Regulation of Trypanosoma brucei Total and Polysomal mRNA during Development within Its Mammalian Host

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Capewell, Paul ^a   Monk, Stephanie ^a   Ivens, Alasdair ^a   MacGregor, Paula ^a   Fenn, Katelyn ^a   Walrad, Pegine ^a   Bringaud, Frederic ^c   Smith, Terry K ^b   Matthews, Keith R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c CNRS University Bordeaux Segalen   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTOZOAL RNA;

ARTICLE; BLOOD FLOW; FEMALE; GENE EXPRESSION; GENE REPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HOST PARASITE INTERACTION; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; POLYSOME; TRYPANOSOMA; TRYPANOSOMA BRUCEI; ANIMAL; BLOOD; GENETICS; GLOSSINIDAE; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; MAMMAL; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PROTEIN SYNTHESIS; TRYPANOSOMA BRUCEI BRUCEI;

ARTHROPODA; GLOSSINA (GENUS); MAMMALIA; TRYPANOSOMA BRUCEI;

ANIMALS; BLOOD; HOST-PATHOGEN INTERACTIONS; MAMMALS; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, PROTOZOAN; TRYPANOSOMA BRUCEI BRUCEI; TSETSE FLIES;

EID: 84879481263     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067069     Document Type: Article

References (58)

1. Matthews KR, (2011) Controlling and coordinating development in vector-transmitted parasites. Science 331: 1149-1153.
2. Roditi I, Lehane MJ, (2008) Interactions between trypanosomes and tsetse flies. Curr Opin Microbiol 11: 345-351.
3. Robertson M, (1912) Notes on the polymorphism of Trypanosoma gambiense in the blood and its relation to the exogenous cycvle in Glossina palpalis. Proceedings of the Royal society B 85: 241-539.
4. Wijers DJ, Willett KC, (1960) Factors that may influence the infection rate of Glossina palpalis with Trypanosoma gambiense. II. The number and morphology of the trypano-somes present in the blood of the host at the time of the infected feed. Ann Trop Med Parasitol 54: 341-350.
5. MacGregor P, Szoor B, Savill NJ, Matthews KR, (2012) Trypanosomal immune evasion, chronicity and transmission: an elegant balancing act. Nat Rev Microbiol 10: 431-438.
6. Nolan DP, Rolin S, Rodriguez JR, Van Den Abbeele J, 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.
7. Ziegelbauer K, Quinten M, Schwarz H, Pearson TW, Overath P, (1990) Synchronous differentiation of Trypanosoma brucei from bloodstream to procyclic forms in vitro. Eur J Biochem 192: 373-378.
8. Matthews KR, Gull K, (1994) Evidence for an interplay between cell cycle progression and the initiation of differentiation between life cycle forms of African trypanosomes. J Cell Biol 125: 1147-1156.
9. Engstler M, 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.
10. Dean SD, Marchetti R, Kirk K, Matthews K, (2009) A surface transporter family conveys the trypanosome differentiation signal. Nature 459: 213-217.
11. Vassella E, Reuner B, Yutzy B, 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 (Pt 21): 2661-2671.
12. Reuner B, Vassella E, Yutzy B, Boshart M, (1997) Cell density triggers slender to stumpy differentiation of Trypanosoma brucei bloodstream forms in culture. Mol Biochem Parasitol 90: 269-280.
13. Hamm B, Schindler A, Mecke D, Duszenko M, (1990) Differentiation of Trypanosoma brucei bloodstream trypomastigotes from long slender to short stumpy-like forms in axenic culture. Mol Biochem Parasitol 40: 13-22.
14. Vanhollebeke B, Uzureau P, Monteyne D, Perez-Morga D, Pays E, (2010) Cellular and molecular remodeling of the endocytic pathway during differentiation of Trypanosoma brucei bloodstream forms. Eukaryot Cell 9: 1272-1282.
15. Shapiro SZ, Naessens J, Liesegang B, Moloo SK, Magondu J, (1984) Analysis by flow cytometry of DNA synthesis during the life cycle of African trypanosomes. Acta Trop 41: 313-323.
16. Barnwell EM, van Deursen FJ, Jeacock L, Smith KA, Maizels RM, et al. (2010) Developmental regulation and extracellular release of a VSG expression-site-associated gene product from Trypanosoma brucei bloodstream forms. J Cell Sci 123: 3401-3411.
17. Jensen BC, Sivam D, Kifer CT, Myler PJ, Parsons M, (2009) Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10: 482.
18. Macgregor P, Matthews KR (2012) Identification of the regulatory elements controlling the transmission stage-specific gene expression of PAD1 in Trypanosoma brucei. Nucleic Acids Res.
19. Macgregor P, Savill NJ, Hall D, Matthews KR, (2011) Transmission Stages Dominate Trypanosome Within-Host Dynamics during Chronic Infections. Cell Host Microbe 9: 310-318.
20. Vickerman K, (1965) Polymorphism and mitochondrial activity in sleeping sickness trypanosomes. Nature 208: 762-766.
21. Clayton C, Shapira M, (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101.
22. Lahav T, Sivam D, Volpin H, Ronen M, Tsigankov P, et al. (2011) Multiple levels of gene regulation mediate differentiation of the intracellular pathogen Leishmania. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 25: 515-525.
23. Greenbaum D, Colangelo C, Williams K, Gerstein M, (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4: 117.
24. Anderson L, Seilhamer J, (1997) A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 18: 533-537.
25. Brecht M, Parsons M, (1998) Changes in polysome profiles accompany trypanosome development. Mol Biochem Parasitol 97: 189-198.
26. Pays E, Hanocq Q-J, Hanocq F, Van A-S, Nolan D, et al. (1993) Abrupt RNA changes precede the first cell division during the differentiation of Trypanosoma brucei bloodstream forms into procyclic forms in vitro. Mol Biochem Parasitol 61: 107-114.
27. Queiroz R, Benz C, Fellenberg K, Hoheisel JD, Clayton C, (2009) Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics 10: 495.
28. Kabani S, Fenn K, Ross A, Ivens A, Smith TK, et al. (2009) Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics 10: 427.
29. Walrad PB, Capewell P, Fenn K, Matthews KR, (2012) The post-transcriptional trans-acting regulator, TbZFP3, co-ordinates transmission-stage enriched mRNAs in Trypanosoma brucei. Nucleic Acids Res 40: 2869-2883.
30. Siegel TN, Hekstra DR, Wang X, Dewell S, Cross GA, (2010) Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res 38: 4946-4957.
31. Langmead B (2010) Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics Chapter 11: Unit 11 17.
32. Muller IB, Domenicali-Pfister D, Roditi I, Vassella E, (2002) Stage-specific requirement of a mitogen-activated protein kinase by Trypanosoma brucei. Mol Biol Cell 13: 3787-3799.
33. Droll D, Archer S, Fenn K, Delhi P, Matthews K, et al. (2010) The trypanosome Pumilio-domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation. FEBS Lett 584: 1156-1162.
34. Szoor B, Ruberto I, Burchmore R, Matthews K, (2010) A novel phosphatase cascade reglates differentiation in trypanosomes via a glycosomal signaling pathway. Genes and Development 24: 1306-1316.
35. Sanchez MA, Drutman S, van Ampting M, Matthews K, Landfear SM, (2004) A novel purine nucleoside transporter whose expression is up-regulated in the short stumpy form of the Trypanosoma brucei life cycle. Mol Biochem Parasitol 136: 265-272.
36. Alsford S, Turner DJ, Obado SO, Sanchez-Flores A, Glover L, et al. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res.
37. Breitling R, Amtmann A, Herzyk P, (2004) Iterative Group Analysis (iGA): a simple tool to enhance sensitivity and facilitate interpretation of microarray experiments. BMC Bioinformatics 5: 34.
38. Jackson AP, Berry A, Aslett M, Allison HC, Burton P, et al. (2012) Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species. Proc Natl Acad Sci U S A 109: 3416-3421.
39. Zhu Y, Davis A, Smith BJ, Curtis J, Handman E, (2009) Leishmania major CorA-like magnesium transporters play a critical role in parasite development and virulence. Int J Parasitol 39: 713-723.
40. Zhang X, Cui J, Nilsson D, Gunasekera K, Chanfon A, et al. (2010) The Trypanosoma brucei MitoCarta and its regulation and splicing pattern during development. Nucleic Acids Res 38: 7378-7387.
41. Vickerman K, (1965) Polymorphism and mitochondrial activity in sleeping sickness. Nature 208: 762-766.
42. Priest JW, Hajduk SL, (1994) Developmental regulation of mitochondrial biogenesis in Trypanosoma brucei. J Bioenerg Biomembr 26: 179-191.
43. Urbaniak MD, Guther ML, Ferguson MA, (2012) Comparative SILAC proteomic analysis of Trypanosoma brucei bloodstream and procyclic lifecycle stages. PLoS One 7: e36619.
44. Gunasekera K, Wuthrich D, Braga-Lagache S, Heller M, Ochsenreiter T, (2012) Proteome remodelling during development from blood to insect-form Trypanosoma brucei quantified by SILAC and mass spectrometry. BMC Genomics 13: 556.
45. Tsigankov P, Gherardini PF, Helmer-Citterich M, Zilberstein D, (2012) What has proteomics taught us about Leishmania development? Parasitology 139: 1146-1157.
46. Minning TA, Weatherly DB, Atwood J 3rd, Orlando R, Tarleton RL, (2009) The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 10: 370.
47. Atwood JA 3rd, Weatherly DB, Minning TA, Bundy B, Cavola C, et al (2005) The Trypanosoma cruzi proteome. Science 309: 473-476.
48. Paape D, Lippuner C, Schmid M, Ackermann R, Barrios-Llerena ME, et al. (2008) Transgenic, fluorescent Leishmania mexicana allow direct analysis of the proteome of intracellular amastigotes. Mol Cell Proteomics 7: 1688-1701.
49. Nilsson D, Gunasekera K, Mani J, Osteras M, Farinelli L, et al. (2010) Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog 6: e1001037.
50. Durrani Z, Weir W, Pillai S, Kinnaird J, Shiels B, (2012) Modulation of activation-associated host cell gene expression by the apicomplexan parasite Theileria annulata. Cell Microbiol 14: 1434-1454.
51. Nagamune K, Acosta-Serrano A, Uemura H, Brun R, Kunz-Renggli C, et al. (2004) Surface sialic acids taken from the host allow trypanosome survival in tsetse fly vectors. J Exp Med 199: 1445-1450.
52. van Helden J, Andre B, Collado-Vides J, (1998) Extracting regulatory sites from the upstream region of yeast genes by computational analysis of oligonucleotide frequencies. J Mol Biol 281: 827-842.
53. Mayho M, Fenn K, Craddy P, Crosthwaite S, Matthews K, (2006) Post-transcriptional control of nuclear-encoded cytochrome oxidase subunits in Trypanosoma brucei: evidence for genome-wide conservation of life-cycle stage-specific regulatory elements. Nucleic Acids Res 34: 5312-5324.
54. Macgregor P, Matthews KR, (2012) Identification of the regulatory elements controlling the transmission stage-specific gene expression of PAD1 in Trypanosoma brucei. Nucleic Acids Res 40: 7705-7717.
55. Kieft R, Capewell P, Turner CM, Veitch NJ, MacLeod A, et al. (2010) Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor. Proc Natl Acad Sci U S A 107: 16137-16141.
56. Herbert WJ, Lumsden WH, (1976) Trypanosoma brucei: a rapid "matching" method for estimating the host's parasitemia. Exp Parasitol 40: 427-431.
57. Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP,et al. TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38: D457-462.
58. Lillico S, Field MC, Blundell P, Coombs GH, Mottram JC, (2003) Essential roles for GPI-anchored proteins in African trypanosomes revealed using mutants deficient in GPI8. Mol Biol Cell 14: 1182-1194.