Subcellular localization of hexokinases I and II directs the metabolic fate of glucose

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  John, Scott ^a   Weiss, James N ^a   Ribalet, Bernard ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; GLUCOSE 6 PHOSPHATE; GLYCOGEN; HEXOKINASE; HEXOKINASE 1; HEXOKINASE ISOENZYME; PROTEIN KINASE B; UNCLASSIFIED DRUG; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; GLUCOSE TRANSPORTER 1;

ANIMAL CELL; ARTICLE; CATABOLISM; CHO CELL; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; GLUCOSE METABOLISM; GLYCOGEN SYNTHESIS; GLYCOLYSIS; HUMAN; HUMAN CELL; METABOLIC REGULATION; MITOCHONDRION; NONHUMAN; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; ANIMAL; CELL FRACTIONATION; CELL MEMBRANE PERMEABILITY; CRICETULUS; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSFECTION; HAMSTER; METABOLISM; PROTEIN BINDING; RAT; TIME;

ANIMALS; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL MEMBRANE PERMEABILITY; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSOL; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE-6-PHOSPHATE; GLYCOGEN; HEXOKINASE; MITOCHONDRIA; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SUBCELLULAR FRACTIONS; TIME FACTORS; TRANSFECTION;

EID: 79952417296     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017674     Document Type: Article

References (30)

1. Lowry OH, Passonneau JV, (1964) The Relationships between Substrates and Enzymes of Glycolysis in Brain. J Biol Chem 239: 31-42.
2. Purich DL, Fromm HJ, (1971) The kinetics and regulation of rat brain hexokinase. J Biol Chem 246: 3456-3463.
3. Mandarino LJ, Printz RL, Cusi KA, Kinchington P, O'Doherty RM, et al. (1995) Regulation of hexokinase II and glycogen synthase mRNA, protein, and activity in human muscle. Am J Physiol 269: E701-708.
4. Postic C, Leturque A, Printz RL, Maulard P, Loizeau M, et al. (1994) Development and regulation of glucose transporter and hexokinase expression in rat. Am J Physiol 266: E548-559.
5. Depre C, Vanoverschelde JL, Taegtmeyer H, (1999) Glucose for the heart. Circulation 99: 578-588.
6. Schulz AR, (1998) Control analysis of muscle glycogen metabolism. Arch Biochem Biophys 353: 172-180.
7. Syed NA, Khandelwal RL, (2000) Reciprocal regulation of glycogen phosphorylase and glycogen synthase by insulin involving phosphatidylinositol-3 kinase and protein phosphatase-1 in HepG2 cells. Mol Cell Biochem 211: 123-136.
8. Ferrer JC, Favre C, Gomis RR, Fernandez-Novell JM, Garcia-Rocha M, et al. (2003) Control of glycogen deposition. FEBS Lett 546: 127-132.
9. Wilson JE, (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057.
10. Galluzzi L, Kepp O, Tajeddine N, Kroemer G, (2008) Disruption of the hexokinase-VDAC complex for tumor therapy. Oncogene 27: 4633-4635.
11. Gimenez-Cassina A, Lim F, Cerrato T, Palomo GM, Diaz-Nido J, (2009) Mitochondrial hexokinase II promotes neuronal survival and acts downstream of glycogen synthase kinase-3. J Biol Chem 284: 3001-3011.
12. Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB, et al. (2001) Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 15: 1406-1418.
13. Majewski N, Nogueira V, Robey RB, Hay N, (2004) Akt inhibits apoptosis downstream of BID cleavage via a glucose-dependent mechanism involving mitochondrial hexokinases. Mol Cell Biol 24: 730-740.
14. Miyamoto S, Murphy AN, Brown JH, (2008) Akt mediates mitochondrial protection in cardiomyocytes through phosphorylation of mitochondrial hexokinase-II. Cell Death Differ 15: 521-529.
15. Pastorino JG, Hoek JB, Shulga N, (2005) Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res 65: 10545-10554.
16. Rose IA, Warms JV, (1967) Mitochondrial hexokinase. Release, rebinding, and location. J Biol Chem 242: 1635-1645.
17. Skaff DA, Kim CS, Tsai HJ, Honzatko RB, Fromm HJ, (2005) Glucose 6-phosphate release of wild-type and mutant human brain hexokinases from mitochondria. J Biol Chem 280: 38403-38409.
18. 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.
19. Jurczak MJ, Danos AM, Rehrmann VR, Brady MJ, (2008) The role of protein translocation in the regulation of glycogen metabolism. J Cell Biochem 104: 435-443.
20. Cifuentes D, Martinez-Pons C, Garcia-Rocha M, Galina A, Ribas de Pouplana L, et al. (2008) Hepatic glycogen synthesis in the absence of glucokinase: the case of embryonic liver. J Biol Chem 283: 5642-5649.
21. Azoulay-Zohar H, Israelson A, Abu-Hamad S, Shoshan-Barmatz V, (2004) In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. Biochem J 377: 347-355.
22. de Cerqueira Cesar M, Wilson JE, (2002) Functional characteristics of hexokinase bound to the type a and type B sites of bovine brain mitochondria. Arch Biochem Biophys 397: 106-112.
23. Ellison WR, Lueck JD, Fromm HJ, (1975) Studies on the mechanism of orthophosphate regulation of bovine brain hexokinase. J Biol Chem 250: 1864-1871.
24. Fang TY, Alechina O, Aleshin AE, Fromm HJ, Honzatko RB, (1998) Identification of a phosphate regulatory site and a low affinity binding site for glucose 6-phosphate in the N-terminal half of human brain hexokinase. J Biol Chem 273: 19548-19553.
25. Fehr M, Lalonde S, Lager I, Wolff MW, Frommer WB, (2003) In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. J Biol Chem 278: 19127-19133.
26. John SA, Ottolia M, Weiss JN, Ribalet B, (2008) Dynamic modulation of intracellular glucose imaged in single cells using a FRET-based glucose nanosensor. Pflugers Arch 456: 307-322.
27. Lerin C, Montell E, Berman HK, Newgard CB, Gomez-Foix AM, (2000) Overexpression of protein targeting to glycogen in cultured human muscle cells stimulates glycogen synthesis independent of glycogen and glucose 6-phosphate levels. J Biol Chem 275: 39991-39995.
28. Aleshin AE, Zeng C, Bartunik HD, Fromm HJ, Honzatko RB, (1998) Regulation of hexokinase I: crystal structure of recombinant human brain hexokinase complexed with glucose and phosphate. J Mol Biol 282: 345-357.
29. Sun L, Shukair S, Naik TJ, Moazed F, Ardehali H, (2008) Glucose phosphorylation and mitochondrial binding are required for the protective effects of hexokinases I and II. Mol Cell Biol 28: 1007-1017.
30. Taylor AJ, Ye JM, Schmitz-Peiffer C, (2006) Inhibition of glycogen synthesis by increased lipid availability is associated with subcellular redistribution of glycogen synthase. J Endocrinol 188: 11-23.