Perturbations of PlasmodiumPuf2 expression and RNA-seq of Puf2-deficient sporozoites reveal a critical role in maintaining RNA homeostasis and parasite transmissibility

Cellular Microbiology

Volumn 15, Issue 7, 2013, Pages 1266-1283

  Lindner, Scott E ^a   Mikolajczak, Sebastian A ^a   Vaughan, Ashley M ^a   Moon, Wonjong ^a   Joyce, Brad R ^c   Sullivan, William J ^c   Kappe, Stefan H I ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; EPITOPE; PROTEIN; PROTEIN PUF2; RNA; UNCLASSIFIED DRUG; PROTOZOAL PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL DEDIFFERENTIATION; CELL GRANULE; CELL INVASION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; EXON; FEMALE; GENE STRUCTURE; GENOTYPE; HOMEOSTASIS; IN VITRO STUDY; LIVER CELL; MALE; MOLECULAR RECOGNITION; MOSQUITO; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; OOCYST; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; PHENOTYPE; PLASMODIUM; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM BERGHEI; PLASMODIUM YOELII; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA BINDING; RNA DEGRADATION; RNA METABOLISM; SALIVARY GLAND; SPOROZOITE; STOP CODON; TOXOPLASMA GONDII; TROPHOZOITE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOGENICITY; RNA STABILITY;

MAMMALIA; PLASMODIUM YOELII;

ANIMALS; CULICIDAE; GENE EXPRESSION REGULATION; HOMEOSTASIS; MICE; PLASMODIUM YOELII; PROTOZOAN PROTEINS; RNA; RNA STABILITY; SPOROZOITES;

EID: 84879220995     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12116     Document Type: Article

References (59)

1. Aly, A.S., Vaughan, A.M., and Kappe, S.H. (2009) Malaria parasite development in the mosquito and infection of the mammalian host. Annu Rev Microbiol 63: 195-221.
2. Aly, A.S., Lindner, S.E., MacKellar, D.C., Peng, X., and Kappe, S.H. (2011) SAP1 is a critical post-transcriptional regulator of infectivity in malaria parasite sporozoite stages. Mol Microbiol 79: 929-939.
3. Anderson, P., and Kedersha, N. (2008) Stress granules: the Tao of RNA triage. Trends Biochem Sci 33: 141-150.
4. Balagopal, V., and Parker, R. (2009) Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 21: 403-408.
5. Campbell, Z.T., Menichelli, E., Friend, K., Wu, J., Kimble, J., Williamson, J.R., and Wickens, M. (2012) A conserved interface between PUF and CPEB proteins. J Biol Chem 287: 18854-18862.
6. Carlton, J.M., Angiuoli, S.V., Suh, B.B., Kooij, T.W., Pertea, M., Silva, J.C., etal. (2002) Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419: 512-519.
7. Drinkwater and Denniston (2011) Statistical Problems in genetics and molecular biology. CreateSpace 1: 1-299.
8. Fan, Q., Li, J., Kariuki, M., and Cui, L. (2004) Characterization of PfPuf2, member of the Puf family RNA-binding proteins from the malaria parasite Plasmodium falciparum. DNA Cell Biol 23: 753-760.
9. Florens, L., Washburn, M.P., Raine, J.D., Anthony, R.M., Grainger, M., Haynes, J.D., etal. (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520-526.
10. Gantt, S.M., Myung, J.M., Briones, M.R., Li, W.D., Corey, E.J., Omura, S., etal. (1998) Proteasome inhibitors block development of Plasmodium spp. Antimicrob Agents Chemother 42: 2731-2738.
11. Goldstrohm, A.C., Hook, B.A., Seay, D.J., and Wickens, M. (2006) PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 13: 533-539.
12. Gomes-Santos, C.S., Braks, J., Prudencio, M., Carret, C., Gomes, A.R., Pain, A., etal. (2011) Transition of Plasmodium sporozoites into liver stage-like forms is regulated by the RNA binding protein Pumilio. PLoS Pathog 7: e1002046.
13. Guttery, D.S., Ferguson, D.J., Poulin, B., Xu, Z., Straschil, U., Klop, O., etal. (2012) A putative homologue of CDC20/CDH1 in the malaria parasite is essential for male gamete development. PLoS Pathog 8: e1002554.
14. Hall, N., Karras, M., Raine, J.D., Carlton, J.M., Kooij, T.W., Berriman, M., etal. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307: 82-86.
15. Jayabalasingham, B., Bano, N., and Coppens, I. (2010) Metamorphosis of the malaria parasite in the liver is associated with organelle clearance. Cell Res 20: 1043-1059.
16. Jones, C.I., Zabolotskaya, M.V., and Newbury, S.F. (2012) The 5′ --> 3′ exoribonuclease XRN1/Pacman and its functions in cellular processes and development. Wiley Interdiscip Rev RNA 3: 455-468.
17. Jongco, A.M., Ting, L.M., Thathy, V., Mota, M.M., and Kim, K. (2006) Improved transfection and new selectable markers for the rodent malaria parasite Plasmodium yoelii. Mol Biochem Parasitol 146: 242-250.
18. Kaiser, K., Camargo, N., and Kappe, S.H. (2003) Transformation of sporozoites into early exoerythrocytic malaria parasites does not require host cells. J Exp Med 197: 1045-1050.
19. Kappe, S.H., Vaughan, A.M., Boddey, J.A., and Cowman, A.F. (2010) That was then but this is now: malaria research in the time of an eradication agenda. Science 328: 862-866.
20. Labaied, M., Harupa, A., Dumpit, R.F., Coppens, I., Mikolajczak, S.A., and Kappe, S.H. (2007) Plasmodium yoelii sporozoites with simultaneous deletion of P52 and P36 are completely attenuated and confer sterile immunity against infection. Infect Immun 75: 3758-3768.
21. Lasonder, E., Janse, C.J., van Gemert, G.J., Mair, G.R., Vermunt, A.M., Douradinha, B.G., etal. (2008) Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog 4: e1000195.
22. Le Roch, K.G., Johnson, J.R., Florens, L., Zhou, Y., Santrosyan, A., Grainger, M., etal. (2004) Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res 14: 2308-2318.
23. Lindner, S.E., De Silva, E.K., Keck, J.L., and Llinas, M. (2010) Structural determinants of DNA binding by a P.falciparum ApiAP2 transcriptional regulator. J Mol Biol 395: 558-567.
24. Lindner, S.E., Llinas, M., Keck, J.L., and Kappe, S.H. (2011) The primase domain of PfPrex is a proteolytically matured, essential enzyme of the apicoplast. Mol Biochem Parasitol 180: 69-75.
25. Lindner, S.E., Miller, J.L., and Kappe, S.H. (2012) Malaria parasite pre-erythrocytic infection: preparation meets opportunity. Cell Microbiol 14: 316-324.
26. Mack, S.R., Vanderberg, J.P., and Nawrot, R. (1978) Column separation of Plasmodium berghei sporozoites. J Parasitol 64: 166-168.
27. Mair, G.R., Braks, J.A., Garver, L.S., Wiegant, J.C., Hall, N., Dirks, R.W., etal. (2006) Regulation of sexual development of Plasmodium by translational repression. Science 313: 667-669.
28. Mair, G.R., Lasonder, E., Garver, L.S., Franke-Fayard, B.M., Carret, C.K., Wiegant, J.C., etal. (2010) Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog 6: e1000767.
29. Matuschewski, K., Ross, J., Brown, S.M., Kaiser, K., Nussenzweig, V., and Kappe, S.H. (2002) Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J Biol Chem 277: 41948-41953.
30. Miao, J., Li, J., Fan, Q., Li, X., and Cui, L. (2010) The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum. J Cell Sci 123: 1039-1049.
31. Mikolajczak, S.A., Silva-Rivera, H., Peng, X., Tarun, A.S., Camargo, N., Jacobs-Lorena, V., etal. (2008a) 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.
32. Mikolajczak, S.A., Aly, A.S., Dumpit, R.F., Vaughan, A.M., and Kappe, S.H. (2008b) An efficient strategy for gene targeting and phenotypic assessment in the Plasmodium yoelii rodent malaria model. Mol Biochem Parasitol 158: 213-216.
33. Miller, J.L., Harupa, A., Kappe, S.H., and Mikolajczak, S.A. (2012) Plasmodium yoelii macrophage migration inhibitory factor is necessary for efficient liver-stage development. Infect Immun 80: 1399-1407.
34. Miller, M.A., and Olivas, W.M. (2011) Roles of Puf proteins in mRNA degradation and translation. Wiley Interdiscip Rev RNA 2: 471-492.
35. Mueller, A.K., Camargo, N., Kaiser, K., Andorfer, C., Frevert, U., Matuschewski, K., and Kappe, S.H. (2005a) Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 102: 3022-3027.
36. Mueller, A.K., Labaied, M., Kappe, S.H., and Matuschewski, K. (2005b) Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433: 164-167.
37. Muller, K., Matuschewski, K., and Silvie, O. (2011) The Puf-family RNA-binding protein Puf2 controls sporozoite conversion to liver stages in the malaria parasite. PloS ONE 6: e19860.
38. Narasimhan, J., Joyce, B.R., Naguleswaran, A., Smith, A.T., Livingston, M.R., Dixon, S.E., etal. (2008) Translation regulation by eukaryotic initiation factor-2 kinases in the development of latent cysts in Toxoplasma gondii. J Biol Chem 283: 16591-16601.
39. Natarajan, R., Thathy, V., Mota, M.M., Hafalla, J.C., Menard, R., and Vernick, K.D. (2001) Fluorescent Plasmodium berghei sporozoites and pre-erythrocytic stages: a new tool to study mosquito and mammalian host interactions with malaria parasites. Cell Microbiol 3: 371-379.
40. Painter, H.J., Campbell, T.L., and Llinas, M. (2011) The Apicomplexan AP2 family: integral factors regulating Plasmodium development. Mol Biochem Parasitol 176: 1-7.
41. Paton, M.G., Barker, G.C., Matsuoka, H., Ramesar, J., Janse, C.J., Waters, A.P., and Sinden, R.E. (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.
42. Porter, R.J., Laird, R.L., and Dusseau, E.M. (1954) Studies on malarial sporozoites. II. Effect of age and dosage of sporozoites on their infectiousness. Exp Parasitol 3: 267-274.
43. Qiu, C., Kershner, A., Wang, Y., Holley, C.P., Wilinski, D., Keles, S., etal. (2012) Divergence of Pumilio/fem-3 mRNA binding factor (PUF) protein specificity through variations in an RNA-binding pocket. J Biol Chem 287: 6949-6957.
44. Quenault, T., Lithgow, T., and Traven, A. (2011) PUF proteins: repression, activation and mRNA localization. Trends Cell Biol 21: 104-112.
45. Sullivan, W.J., Jr, Narasimhan, J., Bhatti, M.M., and Wek, R.C. (2004) Parasite-specific eIF2 (eukaryotic initiation factor-2) kinase required for stress-induced translation control. Biochem J 380: 523-531.
46. Trapnell, C., Pachter, L., and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
47. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., etal. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
48. VanBuskirk, K.M., O'Neill, M.T., De La Vega, P., Maier, A.G., Krzych, U., Williams, J., etal. (2009) Preerythrocytic, live-attenuated Plasmodium falciparum vaccine candidates by design. Proc Natl Acad Sci USA 106: 13004-13009.
49. Vanderberg, J.P. (1975) Development of infectivity by the Plasmodium berghei sporozoite. J Parasitol 61: 43-50.
50. Vaughan, A., Chiu, S.Y., Ramasamy, G., Li, L., Gardner, M.J., Tarun, A.S., etal. (2008) Assessment and improvement of the Plasmodium yoelii yoelii genome annotation through comparative analysis. Bioinformatics 24: i383-i389.
51. Vaughan, A.M., Wang, R., and Kappe, S.H. (2010) Genetically engineered, attenuated whole-cell vaccine approaches for malaria. Hum Vaccin 6: 107-113.
52. Wang, X., McLachlan, J., Zamore, P.D., and Hall, T.M. (2002) Modular recognition of RNA by a human pumilio-homology domain. Cell 110: 501-512.
53. Wek, R.C., Jiang, H.Y., and Anthony, T.G. (2006) Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34: 7-11.
54. WHO (2011) World Malaria Report: 2011. Geneva: World Health Organization.
55. Wickens, M., Bernstein, D.S., Kimble, J., and Parker, R. (2002) A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet 18: 150-157.
56. Yuda, M., Iwanaga, S., Shigenobu, S., Mair, G.R., Janse, C.J., Waters, A.P., etal. (2009) Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol Microbiol 71: 1402-1414.
57. Zhang, K., and Rathod, P.K. (2002) Divergent regulation of dihydrofolate reductase between malaria parasite and human host. Science 296: 545-547.
58. Zhang, M., Fennell, C., Ranford-Cartwright, L., Sakthivel, R., Gueirard, P., Meister, S., etal. (2010) The Plasmodium eukaryotic initiation factor-2alpha kinase IK2 controls the latency of sporozoites in the mosquito salivary glands. J Exp Med 207: 1465-1474.
59. Zhang, M., Mishra, S., Sakthivel, R., Rojas, M., Ranjan, R., Sullivan, W.J., Jr, etal. (2012) PK4, a eukaryotic initiation factor 2alpha(eIF2alpha) kinase, is essential for the development of the erythrocytic cycle of Plasmodium. Proc Natl Acad Sci USA 109: 3956-3961.