Translational control in Plasmodium and Toxoplasma parasites

Eukaryotic Cell

Volumn 12, Issue 2, 2013, Pages 161-167

  Zhang, Min ^a   Joyce, Bradley R ^b   Sullivan, William J ^b   Nussenzweig, Victor ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873179181     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00296-12     Document Type: Review

References (72)

1. Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD. 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379:413-431.
2. Hakimi MA, Deitsch KW. 2007. Epigenetics in Apicomplexa: control of gene expression during cell cycle progression, differentiation and antigenic variation. Curr. Opin. Microbiol. 10:357-362.
3. Mair GR, Braks JA, Garver LS, Wiegant JC, Hall N, Dirks RW, Khan SM, Dimopoulos G, Janse CJ, Waters AP. 2006. Regulation of sexual development of Plasmodium by translational repression. Science 313: 667-669.
4. Painter HJ, Campbell TL, Llinas M. 2011. The Apicomplexan AP2 family: integral factors regulating Plasmodium development. Mol. Biochem. Parasitol. 176:1-7.
5. Sullivan WJ, Jr, Jeffers V. 2012. Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol. Rev. 36:717-733.
6. Montoya JG, Liesenfeld O. 2004. Toxoplasmosis. Lancet 363:1965-1976.
7. Van Der Kelen K, Beyaert R, Inze D, De Veylder L. 2009. Translational control of eukaryotic gene expression. Crit. Rev. Biochem. Mol. Biol. 44: 143-168.
8. Mueller PP, Hinnebusch AG. 1986. Multiple upstream AUG codons mediate translational control of GCN4. Cell 45:201-207.
9. Vattem KM, Wek RC. 2004. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 101:11269-11274.
10. Wek RC, Jiang HY, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34:7-11.
11. Anderson P, Kedersha N. 2009. Stress granules. Curr. Biol. 19:R397-R398.
12. Balagopal V, Parker R. 2009. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol. 21:403-408.
13. Kedersha N, Anderson P. 2007. Mammalian stress granules and processing bodies. Methods Enzymol. 431:61-81.
14. Jackson KE, Habib S, Frugier M, Hoen R, Khan S, Pham JS, Ribas de Pouplana L, Royo M, Santos MA, Sharma A, Ralph SA. 2011. Protein translation in Plasmodium parasites. Trends Parasitol. 27:467-476.
15. Dahl EL, Rosenthal PJ. 2008. Apicoplast translation, transcription and genome replication: targets for antimalarial antibiotics. Trends. Parasitol. 24:279-284.
16. Fichera ME, Roos DS. 1997. A plastid organelle as a drug target in apicomplexan parasites. Nature 390:407-409.
17. Camps M, Arrizabalaga G, Boothroyd J. 2002. An rRNA mutation identifies the apicoplast as the target for clindamycin in Toxoplasma gondii. Mol. Microbiol. 43:1309-1318.
18. Esseiva AC, Naguleswaran A, Hemphill A, Schneider A. 2004. Mitochondrial tRNA import in Toxoplasma gondii. J. Biol. Chem. 279:42363-42368.
19. Pino P, Aeby E, Foth BJ, Sheiner L, Soldati T, Schneider A, Soldati-Favre D. 2010. Mitochondrial translation in absence of local tRNA aminoacylation and methionyl tRNA Met formylation in Apicomplexa. Mol. Microbiol. 76:706-718.
20. Afonso A, Neto Z, Castro H, Lopes D, Alves AC, Tomás AM, Rosário VD. 2010. Plasmodium chabaudi chabaudi malaria parasites can develop stable resistance to atovaquone with a mutation in the cytochrome b gene. Malar. J. 9:135.
21. Painter HJ, Morrisey JM, Mather MW, Vaidya AB. 2007. Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum. Nature 446:88-91.
22. Waters AP, Syin C, McCutchan TF. 1989. Developmental regulation of stage-specific ribosome populations in Plasmodium. Nature 342:438-440.
23. van Spaendonk RM, Ramesar J, van Wigcheren A, Eling W, Beetsma AL, van Gemert GJ, Hooghof J, Janse CJ, Waters AP. 2001. Functional equivalence of structurally distinct ribosomes in the malaria parasite, Plasmodium berghei. J. Biol. Chem. 276:22638-22647.
24. Paton MG, Barker GC, Matsuoka H, Ramesar J, Janse CJ, Waters AP, Sinden RE. 1993. Structure and expression of a post-transcriptionally regulated malaria gene encoding a surface protein from the sexual stages of Plasmodium berghei. Mol. Biochem. Parasitol. 59:263-275.
25. Thompson J, Sinden RE. 1994. In situ detection of Pbs21 mRNA during sexual development of Plasmodium berghei. Mol. Biochem. Parasitol. 68: 189-196.
26. Vervenne RA, Dirks RW, Ramesar J, Waters AP, Janse CJ. 1994. Differential expression in blood stages of the gene coding for the 21-kilodalton surface protein of ookinetes of Plasmodium berghei as detected by RNA in situ hybridisation. Mol. Biochem. Parasitol. 68:259-266.
27. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, Berriman M, Florens L, Janssen CS, Pain A, Christophides GK, James K, Rutherford K, Harris B, Harris D, Churcher C, Quail MA, Ormond D, Doggett J, Trueman HE, Mendoza J, Bidwell SL, Rajandream MA, Carucci DJ, Yates JR, III, Kafatos FC, Janse CJ, Barrell B, Turner CM, Waters AP, Sinden RE. 2005. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307:82-86.
28. Cui L, Fan Q, Li J. 2002. The malaria parasite Plasmodium falciparum encodes members of the Puf RNA-binding protein family with conserved RNA binding activity. Nucleic Acids Res. 30:4607-4617.
29. Braks JA, Mair GR, Franke-Fayard B, Janse CJ, Waters AP. 2008. A conserved U-rich RNA region implicated in regulation of translation in Plasmodium female gametocytes. Nucleic Acids Res. 36:1176-1186.
30. Mair GR, Lasonder E, Garver LS, Franke-Fayard BM, Carret CK, Wiegant JC, Dirks RW, Dimopoulos G, Janse CJ, Waters AP. 2010. Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog. 6:e1000767. doi:10.1371/journal.ppat.1000767.
31. Matuschewski K, Ross J, Brown SM, Kaiser K, Nussenzweig V, Kappe SH. 2002. Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J. Biol. Chem. 277:41948-41953.
32. Mikolajczak SA, Silva-Rivera H, Peng X, Tarun AS, Camargo N, Jacobs-Lorena V, Daly TM, Bergman LW, de la Vega P, Williams J, Aly AS, Kappe SH. 2008. Distinct malaria parasite sporozoites reveal transcriptional changes that cause differential tissue infection competence in the mosquito vector and mammalian host. Mol. Cell. Biol. 28:6196-6207.
33. Le Roch KG, Johnson JR, Florens L, Zhou Y, Santrosyan A, Grainger M, Yan SF, Williamson KC, Holder AA, Carucci DJ, Yates JR, III, Winzeler EA. 2004. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res. 14:2308-2318.
34. Mueller AK, Camargo N, Kaiser K, Andorfer C, Frevert U, Matuschewski K, Kappe SH. 2005. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc. Natl. Acad. Sci. U. S. A. 102:3022-3027.
35. Mueller AK, Labaied M, Kappe SH, Matuschewski K. 2005. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433:164-167.
36. Sharma A, Yogavel M, Akhouri RR, Gill J. 2008. Crystal structure of soluble domain of malaria sporozoite protein UIS3 in complex with lipid. J. Biol. Chem. 283:24077-24088.
37. Mackellar DC, O'Neill MT, Aly AS, Sacci JB, Jr, Cowman AF, Kappe SH. 2010. Plasmodium falciparum PF10-0164 (ETRAMP10.3) is an essential parasitophorous vacuole and exported protein in blood stages. Eukaryot. Cell 9:784-794.
38. Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, Moch JK, Muster N, Sacci JB, Tabb DL, Witney AA, Wolters D, Wu Y, Gardner MJ, Holder AA, Sinden RE, Yates JR, Carucci DJ. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419:520-526.
39. Lasonder E, Janse CJ, van Gemert GJ, Mair GR, Vermunt AM, Douradinha BG, van Noort V, Huynen MA, Luty AJ, Kroeze H, Khan SM, Sauerwein RW, Waters AP, Mann M, Stunnenberg HG. 2008. Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog. 4:e1000195. doi:10.1371/journal.ppat.1000195.
40. Siau A, Silvie O, Franetich JF, Yalaoui S, Marinach C, Hannoun L, van Gemert GJ, Luty AJ, Bischoff E, David PH, Snounou G, Vaquero C, Froissard P, Mazier D. 2008. Temperature shift and host cell contact up-regulate sporozoite expression of Plasmodium falciparum genes involved in hepatocyte infection. PLoS Pathog. 4:e1000121. doi:10.1371/journal.ppat.1000121.
41. Zhou Y, Ramachandran V, Kumar KA, Westenberger S, Refour P, Zhou B, Li F, Young JA, Chen K, Plouffe D, Henson K, Nussenzweig V, Carlton J, Vinetz JM, Duraisingh MT, Winzeler EA. 2008. Evidencebased annotation of the malaria parasite's genome using comparative expression profiling. PLoS One 3:e1570. doi:10.1371/journal.pone.0001570.
42. Zhang M, Fennell C, Ranford-Cartwright L, Sakthivel R, Gueirard P, Meister S, Caspi A, Doerig C, Nussenzweig RS, Tuteja R, Sullivan WJ, Jr, Roos DS, Fontoura BM, Ménard R, Winzeler EA, Nussenzweig V. 2010. The Plasmodium eukaryotic initiation factor-2+ kinase IK2 controls the latency of sporozoites in the mosquito salivary glands. J. Exp. Med. 207:1465-1474.
43. Ward P, Equinet L, Packer J, Doerig C. 2004. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5:79.
44. Kaiser K, Camargo N, Kappe SH. 2003. Transformation of sporozoites into early exoerythrocytic malaria parasites does not require host cells. J. Exp. Med. 97:1045-1050.
45. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J. 2005. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307:935-939.
46. Gomes-Santos CS, Braks J, Prudêncio M, Carret C, Gomes AR, Pain A, Feltwell T, Khan S, Waters A, Janse C, Mair GR, Mota MM. 2011. Transition of Plasmodium sporozoites into liver stage-like forms is regulated by the RNA binding protein Pumilio. PLoS Pathog. 7:e1002046. doi: 10.1371/journal.ppat.1002046.
47. Müller K, Matuschewski K, Silvie O. 2011. The Puf-family RNA-binding protein Puf2 controls sporozoite conversion to liver stages in the malaria parasite. PLoS One 6:e19860. doi:10.1371/journal.pone.0019860.
48. Cowman AF, Berry D, Baum J. 2012. The cell biology of disease: the cellular and molecular basis for malaria parasite invasion of the human red blood cell. J. Cell Biol. 198:961-971.
49. Esposito A, Tiffert T, Mauritz JM, Schlachter S, Bannister LH, Kaminski CF, Lew VL. 2008. FRET imaging of hemoglobin concentration in Plasmodium falciparum-infected red cells. PLoS One 3:e3780. doi:10.1371/journal.pone.0003780.
50. Fitch CD, Kanjananggulpan P. 1987. The state of ferriprotoporphyrin IX in malaria pigment. J. Biol. Chem. 262:15552-15555.
51. Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK. 2000. The structure of malaria pigment beta-haematin. Nature 404:307-310.
52. Zhang M, Mishra S, Sakthivel R, Rojas M, Ranjan R, Sullivan WJ, Jr, Fontoura BM, Ménard R, Dever TE, Nussenzweig V. 2012. PK4, a eukaryotic initiation factor 2+(eIF2+) kinase, is essential for the development of the erythrocytic cycle of Plasmodium. Proc. Natl. Acad. Sci. U. S. A. 109:3956-3961.
53. Bannister LH, Hopkins JM, Fowler RE, Krishna S, Mitchell GH. 2000. A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol. Today 16:427-433.
54. White JH, Kilbey BJ. 1996. DNA replication in the malaria parasite. Parasitol. Today 12:151-155.
55. Mohrle JJ, Zhao Y, Wernli B, Franklin RM, Kappes B. 1997. Molecular cloning, characterization and localization of PfPK4, an eIF-2+ kinaserelated enzyme from the malarial parasite Plasmodium falciparum. Biochem. J. 328:677-687.
56. Solyakov L, Halbert J, Alam MM, Semblat JP, Dorin-Semblat D, Reininger L, Bottrill AR, Mistry S, Abdi A, Fennell C, Holland Z, Demarta C, Bouza Y, Sicard A, Nivez MP, Eschenlauer S, Lama T, Thomas DC, Sharma P, Agarwal S, Kern S, Pradel G, Graciotti M, Tobin AB, Doerig C. 2011. Global kinomic and phospho-proteomic analyses of the human malaria parasite Plasmodium falciparum. Nat. Commun. 2:565.
57. Wastling JM, Xia D, Sohal A, Chaussepied M, Pain A, Langsley G. 2009. Proteomes and transcriptomes of the Apicomplexa-where's the message? Int. J. Parasitol. 39:135-143.
58. Xia D, Sanderson SJ, Jones AR, Prieto JH, Yates JR, Bromley E, Tomley FM, Lal K, Sinden RE, Brunk BP, Roos DS, Wastling JM. 2008. The proteome of Toxoplasma gondii: integration with the genome provides novel insights into gene expression and annotation. Genome Biol. 9:R116.
59. Gastens MH, Fischer HG. 2002. Toxoplasma gondii eukaryotic translation initiation factor 4A associated with tachyzoite virulence is downregulated in the bradyzoite stage. Int. J. Parasitol. 32:1225-1234.
60. Sullivan WJ, Jr, Narasimhan J, Bhatti MM, Wek RC. 2004. Parasitespecific eukaryotic initiation factor-2 (eIF2) kinase required for stressinduced translation control. Biochem. J. 380:523-531.
61. Joyce BR, Queener SF, Wek RC, Sullivan WJ, Jr. 2010. Phosphorylation of eukaryotic initiation factor-2+ promotes the extracellular survival of obligate intracellular parasite Toxoplasma gondii. Proc. Natl. Acad. Sci. U. S. A. 107:17200-17205.
62. Konrad C, Wek RC, Sullivan WJ, Jr. 2011. A GCN2-like eukaryotic initiation factor-2 kinase increases the viability of extracellular Toxoplasma gondii parasites. Eukaryot. Cell 10:1403-1412.
63. Lirussi D, Matrajt M. 2011. RNA granules present only in extracellular Toxoplasma gondii increase parasite viability. Int. J. Biol. Sci. 7:960-967.
64. Beckers CJ, Roos DS, Donald RG, Luft BJ, Schwab JC, Cao Y, Joiner KA. 1995. Inhibition of cytoplasmic and organellar protein synthesis in Toxoplasma gondii. Implications for the target of macrolide antibiotics. J. Clin. Invest. 95:367-376.
65. Takeuchi T, Fujiwara T, Akao S. 1980. Na+, K-dependent ATPase activity and effect of K-on in vitro protein synthesis andNADpyrophosphorylase in Toxoplasma gondii. J. Parasitol. 66:591-595.
66. Braun L, Cannella D, Ortet P, Barakat M, Sautel CF, Kieffer S, Garin J, Bastien O, Voinnet O, Hakimi MA. 2010. A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog. 6:e1000920. doi:10.1371/journal.ppat.1000920.
67. Narasimhan J, et al. 2008. Translation regulation by eukaryotic initiation factor-2 kinases in the development of latent cysts in Toxoplasma gondii. J. Biol. Chem. 283:16591-16601.
68. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218-223.
69. Porter RJ, Laird RL, Dusseau EM. 1954. Studies on malarial sporozoites. II. Effect of age and dosage of sporozoites on their infectiousness. Exp. Parasitol. 3:267-274.
70. Beier JC, Vanderberg JP. 1998. Sporogonic development in the mosquito, p 49-61. In Sherman IW (ed), Malaria: parasite biology, pathogenesis, and protection. ASM Press, Washington, DC.
71. Markus MB. 2011. The hypnozoite concept, with particular reference to malaria. Parasitol. Res. 108:247-252.
72. Smalley ME, Sinden RE. 1977. Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology 74:1-8.