Protein–RNA interactions important for Plasmodium transmission

English version

Autoři: Kelly T. Rios ^aff001; Scott E. Lindner ^aff001
Působiště autorů: Department of Biochemistry and Molecular Biology, The Huck Center for Malaria Research, Pennsylvania State University, University Park, Pennsylvania, United States of America ^aff001
Vyšlo v časopise: Protein–RNA interactions important for Plasmodium transmission. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008095
Kategorie: Pearls
doi: https://doi.org/10.1371/journal.ppat.1008095

Zdroje

1. Cui L, Lindner S, Miao J. Translational regulation during stage transitions in malaria parasites. Ann N Y Acad Sci. 2015;1342 : 1–9. Epub 2014/11/13. doi: 10.1111/nyas.12573 25387887; PubMed Central PMCID: PMC4405408.

2. Hausser J, Mayo A, Keren L, Alon U. Central dogma rates and the trade-off between precision and economy in gene expression. Nat Commun. 2019;10(1):68. Epub 2019/01/10. doi: 10.1038/s41467-018-07391-8 30622246; PubMed Central PMCID: PMC6325141.

3. Holmes MJ, Augusto LDS, Zhang M, Wek RC, Sullivan WJ Jr. Translational Control in the Latency of Apicomplexan Parasites. Trends Parasitol. 2017;33(12):947–60. Epub 2017/09/25. doi: 10.1016/j.pt.2017.08.006 28942109; PubMed Central PMCID: PMC5705472.

4. Cherry AA, Ananvoranich S. Characterization of a homolog of DEAD-box RNA helicases in Toxoplasma gondii as a marker of cytoplasmic mRNP stress granules. Gene. 2014;543(1):34–44. Epub 2014/04/09. doi: 10.1016/j.gene.2014.04.011 24709106.

5. Vembar SS, Droll D, Scherf A. Translational regulation in blood stages of the malaria parasite Plasmodium spp.: systems-wide studies pave the way. Wiley Interdiscip Rev RNA. 2016;7(6):772–92. Epub 2016/05/28. doi: 10.1002/wrna.1365 27230797; PubMed Central PMCID: PMC5111744.

6. Vembar SS, Macpherson CR, Sismeiro O, Coppee JY, Scherf A. The PfAlba1 RNA-binding protein is an important regulator of translational timing in Plasmodium falciparum blood stages. Genome Biol. 2015;16 : 212. Epub 2015/09/30. doi: 10.1186/s13059-015-0771-5 26415947; PubMed Central PMCID: PMC4587749.

7. Foth BJ, Zhang N, Mok S, Preiser PR, Bozdech Z. Quantitative protein expression profiling reveals extensive post-transcriptional regulation and post-translational modifications in schizont-stage malaria parasites. Genome Biol. 2008;9(12):R177. Epub 2008/12/19. doi: 10.1186/gb-2008-9-12-r177 19091060; PubMed Central PMCID: PMC2646281.

8. Le Roch KG, Johnson JR, Florens L, Zhou Y, Santrosyan A, Grainger M, et al. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res. 2004;14(11):2308–18. Epub 2004/11/03. doi: 10.1101/gr.2523904 15520293; PubMed Central PMCID: PMC525690.

9. Bunnik EM, Chung DW, Hamilton M, Ponts N, Saraf A, Prudhomme J, et al. Polysome profiling reveals translational control of gene expression in the human malaria parasite Plasmodium falciparum. Genome Biol. 2013;14(11):R128. Epub 2013/11/26. doi: 10.1186/gb-2013-14-11-r128 24267660; PubMed Central PMCID: PMC4053746.

10. Caro F, Ahyong V, Betegon M, DeRisi JL. Genome-wide regulatory dynamics of translation in the Plasmodium falciparum asexual blood stages. Elife. 2014;3. Epub 2014/12/11. doi: 10.7554/eLife.04106 25493618; PubMed Central PMCID: PMC4371882.

11. Chan S, Frasch A, Mandava CS, Ch'ng JH, Quintana MDP, Vesterlund M, et al. Regulation of PfEMP1-VAR2CSA translation by a Plasmodium translation-enhancing factor. Nat Microbiol. 2017;2 : 17068. Epub 2017/05/10. doi: 10.1038/nmicrobiol.2017.68 28481333.

12. Bancells C, Deitsch KW. A molecular switch in the efficiency of translation reinitiation controls expression of var2csa, a gene implicated in pregnancy-associated malaria. Mol Microbiol. 2013;90(3):472–88. Epub 2013/08/29. doi: 10.1111/mmi.12379 23980802; PubMed Central PMCID: PMC3938558.

13. Amulic B, Salanti A, Lavstsen T, Nielsen MA, Deitsch KW. An upstream open reading frame controls translation of var2csa, a gene implicated in placental malaria. PLoS Pathog. 2009;5(1):e1000256. Epub 2009/01/03. doi: 10.1371/journal.ppat.1000256 19119419; PubMed Central PMCID: PMC2603286.

14. Mok BW, Ribacke U, Rasti N, Kironde F, Chen Q, Nilsson P, et al. Default Pathway of var2csa switching and translational repression in Plasmodium falciparum. PLoS ONE. 2008;3(4):e1982. Epub 2008/04/24. doi: 10.1371/journal.pone.0001982 18431472; PubMed Central PMCID: PMC2292259.

15. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell. 2009;136(4):731–45. Epub 2009/02/26. doi: 10.1016/j.cell.2009.01.042 19239892; PubMed Central PMCID: PMC3610329.

16. Turque O, Tsao T, Li T, Zhang M. Translational Repression in Malaria Sporozoites. Microb Cell. 2016;3(5):227–9. Epub 2017/03/31. doi: 10.15698/mic2016.05.502 28357358; PubMed Central PMCID: PMC5349151.

17. Zhang M, Fennell C, Ranford-Cartwright L, Sakthivel R, Gueirard P, Meister S, et al. The Plasmodium eukaryotic initiation factor-2alpha kinase IK2 controls the latency of sporozoites in the mosquito salivary glands. J Exp Med. 2010;207(7):1465–74. Epub 2010/06/30. doi: 10.1084/jem.20091975 20584882; PubMed Central PMCID: PMC2901070.

18. 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. Epub 2016/07/07. doi: 10.1186/s13059-016-1014-0 27381095; PubMed Central PMCID: PMC4933991.

19. Reddy BP, Shrestha S, Hart KJ, Liang X, Kemirembe K, Cui L, et al. A bioinformatic survey of RNA-binding proteins in Plasmodium. BMC Genomics. 2015;16 : 890. Epub 2015/11/04. doi: 10.1186/s12864-015-2092-1 26525978; PubMed Central PMCID: PMC4630921.

20. del Carmen Rodriguez M, Gerold P, Dessens J, Kurtenbach K, Schwartz RT, Sinden RE, et al. Characterisation and expression of pbs25, a sexual and sporogonic stage specific protein of Plasmodium berghei. Mol Biochem Parasitol. 2000;110(1):147–59. Epub 2000/09/16. doi: 10.1016/s0166-6851(00)00265-6 10989152.

21. Paton MG, Barker GC, Matsuoka H, Ramesar J, Janse CJ, Waters AP, et al. Structure and expression of a post-transcriptionally regulated malaria gene encoding a surface protein from the sexual stages of Plasmodium berghei. Mol Biochem Parasitol. 1993;59(2):263–75. Epub 1993/06/01. doi: 10.1016/0166-6851(93)90224-l 8341324.

22. Mair GR, Braks JA, Garver LS, Wiegant JC, Hall N, Dirks RW, et al. Regulation of sexual development of Plasmodium by translational repression. Science. 2006;313(5787):667–9. Epub 2006/08/05. doi: 10.1126/science.1125129 16888139; PubMed Central PMCID: PMC1609190.

23. Lasonder E, Rijpma SR, van Schaijk BC, Hoeijmakers WA, Kensche PR, Gresnigt MS, et al. Integrated transcriptomic and proteomic analyses of P. falciparum gametocytes: molecular insight into sex-specific processes and translational repression. Nucleic Acids Res. 2016;44(13):6087–101. Epub 2016/06/15. doi: 10.1093/nar/gkw536 27298255; PubMed Central PMCID: PMC5291273.

24. Lindner SE, Swearingen KE, Shears MJ, Walker MP, Vrana EN, Hart KJ, et al. Transcriptomics and proteomics reveal two waves of translational repression during maturation of malaria parasite sporozoites. Nat Commun. 2019;10(1):4964. doi: 10.1038/s41467-019-12936-6 31673027

25. Swearingen KE, Lindner SE, Flannery EL, Vaughan AM, Morrison RD, Patrapuvich R, et al. Proteogenomic analysis of the total and surface-exposed proteomes of Plasmodium vivax salivary gland sporozoites. PLoS Negl Trop Dis. 2017;11(7):e0005791. Epub 2017/08/02. doi: 10.1371/journal.pntd.0005791 28759593; PubMed Central PMCID: PMC5552340.

26. Vivax Sporozoite C. Transcriptome and histone epigenome of Plasmodium vivax salivary-gland sporozoites point to tight regulatory control and mechanisms for liver-stage differentiation in relapsing malaria. Int J Parasitol. 2019;49(7):501–13. Epub 2019/05/10. doi: 10.1016/j.ijpara.2019.02.007 31071319.

27. Lindner SE, Mikolajczak SA, Vaughan AM, Moon W, Joyce BR, Sullivan WJ Jr., et al. Perturbations of Plasmodium Puf2 expression and RNA-seq of Puf2-deficient sporozoites reveal a critical role in maintaining RNA homeostasis and parasite transmissibility. Cell Microbiol. 2013;15(7):1266–83. Epub 2013/01/30. doi: 10.1111/cmi.12116 23356439; PubMed Central PMCID: PMC3815636.

28. Aly AS, Lindner SE, MacKellar DC, Peng X, Kappe SH. SAP1 is a critical post-transcriptional regulator of infectivity in malaria parasite sporozoite stages. Mol Microbiol. 2011;79(4):929–39. Epub 2011/02/09. doi: 10.1111/j.1365-2958.2010.07497.x 21299648.

29. Silvie O, Goetz K, Matuschewski K. A sporozoite asparagine-rich protein controls initiation of Plasmodium liver stage development. PLoS Pathog. 2008;4(6):e1000086. Epub 2008/06/14. doi: 10.1371/journal.ppat.1000086 18551171; PubMed Central PMCID: PMC2398788.

30. Aly AS, Mikolajczak SA, Rivera HS, Camargo N, Jacobs-Lorena V, Labaied M, et al. Targeted deletion of SAP1 abolishes the expression of infectivity factors necessary for successful malaria parasite liver infection. Mol Microbiol. 2008;69(1):152–63. Epub 2008/05/10. doi: 10.1111/j.1365-2958.2008.06271.x 18466298; PubMed Central PMCID: PMC2615191.

31. Tarun AS, Dumpit RF, Camargo N, Labaied M, Liu P, Takagi A, et al. Protracted sterile protection with Plasmodium yoelii pre-erythrocytic genetically attenuated parasite malaria vaccines is independent of significant liver-stage persistence and is mediated by CD8+ T cells. J Infect Dis. 2007;196(4):608–16. Epub 2007/07/13. doi: 10.1086/519742 17624848.

32. Mueller AK, Labaied M, Kappe SH, Matuschewski K. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature. 2005;433(7022):164–7. Epub 2004/12/08. doi: 10.1038/nature03188 15580261.

33. Muller 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. Epub 2011/06/16. doi: 10.1371/journal.pone.0019860 21673790; PubMed Central PMCID: PMC3097211.

34. Yanagi K, Ohyama K, Yamakawa T, Watanabe H, Hirakawa S, Ohkuma S. [Separation of Thomsen-Friedenreich (T) antigen and N antigen precursor glycoproteins from perchloric acid-soluble fraction of cyst fluid of human ovarian clear cell carcinoma and their some chemical and serological properties]. Yakugaku Zasshi. 1990;110(4):273–9. Epub 1990/04/01. doi: 10.1248/yakushi1947.110.4_273 2165527.

35. Silva PA, Guerreiro A, Santos JM, Braks JA, Janse CJ, Mair GR. Translational Control of UIS4 Protein of the Host-Parasite Interface Is Mediated by the RNA Binding Protein Puf2 in Plasmodium berghei Sporozoites. PLoS ONE. 2016;11(1):e0147940. Epub 2016/01/26. doi: 10.1371/journal.pone.0147940 26808677; PubMed Central PMCID: PMC4726560.

36. Silvie O, Briquet S, Muller K, Manzoni G, Matuschewski K. Post-transcriptional silencing of UIS4 in Plasmodium berghei sporozoites is important for host switch. Mol Microbiol. 2014;91(6):1200–13. Epub 2014/01/23. doi: 10.1111/mmi.12528 24446886.

37. Zhang M, Mishra S, Sakthivel R, Fontoura BM, Nussenzweig V. UIS2: A Unique Phosphatase Required for the Development of Plasmodium Liver Stages. PLoS Pathog. 2016;12(1):e1005370. Epub 2016/01/07. doi: 10.1371/journal.ppat.1005370 26735921; PubMed Central PMCID: PMC4712141.

38. Billker O, Lindo V, Panico M, Etienne AE, Paxton T, Dell A, et al. Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito. Nature. 1998;392(6673):289–92. Epub 1998/04/01. doi: 10.1038/32667 9521324.

39. Brochet M, Billker O. Calcium signalling in malaria parasites. Mol Microbiol. 2016;100(3):397–408. Epub 2016/01/11. doi: 10.1111/mmi.13324 26748879.

40. Sebastian S, Brochet M, Collins MO, Schwach F, Jones ML, Goulding D, et al. A Plasmodium calcium-dependent protein kinase controls zygote development and transmission by translationally activating repressed mRNAs. Cell Host Microbe. 2012;12(1):9–19. Epub 2012/07/24. doi: 10.1016/j.chom.2012.05.014 22817984; PubMed Central PMCID: PMC3414820.

41. Mair GR, Lasonder E, Garver LS, Franke-Fayard BM, Carret CK, Wiegant JC, et al. Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog. 2010;6(2):e1000767. Epub 2010/02/20. doi: 10.1371/journal.ppat.1000767 20169188; PubMed Central PMCID: PMC2820534.

42. Guerreiro A, Deligianni E, Santos JM, Silva PA, Louis C, Pain A, et al. Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte. Genome Biol. 2014;15(11):493. Epub 2014/11/25. doi: 10.1186/s13059-014-0493-0 25418785; PubMed Central PMCID: PMC4234863.

43. Yuda M, Iwanaga S, Shigenobu S, Mair GR, Janse CJ, Waters AP, et al. Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol Microbiol. 2009;71(6):1402–14. Epub 2009/02/18. doi: 10.1111/j.1365-2958.2009.06609.x 19220746.

44. Tomas AM, Margos G, Dimopoulos G, van Lin LH, de Koning-Ward TF, Sinha R, et al. P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J. 2001;20(15):3975–83. Epub 2001/08/03. doi: 10.1093/emboj/20.15.3975 11483501; PubMed Central PMCID: PMC149139.

45. Santos JM, Egarter S, Zuzarte-Luis V, Kumar H, Moreau CA, Kehrer J, et al. Malaria parasite LIMP protein regulates sporozoite gliding motility and infectivity in mosquito and mammalian hosts. Elife. 2017;6. Epub 2017/05/20. doi: 10.7554/eLife.24109 28525314; PubMed Central PMCID: PMC5438254.

46. Bennink S, von Bohl A, Ngwa CJ, Henschel L, Kuehn A, Pilch N, et al. A seven-helix protein constitutes stress granules crucial for regulating translation during human-to-mosquito transmission of Plasmodium falciparum. PLoS Pathog. 2018;14(8):e1007249. Epub 2018/08/23. doi: 10.1371/journal.ppat.1007249 30133543; PubMed Central PMCID: PMC6122839.

47. Munoz EE, Hart KJ, Walker MP, Kennedy MF, Shipley MM, Lindner SE. ALBA4 modulates its stage-specific interactions and specific mRNA fates during Plasmodium yoelii growth and transmission. Mol Microbiol. 2017;106(2):266–84. Epub 2017/08/09. doi: 10.1111/mmi.13762 28787542; PubMed Central PMCID: PMC5688949.

48. 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. Epub 2016/07/08. doi: 10.1242/jcs.186908 27383769; PubMed Central PMCID: PMC5004898.

49. Miao J, Li J, Fan Q, Li X, Li X, Cui L. 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. Epub 2010/03/04. doi: 10.1242/jcs.059824 20197405; PubMed Central PMCID: PMC2844316.

50. 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. Epub 2013/05/03. doi: 10.1371/journal.ppat.1003268 23637595; PubMed Central PMCID: PMC3630172.

51. Moon SL, Morisaki T, Khong A, Lyon K, Parker R, Stasevich TJ. Multicolour single-molecule tracking of mRNA interactions with RNP granules. Nat Cell Biol. 2019;21(2):162–8. Epub 2019/01/22. doi: 10.1038/s41556-018-0263-4 30664789; PubMed Central PMCID: PMC6375083.