Loss of Acid Sensing Ion Channel-1a and Bicarbonate Administration Attenuate the Severity of Traumatic Brain Injury

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Yin, Terry ^a   Lindley, Timothy E ^a   Albert, Gregory W ^a   Ahmed, Raheel ^a   Schmeiser, Peter B ^a   Grady, M Sean ^b   Howard, Matthew A ^a   Welsh, Michael J ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 1A; BICARBONATE; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ACIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ACIDOSIS; BRAIN CORTEX; BRAIN DISEASE; BRAIN TISSUE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; MALE; MEMORY DISORDER; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PROTEIN DEPLETION; PROTEIN INDUCTION; SPATIAL MEMORY; TRAUMATIC BRAIN INJURY;

ACID SENSING ION CHANNELS; BICARBONATES; BRAIN INJURIES; FEAR; HUMANS; MEMORY; SEVERITY OF ILLNESS INDEX;

EID: 84883102117     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072379     Document Type: Article

References (80)

1. Faul M, Xu L, Wald MD, Coronado VG (2010) Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. In: Centers for Disease Control and Prevention NCfIPaC, editor. Atlanta, GA.
2. Blennow K, Hardy J, Zetterberg H, (2012) The neuropathology and neurobiology of traumatic brain injury. Neuron 76: 886-899.
3. Marion DW, (1998) Head and spinal cord injury. Neurol Clin 16: 485-502.
4. Golding EM, Robertson CS, Bryan RM Jr, (1999) The consequences of traumatic brain injury on cerebral blood flow and autoregulation: a review. Clin Exp Hypertens 21: 299-332.
5. Werner C, Engelhard K, (2007) Pathophysiology of traumatic brain injury. Br J Anaesth 99: 4-9.
6. Coles JP, Fryer TD, Smielewski P, Chatfield DA, Steiner LA, et al. (2004) Incidence and mechanisms of cerebral ischemia in early clinical head injury. J Cereb Blood Flow Metab 24: 202-211.
7. Cunningham AS, Salvador R, Coles JP, Chatfield DA, Bradley PG, et al. (2005) Physiological thresholds for irreversible tissue damage in contusional regions following traumatic brain injury. Brain 128: 1931-1942.
8. Diringer MN, Videen TO, Yundt K, Zazulia AR, Aiyagari V, et al. (2002) Regional cerebrovascular and metabolic effects of hyperventilation after severe traumatic brain injury. J Neurosurg 96: 103-108.
9. Stiefel MF, Tomita Y, Marmarou A, (2005) Secondary ischemia impairing the restoration of ion homeostasis following traumatic brain injury. J Neurosurg 103: 707-714.
10. Unterberg AW, Stover J, Kress B, Kiening KL, (2004) Edema and brain trauma. Neuroscience 129: 1021-1029.
11. Carbonell WS, Grady MS, (1999) Evidence disputing the importance of excitotoxicity in hippocampal neuron death after experimental traumatic brain injury. Ann N Y Acad Sci 890: 287-298.
12. Robertson CL, Bell MJ, Kochanek PM, Adelson PD, Ruppel RA, et al. (2001) Increased adenosine in cerebrospinal fluid after severe traumatic brain injury in infants and children: association with severity of injury and excitotoxicity. Crit Care Med 29: 2287-2293.
13. Krajewska M, You Z, Rong J, Kress C, Huang X, et al. (2011) Neuronal deletion of caspase 8 protects against brain injury in mouse models of controlled cortical impact and kainic acid-induced excitotoxicity. PLoS ONE 6: e24341.
14. Clausen F, Marklund N, Lewen A, Enblad P, Basu S, et al. (2012) Interstitial F(2)-isoprostane 8-iso-PGF(2alpha) as a biomarker of oxidative stress after severe human traumatic brain injury. J Neurotrauma 29: 766-775.
15. Yamada KH, Kozlowski DA, Seidl SE, Lance S, Wieschhaus AJ, et al. (2012) Targeted gene inactivation of calpain-1 suppresses cortical degeneration due to traumatic brain injury and neuronal apoptosis induced by oxidative stress. J Biol Chem 287: 13182-13193.
16. Zhuang Z, Zhou ML, You WC, Zhu L, Ma CY, et al. (2012) Hydrogen-rich saline alleviates early brain injury via reducing oxidative stress and brain edema following experimental subarachnoid hemorrhage in rabbits. BMC Neurosci 13: 47.
17. Ramlackhansingh AF, Brooks DJ, Greenwood RJ, Bose SK, Turkheimer FE, et al. (2011) Inflammation after trauma: microglial activation and traumatic brain injury. Ann Neurol 70: 374-383.
18. Acosta SA, Tajiri N, Shinozuka K, Ishikawa H, Grimmig B, et al. (2013) Long-term upregulation of inflammation and suppression of cell proliferation in the brain of adult rats exposed to traumatic brain injury using the controlled cortical impact model. PLoS ONE 8: e53376.
19. Johnson VE, Stewart JE, Begbie FD, Trojanowski JQ, Smith DH, et al. (2013) Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 136: 28-42.
20. Tsai YD, Liliang PC, Cho CL, Chen JS, Lu K, et al. (2013) Delayed neurovascular inflammation after mild traumatic brain injury in rats. Brain Inj 27: 361-365.
21. Clausen T, Khaldi A, Zauner A, Reinert M, Doppenberg E, et al. (2005) Cerebral acid-base homeostasis after severe traumatic brain injury. J Neurosurg 103: 597-607.
22. Gupta AK, Zygun DA, Johnston AJ, Steiner LA, Al-Rawi PG, et al. (2004) Extracellular Brain pH and Outcome following Severe Traumatic Brain Injury. J Neurotrauma 21: 678-684.
23. DeSalles AA, Kontos HA, Becker DP, Yang MS, Ward JD, et al. (1986) Prognostic significance of ventricular CSF lactic acidosis in severe head injury. J Neurosurg 65: 615-624.
24. Enevoldsen EM, Cold G, Jensen FT, Malmros R, (1976) Dynamic changes in regional CBF, intraventricular pressure, CSF pH and lactate levels during the acute phase of head injury. J Neurosurg 44: 191-214.
25. Rabow L, DeSalles AF, Becker DP, Yang M, Kontos HA, et al. (1986) CSF brain creatine kinase levels and lactic acidosis in severe head injury. J Neurosurg 65: 625-629.
26. Vespa P, Bergsneider M, Hattori N, Wu HM, Huang SC, et al. (2005) Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab 25: 763-774.
27. Wemmie JA, Price MP, Welsh MJ, (2006) Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 29: 578-586.
28. Sherwood TW, Frey EN, Askwith CC (2012) Structure and Activity of the Acid Sensing Ion Channels. Am J Physiol Cell Physiol.
29. Deval E, Gasull X, Noel J, Salinas M, Baron A, et al. (2010) Acid-sensing ion channels (ASICs): pharmacology and implication in pain. Pharmacol Ther 128: 549-558.
30. Xiong ZG, Pignataro G, Li M, Chang SY, Simon RP, (2008) Acid-sensing ion channels (ASICs) as pharmacological targets for neurodegenerative diseases. Curr Opin Pharmacol 8: 25-32.
31. Grunder S, Chen X, (2010) Structure, function, and pharmacology of acid-sensing ion channels (ASICs): focus on ASIC1a. Int J Physiol Pathophysiol Pharmacol 2: 73-94.
32. Askwith CC, Wemmie JA, Price MP, Rokhlina T, Welsh MJ, (2004) ASIC2 modulates ASIC1 H+-activated currents in hippocampal neurons. J Biol Chem 279: 18296-18305.
33. Sherwood TW, Lee KG, Gormley MG, Askwith CC, (2011) Heteromeric acid-sensing ion channels (ASICs) composed of ASIC2b and ASIC1a display novel channel properties and contribute to acidosis-induced neuronal death. J Neurosci 31: 9723-9734.
34. Weng JY, Lin YC, Lien CC, (2010) Cell type-specific expression of acid-sensing ion channels in hippocampal interneurons. J Neurosci 30: 6548-6558.
35. Wemmie JA, Chen J, Askwith CC, Hruska-Hageman AM, Price MP, et al. (2002) The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34: 463-477.
36. Jasti J, Furukawa H, Gonzales EB, Gouaux E, (2007) Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 449: 316-323.
37. Wemmie JA, Askwith CC, Lamani E, Cassell MD, Freeman JHJ, et al. (2003) Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci 23: 5496-5502.
38. Yermolaieva O, Leonard AS, Schnizler MK, Abboud FM, Welsh MJ, (2004) Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc Natl Acad Sci U S A 101: 6752-6757.
39. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, et al. (2004) Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118: 687-698.
40. Gu L, Liu X, Yang Y, Luo D, Zheng X, (2010) ASICs aggravate acidosis-induced injuries during ischemic reperfusion. Neurosci Lett 479: 63-68.
41. Friese MA, Craner MJ, Etzensperger R, Vergo S, Wemmie JA, et al. (2007) Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med 13: 1483-1489.
42. Joch M, Ase AR, Chen CX, MacDonald PA, Kontogiannea M, et al. (2007) Parkin-mediated monoubiquitination of the PDZ protein PICK1 regulates the activity of acid-sensing ion channels. Mol Biol Cell 18: 3105-3118.
43. Pidoplichko VI, Dani JA, (2006) Acid-sensitive ionic channels in midbrain dopamine neurons are sensitive to ammonium, which may contribute to hyperammonemia damage. Proc Natl Acad Sci U S A 103: 11376-11380.
44. Sun X, Cao YB, Hu LF, Yang YP, Li J, et al. (2011) ASICs mediate the modulatory effect by paeoniflorin on alpha-synuclein autophagic degradation. Brain Res 1396: 77-87.
45. Wong HK, Bauer PO, Kurosawa M, Goswami A, Washizu C, et al. (2008) Blocking acid-sensing ion channel 1 alleviates Huntington's disease pathology via an ubiquitin-proteasome system-dependent mechanism. Hum Mol Genet 17: 3223-3235.
46. Zhao X, Gorin FA, Berman RF, Lyeth BG, (2008) Differential hippocampal protection when blocking intracellular sodium and calcium entry during traumatic brain injury in rats. J Neurotrauma 25: 1195-1205.
47. Turner RJ, Van den Heuvel C, Vink R, (2004) Amiloride increases neuronal damage after traumatic brain injury in rats. J Am Coll Nutr 23: 534S-537S.
48. Carbonell WS, Maris DO, McCall T, Grady MS, (1998) Adaptation of the fluid percussion injury model to the mouse. J Neurotrauma 15: 217-229.
49. Xiong Y, Mahmood A, Chopp M, (2013) Animal models of traumatic brain injury. Nat Rev Neurosci 14: 128-142.
50. Vink R, McIntosh TK, Yamakami I, Faden AI, (1988) 31P NMR characterization of graded traumatic brain injury in rats. Magn Reson Med 6: 37-48.
51. Ziemann AE, Allen JE, Dahdaleh NS, Dbrebot II, Coryell M, et al. (2009) The amygdala is a chemosensor that detects hypercarbia and acidosis to elicit fear behavior. Cell 139: 1012-1021.
52. Hallam TM, Floyd CL, Folkerts MM, Lee LL, Gong QZ, et al. (2004) Comparison of behavioral deficits and acute neuronal degeneration in rat lateral fluid percussion and weight-drop brain injury models. J Neurotrauma 21: 521-539.
53. Sato M, Chang E, Igarashi T, Noble LJ, (2001) Neuronal injury and loss after traumatic brain injury: time course and regional variability. Brain Res 917: 45-54.
54. Sarkar S, Schmued L (2011) Fluoro-Jade dyes: fluorochromes for the histochemical localization of degenerative neurons. In: Bolon B, Butt MT, editors. Fundamental neuropathology for pathologists and toxicologists: principles and techniques. Hoboken: John Wiley & Sons. 171-179.
55. Schmued LC, Albertson C, Slikker W Jr, (1997) Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 751: 37-46.
56. Zhang B, Chen X, Lin Y, Tan T, Yang Z, et al. (2011) Impairment of synaptic plasticity in hippocampus is exacerbated by methylprednisolone in a rat model of traumatic brain injury. Brain Res 1382: 165-172.
57. Wu A, Molteni R, Ying Z, Gomez-Pinilla F, (2003) A saturated-fat diet aggravates the outcome of traumatic brain injury on hippocampal plasticity and cognitive function by reducing brain-derived neurotrophic factor. Neuroscience 119: 365-375.
58. Harrison FE, Reiserer RS, Tomarken AJ, McDonald MP, (2006) Spatial and nonspatial escape strategies in the Barnes maze. Learn Mem 13: 809-819.
59. Lee DJ, Gurkoff GG, Izadi A, Berman RF, Ekstrom AD, et al. (2013) Medial septal nucleus theta frequency deep brain stimulation improves spatial working memory after traumatic brain injury. J Neurotrauma 30: 131-139.
60. Mouzon B, Chaytow H, Crynen G, Bachmeier C, Stewart J, et al. (2012) Repetitive mild traumatic brain injury in a mouse model produces learning and memory deficits accompanied by histological changes. J Neurotrauma 29: 2761-2773.
61. Lehmann H, Rourke BK, Booker A, Glenn MJ (2012) Single session contextual fear conditioning remains dependent on the hippocampus despite an increase in the number of context-shock pairings during learning. Neurobiol Learn Mem.
62. Koseki H, Matsumoto M, Togashi H, Miura Y, Fukushima K, et al. (2009) Alteration of synaptic transmission in the hippocampal-mPFC pathway during extinction trials of context-dependent fear memory in juvenile rat stress models. Synapse 63: 805-813.
63. Curzon P, Rustay NR, Browman KE (2009) Cued and Contextual Fear Conditioning for Rodents. In: Buccafusco JJ, editor. Methods of Behavior Analysis in Neuroscience. 2nd ed. Boca Raton (FL).
64. Szydlowska K, Tymianski M, (2010) Calcium, ischemia and excitotoxicity. Cell Calcium 47: 122-129.
65. Benson CJ, Xie J, Wemmie JA, Price MP, Henss JM, et al. (2002) Heteromultimerics of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc Natl Acad Sci U S A 99: 2338-2343.
66. Yagi J, Wenk HN, Naves LA, McCleskey EW, (2006) Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ Res 99: 501-509.
67. Benson CJ, Sutherland SP, (2001) Toward an understanding of the molecules that sense myocardial ischemia. Ann N Y Acad Sci 940: 96-109.
68. Baron A, Waldmann R, Lazdunski M, (2002) ASIC-like, proton-activated currents in rat hippocampal neurons. J Physiol 539: 485-494.
69. Ziemann AE, Schnizler MK, Albert GW, Severson MA, Howard MA, (2008) Seizure termination by acidosis depends on ASIC1a. Nat Neurosci 11: 816-822.
70. Nedergaard M, Kraig RP, Tanabe J, Pulsinelli WA, (1991) Dynamics of interstitial and intracellular pH in evolving brain infarct. Am J Physiol 260: R581-588.
71. Kraig RP, Ferreira-Filho CR, Nicholson C, (1983) Alkaline and acid transients in cerebellar microenvironment. J Neurophysiol 49: 831-850.
72. Ishrat T, Sayeed I, Atif F, Hua F, Stein DG, (2012) Progesterone is neuroprotective against ischemic brain injury through its effects on the phosphoinositide 3-kinase/protein kinase B signaling pathway. Neuroscience 210: 442-450.
73. Xiao G, Wei J, Yan W, Wang W, Lu Z, (2008) Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: a randomized controlled trial. Crit Care 12: R61.
74. Bourdeaux CP, Brown JM, (2011) Randomized controlled trial comparing the effect of 8.4% sodium bicarbonate and 5% sodium chloride on raised intracranial pressure after traumatic brain injury. Neurocrit Care 15: 42-45.
75. Bourdeaux C, Brown J, (2010) Sodium bicarbonate lowers intracranial pressure after traumatic brain injury. Neurocrit Care 13: 24-28.
76. Muizelaar JP, Marmarou A, Ward JD, Kontos HA, Choi SC, et al. (1991) Adverse effects of prolonged hyperventilation in patients with severe head injury: a randomized clinical trial. J Neurosurg 75: 731-739.
77. Rosner MJ, Becker DP, (1984) Experimental brain injury: successful therapy with the weak base, tromethamine. With an overview of CNS acidosis. J Neurosurg 60: 961-971.
78. Wolf AL, Levi L, Marmarou A, Ward JD, Muizelaar PJ, et al. (1993) Effect of THAM upon outcome in severe head injury: a randomized prospective clinical trial. J Neurosurg 78: 54-59.
79. Yoshida K, Marmarou A, (1991) Effects of tromethamine and hyperventilation on brain injury in the cat. J Neurosurg 74: 87-96.
80. Marmarou A, (1992) Intracellular acidosis in human and experimental brain injury. J Neurotrauma 9Suppl 2: S551-562.