Abstract
Monoamine oxidase (MAO) and semicarbazide-sensitive amine oxidase (SSAO) activities are very high in white adipose tissue (WAT). SSAO, also known as Vascular Adhesion Protein-1 in vessels, is present at the surface of fat cells and independent approaches have evidenced its impressive increase during adipogenesis. However, the factors that might regulate the expression SSAO and MAO in adipose tissue are still poorly defined. Here, we report the influence of fasting on MAO and SSAO activities in adipose depots. A decrease of MAO activity occurred after three days of starvation in the intra-abdominal adipose tissue (INWAT) of male Wistar rats, regardless of their initial adiposity or fat loss. The reduced fat stores of seven-week old rats, loosing 59% of INWAT mass during fasting, contained only one half of the MAO activity found in fed control. The same reduction of MAO was observed after prolonged fasting in older rats which lose only 26% of their INWAT during the same starvation duration, leading to a fat mass comparable to that of younger fed control rats. It was therefore the endocrine and metabolic changes occurring during fasting that were responsible for the reduced MAO activity and not the amount of INWAT. Surprisingly, SSAO activity remained unchanged during starvation. In subcutaneous WAT, the changes in MAO and SSAO activities exhibited the same tendencies than those found in INWAT. Taken together, these data show that both MAO and SSAO activities increase in INWAT with age-dependent fattening, and indicate that only MAO diminishes during fasting.
Resumen
La actividad monoamino oxidasa (MAO) y aminooxidasa sensible al semicarbazide (SSAO) están muy elevadas en el tejido adiposo blanco (TAB). SSAO, también conocida como proteína de adhesión vascular-1, está presente en la superficie de los adipocitos maduros. Diferentes investigaciones muestran incremento de su expresión durante la adipogénesis, aunque los factores que regulan la expresión en el TAB no son bien conocidos. Este trabajo describe la influencia del ayuno sobre la actividad MAO y SSAO en TAB. Se ha observado que tras tres días de ayuno disminuye la actividad MAO en el tejido adiposo intra-abdominal (INWAT) de ratas macho Wistar, independientemente de la grasa inicial o de la pérdida de peso inducida por el ayuno. El ayuno redujo un 59% el peso del INWAT y un 50% la actividad MAO en ratas de 7 semanas de edad comparadas con su control (ratas sin ayuno). La misma disminución de la actividad MAO se encontró en ratas de mayor edad (10 semanas) aunque solo perdieron el 26 % de su INWAT durante el mismo ayuno, igualando dicha reserva grasa a la de las ratas más jóvenes sin ayunar. Los resultados indican que serían los cambios endocrinos y metabólicos que ocurren durante el ayuno los responsables de la disminución de la actividad MAO y no la perdida de tejido adiposo en sí. Sorprendentemente, no se observó ningún cambio significativo en la actividad SSAO durante el ayuno. En el tejido adiposo subcutáneo, los cambios de actividad MAO y SSAO mostraron las mismas tendencias que en el INWAT. Los resultados muestran que la edad conlleva un aumento de la actividad de la MAO y de la SSAO en tejido adiposo blanco de rata y que el ayuno reduce la actividad de la MAO, no la de la SSAO.
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References
Abella, A., García-Vicente, S., Viguerie, N., Ros-Baro, A., Camps, M., Palacin, M., Zorzano, A., Marti, L. (2004): Adipocytes release a soluble form of VAP-1/SSAO by a metalloprotease-dependent process and in a regulated manner.Diabetologia,47, 429–438.
Abella, A., Marti, L., Carpéné, C., Palacin, M., Testar, X., Zorzano, A. (2003): Stimulation of glucose transport by semicarbazide-sensitive amine oxidase activity in adipocytes from diabetic rats.J Physiol Biochem,59, 153–160.
Bairras, C., Ferrand, C., Atgié, C. (2003): Effect of tyramine, a dietary amine, on glycerol and lactate release by isolated adipocytes from old rats.J Physiol Biochem,59, 161–168.
Bairras, C., Mauriège, P., Bukowiecki, L., Atgié, C. (2007): Regulation of lipolysis in white adipose tissues of lean and obese Zucker rats.J Physiol Biochem,63, 287–296.
Boomsma, F., Bhaggoe, U.M., van der Houwen, A.M., van den Meiracker, A.H. (2003): Plasma semicarbazide-sensitive amine oxidase in human (patho) physiology.Biochim Biophys Acta,1647, 48–54.
Bour, S., Daviaud, D., Gres, S., Lefort, C., Prévot, D., Zorzano, A., Wabitsch, M., Saulnier-Blache, J.-S., Valet, P., Carpéné, C. (2007): Adipogenesis-related increase of semicarbazide-sensitive amine oxidase and monoamine oxidase in human adipocytes.Biochimie,89, 916–925.
Conforti, L., Pirisino, R., Ignesti, G., Banchelli, G., Raimondi, L. (1995): Semicarbazide-sensitive amine oxidase activity in white adipose tissue of the insulin-deficient rat.J Pharm Pharmacol,47, 420–424.
Duffaut, C., Bour, S., Prévot, D., Marti, L., Testar, X., Zorzano, A., Carpéné, C. (2006): Prolonged treatment with the β3-adrenergic agonist CL 316243 induces adipose tissue remodeling in rat but not in guinea pig: 2) modulation of glucose uptake and monoamine oxidase activity.J Physiol Biochem,62, 101–112.
Ferrand, C., Redonnet A., Prévot, D., Carpéné, C., Atgié, C. (2006): Prolonged treatment with the β3-adrenergic agonist CL 316243 induces adipose tissue remodeling in rat but not in guinea pig: 1) fat store depletion and desensitization of β3-adrenergic responses.J Physiol Biochem,62, 89–100.
García-Vicente, S., Abella, A., Viguerie, N., Ros-Baró, A., Camps, M., Testar, X., Palacín, M., Zorzano, A., Marti, L. (2005): The release of soluble VAP1/SSAO by 3T3-L1 adipocytes is timulated by isoproterenol and low concentrations of TNF alpha.J Physiol Biochem,61, 395–404.
Giordano, A., Frontini, A., Murano, I., Tonello, C., Marino, M. A., Carruba, M. O., Nisoli, E., Cinti, S. (2005): Regional-dependent increase of sympathetic innervation in rat white adipose tissue during prolonged fasting.J Histochem Cytochem,53, 679–687.
Granneman, J. G., Li, P., Zhu, Z., Lu, Y. (2005): Metabolic and cellular plasticity in white adipose tissue I: effects of β3-adrenergic receptor activation.Am J Physiol Endocrinol Metab,289, E608-E616.
Marti, L., Morin, N., Enrique-Tarancon, G., Prévot, D., Lafontan, M., Testar, X., Zorzano, A., Carpéné, C. (1998): Tyramine and vanadate synergistically stimulate glucose transport in rat adipocytes by amine oxidase-dependent generation of hydrogen peroxide.J Pharmacol Exp Ther,285, 342–349.
Mercier, N., Moldes, M., El Hadri, K., Fève, B. (2001): Semicarbazide-sensitive amine oxidase activation promotes adipose conversion of 3T3-L1 cells.Biochem j,358, 335–342.
Mercier, N., Moldes, M., El Hadri, K., Fève, B. (2003): Regulation of semicarbazide-sensitive amine oxidase expression by tumor necrosis factor-α in adipocytes: functional consequences on glucose trtansport.J Pharmacol Exp Ther,304, 1197–1208.
Minet-Ringuet, J., Even, P.C., Valet, P., Carpéné, C., Visentin, V., Prévot, D., Daviaud, D., Quignard-Boulangé, A., Tomé, D., de Beaurepaire, R. (2007): Alterations of lipid metabolism and gene expression in rat adipocytes during chronic olanzapine treatment.Mol Psychiatry,12, 562–571.
Moldes, M., Fève, B., Pairault, J. (1999): Molecular cloning of a major mRNA species in murine 3T3 adipocyte lineage. Differentiation-dependent expression, regulation, and identification as semicarbazide-sensitive amine oxidase.J Biol Chem,274, 9515–9523.
Morin, N., Lizcano, J.M., Fontana, E., Marti, L., Smih, F., Rouet, P., Prévot, D., Zorzano, A., Unzeta, M., Carpéné, C. (2001). Semicarbazidesensitive amine oxidase substrates stimulate glucose transport and inhibit lipolysis in human adipocytes.J Pharmacol Exp Ther,297, 563–572.
Morin, N., Visentin, V., Calise, D., Marti, L., Zorzano, A., Testar, X., Valet, P., Fischer, Y., Carpéné, C. (2002): Tyramine stimulates glucose uptake in insulin-sensitive tissues in vitro and in vivo via its oxidation by amine oxidases.J Pharmacol Exp Ther,303, 1238–1247.
Salmi, M., Yegutkin, G.G., Lehvonen, R., Koskinen, K., Salminen, T., Jalkanen, S. (2001): A cell surface amine oxidase directly controls lymphocyte migration.Immunity,14, 265–276.
Stolen, C.M., Yegutkin, G.G., Kurkijarvi, R., Bono, P., Alitalo, K., Jalkanen, S. (2004): Origins of serum semicarbazide-sensitive amine oxidase.Circ Res,95, 50–57.
Subra, C., Fontana, E., Visentin, V., Testar, X., Carpéné, C. (2003): Tyramine and benzylamine partially but selectively mimic insulin action on adipose differentiation in 3T3-L1 cells.J Physiol Biochem,59, 209–216.
Visentin, V., Boucher, J., Bour, S., Prévot, D., Castan, I., Carpéné, C., Valet, P. (2005): Influence of high-fat diet on amine oxidase activity in white adipose tissue of mice prone or resistant to diet-induced obesity.J Physiol Biochem,61, 343–352.
Visentin, V., Bour, S., Boucher, J., Prévot, D., Valet, P., Ordener, C., Parini, A., Carpéné, C. (2005): Glucose handling in streptozotocin-induced diabetic rats is improved by tyramine but not by the amine oxidase inhibitor semicar-bazide.Eur J Pharmacol,522, 139–146.
Visentin, V., Prévot, D., De Saint Front, V. D., Morin-Cussac, N., Thalamas, C., Galitzky, J., Valet, P., Zorzano, A., Carpéné, C. (2004): Alteration of amine oxidase activity in the adipose tissue of obese subjects.Obesity Res,12, 547–555.
Visentin, V., Prévot, D., Marti, L., Carpéné, C. (2003): Inhibition of rat fat cell lipolysis by monoamine oxidase and semicarbazide-sensitive amine oxidase substrates.Eur J Pharmacol,466, 235–243.
Wanecq, E., Bour, S., Verwaerde, P., Smih, F., Valet, P., Carpéné, C. (2006): Increased monoamine oxidase and semicarbazide-sensitive amine oxidase activities in white adipose tissue of obese dogs fed a high-fat diet.J Physiol Biochem,62, 113–123.
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Iffiú-Soltész, Z., Prévot, D. & Carpéné, C. Influence of prolonged fasting on monoamine oxidase and semicarbazide-sensitive amine oxidase activities in rat white adipose tissue. J. Physiol. Biochem. 65, 11–23 (2009). https://doi.org/10.1007/BF03165965
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DOI: https://doi.org/10.1007/BF03165965