PUF Proteins as Critical RNA-Binding Proteins in TriTryp Parasites: A Review Article
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Abstract
In eukaryotes, translation is a fundamental step in the long pathway of protein synthesis within the cell. In this process, several proteins and factors have involved directly or indirectly, individually or in association with other elements to contact mRNA. For perfect translation, many essential modifications should be done, such as cis-splicing to remove introns and two main events for capping and poly A polymerization in 5’ and 3’ end of mRNA, respectively. Gene expression is then regulated at both translation and stability of the target mRNA molecule levels. Pumilio/FBFs (PUFs) are the main group of RNA-binding proteins which bind to the 3’-UTR of target RNA and thereby regulate the fate, stability and subcellular localization of mRNAs and adjust the translated protein level. PUF proteins have been found both in nucleus where that bind to precursor mRNA, for processing and maturation of rRNA, and in cytoplasm where that bind to mRNA, stall the ribosomes, suppress the translation and localization of the mRNA. They can regulate the expression of mRNAs through activation or suppression of translation. Therefore, these proteins have recently garnered much attention as new generation of therapeutic targets against diseases such as cancer and neurological disorders. In comparison to other eukaryotes, trypanosomatids have a high number of PUF proteins, which function not only as gene expression regulatory factors but also in several biological processes such as differentiation and life-cycle progression of the cells. Here, we review the molecular and biological roles of known PUF proteins in TriTryp parasites (Trypanosome brucei, T. cruzi and Leishmania) beside some other parasites.
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2. Day D, Tuite MF. Post-transcriptional gene regulatory mechanisms in eukaryotes: an overview. J Endocrinol. 1998;157 (3):361-71.
3. Matoulkova E, Michalova E, Vojtesek B, Hrstka R. The role of the 3'untranslated region in post-transcriptional regulation of protein expression in mammalian cells. RNA Biol. 2012;9 (5):563-76.
4. Wang M, Ogé L, Perez-Garcia MD, et al. The PUF protein family: overview on PUF RNA targets, biological functions, and post transcriptional regulation. Int J Mol Sci. 2018;19 (2):410.
5. Najdrová V, Stairs CW, Vinopalová M, Voleman L, Doležal PJBb. The evolution of the PUF superfamily of proteins across the tree of eukaryotes. BMC Biol. 2020;18 (1):77.
6. Dallagiovanna B, Pérez L, Sotelo-Silveira J, et al. Trypanosoma cruzi: molecular characterization of TcPUF6, a Pumilio protein. Exp Parasitol. 2005;109 (4):260-4.
7. Jalal Kiani S, Taheri T, Rafati S, Samimi-Rad K. PUF proteins: Cellular functions and potential applications. Curr Protein Pept Sci. 2017;18 (3):250-61.
8. Wang X, Zamore PD, Hall TMT. Crystal structure of a Pumilio homology domain. Mol Cell. 2001;7 (4):855-65.
9. Kiani SJ, Ghalejoogh ZY, Samimi-Rad K. Engineered PUF proteins: new flexible toolkits to target the replication of RNA viruses. Future Virol. 2021;16 (1):5-13.
10. Liu M, Miao J, Liu T, et al. Characterization of TgPuf1, a member of the Puf family RNA-binding proteins from Toxoplasma gondii. Parasit Vectors. 2014;7:141.
11. Folgueira C, Martínez-Bonet M, Requena JMJBrn. The Leishmania infantum PUF proteins are targets of the humoral response during visceral Leishmaniasis. BMC Res Notes. 2010;3:13.
12. Sonoda J, Wharton RPJG. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev. 1999;13 (20):2704-12.
13. Moore FL, Jaruzelska J, Fox MS, et al. Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proc Natl Acad Sci U S A. 2003;100 (2):538-43.
14. Kraemer B, Crittenden S, Gallegos M, et al. NANOS-3 and FBF proteins physically interact to control the sperm–oocyte switch in Caenorhabditis elegans. Curr Biol. 1999;9 (18):1009-18.
15. Weidmann CA, Qiu C, Arvola RM, et al. Drosophila Nanos acts as a molecular clamp that modulates the RNA-binding and repression activities of Pumilio. Elife. 2016;5:e17096.
16. Saljoughian N, Taheri T, Rafati S. Live vaccination tactics: possible approaches for controlling visceral Leishmaniasis. Front Immunol. 2014;5:134.
17. Seyed N, Taheri T, Rafati S. Post-genomics and vaccine improvement for Leishmania. Front Microbiol. 2016;7:467.
18. Taheri T, Seyed N, Mizbani A, Rafati S. Leishmania-based expression systems. Appl Microbiol Biotechnol. 2016;100(17):7377-85.
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20. Caro F, Bercovich N, Atorrasagasti C, Levin MJ, Vázquez MP. Trypanosoma cruzi: analysis of the complete PUF RNA-binding protein family. Exp Parasitol. 2006;113 (2):112-24.
21. Wang X, Voronina EJFic, biology d. Diverse roles of PUF proteins in germline stem and progenitor cell development in C. elegans. Front Cell Dev Biol. 2020;8:29.
22. Lee MH, Schedl T. RNA-binding proteins. WormBook. 2006; 1-13. doi: 10.1895/wormbook.1.79.1.
23. Wickens M, Bernstein DS, Kimble J, Parker R. A PUF family portrait: 3′ UTR regulation as a way of life. Trends Genet. 2002;18 (3):150-7.
24. Xu Z, Zhao J, Hong M, Zeng C, Guang S, Shi Y. Structural recognition of the mRNA 3′ UTR by PUF-8 restricts the lifespan of C. elegans. Nucleic Acids Res. 2021;49 (17):10082-97.
25. Zhang C, Muench DGJJoBC. A nucleolar PUF RNA-binding protein with specificity for a unique RNA sequence. J Biol Chem. 2015;290 (50):30108-18.
26. García-Rodríguez LJ, Gay AC, Pon LAJTJocb. Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast. J Cell Biol. 2007;176 (2):197-207.
27. Haramati O, Brodov A, Yelin I, et al. Identification and characterization of roles for Puf1 and Puf2 proteins in the yeast response to high calcium. Sci Rep. 2017;7 (1):3037.
28. Hsiao WY, Wang YT, Wang SW. Fission yeast Puf2, a Pumilio and FBF family RNA-binding protein, links stress granules to processing bodies. Mol Cell Biol. 2020;40 (9):e00589-19.
29. Gerber AP, Herschlag D, Brown PO, Eddy SJPb. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2004;2 (3):E79.
30. Saint-Georges Y, Garcia M, Delaveau T, et al. Yeast mitochondrial biogenesis: a role for the PUF RNA-binding protein Puf3p in mRNA localization. PLoS One. 2008;3 (6):e2293.
31. Zipor G, Haim-Vilmovsky L, Gelin-Licht R, et al. Localization of mRNAs coding for peroxisomal proteins in the yeast, Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2009;106 (47):19848-53.
32. Gu W, Deng Y, Zenklusen D, Singer RH. A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev. 2004;18 (12):1452-65.
33. Uyhazi KE, Yang Y, Liu N, et al. Pumilio proteins utilize distinct regulatory mechanisms to achieve complementary functions required for pluripotency and embryogenesis. Proc Natl Acad Sci U S A. 2020;117 (14):7851-62.
34. Liang X, Hart KJ, Dong G, et al. Puf3 participates in ribosomal biogenesis in malaria parasites. J Cell Sci. 2018;131 (6):jcs212597.
35. Zhang M, Mishra S, Sakthivel R, Fontoura BM, Nussenzweig. UIS2: a unique phosphatase required for the development of Plasmodium liver stages. PLoS Pathog. 2016;12 (1):e1005370.
36. Hoek M, Zanders T, Cross GA. Trypanosoma brucei expression-site-associated-gene-8 protein interacts with a Pumilio family protein. Mol Biochem Parasitol. 2002;120 (2):269-83.
37. Luu VD. The PUF proteins in Trypanosoma brucei; 2006. https://www.researchgate.net/publication/33428575_The_PUF_proteins_in_Trypanosoma_brucei
38. Jha BA, Fadda A, Merce C, Mugo E, Droll D, Clayton C. Depletion of the Trypanosome Pumilio domain protein PUF2 or of some other essential proteins causes transcriptome changes related to coding region length. Eukaryot Cell. 2014;13 (5):664-74.
39. Marucha KK, Clayton C. Roles of the Pumilio domain protein PUF3 in Trypanosoma brucei growth and differentiation. Parasitology. 2020;147 (11):1171-83.
40. Jha BA, Archer SK, Clayton CE. The Trypanosome Pumilio domain protein PUF5. PLoS One. 2013;8 (10):e77371.
41. Droll D, Archer S, Fenn K, Delhi P, Matthews K, Clayton C. The trypanosome Pumilio-domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation. FEBS Lett. 2010;584 (6):1156-62.
42. Archer SK, Luu VD, de Queiroz RA, Brems S, Clayton C. Trypanosoma brucei PUF9 regulates mRNAs for proteins involved in replicative processes over the cell cycle. PLoS Pathog. 2009;5 (8):e1000565.
43. Schumann Burkard G, Käser S, de Araújo PR, et al. Nucleolar proteins regulate stage‐specific gene expression and ribosomal RNA maturation in Trypanosoma brucei. Mol Microbiol. 2013;88 (4):827-40.
44. Dallagiovanna B, Correa A, Probst CM, et al. Functional genomic characterization of mRNAs associated with TcPUF6, a pumilio-like protein from Trypanosoma cruzi. J Biol Chem. 2008;283 (13):8266-73.
45. Azizi H, Dumas C, Papadopoulou B. The Pumilio-domain protein PUF6 contributes to SIDER2 retroposon-mediated mRNA decay in Leishmania. RNA. 2017;23 (12):1874-85.
46. Sanchiz Á, Morato E, Rastrojo A, et al. The experimental proteome of Leishmania infantum promastigote and its usefulness for improving gene annotations. Genes (Basel). 2020;11 (9):1036.
47. Sanchiz Á, López-García D, García-García C, Ozaez I, Aguado B, Requena JM. Proteins interacting with Leishmania major PUF1: A proteomic dataset. Data Brief. 2020;33:106594.
48. De Gaudenzi JG, Noé G, Campo VA, Frasch AC, Cassola A. Gene expression regulation in trypanosomatids. Essays Biochem. 2011;51:31-46.
49. Kramer S, Carrington M. Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol. 2011;27 (1):23-30.
50. Araújo PR, Teixeira SM. Regulatory elements involved in the post-transcriptional control of stage-specific gene expression in Trypanosoma cruzi: a review. Mem Inst Oswaldo Cruz. 2011;106 (3):257-66.
51. Ashworth W, Stoney PN, Yamamoto T. States of decay: the systems biology of mRNA stability. Curr Opin Syst Biol. 2019;15:48-57.
52. Glazier VE, Kaur JN, Brown NT, Rivera AA, Panepinto JC. Puf4 regulates both splicing and decay of HXL1 mRNA encoding the unfolded protein response transcription factor in Cryptococcus neoformans. Eukaryot Cell. 2015;14 (4):385-95.
53. Kiani SJ, Taheri T, Nejati A, et al. Repression of the internal ribosome entry site-dependent translation of hepatitis C virus by an engineered PUF protein. Hepat Mon. 2017;17 (2): e45022.
54. Wang C, Yang C, Liu J, Liu Q. NcPuf1 Is a key virulence factor in Neospora caninum. Pathogens. 2020;9 (12):1019.
55. Zhang M, Joyce BR, Sullivan Jr WJ, Nussenzweig V. Translational control in Plasmodium and Toxoplasma parasites. Eukaryot Cell. 2013;12 (2):161-7.
56. Cui L, Fan Q, Li. The malaria parasite Plasmodium falciparum encodes members of the Puf RNA‐binding protein family with conserved RNA binding activity. Nucleic Acids Res. 2002;30 (21):4607-17.
57. Müller K, Matuschewski K, Silvie O. The Puf-family RNA-binding protein Puf2 controls sporozoite conversion to liver stages in the malaria parasite. PLoS One. 2011;6 (5):e19860.
58. Miao J, Li J, Fan Q, et al. The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum. J Cell Sci. 2010;123 (Pt 7):1039-49.
59. Miao J, Fan Q, Parker D, Li X, Li J, Cui L. Puf mediates translation repression of transmission-blocking vaccine candidates in malaria parasites. PLoS Pathog. 2013;9 (4):e1003268.
60. Bunnik EM, Batugedara G, Saraf A, Prudhomme J, Florens L, Le Roch KG. The mRNA-bound proteome of the human malaria parasite Plasmodium falciparum. Genome Biol. 2016;17 (1):147.
61. Vigneron A, O’Neill MB, Weiss BL, et al. Single-cell RNA sequencing of Trypanosoma brucei from tsetse salivary glands unveils metacyclogenesis and identifies potential transmission blocking antigens. Proc Natl Acad Sci U S A. 2020;117 (5):2613-21.
62. Shrestha S, Li X, Ning G, Miao J, Cui L. The RNA-binding protein Puf1 functions in the maintenance of gametocytes in Plasmodium falciparum. J Cell Sci. 2016;129 (16):3144-52.
63. Martínez-Calvillo S, Florencio-Martínez LE, Nepomuceno-Mejía T. Nucleolar structure and function in trypanosomatid protozoa. Cells. 2019;8 (5):421.
64. Falk F, Melo Palhares R, Waithaka A, Clayton C. Roles and interactions of the specialized initiation factors EIF4E2, EIF4E5, and EIF4E6 in Trypanosoma brucei: EIF4E2 maintains the abundances of S‐phase mRNAs. Mol Microbiol. 2022;118 (4):457-76.
65. D'Orso In, Frasch AC. TcUBP-1, a developmentally regulated U-rich RNA-binding protein involved in selective mRNA destabilization in trypanosomes. J Biol Chem. 2001;276 (37):34801-9.
66. Müller M, Padmanabhan PK, Rochette A, et al. Rapid decay of unstable Leishmania mRNAs bearing a conserved retroposon signature 3′-UTR motif is initiated by a site-specific endonucleolytic cleavage without prior deadenylation. Nucleic Acids Res. 2010;38 (17):5867-83.
67. Morelli KH, Smargon AA, Yeo GW. Programmable macromolecule-based RNA-targeting therapies to treat human neurological disorders. RNA. 2023;29 (4):489-97.
68. Gor R, Gharib A, Dharshini Balaji P, et al. Inducing Cytotoxicity in Colon Cancer Cells and Suppressing Cancer Stem Cells by Dolasetron and Ketoprofen through Inhibition of RNA Binding Protein PUM1. Toxics. 2023;11 (8):669.
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2. Day D, Tuite MF. Post-transcriptional gene regulatory mechanisms in eukaryotes: an overview. J Endocrinol. 1998;157 (3):361-71.
3. Matoulkova E, Michalova E, Vojtesek B, Hrstka R. The role of the 3'untranslated region in post-transcriptional regulation of protein expression in mammalian cells. RNA Biol. 2012;9 (5):563-76.
4. Wang M, Ogé L, Perez-Garcia MD, et al. The PUF protein family: overview on PUF RNA targets, biological functions, and post transcriptional regulation. Int J Mol Sci. 2018;19 (2):410.
5. Najdrová V, Stairs CW, Vinopalová M, Voleman L, Doležal PJBb. The evolution of the PUF superfamily of proteins across the tree of eukaryotes. BMC Biol. 2020;18 (1):77.
6. Dallagiovanna B, Pérez L, Sotelo-Silveira J, et al. Trypanosoma cruzi: molecular characterization of TcPUF6, a Pumilio protein. Exp Parasitol. 2005;109 (4):260-4.
7. Jalal Kiani S, Taheri T, Rafati S, Samimi-Rad K. PUF proteins: Cellular functions and potential applications. Curr Protein Pept Sci. 2017;18 (3):250-61.
8. Wang X, Zamore PD, Hall TMT. Crystal structure of a Pumilio homology domain. Mol Cell. 2001;7 (4):855-65.
9. Kiani SJ, Ghalejoogh ZY, Samimi-Rad K. Engineered PUF proteins: new flexible toolkits to target the replication of RNA viruses. Future Virol. 2021;16 (1):5-13.
10. Liu M, Miao J, Liu T, et al. Characterization of TgPuf1, a member of the Puf family RNA-binding proteins from Toxoplasma gondii. Parasit Vectors. 2014;7:141.
11. Folgueira C, Martínez-Bonet M, Requena JMJBrn. The Leishmania infantum PUF proteins are targets of the humoral response during visceral Leishmaniasis. BMC Res Notes. 2010;3:13.
12. Sonoda J, Wharton RPJG. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev. 1999;13 (20):2704-12.
13. Moore FL, Jaruzelska J, Fox MS, et al. Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proc Natl Acad Sci U S A. 2003;100 (2):538-43.
14. Kraemer B, Crittenden S, Gallegos M, et al. NANOS-3 and FBF proteins physically interact to control the sperm–oocyte switch in Caenorhabditis elegans. Curr Biol. 1999;9 (18):1009-18.
15. Weidmann CA, Qiu C, Arvola RM, et al. Drosophila Nanos acts as a molecular clamp that modulates the RNA-binding and repression activities of Pumilio. Elife. 2016;5:e17096.
16. Saljoughian N, Taheri T, Rafati S. Live vaccination tactics: possible approaches for controlling visceral Leishmaniasis. Front Immunol. 2014;5:134.
17. Seyed N, Taheri T, Rafati S. Post-genomics and vaccine improvement for Leishmania. Front Microbiol. 2016;7:467.
18. Taheri T, Seyed N, Mizbani A, Rafati S. Leishmania-based expression systems. Appl Microbiol Biotechnol. 2016;100(17):7377-85.
19. Alcântara LM, Ferreira TC, Gadelha FR, Miguel DC. Challenges in drug discovery targeting TriTryp diseases with an emphasis on Leishmaniasis. Int J Parasitol Drugs Drug Resist. 2018;8 (3):430-9.
20. Caro F, Bercovich N, Atorrasagasti C, Levin MJ, Vázquez MP. Trypanosoma cruzi: analysis of the complete PUF RNA-binding protein family. Exp Parasitol. 2006;113 (2):112-24.
21. Wang X, Voronina EJFic, biology d. Diverse roles of PUF proteins in germline stem and progenitor cell development in C. elegans. Front Cell Dev Biol. 2020;8:29.
22. Lee MH, Schedl T. RNA-binding proteins. WormBook. 2006; 1-13. doi: 10.1895/wormbook.1.79.1.
23. Wickens M, Bernstein DS, Kimble J, Parker R. A PUF family portrait: 3′ UTR regulation as a way of life. Trends Genet. 2002;18 (3):150-7.
24. Xu Z, Zhao J, Hong M, Zeng C, Guang S, Shi Y. Structural recognition of the mRNA 3′ UTR by PUF-8 restricts the lifespan of C. elegans. Nucleic Acids Res. 2021;49 (17):10082-97.
25. Zhang C, Muench DGJJoBC. A nucleolar PUF RNA-binding protein with specificity for a unique RNA sequence. J Biol Chem. 2015;290 (50):30108-18.
26. García-Rodríguez LJ, Gay AC, Pon LAJTJocb. Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast. J Cell Biol. 2007;176 (2):197-207.
27. Haramati O, Brodov A, Yelin I, et al. Identification and characterization of roles for Puf1 and Puf2 proteins in the yeast response to high calcium. Sci Rep. 2017;7 (1):3037.
28. Hsiao WY, Wang YT, Wang SW. Fission yeast Puf2, a Pumilio and FBF family RNA-binding protein, links stress granules to processing bodies. Mol Cell Biol. 2020;40 (9):e00589-19.
29. Gerber AP, Herschlag D, Brown PO, Eddy SJPb. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2004;2 (3):E79.
30. Saint-Georges Y, Garcia M, Delaveau T, et al. Yeast mitochondrial biogenesis: a role for the PUF RNA-binding protein Puf3p in mRNA localization. PLoS One. 2008;3 (6):e2293.
31. Zipor G, Haim-Vilmovsky L, Gelin-Licht R, et al. Localization of mRNAs coding for peroxisomal proteins in the yeast, Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2009;106 (47):19848-53.
32. Gu W, Deng Y, Zenklusen D, Singer RH. A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev. 2004;18 (12):1452-65.
33. Uyhazi KE, Yang Y, Liu N, et al. Pumilio proteins utilize distinct regulatory mechanisms to achieve complementary functions required for pluripotency and embryogenesis. Proc Natl Acad Sci U S A. 2020;117 (14):7851-62.
34. Liang X, Hart KJ, Dong G, et al. Puf3 participates in ribosomal biogenesis in malaria parasites. J Cell Sci. 2018;131 (6):jcs212597.
35. Zhang M, Mishra S, Sakthivel R, Fontoura BM, Nussenzweig. UIS2: a unique phosphatase required for the development of Plasmodium liver stages. PLoS Pathog. 2016;12 (1):e1005370.
36. Hoek M, Zanders T, Cross GA. Trypanosoma brucei expression-site-associated-gene-8 protein interacts with a Pumilio family protein. Mol Biochem Parasitol. 2002;120 (2):269-83.
37. Luu VD. The PUF proteins in Trypanosoma brucei; 2006. https://www.researchgate.net/publication/33428575_The_PUF_proteins_in_Trypanosoma_brucei
38. Jha BA, Fadda A, Merce C, Mugo E, Droll D, Clayton C. Depletion of the Trypanosome Pumilio domain protein PUF2 or of some other essential proteins causes transcriptome changes related to coding region length. Eukaryot Cell. 2014;13 (5):664-74.
39. Marucha KK, Clayton C. Roles of the Pumilio domain protein PUF3 in Trypanosoma brucei growth and differentiation. Parasitology. 2020;147 (11):1171-83.
40. Jha BA, Archer SK, Clayton CE. The Trypanosome Pumilio domain protein PUF5. PLoS One. 2013;8 (10):e77371.
41. Droll D, Archer S, Fenn K, Delhi P, Matthews K, Clayton C. The trypanosome Pumilio-domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation. FEBS Lett. 2010;584 (6):1156-62.
42. Archer SK, Luu VD, de Queiroz RA, Brems S, Clayton C. Trypanosoma brucei PUF9 regulates mRNAs for proteins involved in replicative processes over the cell cycle. PLoS Pathog. 2009;5 (8):e1000565.
43. Schumann Burkard G, Käser S, de Araújo PR, et al. Nucleolar proteins regulate stage‐specific gene expression and ribosomal RNA maturation in Trypanosoma brucei. Mol Microbiol. 2013;88 (4):827-40.
44. Dallagiovanna B, Correa A, Probst CM, et al. Functional genomic characterization of mRNAs associated with TcPUF6, a pumilio-like protein from Trypanosoma cruzi. J Biol Chem. 2008;283 (13):8266-73.
45. Azizi H, Dumas C, Papadopoulou B. The Pumilio-domain protein PUF6 contributes to SIDER2 retroposon-mediated mRNA decay in Leishmania. RNA. 2017;23 (12):1874-85.
46. Sanchiz Á, Morato E, Rastrojo A, et al. The experimental proteome of Leishmania infantum promastigote and its usefulness for improving gene annotations. Genes (Basel). 2020;11 (9):1036.
47. Sanchiz Á, López-García D, García-García C, Ozaez I, Aguado B, Requena JM. Proteins interacting with Leishmania major PUF1: A proteomic dataset. Data Brief. 2020;33:106594.
48. De Gaudenzi JG, Noé G, Campo VA, Frasch AC, Cassola A. Gene expression regulation in trypanosomatids. Essays Biochem. 2011;51:31-46.
49. Kramer S, Carrington M. Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol. 2011;27 (1):23-30.
50. Araújo PR, Teixeira SM. Regulatory elements involved in the post-transcriptional control of stage-specific gene expression in Trypanosoma cruzi: a review. Mem Inst Oswaldo Cruz. 2011;106 (3):257-66.
51. Ashworth W, Stoney PN, Yamamoto T. States of decay: the systems biology of mRNA stability. Curr Opin Syst Biol. 2019;15:48-57.
52. Glazier VE, Kaur JN, Brown NT, Rivera AA, Panepinto JC. Puf4 regulates both splicing and decay of HXL1 mRNA encoding the unfolded protein response transcription factor in Cryptococcus neoformans. Eukaryot Cell. 2015;14 (4):385-95.
53. Kiani SJ, Taheri T, Nejati A, et al. Repression of the internal ribosome entry site-dependent translation of hepatitis C virus by an engineered PUF protein. Hepat Mon. 2017;17 (2): e45022.
54. Wang C, Yang C, Liu J, Liu Q. NcPuf1 Is a key virulence factor in Neospora caninum. Pathogens. 2020;9 (12):1019.
55. Zhang M, Joyce BR, Sullivan Jr WJ, Nussenzweig V. Translational control in Plasmodium and Toxoplasma parasites. Eukaryot Cell. 2013;12 (2):161-7.
56. Cui L, Fan Q, Li. The malaria parasite Plasmodium falciparum encodes members of the Puf RNA‐binding protein family with conserved RNA binding activity. Nucleic Acids Res. 2002;30 (21):4607-17.
57. Müller K, Matuschewski K, Silvie O. The Puf-family RNA-binding protein Puf2 controls sporozoite conversion to liver stages in the malaria parasite. PLoS One. 2011;6 (5):e19860.
58. Miao J, Li J, Fan Q, et al. The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum. J Cell Sci. 2010;123 (Pt 7):1039-49.
59. Miao J, Fan Q, Parker D, Li X, Li J, Cui L. Puf mediates translation repression of transmission-blocking vaccine candidates in malaria parasites. PLoS Pathog. 2013;9 (4):e1003268.
60. Bunnik EM, Batugedara G, Saraf A, Prudhomme J, Florens L, Le Roch KG. The mRNA-bound proteome of the human malaria parasite Plasmodium falciparum. Genome Biol. 2016;17 (1):147.
61. Vigneron A, O’Neill MB, Weiss BL, et al. Single-cell RNA sequencing of Trypanosoma brucei from tsetse salivary glands unveils metacyclogenesis and identifies potential transmission blocking antigens. Proc Natl Acad Sci U S A. 2020;117 (5):2613-21.
62. Shrestha S, Li X, Ning G, Miao J, Cui L. The RNA-binding protein Puf1 functions in the maintenance of gametocytes in Plasmodium falciparum. J Cell Sci. 2016;129 (16):3144-52.
63. Martínez-Calvillo S, Florencio-Martínez LE, Nepomuceno-Mejía T. Nucleolar structure and function in trypanosomatid protozoa. Cells. 2019;8 (5):421.
64. Falk F, Melo Palhares R, Waithaka A, Clayton C. Roles and interactions of the specialized initiation factors EIF4E2, EIF4E5, and EIF4E6 in Trypanosoma brucei: EIF4E2 maintains the abundances of S‐phase mRNAs. Mol Microbiol. 2022;118 (4):457-76.
65. D'Orso In, Frasch AC. TcUBP-1, a developmentally regulated U-rich RNA-binding protein involved in selective mRNA destabilization in trypanosomes. J Biol Chem. 2001;276 (37):34801-9.
66. Müller M, Padmanabhan PK, Rochette A, et al. Rapid decay of unstable Leishmania mRNAs bearing a conserved retroposon signature 3′-UTR motif is initiated by a site-specific endonucleolytic cleavage without prior deadenylation. Nucleic Acids Res. 2010;38 (17):5867-83.
67. Morelli KH, Smargon AA, Yeo GW. Programmable macromolecule-based RNA-targeting therapies to treat human neurological disorders. RNA. 2023;29 (4):489-97.
68. Gor R, Gharib A, Dharshini Balaji P, et al. Inducing Cytotoxicity in Colon Cancer Cells and Suppressing Cancer Stem Cells by Dolasetron and Ketoprofen through Inhibition of RNA Binding Protein PUM1. Toxics. 2023;11 (8):669.
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| Files | ||
| Issue | Vol 19 No 3 (2024) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i3.16386 | |
| Keywords | ||
| RNA-binding pro-teins PUF proteins Trypanosome brucei Trypanosome cruzi Leishmania | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Taheri T, Davarpanah E, Samimi-Rad K, Seyed N. PUF Proteins as Critical RNA-Binding Proteins in TriTryp Parasites: A Review Article. Iran J Parasitol. 2024;19(3):278-289.
