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Evolution of pyruvate carboxylase and other biotin containing enzymes in developing rat liver and kidney

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Abstract

The evolution of pyruvate carboxylase has been studied in rat liver and kidney during perinatal development. The pyruvate carboxylase activity, amount of enzyme and mRNA levels have been assayed from 2 days before delivery to weaning. In liver, there is a peak of activity and amount of enzyme 24 h before delivery and 2 peaks, at 12 h and 6 days, after parturition. The transcription of the enzyme gene followed a similar pattern, with mRNA peaks preceding those of activity and amount of enzyme. However, in kidney, pyruvate carboxylase activity, amount and mRNA remain low until weaning. These results confirm the limited role of renal gluconeogenesis during the perinatal development. Since all carboxylases contain biotin as prosthetic group, the biotinylation of pyruvate carboxylase during the perinatal period was investigated by western-blot using streptavidin-biotin peroxidase. In the mitochondrial samples from liver and kidney, all the pyruvate carboxylase detected was fully biotinylated, indicating an early development of the holocarboxylase synthetase activity in the perinatal period. This Western-blot technique also allowed us the detection of other biotin-enzymes based on their molecular weight. In liver, during the perinatal development propionyl-coA and 3-methyl-crotonyl-coA carboxylases followed a pattern of induction similar to pyruvate carboxylase. In kidney, the expression of mitochondrial carboxylases was lower compared to liver and propionyl-coA carboxylase was not detected during the studied period

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References

  1. Attwood PV: The structure and mechanism of action of pyruvate carboxylase. Int J Biochem Cell Biol 27: 231–249, 1995

    PubMed  Google Scholar 

  2. Attwood PV, Keech DB: Pyruvate carboxylase. Curr Top Cell Reg 23: 1–55, 1984

    Google Scholar 

  3. Adam PAJ, Haynes RC: Control of hepatic mitochondrial carbon dioxide fixation by glucagon, epinephrine and cortisol. J Biol Chem 44: 6444–6450, 1969

    Google Scholar 

  4. Ballard FJ, Hanson RW: Phosphoenolpyruvate carboxykinase and pyruvate carboxylase in developing rat liver. Biochem J 104: 866–871, 1967

    PubMed  Google Scholar 

  5. Forissier M, Baverel G: The conversion of alanine into glutamine in guinea-pig renal cortex. Essential role of pyruvate carboxylase. Biochem J 200: 27–33, 1981

    PubMed  Google Scholar 

  6. Groen AK, Van Roermund CWT, Vervoorn RC, Tager JM: Control of gluconeogenesis in rat liver cells. Flux control coefficient of the enzymes in the gluconeogenic pathway in the absence and presence of glucagon. Biochem J 237: 379–389, 1986

    PubMed  Google Scholar 

  7. Martin AD, Titheradge MA: Hormonal stimulation of gluconeogenesis through increased mitochondrial metabolic flux. Biochem Soc Trans 11: 78–81, 1983

    PubMed  Google Scholar 

  8. Weinberg MB, Utter MF: Effect of thyroid hormone on the turnover of rat liver pyruvate carboxylase and pyruvate dehydrogenase. J Biol Chem 254: 9492–9499, 1979

    PubMed  Google Scholar 

  9. Cuezva JM, Moreno F, Medina JM, Mayor F: Prematurity in the rat. Fuels and gluconeogenic enzymes. Biol Neonate 37: 88–95, 1980

    PubMed  Google Scholar 

  10. Mayor F, Cuezva M: Hormonal and metabolic changes in the perinatal period. Biol Neonate 48: 185–196, 1985

    PubMed  Google Scholar 

  11. Valcarce C, Izquierdo JM, Chamorro M, Cuezva JM: Mammalian adaptation to extrauterine environment: mitochondrial functional impairments in prematurity. Biochem J 303: 855–862, 1994

    PubMed  Google Scholar 

  12. Kimura RE, Warshaw JB: Metabolic adaptations of the fetus and newborn. J Pediatr Gastroenterol Nutr 2: S12–S15, 1983

    PubMed  Google Scholar 

  13. Salto R, Oliver J, Sola MM, Vargas AM: Distribution of pyruvate carboxylase along the rat nephron: An immunological and enzymatic study. Kidney Int 39: 1162–1167, 1991

    PubMed  Google Scholar 

  14. Salto R, Sola MM, Oliver FJ Vargas AM: Effects of starvation, diabetes and carbon-tetrachloride intoxication on rat-kidney cortex and liver pyruvate carboxylase levels. Arch Physiol Biochem 104: 845–850, 1996

    PubMed  Google Scholar 

  15. Chomczynski P, Sacchi N: Single method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156–159, 1987

    Article  PubMed  Google Scholar 

  16. Jitrapakdee S, Booker GW, Cassady AI, Wallace CJ: Cloning, sequencing and expression of rat liver pyruvate carboxylase. Biochem J 316: 631–637, 1996

    PubMed  Google Scholar 

  17. Chandler CS, Ballard FJ: Multiple biotin-containing proteins in 3T3-L1 cells. Biochem J 237: 123–130, 1986

    PubMed  Google Scholar 

  18. Ruggieroa FP, Sheffielda JB: The use of avidin as a probe for the distribution of mitochondrial carboxylases in developing chick retina. J Histochem Citochem 46: 177–184, 1998

    Google Scholar 

  19. Attardi G, Schatz G: Biogenesis of mitochondria. Annu Rev Biol 4: 289–333, 1988

    Google Scholar 

  20. Stumvoll M, Meyer C, Perriello G, Kreider M, Welle S, Gerich J: Human kidney and liver gluconeogenesis: Evidence for organ substrate selectivity. Am J Physiol 274: E817–E826, 1998

    PubMed  Google Scholar 

  21. Valcarce CR, Navarrete M, Encabo P, Loeches E, SatrÚstegui J, Cuezva JM: Postnatal development of rat liver mitochondrial functions. The role of protein synthesis and of adenine nucleotides. J Biol Chem 263: 7767–7775, 1988

    PubMed  Google Scholar 

  22. Cuezva JM, Valcarce C, Medina JM: Substrates availability for maintenance of energy homeostasis in the immediate postnatal period of the fasted newborn rat. In: C.T. Jones, P.W. Nathanielsz (eds). The Physiological Development of the Fetus and Newborn. Academic Press, New York, 1985, pp 63–69

    Google Scholar 

  23. Serrano E, Luis AM, Encabo P, Alconada A, Ho L, Patel MS, Cuezva JM: Rapid postnatal induction of the pyruvate dehydrogenase complex in rat liver mitochondria. Ann New York Acad Sci 573: 412–415, 1989

    Google Scholar 

  24. Girard J: Gluconeogenesis in late fetal and early neonatal life. Biol Neonate 50: 237–258, 1986

    PubMed  Google Scholar 

  25. Luis AM, Izquierdo JM, Ostronoff LK, Salinas M, Santaren JF, Cuezva JM: Translational regulation of mitochondrial differentiation in neonatal rat liver. Specific increase in the translational efficiency of the nuclear-encoded mitochondrial β-F1-ATPase mRNA. J Biol Chem 268: 1868–1875, 1995

    Google Scholar 

  26. Delaval E, Moreau E, Geloso JP: Development of ammonia and glucose productions from glutamine in foetal rat kidney; effects of metabolic acidosis. Pflügers Arch 379: 95–100, 1979

    Google Scholar 

  27. Fowden AL, Mijovic J, Silver M: The effects of cortisol on hepatic and renal gluconeogenic enzyme activities in the sheep fetus during late gestation. J Endocrinol 137: 213–222, 1993

    PubMed  Google Scholar 

  28. Prieur B, Cordeau-Lossouarn L, Rotig A, Bismuth J, Geloso JP, Delaval E: Perinatal maturation of rat kidney mitochondria. Biochem J 305: 675–680, 1995

    PubMed  Google Scholar 

  29. Delaval E, Razanoelina M, Bastin J, Freund N, Bismuth J, Geloso JP: Mitochondrial activity of rat kidney during ontogeny. J Dev Physiol 14: 1–5, 1990

    PubMed  Google Scholar 

  30. Djouadi F, Bastin J, Gilbert T, Rötig A, Rustin P, Merlet-Benichou C: Mitochondrial biogenesis and development of respiratory chain enzymes in kidney cells: Role of glucocorticoids. Am J Physiol 267: C245–C254, 1994

    PubMed  Google Scholar 

  31. Prieur B, Bismuth J, Delaval E: Effects of adrenal steroid hormones on mitochondrial maturation during the late fetal period. Eur J Biochem 252: 194–199, 1998

    PubMed  Google Scholar 

  32. Wijkhuisen A, Djouadi F, Vilar J, Merlet-Benichou C, Bastin J: Thyroid hormones regulate development of energy metabolism enzymes in rat proximal convoluted tubule Am J Physiol 268: F634–F642, 1995

    PubMed  Google Scholar 

  33. Ahmad F, Ahmad PM, Mendez A: Rat liver pyruvate carboxylase. Purification, detection and quantification of apo and holo forms by immuno-blotting and by an enzyme-linked immunosorbent assay. Biochem J 236: 527–533, 1986

    PubMed  Google Scholar 

  34. Ahmad PM, Ahmad F: Mammalian pyruvate carboxylase: Effect of biotin on the synthesis and translocation of apo-enzyme into 3T3-L adipocyte mitochondria. FASEB J 5: 2482–2485, 1991

    PubMed  Google Scholar 

  35. Chang HI, Cohen ND: Regulation and intracellular localization of the biotin holocarboxylase synthetase of 3T3-L1 cells. Arch Biochem Biophys 225: 237–247, 1983

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Departamento de Bioquímica y Biología Molecular, Facultad de Farmacia, Universidad de Granada, Campus de Cartuja s/n, 18071, Granada, Spain

    Rafael Salto, María Dolores Girón, María del Mar Sola & Alberto Manuel Vargas

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  1. Rafael Salto
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  2. María Dolores Girón
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  3. María del Mar Sola
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  4. Alberto Manuel Vargas
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Salto, R., Girón, M.D., del Mar Sola, M. et al. Evolution of pyruvate carboxylase and other biotin containing enzymes in developing rat liver and kidney. Mol Cell Biochem 200, 111–117 (1999). https://doi.org/10.1023/A:1007091116952

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