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Abstract:

Compartmentalization of cAMP phosphodiesterases plays a key role in the regulation of cAMP signalling in mammals. In the present paper, we report the characterization and subcellular localization of TcPDE1, the first cAMP-specific phosphodiesterase to be identified from Trypanosoma cruzi. TcPDE1 is part of a small gene family and encodes a 929-amino-acid protein that can complement a heat-shock-sensitive yeast mutant deficient in phosphodiesterase genes. Recombinant TcPDE1 strongly associates with membranes and cannot be released with NaCl or sodium cholate, suggesting that it is an integral membrane protein. This enzyme is specific for cAMP and its activity is not affected by cGMP, Ca2+, calmodulin or fenotiazinic inhibitors. TcPDE1 is sensitive to the phosphodiesterase inhibitor dipyridamole but is resistant to 3-isobutyl-1-methylxanthine, theophylline, rolipram and zaprinast. Papaverine, erythro-9-(2-hydroxy-3-nonyl)-adenine hydrochloride, and vinpocetine are poor inhibitors of this enzyme. Confocal laser scanning of T. cruzi epimastigotes showed that TcPDE1 is associated with the plasma membrane and concentrated in the flagellum of the parasite. The association of TcPDE1 with this organelle was confirmed by subcellular fractionation and cell-disruption treatments. The localization of this enzyme is a unique feature that distinguishes it from all the trypanosomatid phosphodiesterases described so far and indicates that compartmentalization of cAMP phosphodiesterases could also be important in these parasites.

Registro:

Documento: Artículo
Título:Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi
Autor:D'Angelo, M.A.; Sanguineti, S.; Reece, J.M.; Birnbaumer, L.; Torres, H.N.; Flawiá, M.M.
Filiación:Inst. Invest. Ing. Genet. Biol. M., Consejo Nac. de Invest. Cie. y Tec., Universidad de Buenos Aires, Vuelta de Obligado 2490, (1428), Buenos Aires, Argentina
Laboratory of Signal Transduction, Natl. Inst. of Environ. Hlth. Sci., National Institutes of Health, 111 Alexander Drive, Research Triangle Park, NC 27709, United States
Palabras clave:cAMP; Flagellum; Membrane; Phosphodiesterase; Trypanosoma cruzi; Biological membranes; Enzyme inhibition; Enzymes; Genes; Hydrochloric acid; Yeast; Cell disruption; Mutants; Biochemistry; 9 (2 hydroxy 3 nonyl)adenine; amino acid; calcium channel blocking agent; calmodulin inhibitor; chloride; cyclic AMP; cyclic AMP phosphodiesterase; cyclic AMP phosphodiesterase 1; cyclic GMP; dipyridamole; enzyme; isobutylmethylxanthine; membrane protein; papaverine; phosphodiesterase; phosphodiesterase inhibitor; protein inhibitor; protein subunit; recombinant protein; rolipram; sodium chloride; theophylline; unclassified drug; vinpocetine; zaprinast; article; cell disruption; cell fractionation; cell membrane; cell organelle; cellular distribution; chemosensitivity; confocal laser microscopy; controlled study; enzyme activity; enzyme localization; enzyme specificity; epimastigote; flagellum; genetic code; heat shock; membrane; multigene family; nonhuman; nucleotide sequence; parasite; priority journal; protein analysis; protein deficiency; protein secretion; temperature sensitive mutant; Trypanosoma; Trypanosoma cruzi; yeast; 3',5'-Cyclic-Nucleotide Phosphodiesterase; Amino Acid Sequence; Animals; Cell Membrane; Cloning, Molecular; Flagella; Gene Components; Genetic Complementation Test; Microscopy, Confocal; Molecular Sequence Data; Subcellular Fractions; Trypanosoma cruzi; Yeasts; Mammalia; Protozoa; Trypanosoma; Trypanosoma cruzi; Trypanosomatidae
Año:2004
Volumen:378
Número:1
Página de inicio:63
Página de fin:72
DOI: http://dx.doi.org/10.1042/BJ20031147
Título revista:Biochemical Journal
Título revista abreviado:Biochem. J.
ISSN:02646021
CODEN:BIJOA
CAS:9 (2 hydroxy 3 nonyl)adenine, 59262-86-1; amino acid, 65072-01-7; chloride, 16887-00-6; cyclic AMP phosphodiesterase, 9036-21-9; cyclic AMP, 60-92-4; cyclic GMP, 7665-99-8; dipyridamole, 58-32-2; isobutylmethylxanthine, 28822-58-4; papaverine, 58-74-2, 61-25-6; rolipram, 61413-54-5; sodium chloride, 7647-14-5; theophylline, 58-55-9, 5967-84-0, 8055-07-0, 8061-56-1, 99007-19-9; vinpocetine, 42971-09-5; zaprinast, 37762-06-4; 3',5'-Cyclic-Nucleotide Phosphodiesterase, EC 3.1.4.17
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02646021_v378_n1_p63_DAngelo

Referencias:

  • Mehats, C., Andersen, C.M., Filopanti, M., Jin, S.-L.C., Conti, M., Cyclic nucleotide phosphodiesterases and their role in endocrine cell signalling (2002) Trends Endocrinol. Metab., 13, pp. 29-35
  • Torphy, T.J., Phosphodiesterase isozymes: Molecular targets for novel antiasthma agents (1998) Am. J. Respir. Crit. Care Med., 157, pp. 351-370
  • Ouaissi, A., Cornette, J., Schoneck, R., Plumas-Marty, B., Taibi, A., Loyens, M., Capron, A., Fibronectin cleavage fragments provide a growth factor-like activity for the differentiation of Trypanosoma cruzi trypomastigotes to amastigotes (1992) Eur. J. Cell Biol., 59, pp. 68-79
  • Fraidenraich, D., Pena, C., Isola, E.L., Lammel, E.M., Coso, O., Añel, A.D., Pongor, S., Flawiá, M.M., Stimulation of Trypanosoma cruzi adenylyl cyclase by an αD-globin fragment from Triatoma hindgut: Effect on differentiation of epimastigote to trypomastigote forms (1993) Proc. Natl. Acad. Sci. U.S.A., 90, pp. 10140-10144
  • Flawiá, M.M., Téllez-Iñón, M.T., Torres, H.N., Signal transduction mechanisms in Trypanosoma cruzi (1997) Parasitol. Today, 13, pp. 30-33
  • Rangel-Aldao, R., Triana, F., Fernandez, V., Comach, G., Abate, T., Montoreano, R., Cyclic AMP as an inducer of the cell differentiation of Trypanosoma cruzi (1988) Biochem. Int., 17, pp. 337-344
  • Naula, C., Seebeck, T., Cyclic AMP signaling in trypanosomatids (2000) Parasitol. Today, 16, pp. 35-38
  • Seebeck, T., Gong, K.W., Kunz, S., Schaub, R., Shalaby, T., Zoraghi, R., cAMP signalling in Trypanosoma brucei (2001) Int. J. Parasitol., 31, pp. 491-498
  • Taylor, M.C., Muhia, D.K., Baker, D.A., Mondragon, A., Schaap, P.B., Kelly, J.M., Trypanosoma cruzi adenylyl cyclase is encoded by a complex multigene family (1999) Mol. Biochem. Parasitol., 104, pp. 205-217
  • D'Angelo, M.A., Montagna, A.E., Sanguineti, S., Torres, H.N., Flawiá, M.M., A novel calcium-stimulated adenylyl cyclase from Trypanosoma cruzi, which interacts with the structural flagellar protein paraflagellar rod (2002) J. Biol. Chem., 277, pp. 35025-35034
  • Paindavoine, P., Rolin, S., Van Assel, S., Geuskens, M., Jauniaux, J.C., Dinsart, C., Huet, G., Pays, E., A gene from the variant surface glycoprotein expression site encodes one of several transmembrane adenylate cyclases located on the flagellum of Trypanosoma brucei (1992) Mol. Cell. Biol., 12, pp. 1218-1225
  • Téllez-Iñón, M.T., Ulloa, R.M., Torreula, M., Torres, H.N., Calmodulin and Ca2+-dependent cyclic AMP phosphodiesterase activity in Trypanosoma cruzi (1985) Mol. Biochem. Parasitol., 17, pp. 143-153
  • Walter, R.D., Opperdoes, F.R., Subcellular distribution of adenylate cyclase, cyclic-AMP phosphodiesterase, protein kinases and phosphoprotein phosphatase in Trypanosoma brucei (1982) Mol. Biochem. Parasitol., 6, pp. 287-295
  • Walter, R.D., 3′:5′-cyclic-AMP phosphodiesterase from Trypanosoma gambiense (1974) Hoppe Seyler's Z. Physiol. Chem., 355, pp. 1443-1450
  • Ráscon, A., Viloria, M.E., De-Chiara, L., Dubra, M.E., Characterization of cyclic AMP phosphodiesterases in Leishmania mexicana and purification of a soluble form (2000) Mol. Biochem. Parasitol., 106, pp. 283-292
  • Gong, W.K., Kunz, S., Zoraghi, R., Kunz Renggli, C., Brun, R., Seebeck, T., cAMP-specific phosphodiesterase TbPDE1 is not essential in Trypanosoma brucei in culture or during midgut infection of tsetse flies (2001) Mol. Biochem. Parasitol., 116, pp. 229-232
  • Zoraghi, R., Kunz, S., Gong, K., Seebeck, T., Characterization of TbPDE2A, a novel cyclic nucleotide-specific phosphodiesterase from the protozoan parasite Trypanosoma brucei (2001) J. Biol. Chem., 276, pp. 11559-11566
  • Zoraghi, R., Seebeck, T., The cAMP-specific phosphodiesterase TbPDE2C is an essential enzyme in bloodstream form Trypanosoma brucei (2002) Proc. Natl. Acad. Scei. U.S.A., 99, pp. 4343-4348
  • Ráscon, A., Soderling, S.H., Schaefer, J.B., Beavo, J.A., Cloning and characterization of a cAMP-specific phosphodiesterase (TbPDE2B) from Trypanosoma brucei (2002) Proc. Natl. Acad. Sci. U.S.A., 99, pp. 4714-4719
  • Houslay, M.D., Milligan, G., Tailoring cAMP-signalling responses through isoform multiplicity (1997) Trends Biochem. Sci., 22, pp. 217-224
  • Schwartz, J.H., The many dimensions of cAMP signaling (2001) Proc. Natl. Acad. Sci. U.S.A., 98, pp. 13482-13484
  • Zaccolo, M., Pozzan, T., Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes (2002) Science, 295, pp. 1171-1175
  • Florio, S.K., Prusti, R.K., Beavo, J.A., Solubilization of membrane-bound rod phosphodiesterase by the rod phosphodiesterase recombinant δ subunit (1996) J. Biol. Chem., 271, pp. 24036-24047
  • Li, N., Florio, S.K., Pettenati, M.J., Rao, P.N., Beavo, J.A., Baehr, W., Characterization of human and mouse rod cGMP phosphodiesterase δ subunit (PDE6D) and chromosomal localization of the human gene (1998) Genomics, 49, pp. 76-82
  • Jin, S.-L.C., Bushnick, T., Lan, L., Conti, M., Subcellular localization of rolipram-sensitive, cAMP-specific phosphodiesterases: Differential targeting and activation of the splicing variants derived from the PDE4D gene (1998) J. Biol. Chem., 273, pp. 19672-19678
  • Shakur, Y., Takeda, K., Kenan, Y., Yu, Z.X., Rena, G., Brandt, D., Houslay, M.D., Manganiello, V.C., Membrane localization of cyclic nucleotide phosphodiesterase 3 (PDE3): Two N-terminal domains are required for the efficient targeting to, and association of, PDE3 with endoplasmic reticulum (2000) J. Biol. Chem., 275, pp. 38749-38761
  • Wechsler, J., Choi, Y.H., Krall, J., Ahmad, F., Manganiello, V.C., Movsesian, M., Isoforms of cyclic nucleotide phosphodiesterase PDE3A in cardiac myocytes (2002) J. Biol. Chem., 277, pp. 38072-38078
  • Beard, M.B., Huston, E., Campbell, L., Gall, I., McPhee, I., Yarwood, S., Scotland, G., Houslay, M.D., In addition to the SH3 binding region, multiple regions within the N-terminal noncatalytic portion of the cAMP-specific phosphodiesterase, PDE4A5, contribute to its intracellular targeting (2002) Cell Signalling, 14, pp. 453-465
  • Ma, P., Wera, S., Van Dijck, P., Thevelein, J.M., The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signalling (1999) Mol. Biol. Cell, 10, pp. 91-104
  • Pereira, C.A., Alonso, G.D., Paveto, M.C., Iribarren, A., Cabanas, M.L., Torres, H.N., Flawiá, M.M., Trypanosoma cruzi arginine kinase characterization and cloning: A novel energetic pathway in protozoan parasites (2000) J. Biol. Chem., 275, pp. 1495-1501
  • Zingales, B., Rondinelli, E., Degrave, W., Da Silevira, F., Levin, M., Le Paslier, D., Modabber, F., Kelly, J.M., The Trypanosoma cruzi genome initiative (1997) Parasitol. Today, 13, pp. 16-22
  • Colicelli, J., Bircheier, C., Michaeli, T., O'Neill, K., Riggs, M., Wigler, M., Isolation and characterization of a mammalian gene encoding a high-affinity cAMP phosphodiesterase (1989) Proc. Natl. Acad. Sci. U.S.A., 86, pp. 3599-3603
  • Gietz, R.D., Schiestl, R.H., Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier (1991) Yeast, 7, pp. 253-263
  • Gómez, M.L., Erijman, L., Arauzo, S., Torres, H.N., Téllez- Iñón, M.T., Protein kinase C in Trypanosoma cruzi epimastigote forms: Partial purification and characterization (1989) Mol. Biochem. Parasitol., 36, pp. 101-108
  • Boudreau, R.J., Drummond, G.I., A modified assay of 3′:5′-cyclic-AMP phosphodiesterase (1975) Anal. Biochem., 63, pp. 388-399
  • Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature (London), 227, pp. 680-685
  • Godsel, L.M., Engman, D.M., Flagellar protein localization mediated by a calcium-myristoyl/palmitoyl switch mechanism (1999) EMBO J., 18, pp. 2057-2065
  • Ersfeld, K., Gull, K., Targeting of cytoskeletal proteins to the flagellum of Trypanosoma brucei (2001) J. Cell Sci., 114, pp. 141-148
  • Henras, A., Henry, Y., Bousquet-Antonelli, C., Noaillac-Depeyre, J., Gélugne, J.P., Caizergues-Ferrer, M., Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs (1998) EMBO J., 17, pp. 7078-7090
  • Pogacic, V., Dragon, F., Filipowicz, W., Human H/ACA small nucleolar RNPs and telomerase share evolutionary conserved proteins NHP2 and NOP10 (2000) Mol. Cell. Biol., 20, pp. 9028-9040
  • Atienza, J.M., Colicelli, J., Yeast model system for study of mammalian phosphodiesterases (1998) Methods, 14, pp. 35-42
  • Kanacher, T., Schultz, A., Linder, J.U., Schultz, J.E., A GAF-domain-regulated adenylyl cyclase from Anabaena is a self-activating cAMP switch (2002) EMBO J., 21, pp. 3672-3680
  • Muradov, K.G., Boyd, K.K., Martinez, S.E., Beavo, J.A., Artemyev, N.O., The GAFa domains of rod cGMP-phosphodiesterase 6 determine the selectivity of the enzyme dimerization (2003) J. Biol. Chem., 278, pp. 10594-10601
  • Martinez, S.E., Wu, A.Y., Glavas, N.A., Tang, X., Turley, S., Hol, W.G.J., Beavo, J.A., The two GAF domains in phosphodiesterase 2A have distinct roles in dimerization and in cGMP binding (2002) Proc. Natl. Acad. Sci. U.S.A., 99, pp. 13260-13265
  • Zaccolo, M., Magalhaes, P., Pozzan, T., Compartmentalisation of cAMP and Ca2+ signals (2002) Curr. Opin. Cell Biol., 14, pp. 160-166
  • Rich, T.C., Fagan, K.A., Tse, T.E., Schaack, J., Cooper, D.M., Karpen, J.W., A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell (2001) Proc. Natl. Acad. Sci. U.S.A., 98, pp. 13049-13054
  • Colledge, M., Scott, J.D., AKAPs: From structure to function (1999) Trends Cell Biol., 9, pp. 216-221

Citas:

---------- APA ----------
D'Angelo, M.A., Sanguineti, S., Reece, J.M., Birnbaumer, L., Torres, H.N. & Flawiá, M.M. (2004) . Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi. Biochemical Journal, 378(1), 63-72.
http://dx.doi.org/10.1042/BJ20031147
---------- CHICAGO ----------
D'Angelo, M.A., Sanguineti, S., Reece, J.M., Birnbaumer, L., Torres, H.N., Flawiá, M.M. "Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi" . Biochemical Journal 378, no. 1 (2004) : 63-72.
http://dx.doi.org/10.1042/BJ20031147
---------- MLA ----------
D'Angelo, M.A., Sanguineti, S., Reece, J.M., Birnbaumer, L., Torres, H.N., Flawiá, M.M. "Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi" . Biochemical Journal, vol. 378, no. 1, 2004, pp. 63-72.
http://dx.doi.org/10.1042/BJ20031147
---------- VANCOUVER ----------
D'Angelo, M.A., Sanguineti, S., Reece, J.M., Birnbaumer, L., Torres, H.N., Flawiá, M.M. Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi. Biochem. J. 2004;378(1):63-72.
http://dx.doi.org/10.1042/BJ20031147