The Cerebellum

, 6:130 | Cite as

Fructose metabolism in the cerebellum

  • Vincent A. Funari
  • James E. Crandall
  • Dean R. Tolan
Review Article Scientific Papers

Abstract

Under normal physiological conditions, the brain utilizes only a small number of carbon sources for energy. Recently, there is growing molecular and biochemical evidence that other carbon sources, including fructose, may play a role in neuroenergetics. Fructose is the number one commercial sweetener in Western civilization with large amounts of fructose being toxic, yet fructose metabolism remains relatively poorly characterized. Fructose is purportedly metabolizedvia either of two pathways, the fructose-1-phosphate pathway and/or the fructose-6-phosphate pathway. Many early metabolic studies could not clearly discriminate which of these two pathways predominates, nor could they distinguish which cell types in various tissues are capable of fructose metabolism. In addition, the lack of good physiological models, the diet-induced changes in gene expression in many tissues, the involvement of multiple genes in multiple pathways involved in fructose metabolism, and the lack of characterization of some genes involved in fructose metabolism have complicated our understanding of the physiological role of fructose in neuro-energetics. A recent neuro-metabolism study of the cerebellum demonstrated fructose metabolism and co-expression of the genes specific for the fructose 1-phosphate pathway, GLUT5 (glut5) and ketohexokinase (khk), in Purkinje cells suggesting this as an active pathway in specific neurons? Meanwhile, concern over the rapid increase in dietary fructose, particularly among children, has increased awareness about how fructose is metabolizedin vivo and what effects a high fructose diet might have. In this regard, establishment of cellular and molecular studies and physiological characterization of the important and/or deleterious roles fructose plays in the brain is critical. This review will discuss the status of fructose metabolism in the brain with special reference to the cerebellum and the physiological roles of the different pathways.

Key words

Energy metabolism sugar transporters ischemia cell-specific metabolism fructose degradation 

References

  1. 1.
    Yudkin J, Kang SS, Bruckdorfer KR. Effects of high dietary sugar. Br Med J. 1980;281:1396.PubMedGoogle Scholar
  2. 2.
    Anderson TA. Recent trends in carbohydrate consumption. Annu Rev Nutr. 1982;2:113–32.PubMedGoogle Scholar
  3. 3.
    Cox TM. The genetic consequences of our sweet tooth. Nat Rev Genet. 2002;3:481–7.PubMedGoogle Scholar
  4. 4.
    Steinmann B, Gitzelmann R, Van denBerghe G. In: Scriver C, Beaudet A, Sly W, Valle D, editors. Disorders of fructose metabolism. The metabolic and molecular basis of inherited disease.. 8th ed, New York: McGraw-Hill, Inc, 2001. pp 1489–520.Google Scholar
  5. 5.
    Mayes PA. Intermediary metabolism of fructose. Am J Clin Nutr. 1993;58:754S-65S.PubMedGoogle Scholar
  6. 6.
    Gaby AR. Adverse effects of dietary fructose. Altern Med Rev. 2005;10:294–306.PubMedGoogle Scholar
  7. 7.
    Katzen HM, Schimke RT. Multiple forms of hexokinase in the rat: Tissue distribution, age dependency, and properties. Proc Natl Acad Sci USA. 1965;54:1218–25.PubMedGoogle Scholar
  8. 8.
    Froesch ER, Ginsberg JL. Fructose metabolism of adipose tissue. I. Comparison of fructose and glucose metabolism in epidiymal adipose tissues of normal rats. J Biol Chem. 1962;237:3317–23.PubMedGoogle Scholar
  9. 9.
    Beyer PL, Caviar EM, McCallum RW. Fructose intake at current levels in the United States may cause gastrointestinal distress in normal adults. J Am Diet Assoc. 2005;105: 1559–66.PubMedGoogle Scholar
  10. 10.
    Perheentupa J, Raivio K. Fructose-induced hyperuricaemia. Lancet. 1967;2:528–31.PubMedGoogle Scholar
  11. 11.
    Bergstrom J, Hultman E, Roch-Norlund AE. Lactic acid accumulation in connection with fructose infusion. Acta Med Scand. 1968;184:359–64.PubMedGoogle Scholar
  12. 12.
    Hers H. Misuses for Fructose. Nature. 1979;227:241.Google Scholar
  13. 13.
    Woods H, Alberti K. Dangers of intravenous fructose. Lancet. 1972;2:1354.PubMedGoogle Scholar
  14. 14.
    Sestoft L. Fructose-en advarsel. Ugeskr Laeger. 1972;134: 571.PubMedGoogle Scholar
  15. 15.
    Baker SS, Cochran WJ, Greer FR, Heyman MB, Jacobson MS, Jaksic T, et al. The use and misuse of fruit juice in pediatrics. Pediatrics. 2001;107:1210–13.Google Scholar
  16. 16.
    Gerrits PM, Tsalikian E. Diabetes and fructose metabolism. Am J Clin Nutr. 1993;58:796S-9S.PubMedGoogle Scholar
  17. 17.
    Silverman M. Structure and function of hexose transporters. Annu Rev Biochem. 1991;60:757–94.PubMedGoogle Scholar
  18. 18.
    Gould GW, Thomas HM, Jess TJ, Bell GI. Expression of human glucose transporters in Xenopus oocytes: Kinetic characterization and substrate specificities of the erythrocyte, liver, and brain isoforms. Biochemistry. 1991;30: 5139–45.PubMedGoogle Scholar
  19. 19.
    Miyamoto K, Tatsumi S, Morimoto A, Minami H, Yamamoto H, Sone K, et al. Characterization of the rabbit intestinal fructose transporter (GLUT5). Biochem J. 1994;303:877–83.PubMedGoogle Scholar
  20. 20.
    Burant CF, Takeda J, Brot-Laroche E, Bell GI, Davidson NO. Fructose transporter in human spermatozoa and small intestine is GLUT5. J Biol Chem. 1992;267: 14523–6.PubMedGoogle Scholar
  21. 21.
    Kayano T, Burant CF, Fukumoto H, Gould GW, Fan YS, Eddy RL, et al. Human facilitative glucose transporters. Isolation, functional characterization, and gene localization of cDNAs encoding an isoform (GLUT5) expressed in small intestine, kidney, muscle, and adipose tissue and an unusual glucose transporter pseudogene-like sequence (GLUT6). J Biol Chem. 1990;265:13276–82.PubMedGoogle Scholar
  22. 22.
    Wood IS, Trayhurn P. Glucose transporters (GLUT and SGLT): Expanded families of sugar transport proteins. Br J Nutr. 2003;89:3–9.PubMedGoogle Scholar
  23. 23.
    Wood IS, Hunter L, Trayhurn P. Expression of Class III facilitative glucose transporter genes (GLUT-10 and GLUT-12) in mouse and human adipose tissues. Biochem Biophys Res Commun. 2003;308:43–9.PubMedGoogle Scholar
  24. 24.
    Joost HG, Thorens B. The extended GLUT-family of sugar/ polyol transport facilitators: Nomenclature, sequence characteristics, and potential function of its novel members (review). Mol Membr Biol. 2001;18:247–56.PubMedGoogle Scholar
  25. 25.
    Phay JE, Hussain HB, Moley JF. Cloning and expression analysis of a novel member of the facilitative glucose transporter family, SLC2A9 (GLUT9). Genomics. 2000;66: 217–20.PubMedGoogle Scholar
  26. 26.
    Johnson JH, Newgard CB, Milburn JL, Lodish HF, Thorens B. The high Km glucose transporter of islets of Langerhans is functionally similar to the low affinity transporter of liver and has an identical primary sequence. J Biol Chem. 1990;265:6548–51.PubMedGoogle Scholar
  27. 27.
    Hers H-G. Le métabolisme du fructose. Brussels: Editions Arsica, 1957.Google Scholar
  28. 28.
    Hers H, Kusaka T. Le Métabolisme du fructose 1-phosphate dans le foie. Biochim Biophys Acta. 1953;11: 427–32.PubMedGoogle Scholar
  29. 29.
    Jenkins BT, Hajra AK. Glycerol kinase and dihydroxyacetone kinase in rat brain. J Neurochem. 1976;26:377–85.PubMedGoogle Scholar
  30. 30.
    Grivell AR, Halls HJ, Berry MN. Role of mitochondria in hepatic fructose metabolism. Biochim Biophys Acta. 1991;1059:45–54.PubMedGoogle Scholar
  31. 31.
    Duran M, Beemer FA, Bruinvis L, Ketting D, Wadman SK. D-glyceric acidemia: An inborn error associated with fructose metabolism. Pediat Res. 1987;21:502–06.PubMedGoogle Scholar
  32. 32.
    Purich DL, Fromm HJ, Rudolph FB. The hexokinases: kinetic, physical, and regulatory properties. Adv Enzymol Relat Areas Mol Biol. 1973;39:249–326.PubMedGoogle Scholar
  33. 33.
    Cardenas ML, Rabajille E, Niemeyer H. Fructose is a good substrate for rat liver ‘glucokinase’ (hexokinase D). Biochem J. 1984;222:363–70.PubMedGoogle Scholar
  34. 34.
    Lebherz HG, Rutter WJ. Distribution of fructose diphosphate aldolase variants in biological systems. Biochemistry. 1969;8:109–21.PubMedGoogle Scholar
  35. 35.
    Penhoet EE, Kochman M, Rutter WJ. Isolation of fructose diphosphate aldolases A, B, and C. Biochemistry. 1969;8: 4391–95.PubMedGoogle Scholar
  36. 36.
    Malay AD, Procious SL, Tolan DR. The temperature dependence of activity and structure for the most prevalent mutant aldolase B associated with hereditary fructose intolerance. Arch Biochem Biophys. 2002;408:295–304.PubMedGoogle Scholar
  37. 37.
    Morris AJ, Tolan DR. Site-directed mutagenesis identifies aspartate 33 as a previously unidentified critical residue in the catalytic mechanism of rabbit aldolase A. J Biol Chem. 1993;268:1095–100.PubMedGoogle Scholar
  38. 38.
    Arakaki TL, Pezza JA, Cronin MA, Hopkins CE, Zimmer DB, Tolan DR, et al. Structure of human brain fructose 1,6-bisphosphate aldolase: Linking isozyme structure with function. Protein Sci. 2004;13:3077–84.PubMedGoogle Scholar
  39. 39.
    Penhoet EE, Kochman M, Rutter WJ. Molecular and catalytic properties of aldolase C. Biochemistry. 1969;8: 4396–402.PubMedGoogle Scholar
  40. 40.
    Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF, Jr. Brain metabolism during fasting. J Clin Invest. 1967;46:1589–95.PubMedGoogle Scholar
  41. 41.
    Hawkins RA, Williamson DH, Krebs HA. Ketone-body utilization by adult and suckling rat brain in vivo. Biochem J. 1971;122:13–18.PubMedGoogle Scholar
  42. 42.
    Magistretti P. In: Squire LR, Bloom FE, McConnell SK, Roberts JL, Spitzer NC, editors. Brain energy metabolism. Fundamental neuroscience. 2nd ed, New York: Academic Press, 2003. pp 339–360.Google Scholar
  43. 43.
    Weber M, deOliveira K, Valle S, Schweigert I, Rotta L, Fagundes I, et al. Study of developmental changes on hexoses metabolism in rat cerebral cortex. Neurochem Res. 2001;26:161–6.PubMedGoogle Scholar
  44. 44.
    Wada H, Okada Y, Uzuo T, Nakamura H. The effects of glucose, mannose, fructose and lactate on the preservation of neural activity in the hippocampal slices from the guinea pig. Brain Res. 1998;788:144–50.PubMedGoogle Scholar
  45. 45.
    Saitoh M, Okada Y, Nabetani M. Effect of mannose, fructose and lactate on the preservation of synaptic potentials in hippocampal slices. Neurosci Lett. 1994;171: 125–8.PubMedGoogle Scholar
  46. 46.
    Allen L, Anderson S, Wender R, Meakin P, Ransom BR, Ray DE, et al. Fructose supports energy metabolism of some, but not all, axons in adult mouse optic nerve. J Neurophysiol. 2006;95:1917–25.PubMedGoogle Scholar
  47. 47.
    Pellerin L, Magistretti P. Neuroenergetics: Calling upon astrocytes to satisfy hungry neurons. Neuroscientist. 2004;l0:53–62.Google Scholar
  48. 48.
    Wiesinger H, Thiess U, Hamprecht B. Sorbitol pathway activity and utilization of polyols in astroglia-rich primary cultures. Glia. 1990;3:277–82.PubMedGoogle Scholar
  49. 49.
    Bergbauer K, Dringen R, Verleysdonk S, Gebhardt R, Hamprecht B, Wiesinger H. Studies on fructose metabolism in cultured astroglial cells and control hepatocytes: lack of fructokinase activity and immunoreactivity in astrocytes. Dev Neurosci. 1996;18:371–9.PubMedGoogle Scholar
  50. 50.
    Allen NJ, Karadottir R, Attwell D. A preferential role for glycolysis in preventing the anoxic depolarization of rat hippocampal area CA1 pyramidal cells. J Neurosci. 2005;25: 848–59.PubMedGoogle Scholar
  51. 51.
    Chain EB, Rose SP, Masi I, Pocchiari F. Metabolism of hexoses in rat cerebral cortex slices. J Neurochem. 1969;16: 93–100.PubMedGoogle Scholar
  52. 52.
    Bais R, James HM, Rofe AM, Conyers RA. The purification and properties of human liver ketohexokinase. A role for ketohexokinase and fructose-bisphosphate aldolase in the metabolic production of oxalate from xylitol. Biochem J. 1985;230:53–60.PubMedGoogle Scholar
  53. 53.
    Haradahira T, Tanaka A, Maeda M, Kanazawa Y, Ichiya YI, Masuda K. Radiosynthesis, rodent biodistribution, and metabolism of l-deoxy-l-[18F]fluoro-D-fructose. Nucl Med Biol. 1995;22:719–25.PubMedGoogle Scholar
  54. 54.
    Watanabe M, Shimono R, Kihara T. The distribution of [U-14] Fructose in the mice studied by whole-body autoradiography. Acta Histochem Cytochem. 1981;14:153–62.Google Scholar
  55. 55.
    Mantych GJ, James DE, Devaskar SU. Jejunal/kidney glucose transporter isoform (Glut-5) is expressed in the human blood-brain barrier. Endocrinol. 1993;132:35–40.Google Scholar
  56. 56.
    Weiser MM, Quill H. Estimation of fructokinase (ketohexokinase) in crude tissue preparations. Methods Enzymol. 1975;41:61–3.PubMedGoogle Scholar
  57. 57.
    Adelman RC, Ballard FJ, Weinhouse S. Purification and properties of rat liver fructokinase. J Biol Chem. 1967;242: 3360–65.PubMedGoogle Scholar
  58. 58.
    Hayward BE, Bonthron DT. Structure and alternative splicing of the ketohexokinase gene. Eur J Biochem. 1998;257:85–91.PubMedGoogle Scholar
  59. 59.
    Funari VA, Herrera VLM, Freeman D, Tolan DR. Genes required for fructose metabolism are expressed in purkinje cells in the cerebellum. Molec Brain Res. 2005;142:115–22.PubMedGoogle Scholar
  60. 60.
    McKenna MC. Introduction: Metabolic trafficking comes of age in the decade of the brain. Dev Neurosci. 1996;18: 333–5.PubMedGoogle Scholar
  61. 61.
    Pellerin L, Magistretti PJ. Excitatory amino acids stimulate aerobic glycolysis in astrocytes via an activation of the Na+/ K+ATPase. Dev Neurosci. 1996;18:336–42.PubMedGoogle Scholar
  62. 62.
    Kishi K, Tanaka T, Igawa M, Takase S, Goda T. Sucraseisomaltase and hexose transporter gene expressions are coordinately enhanced by dietary fructose in rat jejunum. J Nutr. 1999;129:953–6.PubMedGoogle Scholar
  63. 63.
    Gouyon F, Caillaud L, Carriere V, Klein C, Dalet V, Citadelle D, et al. Simple-sugar meals target GLUT2 at enterocyte apical membranes to improve sugar absorption: A study in GLUT2-null mice. J Physiol. 2003; 552:823–32.PubMedGoogle Scholar
  64. 64.
    Payne J, Maher F, Simpson I, Mattice L, Davies P. Glucose transporter Glut5 expression in microglial cells. Glia. 1997;21:327–31.PubMedGoogle Scholar
  65. 65.
    Nualart F, Godoy A, Reinicke K. Expression of the hexose transporters GLUT1 and GLUT2 during the early development of the human brain. Brain Res. 1999;824:97–104.PubMedGoogle Scholar
  66. 66.
    Hundal HS, Darakhshan F, Kristiansen S, Blakemore SJ, Richter EA. GLUT5 expression and fructose transport in human skeletal muscle. Adv Exp Med Biol. 1998;441: 35–45.PubMedGoogle Scholar
  67. 67.
    Lal S, Szwergold BS, Kappler F, Brown T. Detection of fructose-3-phosphokinase activity in intact mammalian lenses by 31P NMR spectroscopy. J Biol Chem. 1993;268: 7763–7.PubMedGoogle Scholar
  68. 68.
    Cui XL, Jiang L, Ferraris RP. Regulation of rat intestinal GLUT2 mRNA abundance by luminal and systemic factors. Biochim Biophys Acta. 2003;1612:178–85.PubMedGoogle Scholar
  69. 69.
    Mesonero J, Matosin M, Cambier D, Rodriguez-Yoldi MJ, Brot-Laroche E. Sugar-dependent expression of the fructose transporter GLUT5 in Caco-2 cells. Biochem J. 1995;312 (Pt. 3):757–62.PubMedGoogle Scholar
  70. 70.
    Maher F, Vannucci SJ, Simpson IA. Glucose transport proteins in brain. FASEB J. 1994;8:1003–11.PubMedGoogle Scholar
  71. 71.
    Pellerin L, Magistretti PJ. How to balance the brain energy budget while spending glucose differently. J Physiol. 2003;546:325.PubMedGoogle Scholar
  72. 72.
    Boado RJ, Black KL, Pardridge WM. Gene expression of GLUT3 and GLUT1 glucose transporters in human brain tumors. Brain Res Mol Brain Res. 1994;27:51–57.PubMedGoogle Scholar
  73. 73.
    Vannucci SJ, Maher F, Simpson IA. Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia. 1997;21:2–21.PubMedGoogle Scholar
  74. 74.
    Maher F. Immunolocalization of GLUT1 and GLUT3 glucose transporters in primary cultured neurons and glia. J Neurosci Res. 1995;42:459–469.PubMedGoogle Scholar
  75. 75.
    Horikoshi Y, Sasaki A, Taguchi N, Maeda M, Tsukagoshi H, Sato K, et al. Human GLUT5 immunolabeling is useful for evaluating microglial status in neuropathological study using paraffin sections. Acta Neuropathol (Berl). 2003; 105:157–62.Google Scholar
  76. 76.
    Choeiri C, Staines W, Messier C. Immunohistochemical localization and quantification of glucose transporters in the mouse brain. Neurosci. 2002; 111:19–34.Google Scholar
  77. 77.
    Klein JR, Hurwitz R, Olsen NS. Distribution of intravenously injected fructose and glucose between blood and brain. J Biol Chem. 1946;164:509–12.Google Scholar
  78. 78.
    Thurston JH, Levy CA, Warren SK, Jones EM. Permeability of the blood-brain barrier to fructose and the anaerobic use of fructose in the brains of young mice. J Neurochem. 1972;19:1685–96.PubMedGoogle Scholar
  79. 79.
    Maher F, Vannucci SJ, Simpson IA. Glucose transporter isoforms in brain: Absence of GLUT3 from the blood-brain barrier. J Cereb Blood Flow Metab. 1993;13:342–5.PubMedGoogle Scholar
  80. 80.
    Arluison M, Quignon M, Nguyen P, Thorens B, Leloup C, Penicaud L. Distribution and anatomical localization of the glucose transporter 2 (GLUT2) in the adult rat brain — an immunohistochemical study. J Chem Neuroanat. 2004;28: 117–36.PubMedGoogle Scholar
  81. 81.
    Takata K. Glucose transporters in the transepithelial transport of glucose. J Elec Microscopy (Tokyo). 1996;45: 275–84.Google Scholar
  82. 82.
    Oldendorf WH. Brain uptake of radiolabeled amino acids, amines, and hexoses after arterial injection. Am J Physiol. 1971;221:1629–39.PubMedGoogle Scholar
  83. 83.
    Popovici T, Berwald-Netter Y, Vibert M, Kahn A, Skala H. Localization of aldolase C mRNA in brain cells. FEBS Lett. 1990;268:189–93.PubMedGoogle Scholar
  84. 84.
    Walther EU, Dichgans M, Maricich SM, Romito RR, Yang F, Dziennis S, et al. Genomic sequences of aldolase C (Zebrin II) direct lacZ expression exclusively in nonneuronal cells of transgenic mice. Proc Natl Acad Sci USA. 1998;95:2615–20.PubMedGoogle Scholar
  85. 85.
    Thompson RJ, Kynoch PA, Willson VJ. Cellular localization of aldolase C subunits in human brain. Brain Res. 1982;232: 489–93.PubMedGoogle Scholar
  86. 86.
    LeFevre P, Marshall J. Conformational specificity in a biological sugar transport system. Am J Physiol. 1958;194: 333–7.PubMedGoogle Scholar
  87. 87.
    Joost HG, Bell GI, Best JD, Birnbaum MJ, Charron MJ, Chen YT, et al. Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am J Physiol Endocrinol Metab. 2002;282:E974–976.PubMedGoogle Scholar
  88. 88.
    Doege H, Schurmann A, Bahrenberg G, Brauers A, Joost HG. GLUT8, a novel member of the sugar transport facilitator family with glucose transport activity. J Biol Chem. 2000;275:16275–80.PubMedGoogle Scholar
  89. 89.
    Doege H, Bocianski A, Scheepers A, Axer H, Eckel J, Joost HG, et al. Characterization of human glucose transporter (GLUT) 11 (encoded by SLC2A11), a novel sugar-transport facilitator specifically expressed in heart and skeletal muscle. Biochem J. 2001;359:443–9.PubMedGoogle Scholar
  90. 90.
    Doege H, Bocianski A, Joost HG, Schurmann A. Activity and genomic organization of human glucose transporter 9 (GLUT9), a novel member of the family of sugar-transport facilitators predominantly expressed in brain and leucocytes. Biochem J. 2000;350(Pt 3):771–6.PubMedGoogle Scholar
  91. 91.
    Augustin R, Carayannopoulos MO, Dowd LO, Phay JE, Moley JF, Moley KH. Identification and characterization of human glucose transporter-like protein-9 (GLUT9): Alternative splicing alters trafficking. J Biol Chem. 2004;279:16229–36.PubMedGoogle Scholar
  92. 92.
    Li Q, Manolescu A, Ritzel M, Yao S, Slugoski M, Young JD, et al. Cloning and functional characterization of the human GLUT7 isoform SLC2A7 from the small intestine. Am J Physiol Gastrointest Liver Physiol. 2004;287:G236–42.PubMedGoogle Scholar
  93. 93.
    Wu X, Li W, Sharma V, Godzik A, Freeze HH. Cloning and characterization of glucose transporter 11, a novel sugar transporter that is alternatively spliced in various tissues. Mol Genet Metab. 2002;76:37–45.PubMedGoogle Scholar
  94. 94.
    Manolescu A, Salas-Burgos AM, Fischbarg J, Cheeseman CI. Identification of a hydrophobic residue as a key determinant of fructose transport by the facilitative hexose transporter SLC2A7 (GLUT7). J Biol Chem. 2005;280:42978–83.PubMedGoogle Scholar
  95. 95.
    Lisinski I, Schurmann A, Joost HG, Cushman SW, AlHasani H. Targeting of GLUT6 (formerly GLUT9) and GLUT8 in rat adipose cells. Biochem J. 2001;358:517–22.PubMedGoogle Scholar
  96. 96.
    Raushel FM, Cleland WW. Bovine liver fructokinase: Purification and kinetic properties. Biochemistry. 1977;16: 2169–75.PubMedGoogle Scholar
  97. 97.
    Adelman RC, Morris HP, Weinhouse S. Fructokinase, triokinase, and aldolases in liver tumors of the rat. Cancer Res. 1967;27:2408–13.PubMedGoogle Scholar
  98. 98.
    Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA. 2004;101: 6062–7.PubMedGoogle Scholar
  99. 99.
    Funari VA.Novel Computational and Classical Molecular Biological Approaches to Discovering Alternative Sites of Fructose Metabolism in Mice and Man, Boston University: PhD Dissertation, 2001.Google Scholar
  100. 100.
    Baron CB, Ozaki S, Watanabe Y, Hirata M, LaBelle EF, Coburn RF. Inositol 1,4,5-trisphosphate binding to porcine tracheal smooth muscle aldolase. J Biol Chem. 1995;270: 20459–65.PubMedGoogle Scholar
  101. 101.
    Sarna JR, Larouche M, Marzban H, Sillitoe RV, Rancourt DE, Hawkes R. Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J Comp Neurol. 2003;456:279–91.PubMedGoogle Scholar
  102. 102.
    Hawkes R, Herrup K. Aldolase C/zebrin II and the regionalization of the cerebellum. J Mol Neurosci. 1995;6:147–58.PubMedGoogle Scholar
  103. 103.
    Ahn AH, Dziennis S, Hawkes R, Herrup K. The cloning of zebrin II reveals its identity with aldolase C. Development. 1994;120:2081–90.PubMedGoogle Scholar
  104. 104.
    Voogd J, Ruigrok TJ. Transverse and longitudinal patterns in the mammalian cerebellum. Prog Brain Res. 1997;114: 21–37.PubMedCrossRefGoogle Scholar
  105. 105.
    Brochu G, Maler L, Hawkes R. Zebrin II: A polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol. 1990;291:538–52.PubMedGoogle Scholar
  106. 106.
    Staugaitis SM, Zerlin M, Hawkes R, Levine JM, Goldman JE. Aldolase C/zebrin II expression in the neonatal rat forebrain reveals cellular heterogeneity within the subventricular zone and early astrocyte differentiation. J Neurosci. 2001;21:6195–205.PubMedGoogle Scholar
  107. 107.
    Beutler E, Guinto E. Dihydroxyacetone metabolism by human erythrocytes: Demonstration of triokinase activity and its characterization. Blood. 1973;41:559–68.PubMedGoogle Scholar
  108. 108.
    Miwa I, Kito Y, Okuda J. Purification and characterization of triokinase from porcine kidney. Prep Biochem. 1994;24: 203–23.PubMedGoogle Scholar
  109. 109.
    Akhtar N, Blomberg A, Adler L. Osmoregulation and protein expression in a pbs2delta mutant of Saccharomyces cerevisiae during adaptation to hypersaline stress. FEBS Lett. 1997;403:173–80.PubMedGoogle Scholar
  110. 110.
    Blomberg A. Osmoresponsive proteins and functional assessment strategies in Saccharomyces cerevisiae. Electrophor. 1997;18:1429–40.Google Scholar
  111. 111.
    Molin M, Norbeck J, Blomberg A. Dihydroxyacetone kinases in Saccharomyces cerevisiae are involved in detoxification of dihydroxyacetone. J Biol Chem. 2003;278: 1415–23.PubMedGoogle Scholar
  112. 112.
    Hagopian K, Ramsey JJ, Weindruch R. Fructose metabolizing enzymes from mouse liver: influence of age and caloric restriction. Biochim Biophys Acta. 2005;1721: 37–43.PubMedGoogle Scholar
  113. 113.
    Welsh JP, Yuen G, Placantonakis DG, Vu TQ, Haiss F, O’Hearn E, et al. Why do Purkinje cells die so easily after global brain ischemia? Aldolase C, EAAT4, and the cerebellar contribution to posthypoxic myoclonus. Adv Neurol. 2002;89:331–59.PubMedGoogle Scholar
  114. 114.
    Jordan J, Simandle S, Tulbert C, Busija D, Miller A. Fructose-fed rats are protected against ischemia/reperfusion injury. J Pharmacol Exp Ther. 2003;307:1007–11.PubMedGoogle Scholar
  115. 115.
    Joyeux-Faure M, Rossini E, Ribuot C, Faure P. Fructosefed rat hearts are protected against ischemia-reperfusion injury. Exp Biol Med (Maywood). 2006;231:456–62.Google Scholar
  116. 116.
    Rosenthal M, Sick TJ. Glycolytic and oxidative metabolic contributions to potassium ion transport in rat cerebral cortex. Can J Physiol Pharmacol. 1992;70(Suppl):S165–9.Google Scholar
  117. 117.
    Kelleher JA, Chan PH, Chan TY, Gregory GA. Energy metabolism in hypoxic astrocytes: Protective mechanism of fructose-l,6-bisphosphate. Neurochem Res. 1995;20: 785–92.PubMedGoogle Scholar
  118. 118.
    Sola A, Berrios M, Sheldon RA, Ferriero DM, Gregory GA. Fructose-1,6-bisphosphate after hypoxic ischemic injury is protective to the neonatal rat brain. Brain Res. 1996;741: 294–9.PubMedGoogle Scholar
  119. 119.
    Lazzarino G, Tavazzi B, Di Pierro D, Giardina B. Ischemia and reperfusion: Effect of fructose-l,6-bisphosphate. Free Radic Res Commun. 1992;16:325–39.PubMedGoogle Scholar
  120. 120.
    Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest. 2005;l15:500–08.Google Scholar
  121. 121.
    Kehrer JP. Concepts related to the study of reactive oxygen and cardiac reperfusion injury. Free Radic Res Commun. 1989;5:305–14.PubMedGoogle Scholar
  122. 122.
    Woods HF, Eggleston LV, Krebs HA. The cause of hepatic accumulation of fructose 1-phosphate on fructose loading. Biochem J. 1970;l19:501–10.Google Scholar
  123. 123.
    Farah V, Elased KM, Chen Y, Key MP, Cunha TS, Irigoyen MC, et al. Nocturnal hypertension in mice consuming a high fructose diet. Auton Neurosci. 2006;130:41–50.PubMedGoogle Scholar
  124. 124.
    Shu HJ, Isenberg K, Cormier RJ, Benz A, Zorumski CF. Expression of fructose sensitive glucose transporter in the brains of fructose-fed rats. Neurosci. 2006;140: 889–95.Google Scholar
  125. 125.
    Doyle SA, Tolan DR. Characterization of recombinant human aldolase B and purification by metal chelate chromatography. Biochem Biophys Res Commun. 1995;206:902–08.PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Vincent A. Funari
    • 1
  • James E. Crandall
    • 2
  • Dean R. Tolan
    • 1
  1. 1.Biology DepartmentBoston UniversityBoston MAUSA
  2. 2.E. Kennedy Shriver for Mental Retardation Center at the University of Massachusetts Medical SchoolWalthamUSA

Personalised recommendations