Defining the role of a FYVE domain in the localization and activity of a cAMP phosphodiesterase implicated in osmoregulation in Trypanosoma cruzi

Molecular Microbiology

Volumn 79, Issue 1, 2011, Pages 50-62

  Schoijet, Alejandra C ^a,b,c   Miranda, Kildare ^b,c,d   Medeiros, Lia Carolina Soares ^c   De Souza, Wanderley ^c,d   Flawiá, Mirtha M ^a,e   Torres, Héctor N ^a,e   Pignataro, Omar P ^e,f   Docampo, Roberto ^b   Alonso, Guillermo D ^a,e  

^a INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

^b UNIVERSITY OF GEORGIA   (United States)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d INSTITUTO NACIONAL DE METROLOGIA   (Brazil)

^e UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^f Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

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;

EID: 78650245392     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07429.x     Document Type: Article

References (58)

1. Allen, R.D., Tominaga, T., and Naitoh, Y. (2009) The contractile vacuole complex and cell volume regulation. In Osmotic and Ionic Regulation. Evans, D.H. (ed.). Boca Raton: CRC Press, Taylor & Francis Group, pp. 69-105.
2. Alonso, G.D., Schoijet, A.C., Torres, H.N., and Flawia, M.M. (2006) TcPDE4, a novel membrane-associated cAMP-specific phosphodiesterase from Trypanosoma cruzi. Mol Biochem Parasitol 145: 40-49.
3. Alonso, G.D., Schoijet, A.C., Torres, H.N., and Flawia, M.M. (2007) TcrPDEA1, a cAMP-specific phosphodiesterase with atypical pharmacological properties from Trypanosoma cruzi. Mol Biochem Parasitol 152: 72-79.
4. Baillie, G.S. (2009) Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. FEBS J 276: 1790-1799.
5. Baillie, G.S., Scott, J.D., and Houslay, M.D. (2005) Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett 579: 3264-3270.
6. Banerjee, S., Basu, S., and Sarkar, S. (2010) Comparative genomics reveals selective distribution and domain organization of FYVE and PX domain proteins across eukaryotic lineages. BMC Genomics 11: 83.
7. Bao, Y., Weiss, L.M., Braunstein, V.L., and Huang, H. (2008) Role of protein kinase A in Trypanosoma cruzi. Infect Immun 76: 4757-4763.
8. Bender, A.T., and Beavo, J.A. (2006) Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58: 488-520.
9. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D.C., et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
10. Bhattacharya, A., Biswas, A., and Das, P.K. (2009) Role of a differentially expressed cAMP phosphodiesterase in regulating the induction of resistance against oxidative damage in Leishmania donovani. Free Radic Biol Med 47: 1494-1506.
11. Blatner, N.R., Stahelin, R.V., Diraviyam, K., Hawkins, P.T., Hong, W., Murray, D., and Cho, W. (2004) The molecular basis of the differential subcellular localization of FYVE domains. J Biol Chem 279: 53818-53827.
12. Caceres, A.J., Portillo, R., Acosta, H., Rosales, D., Quinones, W., Avilan, L., et al. (2003) Molecular and biochemical characterization of hexokinase from Trypanosoma cruzi. Mol Biochem Parasitol 126: 251-262.
13. Callaghan, J., Simonsen, A., Gaullier, J.M., Toh, B.H., and Stenmark, H. (1999) The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer. Biochem J 338: 539-543.
14. Clark, T.B. (1959) Comparative morphology of four genera of trypanosomatidae. J Protozool 6: 227-232.
15. Conti, M. (2000) Phosphodiesterases and cyclic nucleotide signaling in endocrine cells. Mol Endocrinol 14: 1317-1327.
16. Conti, M., and Beavo, J. (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481-511.
17. Cooper, D.M. (2005) Compartmentalization of adenylate cyclase and cAMP signalling. Biochem Soc Trans 33: 1319-1322.
18. Cullen, P.J., Cozier, G.E., Banting, G., and Mellor, H. (2001) Modular phosphoinositide-binding domains - their role in signalling and membrane trafficking. Curr Biol 11: R882-R893.
19. D'Angelo, M.A., Sanguineti, S., Reece, J.M., Birnbaumer, L., Torres, H.N., and Flawia, M.M. (2004) Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi. Biochem J 378: 63-72.
20. Del Punta, K., Charreau, E.H., and Pignataro, O.P. (1996) Nitric oxide inhibits Leydig cell steroidogenesis. Endocrinology 137: 5337-5343.
21. Diraviyam, K., Stahelin, R.V., Cho, W., and Murray, D. (2003) Computer modeling of the membrane interaction of FYVE domains. J Mol Biol 328: 721-736.
22. Drobak, B.K., and Heras, B. (2002) Nuclear phosphoinositides could bring FYVE alive. Trends Plant Sci 7: 132-138.
23. Dumas, J.J., Merithew, E., Sudharshan, E., Rajamani, D., Hayes, S., Lawe, D., et al. (2001) Multivalent endosome targeting by homodimeric EEA1. Mol Cell 8: 947-958.
24. El-Sayed, N.M., Myler, P.J., Bartholomeu, D.C., Nilsson, D., Aggarwal, G., Tran, A.N., et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
25. Flawia, M.M., Tellez-Inon, M.T., and Torres, H.N. (1997) Signal transduction mechanisms in Trypanosoma cruzi. Parasitol Today 13: 30-33.
26. Halpin, D.M. (2008) ABCD of the phosphodiesterase family: interaction and differential activity in COPD. Int J Chron Obstruct Pulmon Dis 3: 543-561.
27. Hayakawa, A., Hayes, S., Leonard, D., Lambright, D., and Corvera, S. (2007) Evolutionarily conserved structural and functional roles of the FYVE domain. Biochem Soc Symp 95-105.
28. Houslay, M.D., and Adams, D.R. (2003) PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 370: 1-18.
29. Houslay, M.D., and Milligan, G. (1997) Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem Sci 22: 217-224.
30. Ivens, A.C., Peacock, C.S., Worthey, E.A., Murphy, L., Aggarwal, G., Berriman, M., et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
31. King-Keller, S., Li, M., Smith, A., Zheng, S., Kaur, G., Yang, X., et al. (2010) Chemical validation of phosphodiesterase C as a chemotherapeutic target in Trypanosoma cruzi, the etiological agent of Chagas' disease. Antimicrob Agents Chemother 54: 3738-3745.
32. Kunz, S., Oberholzer, M., and Seebeck, T. (2005) A FYVE-containing unusual cyclic nucleotide phosphodiesterase from Trypanosoma cruzi. FEBS J 272: 6412-6422.
33. Kutateladze, T.G. (2007) Mechanistic similarities in docking of the FYVE and PX domains to phosphatidylinositol 3-phosphate containing membranes. Prog Lipid Res 46: 315-327.
34. Kutateladze, T., and Overduin, M. (2001) Structural mechanism of endosome docking by the FYVE domain. Science 291: 1793-1796.
35. Kutateladze, T.G., Capelluto, D.G., Ferguson, C.G., Cheever, M.L., Kutateladze, A.G., Prestwich, G.D., and Overduin, M. (2004) Multivalent mechanism of membrane insertion by the FYVE domain. J Biol Chem 279: 3050-3057.
36. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
37. Lawe, D.C., Patki, V., Heller-Harrison, R., Lambright, D., and Corvera, S. (2000) 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. J Biol Chem 275: 3699-3705.
38. Laxman, S., and Beavo, J.A. (2007) Cyclic nucleotide signaling mechanisms in trypanosomes: possible targets for therapeutic agents. Mol Interv 7: 203-215.
39. Lee, S.A., Eyeson, R., Cheever, M.L., Geng, J., Verkhusha, V.V., Burd, C., et al. (2005) Targeting of the FYVE domain to endosomal membranes is regulated by a histidine switch. Proc Natl Acad Sci USA 102: 13052-13057.
40. Lemmon, M.A. (2003) Phosphoinositide recognition domains. Traffic 4: 201-213.
41. Lugnier, C. (2001) Cyclic nucleotide phosphodiesterase families in intracellular signaling and diabetes. Adv Exp Med Biol 498: 253-261.
42. Martin, T.F. (1998) Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu Rev Cell Dev Biol 14: 231-264.
43. Minning, T.A., Weatherly, D.B., Atwood, J., III, Orlando, R., and Tarleton, R.L. (2009) The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 10: 370.
44. Mondillo, C., Pagotto, R.M., Piotrkowski, B., Reche, C.G., Patrignani, Z.J., Cymeryng, C.B., and Pignataro, O.P. (2009) Involvement of nitric oxide synthase in the mechanism of histamine-induced inhibition of Leydig cell steroidogenesis via histamine receptor subtypes in Sprague-Dawley rats. Biol Reprod 80: 144-152.
45. Montalvetti, A., Rohloff, P., and Docampo, R. (2004) A functional aquaporin co-localizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi. J Biol Chem 279: 38673-38682.
46. Omori, K., and Kotera, J. (2007) Overview of PDEs and their regulation. Circ Res 100: 309-327.
47. Payrastre, B., Missy, K., Giuriato, S., Bodin, S., Plantavid, M., and Gratacap, M. (2001) Phosphoinositides: key players in cell signalling, in time and space. Cell Signal 13: 377-387.
48. Pereira, C.A., Alonso, G.D., Paveto, M.C., Iribarren, A., Cabanas, M.L., Torres, H.N., and Flawia, M.M. (2000) Trypanosoma cruzi arginine kinase characterization and cloning. A novel energetic pathway in protozoan parasites. J Biol Chem 275: 1495-1501.
49. Psachoulia, E., and Sansom, M.S. (2009) PX- and FYVE-mediated interactions with membranes: simulation studies. Biochemistry 48: 5090-5095.
50. Rohloff, P., and Docampo, R. (2008) A contractile vacuole complex is involved in osmoregulation in Trypanosoma cruzi. Exp Parasitol 118: 17-24.
51. Rohloff, P., Rodrigues, C.O., and Docampo, R. (2003) Regulatory volume decrease in Trypanosoma cruzi involves amino acid efflux and changes in intracellular calcium. Mol Biochem Parasitol 126: 219-230.
52. Rohloff, P., Montalvetti, A., and Docampo, R. (2004) Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi. J Biol Chem 279: 52270-52281.
53. Scott, J.D. (2006) Compartmentalized cAMP signalling: a personal perspective. Biochem Soc Trans 34: 465-467.
54. Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J.M., Brech, A., Callaghan, J., et al. (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394: 494-498.
55. Stahelin, R.V., Long, F., Diraviyam, K., Bruzik, K.S., Murray, D., and Cho, W. (2002) Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs. J Biol Chem 277: 26379-26388.
56. Vazquez, M.P., and Levin, M.J. (1999) Functional analysis of the intergenic regions of TcP2beta gene loci allowed the construction of an improved Trypanosoma cruzi expression vector. Gene 239: 217-225.
57. Wilkinson, S.R., Meyer, D.J., Taylor, M.C., Bromley, E.V., Miles, M.A., and Kelly, J.M. (2002) The Trypanosoma cruzi enzyme TcGPXI is a glycosomal peroxidase and can be linked to trypanothione reduction by glutathione or tryparedoxin. J Biol Chem 277: 17062-17071.
58. Zhu, Q., and Clarke, M. (1992) Association of calmodulin and an unconventional myosin with the contractile vacuole complex of Dictyostelium discoideum. J Cell Biol 118: 347-358.