci. Lett. 416 (2007), 165–168.
12. 1A receptor agonist 8-OH-DPAT after cortical impact injury facilitates motor recovery and acquisition of spatial learning. Behav. Brain Res. 194 (2008), 79–85.
13. Cheng, J.P., Shaw, K.E., Monaco, C.M., Hoffman, A.N., Sozda, C.N., Olsen, A.S., Kline, A.E., A relatively brief exposure to environmental enrichment after experimental traumatic brain injury confers long-term cognitive benefits. J. Neurotrauma 29 (2012), 2684–2688.
14. Chew, E., Zafonte, R.D., Pharmacological management of neurobehavioral disorders following traumatic brain injury—a state-of-the-art review. J. Rehabil. Res. Dev. 46 (2009), 851–878.
15. Clark, R.S.B., Kochanek, P.M., Marion, D.W., Schiding, J.K., White, M., Palmer, A.M., Dekosky, S.T., Mild posttraumatic hypothermia reduces mortality after severe controlled cortical impact in rats. J. Cereb. Blood Flow Metab. 16 (1996), 252–261.
16. Clifton, G.L., Jiang, J.Y., Lyeth, B.G., Jenkins, L.W., Hamm, R.J., Hayes, R.L., Marked protection by moderate hypothermia after experimental traumatic brain injury. J. Cereb. Blood Flow Metab. 11 (1991), 114–121.
17. De Vry, J., Dietrich, H., Glaser, T., Heine, H.-G., Horváth, E., Jork, R., Maertins, T., Mauler, F., Opitz, W., Scherling, D., Schohe-Loop, R., Schwartz, T., BAY x 3702. Drugs Future 22 (1997), 341–349.
18. 1A receptor agonist BAY x 3702 in the rat. Eur. J. Pharmacol. 357 (1998), 1–8.
19. de Witt, B.W., Ehrenberg, K.M., McAloon, R.L., Panos, A.H., Shaw, K.E., Raghavan, P.V., Skidmore, E.R., Kline, A.E., Abbreviated environmental enrichment enhances neurobehavioral recovery comparably to continuous exposure after traumatic brain injury. Neurorehabil. Neural Repair 25 (2011), 343–350.
20. Dixon, C.E., Markgraf, C.G., Angileri, F., Pike, B.R., Wolfson, B., Newcomb, J.K., Bismar, M.M., Blanco, A.J., Clifton, G.L., Hayes, R.L., Protective effects of moderate hypothermia on behavioral deficits but not necrotic cavitation following cortical impact injury in the rat. J. Neurotrauma 15 (1998), 95–103.
21. Doppenberg, E.M.R., Choi, S.C., Bullock, R., Clinical trials in traumatic brain injury: lessons for the future. J. Neurosurg. Anesthesiol. 16 (2004), 87–94.
22. Faden, A.I., Demediuk, P., Panter, S.S., Vink, R., The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244 (1989), 798–800.
23. Faul, M., Xu, L., Wald, M.M., Coronado, V.G., Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002–2006. Atlanta (GA): Centers for Disease Control and Prevention. Natl. Cent. Inj. Prev. Control, 2010.
24. Fujii, T., Yoshizawa, M., Nakai, K., Fujimoto, K., Suzuki, T., Kawashima, K., Demonstration of the facilitatory role of 8-OH-DPAT on cholinergic transmission in the rat hippocampus using in vivo microdialysis. Brain Res. 761 (1997), 244–249.
25. Garcia, A.N., Shah, M.A., Dixon, C.E., Wagner, A.K., Kline, A.E., Biologic and plastic effects of experimental traumatic brain injury treatment paradigms and their relevance to clinical rehabilitation. PM R 3 (2011), S18–S27.
26. Giacino, J.T., Whyte, J., Bagiella, E., Kalmar, K., Childs, N., Khademi, A., Eifert, B., Long, D., Katz, D.I., Cho, S., Yablon, S.A., Luther, M., Hammond, F.M., Nordenbo, A., Novak, P., Mercer, W., Maurer-Karattup, P., Sherer, M., Placebo-controlled trial of amantadine for severe traumatic brain injury. N. Engl. J. Med. 366 (2012), 819–826.
27. Hamm, R.J., Temple, M.D., O'Dell, D.M., Pike, B.R., Lyeth, B.G., Exposure to environmental complexity promotes recovery of cognitive function after traumatic brain injury. J. Neurotrauma 13 (1996), 41–47.
28. 1A receptor agonist repinotan hydrochloride (BAY x 3702) attenuates NMDA-induced delayed neuronal death in rat magnocellular nucleus basalis. Neuroscience 108 (2001), 629–642.
29. Hawley, C.A., Ward, A.B., Magnay, A.R., Long, J., Outcomes following childhood head injury: a population study. J. Neurol. Neurosurg. Psychiatr. 75 (2004), 737–742.
30. Hoffman, A.N., Cheng, J.P., Zafonte, R.D., Kline, A.E., Administration of haloperidol and risperidone after neurobehavioral testing hinders the recovery of traumatic brain injury-induced deficits. Life Sci. 83 (2008), 602–607.
31. Hyder, A.A., Wunderlich, C.A., Puvanachandra, P., Gururaj, G., Kobusingye, O.C., The impact of traumatic brain injuries: a global perspective. Neurorehabilitation 22 (2007), 341–355.
32. Keenan, H.T., Runyan, D.K., Marshall, S.W., Nocera, M.A., Merten, D.F., A population-based comparison of clinical and outcome characteristics of young children with serious inflicted and noninflicted traumatic brain injury. Pediatrics 114 (2004), 633–639.
33. Kline, A.E., Hoffman, A.N., Cheng, J.P., Zafonte, R.D., Massucci, J.L., Chronic administration of antipsychotics impede behavioral recovery after experimental traumatic brain injury. Neurosci. Lett. 448 (2008), 263–267.
34. 1A receptor agonist 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT) after experimental traumatic brain injury is not mediated by concomitant hypothermia. J. Neurotrauma 21 (2004), 175–185.
35. Kline, A.E., Massucci, J.L., Ma, X., Zafonte, R.D., Dixon, C.E., Bromocriptine reduces lipid peroxidation and enhances spatial learning and hippocampal neuron survival in a rodent model of focal brain trauma. J. Neurotrauma 21 (2004), 1712–1722.
36. Kline, A.E., Massucci, J.L., Marion, D.W., Dixon, C.E., Attenuation of working memory and spatial acquisition deficits after a delayed and chronic bromocriptine treatment regimen in rats subjected to traumatic brain injury by controlled cortical impact. J. Neurotrauma 19 (2002), 415–425.
37. Kline, A.E., Massucci, J.L., Zafonte, R.D., Dixon, C.E., Defeo, J.R., Rogers, E.H., Differential effects of single versus multiple administrations of haloperidol and risperidone on functional outcome after experimental brain trauma. Crit. Care Med. 35 (2007), 919–924.
38. Kline, A.E., McAloon, R.L., Henderson, K.A., Bansal, U.K., Ganti, B.M., Ahmed, R.H., Gibbs, R.B., Sozda, C.N., Evaluation of a combined therapeutic regimen of 8-OH-DPAT and environmental enrichment after experimental traumatic brain injury. J. Neurotrauma 27 (2010), 2021–2032.
39. 1A receptor agonist buspirone after experimental traumatic brain injury. J. Neurotrauma 29 (2012), 1960–1969.
40. 1A receptor agonist 8-OH-DPAT and chronic environmental enrichment confer neurobehavioral benefit after experimental brain trauma. Behav. Brain Res. 177 (2007), 186–194.
41. Kline, A.E., Yan, H.Q., Bao, J., Marion, D.W., Dixon, C.E., Chronic methylphenidate treatment enhances water maze performance following traumatic brain injury in rats. Neurosci. Lett. 280 (2000), 163–166.
42. 1A receptor agonist repinotan HCl attenuates histopathology and spatial learning deficits following traumatic brain injury in rats. Neuroscience 106 (2001), 547–555.
43. 1A receptor agonist 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT) against traumatic brain injury-induced cognitive deficits and neuropathology in adult male rats. Neurosci. Lett. 333 (2002), 179–182.
44. Kokiko, O.N., Hamm, R.J., A review of pharmacological treatments used in experimental models of traumatic brain injury. Brain Inj. 21 (2007), 259–274.
45. 1A receptor-mediated pathways by BAY x 3702 in freely moving rats. Neurosci. Lett. 265 (1999), 33–36.
46. Langlois, J.A., Rutland-Brown, W., Thomas, K.E., Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. Atlanta (GA): Centers for Disease Control and Prevention. Natl. Cent. Inj. Prev. Control, 2004.
47. Mao, Z., Song, Z., Li, G., Lv, W., Zhao, X., Li, B., Feng, X., Chen, Y., 8-hydroxy-2-(di-n-propylamino)tetralin intervenes with neural cell apoptosis following diffuse axonal injury. Neural Regen. Res. 8 (2013), 133–142.
48. Massucci, J.L., Kline, A.E., Ma, X., Zafonte, R.D., Dixon, C.E., Time dependent alterations in dopamine tissue levels and metabolism after experimental traumatic brain injury in rats. Neurosci. Lett. 372 (2004), 127–131.
49. 1A receptor agonist BAY x 3702 in vitro and in vivo. Brain Res. 888 (2001), 150–157.
50. 1A receptor agonist, in animal models of stroke and traumatic brain injury. J. Cereb. Blood Flow Metab. 25 (2005), 451–459.
51. Max, W., Mackenzie, E.J., Rice, D.P., Head injuries: costs and consequences. J. Head Trauma Rehabil. 6 (1991), 76–91.
52. McIntosh, T.K., Yu, T., Gennarelli, T.A., Alterations in regional brain catecholamine concentrations after experimental brain injury in the rat. J. Neurochem. 63 (1994), 1426–1433.
53. 1A receptor agonist 8-OH-DPAT: possible significance for neuroprotection. Eur. J. Pharmacol. 406 (2000), 319–324.
54. Meneses, A., 5-HT system and cognition. Neurosci. Biobehav. Rev. 23 (1999), 1111–1125.
55. 1A receptors and memory. Neurosci. Biobehav. Rev. 31 (2007), 705–727.
56. Menon, D.K., Unique challenges in clinical trials in traumatic brain injury. Crit. Care Med. 37 (2009), S129–S135.
57. Monaco, C.M., Gebhardt, K.M., Chelbowski, S.M., Shaw, K.E., Cheng, J.P., Henchir, J.J., Zupa, M.F., Kline, A.E., A combined therapeutic regimen of buspirone and environmental enrichment is more efficacious than either alone in enhancing spatial learning in brain-injured pediatric rats. J. Neurotrauma 31 (2014), 1934–1941.
58. 1A agonist in traumatically brain injured patients. J. Neurotrauma 18 (2001), 1313–1321.
59. 1A receptor agonist buspirone. J. Neurotrauma 29 (2012), 1898–1907.
60. 1A receptor agonist 8-OH-DPAT protects cholinergic nucleus basalis neurons against NMDA excitotoxicity. Neuroreport 14 (2003), 57–60.
61. Palmer, A.M., Marion, D.W., Botscheller, M.L., Swedlow, P.E., Styren, S.D., DeKosky, S.T., Traumatic brain injury-induced excitotoxicity assessed in a controlled cortical impact model. J. Neurochem. 61 (1993), 2015–2024.
62. Passineau, M.J., Green, E.J., Dietrich, W.D., Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Exp. Neurol. 168 (2001), 373–384.
63. Phelps, T.I., Bondi, C.O., Ahmed, R.H., Olugbade, Y.T., Kline, A.E., Divergent long-term consequences of chronic treatment with haloperidol, risperidone, and bromocriptine on traumatic brain injury-induced cognitive deficits. J. Neurotrauma 32 (2015), 590–597.
64. Plenger, P.M., Dixon, C.E., Castillo, R.M., Frankowski, R.F., Yablon, S.A., Levin, H.S., Subacute methylphenidate treatment for moderate to moderately severe traumatic brain injury: a preliminary double-blind placebo-controlled study. Arch. Phys. Med. Rehab. 77 (1996), 536–540.
65. 1A receptor agonists in rodent models of focal and global cerebral ischemia. Eur. J. Pharmacol. 203 (1991), 213–222.
66. Rose, M.E., Huerbin, M.B., Melick, J., Marion, D.W., Palmer, A.M., Schiding, J.K., Kochanek, P.M., Graham, S.H., Regulation of interstitial excitatory amino acid concentrations after cortical contusion injury. Brain Res. 935 (2002), 40–46.
67. Sakaue, M., Somboonthum, P., Nishihara, B., Koyama, Y., Hashimoto, H., Baba, A., Matsuda, T., Postsynaptic 5-hydroxytryptamine (1A) receptor activation increases in vivo dopamine release in rat prefrontal cortex. Br. J. Pharmacol. 129 (2000), 1029–1034.
68. Selassie, A.W., Zaloshnja, E., Langlois, J.A., Miller, T., Jones, P., Steiner, C., Incidence of long-term disability following traumatic brain injury hospitalization, United States, 2003. J. Head Trauma Rehabil. 23 (2008), 123–131.
69. Sosin, D.M., Sniezek, J.E., Waxweiler, R.J., Trends in death associated with traumatic brain injury, 1979 through 1992. JAMA 273 (1995), 1778–1780.
70. Sozda, C.N., Hoffman, A.N., Olsen, A.S., Cheng, J.P., Zafonte, R.D., Kline, A.E., Empirical comparison of typical and atypical environmental enrichment paradigms on functional and histological outcome after experimental traumatic brain injury. J. Neurotrauma 27 (2010), 1047–1057.
71. Teyler, T.J., Perkins, A.T., Harris, K.M., The development of long-term potentiation in hippocampus and neocortex. Neuropsychologia 27 (1989), 31–39.
72. Thurman, D.J., Alverson, C., Dunn, K.A., Guerrero, J., Sniezek, J.E., Traumatic brain injury in the United States: a public health perspective. J. Head Trauma Rehabil. 14 (1999), 602–615.
73. Wagner, A.K., Sokoloski, J.E., Ren, D., Chen, X., Khan, A.S., Zafonte, R.D., Michael, A.C., Dixon, C.E., Controlled cortical impact injury affects dopaminergic transmission in the rat striatum. J. Neurochem. 95 (2005), 457–465.
74. Wheaton, P., Mathias, J.L., Vink, R., Impact of early pharmacotherapy treatment on cognitive and behavioral outcome after traumatic brain injury in adults: a meta-analysis. J. Clin. Psychopharmacol. 29 (2009), 468–477.
75. Yan, H.Q., Kline, A.E., Ma, X., Li, Y., Dixon, C.E., Traumatic brain injury reduces dopamine transporter protein expression in the rat frontal cortex. NeuroReport 13 (2002), 1899–1901.
76. 7 receptors on 8-OH-DPAT-induced behavioral recovery after experimental traumatic brain injury. Neurosci. Lett. 515 (2012), 153–156.