31P-MRS-Based Determination of Brain Intracellular and Interstitial pH: Its Application to In Vivo H+ Compartmentation and Cellular Regulation during Hypoxic/Ischemic Conditions
Purchase on Springer.com
$39.95 / €34.95 / £29.95*
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.
In the last decade, significant progress has been made in the characterization of pH regulation in nervous tissue in vitro. However, little work has been directed at understanding how pH regulatory mechanisms function in vivo. We are interested in how ischemic acidosis can effect pH regulation and modulate the extent of post-ischemic brain damage. We used 31P-MRS to determine normal in vivo pHi and pHe simultaneously in both the isolated canine brain and the intact rat brain. We observed that the 31Pi peak in the 31P-MRS spectrum is heterogeneous and can be deconvoluted into a number of discrete constituent peaks. In a series of experiments, we identified these peaks as arising from either extracellular or intracellular sources. In particular, we identified the peak representing the neurons and astrocytes and showed that they maintain different basal pH (6.95 and 7.05, respectively) and behave differently during hypoxic/ischemic episodes.
- Chesler, M. 1990. The regulation and modulation of pH in the nervous system. Prog. Neurobiol. 34:401-427.
- Deitmer, J. W. and Rose, C. R. 1996. pH regulation and proton signalling by glial cells. Prog. Neurobiol. 48:73-103.
- Roos, A. and Boron, W. F. 1981. Intracellular pH. Physiol. Rev. 61:296-434.
- Chesler, M. 1986. Regulation of intracellular pH in reticulospinal neurones of the lamprey, Petromyzon marinus. J. Physiol. (Lond) 381:241-261.
- Endres, W., Ballanyi, K., Serve, G., and Grafe, P. 1986. Excitatory amino acids and intracellular pH in motoneurons of the isolated frog spinal cord. Neurosci. Lett. 72:54-58.
- Heiple, J. M. and Taylor, D. L. 1981. An optical technique for measurement of intracellular pH in single living cells. Kroc. Found. Ser. 15:21-54.
- Shrode, L. D. and Putnam, R. W. 1994. Intracellular pH regulation in primary rat astrocytes and C6 glioma cells. Glia 12:196-210.
- Bevensee, M. O., Cummins, T. R., Haddad, G. G., Boron, W. F., and Boyarsky, G. 1996. pH regulation in single CA1 neurons acutely isolated from the hippocampi of immature and mature rats. J. Physiol. (Lond) 494:315-328.
- Volk, C., Albert, T., and Kempski, O. S. 1998. A proton-translocating H+-ATPase is involved in C6 glial pH regulation. Biochim. Biophys. Acta 1372:28-36.
- Hertz, L. and Peng, L. 1992. Energy metabolism at the cellular level of the CNS. Can. J. Physiol. Pharmacol. 70:S145-S157.
- Kusumoto, M., Dux, E., Paschen, W., and Hossmann, K. A. 1996. Susceptibility of hippocampal and cortical neurons to Argon-mediated in vitro ischemia. J. Neurochem. 67:1613-1621.
- Tombaugh, G. C. and Sapolsky, R. M. 1990. Mild acidosis protects hippocampal neurons from injury induced by oxygen and glucose deprivation. Brain Res. 506:343-345.
- Goldberg, M. P. and Choi, D. W. 1900. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J. Neurosci. 13:3510-3524.
- Espanol, M. T., Litt, L., Chang, L.-H., James, T. L., Weinstein, P. R., and Chan, P. H. 1996. Adult rat brain-slice preparation for nuclear magnetic resonance spectroscopy studies of hypoxia. Anesthesiology 84:201-210.
- Schurr, A. and Rigor, B. M. 1989. Cerebral ischemia revisited: New insights as revealed using in vitro brain slice preparations. Experientia 45:684-695.
- Cowan, A. I. and Martin, R. L. 1995. Simultaneous measurement of pH and membrane potential in rat dorsal vagal motoneurons during normoxia and hypoxia: a comparison in bicarbonate and HEPES buffers. J. Neurophysiol. 74:2713-2721.
- Lin, C. W., Kalaria, R. N., Kroon, S. N., Bae, J. Y., Sayre, L. M., and LaManna, J. C. 1996. The amiloride-sensitive Na+/H+exchange antiporter and control of intracellular pH in hippocampal brain slices. Brain Res. 731:108-113.
- Pirttila, T. R. and Kauppinen, R. A. 1994. Regulation of intracellular pH in guinea pig cerebral cortex ex vivo studied by 31P and 1H nuclear magnetic resonance spectroscopy: role of extracellular bicarbonate and chloride. J. Neurochem. 62:656-664.
- Gilboe, D. D., Kintner, D. B., Anderson, M. E., and Fitzpatrick, J. H., Jr. 1998. NMR-based identification of intra-and extracellular compartments of the brain Pi peak. J. Neurochem. 71:2542-2548.
- Voipio, J. and Kaila, K. 1993. Interstitial pCO2 and pH in rat hippocampal slices measured by means of a novel fast CO2/H(+)-sensitive microelectrode based on a PVC-gelled membrane. Pflugers Arch. 423:193-201.
- Jiang, C., Agulian, S., and Haddad, G. G. 1991. O2 tension in adult and neonatal brain slices under several experimental conditions. Brain Res. 568:159-164.
- Whittingham, T. S., Lust, W. D., Christakis, D. A., and Passonneau, J. V. 1984. Metabolic stability of hippocampal slice preparations during prolonged incubation. J. Neurochem. 43: 689-696.
- Roos, A. 1900. Intracellular pH and buffering power of rat brain. Am. J. Physiol. 221:176-181.
- Messeter, K. and Siesjö, B. K. 1971. The intracellular pH'in the brain in acute and sustained hypercapnia. Acta Physiol. Scand. 83:210-219.
- LaManna, J. C. and McCracken, K. A. 1984. The use of neutral red as an intracellular pH indicator in rat brain cortex in vivo. Anal. Biochem. 142:117-125.
- Ammann, D., Lanter, F., Steiner, R. A., Schulthess, P., Shijo, Y., and Simon, W. 1981. Neutral carrier based hydrogen ion selective microelectrode for extra-and intracellular studies. Anal. Chem. 53:2267-2269.
- Chesler, M. and Kraig, R. P. 1989. Intracellular pH transients of mammalian astrocytes. J. Neurosci. 9:2011-2019.
- Silver, I. A. and Erecinska, M. 1992. Ion homeostasis in rat brain in vivo: intra-and extracellular [Ca2+] and [H+] in the hippocampus during recovery from short-term, transient ischemia. J. Cereb. Blood Flow Metab. 12:759-772.
- Chance, B., Nakase, Y., Bond, M., Leigh, J. S., Jr., and McDonald, G. 1978. Detection of 31P nuclear magnetic resonance signals in brain by in vivo and freeze-trapped assays. Proc. Natl. Acad. Sci. U.S.A. 75:4925-4929.
- Ackerman, J. J., Grove, T. H., Wong, G. G., Gadian, D. G., and Radda, G. K. surface coils. Nature 283:167-170.
- Fukushima, E. and Stephen, B. W. 1981. Experimental pulse NMR: a nuts and bolts approach. Addison-Wesley Pub. Co., Reading, Mass.
- Callaghan, P. T. 1991. Principles of nuclear magnetic resonance microscopy. Oxford University Press, New York.
- Petroff, O. A., Prichard, J. W., Behar, K. L., Alger, J. R., den Hollander, J. A., and Shulman, R. G. 1985. Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology 35:781-788.
- Fitzpatrick, J. H., Jr., Kintner, D., Anderson, M., Westler, W. M., Emoto, S. E., and Gilboe, D. D. 1996. NMR studies of Pi-containing extracellular and cytoplasmic compartments in brain. J. Neurochem. 66:2612-2620.
- Griffith, J. K., Cordisco, B. R., Lin, C. W., and LaManna, J. C. 1992. Distribution of intracellular pH in the rat brain cortex after global ischemia as measured by color film histophotometry of neutral red. Brain Res. 573:1-7.
- Hope, P. L., Cady, E. B., Chu, A., Delpy, D. T., Gardiner, R. M., and Reynolds, E. O. 1987. Brain metabolism and intracellular pH during ischaemia and hypoxia: an in vivo 31P and 1H nuclear magnetic resonance study in the lamb. J. Neurochem. 49:75-82.
- Nioka, S., Smith, D., Chance, B., and Lockard, S. 1990. Metabolic heterogeneity in brain tissue during incomplete ischemia and reperfusion. NMR Biomed. 3:239-247.
- Kauppinen, R. A., Williams, S. R., Gadian, D. G., Brock, K. J., and Bachelard, H. S. 1989. Studies on substrate requirements for maintenance of energy state and intracellular pH in cortical brain slices using 31P NMR. Acta Physiol. Scand 136(Suppl. 582):73.
- Robbins, R. C., Balaban, R. S., and Swain, J. A. 1990. Intermittent hypothermic asanguineous cerebral perfusion (cerebroplegia) protects the brain during prolonged circulatory arrest. A phosphorus 31 nuclear magnetic resonance study. J. Thorac. Cardiovasc. Surg. 99:878-884.
- Portman, M. A. and Ning, X. H. 1990. Developmental adaptations in cytosolic phosphate content and pH regulation in the sheep heart in vivo. J. Clin. Invest. 86:1823-1828.
- Sunagawa, S., Buist, R. J., Hruska, F. E., Sutherland, G. R., and Peeling, J. 1994. Hydrogen ion compartmentation during and following cerebral ischemia evaluated by 31P NMR spectroscopy. Brain Res. 641:328-332.
- Macri, M. A., Campanella, R., De Luca, F., Montalbano, A., Taggi, F., and Maraviglia, B. 1995. In vivo 31P spectroscopy study of treated and untreated recovery of rat partial brain ischemia. Magn. Reson. Med. 34:542-547.
- Kintner, D. B., Anderson, M. E., Sailor, K. A., Dienel, G., Fitzpatrick, J. H., Jr., and Gilboe, D. D. 1999. In vivo microdialysis of 2-deoxyglucose 6-phosphate into brain: A novel method for the measurement of interstitial pH using 31P-NMR. J. Neurochem. 72:405-412.
- Kraig, R. P. and Chesler, M. 1990. Astrocytic acidosis in hyperglycemic and complete ischemia. J. Cereb. Blood Flow Metab. 10:104-114.
- Sokoloff, L., Reivich, M., Kennedy, C., Des Rosiers, M. H., Patlak, C. S., Pettigrew, K. D., Sakurada, O., and Shinohara, M. 1977. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28:897-916.
- BeltrandelRio, H. and Wilson, J. E. 1991. Hexokinase of rat brain mitochondria: relative importance of adenylate kinase and oxidative phosphorylation as sources of substrate ATP, and interaction with intramitochondrial compartments of ATP and ADP. Arch. Biochem. Biophys. 286:183-194.
- Pulsinelli, W. A. and Cooper, A. J. 1989. Metabolic encephalopaties and coma, Pages 765-781, in Siegel, G., Agranoff, B., Ablers, R. W., and Molinoff, P. (eds.), Basic Neurochemistry. Raven Press, New York.
- Berl, S. 1971. Cerebral amino acid metabolism in hepatic coma. Exp. Biol. Med. 4:71-84.
- Gilboe, D. D., Kintner, D. B., Sailor, K. A., Anderson, M. E., and Fitzpatrick, J. H., Jr. 1998. Brain intracellular and interstitial pH changes during graded hypoxia, Pages 53-60, in Krieglstein, J. (ed.), Pharmacology of Cerebral Ischemia-1998. Wissenschaftliche Verlagsgesellschaft mbH Stuttgart
- Gottfried, J. A. and Chesler, M. 1996. Temporal resolution of activity-dependent pH shifts in rat hippocampal slices. J. Neurophysiol. 76:2804-2807.
- Grieb, P. 1990. Effect of acetazolamide on brain intracellular pH. J. Cereb. Blood Flow Metab. 10:588-589.
- Li, P. A. and Siesjö, B. K. 1997. Role of hyperglycaemia-related acidosis in ischaemic brain damage. Acta Physiol. Scand. 161: 567-580.
- Choi, D. W. and Koh, J. Y. 1998. Zinc and brain injury. [Review]. Annu. Rev. Neurosci. 21:347-375.
- Tombaugh, G. C. 1994. Mild acidosis delays hypoxic spreading depression and improves neuronal recovery in hippocampal slices. J. Neurosci. 14:5635-5643.
- 31P-MRS-Based Determination of Brain Intracellular and Interstitial pH: Its Application to In Vivo H+ Compartmentation and Cellular Regulation during Hypoxic/Ischemic Conditions
Volume 25, Issue 9-10 , pp 1385-1396
- Cover Date
- Print ISSN
- Online ISSN
- Kluwer Academic Publishers-Plenum Publishers
- Additional Links
- Intracellular pH
- extracellular pH
- pH regulation
- Industry Sectors