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Thyroid Hormone Treatments Differentially Affect the Temperature Kinetics Properties of FoF1 ATPase and Succinate Oxidase as well as the Lipid/Phospholipid Profiles of Rat Kidney Mitochondria: A Correlative Study

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Abstract

Effect of thyroidectomy (Tx) and subsequent treatment with 3,5,3′-triiodo-l-thyronine (T3) or replacement therapy (TR) with T3 + l-thyroxine (T4) on the temperature kinetics properties of FoF1 adenosine triphosphatase (ATPase, ATP synthase, H+-translocating ATP synthase EC 3.6.3.14) and succinate oxidase (SO) and on the lipid/phospholipid makeup of rat kidney mitochondria were examined. Tx lowered ATPase activity, which T3 treatment restored. SO activity was unchanged in Tx but decreased further by T3 treatment. TR restored both activities. The energies of ATPase activation in the high and low temperature ranges (E H and E L) increased in the Tx and T3 animals with decrease in phase transition temperature (Tt). TR restored E H and E L but not Tt to euthyroid levels. E H and E L of SO decreased in Tx animals. T3 and TR restored E H whereas E L was restored only in the TR group; Tt increased in both groups. Total phospholipid and cholesterol contents decreased significantly in Tx and T3-treated animals. In Tx animals, sphingomyelin (SPM) and phosphatidylcholine (PC) components decreased, while phosphatidylserine (PS) and diphosphatidylglycerol components increased. T3 and TR treatments caused decreases in SPM, phosphatidylinositol and PS. PC and phosphatidylethanolamine (PE) increased in the T3 group. TR resulted in increased lysophospolipids and PE. Changes in kinetic parameters of the two enzymes were differently correlated with specific phospholipid components. Both T3 and TR regimens were unable to restore normal membrane structure-function relationships.

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References

  • Balla T (2005) Inositol-lipid binding motifs: signal integrators through protein-lipid and protein-protein interactions. J Cell Sci 118:2093–2104

    Article  PubMed  CAS  Google Scholar 

  • Bangur CS, Howland JL, Katyare SS (1995) Thyroid hormone treatment alters phospholipid composition and membrane fluidity of rat brain mitochondria. Biochem J 305:29–32

    PubMed  CAS  Google Scholar 

  • Bartlett GR (1959) Phosphorus assay in column chromatography. J Biol Chem 234:466–468

    PubMed  CAS  Google Scholar 

  • Booth PJ, Curran AR (1999) Membrane protein folding. Curr Opin Struct Biol 9:115–121

    Article  PubMed  CAS  Google Scholar 

  • Cappello AR, Gnoni GV (1994) Influence of triiodothyronine and insulin on the synthesis of glycerolipids in rat hepatocytes. Biochem Mol Biol Int 34:101–107

    PubMed  CAS  Google Scholar 

  • Daum G (1985) Lipids of mitochondria. Biochim Biophys Acta 822:1–42

    PubMed  CAS  Google Scholar 

  • Dave KR, Katyare SS (2002) Effect of alloxan-induced diabetes on serum and cardiac butyrylcholinesterases in the rat. J Endocrinol 175:241–250

    Article  PubMed  CAS  Google Scholar 

  • Dave KR, Syal AR, Katyare SS (1999) Tissue cholinesterases. A comparative study of their kinetic properties. Z Naturforsch 55c:100–108

    Google Scholar 

  • Del Compare JA, Aguirre JA, Ibarra FR, Barontini M, Armando I (2001) Effects of thyroid hormone on the renal dopaminergic system. Endocrine 15:297–303

    Article  PubMed  Google Scholar 

  • Dixon M, Webb EC (1979) In: Dixon M, Webb EC, Thorne C Jr, Tipton KF (eds), Enzymes Kinetics, 3rd ed. Longman, London, pp 47–206

  • Escobar-Morreale HF, del Rey FE, Obregon MJ, de Escobar GM (1996) Only the combined treatment with thyroxine and triiodothyronine ensures euthyroidism in all tissues of the thyroidectomized rat. Endocrinology 137:2490–2502

    Article  PubMed  CAS  Google Scholar 

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Freyzs L, Lastennet A, Mandel P (1976) Metabolism of brain sphingomyelins: half-lives of sphingosine, fatty acids and phosphate from two types of rat brain sphingomyelins. J Neurochem 27:355–359

    Article  Google Scholar 

  • Fukuda Y, Eklof AC, Malmborg AS, Aperia A (1992) Calcium supplementation and thyroid hormone protect against gentamicin-induced inhibition of proximal tubular Na+,K+-ATPase activity and other renal functional changes. Acta Physiol Scand 145:93–98

    PubMed  CAS  Google Scholar 

  • Gustafsson R, Tata JR, Lindberg O, Ernster L (1965) The relationship between the structure and activity of rat skeletal muscle mitochondria after thyroidectomy and thyroid hormone treatment. J Cell Biol 26:553–578

    Article  Google Scholar 

  • Hoch FL (1988) Lipids and thyroid hormones. Prog Lipid Res 27:199–270

    Article  PubMed  CAS  Google Scholar 

  • Horowitz B, Hensley CB, Quintero M, Azuma KK, Putnam D, McDonough AA (1990) Differential regulation of Na,K-ATPase alpha 1, alpha 2, and beta subunit mRNA and protein levels by thyroid hormone. J Biol Chem 265:14308–14314

    PubMed  CAS  Google Scholar 

  • Hostetler KY (1991) Effect of tyroxine on the activity of mitochondrial cardiolipin synthase in rat liver. Biochim Biophys Acta 1086:139–140

    PubMed  CAS  Google Scholar 

  • Iverson SL, Orrenius S (2004) The cardiolipin-cytochrome c interaction and the mitochondrial regulation of apoptosis. Arch Biochem Biophys 423:37–46

    Article  PubMed  CAS  Google Scholar 

  • Izquierdo JM, Cuezva JM (1993) Thyroid hormones promote transcriptional activation of the nuclear gene coding for mitochondrial beta-F1-ATPase in rat liver. FEBS Lett 323:109–112

    Article  PubMed  CAS  Google Scholar 

  • Katewa SD, Katyare SS (2003) A simplified method for inorganic phosphate determination and its application for phosphate analysis in enzyme assays. Anal Biochem 323:180–187

    Article  PubMed  CAS  Google Scholar 

  • Katyare SS, Fatterpaker P, Sreenivasan A (1971) Effect of cytochrome c on succinate oxidation in rat liver mitochondria. Indian J Biochem Biophys 8:130–132

    PubMed  CAS  Google Scholar 

  • Katyare SS, Joshi MV, Fatterpaker P, Sreenivasan A (1977) Effect of thyroid deficiency on oxidative phosphorylation in rat liver, kidney, and brain mitochondria. Arch Biochem Biophys 182:155–163

    Article  PubMed  CAS  Google Scholar 

  • Katyare SS, Shallom JM (1988) Altered cerebral protein turnover in rats following prolonged in vivo treatment with nicotine. J Neurochem 50:1356–1363

    Article  PubMed  CAS  Google Scholar 

  • Katz AI, Emmanouel DS, Lindheimer MD (1975) Thyroid hormone and the kidney. Nephron 15:223–249

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Maggio B, Rosetti CM, Borioli GA, Fanani ML, Del Boca M (2005) Protein-mediated surface structuring in Biomembranes. Braz J Med Biol Res 38:1735–1748

    Article  PubMed  CAS  Google Scholar 

  • Marsh D, Horvath LI, Swamy MJ, Mantripragada S, Kleinschmidt JH (2002) Interaction of membrane-spanning proteins with peripheral and lipid-anchored membrane proteins: perspectives from protein-lipid interactions. Mol Membr Biol 19:247–255

    Article  PubMed  CAS  Google Scholar 

  • McMillin JB, Dowhan W (2002) Cardiolipin and apoptosis. Biochim Biophys Acta 1585:97–107

    PubMed  CAS  Google Scholar 

  • Ohanian J, Ohanian V (2001) Sphingolipids in mammalian cell signaling. Cell Mol Life Sci 58:2053–2068

    Article  PubMed  CAS  Google Scholar 

  • Pandya JD, Dave KR, Katyare SS (2004) Effect of long-term aluminum feeding on lipid/phospholipid profiles of rat brain myelin. Lipids Health Dis 3:13–18

    Article  PubMed  CAS  Google Scholar 

  • Papadopoulo V (2003) Peripheral benzodiazepine receptor: structure and function in health and disease. Ann Pharm Fr 61:30–50

    PubMed  CAS  Google Scholar 

  • Paradies G, Ruggiero FM, Dinoi P (1991) The influence of hypothyroidism on the transport of phosphate and on the lipid composition in rat-liver mitochondria. Biochim Biophys Acta 1070:180–186

    Article  PubMed  CAS  Google Scholar 

  • Parmar DV, Khandkar MA, Pareira L, Bangur CS, Katyare SS (1995) Thyroid hormones alter Arrhenius kinetics of succinate-2,6-dichloroindophenol reductase, and the lipid composition and membrane fluidity of rat liver mitochondria. Eur J Biochem 230:576–581

    Article  PubMed  CAS  Google Scholar 

  • Pasquini JM, Faryra de Raveglia I, Capitman N, Soto EF (1980) Differential effect of l-thyroxine on phospholipid biosynthesis in mitochondria and microsomal fraction. Biochem J 186:127–133

    PubMed  CAS  Google Scholar 

  • Patel SP, Katyare SS (2006) Effect of alloxan-diabetes and subsequent treatment with insulin on kinetic properties of succinate oxidase activity from rat liver mitochondria. Z Naturforsch 61c:756–762

    Google Scholar 

  • Porcellati G, Arienti G (1983) Metabolism of phosphoglycerides In: Lajtha A (ed), Handbook of Neurochemistry, 2nd ed, vol 3. Plenum Press, New York, pp 133–161

    Google Scholar 

  • Rajwade MS, Katyare SS, Fatterpaker P, Sreenivasan A (1975) Regulation of mitochondrial protein turnover by thyroid hormone(s). Biochem J 152:379–387

    PubMed  CAS  Google Scholar 

  • Rapaport D (2005) How does the TOM complex mediate insertion of precursor proteins into the mitochondrial outer membrane? J Cell Biol 171:419–423

    Article  PubMed  CAS  Google Scholar 

  • Resh MD (2004) Membrane targeting of lipid modified signal transduction proteins. Subcell Biochem 37:217–232

    PubMed  CAS  Google Scholar 

  • Richter C, Ghafourifar P (1999) Ceramide induces cytochrome c release from isolated mitochondria. Biochem Soc Symp 66:27–31

    PubMed  CAS  Google Scholar 

  • Satav JG, Katyare SS (1982) Effect of experimental thyrotoxicosis on oxidative phosphorylation in rat liver, kidney and brain mitochondria. Mol Cell Endocrinol 28:173–189

    Article  PubMed  CAS  Google Scholar 

  • Satav JG, Katyare SS (1991) Effect of thyroidectomy and subsequent treatment with triiodothyronine on kidney mitochondrial oxidative phosphorylation in the rat. J Biosci 16:81–89

    CAS  Google Scholar 

  • Skipski VP, Peterson RF, Barclay M (1964) Quantitative analysis of phospholipids by thin-layer chromatography. Biochem J 90:374–378

    PubMed  CAS  Google Scholar 

  • Swick RW, Ip MM (1974) Measurement of protein turnover in rat liver with [14C] carbonate. J Biol Chem 249:6836–6841

    PubMed  CAS  Google Scholar 

  • Tata JR (1964) Biological action of thyroid hormones at the cellular and molecular levels. In: Litwack G, Kritchevsky D (eds), Action of Hormones on Molecular Processes. Wiley, New York, pp 58–131

    Google Scholar 

  • Tata JR (1966) The regulation of mitochondrial structure and function by thyroid hormones under physiological conditions. In: Tager JM, Papa S, Quagliariello E, Slater EC (eds), Regulation of Metabolic Processes in Mitochondria. Elsevier Biomedical Press, Amsterdam, pp 489–507

    Google Scholar 

  • Tata JR, Ernster L, Lindberg O, Arrhenius E, Pedersen S, Hedman R (1963) The action of thyroid hormones at the cell level. Biochem J 86:408–428

    PubMed  CAS  Google Scholar 

  • Tata JR, Widnell CC (1966) Ribonucleic acid synthesis during the early action of thyroid hormones. Biochem J 98:604–620

    PubMed  CAS  Google Scholar 

  • Vargas F, Moreno JM, Rodriguez-Gomez I, Wangensteen R, Osuna A, Alvarez-Guerra M, Garcia-Estan J (2006) Vascular and renal function in experimental thyroid disorders. Eur J Endocrinol 154:197–212

    Article  PubMed  CAS  Google Scholar 

  • Wrutniak-Cabello C, Casas F, Cabello G (2001) Thyroid hormone action in mitochondria. J Mol Endocrinol 26:67–77

    Article  PubMed  CAS  Google Scholar 

  • Zlatkis A, Zak B (1969) Study of a new cholesterol reagent. Anal Biochem 29:143–148

    Article  PubMed  CAS  Google Scholar 

Download references

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Correspondence to Hiren R. Modi.

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Modi, H.R., Patel, S.P., Katyare, S.S. et al. Thyroid Hormone Treatments Differentially Affect the Temperature Kinetics Properties of FoF1 ATPase and Succinate Oxidase as well as the Lipid/Phospholipid Profiles of Rat Kidney Mitochondria: A Correlative Study. J Membrane Biol 215, 135–145 (2007). https://doi.org/10.1007/s00232-007-9013-4

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