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Compartmentation of ATP synthesis and utilization in smooth muscle: roles of aerobic glycolysis and creatine kinase

  • Muscle Energy Metabolism
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Abstract

The phosphocreatine content of smooth muscle is of similar magnitude to ATP. Thus the function of the creatine kinase system in this tissue cannot simply be regarded as an energy buffer. Thus an understanding of its role in smooth muscle behavior can point to CK function in other systems. From our perspective CK function in smooth muscle is one example of a more general phenomenon, that of the co-localization of ATP synthesis and utilization. In an interesting and analogous fashion distinct glycolytic cascades are also localized in regions of the cell with specialized energy requirements. Similar to CK, glycolytic enzymes are known to be localized on thin filaments, sarcoplasmic reticulum and plasma membrane. In this chapter we will describe the relations between glycolysis and smooth muscle function and compare and contrast to that of the CK system. Our goal is to more fully understand the significance of the compartmentation of distinct pathways for ATP synthesis with specific functions in smooth muscle. This organization of metabolism and function seen most clearly in smooth muscle is likely representative of many other cell types.

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References

  1. Paul RJ: Chemical energetics of vascular smooth muscle. In: DF Bohr, AP Somlyo, HV Sparks (eds.), Handbook of Physiology, 2, Vol. II. pp. 201–236. American Physiological Society, Bethesda, MD (1980)

    Google Scholar 

  2. Kushmerick MJ, Paul RJ: Aerobic recovery metabolism following single isometric tetani in frog sartorius at 0° C. J Physiol 254: 693–709, 1976

    PubMed  Google Scholar 

  3. Paul RJ, Bauer M, Pease W: Vascular smooth muscle: Aerobic glycolysis linkled to Na−K transport processes. Science 206: 1414–1416, 1979

    PubMed  Google Scholar 

  4. Paul RJ: Aerobic glycolysis and ion transport in vascular smooth muscle. Am J Physiol 244: C399-C409, 1983

    PubMed  Google Scholar 

  5. Campbell JD, Paul RJ: The nature of fuel provision for the Na+, K+-ATPase in porcine vascular smooth muscle. J Physiol 447: 67–82, 1992

    PubMed  Google Scholar 

  6. Lynch RM, Paul RJ: Glucose uptake by porcine carotid artery: Relation to alterations in Na,K-transport. Am J Physiol 247 (Cell Physiol 16): C433-C440, 1984

    PubMed  Google Scholar 

  7. Lynch RM, Kuettner CP, Paul RJ: Regulation of glycogen metabolism during tension generation and maintenance in vascular smooth muscle. Am J Physiol 257: C736-C742, 1989

    PubMed  Google Scholar 

  8. Lynch RM, Paul RJ: Compartmentation of glycolysis and glycogenolysis in vascular smooth muscle. Science 222: 1344–1346, 1983

    PubMed  Google Scholar 

  9. Lynch RM, Paul RJ: Compartmentation of carbohydrate metabolism in vascular smooth muscle: Evidence for at least two functionally independent pools of glucose-6-phosphate. Biochim Biophys Acta 887: 315–318, 1986

    PubMed  Google Scholar 

  10. Hardin CD, Wiseman RW, Kushmerick MJ: Vascular oxidative metabolism under different metabolic conditions. Biochim Biophys Acta 1133: 133–141, 1992

    PubMed  Google Scholar 

  11. Lynch RM, Balaban RS: Coupling of aerobic glycolysis and Na+−K+-ATPase in the renal cell line MDCK. Am J Physiol 253: C269-C276, 1987

    PubMed  Google Scholar 

  12. Weiss JN, Lamp ST: Glycolysis preferentially inhibits ATP-sensitive K+ channels in isolated guinea pig cardiac myocytes. Science 238: 67–69, 1987

    PubMed  Google Scholar 

  13. Paul RJ, Hardin C, Wuytack F, Raeymaekers L, Casteels R: An endogenous glycolytic cascade can preferentially support Ca uptake in smooth muscle plasma membrane vesicles. FASEB J 3: 2298–3201, 1989

    PubMed  Google Scholar 

  14. Hardin C, Raeymaekers L, Paul RJ: Comparison of endogenous and exogenous sources of ATP in fueling Ca uptake in smooth muscle plasma membrane vesicles. J Gen Physiol 99: 21–40, 1992

    PubMed  Google Scholar 

  15. Rossi AM, Eppenberger HM, Volpe P, Cotrufo R, Wallimann T: Muscle-type MM creatine kinase is specifically bound to sarcoplasmic reticulum and can support Ca2+-uptake and regulate local ATP/ADP ratios. J Biol Chem 265: 5258–5266, 1990

    PubMed  Google Scholar 

  16. Läuger P: Ca2+-pumps from sarcoplasmic reticulum. In: P Läuger (ed) Electrogenic Ion Pumps, Sinderland, MA, USA, pp 227–251, 1991

  17. Korge P, Byre SK, Campbell KB: Functional coupling between SR-bound creatine kinase and Ca2+-ATPase. Eur J Biochem 213: 923–980, 1993

    Google Scholar 

  18. Proverbio F, Shoemaker DG, Hoffmann JF: Functional consequences of the membrane pool of ATP associated with the human red blood cell Na/K pump. Prog Clin Biol Res 268A: 561–567, 1988

    PubMed  Google Scholar 

  19. Iyengar MR: Creatine kinase as an intracellular regulator. J Muscle Res Cell Motil 5: 527–534, 1984

    PubMed  Google Scholar 

  20. Paul RJ, Ishida Y, Rubanyi G: Vascular smooth muscle metabolism and mechanisms of oxygen sensing. In: JA Will, CA Dawson, EK Weir, CK Buckner (eds), The Pulmonary Circulation in Health and Disease. pp. 97–108. Academic Press, Orland, 1987

    Google Scholar 

  21. Cain DF, Davies RE: Breakdown of adenosine triphosphate during a single contraction of working muscle. Biochem Biophys Res Commun 8: 361–366, 1962

    PubMed  Google Scholar 

  22. Butler TM, Davies RE: High energy phosphates in smooth muscle. In: DF Bohr, AP Somlyo, HV Sparks (eds), Handbook of Physiology, section 2, Vol. II. pp. 237–252. American Physiological Society, Bethesda, MD, 1980

    Google Scholar 

  23. Paul RJ: Smooth muscle energetics. Ann Rev Physiol 51: 331–349, 1989

    Google Scholar 

  24. Ishida Y, Hashimoto M, Paul RJ: Effects of substrate depletion and hypoxia on the energy metabolism and isometric force of the hog coronary artery. Fed Proc 46: 1096, 1987

    Google Scholar 

  25. Ishida Y, Paul RJ: Effects of hypoxia on high-energy phosphagen content, energy metabolism and isometric force in guinea-pig taenia caeci. J Physiol (Lond.) 424: 41–56, 1990

    Google Scholar 

  26. Krisanda JM, Paul RJ: High energy phosphate and metabolite content during isometric contraction in porcine carotid artery. Am J Physiol 244: C385-C390, 1983

    PubMed  Google Scholar 

  27. Ozaki H, Satoh T, Karaki H, Ishida Y: Regulation of metabolism and contraction by cytoplasmic calcium in the intestinal smooth muscle. J Biol Chem 263: 14074–14079, 1988

    PubMed  Google Scholar 

  28. Hellstrand P, Paul RJ: Phosphagen content, breakdown during contraction and oxygen consumption in rat portal vein. Am J Physiol 244: C250-C258, 1983

    PubMed  Google Scholar 

  29. Hellstrand P, Vogel HJ: Phosphagens and intracellular pH in intact rabbit smooth muscle by31P-NMR. Am J Physiol 248: C320-C329, 1985

    PubMed  Google Scholar 

  30. Butler TM, Siegman MJ, Mooers SV, Davies RE: Chemical energetics of single isometric tetani in mammalian smooth muscle. Am J Physiol 235: C1-C7, 1977

    Google Scholar 

  31. Daemers-Lambert C: Action du fluorodinitrobenzene sur le metabolisme phosphore du muscle lisse arteriel pendant la stimulation electrique (carotide de bovide). Angiologica 6: 1–12, 1969

    PubMed  Google Scholar 

  32. Daemers-Lambert C: Mechanochemical coupling in smooth muscle. In: NL Stephens (ed), The Biochemistry of Smooth Muscle. pp. 51–82. University Park Press, Baltimore, MD, 1977

    Google Scholar 

  33. Furchgott RF, Shorr E: The effect of succinate on respiration and certain metabolic processes of mammalian tissues at low oxygen tensionsin vitro. J Biol Chem 175: 201–215, 1948

    Google Scholar 

  34. Born GVR: The relation between the tension and the high-energy phosphate content of smooth muscle. J Physiol (Lond.) 131: 704–711, 1956

    Google Scholar 

  35. Nakayama S, Seo Y, Takai A, Tomita T, Watari H: Phosphorus compounds studied by31P nuclear magnetic resonance spectroscopy in the taenia of guinea-pig caecum. J Physiol (Lond.) 402: 565–578, 1988

    Google Scholar 

  36. Dillon PF, Fisher MJ, Adams GR, Clark JF: The use of31P-NMR to study smooth muscle. Prog Clin Biol Res 315: 439–449, 1989

    PubMed  Google Scholar 

  37. Ishida Y, Paul RJ: Evidence for compartmentation of high energy phosphagens in smooth muscle. Prog Clin Biol Res 315: 417–428, 1989

    PubMed  Google Scholar 

  38. Coburn RF, Moreland S, Moreland RS, Baron C: Rate-limiting energy-dependent steps controlling oxidative metabolism-contraction coupling in rabbit aorta. J Physiol (Lond.) 448: 473–492, 1992

    Google Scholar 

  39. Ishida Y, Takagi K, Urakawa N: Tension maintenance, calcium content and energy production of the taenia of the guinea-pig caecum under hypoxia. J Physiol (Lond.) 347: 149–159, 1984

    Google Scholar 

  40. Bueding E, Bulbring E, Gercken G, Hawkins JT, Kuriyarna H: The effect of adrenaline on the adenosinetriphosphate and creatine phosphate content of intestinal smooth muscle. J Physiol (Lond) 193: 187–212, 1967

    Google Scholar 

  41. Urakawa N, Ikeda M, Saito Y, Sakai Y: Effects of factors inhibiting tension development on oxygen consumption of guinea pig taenia coli. Jpn J Pharmacol 19: 578–579, 1969

    PubMed  Google Scholar 

  42. Adams GR, Dillon PF: Glucose dependence of sequential norepinephrine contractions of vascular smooth muscle. Blood Vessels 26: 77–83, 1989

    PubMed  Google Scholar 

  43. Geiger WB: The creatine phosphokinase of a visceral muscle. J Biol Chem 220: 871–877, 1956

    PubMed  Google Scholar 

  44. Dawson DM, Fine IH: Creatine kinase in human tissues. Arch Neurol 16: 175–180, 1967

    PubMed  Google Scholar 

  45. Allard D, Cabrol D: Etude electrophoretique des isozymes de la creatine phosphokinase dans les tissus de l'Homme et du Lapin. Pathol Biol 18: 847–950, 1970

    PubMed  Google Scholar 

  46. Focant B: Isolemente et proprietes de la creatine-kinase de muscle lisse de boeuf. FEBS Lett 10: 57–61, 1970

    PubMed  Google Scholar 

  47. Traugott C, Massaro EJ: An electrophoretic analysis of rodent creatine phosphokinase isoenzymes. Comp Biochem Physiol 42B: 255–262, 1972

    Google Scholar 

  48. Ishida Y, Wyss M, Hemmer W, Wallimann T: Identification of creatine kinase isoenzymes in the guinea-pig: Presence of mitochondrial creatine kinase in smooth muscle. FEBS Lett 283: 37–43, 1991b

    PubMed  Google Scholar 

  49. Clark JF, Khuchua Z, Ventura-Clapier R Creatine kinase binding and possible role in chemically skinned guinea-pig taenia coli. Biochim Biophys Acta 1100: 137–145, 1992

    PubMed  Google Scholar 

  50. Jacobus WE, Lehninger AL: Creatine kinase of rat heart mitochondria: Coupling of creatine phosphorylation to electron transport. J Biol Chem 248: 4803–4810, 1973

    PubMed  Google Scholar 

  51. Haas RC, Strauss AW: Separate nuclear genes encode sarcomere-specific and ubiquitous human mitochondrial creatine kinase isoenzymes. J Biol Chem 265: 6921–6927, 1990

    PubMed  Google Scholar 

  52. Ishida Y, Honda H, Riesinger I, Wallimann T: Localization of creatine kinase isoenzymes in smooth muscle cells. Jpn J Physiol 41: S301, 1991a

    Google Scholar 

  53. Adams V, Bosch W, Schlegel J, Wallimann T, Brdiczka D: Further characterization of contact sites from mitochondria of different tissues: Topology of peripheral kinases. Biochim Biophys Acta 981: 213–225, 1989

    PubMed  Google Scholar 

  54. Biermans W, Bernaert I, De Bie M, Nijs B, Jacob W: Ultrastructural localization of creatine kinase activity in the contact sites between inner and outer mitochondrial membranes of rat myometrium. Biochim Biophys Acta 974: 74–80, 1989

    PubMed  Google Scholar 

  55. Lipskaya TY, Trofimova ME: Study on heart mitochondrial creatine kinase using a cross-linking bifunctional reagent. I. The binding involves the octameric form of the enzyme. Biochem Int 18: 1029–1039, 1989

    PubMed  Google Scholar 

  56. Wyss M, Smeitink J, Wevers RA, Wallimann T: Mitochondrial creatine kinase: a key enzyme of aerobic energy metabolism. Biochim Biophys Acta 1102: 119–166, 1992

    PubMed  Google Scholar 

  57. Strehler EE, Carlsson E, Eppenberger HM, Thornell LE: Ultrastructural localization of M-band proteins in chicken breast muscle as revealed by combined immunocytochemistry and ultracryotomy. J Mol Biol 166: 141–158, 1983

    PubMed  Google Scholar 

  58. Wallimann T, Moser H, Eppenberger H: Isoenzymes specific localization of M-line-bound creatine kinase in myogenic cells. J Muscle Res Cell Motil 4: 429–441, 1983

    PubMed  Google Scholar 

  59. Wallimann T, Eppenberger HM: Localization and function of M-line bound creatine kinase: M-band model and creatine phosphate shuttle. In: JW Shay (ed), Cell and Muscle Motility, pp 239–285, Plenum, NY, 1985

    Google Scholar 

  60. Wallimann T, Schnyder T, Schlegel J, Wyss M, Wegmann G, Rossi AM, Hemmer W, Eppenberger HM, Quest AFG: Subcellular compartmentation of creatine kinase isoenzymes of CK and octa meric structure of mitochondrial CK: Important aspects of the phosphoryl-creatine circuit. Prog Clin Biol Res 315: 159–176, 1989

    PubMed  Google Scholar 

  61. Fischer W, Pfitzer G: Rapid myosin phosphorylation transients in phasic contractions in chicken gizzard smooth muscle. FEBS Lett 258: 59–62, 1989

    PubMed  Google Scholar 

  62. Ozaki H, Kasai H, Hori M, Sato K, Ishihara H, Karaki H: Direct inhibition of chicken gizzard smooth muscle contractile apparatus by caffeine. Naunyn-Schrniecleberg's Arch Pharmacol 341: 262–267, 1990

    Google Scholar 

  63. Stephens NL, Kroeger EA, Wrogeman K: Energy metabolism: Methods in isolated smooth muscle and methods at cellular and subcellular levels. In: Daniel EE, Paton DM (eds), Methods in Pharmacology, Vol. 3, Smooth Muscle. pp. 555–591. Plenum Press, New York, 1975

    Google Scholar 

  64. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM: Intracellular comparmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochem J 281: 21–40, 1992

    PubMed  Google Scholar 

  65. Iyengar MR, Fluellen CE, Iyengar C: Creatine kinase from the bovine myometrium; purification and characterization. J Muscle Res Cell Motilit 3: 312–346, 1982

    Google Scholar 

  66. Quest AFG, Soldati T, Hemmer W, Perriard JC, Eppenberger HM, Wallimann T: Phosphorylation of chicken brain-type creatine kinase affects a physiologically important kinetic parameter and gives rise to protein microheterogeneityin vivo. FEBS Lett 269: 457–464, 1990

    PubMed  Google Scholar 

  67. Ishida Y, Hashimoto M, Paul RJ: Does a limitation of energy supply to the contractile apparatus underlie the relaxation induced by hypoxia in smooth muscle? Prog Clin Biol Res 245: 463–464, 1989

    Google Scholar 

  68. Coburn RF, Grubb B, Aronson RD: Effect of cyanide on oxygen tension dependent mechanical tension in rabbit aorta. Circ Res 44: 368–378, 1979

    PubMed  Google Scholar 

  69. Chida K, Tsunenaga M, Kasahara K, Kohno Y, Kuroki T: Regulation of creatine kinase-B activity by protein kinase-C. Biochem Biophys Res Commun 173: 346–350, 1990

    PubMed  Google Scholar 

  70. Coburn RF, Baron C, Papadopoulos MT: Phosphoinositide metabolism and metabolism-contraction coupling in rabbit aorta. Am J Physiol 255: H1476-H1483, 1988

    PubMed  Google Scholar 

  71. Liou RS, Anderson SR: Binding of ATP and of 1,N6-ethenoadenosine triphosphate to rabbit muscle phosphofructokinase. Biochemistry 17: 999–1004, 1978

    PubMed  Google Scholar 

  72. Neidl C, Engel J: Exchange of ADP, ATP and 1:N6-ethenoadenosine 5′-triphosphate at G-actin. Equilibrium and kinetics. Eur J Biochem 101: 163–169, 1979

    PubMed  Google Scholar 

  73. Van Waade A, Van Den Thillart G, Erkelens C, Addink A, Lugtenburg J: Functional coupling of glycolysis and phosphocreatine utilization in anoxic fish muscle. J Biol Chem 265: 914–923, 1990

    PubMed  Google Scholar 

  74. Wegmann G, Zanolla E, Eppenberger HM, Wallimann T: In situ compartmentation of creatine kinase in intact sarcomeric muscle: the acto-myosin overlap zone as a molecular sieve. J Muscle Res Cell Motil 13: 420–435, 1992

    PubMed  Google Scholar 

  75. Dillon PF, Clark JF: The theory of diazymes and functional coupling of pyruvate kinase and creatine kinase. J Theo Biol 143: 275–284, 1990

    Google Scholar 

  76. Walliman T, Wlazthony D, Wegmann G, Moser H, Eppenberger HM, Barrantes FJ: Subcellular localization of creatine kinase in torpedo electrocytes: association with acetylcholine receptor-rich membranes. J Cell Biol 100: 1063–1072, 1985

    PubMed  Google Scholar 

  77. Blum H, Balshi JA, Johnson RG: Coupledin vivo activity of creatine phosphokinase and membrane bound (Na+, K+)-ATPase in the resting and stimulated electric organ of the electric fish narcine brasiliensis. J Biol Chem 266: 10254–10259, 1991

    PubMed  Google Scholar 

  78. Hardin CD, Paul RJ: Localization of two glycolytic enzymes in guinea pigtaenia coli. Biochim Biophys Acta 1134(3): 256–259, 1992

    PubMed  Google Scholar 

  79. Meyer RA, Sweeney HL, Kushmerick MJ: A simple analysis of the ‘phosphocreatine shuttle’. Am J Physiol 246: C365-C377, 1984

    PubMed  Google Scholar 

  80. Ekmehag BL, Hellstrand P: Contractile and metabolic characteristics of creatine-depleted vascular smooth muscle of the rat portal vein. Acta Physiol Scand 133: 525–533, 1988

    PubMed  Google Scholar 

  81. Lynch RM, Paul RJ: Functional compartmentation of carbohydrate metabolism. In: D Jones (ed), CRC Reviews Microcompartmentation, CRC Press, pp. 17–35, 1988

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Authors and Affiliations

  1. Mitsubishi Kasei Institute of Life Sciences, 11 Minamiooya, 194, Machida-Shi, Tokyo, Japan

    Y. Ishida

  2. Institute for Cell Biology, ETH-Hönggerberg, CH 8093, Zürich, Switzerland

    I. Riesinger & T. Wallimann

  3. Department of Physiology & Biophysics, University of Cincinnati, College of Medicine, 45267-0576, Cincinnati, OH, USA

    R. J. Paul

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  1. Y. Ishida
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  4. R. J. Paul
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Ishida, Y., Riesinger, I., Wallimann, T. et al. Compartmentation of ATP synthesis and utilization in smooth muscle: roles of aerobic glycolysis and creatine kinase. Mol Cell Biochem 133, 39–50 (1994). https://doi.org/10.1007/BF01267946

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