Extracellular potassium homeostasis: insights from hypokalemic periodic paralysis.

Extracellular potassium makes up only about 2% of the total body's potassium store. The majority of the body potassium is distributed in the intracellular space, of which about 80% is in skeletal muscle. Movement of potassium in and out of skeletal muscle thus plays a pivotal role in extracellular potassium homeostasis. The exchange of potassium between the extracellular space and skeletal muscle is mediated by specific membrane transporters. These include potassium uptake by Na(+), K(+)-adenosine triphosphatase and release by inward-rectifier K(+) channels. These processes are regulated by circulating hormones, peptides, ions, and by physical activity of muscle as well as dietary potassium intake. Pharmaceutical agents, poisons, and disease conditions also affect the exchange and alter extracellular potassium concentration. Here, we review extracellular potassium homeostasis, focusing on factors and conditions that influence the balance of potassium movement in skeletal muscle. Recent findings that mutations of a skeletal muscle-specific inward-rectifier K(+) channel cause hypokalemic periodic paralysis provide interesting insights into the role of skeletal muscle in extracellular potassium homeostasis. These recent findings are reviewed.

[1]  D. Kullmann,et al.  Voltage sensor charge loss accounts for most cases of hypokalemic periodic paralysis , 2009, Neurology.

[2]  T. Clausen,et al.  The effect of catecholamines on Na—K transport and membrane potential in rat soleus muscle , 1977, The Journal of physiology.

[3]  B. Phakdeekitcharoen,et al.  Thyroid Hormone Increases mRNA and Protein Expression of Na+-K+-ATPase α2 and β1 Subunits in Human Skeletal Muscles , 2007 .

[4]  Yuh-Feng Lin,et al.  Laboratory tests to determine the cause of hypokalemia and paralysis. , 2004, Archives of internal medicine.

[5]  N. Madias,et al.  Drug‐Induced Hyperkalemia , 1985, Medicine.

[6]  K. Kjeldsen,et al.  Effect of K-depletion on 3H-ouabain binding and Na-K-contents in mammalian skeletal muscle. , 1984, Acta physiologica Scandinavica.

[7]  T. Clausen Na+-K+ pump regulation and skeletal muscle contractility. , 2003, Physiological reviews.

[8]  T. Clausen Clearance of Extracellular K+ during Muscle Contraction—Roles of Membrane Transport and Diffusion , 2008, The Journal of general physiology.

[9]  I. Schaafsma,et al.  Exercise-induced hyperkalemia in hypothyroid dogs. , 2002, Domestic animal endocrinology.

[10]  E. Reuveny,et al.  Mechanism of Ba2+ block of a mouse inwardly rectifying K+ channel: differential contribution by two discrete residues , 2001, The Journal of physiology.

[11]  Zhe Lu,et al.  Mechanism of rectification in inward-rectifier K+ channels. , 2004, Annual review of physiology.

[12]  R. DeFronzo,et al.  Extrarenal potassium homeostasis. , 1981, The American journal of physiology.

[13]  T. Clausen Regulatory role of translocation of Na+-K+ pumps in skeletal muscle: hypothesis or reality? , 2008, American Journal of Physiology. Endocrinology and Metabolism.

[14]  W. Catterall,et al.  Gating pore current in an inherited ion channelopathy , 2007, Nature.

[15]  H. Glitsch,et al.  Activation of the cAMP–protein kinase A pathway facilitates Na+ translocation by the Na+–K+ pump in guinea‐pig ventricular myocytes , 2000, The Journal of physiology.

[16]  Shih-Hua Lin Thyrotoxic periodic paralysis. , 2005, Mayo Clinic proceedings.

[17]  A. Chibalin,et al.  Na+,K+‐ATPase trafficking in skeletal muscle: insulin stimulates translocation of both α1‐ and α2‐subunit isoforms , 2003 .

[18]  Anuj K. Dalal,et al.  Acquired long QT syndrome and monomorphic ventricular tachycardia after alternative treatment with cesium chloride for brain cancer. , 2004, Mayo Clinic proceedings.

[19]  L. Ptáček,et al.  Mutations in Potassium Channel Kir2.6 Cause Susceptibility to Thyrotoxic Hypokalemic Periodic Paralysis , 2010, Cell.

[20]  F. N. Lee,et al.  Independent regulation of in vivo insulin action on glucose versus K(+) uptake by dietary fat and K(+) content. , 2002, Diabetes.

[21]  J C SKOU,et al.  The influence of some cations on an adenosine triphosphatase from peripheral nerves. , 1957, Biochimica et biophysica acta.

[22]  C. Juel Na+-K+-ATPase in rat skeletal muscle: muscle fiber-specific differences in exercise-induced changes in ion affinity and maximal activity. , 2009, American journal of physiology. Regulatory, integrative and comparative physiology.

[23]  S. Cannon Voltage‐sensor mutations in channelopathies of skeletal muscle , 2010, The Journal of physiology.

[24]  Y. Marunaka,et al.  Apparent affinity changes induced by insulin of Na-K transport system in frog skeletal muscle. , 1980, The Japanese journal of physiology.

[25]  G. Ebers,et al.  A novel sodium channel mutation in a family with hypokalemic periodic paralysis , 1999, Neurology.

[26]  C. Juel,et al.  Na+,K+-ATPase Na+ Affinity in Rat Skeletal Muscle Fiber Types , 2010, Journal of Membrane Biology.

[27]  K. Håkansson,et al.  Structure and mechanism of Na,K-ATPase: functional sites and their interactions. , 2003, Annual review of physiology.

[28]  T. Clausen Role of Na+,K+‐pumps and transmembrane Na+,K+‐distribution in muscle function , 2008, Acta physiologica.

[29]  K. Kjeldsen,et al.  EFFECT OF THYROID FUNCTION ON NUMBER OF Na-K PUMPS IN HUMAN SKELETAL MUSCLE , 1984, The Lancet.

[30]  K. Takeyasu,et al.  Regulation of the sodium pump in excitable cells. , 1987, Kidney international. Supplement.

[31]  V. Thakur,et al.  From profound hypokalemia to life-threatening hyperkalemia: a case of barium sulfide poisoning. , 2000, Archives of internal medicine.

[32]  M. Lindinger Potassium regulation during exercise and recovery in humans: implications for skeletal and cardiac muscle. , 1995, Journal of molecular and cellular cardiology.

[33]  Sugden Al,et al.  Effects of high potassium or low sodium diet on vascular Na+,K+-ATPase activity and blood pressure in young spontaneously hypertensive rats. , 1987 .

[34]  H. Ravn,et al.  The concentration of sodium,potassium pumps in chronic obstructive lung disease (COLD) patients: the impact of magnesium depletion and steroid treatment , 1997, Journal of internal medicine.

[35]  Andrew G. Engel,et al.  Dihydropyridine receptor mutations cause hypokalemic periodic paralysis , 1994, Cell.

[36]  A. McDonough,et al.  Glucocorticoids increase sodium pump α2- and β1-subunit abundance and mRNA in rat skeletal muscle , 2001 .

[37]  J C SKOU,et al.  ENZYMATIC BASIS FOR ACTIVE TRANSPORT OF NA+ AND K+ ACROSS CELL MEMBRANE. , 1965, Physiological reviews.

[38]  J. Youn,et al.  Recent advances in understanding integrative control of potassium homeostasis. , 2009, Annual review of physiology.

[39]  P. Hopkins,et al.  Skeletal muscle physiology , 2006 .

[40]  J. Lingrel,et al.  Regulation of the Human Na/K-ATPase β1 Gene Promoter by Mineralocorticoid and Glucocorticoid Receptors* , 1998, The Journal of Biological Chemistry.

[41]  T. Clausen Clinical and therapeutic significance of the Na+,K+ pump*. , 1998, Clinical science.

[42]  G. Sjøgaard,et al.  Water and ion shifts in skeletal muscle of humans with intense dynamic knee extension. , 1985, The American journal of physiology.

[43]  S. Mandal,et al.  Identification of thyroid regulatory elements in the Na-K-ATPase α3 gene promoter , 2001, Molecular Biology Reports.

[44]  E. Vicaut,et al.  Hypokalaemia related to acute chloroquine ingestion , 1995, The Lancet.

[45]  K. Kjeldsen,et al.  Quantification of the maximum capacity for active sodium‐potassium transport in rat skeletal muscle. , 1987, The Journal of physiology.

[46]  G. Giebisch,et al.  Effects of pH on potassium: new explanations for old observations. , 2011, Journal of the American Society of Nephrology : JASN.

[47]  R. Shieh,et al.  Extracellular K+ elevates outward currents through Kir2.1 channels by increasing single-channel conductance. , 2011, Biochimica et biophysica acta.

[48]  Christian Derst,et al.  Heteromerization of Kir2.x potassium channels contributes to the phenotype of Andersen's syndrome , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  J. Youn,et al.  Role of muscle in regulating extracellular [K+]. , 2005, Seminars in nephrology.

[50]  B. Surawicz Factors affecting tolerance to digitalis. , 1985, Journal of the American College of Cardiology.

[51]  K. Kjeldsen,et al.  Exercise‐induced hyperkalaemia can be reduced in human subjects by moderate training without change in skeletal muscle Na, K‐ATPase concentration , 1990, European journal of clinical investigation.

[52]  R. Chaisson,et al.  Cocaine use and HIV infection in intravenous drug users in San Francisco. , 1989, JAMA.

[53]  V. Chatsudthipong,et al.  Aldosterone increases Na+‐K+‐ATPase activity in skeletal muscle of patients with Conn’s syndrome , 2011, Clinical endocrinology.

[54]  L. Hayward,et al.  Na+,K+-pump stimulation improves contractility in isolated muscles of mice with hyperkalemic periodic paralysis , 2011, The Journal of general physiology.

[55]  M. Neil,et al.  Hypokalaemia with severe rebound hyperkalaemia after therapeutic barbiturate coma. , 2009, Anesthesia and analgesia.

[56]  J. Castro-Tavares Effects of isoprenaline and phenylephrine on plasma potassium: role of the liver. , 1975, Archives internationales de pharmacodynamie et de therapie.

[57]  N. Sperelakis,et al.  Isoproterenol‐ and insulin‐induced hyperpolarization in rat skeletal muscle , 1993, Journal of cellular physiology.

[58]  S. Cannon,et al.  Identification and Functional Characterization of Kir2.6 Mutations Associated with Non-familial Hypokalemic Periodic Paralysis* , 2011, The Journal of Biological Chemistry.

[59]  F. Lehmann-Horn,et al.  Sodium channelopathies of skeletal muscle result from gain or loss of function , 2010, Pflügers Archiv - European Journal of Physiology.

[60]  Shih-Hua Lin,et al.  Mechanism of thyrotoxic periodic paralysis. , 2012, Journal of the American Society of Nephrology : JASN.

[61]  A. S. Allen Pa Ping, or Kiating Paralysis. , 1943 .

[62]  S. Subramony,et al.  Mutations in Kir2.1 Cause the Developmental and Episodic Electrical Phenotypes of Andersen's Syndrome , 2001, Cell.

[63]  N. Robertson,et al.  Identification of a mineralocorticoid/glucocorticoid response element in the human Na/K ATPase alpha1 gene promoter. , 1999, Biochemical and biophysical research communications.

[64]  L. Pott,et al.  Altered stress stimulation of inward rectifier potassium channels in Andersen‐Tawil syndrome , 2012, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[65]  R. DeFronzo,et al.  Effect of graded doses of insulin on splanchnic and peripheral potassium metabolism in man. , 1980, The American journal of physiology.

[66]  Paul R Shorten,et al.  Anomalous ion diffusion within skeletal muscle transverse tubule networks , 2007, Theoretical Biology and Medical Modelling.

[67]  D. Galuska,et al.  Altered expression and insulin-induced trafficking of Na+-K+-ATPase in rat skeletal muscle: effects of high-fat diet and exercise. , 2009, American journal of physiology. Endocrinology and metabolism.

[68]  M. Perazella,et al.  Drug-induced hyperkalemia: old culprits and new offenders. , 2000, The American journal of medicine.

[69]  J. H. Johnson,et al.  Muscle cell electrical hyperpolarization and reduced exercise hyperkalemia in physically conditioned dogs. , 1985, The Journal of clinical investigation.

[70]  D. Green,et al.  Homeostatic potassium excretion in fed and fasted sheep. , 1988, The American journal of physiology.

[71]  G Sjøgaard,et al.  Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. , 2000, Physiological reviews.

[72]  T. Clausen,et al.  Effects of adrenal steroids on the concentration of Na(+)-K+ pumps in rat skeletal muscle. , 1997, The Journal of endocrinology.

[73]  M. Weber,et al.  K+-dependent paradoxical membrane depolarization and Na+ overload, major and reversible contributors to weakness by ion channel leaks , 2009, Proceedings of the National Academy of Sciences.

[74]  T. Clausen,et al.  β2‐ADRENOCEPTORS MEDIATE THE STIMULATING EFFECT OF ADRENALINE ON ACTIVE ELECTROGENIC NA‐K‐TRANSPORT IN RAT SOLEUS MUSCLE , 1980 .

[75]  M. Tang,et al.  Thyroid hormone specifically regulates skeletal muscle Na+-K+-ATPase α2- and β2-isoforms , 1993 .

[76]  Kazuharu Furutani,et al.  Inwardly rectifying potassium channels: their structure, function, and physiological roles. , 2010, Physiological reviews.

[77]  V. Basrur,et al.  Isolation and characterization of BetaM protein encoded by ATP1B4--a unique member of the Na,K-ATPase β-subunit gene family. , 2011, Biochemical and biophysical research communications.

[78]  T. Clausen Hormonal and pharmacological modification of plasma potassium homeostasis , 2010, Fundamental & clinical pharmacology.

[79]  V. J. VanTassell,et al.  Acute barium poisoning with respiratory failure and rhabdomyolysis. , 1991, Annals of emergency medicine.

[80]  S. Cannon,et al.  Paradoxical depolarization of BA2+‐ treated muscle exposed to low extracellular K+: Insights into resting potential abnormalities in hypokalemic paralysis , 2008, Muscle & nerve.