Modelling of pH dynamics in brain cells after stroke

Interface Focus

Volumn 1, Issue 3, 2011, Pages 408-416

  Orlowski, Piotr ^a   Chappell, Michael ^a   Park, Chang Sub ^a   Grau, Vicente ^a   Payne, Stephen ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Biochemical marker of stroke; Cellular metabolism; pH regulation; Predictive medicine; Stroke

Indexed keywords

EID: 84855679242     PISSN: 20428898     EISSN: 20428901     Source Type: Journal    
DOI: 10.1098/rsfs.2010.0025     Document Type: Article

References (62)

1. Feigin, V. L., Lawes, C. M. M., Benett, D. A., Baker-Collo, S. L. B. & Parag, V. 2009 Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review. Lancet Neurol. 8, 355-369. (doi:10. 1016/S1474-4422(09)70025-0)
2. Lloyd-Jones, D. et al. On behalf of the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. 2010 Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 121, e46-e215. (doi:10.1161/CIRCULATIO NAHA.109.192667)
3. Hossmann, K.-A. 1994 Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 36, 557-565. (doi:10.1002/ana.410360404)
4. Furlan, A. J., Katzan, I. L. & Caplan, L. R. 2003 Thrombolytic therapy in acute ischemic stroke. Curr. Treat. Options Cardiovasc. Med. 5, 171-180. (doi:10.1007/s11936-003-0001-4)
5. Smith, W. S. et al. 2005 Safety and efficacy of mechanical embolectomy in acute ischemic stroke. Stroke 36, 1432-1438. (doi:10.1161/01.STR.0000171066.25248.1d)
6. Haley Jr, E. C. et al. 1993 Pilot randomized trial of tissue plasminogen activator in acute ischemic stroke. Stroke 24, 1000-1004.
7. Nesbit, G. M., Luh, G., Tien, R. & Barnwell, S. L. 2004 New and future endovascular treatment strategies for acute ischemic stroke. J. Vasc. Interv. Radiol. 15, 103-110. (doi:10.1097/01.RVI.0000112578.95689.66)
8. The ATLANTIS, ECASS, and NINDS rt-PA Study Group Investigators. 2004 Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet 363, 768-774. (doi:10.1016/S0140-6736(04)15692-4)
9. Neumann-Haefelin, T., Wittsack, H.-J., Wenserski, F., Siebler, M., Rüdiger, J., Mödder, U. & Freund, H.-J. 1999 Diffusion-and perfusion-weighted MRI. The DWI/PWI mismatch region in acute stroke. Stroke 30, 1591-1597.
10. Sobesky, J., Weber, O. Z., Lehnhardt, F.-G., Hesselmann, V., Neveling, M., Jacobs, A. & Heiss, W.-D. 2005 Does the mismatch match the penumbra? Magnetic resonance imaging and positron emission tomography in early ischemic stroke. Stroke 36, 980-985. (doi:10.1161/01.STR.0000160751. 79241.a3)
11. Kidwell, C. S., Alger, J. R. & Saver, J. L. 2003 Beyond mismatch: evolving paradigms in imaging the ischemic penumbra with multimodal magnetic resonance imaging. Stroke 34, 2729-2735. (doi:10.1161/01.STR.0000097608. 38779.CC)
12. Sylaja, P. N. & Demchuk, A. M. 2008 Intravenous thrombolytic therapy in acute ischemic stroke: the art and science of treatment decision making. Ann. Indian Acad. Neurol. 11, 24-29.
13. Kaila, K. & Ransom, B. R. 1998 pH and brain function. New York, NY: Wiley & Sons.
14. Zhou, J., Payen, J. F., Wilson, D. A., Traystman, R. J. & van Zijl, P. C. 2003 Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat. Med. 9, 1085-1090. (doi:10.1038/nm907)
15. Sun, P. Z., Benner, T., Copen, W. A. & Sorensen, A. G. 2010 Early experience of translating pH-weighted MRI to image human subjects at 3 Tesla. Stroke 41, 147-151. (doi:10.1161/STROKEAHA.110.595777)
16. Casey, J. R., Grinstein, S. & Orlowski, J. 2010 Sensors and regulators of intracellular pH. Nat. Rev. Mol. Biol. 11, 50-61. (doi:10.1038/nrm2820)
17. Ekholm, A., Kenichiro, K. & Siesjö, B. K. 1991 Tissue lactate content and tissue PCO2: implications for compartmentation of H{thorn}. Neurol. Res. 13, 74-76.
18. Busa, W. B. & Nuccielli, R. 1984 Metabolic regulation via intracellular pH. Am. J. Physiol. 246, R409-R438.
19. Traystman, R., Kirsh, J. & Koehler, R. 1991 Oxygen radical mechanisms of brain injury following ischemia and reperfusion. J. Appl. Physiol. 71, 1185-1195.
20. Folbergová, J., Zhao, Q., Katsura, K. & Siesjö, B. K. 1995 N-tert-butyl-a-phenylnitrone improves recovery of brain energy state in rats following transient focal ischemia. Proc. Natl Acad. Sci. USA 92, 5057-5061. (doi:10.1073/pnas.92.11.5057)
21. Gebicki, J. M. & Bielski, B. H. J. 1981 Comparison of the capacities of the perhydroxyl and the superoxide radicals to initiate chain oxidation of linoleic acid. J. Am. Chem. Soc. 103, 7020-7022. (doi:10.1021/ja00413a066)
22. Siesjö, B. K., Bendek, G., Koide, T., Westerberg, E. & Wieloch, T. 1985 Influence of acidosis on lipid peroxidation in brain tissues in vitro. J. Cereb. Blood Flow Metab. 5, 253-258.
23. Bralet, J., Schreiber, L. & Bouvier, C. 1992 Effect of acidosis and anoxia on iron delocalization from brain homogenates. Biochem. Pharmacol. 43, 979-983. (doi:10.1016/0006-2952(92)90602-F)
24. Kristián, T. & Siesjö, B. 1997 Changes in ionic fluxes during cerebral ischemia. In Neuroprotective agents and cerebral ischemia (eds A. Cross & A. Green), pp. 27-45. New York, NY: Academic Press.
25. Barry, M. A. & Eastman, A. 1992 Endonuclease activation during apoptosis: the role of cytosolic Ca2{thorn} and pH. Biochem. Biophys. Res. Commun. 186, 782-789. (doi:10. 1016/0006-291X(92)90814-2)
26. Barry, M. A. & Eastman, A. 1993 Identification of deoxyribonuclease II as an endonuclease involved in apoptosis. Arch. Biochem. Biophys. 300, 440-450. (doi:10.1006/abbi.1993.1060)
27. Plum, F. 1983 What causes infarction in ischemic brain? The Robert Wartenburg lecture. Neurology 33, 222-233.
28. del Zoppo, G. J. 1994 Microvascular changes during cerebral ischemia and reperfusion. Cerebrovasc. Brain Metab. Rev. 6, 47-96.
29. Bruno, A., Biller, J., Adams Jr, H. P., Clarke, W. R., Woolson, R. F., Williams, L. S. & Hansen, M. D. 1999 Acute blood glucose level and outcome from ischemic stroke. Neurology 52, 280-284.
30. Cloutier, M., Bolger, F. B., Lowry, J. P. & Wellstaed, P. 2009 An integrative dynamic model of brain energy metabolism using in vivo neurochemical measurements. J. Comput. Neurosci. 27, 391-414. (doi:10.1007/s10827-009-0152-8)
31. DiNuzzo, M., Mangia, S., Maraviglia, B. & Giove, F. 2010 Glycogenolysis is astrocytes supports blood-borne glucose channelling not glycogen-derived lactate shuttling to neurons: evidence from mathematical modelling. J. Cereb. Blood Flow Metab. 30, 1895-1904. (doi:10.1038/jcbfm.2010.151)
32. Kashiwaya, Y., Sato, K., Tsuchiya, N., Thomas, S., Fell, D. A., Veech, R. L. & Passonneau, J. V. 1994 Control of glucose utilization in working perfused rat heart. J. Biol. Chem. 269, 25 502-25 514.
33. Sanyal, G. & Maren, T. H. 1981 Thermodynamics of carbonic anhydrase catalysis. A comparison between human isoenzymes B and C. J. Biol. Chem. 256, 608-612.
34. Maren, T. H. 1988 The kinetics of HCO32 synthesis related to fluid secretion, pH control, and CO2 elimination. Annu. Rev. Physiol. 50, 695-717. (doi:10.1146/annurev.ph.50. 030188.003403)
35. Khalifar, R. G. 1971 The carbon dioxide hydration activity of carbonic anhydrase. J. Biol. Chem. 246, 2561-2573.
36. Schultz, K. G., Riebesell, U., Rost, B., Thoms, S. & Zeebe, R. E. 2006 Determination of the rate constants for the carbon dioxide to bicarbonate inter-conversion in pHbuffered seawater systems. Mar. Chem. 100, 53-65. (doi:10.1016/j.marchem.2005.11.001)
37. Roy, R. N., Roy, L. N., Lawson, M., Vogel, K. M., Porter-Moore, C., Pearson, T., Good, C. E., Millero, F. J. & Cambel, D. J. 1993 Determination of the ionization constants of carbonic acid in seawater in salinities 5 to 45 and temperatures 0 to 458C. Mar. Chem. 44, 249-267. (doi:10.1016/0304-4203(93)90207-5)
38. Helbig, H., Korbmacher, C., Berweck, S., Kuhmer, D. & Wiederholt, M. 1988 Kinetic properties of Na{thorn}/H{thorn} exchange in cultured bovine pigmented ciliary epithelial cells. Eur. J. Phys. 412, 80-85.
39. Fuster, D., Moe, O. W. & Hilgemann, D. W. 2009 Steadystate function of the ubiquitous mammalian Na/H exchanger (NHE1) in reaction to dimer coupling models with 2NA/2H stoichiometry. J. Gen. Physiol. 132, 465-480. (doi:10.1085/jgp.200810016)
40. Endresen, L. P., Hall, K., Høye, J. S. & Myrheim, J. 2000 A theory for the membrane potential of living cells. Eur. Biophys. J. 29, 90-103. (doi:10.1007/s002490050254)
41. Ljunggren, B., Ratcheson, R. A. & Siesjö, B. K. 1974 Cerebral metabolic state following complete compression ischemia. Brain Res. 73, 291-307. (doi:10.1016/0006-8993(74)91050-6)
42. Silver, I. A. & Erecinska, M. 1994 Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neuronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycaemic animals. J. Neurosci. 14, 5068-5076.
43. Chow, S. Y., Yen Chow, Y. C., White, H. S. & Woodbury, D. M. 1991 pH regulation after acid load in primary cultures of mouse astrocytes. Brain Res. Dev. Brain Res. 60, 69-78. (doi:10.1016/0165-3806(91)90156-D)
44. + uptake. Can. J. Phyisol. Pharmacol. 70, S314-S322.
45. Nicholson, C. 1993 Ion-selective microelectrodes and diffusion measurements as tools to explore the brain cell microenvironment. J. Neurosci. Methods 48, 199-213. (doi:10.1016/0165-0270(93)90092-6)
46. Hunter, P. et al. 2010 A vision and stratedy for the VPH in 2010 and beyond. Phil. Trans. R. Soc. A 368, 2595-2614. (doi:10.1098/rsta.2010.0048)
47. Beard, D. A. et al. 2009 CellML metadata: standards, associated tools and repositories. Phil. Trans. R. Soc. A. 367, 1845-1867. (doi:10.1098/rsta.2008.0310)
48. Christie, G. R., Nielsen, P. M. F., Blackett, S. A., Bradley, C. P. & Hunter, P. J. 2009 FieldML: concepts and implementation. Phil. Trans. R. Soc. A. 367, 1869-1884. (doi:10. 1098/rsta.2009.0025)
49. Lapin, A., Klann, M. & Reuss, M. 2010 Multi-scale spatiotemporal modeling: lifelines of microorganisms in bioreactors and tracking molecules in cells. Adv. Biochem. Eng. Biotechnol. 121, 23-43. (doi:10.1007/10_2009_53)
50. Chow, S. Y., Yen Chow, Y. C. & Woodbury, D. M. 1992 Studies of pH regulatory mechanisms in cultured astrocytes of DBA and C57 mice. Epilepsia 33, 775-784. (doi:10.1111/j.1528-1157.1992.tb02181.x)
51. Burton, R. F. 1978 Intracellular buffering. Resp. Physiol. 33, 51-58. (doi:10.1016/0034-5687(78)90083-X)
52. Lagadic-Gossmann, D., Buckler, K. J. & Vaughan-Jones, R. D. 1992 Role of bicarbonate in pH recovery from intracellular acidosis in the guinea-pig ventricular myocyte. J. Physiol. 458, 361-384.
53. Law, R. O. 1994 Regulation of mammalian brain cell volume. J. Exp. Zool. 268, 90-96. (doi:10.1002/jez.1402680204)
54. van der Worp, H. B., Sena, E. S., Donnan, G. A., Howells, D. W. & Macleod, M. R. 2007 Hypothermia in animal models of acute ischaemic stroke: a systematic review and metaanalysis. Brain 130, 3063-3074. (doi:10.1093/brain/awm083)
55. Boutilier, R. G. 2001 Mechanisms of cell survival in hypoxia and hypothermia. J. Exp. Biol. 204, 3171-3181.
56. Wang, Y. & Zhu, L. 2007 Targeted brain hypothermia induced by an interstitial cooling device in human neck: theoretical analyses. Eur. J. Appl. Physiol. 101, 31-40. (doi:10.1007/s00421-007-0451-6)
57. Shrivastava, D. & Roemer, R. B. Readdressing the issue of thermally significant blood vessels using a countercurrent vessel network. Trans. ASME 128, 210-216.
58. van der Worp, H. B., Macelod, M. R. & Kollmar, R. 2010 Therapeutic hypothermia for acute ischemic stroke: ready to start large randomized trials? J. Cereb. Blood Flow Metab. 30, 1079-1093. (doi:10.1038/jcbfm.2010.44)
59. del Zoppo, G. J., Schmid-Schonbein, G. W., Mori, E., Copeland, B. R. & Chang, C. M. 1991 Polymophonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and perfusion in baboons. Stroke 22, 1276-1283.
60. Siesjö, B. K., Katsura, K. & Kristián, T. 1996 Acidosisrelated damage. Adv. Neurol. 71, 209-236.
61. Siesjö, B. K., Bendek, G., Koide, T., Westerberg, E. & Wieloch, T. 1985 Influence of oxidation in brain tissues in vitro. J. Cereb. Blood Flow Metab. 5, 253-258.
62. Wang, Q., Tang, X. N. & Yenari, M. A. 2007 The inflamatory response in stroke. J. Neuroimmunol. 184, 53-68. (doi:10.1016/j.jneuroim.2006.11.014)