Displacing hexokinase from mitochondrial voltage-dependent anion channel impairs GLT-1-mediated glutamate uptake but does not disrupt interactions between GLT-1 and mitochondrial proteins

Journal of Neuroscience Research

Volumn 93, Issue 7, 2015, Pages 999-1008

  Jackson, Joshua G ^a,b   O'Donnell, John C ^a,b   Krizman, Elizabeth ^a   Robinson, Michael B ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Glutamate transporter; Hexokinase; Mitochondria

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); GLUTAMIC ACID; HEXOKINASE 1; MITOCHONDRIAL PROTEIN; MOLECULAR SCAFFOLD; SODIUM GLUCOSE COTRANSPORTER 1; VOLTAGE DEPENDENT ANION CHANNEL; EXCITATORY AMINO ACID TRANSPORTER 2; HEXOKINASE; SLC1A2 PROTEIN, RAT;

ADULT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BINDING SITE; BRAIN CORTEX; BRAIN MITOCHONDRION; BRAIN SYNAPTOSOME; CONTROLLED STUDY; ENZYME LOCALIZATION; IMMUNOPRECIPITATION; IN VIVO STUDY; MALE; MASS SPECTROMETRY; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RAT; SEQUENCE HOMOLOGY; ANIMAL; CHEMISTRY; METABOLISM; SPRAGUE DAWLEY RAT; SYNAPTOSOME; ULTRASTRUCTURE;

ANIMALS; CEREBRAL CORTEX; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMIC ACID; HEXOKINASE; IMMUNOPRECIPITATION; MALE; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTOSOMES; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84929656077     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23533     Document Type: Article

References (63)

1. Abu-Hamad S, Zaid H, Israelson A, Nahon E, Shoshan-Barmatz V . 2008. Hexokinase-1 protection against apoptotic cell death is mediated via interaction with the voltage-dependent anion channel-1: mapping the site of binding. J Biol Chem 283:13482-13490.
2. Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA. 2008. Respiratory active mitochondrial supercomplexes. Mol Cell 32:529-539.
3. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG. 1994. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14:5559-5569.
4. Bauer DE, Jackson JG, Genda EN, Montoya MM, Yudkoff M, Robinson MB. 2012. The glutamate transporter GLAST participates in a macromolecular complex that supports glutamate metabolism. Neurochem Int 61:566-574.
5. BeltrandelRio H, Wilson JE. 1991. Hexokinase of rat brain mitochondria: relative importance of adenylate kinase and oxidative phosphorylation as sources of substrate ATP and interaction with intramitochondrial compartments of ATP and ADP. Arch Biochem Biophys 286:183-194.
6. Beutner G, Ruck A, Riede B, Brdiczka D. 1998. Complexes between porin, hexokinase, mitochondrial creatine kinase, and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. Biochim Biophys Acta 1368:7-18.
7. Buck CR, Jurynec MJ, Gupta DK, Law AK, Bilger J, Wallace DC, McKeon RJ. 2003. Increased adenine nucleotide translocator 1 in reactive astrocytes facilitates glutamate transport. Exp Neurol 181:149-158.
8. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA. 2008. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264-278.
9. Campanella ME, Chu H, Low PS. 2005. Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. Proc Natl Acad Sci U S A 102:2402-2407.
10. Chen W, Mahadomrongkul V, Berger UV, Bassan M, DeSilva T, Tanaka K, Irwin N, Aoki C, Rosenberg PA. 2004. The glutamate transporter GLT1a is expressed in excitatory terminals of mature hippocampal neurons. J Neurosci 24:1136-1148.
11. Crompton M, Virji S, Ward JM. 1998. Cyclophilin-D binding proteins. Biochem Soc Trans 26:S330.
12. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
13. Dienel GA. 2013. Astrocytic energetics during excitatory neurotransmission: what are contributions of glutamate oxidation and glycolysis? Neurochem Int 63:244-258.
14. Dienel GA, McKenna MC. 2014. A dogma-breaking concept: glutamate oxidation in astrocytes is the source of lactate during aerobic glycolysis in resting subjects. J Neurochem 131:395-398.
15. +-ATPase pump. Biochem J 460:353-361.
16. Furness DN, Dehnes Y, Akhtar AQ, Rossi DJ, Hamann M, Grutle NJ, Gundersen V, Holmseth S, Lehre KP, Ullensvang K, Wojewodzic M, Zhou Y, Attwell D, Danbolt NC. 2008. A quantitative assessment of glutamate uptake into hippocampal synaptic terminals and astrocytes: new insights into a neuronal role for excitatory amino acid transporter 2 (EAAT2). Neuroscience 157:80-94.
17. Genda EN, Jackson JG, Sheldon AL, Locke SF, Greco TM, O'Donnell JC, Spruce LA, Xiao R, Guo W, Putt M, Seeholzer S, Ischiropoulos H, Robinson MB. 2011. Co-compartmentalization of the astroglial glutamate transporter GLT-1 with glycolytic enzymes and mitochondria. J Neurosci 31:18275-18288.
18. Hamai M, Minokoshi Y, Shimazu T. 1999. L-glutamate and insulin enhance glycogen synthesis in cultured astrocytes from the rat brain through different intracellular mechanisms. J Neurochem 73:400-407.
19. Haugeto Ø, Ullensveng K, Levy LM, Chaudhry FA, Honore T, Neilsen M, Lehre KP, Danbolt NC. 1996. Brain glutamate transporter proteins form homomultimers. J Biol Chem 271:27715-27722.
20. Herman MA, Jahr CE. 2007. Extracellular glutamate concentration in hippocampal slice. J Neurosci 27:9736-9741.
21. Huang Y, Zuo Z. 2005. Isoflurane induces a protein kinase Ca-dependent increase in cell surface protein level and activity of glutamate transporter type 3. Mol Pharmacol 67:1522-1533.
22. Illarionava NB, Brismar H, Aperia A, Gunnarson E. 2014. Role of Na, K-ATPase alpha1 and alpha2 isoforms in the support of astrocyte glutamate uptake. PLoS One 9:e98469.
23. Jabaudon D, Scanziani M, Gähwiler BH, Gerber U. 2000. Acute decrease in net glutamate upatke during energy failure. Proc Natl Acad Sci U S A 97:5610-5615.
24. Jackson JG, O'Donnell JC, Takano H, Coulter DA, Robinson MB. 2014. Neuronal activity and glutamate uptake decrease mitochondrial mobility in astrocytes and position mitochondria near glutamate transporters. J Neurosci 34:1613-1624.
25. Kerner J, Lee K, Tandler B, Hoppel CL. 2012. VDAC proteomics: posttranslation modifications. Biochim Biophys Acta 1818:1520-1525.
26. Lehre KP, Danbolt NC. 1998. The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18:8751-8757.
27. Levitan IB. 2006. Signaling protein complexes associated with neuronal ion channels. Nat Neurosci 9:305-310.
28. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF. 2004. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24:4070-4081.
29. Linden M, Gellerfors P, Nelson BD. 1982. Pore protein and the hexokinase-binding protein from the outer membrane of rat liver mitochondria are identical. FEBS Lett 141:189-192.
30. Loaiza A, Porras OH, Barros LF. 2003. Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23:7337-7342.
31. 2+ exchanger and excitatory amino acid transporters in brain and heart cell models. Mol Pharmacol 84:603-614.
32. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gottlob K, Chandel NS, Thompson CB, Robey RB, Hay N. 2004. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16:819-830.
33. McKenna MC, Sonnewald U, Huang X, Stevenson J, Zielke HR. 1996. Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J Neurochem 66:386-393.
34. Mercer RW, Dunham PB. 1981. Membrane-bound ATP fuels the Na/K pump. Studies on membrane-bound glycolytic enzymes on inside-out vesicles from human red cell membranes. J Gen Physiol 78:547-568.
35. Nakashima RA, Mangan PS, Colombini M, Pedersen PL. 1986. Hexokinase receptor complex in hepatoma mitochondria: evidence from N, N′-dicyclohexylcarbodiimide-labeling studies for the involvement of the pore-forming protein VDAC. Biochemistry 25:1015-1021.
36. Parker JC, Hoffman JF. 1967. The role of membrane phosphoglycerate kinase in the control of glycolytic rate by active cation transport in human red blood cells. J Gen Physiol 50:893-916.
37. Pastorino JG, Shulga N, Hoek JB. 2002. Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J Biol Chem 277:7610-7618.
38. Pellerin L, Magistretti PJ. 1994. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91:10625-10629.
39. +-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J Neurochem 69:2132-2137.
40. Robinson MB. 1999. The family of sodium-dependent glutamate transporters: a focus on the GLT-1/EAAT2 subtype. Neurochem Int 33:479-491.
41. 3H]glutamate transport processes in rat brain. Brain Res 544:196-202.
42. Rodrigues-Ferreira C, da Silva AP, Galina A. 2012. Effect of the antitumoral alkylating agent 3-bromopyruvate on mitochondrial respiration: role of mitochondrially bound hexokinase. J Bioenerg Biomembr 44:39-49.
43. Rose EM, Koo JC, Antflick JE, Ahmed SM, Angers S, Hampson DR. 2009. Glutamate transporter coupling to Na, K-ATPase. J Neurosci 29:8143-8155.
44. Rossi DJ, Oshima T, Attwell D. 2000. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-321.
45. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW. 1994. Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
46. Schmoll D, Fuhrmann E, Gebhardt R, Hamprecht B. 1995. Significant amounts of glycogen are synthesized from 3-carbon compounds in astroglial primary cultures from mice with participation of the mitochondrial phosphoenolpyruvate carboxykinase isoenzyme. Eur J Biochem 227:308-315.
47. Schousboe A. 1981. Transport and metabolism of glutamate and GABA in neurons are glial cells. Int Rev Neurobiol 22:1-45.
48. Shan D, Mount D, Moore S, Haroutunian V, Meador-Woodruff JH, McCullumsmith RE. 2014. Abnormal partitioning of hexokinase 1 suggests disruption of a glutamate transport protein complex in schizophrenia. Schizophr Res 154:1-13.
49. Shoshan-Barmatz V, Golan M. 2012. Mitochondrial VDAC1: function in cell life and death and a target for cancer therapy. Curr Med Chem 19:714-735.
50. Sickmann HM, Walls AB, Schousboe A, Bouman SD, Waagepetersen HS. 2009. Functional significance of brain glycogen in sustaining glutamatergic neurotransmission. J Neurochem 109(Suppl 1):80-86.
51. Sonnewald U, McKenna M. 2002. Metabolic compartmentation in cortical synaptosomes: influence of glucose and preferential incorporation of endogenous glutamate into GABA. Neurochem Res 27:43-50.
52. Sui D, Wilson JE. 1997. Structural determinants for the intracellular localization of the isozymes of mammalian hexokinase: intracellular localization of fusion constructs incorporating structural elements from the hexokinase isozymes and the green fluorescent protein. Arch Biochem Biophys 345:111-125.
53. Sukumaran SK, Fu NY, Tin CB, Wan KF, Lee SS, Yu VC. 2010. A soluble form of the pilus protein FimA targets the VDAC-hexokinase complex at mitochondria to suppress host cell apoptosis. Mol Cell 37:768-783.
54. Swanson RA, Yu AC, Chan PH, Sharp FR. 1990. Glutamate increases glycogen content and reduces glucose utilization in primary astrocyte culture. J Neurochem 54:490-496.
55. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K. 1997. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276:1699-1702.
56. Ugbode CI, Hirst WD, Rattray M. 2014. Neuronal influences are necessary to produce mitochondrial colocalization with glutamate transporters in astrocytes. J Neurochem 130:668-677.
57. Vyssokikh MY, Brdiczka D. 2003. The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism and apoptosis. Acta Biochim Pol 50:389-404.
58. Vyssokikh MY, Katz A, Rueck A, Wuensch C, Dorner A, Zorov DB, Brdiczka D. 2001. Adenine nucleotide translocator isoforms 1 and 2 are differently distributed in the mitochondrial inner membrane and have distinct affinities to cyclophilin D. Biochem J 358:349-358.
59. Whitelaw BS, Robinson MB. 2013. Inhibitors of glutamate dehydrogenase block sodium-dependent glutamate uptake in rat brain membranes. Front Endocrinol 4:123.
60. Yamamoto T, Yamada A, Watanabe M, Yoshimura Y, Yamazaki N, Yoshimura Y, Yamauchi T, Kataoka M, Nagata T, Terada H, Shinohara Y. 2006. VDAC1, having a shorter N-terminus than VDAC2 but showing the same migration in an SDS-polyacrylamide gel, is the predominant form expressed in mitochondria of various tissues. J Proteome Res 5:3336-3344.
61. Yu AC, Schousboe A, Hertz L. 1982. Metabolic fate of 14C-labeled glutamate in astrocytes in primary cultures. J Neurochem 39:954-960.
62. Zaid H, Talior-Volodarsky I, Antonescu C, Liu Z, Klip A. 2009. GAPDH binds GLUT4 reciprocally to hexokinase-II and regulates glucose transport activity. Biochem J 419:475-484.
63. Zerangue N, Kavanaugh MP. 1996. Flux coupling in a neuronal glutamate transporter. Nature 383:634-637.