Regulatory mechanisms for glycogenolysis and K+ uptake in brain astrocytes

Neurochemistry International

Volumn 63, Issue 5, 2013, Pages 458-464

  Dinuzzo, Mauro ^a   Mangia, Silvia ^b   Maraviglia, Bruno ^c,d   Giove, Federico ^a,c  

^a MUSEO STORICO DELLA FISICA E CENTRO STUDI E RICERCHE ENRICO FERMI   (Italy)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Astrocytes; ATPase; Glycogen; Glycogen phosphorylase; Na+ K +; Potassium

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COTRANSPORTER; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE KINASE 3; PROTEIN KINASE;

ASTROCYTE; GLYCOGEN METABOLISM; GLYCOGENOLYSIS; HUMAN; INTRACELLULAR SIGNALING; ION TRANSPORT; PHOSPHORYLATION; POTASSIUM TRANSPORT; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

1,4-DIDEOXY-1,4-IMINO-D-ARABINITOL; 4,4′-DIISOTHIOCYANOSTILBENE-2,2′-DISULFONIC ACID; AE; AMP-ACTIVATED PROTEIN KINASE; AMPK; ANION EXCHANGER; ASTROCYTES; CA; CAMP-DEPENDENT PROTEIN KINASE A; CARBONIC ANHYDRASE; CARDIOTONIC STEROIDS; CTS; DAB; DIDS; EGFR; EPIDERMAL GROWTH FACTOR RECEPTOR; ERK; EXTRACELLULAR NA(+) LEVEL SENSITIVE NA(+) CHANNEL; EXTRACELLULAR-SIGNAL REGULATED KINASE; GBD; GLYCOGEN; GLYCOGEN BINDING DOMAIN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3; GP; GS; GSK3; INOSITOL TRISPHOSPHATE RECEPTOR; IP3R; L-TYPE VOLTAGE-DEPENDENT CA(2+) CHANNEL; LCC; MEK; MITOGEN-ACTIVATED PROTEIN AND EXTRACELLULAR-SIGNAL REGULATED KINASE; NA(+)/ COTRANSPORTER; NA(+)/CA(2+) EXCHANGER; NA(+)/K(+) ATPASE; NA(+)/K(+)/2CL(-) COTRANSPORTER; NAX; NBC; NCX; NKA; NKCC; PDE; PHK; PHOSPHATIDYLINOSITIDE 3-KINASE; PHOSPHODIESTERASE; PHOSPHOLIPASE C; PHOSPHORYLASE KINASE; PI3K; PKA; PKB/AKT; PKC; PLC; POTASSIUM; PROTEIN KINASE B; PROTEIN KINASE C; RAF; RAPIDLY ACCELERATED FIBROSARCOMA; RAS; RAT SARCOMA; SAC; SOLUBLE ADENYLATE CYCLASE.;

ASTROCYTES; BRAIN; GLYCOGEN; POTASSIUM;

EID: 84883529735     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2013.08.004     Document Type: Review

References (75)

1. O. Aizman, and A. Aperia Na, K-ATPase as a signal transducer Ann. NY Acad. Sci. 986 2003 489 496
2. M.A. Baker, L. Hetherington, and R.J. Aitken Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa J. Cell Sci. 119 2006 3182 3192 (Pubitemid 44322132)
3. P. Beguin, G. Crambert, F. Monnet-Tschudi, M. Uldry, J.D. Horisberger, H. Garty, and K. Geering FXYD7 is a brain-specific regulator of Na, K-ATPase alpha 1-beta isozymes EMBO J. 21 2002 3264 3273 (Pubitemid 34760559)
4. A. Bogdelis, R. Treinys, E. Stankevicius, J. Jurevicius, and V.A. Skeberdis Src family protein tyrosine kinases modulate L-type calcium current in human atrial myocytes Biochem. Biophys. Res. Commun. 413 2011 116 121
5. M.L. Brines, and R.J. Robbins Cell-type specific expression of Na+, K(+)-ATPase catalytic subunits in cultured neurons and glia: evidence for polarized distribution in neurons Brain Res. 631 1993 1 11 (Pubitemid 23351479)
6. N. Brookes, and R.J. Turner K(+)-induced alkalinization in mouse cerebral astrocytes mediated by reversal of electrogenic Na(+)- HCO 3 - cotransport Am. J. Physiol. 267 1994 C1633 C1640
7. R.J. Brushia, and D.A. Walsh Phosphorylase kinase: the complexity of its regulation is reflected in the complexity of its structure Front. Biosci. 4 1999 D618 D641
8. X.J. Cheng, G. Fisone, O. Aizman, R. Aizman, R. Levenson, P. Greengard, and A. Aperia PKA-mediated phosphorylation and inhibition of Na(+)-K(+)-ATPase in response to beta-adrenergic hormone Am. J. Physiol. 273 1997 C893 C901
9. M. Chesler, and K. Kaila Modulation of pH by neuronal activity Trends Neurosci. 15 1992 396 402
10. H.B. Choi, G.R. Gordon, N. Zhou, C. Tai, R.L. Rungta, J. Martinez, T.A. Milner, J.K. Ryu, J.G. McLarnon, M. Tresguerres, L.R. Levin, J. Buck, and B.A. MacVicar Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl cyclase Neuron 75 2012 1094 1104
11. G. Crambert, and K. Geering FXYD proteins: new tissue-specific regulators of the ubiquitous Na, K-ATPase Sci STKE 2003 2003 RE1
12. G. Crambert, U. Hasler, A.T. Beggah, C. Yu, N.N. Modyanov, J.D. Horisberger, L. Lelievre, and K. Geering Transport and pharmacological properties of nine different human Na, K-ATPase isozymes J. Biol. Chem. 275 2000 1976 1986 (Pubitemid 30060824)
13. M.M. Crerar, O. Karlsson, R.J. Fletterick, and P.K. Hwang Chimeric muscle and brain glycogen phosphorylases define protein domains governing isozyme-specific responses to allosteric activation J. Biol. Chem. 270 1995 13748 13756
14. M. DiNuzzo Kinetic analysis of glycogen turnover: relevance to human brain 13C-NMR spectroscopy J. Cereb. Blood Flow Metab. 2013 in print
15. M. DiNuzzo, S. Mangia, B. Maraviglia, and F. Giove Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: evidence from mathematical modeling J. Cereb. Blood Flow Metab. 30 2010 586 602
16. M. DiNuzzo, B. Maraviglia, and F. Giove Why does the brain (not) have glycogen? BioEssays 33 2011 319 326
17. M. DiNuzzo, S. Mangia, B. Maraviglia, and F. Giove The role of astrocytic glycogen in supporting the energetics of neuronal activity Neurochem. Res. 37 2012 2432 2438
18. S. Duffy, and B.A. MacVicar Potassium-dependent calcium influx in acutely isolated hippocampal astrocytes Neuroscience 61 1994 51 61 (Pubitemid 24199510)
19. W.O. Fenn THE deposition of potassium and phosphate with glycogen in rat livers J. Biol. Chem. 128 1939 297 308
20. E. Fridman, D. Lichtstein, and H. Rosen Formation of new high density glycogen-microtubule structures is induced by cardiac steroids J. Biol. Chem. 287 2012 6518 6529
21. K. Geering Function of FXYD proteins, regulators of Na, K-ATPase J. Bioenerg. Biomembr. 37 2005 387 392 (Pubitemid 43725163)
22. - cotransporter activity in rat skeletal muscle and intestinal epithelial cells Tsitologiia 45 2003 812 816
23. T. Grisar, J.M. Frere, and G. Franck Effect of K+ ions on kinetic properties of the (Na+, K+)-ATPase (EC 3.6.1.3) of bulk isolated glial cells, perikarya and synaptosomes from rabbit brain cortex Brain Res. 165 1979 87 103 (Pubitemid 9148698)
24. D. Guenard, M. Morange, and H. Buc Comparative study of the effect of 5′ AMP and its analogs on rabbit glycogen phosphorylase b isoenzymes Eur. J. Biochem. 76 1977 447 452 (Pubitemid 8112675)
25. M. Haas, A. Askari, and Z. Xie Involvement of Src and epidermal growth factor receptor in the signal-transducing function of Na+/K+-ATPase J. Biol. Chem. 275 2000 27832 27837
26. I. Hajek, K.V. Subbarao, and L. Hertz Acute and chronic effects of potassium and noradrenaline on Na+, K+-ATPase activity in cultured mouse neurons and astrocytes Neurochem. Int. 28 1996 335 342 (Pubitemid 26063023)
27. D.G. Hardie, D. Carling, and S.J. Gamblin AMP-activated protein kinase: also regulated by ADP? Trends Biochem. Sci. 36 2011 470 477
28. S. He, A. Ruknudin, L.L. Bambrick, W.J. Lederer, and D.H. Schulze Isoform-specific regulation of the Na+/Ca2+ exchanger in rat astrocytes and neurons by PKA J. Neurosci. 18 1998 4833 4841 (Pubitemid 28285392)
29. J.W. Hell Beta-adrenergic regulation of the L-type Ca2+ channel Ca(V)1.2 by PKA rekindles excitement Sci. Signal. 3 2010 pe33
30. L. Hertz, and W.E. Code Calcium channel signalling in astrocytes R. Paoletti, T. Godfraind, P.M. Vankoullen, Caclium Antagonists: Pharmacology and Clinical Research 1993 Kluwer 205 213
31. L. Hertz, L. Peng, and G.A. Dienel Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis J. Cereb. Blood Flow Metab. 27 2007 219 249 (Pubitemid 46148451)
32. P.R. Hof, E. Pascale, and P.J. Magistretti K+ at concentrations reached in the extracellular space during neuronal activity promotes a Ca2+-dependent glycogen hydrolysis in mouse cerebral cortex J. Neurosci. 8 1988 1922 1928
33. O. Kotova, L. Al-Khalili, S. Talia, C. Hooke, O.V. Fedorova, A.Y. Bagrov, and A.V. Chibalin Cardiotonic steroids stimulate glycogen synthesis in human skeletal muscle cells via a Src- and ERK1/2-dependent mechanism J. Biol. Chem. 281 2006 20085 20094 (Pubitemid 44065783)
34. S.L. Longnus, R.B. Wambolt, H.L. Parsons, R.W. Brownsey, and M.F. Allard 5-Aminoimidazole-4-carboxamide 1-beta-d-ribofuranoside (AICAR) stimulates myocardial glycogenolysis by allosteric mechanisms Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 2003 R936 R944
35. O.H. Lowry, D.W. Schulz, and J.V. Passonneau The kinetics of glycogen phosphorylases from brain and muscle J. Biol. Chem. 242 1967 271 280
36. V. Madelian, and E. La Vigne Rapid regulation of a cyclic AMP-specific phosphodiesterase (PDE IV) by forskolin and isoproterenol in LRM55 astroglial cells Biochem. Pharmacol. 51 1996 1739 1747 (Pubitemid 26176730)
37. S. Mangia, F. Giove, I. Tkac, N.K. Logothetis, P.G. Henry, C.A. Olman, B. Maraviglia, F. Di Salle, and K. Ugurbil Metabolic and hemodynamic events after changes in neuronal activity: current hypotheses, theoretical predictions and in vivo NMR experimental findings J. Cereb. Blood Flow Metab. 29 2009 441 463
38. S. Mangia, F. Giove, and M. DiNuzzo K(+) homeostasis in the brain: a new role for glycogenolysis Neurochem. Res. 38 2013 470 471
39. A. McBride, S. Ghilagaber, A. Nikolaev, and D.G. Hardie The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor Cell Metab. 9 2009 23 34
40. K.M. McGrail, J.M. Phillips, and K.J. Sweadner Immunofluorescent localization of three Na, K-ATPase isozymes in the rat central nervous system: both neurons and glia can express more than one Na, K-ATPase J. Neurosci. 11 1991 381 391
41. S. Meuth, H.C. Pape, and T. Budde Modulation of Ca2+ currents in rat thalamocortical relay neurons by activity and phosphorylation Eur. J. Neurosci. 15 2002 1603 1614 (Pubitemid 35471917)
42. A. Miyakawa-Naito, P. Uhlen, M. Lal, O. Aizman, K. Mikoshiba, H. Brismar, S. Zelenin, and A. Aperia Cell signaling microdomain with Na, K-ATPase and inositol 1,4,5-trisphosphate receptor generates calcium oscillations J. Biol. Chem. 278 2003 50355 50361 (Pubitemid 37548878)
43. J.S. Munzer, S.E. Daly, E.A. Jewell-Motz, J.B. Lingrel, and R. Blostein Tissue- and isoform-specific kinetic behavior of the Na, K-ATPase J. Biol. Chem. 269 1994 16668 16676 (Pubitemid 24200424)
44. E.A. Newman Glial cell regulation of extracellular potassium H. Kettenmann, B.R. Ransom, Neuroglia 1995 Oxford University Press 717 731
45. Y. Obara, K. Labudda, T.J. Dillon, and P.J. Stork PKA phosphorylation of Src mediates Rap1 activation in NGF and cAMP signaling in PC12 cells J. Cell Sci. 117 2004 6085 6094 (Pubitemid 40123973)
46. G. Oz, E.R. Seaquist, A. Kumar, A.B. Criego, L.E. Benedict, J.P. Rao, P.-G. Henry, P.-F.V.D. Moortele, and R. Gruetter Human brain glycogen content and metabolism: implications on its role in brain energy metabolism Am. J. Physiol. Endocrinol. Metab. 292 2007 E946 E951
47. E. Ozawa Regulation of phosphorylase kinase by low concentrations of Ca ions upon muscle contraction: the connection between metabolism and muscle contraction and the connection between muscle physiology and Ca-dependent signal transduction Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 87 2011 486 508
48. L. Peng, T. Du, J. Xu, D. Song, B. Li, M. Zhang, and L. Hertz Adrenergic and V1-ergic agonists/antagonists affecting recovery from brain trauma in the Lund project act on astrocytes Curr. Signal Transduct. Ther. 7 2012 43 55
49. B. Pfeiffer-Guglielmi, B. Fleckenstein, G.n. Jung, and B. Hamprecht Immunocytochemical localization of glycogen phosphorylase isozymes in rat nervous tissues by using isozyme-specific antibodies J. Neurochem. 85 2003 73 81 (Pubitemid 36389696)
50. D. Plourde, and S.P. Soltoff Ouabain potentiates the activation of ERK1/2 by carbachol in parotid gland epithelial cells; inhibition of ERK1/2 reduces Na(+)-K(+)-ATPase activity Am. J. Physiol. Cell Physiol. 290 2006 C702 C710
51. G. Polekhina, A. Gupta, B.J. Michell, B. van Denderen, S. Murthy, S.C. Feil, I.G. Jennings, D.J. Campbell, L.A. Witters, M.W. Parker, B.E. Kemp, and D. Stapleton AMPK beta subunit targets metabolic stress sensing to glycogen Curr. Biol. 13 2003 867 871 (Pubitemid 36573256)
52. K.J. Poppen, D.M. Green, and H.T. Wrenn The histochemical localization of potassium and glycogen J. Histochem. Cytochem. 1 1953 160 173
53. B.R. Ransom Glial modulation of neural excitability mediated by extracellular pH: a hypothesis Prog. Brain Res. 94 1992 37 46 (Pubitemid 23026634)
54. C.B. Ransom, B.R. Ransom, and H. Sontheimer Activity-dependent extracellular K+ accumulation in rat optic nerve: the role of glial and axonal Na+ pumps J. Physiol. 522 Pt 3 2000 427 442 (Pubitemid 30088555)
55. A. Reynolds, A. Parris, L.A. Evans, S. Lindqvist, P. Sharp, M. Lewis, R. Tighe, and M.R. Williams Dynamic and differential regulation of NKCC1 by calcium and cAMP in the native human colonic epithelium J. Physiol. 582 2007 507 524 (Pubitemid 47040541)
56. P.J. Roach Glycogen and its metabolism Curr. Mol. Med. 2 2002 101 120 (Pubitemid 34649835)
57. P.J. Roach, A.A. Depaoli-Roach, T.D. Hurley, and V.S. Tagliabracci Glycogen and its metabolism: some new developments and old themes Biochem J 441 2012 763 787
58. H. Rosen, V. Glukmann, T. Feldmann, E. Fridman, and D. Lichtstein Short-term effects of cardiac steroids on intracellular membrane traffic in neuronal NT2 cells Cell Mol Biol (Noisy-le-grand) 52 2006 78 86 (Pubitemid 46799709)
59. I. Ruminot, R. Gutierrez, G. Pena-Munzenmayer, C. Anazco, T. Sotelo-Hitschfeld, R. Lerchundi, M.I. Niemeyer, G.E. Shull, and L.F. Barros NBCe1 mediates the acute stimulation of astrocytic glycolysis by extracellular K+ J. Neurosci. 31 2011 14264 14271
60. W. Schoner, and G. Scheiner-Bobis Endogenous and exogenous cardiac glycosides: their roles in hypertension, salt metabolism, and cell growth Am. J. Physiol. Cell Physiol. 293 2007 C509 C536
61. T. Shibayama, K. Nakaya, and Y. Nakamura Differential binding activity of erythrocyte ankyrin to the alpha-subunits of Na+, K(+)-ATPases from rat cerebral and axonal membrane Cell Struct. Funct. 18 1993 79 85 (Pubitemid 23139629)
62. J.C. Skou The influence of some cations on an adenosine triphosphatase from peripheral nerves Biochim. Biophys. Acta 23 1957 394 401
63. J.C. Skou The identification of the sodium pump Biosci. Rep. 24 2004 436 451
64. K.V. Subbarao, J.U. Stolzenburg, and L. Hertz Pharmacological characteristics of potassium-induced, glycogenolysis in astrocytes Neurosci. Lett. 196 1995 45 48
65. N. Svichar, S. Esquenazi, A. Waheed, W.S. Sly, and M. Chesler Functional demonstration of surface carbonic anhydrase IV activity on rat astrocytes Glia 53 2006 241 247 (Pubitemid 43221346)
66. J. Tian, X. Gong, and Z. Xie Signal-transducing function of Na+-K+-ATPase is essential for ouabain's effect on [Ca2+]i in rat cardiac myocytes Am. J. Physiol. Heart Circ. Physiol. 281 2001 H1899 H1907
67. D. Ververken, P. Van Veldhoven, C. Proost, H. Carton, and H. De Wulf On the role of calcium ions in the regulation of glycogenolysis in mouse brain cortical slices J. Neurochem. 38 1982 1286 1295 (Pubitemid 12091488)
68. S. Walcott, and S.L. Lehman Enzyme kinetics of muscle glycogen phosphorylase b Biochemistry 46 2007 11957 11968 (Pubitemid 47623764)
69. W. Walz Role of Na/K/Cl cotransport in astrocytes Can. J. Physiol. Pharmacol. 70 Suppl. 1992 S260 S262
70. F. Wang, Q. Xu, W. Wang, T. Takano, and M. Nedergaard Bergmann glia modulate cerebellar Purkinje cell bistability via Ca2+-dependent K+ uptake Proc. Natl. Acad. Sci. USA 109 2012 7911 7916
71. F. Wang, N.A. Smith, Q. Xu, T. Fujita, A. Baba, T. Matsuda, T. Takano, L. Bekar, and M. Nedergaard Astrocytes modulate neural network activity by Ca(2)+-dependent uptake of extracellular K+ Sci. Signal. 5 2012 ra26
72. J.A. Wong, A.R. Gosmanov, E.G. Schneider, and D.B. Thomason Insulin-independent, MAPK-dependent stimulation of NKCC activity in skeletal muscle Am. J. Physiol. Regul. Integr. Comp. Physiol. 281 2001 R561 R571
73. J. Xu, D. Song, Z. Xue, L. Gu, L. Hertz, and L. Peng Requirement of glycogenolysis for uptake of increased extracellular K(+) in astrocytes: potential implications for K (+) homeostasis and glycogen usage in brain Neurochem. Res. 38 2013 472 485
74. Y. Yan, R.J. Dempsey, and D. Sun Expression of Na(+)-K(+)-Cl(-) cotransporter in rat brain during development and its localization in mature astrocytes Brain Res. 911 2001 43 55 (Pubitemid 32728237)
75. J.S. Yu, and S.D. Yang Phosphorylation/activation of phosphorylase b kinase by cAMP/Ca2(+)-independent, autophosphorylation-dependent protein kinase Biochem. Biophys. Res. Commun. 207 1995 140 147