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Signalling components involved in contraction-inducible substrate uptake into cardiac myocytes

Published online by Cambridge University Press:  05 March 2007

Joost J. F. P. Luiken ,
Susan L. M. Coort ,
Debby P. Y. Koonen ,
Arend Bonen  and
Jan F. C. Glatz
Joost J. F. P. Luiken*
Affiliation:
Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, NL-6200 MD, Maastricht, The Netherlands
Susan L. M. Coort
Affiliation:
Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, NL-6200 MD, Maastricht, The Netherlands
Debby P. Y. Koonen
Affiliation:
Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, NL-6200 MD, Maastricht, The Netherlands
Arend Bonen
Affiliation:
Department of Human Biology and Nutritional Sciences, University of Guelph, Guelph, Ontario, N1G 2W1, Canada
Jan F. C. Glatz
Affiliation:
Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, NL-6200 MD, Maastricht, The Netherlands
*
*Corresponding author: Joost J. F. P. Luiken Fax: +31 43 388 4574, Email: [email protected]
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Abstract

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Glucose and long-chain fatty acids (LCFA) are two major substrates used by heart and skeletal muscle to support contractile activity. In quiescent cardiac myocytes a substantial portion of the glucose transporter GLUT4 and the putative LCFA transporter fatty acid translocase (FAT)/CD36 are stored in intracellular compartments. Induction of cellular contraction by electrical stimulation results in enhanced uptake of both glucose and LCFA through translocation of GLUT4 and FAT/CD36 respectively to the sarcolemma. The involvement of protein kinase A, AMP-activated protein kinase (AMPK), protein kinase C (PKC) isoforms and the extracellular signal-regulated kinases was evaluated in cardiac myocytes as candidate signalling enzymes involved in recruiting these transporters in response to contraction. The collected evidence excluded the involvement of PKA and implicated an important role for AMPK and for one (or more) PKC isoform(s) in contraction-induced translocation of both GLUT4 and FAT/CD36. The unravelling of further components along this contraction pathway can provide valuable information on the coordinated regulation of the uptake of glucose and of LCFA by an increase in mechanical activity of heart and skeletal muscle.

Type
Symposium 2: The fatty acid transporters of skeletal muscle
Information
Proceedings of the Nutrition Society , Volume 63 , Issue 2 , May 2004 , pp. 251 - 258
Copyright
Copyright © The Nutrition Society 2004

References

Bonen, A, Luiken, JJ, Arumugam, Y, Glatz, JF & Tandon, NN (2000) Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. Journal of Biological Chemistry 275, 14501–14508.Google Scholar
Bonen, A, Luiken, JJ & Glatz, JF, (2002) Regulation of fatty acid transport and membrane transporters in health and disease. Molecular and Cellular Biochemistry 239, 181–192.Google Scholar
Boone, AN, Rodrigues, B & Brownsey, RW (1998) Multiple-site phosphorylation of the 280 kDa isoform of acetyl-CoA carboxylase in rat cardiac myocytes: evidence that cAMP-dependent protein kinase mediates effects of beta-adrenergic stimulation. Biochemical Journal 341, 347–354.CrossRefGoogle Scholar
Chen, HC, Bandyopadhyay, G, Sajan, MP, Kanoh, Y, Standaert, M, Farese, RV Jr & Farese, RV (2002) Activation of the ERK pathway and atypical protein kinase C isoforms in exercise- and aminoimidazole-4-carboxamide-1-beta- D -riboside (AICAR)-stimulated glucose transport. Journal of Biological Chemistry 277, 23554–23562.Google Scholar
Clerk, A, Bogoyevitch, MA, Fuller, SJ, Lazou, A, Parker, PJ & Sugden, PH, (1995) Expression of protein kinase C isoforms during cardiac ventricular development. American Journal of Physiology 269, H1087–H1097.Google Scholar
Corton, JM, Gillespie, JG, Hawley, SA & Hardie, DG (1995) 5-Aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells. European Journal of Biochemistry 229, 558–565.Google Scholar
Cushman, SW, Goodyear, LJ, Pilch, PF, Ralston, E, Galbo, H, Ploug, T, Kristiansen, S & Klip, A (1998) Molecular mechanisms involved in GLUT4 translocation in muscle during insulin and contraction stimulation. Advances in Experimental Medicine and Biology 441, 63–71.Google Scholar
Disatnik, MH, Buraggi, G & Mochly-Rosen, D (1994) Localization of protein kinase C isozymes in cardiac myocytes. Experimental Cell Research 210, 287–297.Google Scholar
Egert, S, Nguyen, N & Schwaiger, M, (1999) Contribution of alpha-adrenergic and beta-adrenergic stimulation to ischemia-induced glucose transporter (GLUT) 4 and GLUT1 translocation in the isolated perfused rat heart. Circulation Research 84, 1407–1415.Google Scholar
Farese, RV (2002) Function and dysfunction of aPKC isoforms for glucose transport in insulin-sensitive and insulin-resistant states. American Journal of Physiology 283, E1–E11.Google Scholar
Fischer, Y, Rose, H, Thomas, J, Deuticke, B, Kammermeier, H, (1993) Phenylarsine oxide and hydrogen peroxide stimulate glucose transport via different pathways in isolated cardiac myocytes. Biochimica et Biophysica Acta 1153, 97–104.CrossRefGoogle ScholarPubMed
Glatz, JF, Bonen, A & Luiken, JJ (2002) Exercise and insulin increase muscle fatty acid uptake by recruiting putative fatty acid transporters to the sarcolemma. Current Opinion in Clinical Nutrition and Metabolic Care 5, 365–370.Google Scholar
Goldberg, M, Zhang, HL, Steinberg, SF, (1997) Hypoxia alters the subcellular distribution of protein kinase C isoforms in neonatal rat ventricular myocytes. Journal of Clinical Investigation 99, 55–61.CrossRefGoogle ScholarPubMed
Hamilton, JA (1998) Fatty acid transport: difficult or easy. Journal of Lipid Research 39, 467–481.Google Scholar
Hardie, DG, Carling, D, Carlson, M, (1998) The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell. Annual Review of Biochemistry 67, 821–855.Google Scholar
Hardie, DG & Hawley, SA (2001) AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 23, 1112–1119.Google Scholar
Hayashi, T, Hirshman, MF, Dufresne, SD & Goodyear, LJ (1999) Skeletal muscle contractile activity in vitro stimulates mitogen-activated protein kinase signaling. American Journal of Physiology 277, C701–C707.Google Scholar
Hussain, M & Orchard, CH (1997) Sarcoplasmic reticulum Ca 2+ content, L-type Ca 2+ current and the Ca 2+ transient in rat myocytes during beta-adrenergic stimulation. Journal of Physiology (London) 505, 385–402.Google Scholar
Javaux, F, Vincent, MF, Wagner, DR, van den Berghe, G (1995) Cell-type specificity of inhibition of glycolysis by 5-amino-4-imidazolecarboxamide riboside. Lack of effect in rabbit cardiomyocytes and human erythrocytes, and inhibition in FTO-2B rat hepatoma cells. Biochemical Journal 305, 913–919.Google Scholar
Keizer, HA, Schaart, G, Tandon, NN, Glatz, JFC & Luiken, JJFP (2004) Subcellular immunolocalisation of fatty acid translocase (FAT)/CD36 in human type-1 and type-2 skeletal muscle fibres. Histochemical Cell Biology 121, 101–107.Google Scholar
Kones, RJ & Phillips, JH (1975) Insulin: fundamental mechanism of action and the heart. Cardiology 60, 280–303.CrossRefGoogle ScholarPubMed
Luiken, JJ, Coort, SL, Willems, J, Coumans, WA, Bonen, A, van der Vusse, GJ, Glatz, JF, (2003) Contraction-induced fatty acid translocase/CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling. Diabetes 52, 1627–1634.Google Scholar
Luiken, JJ, Koonen, DP, Willems, J, Zorzano, A, Becker, C, Fischer, Y, Tandon, NN, Van Der Vusse, GJ, Bonen, A & Glatz, JF (2002a) Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes 51, 3113–3119.Google Scholar
Luiken, JJ, Willems, J, Coort, SL, Coumans, WA, Bonen, A, Van, D, er Vusse, GJ & Glatz, JF, (2002b) Effects of cAMP modulators on long-chain fatty-acid uptake and utilization by electrically stimulated rat cardiac myocytes. Biochemical Journal 367, 881–887.Google Scholar
Luiken, JJ, Willems, J van der Vusse, GJ, Glatz, JF, (2001) Electrostimulation enhances FAT/CD36-mediated long-chain fatty acid uptake by isolated rat cardiac myocytes. American Journal of Physiology 281, E704–E712.Google Scholar
Mauvais-Jarvis, F, Andreelli, F Hanaire-Broutin, H Charbonnel, B, Girard, J, (2001) Therapeutic perspectives for type 2 diabetes mellitus: molecular and clinical insights. Diabetes Metabolism 27, 415–423.Google Scholar
Murray, KJ, Reeves, ML & England, PJ, (1989) Protein phosphorylation and compartments of cyclic AMP in the control of cardiac contraction. Molecular and Cellular Biochemistry 89, 175–179.Google Scholar
Musi, N & Goodyear, LJ (2003) AMP-activated protein kinase and muscle glucose uptake. Acta Physiologica Scandinavica 178, 337–345.Google Scholar
Nishimura, H & Simpson, IA (1994) Staurosporine inhibits phorbol 12-myristate 13-acetate- and insulin-stimulated translocation of GLUT1 and GLUT4 glucose transporters in rat adipose cells. Biochemical Journal 302, 271–277.Google Scholar
Ploug, T & Ralston, E (2002) Exploring the whereabouts of GLUT4 in skeletal muscle (review). Molecular Membrane Biology 19, 39–49.Google Scholar
Puceat, M, Hilal-Dandan, R, Strulovici, B, Brunton, LL, Brown, JH, (1994) Differential regulation of protein kinase C isoforms in isolated neonatal and adult rat cardiomyocytes. Journal of Biological Chemistry 269, 16938–16944.Google Scholar
Rodrigues, B, Cam, MC & McNeill, JH (1998) Metabolic disturbances in diabetic cardiomyopathy. Molecular and Cellular Biochemistry 180, 53–57.Google Scholar
Rose, H, Strotmann, KH, Popping, S, Fischer, Y, Kulsch, D & Kammermeier, H, (1991) Simultaneous measurement of contraction and oxygen consumption in cardiac myocytes. American Journal of Physiology 261, H1329–H1334.Google ScholarPubMed
Ruderman, NB, Park, H, Kaushik, VK, Dean, D, Constant, S, Prentki, M & Saha, AK (2003) AMPK as a metabolic switch in rat muscle, liver and adipose tissue after exercise. Acta Physiologica Scandinavica 178, 435–442.Google Scholar
Ruderman, NB, Saha, AK, Vavvas, D & Witters, LA (1999) Malonyl-CoA, fuel sensing, and insulin resistance. American Journal of Physiology 276, E1–E18.Google Scholar
Russell, RR 3rd Bergeron, R, Shulman, GI & Young, LH, (1999) Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. American Journal of Physiology 277, H643–H649.Google Scholar
Samari, HR & Seglen, PO (1998) Inhibition of hepatocytic autophagy by adenosine, aminoimidazole-4-carboxamide riboside, and N6-mercaptopurine riboside. Evidence for involvement of AMP-activated protein kinase. Journal of Biological Chemistry 273, 23758–23763.Google Scholar
Schaub, MC & Kunz, B (1986) Regulation of contraction in cardiac and smooth muscles. Journal of Cardiovascular Pharmacology 8, Suppl. 8, S117–S123.Google Scholar
Shulman, GI (2000) Cellular mechanisms of insulin resistance. Journal of Clinical Investigation 106, 171–176.Google Scholar
Steinberg, SF, Goldberg, M & Rybin, VO (1995) Protein kinase C isoform diversity in the heart. Journal of Molecular and Cellular Cardiology 27, 141–153.Google Scholar
Till, M, Kolter, T, Eckel, J, (1997) Molecular mechanisms of contraction-induced translocation of GLUT4 in isolated cardiomyocytes. American Journal of Cardiology 80, 85A–89A.Google Scholar
Unger, RH & Orci, L (2001) Diseases of liporegulation: new perspective on obesity and related disorders. FASEB Journal 15, 312–321.Google Scholar
Van Bilsen, M, de Vries, JE Van der Vusse, GJ (1997) Long-term effects of fatty acids on cell viability and gene expression of neonatal cardiac myocytes. Prostaglandins, Leukotrienes and Essential Fatty Acids 57, 39–45.Google Scholar
van der Vusse, GJ, Glatz, JF, Stam, HC, Reneman, RS, (1992) Fatty acid homeostasis in the normoxic and ischemic heart. Physiological Reviews 72, 881–940.Google Scholar
van der Vusse, GJ, Van Bilsen, M & Glatz, JF (2000) Cardiac fatty acid uptake and transport in health and disease. Cardiovascular Research 45, 279–293.Google Scholar
Vogt, B, Mushack, J, Seffer, E & Haring, HU (1991) The translocation of the glucose transporter sub-types GLUT1 and GLUT4 in isolated fat cells is differently regulated by phorbol esters. Biochemical Journal 275, 597–600.Google Scholar
Wheeler, TJ, Fell, RD, Hauck, MA, (1994) Translocation of two glucose transporters in heart: effects of rotenone, uncouplers, workload, palmitate, insulin and anoxia. Biochimica et Biophysica Acta 1196, 191–200.Google Scholar
Wojtaszewski, JF, Lynge, J, Jakobsen, AB, Goodyear, LJ & Richter, EA (1999) Differential regulation of MAP kinase by contraction and insulin in skeletal muscle: metabolic implications. American Journal of Physiology 277, E724–E732.Google Scholar
Zorzano, A, Fandos, C, Palacin, M, (2000) Role of plasma membrane transporters in muscle metabolism. Biochemical Journal 349, 667–688.Google Scholar