Traumatic brain injury: Central and peripheral role of α7 nicotinic acetylcholine receptors

Current Drug Targets

Volumn 13, Issue 5, 2012, Pages 631-636

  Kelso, Matthew L ^a   Oestreich, Julie H ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Cytokine; Excitotoxicity; Inflammation; Leukocyte; Macrophage; Neurodegeneration; Platelet; Traumatic brain injury

Indexed keywords

BIOLOGICAL MARKER; BUNGAROTOXIN RECEPTOR;

ARTICLE; BRAIN BLOOD FLOW; BRAIN REGION; DISEASE COURSE; EXCITOTOXICITY; HUMAN; NEUROLOGIC DISEASE; NEUROTRANSMISSION; NONHUMAN; PROTEIN EXPRESSION; TRAUMATIC BRAIN INJURY;

EID: 84860439221     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/138945012800398964     Document Type: Article

References (70)

1. Faul M, Xu L, Wald MM, Coronado VG. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002-2006. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control 2010.
2. Menon DK, Schwab K, Wright DW, Maas AI. Position statement: definition of traumatic brain injury. Arch Physical Med Rehab 2010; 91(11): 1637-1640.
3. Faden AI, Demediuk P, Panter SS, Vink R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 1989; 244(4906): 798-800.
4. Palmer AM, Marion DW, Botscheller ML, Bowen DM, DeKosky ST. Increased transmitter amino acid concentration in human ventricular CSF after brain trauma. Neuroreport 1994; 6(1): 153-156.
5. Palmer AM, Marion DW, Botscheller ML, Swedlow PE, Styren SD, DeKosky ST. Traumatic brain injury-induced excitotoxicity assessed in a controlled cortical impact model. J Neurochem 1993; 61(6): 2015-2024.
6. Baker AJ, Moulton RJ, MacMillan VH, Shedden PM. Excitatory amino acids in cerebrospinal fluid following traumatic brain injury in humans. J Neurosurg 1993; 79(3): 369-372.
7. Seifman MA, Adamides AA, Nguyen PN, et al. Endogenous melatonin increases in cerebrospinal fluid of patients after severe traumatic brain injury and correlates with oxidative stress and metabolic disarray. J Cereb Blood Flow Metab 2008; 28(4):684-696.
8. Zhang H, Zhang X, Zhang T, Chen L. Excitatory amino acids in cerebrospinal fluis of patients with acute head injuries. Clin Chem 2001; 47(8): 1458-1462.
9. Rothstein JD, Dykes-Hoberg M, Pardo CA, et al. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996; 16(3): 675-686.
10. Rao VL, Baskaya MK, Dogan A, Rothstein JD, Dempsey RJ. Traumatic brain injury down-regulates glial glutamate transporter (GLT-1 and GLAST) proteins in rat brain. J Neurochem 1998; 70(5): 2020-2027.
11. van Landeghem FK, Stover JF, Bechmann I, et al. Early expression of glutamate transporter proteins in ramified microglia after controlled cortical impact injury in the rat. Glia 2001; 35(3): 167-179.
12. van Landeghem FK, Weiss T, Oehmichen M, von Deimling A. Decreased expression of glutamate transporters in astrocytes after human traumatic brain injury. J Neurotrauma 2006; 23(10): 1518-1528.
13. Ikonomidou C, Turski L. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet Neurol 2002; 1(6): 383-386.
14. Narayan RK, Michel ME, Ansell B, et al. Clinical trials in head injury. J Neurotrauma 2002; 19(5): 503-557.
15. Bornstein MB. Presence and action of acetylcholine in experimental brain trauma. J Neurophysiol 1946; 9: 349-366.
16. Metz B. Acetylcholine and experimental brain injury. J Neurosurg 1971; 35(5): 523-528.
17. Saija A, Hayes RL, Lyeth BG, Dixon CE, Yamamoto T, Robinson SE. The effect of concussive head injury on central cholinergic neurons. Brain Res 1988; 452(1-2): 303-311.
18. Scremin OU, Li MG, Roch M, Booth R, Jenden DJ. Acetylcholine and choline dynamics provide early and late markers of traumatic brain injury. Brain Res 2006; 1124(1): 155-166.
19. Dixon CE, Bao J, Long DA, Hayes RL. Reduced evoked release of acetylcholine in the rodent hippocampus following traumatic brain injury. Pharmacol Biochem Behav 1996; 53(3): 679-686.
20. Dixon CE, Ma X, Marion DW. Reduced evoked release of acetylcholine in the rodent neocortex following traumatic brain injury. Brain Res 1997; 749(1): 127-130.
21. Dixon CE, Bao J, Johnson KM, et al. Basal and scopolamineevoked release of hippocampal acetylcholine following traumatic brain injury in rats. Neurosci Lett 1995; 198(2): 111-114.
22. Donat CK, Schuhmann MU, Voigt C, Nieber K, Schliebs R, Brust P. Alterations of acetylcholinesterase activity after traumatic brain injury in rats. Brain Inj 2007; 21(10): 1031-1037.
23. Ostberg A, Virta J, Rinne JO, et al. Cholinergic dysfunction after traumatic brain injury: preliminary findings from a PET study. Neurology 2011; 76(12): 1046-1050.
24. Alkondon M, Pereira EF, Cortes WS, Maelicke A, Albuquerque EX. Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 1997; 9(12): 2734-2742.
25. Guseva MV, Hopkins DM, Pauly JR. An autoradiographic analysis of rat brain nicotinic receptor plasticity following dietary choline modification. Pharmacol Biochem Behav 2006; 84(1): 26-34.
26. Verbois SL, Sullivan PG, Scheff SW, Pauly JR. Traumatic brain injury reduces hippocampal alpha7 nicotinic cholinergic receptor binding. J Neurotrauma 2000; 17(11): 1001-1011.
27. Verbois SL, Scheff SW, Pauly JR. Time-dependent changes in rat brain cholinergic receptor expression after experimental brain injury. J Neurotrauma 2002; 19(12): 1569-1585.
28. Guseva MV, Hopkins DM, Scheff SW, Pauly JR. Dietary choline supplementation improves behavioral, histological, and neurochemical outcomes in a rat model of traumatic brain injury. J Neurotrauma 2008; 25(8): 975-983.
29. Verbois SL, Hopkins DM, Scheff SW, Pauly JR. Chronic intermittent nicotine administration attenuates traumatic brain injury-induced cognitive dysfuntion. Neuroscience 2003; 119(4): 1199-1208.
30. Verbois SL, Scheff SW, Pauly JR. Chronic nicotine treatment attenuates alpha7 nicotinic receptor deficits following traumatic brain injury. Neuropharmacology 2003; 44(2): 224-233.
31. Kelso ML, Wehner JM, Collins AC, Scheff SW, Pauly JR. The pathophysiology of traumatic brain injury in alpha7 nicotinic cholinergic receptor knockout mice. Brain Res 2006; 1083(1): 204-210.
32. Hoffmeister PG, Donat CK, Schuhmann MU, et al. Traumatic brain injury elicits similar alterations in alpha7 nicotinic receptor density in two different experimental models. Neuromolecular Med 2011; 13(1): 44-53.
33. Donat CK, Schuhmann MU, Voigt C, Nieber K, Deuther-Conrad W, Brust P. Time-dependent alterations of cholinergic markers after experimental traumatic brain injury. Brain Res 2008; 1246: 167-177.
34. Dwyer JB, McQuown SC, Leslie FM. The dynamic effects of nicotine on the developing brain. Pharmacol Ther 2009; 122(2): 125-139.
35. Murdoch I, Perry EK, Court JA, Graham DI, Dewar D. Cortical cholinergic dysfunction after human head injury. J Neurotrauma 1998; 15(5): 295-305.
36. Toyohara J, Wu J, Hashimoto K. Recent development of radioligands for imaging alpha7 nicotinic acetylcholine receptors in the brain. Curr Top Med Chem 2010; 10(15): 1544-1557.
37. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW. Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 1993; 13(2): 596-604.
38. 2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 2004; 35(1): 1-8.
39. Khiroug L, Giniatullin R, Klein RC, Fayuk D, Yakel JL. Functional mapping and Ca2+ regulation of nicotinic acetylcholine receptor channels in rat hippocampal CA1 neurons. J Neurosci 2003; 23(27): 9024-9031.
40. 2+/calmodulin signaling pathway in rat prefrontal cortex nerve terminals. Synapse 2006; 59(8): 491-501.
41. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 1996; 383(6602): 713-716.
42. Kanno T, Yaguchi T, Yamamoto S, et al. Bidirectional regulations for glutamate and GABA release in the hippocampus by alpha7 and non-alpha7 ACh receptors. Biochem Biophys Res Commun 2005; 338(2): 742-747.
43. Shytle RD, Mori T, Townsend K, et al. Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors. J Neurochem 2004; 89(2): 337-343.
44. Wang H, Yu M, Ochani M, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003; 421(6921): 384-388.
45. De Simone R, Ajmone-Cat M, Carnevale D, Minghetti L. Activation of alpha7 nicotinic acetylcholine receptor by nicotine selectively up-regulates cyclooxygenase-2 and prostaglandin E2 in rat microglial cultures. J Neuroinflammation 2005; 2(1): 4.
46. Suzuki T, Hide I, Matsubara A, et al. Microglial alpha7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role. J Neurosci Res 2006; 83(8): 1461-1470.
47. Sato KZ, Fujii T, Watanabe Y, et al. Diversity of mRNA expression for muscarinic acetylcholine receptor subtypes and neuronal nicotinic acetylcholine receptor subunits in human mononuclear leukocytes and leukemic cell lines. Neurosci Lett 1999; 266(1): 17-20.
48. Benhammou K, Lee M, Strook M, et al. [(3)H]Nicotine binding in peripheral blood cells of smokers is correlated with the number of cigarettes smoked per day. Neuropharmacology 2000; 39(13): 2818-2829.
49. Wang H, Yu M, Ochani M, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003; 421(6921): 384-388.
50. Saeed RW, Varma S, Peng-Nemeroff T, et al. Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation. J Exp Med 2005; 201(7): 1113-1123.
51. Neumann S, Razen M, Habermehl P, et al. The non-neuronal cholinergic system in peripheral blood cells: effects of nicotinic and muscarinic receptor antagonists on phagocytosis, respiratory burst and migration. Life Sci 2007; 80(24-25): 2361-2364.
52. De Rosa MJ, Dionisio L, Agriello E, Bouzat C, Esandi Mdel C. Alpha 7 nicotinic acetylcholine receptor modulates lymphocyte activation. Life Sci 2009; 85(11-12): 444-449.
53. Kox M, Pompe JC, Pickkers P, Hoedemaekers CW, van Vugt AB, van der Hoeven JG. Increased vagal tone accounts for the observed immune paralysis in patients with traumatic brain injury. Neurology 2008; 70(6): 480-485.
54. Schwarzmaier SM, Kim SW, Trabold R, Plesnila N. Temporal profile of thrombogenesis in the cerebral microcirculation after traumatic brain injury in mice. J Neurotrauma 2010; 27(1): 121-130.
55. Stein SC, Chen XH, Sinson GP, Smith DH. Intravascular coagulation: a major secondary insult in nonfatal traumatic brain injury. J Neurosurg 2002; 97(6): 1373-1377.
56. Schedel A, Thornton S, Schloss P, Kluter H, Bugert P. Human platelets express functional {alpha}7-nicotinic acetylcholine receptors. Arterioscler Thromb Vasc Biol 2011; 31(4): 928-934.
57. Ottani A, Giuliani D, Mioni C, et al. Vagus nerve mediates the protective effects of melanocortins against cerebral and systemic damage after ischemic stroke. J Cereb Blood Flow Metab 2009; 29(3): 512-523.
58. Heeschen C, Weis M, Aicher A, Dimmeler S, Cooke JP. A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors. J Clin Invest 2002; 110(4): 527-536.
59. Lau PP, Li L, Merched AJ, Zhang AL, Ko KW, Chan L. Nicotine induces proinflammatory responses in macrophages and the aorta leading to acceleration of atherosclerosis in low-density lipoprotein receptor(-/-) mice. Arterioscler Thromb Vasc Biol 2006; 26(1): 143-149.
60. Cucina A, Fuso A, Coluccia P, Cavallaro A. Nicotine inhibits apoptosis and stimulates proliferation in aortic smooth muscle cells through a functional nicotinic acetylcholine receptor. J Surg Res 2008; 150(2): 227-235.
61. Chu LW, Ma ES, Lam KK, Chan MF, Lee DH. Increased alpha 7 nicotinic acetylcholine receptor protein levels in Alzheimer's disease patients. Dement Geriatr Cogn Disord 2005; 19(2-3): 106-112.
62. Perl O, Ilani T, Strous RD, Lapidus R, Fuchs S. The alpha7 nicotinic acetylcholine receptor in schizophrenia: decreased mRNA levels in peripheral blood lymphocytes. FASEB J 2003; 17(13): 1948-50.
63. Perl O, Strous RD, Dranikov A, Chen R, Fuchs S. Low levels of alpha7-nicotinic acetylcholine receptor mRNA on peripheral blood lymphocytes in schizophrenia and its association with illness severity. Neuropsychobiol 2006; 53(2): 88-93.
64. Baskin F, Rosenberg RN, Iyer L, Hynan L, Cullum CM. Platelet APP isoform ratios correlate with declining cognition in AD. Neurology 2000; 54(10): 1907-1909.
65. Davies TA, Long HJ, Tibbles HE, et al. Moderate and advanced Alzheimer's patients exhibit platelet activation differences. Neurobiol Aging 1997; 18(2): 155-162.
66. Di Luca M, Pastorino L, Bianchetti A, et al. Differential level of platelet amyloid beta precursor protein isoforms: an early marker for Alzheimer disease. Arch Neurol 1998; 55(9): 1195-200.
67. Gurguis GN, Ed. Psychiatric Disorders. 2nd ed. Oxford, UK: Elsevier, Inc.; 2007.
68. Kem WR. The brain alpha7 nicotinic receptor may be an important therapeutic target for the treatment of Alzheimer's disease: studies with DMXBA (GTS-21). Behav Brain Res 2000; 113(1-2): 169-181.
69. Olincy A, Stevens KE. Treating schizophrenia symptoms with an alpha7 nicotinic agonist, from mice to men. Biochem Pharmacol 2007; 74(8): 1192-1201.
70. Shytle RD, Silver AA, Sheehan KH, Sheehan DV, Sanberg PR. Neuronal nicotinic receptor inhibition for treating mood disorders: preliminary controlled evidence with mecamylamine. Depress Anxiety 2002; 16(3): 89-92.