Ecto- and cytosolic 5′-nucleotidases in normal and AMP deaminase-deficient human skeletal muscle
-
Frank Hanisch
Abstract
In skeletal muscle, adenosine monophosphate (AMP) is mainly deaminated by AMP deaminase. However, the C34T mutation in the AMPD1 gene severely reduces AMP deaminase activity. Alternatively, intracellular AMP is dephosphorylated to adenosine via cytosolic AMP 5′-nucleotidase (cN-I). In individuals with a homozygous C34T mutation, cN-I might be a more important pathway for AMP removal. We determined activities of AMP deaminase, cN-I, total cytosolic 5′-nucleotidase (total cN), ecto-5′-nucleotidase (ectoN) and whole homogenate 5′-nucleotidase activity in skeletal muscle biopsies from patients with different AMPD1 genotypes [homozygotes for C34T mutation (TT); heterozygotes for C34T mutation (CT); and homozygotes for wild type (CC): diseased controls CC; and normal controls CC]. AMP deaminase activity showed genotype-dependent differences. Total cN activity in normal controls accounted for 57±22% of whole homogenate 5′-nucleotidase activity and was not significantly different from the other groups. A weak inverse correlation was found between AMP deaminase and cN-I activities (r2=0.18, p<0.01). There were no significant differences between different groups in the activities of cN-I, whole homogenate 5′-nucleotidase and ectoN, or in cN-I expression on Western blots. No correlation for age, fibre type distribution and AMPD1 genotype was found for whole homogenate nucleotidase, total cN and cN-I using multiple linear regression analysis. There was no gender-specific difference in the activities of whole homogenate nucleotidase, total cN and cN-I. The results indicate no changes in the relative expression or catalytic behaviour of cN-I in AMP deaminase-deficient human skeletal muscle, but suggest that increased turnover of AMP by cN-I in working skeletal muscle is due to higher substrate availability of AMP.
References
Anderson, J.L. (2004). A common variant of the AMPD1 gene predicts improved survival in patients with ischemic left ventricular dysfunction. J. Card. Fail.10, 316–320.Suche in Google Scholar
Anderson, J.L., Habashi, J., Carlquist, J.F., Muhlestein, J.B., Horne, B.D., Bair, T.L., Pearson, R.R., and Hart, N. (2000). A common variant of the AMPD1 gene predicts improved cardiovascular survival in patients with coronary artery disease. J. Am. Coll. Cardiol.36, 1248–1252.10.1016/S0735-1097(00)00850-0Suche in Google Scholar
Arabadjis, P.G., Tullson P.C., and Terjung, R.L. (1993). Purine nucleoside formation in rat skeletal muscle fiber types. Am. J. Physiol.264, C1246–1251.10.1152/ajpcell.1993.264.5.C1246Suche in Google Scholar
Bockman, E.L. and McKenzie, J.E. (1993). Tissue adenosine content in active soleus and gracilis muscles of cats. Am. J. Physiol.244, H552–559.Suche in Google Scholar
Camici, M., Fini, C., and Ipata, P.L. (1985). Isolation and kinetic properties of 5′-nucleotidase from guinea-pig skeletal muscle. Biochim. Biophys. Acta840, 6–12.10.1016/0304-4165(85)90155-2Suche in Google Scholar
Cheng, B., Essackjee, H.C., and Ballard, H.J. (2000). Evidence for control of adenosine metabolism in rat oxidative skeletal muscle by changes in pH. J. Physiol.522, 467–477.10.1111/j.1469-7793.2000.t01-1-00467.xSuche in Google Scholar
Crowther, G.J., Carey, M.F., Kemper, W.F., and Conley, K.E. (2002). Control of glycolysis in contracting skeletal muscle. I. Turning it on. Am. J. Physiol. Endocrinol. Metab.282, E67–E73.Suche in Google Scholar
Fishbein, W.N., Griffin, J.L., and Armbrustmacher, V.W. (1980). Stain for skeletal muscle adenylate deaminase. An effective tetrazolium stain for frozen biopsy specimens. Arch. Pathol. Lab. Med.104, 462–466.Suche in Google Scholar
Gastmann, A, Sigusch, H.H., Henke, A., Reinhardt, D., Surber, R., Gastmann, O., and Figulla, H.R. (2004). Role of adeno-sine monophosphate deaminase-1 gene polymorphism in patients with congestive heart failure: influence on tumor necrosis factor-α level and outcome. Am. J. Cardiol.93, 1260–1264.10.1016/j.amjcard.2004.02.011Suche in Google Scholar
Gross, M. (1997). Clinical heterogeneity and molecular mechanisms in inborn muscle AMP deaminase deficiency. J. Inherit. Metab. Dis.20, 186–192.10.1023/A:1005352605421Suche in Google Scholar
Gross, M., Rotzer, E., Kolle, P., Mortier, W., Reichmann, H., Goebel, H.H., Lochmüller, H., Pongratz, D., Mahnke-Zizelman, D.K., and Sabina, R.L. (2002). A G468-T AMPD1 mutant allele contributes to the high incidence of myoadenylate deaminase deficiency in the Caucasian population. Neuromuscul. Disord.12, 558–565.10.1016/S0960-8966(02)00008-1Suche in Google Scholar
Hellsten, Y. (1999). The effect of muscle contraction on the regulation of adenosine formation in rat skeletal muscle cells. J. Physiol.518, 761–768.10.1111/j.1469-7793.1999.0761p.xSuche in Google Scholar PubMed PubMed Central
Hellsten, Y., Maclean, D., Rådegran, G., Saltin, B., and Bangsbo, J. (1998). Adenosine concentrations in the interstitium of resting and contracting human skeletal muscle. Circulation98, 6–8.10.1161/01.CIR.98.1.6Suche in Google Scholar
Hellsten, Y., Richter, E.A., Kiens, B., and Bangsbo, J. (1999). AMP deamination and purine exchange in human skeletal muscle during and after intense exercise. J. Physiol.520, 909–920.10.1111/j.1469-7793.1999.00909.xSuche in Google Scholar PubMed PubMed Central
Hunsucker, S.A., Spychala, J., and Mitchell, B.S. (2001). Human cytosolic 5′-nucleotidase I: characterization and role in nucleotide analog resistance. J. Biol. Chem.276, 10498–10504.10.1074/jbc.M011218200Suche in Google Scholar
Itoh, R. and Yamada, K. (1991). Determination of cytoplasmic 5′-nucleotidase which preferentially hydrolyses 6-hydroxypurine nucleotides in pig, rat and human tissues by immunotitration. Int. J. Biochem.23, 461–465.Suche in Google Scholar
Itoh, R., Echizen, H., Higuchi, M., Oka, J., and Yamada, K. (1992). A comparative study on tissue distribution and metabolic adaptation of IMP-GMP 5′-nucleotidase. Comp. Biochem. Physiol. B 103, 153–159.10.1016/0305-0491(92)90427-SSuche in Google Scholar
Kalsi, K.K., Yuen, A.H., Rybakowska, I.M., Johnson, P.H., Slominska, E., Birks, K. Kaletha, K., Yacoub, M.H., and Smolenski, R.T. (2003). Decreased cardiac activity of AMP deaminase in subjects with the AMPD1 mutation – a potential mechanism for protection in heart failure. Cardiovasc. Res.59, 678–684.10.1016/S0008-6363(03)00497-8Suche in Google Scholar
Loh, E., Rebbeck, T.R., Mahoney, P.D., DeNofrio, D., Swain, J.L., and Holmes, E.W. (1999). Common variant in AMPD1 gene predicts improved clinical outcome in patients with heart failure. Circulation99, 1422–1425.10.1161/01.CIR.99.11.1422Suche in Google Scholar
Lynge, J., Juel, C., and Hellsten, Y. (2001). Extracellular formation and uptake of adenosine during skeletal muscle contraction in the rat: role of adenosine transporters. J. Physiol.537, 597–605.10.1111/j.1469-7793.2001.00597.xSuche in Google Scholar PubMed PubMed Central
Morisaki, T., Gross, M., Morisaki, H., Pongratz, D., Zöllner, N., and Holmes, E.W. (1992). Molecular basis of AMP deaminase deficiency in skeletal muscle. Proc. Natl. Acad. Sci. USA89, 6457–6461.10.1073/pnas.89.14.6457Suche in Google Scholar PubMed PubMed Central
Newby, A.C., Luzio, J.P., and Hales, C.N. (1975). The properties and extracellular location of 5′ nucleotidase of the rat fat-cell plasma membrane. Biochem. J.146, 625–633.10.1042/bj1460625Suche in Google Scholar PubMed PubMed Central
Norman, B., Mahnke-Zizelman, D.K., Vallis, A., and Sabina, R.L. (1998). Genetic and other determinants of AMP deaminase activity in healthy adult skeletal muscle. J. Appl. Physiol.85, 1273–1278.10.1152/jappl.1998.85.4.1273Suche in Google Scholar PubMed
Norman, B., Sabina, R.L., and Jansson, E. (2001). Regulation of skeletal muscle ATP catabolism by AMPD1 genotype during sprint exercise in asymptomatic subjects. J. Appl. Physiol.91, 258–264.10.1152/jappl.2001.91.1.258Suche in Google Scholar PubMed
Rådegran, G. and Hellsten, Y. (2000). Adenosine and nitric oxide in exercise-induced human skeletal muscle vasodilatation. Acta Physiol. Scand.168, 575–591.10.1046/j.1365-201x.2000.00705.xSuche in Google Scholar PubMed
Rubio, J.C., Martin, M.A., Del Hoyo, P., Bautista, J., Campos, Y., Segura, D., Navarro, C., Ricoy, J.R., Cabello, A., and Arenas, J. (2000). Molecular analysis of Spanish patients with AMP deaminase deficiency. Muscle Nerve23, 1175–11178.10.1002/1097-4598(200008)23:8<1175::AID-MUS3>3.0.CO;2-MSuche in Google Scholar
Rohnd, J.M., Matthews, Y., and Jones, D.A. (1980). A quick simple and reliable method for ATPase in human muscle preparations. Histochem. J.12, 707–709.10.1007/BF01012026Suche in Google Scholar
Rundell, K.W., Tullson, P.C., and Terjung, R.L. (1992). Altered kinetics of AMP deaminase by myosin binding. Am. J. Physiol.263, C294–299.10.1152/ajpcell.1992.263.2.C294Suche in Google Scholar
Sabina, R.L., Swain, J.L., Olanow, C.W., Bradley, W.G., Fishbein, W.N., DiMauro, S., and Holmes, H.W. (1984). Myoadenylate deaminase deficiency. Functional and metabolic abnormalities associated with disruption of the purine nucleotide cycle. J. Clin. Invest.73, 720–730.Suche in Google Scholar
Sabina, R.L., Morisaki, T., Clarke, P., Eddy, R., Shows, T.B., Morton, C.C., and Holmes, W. (1990). Characterization of the human and rat myoadenylate deaminase genes. J. Biol. Chem.265, 9423–19433.10.1016/S0021-9258(19)38866-0Suche in Google Scholar
Sabina, R.L., Fishbein, W.N., Pezeshkpour, G., Clarke, P.R., and Holmes, E.W. (1992). Molecular analysis of the myoadenylate deaminase deficiencies. Neurology42, 170–179.10.1212/WNL.42.1.170Suche in Google Scholar
Tarnopolsky, M.A., Parise, G., Gibala, M.J., Graham, T.E., and Rush, J.W.E. (2001). Myoadenylate deaminase deficiency does not affect muscle anaplerosis during exhaustive exercise in humans. J. Physiol.533, 881–889.10.1111/j.1469-7793.2001.t01-1-00881.xSuche in Google Scholar
Tullson, P.C. and Terjung, R.L. (1991). Adenosine nucleotide metabolism in contracting skeletal muscle. Exer. Sport Sci. Rev.14, 507–536.Suche in Google Scholar
Tullson, P.C. and Terjung, R.L. (1999). IMP degradative capacity in rat skeletal muscle fiber types. Mol. Cell. Biochem.199, 111–117.10.1023/A:1006924318114Suche in Google Scholar
Tullson, P.C., Whitlock, D.M., and Terjung, R.L. (1990). Adenine nucleotide degradation in slow-twitch red muscle. Am. J. Physiol.258, C258–265.10.1152/ajpcell.1990.258.2.C258Suche in Google Scholar
Verzijl, H.T., van Engelen, B.G., Luyten, J.A., Steenbergen, G.C., van den Heuvel, L.P., ter Laak, H.J., Padberg, G.W., and Wevers, R.A. (1998). Genetic characterization of myoadenylate deaminase deficiency. Ann. Neurol.44, 140–143.10.1002/ana.410440124Suche in Google Scholar
Yazaki, Y., Muhlestein, J.B., Carlquist, J.F., Bair, T.L., Horne, B.D., Renlund, D.G., and Anderson, J.L. (2004). A common variant of the AMPD1 gene predicts improved survival in patients with ischemic left ventricular dysfunction. J. Card. Fail.10, 316–1320.10.1016/j.cardfail.2003.10.008Suche in Google Scholar
Zimmermann, H. (2000). Extracellular metabolism of ATP and other nucleotides. Naunyn-Schmiedeberg's Arch. Pharmacol.362, 299–309.10.1007/s002100000309Suche in Google Scholar PubMed
Zöllner, N., Reiter, S., and Gross, M. (1986). Myoadenylate deaminase deficiency: successful symptomatic therapy by high dose oral administration of ribose. Klin. Wochenschr.64, 1281–1290.10.1007/BF01785710Suche in Google Scholar PubMed
©2006 by Walter de Gruyter Berlin New York
Artikel in diesem Heft
- Editor's Note
- Endothelial mediators and communication through vascular gap junctions
- Bradykinin and peripheral sensitization
- Renal gene expression profiling using kinin B1 and B2 receptor knockout mice reveals comparable modulation of functionally related genes
- Solvent-induced changes in photochemical activity and conformation of photosystem I particles by glycerol
- Interaction of the BELL-like protein ATH1 with DNA: role of homeodomain residue 54 in specifying the different binding properties of BELL and KNOX proteins
- Vitamin B1de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine
- Ecto- and cytosolic 5′-nucleotidases in normal and AMP deaminase-deficient human skeletal muscle
- Dual signal transduction mediated by a single type of olfactory receptor expressed in a heterologous system
- Modulation of autocrine TNF-α-stimulated matrix metalloproteinase 9 (MMP-9) expression by mitogen-activated protein kinases in THP-1 monocytic cells
- The PAK1 autoregulatory domain is required for interaction with NIK in Helicobacter pylori-induced NF-κB activation
- Aflatoxin B1-induced toxicity in HepG2 cells inhibited by carotenoids: morphology, apoptosis and DNA damage
- Detection of prion particles in samples of BSE and scrapie by fluorescence correlation spectroscopy without proteinase K digestion
- A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration
- NF-κB contributes to transcription of placenta growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells
Artikel in diesem Heft
- Editor's Note
- Endothelial mediators and communication through vascular gap junctions
- Bradykinin and peripheral sensitization
- Renal gene expression profiling using kinin B1 and B2 receptor knockout mice reveals comparable modulation of functionally related genes
- Solvent-induced changes in photochemical activity and conformation of photosystem I particles by glycerol
- Interaction of the BELL-like protein ATH1 with DNA: role of homeodomain residue 54 in specifying the different binding properties of BELL and KNOX proteins
- Vitamin B1de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine
- Ecto- and cytosolic 5′-nucleotidases in normal and AMP deaminase-deficient human skeletal muscle
- Dual signal transduction mediated by a single type of olfactory receptor expressed in a heterologous system
- Modulation of autocrine TNF-α-stimulated matrix metalloproteinase 9 (MMP-9) expression by mitogen-activated protein kinases in THP-1 monocytic cells
- The PAK1 autoregulatory domain is required for interaction with NIK in Helicobacter pylori-induced NF-κB activation
- Aflatoxin B1-induced toxicity in HepG2 cells inhibited by carotenoids: morphology, apoptosis and DNA damage
- Detection of prion particles in samples of BSE and scrapie by fluorescence correlation spectroscopy without proteinase K digestion
- A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration
- NF-κB contributes to transcription of placenta growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells