Abstract:
Intracellular levels of cyclic nucleotide second messengers are regulated predominantly by a large superfamily of phosphodiesterases (PDEs). Trypanosoma cruzi, the causative agent of Chagas disease, encodes four different PDE families. One of these PDEs, T. cruzi PDE C2 (TcrPDEC2) has been characterized as a FYVE domain containing protein. Here, we report a novel role for TcrPDEC2 in osmoregulation in T. cruzi and reveal the relevance of its FYVE domain. Our data show that treatment of epimastigotes with TcrPDEC2 inhibitors improves their regulatory volume decrease, whereas cells overexpressing this enzyme are unaffected by the same inhibitors. Consistent with these results, TcrPDEC2 localizes to the contractile vacuole complex, showing strong labelling in the region corresponding to the spongiome. Furthermore, transgenic parasites overexpressing a truncated version of TcrPDEC2 without the FYVE domain show a failure in its targeting to the contractile vacuole complex and a marked decrease in PDE activity, supporting the importance of this domain to the localization and activity of TcrPDEC2. Taking together, the results here presented are consistent with the importance of the cyclic AMP signalling pathway in regulatory volume decrease and implicate TcrPDEC2 as a specifically localized PDE involved in osmoregulation in T. cruzi. © 2010 Blackwell Publishing Ltd.
Registro:
Documento: |
Artículo
|
Título: | Defining the role of a FYVE domain in the localization and activity of a cAMP phosphodiesterase implicated in osmoregulation in Trypanosoma cruzi |
Autor: | Schoijet, A.C.; Miranda, K.; Medeiros, L.C.S.; De Souza, W.; Flawiá, M.M.; Torres, H.N.; Pignataro, O.P.; Docampo, R.; Alonso, G.D. |
Filiación: | Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Consejo Nacional de Investigaciones Científicas y Técnicas, Vuelta de Obligado 2490, C1428ADN Buenos Aires, Argentina Center for Tropical and Emerging Global Diseases, Department of Cellular Biology, University of Georgia, Athens, GA 30602, United States Lab. de Ultraestrutura Celular Hertha Meyer, Instituto de Biofisica Carlos Chagas Filho, Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Universidade Federal do Rio de Janeiro, Brazil Instituto Nacional de Metrologia, Normalização e Qualidade Industrial, INMETRO, Rio de Janeiro, Brazil Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina Laboratorio de Endocrinología Molecular y Transducción de Señales, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas, Vuelta de Obligado 2490, C1428ADN Buenos Aires, Argentina Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
|
Palabras clave: | cyclic AMP phosphodiesterase; article; cell vacuole; controlled study; enzyme activity; epimastigote; gene overexpression; immunofluorescence microscopy; nonhuman; osmoregulation; priority journal; protein binding; protein domain; protein localization; radioimmunoassay; signal transduction; transgene; Trypanosoma cruzi; 3',5'-Cyclic-AMP Phosphodiesterases; Enzyme Inhibitors; Gene Expression; Microscopy, Immunoelectron; Protein Structure, Tertiary; Trypanosoma cruzi; Vacuoles; Water-Electrolyte Balance; Trypanosoma cruzi |
Año: | 2011
|
Volumen: | 79
|
Número: | 1
|
Página de inicio: | 50
|
Página de fin: | 62
|
DOI: |
http://dx.doi.org/10.1111/j.1365-2958.2010.07429.x |
Título revista: | Molecular Microbiology
|
Título revista abreviado: | Mol. Microbiol.
|
ISSN: | 0950382X
|
CODEN: | MOMIE
|
CAS: | cyclic AMP phosphodiesterase, 9036-21-9; 3',5'-Cyclic-AMP Phosphodiesterases, 3.1.4.17; Enzyme Inhibitors
|
PDF: | https://bibliotecadigital.exactas.uba.ar/download/paper/paper_0950382X_v79_n1_p50_Schoijet.pdf |
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0950382X_v79_n1_p50_Schoijet |
Referencias:
- Allen, R.D., Tominaga, T., Naitoh, Y., Osmotic and Ionic Regulation (2009) The contractile vacuole complex and cell volume regulation, pp. 69-105. , Evans, D.H. (ed.). Boca Raton: CRC Press, Taylor & Francis Group
- Alonso, G.D., Schoijet, A.C., Torres, H.N., Flawia, M.M., TcPDE4, a novel membrane-associated cAMP-specific phosphodiesterase from Trypanosoma cruzi (2006) Mol Biochem Parasitol, 145, pp. 40-49
- Alonso, G.D., Schoijet, A.C., Torres, H.N., Flawia, M.M., TcrPDEA1, a cAMP-specific phosphodiesterase with atypical pharmacological properties from Trypanosoma cruzi (2007) Mol Biochem Parasitol, 152, pp. 72-79
- Baillie, G.S., Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases (2009) FEBS J, 276, pp. 1790-1799
- Baillie, G.S., Scott, J.D., Houslay, M.D., Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract (2005) FEBS Lett, 579, pp. 3264-3270
- Banerjee, S., Basu, S., Sarkar, S., Comparative genomics reveals selective distribution and domain organization of FYVE and PX domain proteins across eukaryotic lineages (2010) BMC Genomics, 11, p. 83
- Bao, Y., Weiss, L.M., Braunstein, V.L., Huang, H., Role of protein kinase A in Trypanosoma cruzi (2008) Infect Immun, 76, pp. 4757-4763
- Bender, A.T., Beavo, J.A., Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use (2006) Pharmacol Rev, 58, pp. 488-520
- Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D.C., The genome of the African trypanosome Trypanosoma brucei (2005) Science, 309, pp. 416-422
- Bhattacharya, A., Biswas, A., Das, P.K., Role of a differentially expressed cAMP phosphodiesterase in regulating the induction of resistance against oxidative damage in Leishmania donovani (2009) Free Radic Biol Med, 47, pp. 1494-1506
- Blatner, N.R., Stahelin, R.V., Diraviyam, K., Hawkins, P.T., Hong, W., Murray, D., Cho, W., The molecular basis of the differential subcellular localization of FYVE domains (2004) J Biol Chem, 279, pp. 53818-53827
- Caceres, A.J., Portillo, R., Acosta, H., Rosales, D., Quinones, W., Avilan, L., Molecular and biochemical characterization of hexokinase from Trypanosoma cruzi (2003) Mol Biochem Parasitol, 126, pp. 251-262
- Callaghan, J., Simonsen, A., Gaullier, J.M., Toh, B.H., Stenmark, H., The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer (1999) Biochem J, 338, pp. 539-543
- Clark, T.B., Comparative morphology of four genera of trypanosomatidae (1959) J Protozool, 6, pp. 227-232
- Conti, M., Phosphodiesterases and cyclic nucleotide signaling in endocrine cells (2000) Mol Endocrinol, 14, pp. 1317-1327
- Conti, M., Beavo, J., Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling (2007) Annu Rev Biochem, 76, pp. 481-511
- Cooper, D.M., Compartmentalization of adenylate cyclase and cAMP signalling (2005) Biochem Soc Trans, 33, pp. 1319-1322
- Cullen, P.J., Cozier, G.E., Banting, G., Mellor, H., Modular phosphoinositide-binding domains - their role in signalling and membrane trafficking (2001) Curr Biol, 11, pp. R882-R893
- D'Angelo, M.A., Sanguineti, S., Reece, J.M., Birnbaumer, L., Torres, H.N., Flawia, M.M., Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi (2004) Biochem J, 378, pp. 63-72
- Del Punta, K., Charreau, E.H., Pignataro, O.P., Nitric oxide inhibits Leydig cell steroidogenesis (1996) Endocrinology, 137, pp. 5337-5343
- Diraviyam, K., Stahelin, R.V., Cho, W., Murray, D., Computer modeling of the membrane interaction of FYVE domains (2003) J Mol Biol, 328, pp. 721-736
- Drobak, B.K., Heras, B., Nuclear phosphoinositides could bring FYVE alive (2002) Trends Plant Sci, 7, pp. 132-138
- Dumas, J.J., Merithew, E., Sudharshan, E., Rajamani, D., Hayes, S., Lawe, D., Multivalent endosome targeting by homodimeric EEA1 (2001) Mol Cell, 8, pp. 947-958
- El-Sayed, N.M., Myler, P.J., Bartholomeu, D.C., Nilsson, D., Aggarwal, G., Tran, A.N., The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease (2005) Science, 309, pp. 409-415
- Flawia, M.M., Tellez-Inon, M.T., Torres, H.N., Signal transduction mechanisms in Trypanosoma cruzi (1997) Parasitol Today, 13, pp. 30-33
- Halpin, D.M., ABCD of the phosphodiesterase family: interaction and differential activity in COPD (2008) Int J Chron Obstruct Pulmon Dis, 3, pp. 543-561
- Hayakawa, A., Hayes, S., Leonard, D., Lambright, D., Corvera, S., Evolutionarily conserved structural and functional roles of the FYVE domain (2007) Biochem Soc Symp, pp. 95-105
- Houslay, M.D., Adams, D.R., PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization (2003) Biochem J, 370, pp. 1-18
- Houslay, M.D., Milligan, G., Tailoring cAMP-signalling responses through isoform multiplicity (1997) Trends Biochem Sci, 22, pp. 217-224
- Ivens, A.C., Peacock, C.S., Worthey, E.A., Murphy, L., Aggarwal, G., Berriman, M., The genome of the kinetoplastid parasite, Leishmania major (2005) Science, 309, pp. 436-442
- King-Keller, S., Li, M., Smith, A., Zheng, S., Kaur, G., Yang, X., Chemical validation of phosphodiesterase C as a chemotherapeutic target in Trypanosoma cruzi, the etiological agent of Chagas' disease (2010) Antimicrob Agents Chemother, 54, pp. 3738-3745
- Kunz, S., Oberholzer, M., Seebeck, T., A FYVE-containing unusual cyclic nucleotide phosphodiesterase from Trypanosoma cruzi (2005) FEBS J, 272, pp. 6412-6422
- Kutateladze, T.G., Mechanistic similarities in docking of the FYVE and PX domains to phosphatidylinositol 3-phosphate containing membranes (2007) Prog Lipid Res, 46, pp. 315-327
- Kutateladze, T., Overduin, M., Structural mechanism of endosome docking by the FYVE domain (2001) Science, 291, pp. 1793-1796
- Kutateladze, T.G., Capelluto, D.G., Ferguson, C.G., Cheever, M.L., Kutateladze, A.G., Prestwich, G.D., Overduin, M., Multivalent mechanism of membrane insertion by the FYVE domain (2004) J Biol Chem, 279, pp. 3050-3057
- Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature, 227, pp. 680-685
- Lawe, D.C., Patki, V., Heller-Harrison, R., Lambright, D., Corvera, S., The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization (2000) J Biol Chem, 275, pp. 3699-3705
- Laxman, S., Beavo, J.A., Cyclic nucleotide signaling mechanisms in trypanosomes: possible targets for therapeutic agents (2007) Mol Interv, 7, pp. 203-215
- Lee, S.A., Eyeson, R., Cheever, M.L., Geng, J., Verkhusha, V.V., Burd, C., Targeting of the FYVE domain to endosomal membranes is regulated by a histidine switch (2005) Proc Natl Acad Sci USA, 102, pp. 13052-13057
- Lemmon, M.A., Phosphoinositide recognition domains (2003) Traffic, 4, pp. 201-213
- Lugnier, C., Cyclic nucleotide phosphodiesterase families in intracellular signaling and diabetes (2001) Adv Exp Med Biol, 498, pp. 253-261
- Martin, T.F., Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking (1998) Annu Rev Cell Dev Biol, 14, pp. 231-264
- Minning, T.A., Weatherly, D.B., Atwood III, J., Orlando, R., Tarleton, R.L., The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi (2009) BMC Genomics, 10, p. 370
- Mondillo, C., Pagotto, R.M., Piotrkowski, B., Reche, C.G., Patrignani, Z.J., Cymeryng, C.B., Pignataro, O.P., Involvement of nitric oxide synthase in the mechanism of histamine-induced inhibition of Leydig cell steroidogenesis via histamine receptor subtypes in Sprague-Dawley rats (2009) Biol Reprod, 80, pp. 144-152
- Montalvetti, A., Rohloff, P., Docampo, R., A functional aquaporin co-localizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi (2004) J Biol Chem, 279, pp. 38673-38682
- Omori, K., Kotera, J., Overview of PDEs and their regulation (2007) Circ Res, 100, pp. 309-327
- Payrastre, B., Missy, K., Giuriato, S., Bodin, S., Plantavid, M., Gratacap, M., Phosphoinositides: key players in cell signalling, in time and space (2001) Cell Signal, 13, pp. 377-387
- Pereira, C.A., Alonso, G.D., Paveto, M.C., Iribarren, A., Cabanas, M.L., Torres, H.N., Flawia, M.M., Trypanosoma cruzi arginine kinase characterization and cloning. A novel energetic pathway in protozoan parasites (2000) J Biol Chem, 275, pp. 1495-1501
- Psachoulia, E., Sansom, M.S., PX- and FYVE-mediated interactions with membranes: simulation studies (2009) Biochemistry, 48, pp. 5090-5095
- Rohloff, P., Docampo, R., A contractile vacuole complex is involved in osmoregulation in Trypanosoma cruzi (2008) Exp Parasitol, 118, pp. 17-24
- Rohloff, P., Rodrigues, C.O., Docampo, R., Regulatory volume decrease in Trypanosoma cruzi involves amino acid efflux and changes in intracellular calcium (2003) Mol Biochem Parasitol, 126, pp. 219-230
- Rohloff, P., Montalvetti, A., Docampo, R., Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi (2004) J Biol Chem, 279, pp. 52270-52281
- Scott, J.D., Compartmentalized cAMP signalling: a personal perspective (2006) Biochem Soc Trans, 34, pp. 465-467
- Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J.M., Brech, A., Callaghan, J., EEA1 links PI(3)K function to Rab5 regulation of endosome fusion (1998) Nature, 394, pp. 494-498
- Stahelin, R.V., Long, F., Diraviyam, K., Bruzik, K.S., Murray, D., Cho, W., Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs (2002) J Biol Chem, 277, pp. 26379-26388
- Vazquez, M.P., Levin, M.J., Functional analysis of the intergenic regions of TcP2beta gene loci allowed the construction of an improved Trypanosoma cruzi expression vector (1999) Gene, 239, pp. 217-225
- Wilkinson, S.R., Meyer, D.J., Taylor, M.C., Bromley, E.V., Miles, M.A., Kelly, J.M., The Trypanosoma cruzi enzyme TcGPXI is a glycosomal peroxidase and can be linked to trypanothione reduction by glutathione or tryparedoxin (2002) J Biol Chem, 277, pp. 17062-17071
- Zhu, Q., Clarke, M., Association of calmodulin and an unconventional myosin with the contractile vacuole complex of Dictyostelium discoideum (1992) J Cell Biol, 118, pp. 347-358
Citas:
---------- APA ----------
Schoijet, A.C., Miranda, K., Medeiros, L.C.S., De Souza, W., Flawiá, M.M., Torres, H.N., Pignataro, O.P.,..., Alonso, G.D.
(2011)
. Defining the role of a FYVE domain in the localization and activity of a cAMP phosphodiesterase implicated in osmoregulation in Trypanosoma cruzi. Molecular Microbiology, 79(1), 50-62.
http://dx.doi.org/10.1111/j.1365-2958.2010.07429.x---------- CHICAGO ----------
Schoijet, A.C., Miranda, K., Medeiros, L.C.S., De Souza, W., Flawiá, M.M., Torres, H.N., et al.
"Defining the role of a FYVE domain in the localization and activity of a cAMP phosphodiesterase implicated in osmoregulation in Trypanosoma cruzi"
. Molecular Microbiology 79, no. 1
(2011) : 50-62.
http://dx.doi.org/10.1111/j.1365-2958.2010.07429.x---------- MLA ----------
Schoijet, A.C., Miranda, K., Medeiros, L.C.S., De Souza, W., Flawiá, M.M., Torres, H.N., et al.
"Defining the role of a FYVE domain in the localization and activity of a cAMP phosphodiesterase implicated in osmoregulation in Trypanosoma cruzi"
. Molecular Microbiology, vol. 79, no. 1, 2011, pp. 50-62.
http://dx.doi.org/10.1111/j.1365-2958.2010.07429.x---------- VANCOUVER ----------
Schoijet, A.C., Miranda, K., Medeiros, L.C.S., De Souza, W., Flawiá, M.M., Torres, H.N., et al. Defining the role of a FYVE domain in the localization and activity of a cAMP phosphodiesterase implicated in osmoregulation in Trypanosoma cruzi. Mol. Microbiol. 2011;79(1):50-62.
http://dx.doi.org/10.1111/j.1365-2958.2010.07429.x