Ribosome profiling reveals translation control as a key mechanism generating differential gene expression in Trypanosoma cruzi

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Smircich, Pablo ^b,c   Eastman, Guillermo ^a   Bispo, Saloe ^d   Duhagon, María Ana ^b,c   Guerra Slompo, Eloise P ^d   Garat, Beatriz ^b   Goldenberg, Samuel ^d   Munroe, David J ^e   Dallagiovanna, Bruno ^d   Holetz, Fabiola ^d   Sotelo Silveira, Jose R ^a,b  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^d INSTITUTO OSWALDO CRUZ   (Brazil)

^e FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

Neglected disease; Ribosomal proteins; Ribosome profiling; Trans sialidases; Transcriptome; Translation regulation; Translatome; Trypanosoma cruzi

Indexed keywords

MESSENGER RNA; PROTEOME; SIALIDASE; TRANSCRIPTOME; TRANSIALIDASE; UNCLASSIFIED DRUG; PROTOZOAL PROTEIN; PROTOZOAL RNA;

ARTICLE; CHAGAS DISEASE; CONTROLLED STUDY; EPIMASTIGOTE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENOME; NONHUMAN; PARASITE DEVELOPMENT; PARASITE VIRULENCE; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEOMICS; RIBOSOME; RNA ANALYSIS; RNA SEQUENCE; STEADY STATE; TRANSLATION REGULATION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; DOWN REGULATION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; METABOLISM; PROCEDURES; UPREGULATION;

HEXAPODA; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIFE CYCLE STAGES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; PROTOZOAN PROTEINS; RIBOSOMES; RNA, PROTOZOAN; TRYPANOSOMA CRUZI; UP-REGULATION;

EID: 85019182484     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1563-8     Document Type: Article

References (57)

1. WHO. Control. of Chagas disease. World Health Organ Tech Rep Ser. 2002;905:i-vi, 1-109, back cover.
2. de Souza W. Cell biology of Trypanosoma cruzi. Int Rev Cytol. 1984;86:197-283.
3. Goldenberg S, Salles JM, Contreras VT, Lima Franco MP, Katzin AM, Colli W, et al. Characterization of messenger RNA from epimastigotes and metacyclic trypomastigotes of Trypanosoma cruzi. FEBS Lett. 1985;180(2):265-70.
4. Walker G, Dorrell RG, Schlacht A, Dacks JB. Eukaryotic systematics: a user's guide for cell biologists and parasitologists. Parasitology. 2011;138(13):1638-63.
5. Cavalier-Smith T. Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett. 2010;6(3):342-5.
6. Martinez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, Myler PJ. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell. 2003;11(5):1291-9.
7. Worthey EA, Martinez-Calvillo S, Schnaufer A, Aggarwal G, Cawthra J, Fazelinia G, et al. Leishmania major chromosome 3 contains two long convergent polycistronic gene clusters separated by a tRNA gene. Nucleic Acids Res. 2003;31(14):4201-10.
8. Kolev NG, Franklin JB, Carmi S, Shi H, Michaeli S, Tschudi C. The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog. 2010;6(9), e1001090.
9. Smircich P, Forteza D, El-Sayed NM, Garat B. Genomic analysis of sequence-dependent DNA curvature in Leishmania. PLoS One. 2013;8(4), e63068.
10. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science. 2005;309(5733):409-15.
11. Clayton CE. Life without transcriptional control? From fly to man and back again. EMBO J. 2002;21(8):1881-8.
12. Clayton C. The regulation of trypanosome gene expression by RNA-binding proteins. PLoS Pathog. 2013;9(11), e1003680.
13. Minning TA, Weatherly DB, Atwood 3rd J, Orlando R, Tarleton RL. The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics. 2009;10:370.
14. Kramer S. Developmental regulation of gene expression in the absence of transcriptional control: the case of kinetoplastids. Mol Biochem Parasitol. 2012;181(2):61-72.
15. Avila AR, Yamada-Ogatta SF, da Silva MV, Krieger MA, Nakamura CV, de Souza W, et al. Cloning and characterization of the metacyclogenin gene, which is specifically expressed during Trypanosoma cruzi metacyclogenesis. Mol Biochem Parasitol. 2001;117(2):169-77.
16. Dallagiovanna B, Plazanet-Menut C, Ogatta SF, Avila AR, Krieger MA, Goldenberg S. Trypanosoma cruzi: a gene family encoding chitin-binding-like proteins is posttranscriptionally regulated during metacyclogenesis. Exp Parasitol. 2001;99(1):7-16.
17. Nardelli SC, Avila AR, Freund A, Motta MC, Manhaes L, de Jesus TC, et al. Small-subunit rRNA processome proteins are translationally regulated during differentiation of Trypanosoma cruzi. Eukaryot Cell. 2007;6(2):337-45.
18. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. Genome-wide analysis of in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009;324(5924):218-23.
19. Ingolia NT. Ribosome profiling: new views of translation, from single codons to genome scale. Nat Rev Genet. 2014;15(3):205-13.
20. Nilsson D, Gunasekera K, Mani J, Osteras M, Farinelli L, Baerlocher L, et al. Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog. 2010;6(8), e1001037.
21. Siegel TN, Hekstra DR, Wang X, Dewell S, Cross GA. Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res. 2010;38(15):4946-4957
22. Manful T, Fadda A, Clayton C. The role of the 5'-3' exoribonuclease XRNA in transcriptome-wide mRNA degradation. RNA. 2011;17(11):2039-47.
23. Vasquez JJ, Hon CC, Vanselow JT, Schlosser A, Siegel TN. Comparative ribosome profiling reveals extensive translational complexity in different Trypanosoma brucei life cycle stages. Nucleic Acids Res. 2014;42(6):3623-3637
24. Michel AM, Choudhury KR, Firth AE, Ingolia NT, Atkins JF, Baranov PV. Observation of dually decoded regions of the human genome using ribosome profiling data. Genome Res. 2012;22(11):2219-29.
25. Atwood JA, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, et al. The Trypanosoma cruzi proteome. Science. 2005;309(5733):473-6.
26. de Godoy LM, Marchini FK, Pavoni DP, Rampazzo Rde C, Probst CM, Goldenberg S, et al. Quantitative proteomics of Trypanosoma cruzi during metacyclogenesis. Proteomics. 2012;12(17):2694-703.
27. Ingolia NT. Genome-wide translational profiling by ribosome footprinting. Methods Enzymol. 2010;470:119-42.
28. Ingolia NT, Brar GA, Rouskin S, McGeachy AM, Weissman JS. The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc. 2012;7(8):1534-50.
29. Ingolia NT, Lareau LF, Weissman JS. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell. 2011;147(4):789-802.
30. Cuevas IC, Cazzulo JJ, Sanchez DO. gp63 homologues in Trypanosoma cruzi: surface antigens with metalloprotease activity and a possible role in host cell infection. Infect Immun. 2003;71(10):5739-49.
31. Manque PM, Neira I, Atayde VD, Cordero E, Ferreira AT, da Silveira JF, et al. Cell adhesion and Ca2+ signaling activity in stably transfected Trypanosoma cruzi epimastigotes expressing the metacyclic stage-specific surface molecule gp82. Infect Immun. 2003;71(3):1561-5.
32. Bayer-Santos E, Gentil LG, Cordero EM, Correa PR, da Silveira JF. Regulatory elements in the 3' untranslated region of the GP82 glycoprotein are responsible for its stage-specific expression in Trypanosoma cruzi metacyclic trypomastigotes. Acta Trop. 2012;123(3):230-3.
33. De Pablos LM, Osuna A. Multigene families in Trypanosoma cruzi and their role in infectivity. Infect Immun. 2012;80(7):2258-64.
34. Alves MJ, Colli W. Role of the gp85/trans-sialidase superfamily of glycoproteins in the interaction of Trypanosoma cruzi with host structures. Subcell Biochem. 2008;47:58-69.
35. Rossi D, Kuroshu R, Zanelli CF, Valentini SR. eIF5A and EF-P: two unique translation factors are now traveling the same road. Wiley interdisciplinary reviews RNA. 2014;5(2):209-22.
36. Kang HA, Hershey JW. Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem. 1994;269(6):3934-40.
37. Chung J, Rocha AA, Tonelli RR, Castilho BA, Schenkman S. Eukaryotic initiation factor 5A dephosphorylation is required for translational arrest in stationary phase cells. Biochem J. 2013;451(2):257-67.
38. Pascoalino B, Dindar G, Vieira-da-Rocha JP, Machado CR, Janzen CJ, Schenkman S. Characterization of two different Asf1 histone chaperones with distinct cellular localizations and functions in Trypanosoma brucei. Nucleic Acids Res. 2014;42(5):2906-18.
39. Avila AR, Dallagiovanna B, Yamada-Ogatta SF, Monteiro-Goes V, Fragoso SP, Krieger MA, et al. Stage-specific gene expression during Trypanosoma cruzi metacyclogenesis. Genet Mol Res. 2003;2(1):159-68.
40. Baptista CS, Vencio RZ, Abdala S, Valadares MP, Martins C, de Braganca Pereira CA, et al. DNA microarrays for comparative genomics and analysis of gene expression in Trypanosoma cruzi. Mol Biochem Parasitol. 2004;138(2):183-94.
41. Paba J, Santana JM, Teixeira AR, Fontes W, Sousa MV, Ricart CA. Proteomic analysis of the human pathogen Trypanosoma cruzi. Proteomics. 2004;4(4):1052-9.
42. Parodi-Talice A, Monteiro-Goes V, Arrambide N, Avila AR, Duran R, Correa A, et al. Proteomic analysis of metacyclic trypomastigotes undergoing Trypanosoma cruzi metacyclogenesis. J Mass Spectrom. 2007;42(11):1422-32.
43. De Gaudenzi JG, Noe G, Campo VA, Frasch AC, Cassola A. Gene expression regulation in trypanosomatids. Essays Biochem. 2011;51:31-46.
44. Urbaniak MD, Guther ML, Ferguson MA. Comparative SILAC proteomic analysis of Trypanosoma brucei bloodstream and procyclic lifecycle stages. PLoS One. 2012;7(5), e36619.
45. Freitas LM, dos Santos SL, Rodrigues-Luiz GF, Mendes TA, Rodrigues TS, Gazzinelli RT, et al. Genomic analyses, gene expression and antigenic profile of the trans-sialidase superfamily of Trypanosoma cruzi reveal an undetected level of complexity. PLoS One. 2011;6(10), e25914.
46. Jager AV, Muia RP, Campetella O. Stage-specific expression of Trypanosoma cruzi trans-sialidase involves highly conserved 3' untranslated regions. FEMS Microbiol Lett. 2008;283(2):182-8.
47. Ayub MJ, Atwood J, Nuccio A, Tarleton R, Levin MJ. Proteomic analysis of the Trypanosoma cruzi ribosomal proteins. Biochem Biophys Res Commun. 2009;382(1):30-4.
48. Johnsson P, Morris KV, Grander D. Pseudogenes: a novel source of trans-acting antisense RNAs. Methods Mol Biol. 2014;1167:213-26.
49. Kandouz M, Bier A, Carystinos GD, Alaoui-Jamali MA, Batist G. Connexin43 pseudogene is expressed in tumor cells and inhibits growth. Oncogene. 2004;23(27):4763-70.
50. Ucciferri N, Rocchiccioli S. Proteomics techniques for the detection of translated pseudogenes. Methods Mol Biol. 2014;1167:187-95.
51. Contreras VT, Salles JM, Thomas N, Morel CM, Goldenberg S. In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol Biochem Parasitol. 1985;16(3):315-27.
52. Bonaldo MC, Souto-Padron T, de Souza W, Goldenberg S. Cell-substrate adhesion during Trypanosoma cruzi differentiation. J Cell Biol. 1988;106(4):1349-58.
53. Holetz FB, Correa A, Avila AR, Nakamura CV, Krieger MA, Goldenberg S. Evidence of P-body-like structures in Trypanosoma cruzi. Biochem Biophys Res Commun. 2007;356(4):1062-7.
54. Alves LR, Avila AR, Correa A, Holetz FB, Mansur FC, Manque PA, et al. Proteomic analysis reveals the dynamic association of proteins with translated mRNAs in Trypanosoma cruzi. Gene. 2010;452(2):72-8.
55. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106.
56. Dennis Jr G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003;4(5):3.
57. Huang D, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57.