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Am J Physiol Endocrinol Metab 295: E729, 2008; doi:10.1152/ajpendo.90537.2008
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LETTERS TO THE EDITOR

Reply to Clausen letter

Alexander V. Chibalin and Boubacar Benziane

Department of Molecular Medicine and Surgery, Integrative Physiology, Karolinska Institutet, Stockholm, Sweden

TO THE EDITOR: Professor Torben Clausen has made, and continues to make, seminal contributions to the field of skeletal muscle Na+-K+-ATPase regulation. The aim of our article (3) was to highlight recent developments in the field and how this builds on the important earlier data highlighted in Professor Clausen's Letter to the Editor in this issue (4). The important paper from Erlij and Grinstejn (5) is in fact quoted in our paper.

Membrane traffic of plasma membrane proteins, and existence of an intracellular pool of these proteins, is a well-established phenomenon in skeletal muscle (9, 11). Evidence from the same fractionation procedures discussed in our article (3) have revealed GLUT4 translocation in skeletal muscle, a phenomenon that has now been verified by live-cell microscopy. Thus, the possibility that sodium pump cell surface abundance is similarly regulated by exocytosis or endocytosis in skeletal muscle should not be ignored. The internalization of the Na+-K+-ATPase:ouabain complex may occur due to constitutive or ouabain-stimulated endocytosis (9, 11). A considerable amount of evidence has now accumulated supporting the occurrence of sodium pump translocation. There are a number of research laboratories that have demonstrated hormonal and contraction-stimulated translocation of Na+-K+-ATPase in skeletal muscle utilizing a variety of different experimental techniques (1, 2, 6–8, 10, 12, 13, 15, and 16). These results are based on membrane fractionation using different techniques, and measurements have not been based only on the assessment of ouabain binding but also on assessment of sodium pump abundance with specific antibodies.

As highlighted by these ongoing discussions, there is a further need to investigate the precise molecular mechanisms involved. As methodologies improve, and novel, real-time, noninvasive techniques of membrane traffic monitoring develop further, we believe that future studies will bring new insights to this important topic of sodium pump membrane traffic in skeletal muscle.

FOOTNOTES


Address for reprint requests and other correspondence: A. V. Chibalin, Dept. of Molecular Medicine and Surgery, Integrative Physiology, Karolinska Institutet, SE 171 77 Stockholm, Sweden (e-mail: alexander.chibalin{at}ki.se)

REFERENCES

  1. Al-Khalili L, Kotova O, Tsuchida H, Ehren I, Feraille E, Krook A, Chibalin AV. ERK1/2 mediates insulin stimulation of Na+-K+-ATPase by phosphorylation of the alpha-subunit in human skeletal muscle cells. J Biol Chem 279: 25211–25218, 2004.[Abstract/Free Full Text]
  2. Al-Khalili L, Yu M, Chibalin AV. Na+-K+-ATPase trafficking in skeletal muscle: insulin stimulates translocation of both {alpha}1- and {alpha}2-subunit isoforms. FEBS Lett 536: 198–202, 2003.[CrossRef][Web of Science][Medline]
  3. Benziane B, Chibalin AV. Skeletal muscle sodium pump regulation: a translocation paradigm. Am J Physiol Endocrinol Metab (April 28, 2008); doi:10.1152/ajpendo.90261.2008.[Abstract/Free Full Text]
  4. Clausen T. Regulatory role of translocation of Na+-K+ pumps in skeletal muscle: hypothesis or reality? Am J Physiol Endocrinol Metab; doi:10.1152/ajpendo.90494.2008.[Free Full Text]
  5. Erlij D, Grinstein S. The number of sodium ion pumping sites in skeletal muscle and its modification by insulin. J Physiol 259: 13–31, 1976.[Abstract/Free Full Text]
  6. Hundal HS, Marette A, Mitsumoto Y, Ramlal T, Blostein R, Klip A. Insulin induces translocation of the {alpha}2 and β1 subunits of the Na+-K+-ATPase from intracellular compartments to the plasma membrane in mammalian skeletal muscle. J Biol Chem 267: 5040–5043, 1992.[Abstract/Free Full Text]
  7. Juel C, Grunnet L, Holse M, Kenworthy S, Sommer V, Wulff T. Reversibility of exercise-induced translocation of Na+-K+ pump subunits to the plasma membrane in rat skeletal muscle. Pflügers Arch 443: 212–217, 2001.[CrossRef][Web of Science][Medline]
  8. Juel C, Nielsen JJ, Bangsbo J. Exercise-induced translocation of Na+-K+ pump subunits to the plasma membrane in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 278: R1107–R1110, 2000.[Abstract/Free Full Text]
  9. Kotova O, Al-Khalili L, Talia S, Hooke C, Fedorova OV, Bagrov AY, Chibalin AV. Cardiotonic steroids stimulate glycogen synthesis in human skeletal muscle cells via a Src- and ERK1/2-dependent mechanism. J Biol Chem 281: 20085–20094, 2006.[Abstract/Free Full Text]
  10. Lavoie L, He L, Ramlal T, Ackerley C, Marette A, Klip A. The GLUT4 glucose transporter and the {alpha}2 subunit of the Na+-K+-ATPase do not localize to the same intracellular vesicles in rat skeletal muscle. FEBS Lett 366: 109–114, 1995.[CrossRef][Web of Science][Medline]
  11. Liu J, Shapiro JI. Regulation of sodium pump endocytosis by cardiotonic steroids: molecular mechanisms and physiological implications. Pathophysiology 14: 171–181, 2007.[CrossRef][Medline]
  12. Marette A, Krischer J, Lavoie L, Ackerley C, Carpentier JL, Klip A. Insulin increases the Na+-K+-ATPase {alpha}2-subunit in the surface of rat skeletal muscle: morphological evidence. Am J Physiol Cell Physiol 265: C1716–C1722, 1993.[Abstract/Free Full Text]
  13. Omatsu-Kanbe M, Kitasato H. Insulin stimulates the translocation of Na+-K+-dependent ATPase molecules from intracellular stores to the plasma membrane in frog skeletal muscle. Biochem J 272: 727–733, 1990.[Web of Science][Medline]
  14. Ploug T, van Deurs B, Ai H, Cushman SW, Ralston E. Analysis of GLUT4 distribution in whole skeletal muscle fibers: identification of distinct storage sompartments that are recruited by insulin and muscle contractions. J Cell Biol 142: 1429–1446, 1998.[Abstract/Free Full Text]
  15. Sandiford SD, Green HJ, Ouyang J. Mechanisms underlying increases in rat soleus Na+-K+-ATPase activity by induced contractions. J Appl Physiol 99: 2222–2232, 2005.[Abstract/Free Full Text]
  16. Tsakiridis T, Wong PP, Liu Z, Rodgers CD, Vranic M, Klip A. Exercise increases the plasma membrane content of the Na+-K+ pump and its mRNA in rat skeletal muscles. J Appl Physiol 80: 699–705, 1996.[Abstract/Free Full Text]




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