Cytokinesis of Trypanosoma brucei bloodstream forms depends on expression of adenylyl cyclases of the ESAG4 or ESAG4-like subfamily

Molecular Microbiology

Volumn 84, Issue 2, 2012, Pages 225-242

  Salmon, Didier ^a,c   Bachmaier, Sabine ^b   Krumbholz, Carsten ^b,d   Kador, Markus ^b   Gossmann, Jasmin A ^b   Uzureau, Pierrick ^a   Pays, Etienne ^a   Boshart, Michael ^b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF MUNICH   (Germany)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d Human GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; SMALL INTERFERING RNA; VARIANT SURFACE GLYCOPROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANTIGENIC VARIATION; ARTICLE; CELL DIVISION; CISTRON; CONTROLLED STUDY; CYTOKINESIS; ENZYME ACTIVITY; EXPRESSION SITE ASSOCIATED GENE; EXPRESSION SITE ASSOCIATED GENE 4 LIKE GENE; GENE; GENE EXPRESSION; GENE FUNCTION; LIFE CYCLE STAGE; MOUSE; NONHUMAN; PARASITE DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TRYPANOSOMA BRUCEI; UPREGULATION;

ADENYLATE CYCLASE; CLUSTER ANALYSIS; CYTOKINESIS; GENE DELETION; GENE EXPRESSION; GENETIC COMPLEMENTATION TEST; PHYLOGENY; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRYPANOSOMA BRUCEI BRUCEI;

RODENTIA; TRYPANOSOMA BRUCEI;

EID: 84859438417     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08013.x     Document Type: Article

References (82)

1. Alarcon, C.M., Son, H.J., Hall, T., and Donelson, J.E. (1994) A monocistronic transcript for a trypanosome variant surface glycoprotein. Mol Cell Biol 14: 5579-5591.
2. Alexandre, S., Paindavoine, P., Tebabi, P., Pays, A., Halleux, S., Steinert, M., and Pays, E. (1990) Differential expression of a family of putative adenylate/guanylate cyclase genes in Trypanosoma brucei. Mol Biochem Parasitol 43: 279-288.
3. Alexandre, S., Paindavoine, P., Hanocq-Quertier, J., Paturiaux-Hanocq, F., Tebabi, P., and Pays, E. (1996) Families of adenylate cyclase genes in Trypanosoma brucei. Mol Biochem Parasitol 77: 173-182.
4. Altekar, G., Dwarkadas, S., Huelsenbeck, J., and Ronquist, F. (2004) Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20: 407-415.
5. Amiguet-Vercher, A., Perez-Morga, D., Pays, A., Poelvoorde, P., Xong, H.V., Tebabi, P., etal. (2004) Loss of the mono-allelic control of the VSG expression sites during the development of Trypanosoma brucei in the bloodstream. Mol Microbiol 51: 1577-1588.
6. Archer, S.K., Inchaustegui, D., Queiroz, R., and Clayton, C. (2011) The cell cycle regulated transcriptome of Trypanosoma brucei. PLoS ONE 6: e18425. doi: 10.1371/journal.pone.0018425.
7. Barry, J.D., Marcello, L., Morrison, L.J., Read, A.F., Lythgoe, K., Jones, N., etal. (2005) What the genome sequence is revealing about trypanosome antigenic variation. Biochem Soc Trans 33: 986-989.
8. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D.C., etal. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
9. Biebinger, S., Wirtz, L.E., Lorenz, P., and Clayton, C. (1997) Vectors for inducible expression of toxic gene products in bloodstream and procyclic Trypanosoma brucei. Mol Biochem Parasitol 85: 99-112.
10. Bitter, W., Gerrits, H., Kieft, R., and Borst, P. (1998) The role of transferrin-receptor variation in the host range of Trypanosoma brucei. Nature 391: 499-502.
11. Borst, P., and Fairlamb, A.H. (1998) Surface receptors and transporters of Trypanosoma brucei. Annu Rev Microbiol 52: 745-778.
12. Bridges, D.J., Pitt, A.R., Hanrahan, O., Brennan, K., Voorheis, H., Herzyk, P., etal. (2008) Characterisation of the plasma membrane subproteome of bloodstream form Trypanosoma brucei. Proteomics 8: 83-99.
13. Broadhead, R., Dawe, H.R., Farr, H., Griffiths, S., Hart, S.R., Portman, N., etal. (2006) Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440: 224-227.
14. Bucerius, F., Kador, M., Boshart, M., and Janzen, C.J. (2011) Reliable quantification of cell cycle-dependent mRNA abundance using fluorescence-activated cell sorting in Trypanosoma brucei. Mol Biochem Parasitol 175: 205-208.
15. Burkard, G., Fragoso, C.M., and Roditi, I. (2007) Highly efficient stable transformation of bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 153: 220-223.
16. Cross, G.A. (1975) Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitology 71: 393-417.
17. Delauw, M.F., Pays, E., Steinert, M., Aerts, D., Van Meirvenne, N., and Ray, D.L. (1985) Inactivation and reactivation of a variant-specific antigen gene in cyclically transmitted Trypanosoma brucei. EMBO J 4: 989-993.
18. Djikeng, A., Shi, H., Tschudi, C., and Ullu, E. (2001) RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24-26-nucleotide RNAs. RNA 7: 1522-1530.
19. El-Sayed, N.M., Myler, P.J., Bartholomeu, D.C., Nilsson, D., Aggarwal, G., Tran, A.N., etal. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
20. Engstler, M., and Boshart, M. (2004) Cold shock and regulation of surface protein trafficking convey sensitization to inducers of stage differentiation in Trypanosoma brucei. Genes Dev 18: 2798-2811.
21. Fenn, K., and Matthews, K.R. (2007) The cell biology of Trypanosoma brucei differentiation. Curr Opin Microbiol 10: 539-546.
22. Graham, S.V., Matthews, K.R., and Barry, J.D. (1993) Trypanosoma brucei: unusual expression-site-associated gene homologies in a metacyclic VSG gene expression site. Exp Parasitol 76: 96-99.
23. Hammarton, T.C., Clark, J., Douglas, F., Boshart, M., and Mottram, J.C. (2003) Stage-specific differences in cell cycle control in Trypanosoma brucei revealed by RNA interference of a mitotic cyclin. J Biol Chem 278: 22877-22886.
24. Hammarton, T.C., Lillico, S.G., Welburn, S.C., and Mottram, J.C. (2005) Trypanosoma brucei MOB1 is required for accurate and efficient cytokinesis but not for exit from mitosis. Mol Microbiol 56: 104-116.
25. Hammarton, T.C., Kramer, S., Tetley, L., Boshart, M., and Mottram, J.C. (2007a) Trypanosoma brucei Polo-like kinase is essential for basal body duplication, kDNA segregation and cytokinesis. Mol Microbiol 65: 1229-1248.
26. Hammarton, T.C., Monnerat, S., and Mottram, J.C. (2007b) Cytokinesis in trypanosomatids. Curr Opin Microbiol 10: 520-527.
27. Helms, M.J., Ambit, A., Appleton, P., Tetley, L., Coombs, G.H., and Mottram, J.C. (2006) Bloodstream form Trypanosoma brucei depend upon multiple metacaspases associated with RAB11-positive endosomes. J Cell Sci 119: 1105-1117.
28. Hertz-Fowler, C., Figueiredo, L.M., Quail, M.A., Becker, M., Jackson, A., Bason, N., etal. (2008) Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS ONE 3: e3527.
29. Kohl, L., Sherwin, T., and Gull, K. (1999) Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. J Eukaryot Microbiol 46: 105-109.
30. de Koning, H.P., Gould, M.K., Sterk, G.J., Tenor, H., Kunz, S., Luginbuehl, E., and Seebeck, T. (2012) Pharmacological validation of Trypanosoma brucei phosphodiesterases as novel drug targets. J Infect Dis Advance Access, doi: 10.1093/infdis/jir857.
31. Kramer, S., Klockner, T., Selmayr, M., and Boshart, M. (2007) Interstrain sequence comparison, transcript map and clonal genomic rearrangement of a 28kb locus on chromosome 9 of Trypanosoma brucei. Mol Biochem Parasitol 151: 129-132.
32. Kunz, S., Kloeckner, T., Essen, L.O., Seebeck, T., and Boshart, M. (2004) TbPDE1, a novel class I phosphodiesterase of Trypanosoma brucei. Eur J Biochem 271: 637-647.
33. LaCount, D.J., Bruse, S., Hill, K.L., and Donelson, J.E. (2000) Double-stranded RNA interference in Trypanosoma brucei using head-to-head promoters. Mol Biochem Parasitol 111: 67-76.
34. Larkin, M.A., Blackshields, G., Brown, N., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
35. Laxman, S., Rascon, A., and Beavo, J.A. (2005) Trypanosome cyclic nucleotide phosphodiesterase 2B binds cAMP through its GAF-A domain. J Biol Chem 280: 3771-3779.
36. Laxman, S., Riechers, A., Sadilek, M., Schwede, F., and Beavo, J.A. (2006) Hydrolysis products of cAMP analogs cause transformation of Trypanosoma brucei from slender to stumpy-like forms. Proc Natl Acad Sci USA 103: 19194-19199.
37. Lillico, S., Field, M.C., Blundell, P., Coombs, G.H., and Mottram, J.C. (2003) Essential roles for GPI-anchored proteins in African trypanosomes revealed using mutants deficient in GPI8. Mol Biol Cell 14: 1182-1194.
38. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
39. Ma, J., Benz, C., Grimaldi, R., Stockdale, C., Wyatt, P., Frearson, J., and Hammarton, T.C. (2010) Nuclear DBF-2-related kinases are essential regulators of cytokinesis in bloodstream stage Trypanosoma brucei. J Biol Chem 285: 15356-15368.
40. Maddison, D.R., and Maddison, W. (2005) MacClade: Analysis of Phylogeny and Character Evolution. Sunderland, MA: Sinauer Associates.
41. Mancini, P.E., and Patton, C.L. (1981) Cyclic 3′, 5′-adenosine monophosphate levels during the developmental cycle of Trypanosoma brucei brucei in the rat. Mol Biochem Parasitol 3: 19-31.
42. Marmur, J. (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3: 208-218.
43. Naula, C., Schaub, R., Leech, V., Melville, S., and Seebeck, T. (2001) Spontaneous dimerization and leucine-zipper induced activation of the recombinant catalytic domain of a new adenylyl cyclase of Trypanosoma brucei, GRESAG4.4B. Mol Biochem Parasitol 112: 19-28.
44. Nolan, D.P., Rolin, S., Rodriguez, J.R., Den, J.V., and Pays, E. (2000) Slender and stumpy bloodstream forms of Trypanosoma brucei display a differential response to extracellular acidic and proteolytic stress. Eur J Biochem 267: 18-27.
45. Oberholzer, M., Marti, G., Baresic, M., Kunz, S., Hemphill, A., and Seebeck, T. (2007) The Trypanosoma brucei cAMP phosphodiesterases TbrPDEB1 and TbrPDEB2: flagellar enzymes that are essential for parasite virulence. FASEB J 21: 720-731.
46. Paindavoine, P., Rolin, S., Assel, S.V., Geuskens, M., Jauniaux, J.C., Dinsart, C., etal. (1992) A gene from the variant surface glycoprotein expression site encodes one of several transmembrane adenylate cyclases located on the flagellum of Trypanosoma brucei. Mol Cell Biol 12: 1218-1225.
47. Parsons, M., and Ruben, L. (2000) Pathways involved in environmental sensing in trypanosomatids. Parasitol Today 16: 56-62.
48. Pays, E. (2006) The variant surface glycoprotein as a tool for adaptation in African trypanosomes. Microbes Infect 8: 930-937.
49. Pays, E., Tebabi, P., Pays, A., Coquelet, H., Revelard, P., Salmon, D., and Steinert, M. (1989) The genes and transcripts of an antigen gene expression site from T. brucei. Cell 57: 835-845.
50. Pays, E., Lips, S., Nolan, D., Vanhamme, L., and Perez-Morga, D. (2001) The VSG expression sites of Trypanosoma brucei: multipurpose tools for the adaptation of the parasite to mammalian hosts. Mol Biochem Parasitol 114: 1-16.
51. Ralston, K.S., Lerner, A.G., Diener, D.R., and Hill, K.L. (2006) Flagellar motility contributes to cytokinesis in Trypanosoma brucei and is modulated by an evolutionarily conserved dynein regulatory system. Eukaryot Cell 5: 696-711.
52. Rascon, A., Soderling, S.H., Schaefer, J.B., and Beavo, J.A. (2002) Cloning and characterization of a cAMP-specific phosphodiesterase (TbPDE2B) from Trypanosoma brucei. Proc Natl Acad Sci USA 99: 4714-4719.
53. Rolin, S., Paindavoine, P., Hanocq-Quertier, J., Hanocq, F., Claes, Y., Le Ray, D., etal. (1993) Transient adenylate cyclase activation accompanies differentiation of Trypanosoma brucei from bloodstream to procyclic forms. Mol Biochem Parasitol 61: 115-125.
54. Rolin, S., Hanocq-Quertier, J., Paturiaux-Hanocq, F., Nolan, D., Salmon, D., Webb, H., etal. (1996) Simultaneous but independent activation of adenylate cyclase and glycosylphosphatidylinositol-phospholipase C under stress conditions in Trypanosoma brucei. J Biol Chem 271: 10844-10852.
55. Rolin, S., Hancocq-Quertier, J., Paturiaux-Hanocq, F., Nolan, D., and Pays, E. (1998) Mild acid stress as a differentiation trigger in Trypanosoma brucei. Mol Biochem Parasitol 93: 251-262.
56. Ronquist, F., and Huelsenbeck, J. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
57. Ross, D.T., Raibaud, A., Florent, I.C., Sather, S., Gross, M.K., Storm, D.R., and Eisen, H. (1991) The trypanosome VSG expression site encodes adenylate cyclase and a leucine-rich putative regulatory gene. EMBO J 10: 2047-2053.
58. Salmon, D., Hanocq-Quertier, J., Paturiaux-Hanocq, F., Pays, A., Tebabi, P., Nolan, D., etal. (1997) Characterization of the ligand-binding site of the transferrin receptor in Trypanosoma brucei demonstrates a structural relationship with the N-terminal domain of the variant surface glycoprotein. EMBO J 16: 7272-7278.
59. Salmon, D., Paturiaux-Hanocq, F., Poelvoorde, P., Vanhamme, L., and Pays, E. (2005) Trypanosoma brucei: growth differences in different mammalian sera are not due to the species-specificity of transferrin. Exp Parasitol 109: 188-194.
60. Salomon, Y., Londos, C., and Rodbell, M. (1974) A highly sensitive adenylate cyclase assay. Anal Biochem 58: 541-548.
61. Seebeck, T., Schaub, R., and Johner, A. (2004) cAMP signalling in the kinetoplastid protozoa. Curr Mol Med 4: 585-599.
62. Seed, J.R., and Black, S.J. (1997) A proposed density-dependent model of long slender to short stumpy transformation in the African trypanosomes. J Parasitol 83: 656-662.
63. Shalaby, T., Liniger, M., and Seebeck, T. (2001) The regulatory subunit of a cGMP-regulated protein kinase A of Trypanosoma brucei. Eur J Biochem 268: 6197-6206.
64. Sheader, K., Vaughan, S., Minchin, J., Hughes, K., Gull, K., and Rudenko, G. (2005) Variant surface glycoprotein RNA interference triggers a precytokinesis cell cycle arrest in African trypanosomes. Proc Natl Acad Sci USA 102: 8716-8721.
65. Smith, T.K., Vasileva, N., Gluenz, E., Terry, S., Portman, N., Kramer, S., etal. (2009) Blocking variant surface glycoprotein synthesis in Trypanosoma brucei triggers a general arrest in translation initiation. PLoS ONE 4: e7532.
66. Steverding, D. (2006) On the significance of host antibody response to the Trypanosoma brucei transferrin receptor during chronic infection. Microbes Infect 8: 2777-2782.
67. Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4. Sunderland, MA: Sinauer Associates.
68. Tang, W.J., and Gilman, A.G. (1992) Adenylyl cyclases. Cell 70: 869-872.
69. Taylor, J.E., and Rudenko, G. (2006) Switching trypanosome coats: what's in the wardrobe? Trends Genet 22: 614-620.
70. Uzureau, P., Felu, C., Muylder, G.D., Pays, E., and Vanhamme, L. (2007) G418, phleomycin and hygromycin selection of recombinant Trypanosoma brucei parasites refractory to long-term in vitro culture. Mol Biochem Parasitol 154: 90-94.
71. Vassella, E., and Boshart, M. (1996) High molecular mass agarose matrix supports growth of bloodstream forms of pleomorphic Trypanosoma brucei strains in axenic culture. Mol Biochem Parasitol 82: 91-105.
72. Vassella, E., Reuner, B., Yutzy, B., and Boshart, M. (1997) Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. J Cell Sci 110 (Part 21): 2661-2671.
73. Vassella, E., Abbeele, J.V.D., Butikofer, P., Renggli, C.K., Furger, A., Brun, R., and Roditi, I. (2000) A major surface glycoprotein of Trypanosoma brucei is expressed transiently during development and can be regulated post-transcriptionally by glycerol or hypoxia. Genes Dev 14: 615-626.
74. Vassella, E., Kramer, R., Turner, C.M., Wankell, M., Modes, C., van den Bogaard, M., and Boshart, M. (2001) Deletion of a novel protein kinase with PX and FYVE-related domains increases the rate of differentiation of Trypanosoma brucei. Mol Microbiol 41: 33-46.
75. Vickerman, K. (1965) Polymorphism and mitochondrial activity in sleeping sickness trypanosomes. Nature 208: 762-766.
76. Voorheis, H.P., and Martin, B.R. (1980) 'Swell dialysis' demonstrates that adenylate cyclase in Trypanosoma brucei is regulated by calcium ions. Eur J Biochem 113: 223-227.
77. Voorheis, H.P., and Martin, B.R. (1982) Local anaesthetics including benzyl alcohol activate the adenylate cyclase in Trypanosoma brucei by a calcium-dependent mechanism. Eur J Biochem 123: 371-376.
78. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99: 89-101.
79. Xong, H.V., Vanhamme, L., Chamekh, M., Chimfwembe, C.E., Van Den Abbeele, J., Pays, A., etal. (1998) A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95: 839-846.
80. Young, R., Taylor, J.E., Kurioka, A., Becker, M., Louis, E.J., and Rudenko, G. (2008) Isolation and analysis of the genetic diversity of repertoires of VSG expression site containing telomeres from Trypanosoma brucei gambiense, T.b.brucei and T. equiperdum. BMC Genomics 9: 385.
81. Zoraghi, R., and Seebeck, T. (2002) The cAMP-specific phosphodiesterase TbPDE2C is an essential enzyme in bloodstream form Trypanosoma brucei. Proc Natl Acad Sci USA 99: 4343-4348.
82. Zoraghi, R., Kunz, S., Gong, K., and Seebeck, T. (2001) Characterization of TbPDE2A, a novel cyclic nucleotide-specific phosphodiesterase from the protozoan parasite Trypanosoma brucei. J Biol Chem 276: 11559-11566.