Ribosomal RNA gene transcription in trypanosomes

Parasitology Research

Volumn 113, Issue 7, 2014, Pages 2415-2424

  Hernández, Roberto ^a   Cevallos, Ana María ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Gene expression; Kinetoplastid; Ribosomes

Indexed keywords

CELL SURFACE PROTEIN; DNA DIRECTED RNA POLYMERASE; RIBOSOME DNA; RNA;

ANTIGENIC VARIATION; BIOCHEMISTRY; BIOGENESIS; BIOINFORMATICS; CELL MATURATION; CHROMATIN STRUCTURE; EPIGENETICS; EUKARYOTE EVOLUTION; EUKARYOTIC SPORE; GENE EXPRESSION; GENE STRUCTURE; GENETIC TRANSCRIPTION; HUMAN; KINETOPLASTIDA; LIFE CYCLE; MICROORGANISM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; REVIEW; RIBOSOME; RNA GENE; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; TRYPANOSOMA;

EUKARYOTA; KINETOPLASTIDA; LEISHMANIA MAJOR; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

GENES, RRNA; LEISHMANIA MAJOR; RNA POLYMERASE I; RNA, RIBOSOMAL; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA CRUZI;

EID: 84903820277     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-014-3940-7     Document Type: Review

References (76)

1. Abreu-Blanco MT, Ramírez JL, Pinto-Santini DM, Papadopoulou B, Guevara P (2010) Analysis of ribosomal RNA transcription termination and 3′ end processing in Leishmania amazonensis. Gene 451:15-22
2. Alkemar G, Nygard O (2004) Secondary structure of two regions in expansion segments ES3 and ES6 with the potential of forming a tertiary interaction in eukaryotic 40S ribosomal subunits. RNA 10:403-411 (Pubitemid 38241001)
3. Alsford S, duBois K, Horn D, Field MC (2012) Epigenetic mechanisms, nuclear architecture and the control of gene expression in trypanosomes. Expert Rev Mol Med 14:e13. doi:10.1017/erm.2012.7
4. Alsford S, Horn D (2011) Elongator protein 3b negatively regulates ribosomal DNA transcription in African trypanosomes. Mol Cell Biol 31:1822-1832
5. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Böhme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A, Davies RM, Doggett J, Djikeng A, Feldblyum T, Field MC, Fraser A, Goodhead I, Hance Z, Harper D, Harris BR, Hauser H, Hostetler J, Ivens A, Jagels K, Johnson D, Johnson J, Jones K, Kerhornou AX, Koo H, Larke N, Landfear S, Larkin C, Leech V, Line A, Lord A, Macleod A, Mooney PJ, Moule S, Martin DM, Morgan GW, Mungall K, Norbertczak H, Ormond D, Pai G, Peacock CS, Peterson J, Quail MA, Rabbinowitsch E, Rajandream MA, Reitter C, Salzberg SL, Sanders M, Schobel S, Sharp S, Simmonds M, Simpson AJ, Tallon L, Turner CM, Tait A, Tivey AR, Van Aken S, Walker D, Wanless D, Wang S, White B, White O, Whitehead S, Woodward J,Wortman J, Adams MD, Embley TM, Gull K, Ullu E, Barry JD, Fairlamb AH, Opperdoes F, Barrell BG, Donelson JE, Hall N, Fraser CM, Melville SE, El-Sayed NM (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309:416-422 (Pubitemid 40994676)
6. Borst P, Sabatini R (2008) Base J: discovery, biosynthesis, and possible functions. Annu Rev Microbiol 62:235-251
7. Brandenburg J, Schimanski B, Nogoceke E, Nguyen TN, Padovan JC, Chait BT, Cross GA, Günzl A (2007) Multifunctional class I transcription in Trypanosoma brucei depends on a novel protein complex. EMBO J 26:4856-4866 (Pubitemid 350191303)
8. Campbell DA, Kubo K, Clark CG, Boothroyd JC (1987) Precise identification of cleavage sites involved in the unusual processing of trypanosome ribosomal RNA. J Mol Biol 196:113-124
9. Castro C, Hernández R, Castañeda M (1981) Trypanosoma cruzi ribosomal RNA: internal break in the large-molecular-mass species and number of genes. Mol Biochem Parasitol 2:219-233
10. Cavalier-Smith T (2010) Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett 6:342-345
11. Clayton CE, Fueri JP, Itzhaki JE, Bellofatto V, Sherman DR, Wisdom GS, Vijayasarathy S, Mowatt MR (1990) Transcription of the procyclic acidic repetitive protein genes of Trypanosoma brucei. Mol Cell Biol 10:3036-3047
12. Cordingley JS, Turner MJ (1980) 6.5 S RNA; preliminary characterisation of unusual small RNAs in Trypanosoma brucei. Mol Biochem Parasitol 1:91-96
13. Daniels JP, Gull K, Wickstead B (2012) The trypanosomatid-specific N terminus of RPA2 is required for RNA polymerase I assembly, localization, and function. Eukaryot Cell 11:662-672
14. de Andrade SV, Floeter-Winter LM (2002) Functional domains of the rDNA promoter display a differential recognition in Leishmania. Int J Parasitol 32:437-447
15. Decatur WA, Fournier MJ (2003) RNA-guided nucleotide modification of ribosomal and other RNAs. J Biol Chem 278:695-698 (Pubitemid 36790737)
16. Dietrich P, Soares MB, Affonso MH, Floeter-Winter LM (1993) The Trypanosoma cruzi ribosomal RNA-encoding gene: analysis of promoter and upstream intergenic spacer sequences. Gene 125:103-107
17. Elias MC, Marques-Porto R, Freymüller E, Schenkman S (2001) Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Mol Biochem Parasitol 112:79-90 (Pubitemid 32144839)
18. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou L, Huang Y, Kindlund E, Klingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarleton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409-415
19. Figueiredo LM, Cross GA (2010) Nucleosomes are depleted at the VSG expression site transcribed by RNA polymerase I in African trypanosomes. Eukaryot Cell 9:148-154
20. Figueroa-Angulo E, Cevallos AM, Zentella A, López-Villaseñor I, Hernández R (2006) Potential regulatory elements in the Trypanosoma cruzi rRNA gene promoter. Biochim Biophys Acta 1759:497-501
21. Gadelha C, Holden JM, Allison HC, Field MC (2011) Specializations in a successful parasite: what makes the bloodstream-form African trypanosome so deadly? Mol Biochem Parasitol 179:51-58
22. Gao H, Ayub MJ, Levin MJ, Frank J (2005) The structure of the 80S ribosome from Trypanosoma cruzi reveals unique rRNA components. Proc Natl Acad Sci U S A 102:10206-10211 (Pubitemid 41023350)
23. Gay LS, Wilson ME, Donelson JE (1996) The promoter for the ribosomal RNA genes of Leishmania chagasi. Mol Biochem Parasitol 77:193-200 (Pubitemid 26201599)
24. Gerbi SA (1996) Expansion segments: regions of variable size that interrupt the universal core secondary structure of ribosomal RNA. In: Zimmerman RA, Dahlberg AE (eds) Ribosomal RNA. Structure, evolution, processing, and function in protein biosynthesis. CRC, New York, pp 71-87
25. Gray MW, Schnare MN (1990) Evolution of the modular structure of rRNA. In: Warner JR (ed) The ribosome: structure, function, & evolution. American Society for Microbiology, Washington DC, pp 589-597
26. Günzl A (2012) RNA polymerases and transcription factors of trypanosomes. In: Bindereif A (ed) RNA metabolism in trypanosomes. Nucleic Acids Mol Biol 28. Springer-Verlag, Berlin Heidelberg. DOI 10.1007/978-3-642-28687-2- 1
27. Günzl A, Bruderer T, Laufer G, Schimanski B, Tu LC, Chung HM, Lee PT, Lee MG (2003) RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei. Eukaryot Cell 2:542-551 (Pubitemid 36774702)
28. Gupta SK, Hury A, Ziporen Y, Shi H, Ullu E, Michaeli S (2010) Small nucleolar RNAinterference in Trypanosoma brucei:mechanism and utilization for elucidating the function of snoRNAs. Nucleic Acids Res 38:7236-7247
29. Hashem Y, des Georges A, Fu J, Buss SN, Jossinet F, Jobe A, Zhang Q, Liao HY, Grassucci RA, Bajaj C, Westhof E, Madison-Antenucci S, Frank J (2013) High-resolution cryo-electron microscopy structure of the Trypanosoma brucei ribosome. Nature 494:385-389
30. Hernández R, Castañeda M (1983) An endonuclease restriction analysis of the ribosomal RNA genes of Trypanosoma cruzi. Mol Biochem Parasitol 8:305-315
31. Hernández R, Díaz-de Léon F, Castañeda M (1988) Molecular cloning and partial characterization of ribosomal RNA genes from Trypanosoma cruzi. Mol Biochem Parasitol 27:275-279
32. Hernández R, Nava G, Castañeda M (1983) Small-size ribosomal RNA species in Trypanosoma cruzi. Mol Biochem Parasitol 8:297-304
33. Ide S, Miyazaki T, Maki H, Kobayashi T (2010) Abundance of ribosomal RNA gene copiesmaintains genome integrity. Science 327:693-696
34. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, Beck A, Beverley SM, Bianchettin G, Borzym K, Bothe G, Bruschi CV, Collins M, Cadag E, Ciarloni L, Clayton C, Coulson RM, Cronin A, Cruz AK, Davies RM, De Gaudenzi J, Dobson DE, Duesterhoeft A, Fazelina G, Fosker N, Frasch AC, Fraser A, Fuchs M, Gabel C, Goble A, Goffeau A, Harris D, Hertz-Fowler C, Hilbert H, Horn D, Huang Y, Klages S, Knights A, Kube M, Larke N, Litvin L, Lord A, Louie T, Marra M, Masuy D, Matthews K, Michaeli S, Mottram JC, Müller-Auer S, Munden H, Nelson S, Norbertczak H, Oliver K, O'neil S, Pentony M, Pohl TM, Price C, Purnelle B, Quail MA, Rabbinowitsch E, Reinhardt R, Rieger M, Rinta J, Robben J, Robertson L, Ruiz JC, Rutter S, Saunders D, Schäfer M, Schein J, Schwartz DC, Seeger K, Seyler A, Sharp S, Shin H, Sivam D, Squares R, Squares S, Tosato V, Vogt C, Volckaert G, Wambutt R, Warren T, Wedler H, Woodward J, Zhou S, Zimmermann W, Smith DF, Blackwell JM, Stuart KD, Barrell B, Myler PJ (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309:436-442 (Pubitemid 40994677)
35. Janz L, Clayton C (1994) The PARP and rRNA promoters of Trypanosoma brucei are composed of dissimilar sequence elements that are functionally interchangeable. Mol Cell Biol 14:5804-5811 (Pubitemid 24264409)
36. Kelly S, Wickstead B, Gull K (2005) An in silico analysis of trypanosomatid RNA polymerases: insights into their unusual transcription. Biochem Soc Trans 33:1435-1437 (Pubitemid 41779708)
37. Kooter JM, Borst P (1984) Alpha-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes. Nucleic Acids Res 12:9457-9472
38. Krogan NJ, Greenblatt JF (2001) Characterization of a six-subunit holoelongator complex required for the regulated expression of a group of genes in Saccharomyces cerevisiae.Mol Cell Biol 21:8203-8212 (Pubitemid 33051809)
39. Laufer G, Schaaf G, Bollgönn S, Günzl A (1999) In vitro analysis of alpha-amanitin-resistant transcription from the rRNA, procyclic acidic repetitive protein, and variant surface glycoprotein gene promoters in Trypanosoma brucei. Mol Cell Biol 19:5466-5473 (Pubitemid 29339904)
40. Malarkey CS, Churchill ME (2012) The high mobility group box: the ultimate utility player of a cell. Trends Biochem Sci 37:553-562
41. Marchant A, Hartley MR (1994) Mutational studies on the α-sarcin loop of Escherichia coli 23S ribosomal RNA. Eur J Biochem 226:141-147
42. Martínez-Calvillo S, Sunkin SM, Yan S, Fox M, Stuart K, Myler PJ (2001) Genomic organization and functional characterization of the Leishmania major Friedlin ribosomal RNA gene locus. Mol Biochem Parasitol 116:147-157 (Pubitemid 32777824)
43. Martínez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, Myler PJ (2003) Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11:1291-1299 (Pubitemid 36645147)
44. Matthews KR (2005) The developmental cell biology of Trypanosoma brucei. J Cell Sci 118:283-290
45. Merz K, Hondele M, Goetze H, Gmelch K, Stoeckl U, Griesenbeck J (2008) Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev 22:1190-1204 (Pubitemid 351656578)
46. Michaeli S (2012) rRNA Biogenesis in Trypanosomes. In: Bindereif A (ed) RNA metabolism in trypanosomes. Nucleic Acids Mol Biol 28. Springer-Verlag, Berlin Heidelberg. doi 10.1007/978-3-642-28687- 2
47. Michaeli S, Doniger T, Gupta SK, Wurtzel O, Romano M, Visnovezky D, Sorek R, Unger R, Ullu E (2012) RNA-seq analysis of small RNPs in Trypanosoma brucei reveals a rich repertoire of non-coding RNAs. Nucleic Acids Res 40:1282-1298
48. Narayanan MS, Rudenko G (2013) TDP1 is an HMG chromatin protein facilitating RNA polymerase I transcription in African trypanosomes. Nucleic Acids Res 41:2981-2992
49. Navarro M, Gull K (2001) A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei. Nature 414: 759-763 (Pubitemid 34000774)
50. Nepomuceno-Mejía T, Lara-Martínez R, Cevallos AM, López-Villaseñor I, Jiménez-García LF, Hernández R (2010) The Trypanosoma cruzi nucleolus: a morphometrical analysis of cultured epimastigotes in the exponential and stationary phases. FEMS Microbiol Lett 313: 41-46
51. Nguyen TN, Nguyen BN, Lee JH, Panigrahi AK, Günzl A (2012) Characterization of a novel class I transcription factor A (CITFA) subunit that is indispensable for transcription by the multifunctional RNA polymerase I of Trypanosoma brucei. Eukaryot Cell 11:1573-1581
52. Nguyen TN, Schimanski B, Günzl A (2007)Active RNA polymerase I of Trypanosoma brucei harbors a novel subunit essential for transcription. Mol Cell Biol 27:6254-6263 (Pubitemid 47326711)
53. Nguyen TN, Schimanski B, Zahn A, Klumpp B, Günzl A (2006) Purification of an eight subunit RNA polymerase I complex in Trypanosoma brucei. Mol Biochem Parasitol 149:27-37 (Pubitemid 44037838)
54. Nguyen TN, Müller LS, Park SH, Siegel TN, Günzl A (2014) Promoter occupancy of the basal class I transcription factor A differs strongly between active and silent VSG expression sites in Trypanosoma brucei. Nucleic Acids Res 42:3164-3176
55. Park SH, Nguyen TN, Kirkham JK, Lee JH, Günzl A (2011) Transcription by the multifunctional RNA polymerase I in Trypanosoma brucei functions independently of RPB7. Mol Biochem Parasitol 180:35-42
56. Reeder RH (1992) Regulation of transcription by RNA polymerase I. In: McKnight SL, Yamamoto KR (eds) Transcriptional regulation, vol I. Cold Spring Harbor Laboratory, New York, pp 315-347
57. Reeder RH, Guevara P, Roan JG (1999) Saccharomyces cerevisiae RNA polymerase I terminates transcription at the Reb1 terminator in vivo. Mol Cell Biol 19:7369-7376 (Pubitemid 29493400)
58. Requena JM, Soto M, Quijada L, Carrillo G, Alonso C (1997) A region containing repeated elements is associated with transcriptional termination of Leishmania infantum ribosomal RNA genes. Mol Biochem Parasitol 84:101-110 (Pubitemid 27090510)
59. Respuela P, Ferella M, Rada-Iglesias A, Aslund L (2008) Histone acetylation and methylation at sites initiating divergent polycistronic transcription in Trypanosoma cruzi. J Biol Chem 283:15884-15892
60. Rudenko G, Bishop D, Gottesdiener K, Van der Ploeg LH (1989) Alpha-amanitin resistant transcription of protein coding genes in insect and bloodstream form Trypanosoma brucei. EMBO J 8:4259-4263 (Pubitemid 20066869)
61. Rudenko G, Chung HM, Pham VP, Van der Ploeg LH (1991) RNA polymerase I can mediate expression of CAT and neo protein-coding genes in Trypanosoma brucei. EMBO J 10:3387-3397 (Pubitemid 21905364)
62. Schimanski B, Klumpp B, Laufer G, Marhöfer RJ, Selzer PM, Günzl A (2003) The second largest subunit of Trypanosoma brucei's multifunctional RNA polymerase I has a unique N-terminal extension domain. Mol Biochem Parasitol 126:193-200 (Pubitemid 36255618)
63. Schimanski B, Laufer G, Gontcharova L, Günzl A (2004) The Trypanosoma brucei spliced leader RNA and rRNA gene promoters have interchangeable TbSNAP50-binding elements. Nucleic Acids Res 32:700-709 (Pubitemid 38263061)
64. Schwede A, Jones N, Engstler M, Carrington M (2011) The VSG C-terminal domain is inaccessible to antibodies on live trypanosomes. Mol Biochem Parasitol 175:201-204
65. Stanne TM, Rudenko G (2010) Active VSG expression sites in Trypanosoma brucei are depleted of nucleosomes. Eukaryotic Cell 9:136-147
66. Stuart K, Panigrahi AK (2002) RNA editing: complexity and complications. Mol Microbiol 45:591-596 (Pubitemid 34989168)
67. Sutton RE, Boothroyd JC (1986) Evidence for trans splicing in trypanosomes. Cell 47:527-535 (Pubitemid 17215344)
68. Tanowitz HB, Weiss LM, Montgomery SP (2011) Chagas disease has now gone global. PLoS Negl Trop Dis 5:e1136. doi:10.1371/journal.pntd.0001136
69. Torres-Machorro AL, Hernández R, Cevallos AM, López- Villaseñor I (2010) Ribosomal RNA genes in eukaryotic microorganisms: witnesses of phylogeny? FEMS Microbiol Rev 34:59-86
70. Walgraffe D, Devaux S, Lecordier L, Dierick JF, Dieu M, Van den Abbeele J, Pays E,Vanhamme L (2005) Characterization of subunits of the RNA polymerase I complex in Trypanosoma brucei. Mol Biochem Parasitol 139:249-260 (Pubitemid 40128220)
71. White TC, Rudenko G, Borst P (1986) Three small RNAs within the 10 kb trypanosome rRNA transcription unit are analogous to domain VII of other eukaryotic 28S rRNAs. Nucleic Acids Res 14:9471-9489
72. Woolford JL Jr, Baserga SJ (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195:643-681
73. Yan S, Lodes MJ, Fox M, Myler PJ, Stuart K (1999) Characterization of the Leishmania donovani ribosomal RNA promoter. Mol Biochem Parasitol 103:197-210 (Pubitemid 29469773)
74. Yokoyama T, Suzuki T (2008) Ribosomal RNAs are tolerant toward genetic insertions: evolutionary origin of the expansion segments. Nucleic Acids Res 36:3539-3551 (Pubitemid 351917519)
75. Zomerdijk JCBM, Kieft R, Borst P (1991a) Efficient production of functional mRNA mediated by RNA polymerase I in Trypanosoma brucei. Nature 353:772-775 (Pubitemid 21912619)
76. Zomerdijk JCBM, Kieft R, Shiels PG, Borst P (1991b) Alpha-amanitin- resistant transcription units in trypanosomes: a comparison of promoter sequences for a VSG gene expression site and for the ribosomal RNA genes. Nucleic Acids Res 19:5153-5158 (Pubitemid 21912904)