RNA-binding proteins and their role in the regulation of gene expression in <i>Trypanosoma cruzi</i> and <i>Saccharomyces cerevisiae</i>

Oliveira, Camila; Faoro, Helisson; Alves, Lysangela Ronalte; Goldenberg, Samuel

doi:10.1590/1678-4685-GMB-2016-0258

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Special Series of Articles - 60 Years of The Brazilian Society of Genetics • Genet. Mol. Biol. 40 (01) • Mar 2017 • https://doi.org/10.1590/1678-4685-GMB-2016-0258 copy

RNA-binding proteins and their role in the regulation of gene expression in Trypanosoma cruzi and Saccharomyces cerevisiae

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

RNA-binding proteins (RBPs) have important functions in the regulation of gene expression. RBPs play key roles in post-transcriptional processes in all eukaryotes, such as splicing regulation, mRNA transport and modulation of mRNA translation and decay. RBPs assemble into different mRNA-protein complexes, which form messenger ribonucleoprotein complexes (mRNPs). Gene expression regulation in trypanosomatids occurs mainly at the post-transcriptional level and RBPs play a key role in all processes. However, the functional characterization of RBPs in Trypanosoma cruzi has been impaired due to the lack of reliable reverse genetic manipulation tools. The comparison of RBPs from Saccharomyces cerevisiae and T. cruzi might allow inferring on the function of these proteins based on the information available for the orthologous RNA-binding proteins from the S. cerevisiae model organism. In this review, we discuss the role of some RBPs from T. cruzi and their homologues in regulating gene expression in yeast.

Keywords:
RNA-binding proteins; Trypanosoma cruzi; Saccharomyces cerevisiae; gene expression regulation

Protein	Function	Ref.	Domain
SR62	mRNA processing/stability	*Názer et al.* (2011)**Názer E, Verdún RE and Sánchez DO (2011) Nucleolar localization of RNA binding proteins induced by actinomycin D and heat shock in Trypanosoma cruzi. PLoS One 6:e19920.	SR-related
ZC3H39	Regulator of a specific subset of mRNAs	*Alves et al., 2014*Alves LR, Oliveira C, Mörking PA, Kessler RL, Martins ST, Romagnoli BA, Marchini FK and Goldenberg S (2014) The mRNAs associated to a zinc finger protein from Trypanosoma cruzi shift during stress conditions. RNA Biol 11:921-933.	CCCH
UBP1	mRNA destabilizing factor	D’Orso and Frasch (2002)D’Orso I and Frasch AC (2002) TcUBP-1, an mRNA destabilizing factor from trypanosomes, homodimerizes and interacts with novel AU-rich element- and Poly(A)-binding proteins forming a ribonucleoprotein complex. J Biol Chem 277:50520-50528.	RRM
UBP2	mRNA destabilizing factor	D’Orso and Frasch (2002)D’Orso I and Frasch AC (2002) TcUBP-1, an mRNA destabilizing factor from trypanosomes, homodimerizes and interacts with novel AU-rich element- and Poly(A)-binding proteins forming a ribonucleoprotein complex. J Biol Chem 277:50520-50528.	RRM
PUF6	mRNA destabilizing factor	*Dallagiovanna et al.* (2008)**Dallagiovanna B, Correa A, Probst CM, Holetz F, Smircich P, de Aguiar AM, Mansur F, da Silva CV, Mortara RA, Garat G, et al. (2008) Functional genomic characterization of mRNAs associated with TcPUF6, a pumilio-like protein from Trypanosoma cruzi. J Biol Chem 283:8266-8273.	Pumilio
ZFP1	Involved in differentiation	*Mörking et al.* (2004)**Mörking PA, Dallagiovanna BM, Foti L, Garat B, Picchi GF, Umaki AC, Probst CM, Krieger MA, Goldenberg S and Fragoso SP (2004) TcZFP1: a CCCH zinc finger protein of Trypanosoma cruzi that binds poly-C oligoribonucleotides in vitro. Biochem Biophys Res Commun 319:169-177.	CCCH
ZFP2	Involved in differentiation	*Mörking et al.* (2004Mörking PA, Dallagiovanna BM, Foti L, Garat B, Picchi GF, Umaki AC, Probst CM, Krieger MA, Goldenberg S and Fragoso SP (2004) TcZFP1: a CCCH zinc finger protein of Trypanosoma cruzi that binds poly-C oligoribonucleotides in vitro. Biochem Biophys Res Commun 319:169-177., 2012**Mörking PA, Rampazzo RC, Walrad P, Probst CM, Soares MJ, Gradia DF, Pavoni DP, Krieger MA, Matthews K, Goldenberg S, et al. (2012) The zinc finger protein TcZFP2 binds target mRNAs enriched during Trypanosoma cruzi metacyclogenesis. Mem Inst Oswaldo Cruz 107:790-799.)	CCCH
ZFP3	Involved in differentiation, translation regulator	*Mörking et al.* (2004)**Mörking PA, Dallagiovanna BM, Foti L, Garat B, Picchi GF, Umaki AC, Probst CM, Krieger MA, Goldenberg S and Fragoso SP (2004) TcZFP1: a CCCH zinc finger protein of Trypanosoma cruzi that binds poly-C oligoribonucleotides in vitro. Biochem Biophys Res Commun 319:169-177.	CCCH
RBP40	Regulator of a specific subset of mRNAs	*Guerra-Slompo et al.* (2012)**Guerra-Slompo EP, Probst CM, Pavoni DP, Goldenberg S, Krieger MA and Dallagiovanna B (2012) Molecular characterization of the Trypanosoma cruzi specific RNA binding protein TcRBP40 and its associated mRNAs. Biochem Biophys Res Commun 420:302-307.	RRM
RBP19	Involved in differentiation	*Pérez-Díaz et al.* (2012Pérez-Díaz L, Correa A, Moretão MP, Goldenberg S, Dallagiovanna B and Garat B (2012) The overexpression of the trypanosomatid-exclusive TcRBP19 RNA-binding protein affects cellular infection by Trypanosoma cruzi. Mem Inst Oswaldo Cruz 107:1076-1079., 2013**Pérez-Díaz L, Pastro L, Smircich P, Dallagiovanna B and Garat B (2013) Evidence for a negative feedback control mediated by the 3’ untranslated region assuring the low expression level of the RNA binding protein TcRBP19 in T. cruzi epimastigotes. Biochem Biophys Res Commun 436:295-299.)	RRM
DRBD4/PTB2	Involved regulation of splicing	*De Gaudenzi et al., (2016)*De Gaudenzi JG, Jäger AV, Izcovich R and Campo VAO (2016) Insights into the regulation of mRNA processing of polycistronic transcripts mediated by DRBD4/PTB2, a trypanosome homolog of the polypyrimidine tract-binding protein. J Eukaryot Microbiol 63440-452.	RRM
PABP1	Involved in translation	*Batista et al.* (1994)**Batista JA, Teixeira SM, Donelson JE, Kirchhoff LV and de Sá CM (1994) Characterization of a Trypanosoma cruzi poly(A)-binding protein and its genes. Mol Biochem Parasitol 67:301-312.	RRM

Trypanosoma cruzi id (Tc)	Domains	Saccharomyces cerevisiae id (Sc)	Domains	Tc length	Sc length	Tc qcovhsp	Sc qcovhsp	pident
TcCLB.506885.70	RRM	sp\|P04147\|PABP	RRM	570	577	94	92	38.52
TcCLB.511741.40	RRM	sp\|P40561\|SGN1	RRM	231	250	39	35	43.33
TcCLB.504431.90	RRM	sp\|P40567\|MSL1	RRM	114	111	76	76	32.58
TcCLB.503577.20	Zinc Finger	sp\|Q06102\|YTH1	Zinc Finger	233	208	11	12	44
TcCLB.504071.80	RRM	sp\|Q08920\|NCBP2	RRM	188	208	60	68	40.85
TcCLB.511303.60	Eukaryotic translation initiation factor eIF2A / RRM	sp\|P06103\|EIF3B	Eukaryotic translation initiation factor eIF2A /RRM	696	763	90	83	22.17
TcCLB.511367.60	La / RRM	sp\|P33399\|LHP1	La / RRM	333	275	56	73	33.18
TcCLB.508299.89	RRM	sp\|P53743\|ESF2	RRM	238	316	44	34	32.41
TcCLB.511863.20	RRM	sp\|P32605\|RU1A	RRM	371	298	27	33	27.72
TcCLB.507037.20	RRM	sp\|P37838\|NOP4	RRM	486	685	70	53	27.59
TcCLB.507515.60	RRM	sp\|P40565\|IST3	RRM	156	148	40	43	44.44
TcCLB.504045.114	Tryptophan synthase alpha chain / RRM	sp\|P00931\|TRP	Tryptophan synthase alpha chain / RRM	185	707	54	14	25.23
TcCLB.510657.160	RRM	sp\|Q08208\|NOP12	RRM	421	459	50	48	24.68
TcCLB.503897.90	RRM	sp\|Q06106\|MRD1	RRM	878	887	99	77	27.14
TcCLB.504157.10	RRM	sp\|P34167\|IF4B	RRM	450	436	20	21	34.38
TcCLB.508409.80	MIF4G / RRM	sp\|P39935\|IF4F1	MIF4G / RRM	501	952	27	11	25.66
TcCLB.506693.30	RRM	sp\|Q00539\|NAM8	RRM	243	523	30	17	38.64
TcCLB.511127.10	RRM	sp\|Q00916\|RU17	RRM	240	300	33	26	33.75
TcCLB.508567.100	Adaptin N terminal region / RRM	sp\|P38065\|AP2A	Adaptin N terminal region / RRM	1405	1025	11	14	24.38
TcCLB.511867.180	PUB	sp\|P32900\|SKG6	Transmembrane alpha-helix domain	365	734	37	16	23.53

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[1] Send correspondence to Lysangela Ronalte Alves or Samuel Goldenberg. Instituto Carlos Chagas, Fiocruz-Paraná, Rua Professor Algacyr Munhoz Mader 3775, Cidade Industrial de Curitiba, 81350-010 Curitiba, PR, Brazil. E-mail: lysalves@fiocruz.br; sgoldenb@fiocruz.br.