Metabolic multianalyte microphysiometry reveals extracellular acidosis is an essential mediator of neuronal preconditioning

ACS Chemical Neuroscience

Volumn 3, Issue 7, 2012, Pages 510-518

  McKenzie, Jennifer R ^a   Palubinsky, Amy M ^a   Brown, Jacquelynn E ^a   McLaughlin, Bethann ^b,c   Cliffel, David E ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

acidosis; electrochemical; Glycemic stress; metabolism; multianalyte microphysiometry; real time; stroke

Indexed keywords

GLUCOSE; LACTIC ACID;

ACIDIFICATION; ACIDOSIS; ANIMAL CELL; ARTICLE; CELL FATE; CELL METABOLISM; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; ELECTROCHEMICAL DETECTION; EMBRYO; EXTRACELLULAR ACIDOSIS; EXTRACELLULAR SPACE; GLIA CELL; MIXED CELL CULTURE; MULTIANALYTE MICROPHYSIOMETRY; NERVE CELL; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; OXYGEN CONSUMPTION; PREDICTIVE VALUE; PRIORITY JOURNAL; RAT;

ACIDOSIS; ANIMALS; CELL CULTURE TECHNIQUES; CELL SURVIVAL; COCULTURE TECHNIQUES; EXTRACELLULAR SPACE; METABOLIC NETWORKS AND PATHWAYS; NEUROGLIA; NEURONS; OXYGEN CONSUMPTION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84863898743     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn300003r     Document Type: Article

References (38)

1. Kety, S. S. (1957) The general metabolism of the brain in vivo. In Metabolism of the Nervous System (Richter, D.), pp 221-237, Pergamon Press, London.
2. Kety, S. S. and Schmidt, C. F. (1948) The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values J. Clin. Invest. 27, 476-483
3. Peters, A. and Langemann, D. (2009) Build-ups in the supply chain of the brain: on the neuroenergetic cause of obesity and type 2 diabetes mellitus Front. Neuroenerg. 2, 12
4. Gidday, J. M. (2006) Cerebral preconditioning and ischaemic tolerance Nat. Rev. Neurosci. 7, 437-448 (Pubitemid 44012284)
5. Zeiger, S. L. H., McKenzie, J. R., Stankowski, J. N., Martin, J. A., Cliffel, D. E., and McLaughlin, B. (2010) Neuron specific metabolic adaptations following multi-day exposures to oxygen glucose deprivation Biochim. Biophys. Acta, Mol. Basis Dis. 1802, 1095-1104
6. McLaughlin, B., Hartnett, K. A., Erhardt, J. A., Legos, J. J., White, R. F., Barone, F. C., and Aizenman, E. (2003) Caspase 3 activation is essential for neuroprotection in preconditioning Proc. Natl. Acad. Sci. U.S.A. 100, 715-720 (Pubitemid 36126118)
7. ODuffy, A. E., Bordelon, Y. M., and McLaughlin, B. (2006) Killer proteases and little strokes-how the things that do not kill you make you stronger J. Cereb. Blood Flow Metab. 27, 655-668 (Pubitemid 46474612)
8. Schurr, A. (2006) Lactate: the ultimate cerebral oxidative energy substrate? J. Cereb. Blood Flow Metab. 26, 142-152 (Pubitemid 41818078)
9. Aguilera, P., Vazquez-Contreras, E., Gomez-Martinez, C. D., and Cardenas, M. E. C. (2009) Hypoxia inducible factor-1 as a therapeutic target in cerebral ischemia Curr. Signal Transduction Ther. 4, 162-173
10. Xiong, Z. G., Chu, X. P., and Simon, R. P. (2006) Ca2+-Permeable Acid-sensing Ion Channels and Ischemic Brain Injury J. Membr. Biol. 209, 59
11. Barone, F. C. (2004) Endogenous Brain Protection Stroke Genomics: Methods and Reviews 105-184
12. Vazquez, A. L., Masamoto, K., Fukuda, M., and Kim, S.-G. (2010) Cerebral oxygen delivery and consumption during evoked neural activity Front. Neuroenerg. 2, 11
13. Eklund, S., Thompson, R., Snider, R., Carney, C., Wright, D., Wikswo, J., and Cliffel, D. (2009) Metabolic Discrimination of Select List Agents by Monitoring Cellular Responses in a Multianalyte Microphysiometer Sensors 9, 2117-2133
14. Snider, R. M., McKenzie, J. R., Kraft, L., Kozlov, E., Wikswo, J. P., and Cliffel, D. E. (2010) The Effects of Cholera Toxin on Cellular Energy Metabolism Toxins 2, 632-648
15. Eklund, S. E., Snider, R. M., Wikswo, J., Baudenbacher, F., Prokop, A., and Cliffel, D. E. (2006) Multianalyte microphysiometry as a tool in metabolomics and systems biology J. Electroanal. Chem. 587, 333
16. Snider, R. M., Ciobanu, M., Rue, A. E., and Cliffel, D. E. (2008) A multiwalled carbon nanotube/dihydropyran composite film electrode for insulin detection in a microphysiometer chamber Anal. Chim. Acta 609, 44-52
17. Sickmann, H. M., Waagepetersen, H. S., Schousboe, A., Benie, A. J., and Bouman, S. D. (2012) Brain glycogen and its role in supporting glutamate and GABA homeostasis in a type 2 diabetes rat model Neurochem. Int. 60, 267-275
18. Zeiger, S. L. H., Musiek, E. S., Zanoni, G., Vidari, G., Morrow, J. D., Milne, G. J., and McLaughlin, B. (2009) Neurotoxic lipid peroxidation species formed by ischemic stroke increase injury Free Radical Biol. Med. 47, 1422-1431
19. Brown, J. E., Zeiger, S. L. H., Hettinger, J. C., Brooks, J. D., Holt, B., Morrow, J. D., Musiek, E. S., Milne, G., and McLaughlin, B. (2010) Essential role of the redox-sensitive kinase p66shc in determining energetic and oxidative status and cell fate in neuronal preconditioning J. Neurosci. 30, 5242-5252
20. Busse, O. and Hoffmann, O. (1983) CSF lactate and CT findings in middle cerebral artery infarction. A comparative study Stroke 14, 960-963 (Pubitemid 14205249)
21. Jung, J. Y., Lee, H. S., Kang, D. G., Kim, N. S., Cha, M. H., Bang, O. S., Ryu, D. H., and Hwang, G. S. (2011) (1)H-NMR-Based Metabolomics Study of Cerebral Infarction Stroke 42, 1282-1288
22. Simon, R. and Xiong, Z. (2006) Acidotoxicity in brain ischemia Biochem. Soc. Trans. 34, 1356-1361
23. Xiong, Z.-G., Chu, X.-P., and Simon, R. P. (2007) Acid sensing ion channels-novel therapeutic targets for ischemic brain injury Front. Biosci. 12, 1376-1386 (Pubitemid 46846840)
24. Chen, Y., Stevens, B., Chang, J., Milbrandt, J., Barres, B. A., and Hell, J. W. (2008) NS21: Re-defined and modified supplement B27 for neuronal cultures J. Neurosci. Methods 171, 239
25. Roberts, L. J., 2nd, Montine, T. J., Markesbery, W. R., Tapper, A. R., Hardy, P., Chemtob, S., Dettbarn, W. D., and Morrow, J. D. (1998) Formation of isoprostane-like compounds (neuroprostanes) in vivo from docosahexaenoic acid J. Biol. Chem. 273, 13605-13612 (Pubitemid 28268404)
26. Reich, E. E., Zackert, W. E., Brame, C. J., Chen, Y., Roberts, L. J., 2nd, Hachey, D. L., Montine, T. J., and Morrow, J. D. (2000) Formation of novel D-ring and E-ring isoprostane-like compounds (D4/E4- neuroprostanes) in vivo from docosahexaenoic acid Biochemistry 39, 2376-2383 (Pubitemid 30130089)
27. Montine, T. J., Quinn, J. F., Milatovic, D., Silbert, L. C., Dang, T., Sanchez, S., Terry, E., Roberts, L. J., 2nd, Kaye, J. A., and Morrow, J. D. (2002) Peripheral F2-isoprostanes and F4-neuroprostanes are not increased in Alzheimers disease Ann. Neurol. 52, 175-179 (Pubitemid 34810597)
28. Roberts, L. J., Fessel, J. P., and Davies, S. S. (2005) The Biochemistry of the Isoprostane, Neuroprostane, and Isofuran Pathways of Lipid Peroxidation Brain Pathol. 15, 143-148 (Pubitemid 40546170)
29. Petroni, A., Salami, M., Blasevich, M., Papini, N., and Galli, C. (1994) Inhibition by n-3 fatty acids of arachidonic acid metabolism in a primary culture of astroglial cells Neurochem. Res. 19, 1187-1193 (Pubitemid 24284795)
30. Milne, G. L., Sanchez, S. C., Musiek, E. S., and Morrow, J. D. (2007) Quantification of F2-isoprostanes as a biomarker of oxidative stress.(Report) Nat. Protoc. 2, 221(6)
31. McLaughlin, B., Pal, S., Tran, M. P., Parsons, A. A., Barone, F. C., Erhardt, J. A., and Aizenman, E. (2001) p38 Activation Is Required Upstream of Potassium Current Enhancement and Caspase Cleavage in Thiol Oxidant-Induced Neuronal Apoptosis J. Neurosci. 21, 3303-3311 (Pubitemid 32422795)
32. Eklund, S. E., Taylor, D., Kozlov, E., Prokop, A., and Cliffel, D. E. (2004) A Microphysiometer for Simultaneous Measurement of Changes in Extracellular Glucose, Lactate, Oxygen, and Acidification Rate Anal. Chem. 76, 519-527 (Pubitemid 38166553)
33. Eklund, S. E., Cliffel, D. E., Kozlov, E., Prokop, A., Wikswo, J., and Baudenbacher, F. (2003) Modification of the Cytosensor(TM) microphysiometer to simultaneously measure extracellular acidification and oxygen consumption rates Anal. Chim. Acta 496, 93-101 (Pubitemid 37352704)
34. Jin, L., Jin, P., Ye, J., and Fang, Y. (1992) Determination of dissolved oxygen by catalytic reduction on Nafion-methyl viologen chemically modified electrode Talanta 39, 145-7
35. Ohara, T. J., Rajagopalan, R., and Heller, A. (1994) "Wired" Enzyme Electrodes for Amperometric Determination of Glucose or Lactate in the Presence of Interfering Substances Anal. Chem. 66, 2451-2457 (Pubitemid 124005702)
36. Oldenziel, W. H., Dijkstra, G., Cremers, T. I. F. H., and Westerink, B. H. C. (2006) Evaluation of Hydrogel-Coated Glutamate Microsensors Anal. Chem. 78, 3366-3378
37. Casciari, J. J., Sotirchos, S. V., and Sutherland, R. M. (1992) Variations in tumor cell growth rates and metabolism with oxygen concentration, glucose concentration, and extracellular pH J. Cell. Physiol. 151, 386-394
38. Owicki, J. C., Bousse, L. J., Hafeman, D. G., Kirk, G. L., Olson, J. D., Wada, H. G., and Parce, J. W. (1994) The light-addressable potentiometric sensor: principles and biological applications Annu. Rev. Biophys. Biomol. Struct. 23, 87-113 (Pubitemid 24217363)