Fructose-2,6-bisphosphate is lower in copper deficient rat cerebellum despite higher content of phosphorylated AMP-activated protein kinase

Experimental Biology and Medicine

Volumn 233, Issue 10, 2008, Pages 1262-1270

  Gybina, Anna A ^a   Prohaska, Joseph R ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

AMPK; Citrate; Copper deficient; Fructose 2,6 bisphosphate; Rat, cerebellum

Indexed keywords

6 PHOSPHOFRUCTO 2 KINASE; CITRIC ACID; FRUCTOSE 2,6 BISPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LACTIC ACID; MESSENGER RNA; PROTEIN; AMP ACTIVATED PROTEIN KINASES; AMP-ACTIVATED PROTEIN KINASES; COPPER; FRUCTOSE 2,6-DIPHOSPHATE; FRUCTOSE BISPHOSPHATE; GLUCOSE; GLUCOSE 6 PHOSPHATE; ISOENZYME; LACTIC ACID DERIVATIVE; MULTIENZYME COMPLEX; PROTEIN SERINE THREONINE KINASE;

ANAEROBIC GLYCOLYSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CELL ENERGY; CEREBELLUM; CONTROLLED STUDY; COPPER DEFICIENCY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; GLUCOSE METABOLISM; NONHUMAN; PROTEIN CONTENT; PUP (RODENT); RAT; ANIMAL; DIET; GLYCOLYSIS; MALE; METABOLISM; MITOCHONDRION; PHOSPHORYLATION; PHYSIOLOGY;

EPICOCCUM; RATTUS;

ANIMALS; CEREBELLUM; COPPER; DIET; FRUCTOSEDIPHOSPHATES; GLUCOSE; GLUCOSE-6-PHOSPHATE; GLYCOLYSIS; ISOENZYMES; LACTATES; MALE; MITOCHONDRIA; MULTIENZYME COMPLEXES; PHOSPHOFRUCTOKINASE-2; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RATS; RNA, MESSENGER;

EID: 54549108051     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.3181/0804-RM-132     Document Type: Article

References (51)

1. Prohaska JR. Copper. In: Bowman BA, Russell RM, Eds. Present Knowledge in Nutrition. Washington, DC: International Life Sciences Institute, pp458-170, 2006.
2. Danks DM, Campbell PE, Stevens BJ, Mayne V, Cartwright E. Menkes's kinky hair syndrome. An inherited defect in copper absorption with widespread effects. Pediatrics 50:188-201, 1972.
3. Menkes JH, Alter M, Steigleder GK, Weakley DR, Sung JH. A sex- linked recessive disorder with retardation of growth, peculiar hair, and focal cerebral and cerebellar degeneration. Pediatrics 29:764-779, 1962.
4. Mercer JF. Menkes syndrome and animal models. Am J Clin Nutr 67: 1022S-1028S, 1998.
5. Prohaska JR, Wells WW. Copper deficiency in the developing rat brain: a possible model for Menkes' steely-hair disease. J Neurochem 23:91-98, 1974.
6. Everson GJ, Tsai HC, Wang TI. Copper deficiency in the guinea pig. J Nutr 93:533-540, 1967.
7. El Meskini R, Crabtree KL, Cline LB, Mains RE, Eipper BA, Ronnett GV. ATP7A (Menkes protein) functions in axonal targeting and synaptogenesis. Mol Cell Neurosci 34:409-421, 2007.
8. Prohaska JR. Changes in brain enzymes accompanying deficiencies of the trace elements, copper, selenium, or zinc. In: Howell JM, Gawthorne JM, White CL, Eds. Trace Element Metabolism in Man and Animals (TEMA-4). Canberra: Australian Academy of Science, pp275-282, 1981.
9. Zimmerman AW, Matthieu JM, Quarles RH, Brady RO, Hsu JM. Hypomyelination in copper-deficient rats. Prenatal and postnatal copper replacement. Arch Neurol 33:111-119, 1976.
10. Gybina AA, Prohaska JR. Copper deficiency results in AMP-activated protein kinase activation and acetyCoA carboxylase phosphorylation in rat cerebellum. Brain Res 1204:69-76, 2008.
11. Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1:15-25, 2005.
12. Marsin AS, Bertrand L, Rider MH, Deprez J, Beauloye C, Vincent MF, Van den Berghe G, Carling D, Hue L. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol 10:1247-1255, 2000.
13. Ramamurthy S, Ronnett GV. Developing a head for energy sensing: AMP-activated protein kinase as a multifunctional metabolic sensor in the brain. J Physiol 574:85-93, 2006.
14. Gybina AA, Prohaska JR. Increased rat brain cytochrome c correlates with degree of perinatal copper deficiency rather than apoptosis. J Nutr 133:3361-3368, 2003.
15. Gybina AA, Prohaska JR. Variable response of selected cuproproteins in rat choroid plexus and cerebellum following perinatal copper deficiency. Genes Nutr 1:51-60, 2006.
16. Prohaska JR, Wells WW. Copper deficiency in the developing rat brain: evidence for abnormal mitochondria. J Neurochem 25:221-228, 1975.
17. Rusinko N, Prohaska JR. Adenine nucleotide and lactate levels in organs from copper-deficient mice and brindled mice. J Nutr 115:936-943, 1985.
18. Markwell MA, Haas SM, Bieber LL, Tolbert NE. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87:206-210, 1978.
19. Lowry OH, Passonneau JV. A Flexible System of Enzymatic Analysis. New York: Academic Press, Inc., 1972.
20. Van Schaftingen E, Lederer B, Bartrons R, Hers HG. A kinetic study of pyrophosphate: fructose-6-phosphate phosphotransferase from potato tubers. Application to a microassay of fructose-2,6-bisphosphate. Eur J Biochem 129:191-195, 1982.
21. Ambrosio S, Ventura F, Rosa JL, Bartons R. Fructose-2,6-bisphosphate in hypoglycemic rat brain. J Neurochem 57:200-203, 1991.
22. Knull HR, Taylor WF, Wells WW. Effects of energy metabolism on in vivo distribution of hexokinase in brain. J Biol Chem 248:5414-5417, 1973.
23. Prohaska JR, Brokate B. Copper deficiency alters rat dopamine beta-monooxygenase mRNA and activity. J Nutr 129:2147-2153, 1999.
24. Watanabe F, Sakai A, Furuya E. Novel isoforms of rat brain fructose 6-phosphate 2-kinase/fructose-2,6-bisphosphatase are generated by tissue-specific alternative splicing. J Neurochem 69:1-9, 1997.
25. Watanabe F, Furuya E. Alternative splicing of novel exons of rat heart- type fructose-6-phosphate 2-kinase/fructose-2,6-bisphosphatase gene. Biochem Biophys Res Commun 282:803-810, 2001.
26. Watanabe F, Sakai A, Furuya E, Uyeda K. Molecular cloning and tissue specific expression of fructose 6-phosphate,2-kinase:fructose-2,6-bisphosphatase of rat brain. Biochem Biophys Res Commun 198:335-340, 1994.
27. Prohaska JR, Gybina AA. Rat brain iron concentration is lower following perinatal copper deficiency. J Neurochem 93:698-705, 2005.
28. Prohaska JR, Brokate B. Dietary copper deficiency alters protein levels of rat dopamine beta-monooxygenase and tyrosine monooxygenase. Exp Biol Med (Maywood) 226:199-207, 2001.
29. West EC, Prohaska JR. Cu,Zn-superoxide dismutase is lower and copper chaperone CCS is higher in erythrocytes of copper-deficient rats and mice. Exp Biol Med (Maywood) 229:756-764, 2004.
30. Leino RL, Gerhart DZ, van Bueren AM, McCall AL, Drewes LR. Ultrastructural localization of GLUT 1 and GLUT 3 glucose transporters in rat brain. J Neurosci Res 49:617-626, 1997.
31. Van Bueren AM, Moholt-Siebert M, Begley DE, McCall AL. An immunization method for generation of high affinity antisera against glucose transporters useful in immunohistochemistry. Biochem Biophys Res Commun 197:1492-1498, 1993.
32. Prohaska JR, Broderius M, Brokate B. Metallochaperone for Cu,Zn-superoxide dismutase (CCS) protein but not mRNA is higher in organs from copper-deficient mice and rats. Arch Biochem Biophys 417:227-234, 2003.
33. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D. Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403:139-148, 2007.
34. Stein SC, Woods A, Jones NA, Davison MD, Carling D. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J 345 (Pt 3):437-443, 2000.
35. Almeida A, Moncada S, Bolanos JP. Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2- kinase pathway. Nat Cell Biol 6:45-51, 2004.
36. Pauwels PJ, Trouet A. Role of fructose-2,6-bisphosphate in the regulation of glycolysis in various types of cultivated brain cell. Neurosci Lett 46:173-177, 1984.
37. Rider MH, Bertrand L, Vertommen D, Michels PA, Rousseau GG, Hue L. 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem J 381: 561-579, 2004.
38. Watanabe F, Furuya E. Tissue-specific alternative splicing of rat brain fructose 6-phosphate 2-kinase/fructose 2,6-bisphosphatase. FEBS Lett 458:304-308, 1999.
39. Marsin AS, Bouzin C, Bertrand L, Hue L. The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. J Biol Chem 277:30778-30783, 2002.
40. Ventura F, Rosa JL, Ambrosio S, Gil J, Bartrons R. 6-phosphofructo-2- kinase/fructose-2,6-bisphosphatase in rat brain. Biochem J 276 (Pt 2):455-460, 1991.
41. John SA, Ottolia M, Weiss JN, Ribalet B. Dynamic modulation of intracellular glucose imaged in single cells using a FRET-based glucose nanosensor. Pflugers Arch (in press), 2007.
42. Rovetto MJ, Lamberton WF, Neely JR. Mechanisms of glycolytic inhibition in ischemic rat hearts. Circ Res 37:742-751, 1975.
43. Newsholme EA, Sugden PH, Williams T. Effect of citrate on the activities of 6-phosphofructokinase from nervous and muscle tissues from different animals and its relationships to the regulation of glycolysis. Biochem J 166:123-129, 1977.
44. Ruderman NB, Ross PS, Berger M, Goodman MN. Regulation of glucose and ketone-body metabolism in brain of anaesthetized rats. Biochem J 138:1-10, 1974.
45. Turnley AM, Stapleton D, Mann RJ, Witters LA, Kemp BE, Bartlett PF. Cellular distribution and developmental expression of AMP- activated protein kinase isoforms in mouse central nervous system. J Neurochem 72:1707-1716, 1999.
46. John SA, Ottolia M, Weiss JN, Ribalet B. Dynamic modulation of intracellular glucose imaged in single cells using a FRET-based glucose nanosensor. Pflugers Arch 456:307-322, 2008.
47. Molnar MJ, Valikovics A, Molnar S, Tron L, Dioszeghy P, Mechler F, Gulyas B. Cerebral blood flow and glucose metabolism in mitochondrial disorders. Neurology 55:544-548, 2000.
48. Kauppinen RA, Hiltunen JK, Hassinen IE. Compartmentation of citrate in relation to the regulation of glycolysis and the mitochondrial transmembrane proton electrochemical potential gradient in isolated perfused rat heart. Biochim Biophys Acta 681:286-291, 1982.
49. Vora S, Oskam R, Staal GE. Isoenzymes of phosphofructokinase in the rat. Demonstration of the three non-identical subunits by biochemical, immunochemical and kinetic studies. Biochem J 229:333-341, 1985.
50. Chao JC, Medeiros DM, Altschuld RA, Hohl CM. Cardiac nucleotide levels and mitochondrial respiration in copper-deficient rats. Comp Biochem Physiol 104:163-168, 1993.
51. Matz JM, Saari JT, Bode AM. Functional aspects of oxidative phosphorylation and electron transport in cardiac mitochondria of copper-deficient rats. J Nutr Biochem 6:644-652, 1995.