Abstract
Nuclear magnetic resonance (NMR) is a non-invasive technique which allows us to examine the biochemical, physiological and metabolic events occurring inside living tissue; such as vascular and other smooth muscles.
It has been found that the smooth muscle metabolism is compartmented such that mitochondrial function fuels contraction and that much glycolytic ATP production is used for membrane pumps. Using NMR we have been able to observe the ATP and phosphocreatine (PCr) concentrations and estimate the ADP concentration, as well as flux through the creatine kinase (CK) system. It has also been found that the smooth muscle metabolism is able to maintain ATP concentration in the absence of mitochondrial function (cyanide inhibition). Therefore, the vessels are able to adapt to metabolic demands as necessary.
NMR is versatile in the information it can provide because it has also yielded important contributions with regard to the intracellular pH and ionic status. For example, the intracellular free Mg2+ ([Mg2+],) can be measured with NMR simultaneously with ATP concentrations and NMR has shown us that the [Mg2+], is highly protected in the muscle (within confined range), but also responds to the environment around it.
In this review we conclude that NMR measurements of smooth muscle research is a useful technique for assessing chronic and acute changes that occur in the tissue and during diseases. (Mol Cell Biochem 244: 17-30, 2003)
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Paul RJ: Functional compartmentalization of oxidative and glycolytic metabolism in vascular smooth muscle. Am J Physiol 244: C399–C409, 1983
Lynch RM, Paul RJ: Compartmentation of glycolytic and glycogenolytic metabolism in vascular smooth muscle. Science 222: 1344–1346, 1983
Lynch RM, Paul RJ: Compartmentation of carbohydrate metabolism in vascular smooth muscle. Am J Physiol 252: C328–C334, 1987
Ishida Y, Paul RJ: Evidence for compartmentation of high energy phosphagens in smooth muscle. Prog Clin Biol Res 315: 417–428, 1989
Clark JF, Khuchua Z, Kuznetsov AV, Saks VA, Ventura-Clapier R: Compartmentation of creatine kinase isoenzymes in myometrium of gravid guinea-pig. J Physiol 466: 553–573, 1993
Boehm EA, Clark JF, Radda GK: Metabolite utilization and possible compartmentation in porcine carotid artery: A study using 13guanidinopropionic acid. Am J Physiol 268: C628–C635, 1995
Nakayama S, Hachisuka T, Itoh K, Matsumoto T, Tomita T: Phosphomonoesters in the guinea-pig taenia caeci: pH-Dependency of the phosphomonoester peaks in 31P-NMR. Jpn J Physiol 45: 411–422, 1995
Fisher MJ, Dillon PF: Direct determination of ADP in hypoxic porcine carotid artery using 31 P NMR. NMR Biomed 1: 121–126, 1988
Kushmerick MJ, Dillon PF, Meyer RA, Brown TR, Krisanda JM, Sweeney HL: 31P NMR spectroscopy, chemical analysis, and free Mg’ of rabbit bladder and uterine smooth muscle. J Biol Chem 261: 14420–14429, 1986
Nakayama S, Chihara S, Clark JF, Huang S-M, Horiuchi T, Tomita T: Consequences of metabolic inhibition in smooth muscle isolated from guinea-pig stomach. J Physiol 505: 229–240, 1997
Clark JF, Harris GI, Dillon PF: Multisite saturation transfer using DANTE and continuous wave. Magn Reson Med 17: 274–278, 1991
Pyne GJ, Cadoux-Hudson TAD, Clark JF: Force function relations in vascular smooth muscle during cerebral vasospasm. Biophys J 72: A256, 1998
Yoshizaki K, Radda GK, Inubushi T, Chance B: ‘H and 31P-NMR studies on smooth muscle of bullfrog stomach. Biochem Biophys Acta 928: 36–44, 1987
Degani H, Victor TA, Kaye AM: Effects of 1713-estradiol on high energy phosphate concentrations and the flux catalyzed by creatine kinase in immature rat uteri: 37P NMR studies. Endocrinology 122: 1631–1637, 1988
Degani H, Shaer A, Victor TA, Kaye AM: Estrogen-induced changes in high-energy phosphate metabolism in rat uterus. Biochemistry 23: 2572–2577,1984
Clark JF, Dillon PF: Porcine carotid artery creatine kinase kinetics using NMR saturation transfer. Biophys J 57: 156a, 1990
Verume NA, Nicolay K: Energetics of smooth muscle taenia caecum of guinea-pig: A 31P NMR study. FEBS Lett 156: 293–297, 1983
Butler TM, Siegman MJ: High-energy phosphate metabolism in vascular smooth muscle. Annu Rev Physiol 47: 629–643, 1985
Vogel HJ, Lilja H, Hellstrand P: Phosphorus-37NMR studies of smooth muscle from guinea pig taenia coli. Biosci Rep 3: 863–870, 1983
Dawson MJ, Wray S: The effects of pregnancy and parturition on phosphorus metabolites in rat uterus studied by 31P NMR. J Physiol 368: 19–31, 1985
Iyengar MR: Creatine kinase as an intracellular regulator. J Muscle Res Cell Motil 5: 527–534, 1984
Wray S: The effects of metabolic inhibition on uterine metabolism and intracellular pH in the rat. J Physiol 423: 411–423, 1990
Wray S, Duggins K, Iles R, Nyman L, Osman VA: The effects of metabolic inhibition and intracellular pH on rat uterine force production. Exp Physiol 77: 307–319, 1992
Boehm EA, Clark JF, Radda GK: Metabolite utilization in the porcine carotid artery: A 31P NMR study using the creatine analogue ßguanidinopropionic acid. J Physiol 477: 40P, 1994
Hellstrand P, Vogel HJ: Phosphagens and intracellular pH in intact rabbit smooth muscle studied by 31P-NMR. Am J Physiol 248: C320–C329, 1985
Nakayama S, Seo Y, Takai A, Tomita T, Watari H: Phosphorous corn-pounds studied by 31P nuclear magnetic resonance spectroscopy in the taenia of guinea-pig caecum. J Physiol 402: 565–578, 1988
Ashoori F, Takai A, Tokuno H, Tomita T: Effects of glucose removal and readmission on the potassium contracture in the guinea-pig taenia coli. J Physiol 356: 33–48, 1984
Katayama N, Huang S-M, Tomita T, Brading AF: Effects of cromakalim on the electrical slow wave in the circular muscle of guinea-pig gastric antrum. Br J Pharmacol 109: 1097–1100, 1993
Beech DJ, Zhang H, Nakao K, Bolton, TB: K channel activation by nucleotide diphosphates and its inhibition by glibenclamide in vascular smooth muscle cells. Br J Pharmacol 110: 573–582, 1993
Beech DJ, Zhang H, Nakao K, Bolton TB: Single channel and whole-cell K-currents evoked by levocromakalim in smooth muscle cells from the rabbit portal vein. Br J Pharmacol 110: 583–590, 1993
Kajioka S, Kitamura K, Kuriyama H: Guanosine diphosphate activates an adenosine-5’-triphosphate-sensitive K. channels in the rabbit portal vein. J Physiol 444: 397–418, 1991
Adams GR, Dillon PF: Glucose dependence of sequential norepinephrine contractions of vascular smooth muscle. Blood vessels 26: 7783, 1989
Clark JF, Dillon PF: Mechanical and metabolic toxicity of 3-(trimethylsilyl) propanesulfonic acid to porcine carotid arteries. Biochim Biophys Acta 1014: 235–238, 1989
Fisher MJ, Dillon PF: Phenylphosphonate: A 31P-NMR indicator of extracellular pH and volume in the isolated perfused rabbit bladder. Circ Res 60: 472–477, 1987
Clark JF, Khuchua Z, Kuznetsov AV, Vassileva AV, Boehm E, Radda GK, Saks VA: Actions of the creatine analogue ß-guanidinopropionic acid on rat heart mitochondria. Biochem J 300: 211–216, 1994
Carlier PG, Grandjean J, Michel P, D’Orio V, Rorive GL: Arterial metabolism as studied in vitro by NMR: Preliminary results in normotensive and hypertensive aortas. Arch Int Physiol Biochem 93: 107–118, 1985
Hardin CD, Roberts TM: Metabolism of exogenously applied fructose 1,6-bisphosphate in hypoxic vascular smooth muscle. Am J Physiol 267: H2325–H2332, 1994
Hardin CD, Roberts TM: Gluconeogenesis during hypoxia in vascular smooth muscle studied by 13C-NMR. Physiol Res 44: 257–260,1995
Hardin CD, Roberts TM: Compartmentation of glucose and fructose 1,6-bisphosphate metabolism in vascular smooth muscle. Biochemistry 34: 1323–1331, 1995
Hardin CD, Roberts TM: Regulation of glycogen utilisation, but not glucose utilisation, by precontraction glycogen levels in vascular smooth muscle. Biochemistry 36: 6954–6959, 1997
Hardin CD, Finder DR: Glycolytic flux in permeabilized freshly isolated vascular smooth muscle cells. Am J Physiol 274: C88–C96, 1998
Moon RB, Richards JH: Determination of intracellular pH by 31P nuclear magnetic resonance. J Biol Chem 248: 7276–7278, 1973
Nakayama S, Nomura H, Tomita T: Intracellular-free magnesium in the smooth muscle of guinea pig taenia caeci: A concomitant analysis for magnesium and pH upon sodium removal. J Gen Physiol 103: 833851, 1994
Nakayama S, Tomita T: Depletion of intracellular free Mg’ in Mg“- and Caz+-free solution in the taenia isolated from guinea-pig caecum. J Physiol 421: 363–378,1990
Nakayama S, Tomita T: Regulation of intracellular free magnesium concentration in the taenia of guinea-pig caecum. J Physiol 435: 559–572, 1991
Spurway NC, Wray S: A phosphorus NMR study of metabolites and intracellular pH in rabbit vascular smooth muscle. J Physiol 393: 57–71, 1987
Taggart M, Wray S: Simultaneous measurement of intracellular pH and contraction in uterine smooth muscle. Pflügers Arch 423: 527–529,1993
Parratt J, Taggart M, Wray S: Abolition of contractions in the myometrium by acidification in vitro. Lancet 344: 717–718, 1994
Harrison N, Larcombe-McDouall JB, Wray S: A 31P NMR investigation into the effects of repeated vascular occlusion on uterine metabolites, intracellular pH and force. NMR Biomed 8: 28–32, 1995
Harrison N, Larcombe-McDouall JB, Earley L, Wray S: An in vivo study of the effects of ischaemia on uterine contraction, intracellular pH and metabolites in the rat. J Physiol 476: 349–354, 1994
Larcombe-McDoual J, Buttell N, Harrison N, Wray S: In vivo pH and metabolite changes during a single contraction in rat uterine smooth muscle. J Physiol 518: 783–790, 1999
Eisner DA, Nichols CG, O’Neill SC, Smith GL, Valdeolmillos M: The effects of metabolic inhibition on intracellular calcium and pH in isolated rat ventricular cells. J Physiol 411: 393–418, 1989
Demaurex N, Romanek RR, Orlowski J, Grinstein S: ATP dependence of Na+/H+ exchange: Nucleotide specificity and assessment of the role of phospholipide. J Gen Physiol 109: 117–128, 1997
Dawson MJ, Gadian DG, Wilkie DR: Contraction and recovery of living muscles studied by 31P nuclear magnetic resonance. J Physiol 267: 703–735,1977
Obara K, Bowman PS, Ishida Y, Paul RJ: Effects of hypoxia on [Caz+]., pH, myosin light chain phosphorylation in guinea-pig taenia caeci. J Physiol 503: 427–433, 1997
Aickin CC: Movement of acid equivalents across the mammalian smooth muscle cell membrane. In: Proton Passage Across Cell Membrane. Ciba, Foundation Symposium 139. John Wiley & Sons Ltd., Chichester, 1988, pp 3–22
Allen DG, Morris PG, Orchard CH, Pirolo JS: A nuclear magnetic resonance study of metabolism in the ferret heart during hypoxia and inhibition of glycolysis. J Physiol 361: 185–204, 1985
Yamada T, Kikuchi K, Sugi H: 31P nuclear magnetic resonance studies on the glycogenolysis regulation in resting and contracting frog skeletal muscle. J Physiol 460: 273–286, 1993
Clark JF, Kemp GJ, Radda GK: The creatine kinase equilibrium free [ADP] and myosin ATPase in vascular smooth muscle cross-bridges. J Theor Biol 173: 207–211, 1995
Clark JF, Dillon PF: Phosphocreatine and creatine kinase in energetic metabolism of the porcine carotid artery. J Vasc Res 32: 24–30, 1995
Nageswara Rao BD: Phosphorus-31NMR of enzyme complexes. In: G.D. Gorenstein (ed). Phosphorus-31NMR. Academic Press, Orlando, Florida, 1984, pp 57–103
Raju B, Murphy E, Levy LA, Hall RD, London RE: A fluorescent indicator for measuring cytosolic free magnesium. Am J Physiol 256: C540–0548, 1989
Tashiro M, Konishi M: Basal intracellular free Mg“ concentration in smooth muscle cells of guinea-pig taenia cecum: Intracellular calibration of the fluorescent indicator fraptra. Biophys J 73: 3358–3370, 1997
Gupta RK, Gupta P, Moore RD: NMR studies of intracellular metal ions in intact cells and tissues. Annu Rev Biophys Bioeng 13, 221–246, 1984
Nakayama S, Nomura H: Mechanisms of intracellular Mg“ regulation affected by amiloride and ouabain in the guinea-pig taenia caeci. J Physiol 488: 1–12, 1995
Bock JL, Wenz B, Gupta RK: Changes in intracellular Mg adenosine triphosphate and ionized Mg“ during blood storage: Detection by 31P nuclear magnetic resonance. Blood 65: 1526–1530, 1985
Dillon PR Free intracellular Mg“ in relaxed and contracted porcine carotid artery. J Physiol 371: 161P, 1986
Kopp SJ, Barron JT, Tow JP. Phosphatic metabolites, intracellular pH and free [Mg2+] in single intact porcine carotid artery segments studied by 31P NMR. Biochim Biophys Acta 1055: 27–35, 1990
Gupta RK, Moore RD: 31P NMR studies of intracellular free Mg“ in intact frog skeletal muscle. J Biol Chem 255: 3987–3993, 1980
Dawson MJ, Gadian DG, Wilkie DR: Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature 274: 4271–4275, 1978
Dillon PF: 31P Nuclear magnetic resonance spectroscopy In: M. Bárány (ed). Biochemistry of Smooth Muscle Contraction. Academic Press, San Diego, 1996, pp 393–404
Lawson JW, Veech RL, Effects of pH and free Mg“ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem 254, 6528–6537, 1979
Dillon PF: Influence of cellular energy metabolism on contractions of porcine carotid artery smooth muscle. J Vasc Res 37: 532–539, 2000
Fisher MJ, Dillon PF: 31P NMR study of insulin effects on the isolated perfused rabbit urinary bladder. Magn Reson Med 9: 53–65, 1989
Flatman PW: Mechanisms of magnesium transport. Annu Rev Physiol 53: 259–271, 1991
Tashiro M, Konishi M: Na+ gradient dependent Mg“ transport in smooth muscle cells of guinea pig taenia cecum. Biophys J 73: 33713384, 1997
Jelick LA, Gupta RK: NMR measurement of cytosolic free calcium, free magnesium, and intracellular sodium in the aorta of normal and spontaneously hypertensive rat. J Biol Chem 265: 1391–1400, 1990
Nishiye E, Somlyo AV, Somlyo AP: The effects of MgADP on cross-bridge kinetics: A laser flash photolysis study of guinea pig smooth muscle. J Physiol 460: 247–271, 1993
Fuglsang A, Khromov A, Torok K, Somlyo AV, Somlyo AP: Flash photolysis studies of relaxation and cross-bridge detachment: Higher sensitivity of tonic than phasic smooth muscle to MgADP. J Muscle Res Cell Motil 14: 666–673, 1993
Zhang W, Truttmann AC, Lüthi D, McGugan JAS: Apparent Mg“- adenosine 5-triphosphate dissociation constant measured with Mg2+ macroelectrodes under conditions pertinent to 31P NMR ionized magnesium determinations. Anal Biochem 251: 246–250, 1997
Hardin CD, Wisemand RW, Kushmerick MJ: Tension responses of sheep aorta to simultaneous decreases in phosphocreatine inorganic phosphate and ATP. J Physiol 458: 139–150, 1992
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2003 Springer Science+Business Media New York
About this chapter
Cite this chapter
Nakayama, S., Clark, J.F. (2003). Smooth muscle and NMR review: An overview of smooth muscle metabolism. In: Clark, J.F. (eds) Guanidino Compounds in Biology and Medicine. Molecular and Cellular Biochemistry, vol 40. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0247-0_3
Download citation
DOI: https://doi.org/10.1007/978-1-4615-0247-0_3
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-4985-3
Online ISBN: 978-1-4615-0247-0
eBook Packages: Springer Book Archive