The N terminus of phosphodiesterase TbrPDEB1 of Trypanosoma brucei contains the signal for integration into the flagellar skeleton

Eukaryotic Cell

Volumn 9, Issue 10, 2010, Pages 1466-1475

  Luginbuehl, Edith ^a   Ryter, Damaris ^a   Schranz Zumkehr, Judith ^a   Oberholzer, Michael ^b   Kunz, Stefan ^a   Seebeck, Thomas ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP PHOSPHODIESTERASE; GREEN FLUORESCENT PROTEIN; ISOENZYME; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; CYTOSKELETON; ENZYMOLOGY; FLAGELLUM; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; SIGNAL TRANSDUCTION; TRYPANOSOMA BRUCEI;

3',5'-CYCLIC-AMP PHOSPHODIESTERASES; AMINO ACID SEQUENCE; ANIMALS; CYCLIC AMP; CYTOSKELETON; FLAGELLA; GREEN FLUORESCENT PROTEINS; HUMANS; ISOENZYMES; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS; SIGNAL TRANSDUCTION; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 77957759257     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00112-10     Document Type: Article

References (57)

1. Baillie, G. S. 2009. Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. FEBS J. 276:1790-1799.
2. Bangs, J. D., L. Uyetake, K. J. Brickman, A. E. Balber, and J. C. Boothroyd. 1993. Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei. Divergent ER retention signals in a lower eukaryote. J. Cell Sci. 105:1101-1113.
3. Berger, K., R. Lindh, N. Wierup, E. Zmuda-Trzebiatowska, A. Lindqvist, V. C. Manganiello, and E. Degerman. 2009. Phosphodiesterase 3B is localized in caveolae and smooth ER in mouse hepatocytes and is important in the regulation of glucose and lipid metabolism. PLoS One 4:e4671.
4. Biel, M. 2009. Cyclic nucleotide-regulated cation channels. J. Biol. Chem. 284:9017-9021.
5. Bradshaw, N. J., F. Ogawa, B. Antolin-Fontes, J. E. Chubb, B. C. Carlyle, S. Christie, A. Claessens, D. J. Porteous, and J. K. Millar. 2008. DISC1, PDE4B and NDE1 at the centrosome and synapse. Biochem. Biophys. Res. Commun. 377:1091-1096.
6. Broadhead, R., H. R. Dawe, H. Farr, S. Griffiths, S. R. Hart, N. Portman, M. K. Shaw, M. L. Ginger, S. J. Gaskell, P. G. McKean, and K. Gull. 2006. Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440:224-227.
7. Brun, R., and M. Schoenenberger. 1979. Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop. 36:289-292.
8. Chen, C., T. Nakamura, and Y. Koutalos. 1999. Cyclic AMP diffusion coefficient in frog olfactory cilia. Biophys. J. 76:2861-2867.
9. Conti, M., and J. Beavo. 2007. Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu. Rev. Biochem. 76:481-511.
10. Cooper, D. M. 2003. Regulation and organization of adenylyl cyclases and cAMP. Biochem. J. 375:517-529.
11. Cygnar, K. D., and H. Zhao. 2009. Phosphodiesterase 1C is dispensable for rapid response termination of olfactory sensory neurons. Nature Neurosci. 12:454-462.
12. D'Angelo, M. A., S. Sanguineti, J. M. Reece, L. Birnbaumer, H. N. Torres, and M. M. Flawia. 2004. Identification, characterization and subcellular localization of TcPDE1, a novel cAMP-specific phosphodiesterase from Trypanosoma cruzi. Biochem. J. 378:63-72.
13. De Arcangelis, V., R. Liu, D. Soto, and Y. Xiang. 2009. Differential binding of phosphodiesterase 4D isoforms to β2 adrenoceptor in cardiac myocytes. J. Biol. Chem. 284:33824-33832.
14. DiPilato, L. M., and J. Zhang. 2006. FRETting mice shed light on cardiac adrenergic signaling. Circ. Res. 99:1021-1023.
15. Dworkin, M., and K. H. Keller. 1977. Solubility and diffusion coefficient of adenosine 3':5'-monophosphate. J. Biol. Chem. 252:864-865.
16. Ersfeld, K., and K. Gull. 2001. Targeting of cytoskeletal proteins to the flagellum of Trypanosoma brucei. J. Cell Sci. 114:141-148.
17. Fischmeister, R. 2006. Is cAMP good or bad?: depends on where it's made. Circ. Res. 98:582-584.
18. Furger, A., N. Schurch, U. Kurath, and I. Roditi. 1997. Elements in the 3' untranslated region of procyclin mRNA regulate expression in insect forms of Trypanosoma brucei by modulating RNA stability and translation. Mol. Cell. Biol. 17:4372-4380.
19. Ginger, M. L., E. S. Nagoza, C. A. Pereira, T. J. Pullen, M. Kabiri, K. Becker, K. Gull, and D. Steverding. 2005. Intracellular positioning of isoforms explains an unusually large adenylate kinase gene family in the parasite Trypanosoma brucei. J. Biol. Chem. 280:11781-11789.
20. Gong, K. W., S. Kunz, R. Zoraghi, C. Kunz Renggli, R. Brun, and T. Seebeck. 2001. cAMP-specific phosphodiesterase TbPDE1 is not essential in Trypano-soma brucei in culture or during midgut infection of tsetse flies. Mol. Biochem. Parasitol. 116:229-232.
21. Heikaus, C. C., J. Pandit, and R. Klevit. 2009. Cyclic nucleotide binding GAF domains from phosphodiesterases: structural and mechanistic insights. Structure 17:1551-1557.
22. Hesse, F., P. M. Selzer, K. Muehlstadt, and M. Duszenko. 1995. A novel cultivation technique for long-term maintenance of bloodstream form trypanosomes in vitro. Mol. Biochem. Parasitol. 70:157-166.
23. Houslay, M. D., G. S. Baillie, and D. H. Maurice. 2007. cAMP-specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ. Res. 100:950-966.
24. Johner, A., S. Kunz, M. Linder, Y. Shakur, and T. Seebeck. 2006. Cyclic nucleotide specific phosphodiesterases of Leishmania major. BMC Microbiol. 6:25.
25. Kunz, S., J. A. Beavo, M. A. D'Angelo, M. M. Flawia, S. H. Francis, A. Johner, S. Laxman, M. Oberholzer, A. Rascon, Y. Shakur, L. Wentzinger, R. Zoraghi, and T. Seebeck. 2005. Cyclic nucleotide specific phosphodiesterases of the kinetoplastida: a unified nomenclature. Mol. Biochem. Parasitol. 145: 133-135.
26. Kunz, S., E. Luginbuehl, and T. Seebeck. 2009. Gene conversion transfers the GAF-A domain of phosphodiesterase TbrPDEB1 to one allele of TbrPDEB2 of Trypanosoma brucei. PLoS Negl. Trop. Dis. 3:e455.
27. Maudlin, I., P. H. Holmes, and M. A. Miles. 2004. The trypanosomiases. CABI Publishing, Wallingford, Oxfordshire, United Kingdom.
28. Murray, A. J. 2008. Pharmacological PKA inhibition: all may not be what it seems. Sci. Signal. 3:re4.
29. Nikolaev, V. O., M. Bünemann, L. Hein, A. Hannawacker, and M. J. Lohse. 2004. Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279:37215-37218.
30. Nikolaev, V. O., M. Bünemann, E. Schmitteckert, M. J. Lohse, and S. Engelhardt. 2006. Cyclic AMP imaging in adult cardiac myocytes revealsfar-reaching β1-adrenergic but locally confined β 2-adrenergic receptormediated signaling. Circ. Res. 99:1084-1091.
31. Oberholzer, M., G. Marti, M. Baresic, S. Kunz, A. Hemphill, and T. Seebeck. 2007. The Trypanosoma brucei cAMP phosphodiesterases TbrPDEB1 and TbrPDEB2-flagellar enzymes that are essential for virulence. FASEB J. 21:720-731.
32. Oberholzer, M., S. Morand, S. Kunz, and T. Seebeck. 2006. A vector series for rapid PCR-mediated C-terminal in situ tagging of Trypanosoma brucei brucei genes. Mol. Biochem. Parasitol. 145:117-120.
33. Oberholzer, M., P. Bregy, G. Marti, M. Minca, M. Peier, and T. Seebeck. 2006. Trypanosomes and mammalian sperm: one of a kind? Trends Parasitol. 23:71-77.
34. Pandit, J., M. D. Forman, K. F. Fennell, K. S. Dillman, and F. S. Menniti. 2009. Mechanism for the allosteric regulation of phosphodiesterase 2A deduced from the X-ray structure of a near full-length construct. Proc. Natl. Acad. Sci. U. S. A. 106:18225-18230.
35. Pierre, S., T. Eschenhagen, G. Geisslinger, and K. Scholich. 2009. Capturing adenylyl cyclases as potential drug targets. Nat. Rev. Drug Discov. 8:321-335.
36. Portman, N., S. Lacomble, B. Thomas, P. G. McKean, and K. Gull. 2006. Combining RNA interference mutants and comparative proteomics to identify protein components and dependence in a eukaryotic flagellum. J. Biol. Chem. 224:5610-5619.
37. Pullen, T. J., M. L. Ginger, S. J. Gaskell, and K. Gull. 2004. Protein targeting of an unusual, evolutionarily conserved adenylate kinase to a eukaryotic flagellum. Mol. Biol. Cell 15:3257-3265.
38. Rascon, A., S. H. Soderling, J. B. Schaefer, and J. A. Beavo. 2002. Cloning and characterization of a cAMP-specific phosphodiesterase (TbPDE2B) from Trypanosoma brucei. Proc. Natl. Acad. Sci. U. S. A. 99:4714-4719.
39. Rehmann, H., A. Wittinghofer, and J. L. Bos. 2007. Capturing cyclic nucleotides in action: snapshots from crystallographic studies. Nat. Rev. Mol. Cell Biol. 8:63-73.
40. Rich, T. C., K. A. Fagan, T. E. Tse, J. Schaack, D. M. Cooper, and J. W. Karpen. 2001. A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc. Natl. Acad. Sci. U. S. A. 98:13049-13054.
41. Richter, W., P. Day, R. Agrawal, M. D. Bruss, S. Granier, Y. L. Wang, S. G. Rasmussen, K. Horner, P. Wang, T. Lei, A. J. Patterson, B. Kobilka, and M. Conti. 2008. Signaling from beta1- and beta2-adrenergic receptors is defined by differential interactions with PDE4. EMBO J. 27:384-393.
42. Rochais, F., A. Abi-Gerges, K. Horner, F. Lefebvre, D. M. F. Cooper, M. Conti, R. Fischmeister, and G. Vandecasteele. 2006. A specific pattern of phosphodiesterases controls the cAMP signals generated by different Gscoupled receptors in adult rat ventricular monocytes. Circ. Res. 98:1081-1088.
43. Roy, A., A. Kucukural, and Y. Zhang. 2010. I_TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5:725-738.
44. Sadana, R., and C. W. Dessauer. 2009. Physiological roles for G proteinregulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neurosignals 17:5-22.
45. Sayner, S. L., M. Alexeyev, C. W. Dessauer, and T. Stevens. 2006. Soluble adenylyl cyclase reveals the significance of cAMP compartmentation on pulmonary microvascular endothelial cell barrier. Circ. Res. 98:675-681.
46. Schlaeppi, K., J. Deflorin, and T. Seebeck. 1989. The major component of the paraflagellar rod of Trypanosoma brucei is a helical protein that is encoded by two identical, tandemly linked genes. J. Cell Biol. 109:1695-1709.
47. Schneider, A., T. Sherwin, R. Sasse, D. G. Russell, K. Gull, and T. Seebeck. 1987. Subpellicular and flagellar microtubules of Trypanosoma brucei brucei contain the same alpha-tubulin isotypes. J. Cell Biol. 104:431-438.
48. Sherwin, T., A. Schneider, R. Sasse, T. Seebeck, and K. Gull. 1987. Distinct localization and cell cycle dependence of COOH terminally tyrosinolated -tubulin in the microtubules of Trypanosoma brucei brucei. J. Cell Biol. 104:439-446.
49. Tasken, K., and E. M. Aandahl. 2004. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev. 84:137-167.
50. Terrenoire, C., M. D. Houslay, G. S. Baillie, and R. S. Kass. 2009. The cardiac IKS potassium channel macromolecular complex includes the phosphodiesterase PDE4D3. J. Biol. Chem. 284:9140-9146.
51. Tyler, K. M., A. Fridberg, K. M. Toriello, C. L. Olson, J. A. Cieslak, T. L. Hazlett, and D. M. Engman. 2009. Flagellar membrane localization via association with lipid rafts. J. Cell Sci. 122:859-866.
52. Wang, H., Z. Yan, J. Geng, S. Kunz, T. Seebeck, and H. Ke. 2007. Crystal structure of the Leishmania major phosphodiesterase LmjPDEB1 and insight into the design of parasite selective inhibitors. Mol. Microbiol. 66:1029-1038.
53. Wentzinger, L., and T. Seebeck. 2007. Protozoal phosphodiesterases, p. 277-300. In J. A. Beavo, S. Francis, and M. Houslay (ed.), Phosphodiesterases in health and disease. CRC Press, Boca Raton, FL.
54. Wirtz, E., S. Leal, G. Ochatt, and G. A. M. Cross. 1999. A tightly regulated inducible expression system for conditional gene knock-outs and dominantnegative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:89-101.
55. Zaccolo, M., and T. Pozzan. 2002. Discrete microdomains with high concentrations of cAMP in stimulated rat neonatal cardiac myocytes. Science 295: 1711-1715.
56. Zhang, J., Y. Ma, S. S. Taylor, and R. Y. Tsien. 2001. Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc. Natl. Acad. Sci. U. S. A. 98:14997-15002.
57. Zoraghi, R., and T. Seebeck. 2002. The cAMP-specific phosphodiesterase TbPDE2C is an essential enzyme in bloodstream form Trypanosoma brucei. Proc. Natl. Acad. Sci. U. S. A. 99:4343-4348.