Phosphoinositide Metabolism Links cGMP-Dependent Protein Kinase G to Essential Ca2+ Signals at Key Decision Points in the Life Cycle of Malaria Parasites

PLoS Biology

Volumn 12, Issue 3, 2014, Pages

  Brochet, Mathieu ^a   Collins, Mark O ^a,d   Smith, Terry K ^b   Thompson, Eloise ^c   Sebastian, Sarah ^a   Volkmann, Katrin ^a   Schwach, Frank ^a   Chappell, Lia ^a   Gomes, Ana Rita ^a   Berriman, Matthew ^a   Rayner, Julian C ^a   Baker, David A ^c   Choudhary, Jyoti ^a   Billker, Oliver ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CALCIUM SIGNALING; CULICIDAE; CYCLIC GMP-DEPENDENT PROTEIN KINASES; HOST-PARASITE INTERACTIONS; HUMANS; LIFE CYCLE STAGES; MALARIA; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOLS; PLASMODIUM FALCIPARUM;

EID: 84899004901     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001806     Document Type: Article

References (62)

1. Collins CR, Hackett F, Strath M, Penzo M, Withers-Martinez C, et al. (2013) Malaria parasite cGMP-dependent protein kinase regulates blood stage merozoite secretory organelle discharge and egress. PLoS Pathog 9: e1003344.
2. Billker O, Lindo V, Panico M, Etienne AE, Paxton T, et al. (1998) Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito. Nature 392: 289-292.
3. Baker DA, (2011) Cyclic nucleotide signalling in malaria parasites. Cell Microbiol 13: 331-339.
4. Taylor HM, McRobert L, Grainger M, Sicard A, Dluzewski AR, et al. (2010) The malaria parasite cyclic GMP-dependent protein kinase plays a central role in blood-stage schizogony. Eukaryot Cell 9: 37-45.
5. Moon RW, Taylor CJ, Bex C, Schepers R, Goulding D, et al. (2009) A cyclic GMP signalling module that regulates gliding motility in a malaria parasite. PLoS Pathog 5: e1000599.
6. Taylor CJ, McRobert L, Baker DA, (2008) Disruption of a Plasmodium falciparum cyclic nucleotide phosphodiesterase gene causes aberrant gametogenesis. Mol Microbiol 69: 110-118.
7. Deng W, Baker DA, (2002) A novel cyclic GMP-dependent protein kinase is expressed in the ring stage of the Plasmodium falciparum life cycle. Mol Microbiol 44: 1141-1151.
8. Donald RG, Allocco J, Singh SB, Nare B, Salowe SP, et al. (2002) Toxoplasma gondii cyclic GMP-dependent kinase: chemotherapeutic targeting of an essential parasite protein kinase. Eukaryot Cell 1: 317-328.
9. Wiersma HI, Galuska SE, Tomley FM, Sibley LD, Liberator PA, et al. (2004) A role for coccidian cGMP-dependent protein kinase in motility and invasion. Int J Parasitol 34: 369-380.
10. McRobert L, Taylor CJ, Deng W, Fivelman QL, Cummings RM, et al. (2008) Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. PLoS Biol 6: e139.
11. Dvorin JD, Martyn DC, Patel SD, Grimley JS, Collins CR, et al. (2010) A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science 328: 910-912.
12. Carvajal JA, Germain AM, Huidobro-Toro JP, Weiner CP, (2000) Molecular mechanism of cGMP-mediated smooth muscle relaxation. J Cell Physiol 184: 409-420.
13. Zhang X, Cote RH, (2005) cGMP signaling in vertebrate retinal photoreceptor cells. Front Biosci 10: 1191-1204.
14. Potter LR, (2011) Guanylyl cyclase structure, function and regulation. Cell Signal 23: 1921-1926.
15. Martin SK, Jett M, Schneider I, (1994) Correlation of phosphoinositide hydrolysis with exflagellation in the malaria microgametocyte. J Parasitol 80: 371-378.
16. O'Halloran DM, Altshuler-Keylin S, Lee JI, L'Etoile ND, (2009) Regulators of AWC-mediated olfactory plasticity in Caenorhabditis elegans. PLoS Genet 5: e1000761.
17. Schwappacher R, Weiske J, Heining E, Ezerski V, Marom B, et al. (2009) Novel crosstalk to BMP signalling: cGMP-dependent kinase I modulates BMP receptor and Smad activity. EMBO J 28: 1537-1550.
18. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127: 635-648.
19. Sebastian S, Brochet M, Collins MO, Schwach F, Jones ML, et al. (2012) A Plasmodium calcium-dependent protein kinase controls zygote development and transmission by translationally activating repressed mRNAs. Cell Host Microbe 12: 9-19.
20. Nolen B, Taylor S, Ghosh G, (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 15: 661-675.
21. Kotera J, Grimes KA, Corbin JD, Francis SH, (2003) cGMP-dependent protein kinase protects cGMP from hydrolysis by phosphodiesterase-5. Biochem J 372: 419-426.
22. Zhou Z, Sayed N, Pyriochou A, Roussos C, Fulton D, et al. (2008) Protein kinase G phosphorylates soluble guanylyl cyclase on serine 64 and inhibits its activity. Arterioscler Thromb Vasc Biol 28: 1803-1810.
23. Siden-Kiamos I, Ecker A, Nyback S, Louis C, Sinden RE, et al. (2006) Plasmodium berghei calcium-dependent protein kinase 3 is required for ookinete gliding motility and mosquito midgut invasion. Mol Microbiol 60: 1355-1363.
24. Mair GR, Lasonder E, Garver LS, Franke-Fayard BM, Carret CK, et al. (2010) Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog 6: e1000767.
25. Raabe AC, Wengelnik K, Billker O, Vial HJ, (2011) Multiple roles for Plasmodium berghei phosphoinositide-specific phospholipase C in regulating gametocyte activation and differentiation. Cell Microbiol 13: 955-966.
26. Bankaitis VA, Mousley CJ, Schaaf G, (2010) The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trends Biochem Sci 35: 150-160.
27. Leber W, Skippen A, Fivelman QL, Bowyer PW, Cockcroft S, et al. (2009) A unique phosphatidylinositol 4-phosphate 5-kinase is activated by ADP-ribosylation factor in Plasmodium falciparum. Int J Parasitol 39: 645-653.
28. Nagai T, Sawano A, Park ES, Miyawaki A, (2001) Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc Natl Acad Sci U S A 98: 3197-3202.
29. Muhia DK, Swales CA, Deng W, Kelly JM, Baker DA, (2001) The gametocyte-activating factor xanthurenic acid stimulates an increase in membrane-associated guanylyl cyclase activity in the human malaria parasite Plasmodium falciparum. Mol Microbiol 42: 553-560.
30. Baubet V, Le Mouellic H, Campbell AK, Lucas-Meunier E, Fossier P, et al. (2000) Chimeric green fluorescent protein-aequorin as bioluminescent Ca2+ reporters at the single-cell level. Proc Natl Acad Sci U S A 97: 7260-7265.
31. Billker O, Dechamps S, Tewari R, Wenig G, Franke-Fayard B, et al. (2004) Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117: 503-514.
32. Glushakova S, Lizunov V, Blank PS, Melikov K, Humphrey G, et al. (2013) Cytoplasmic free Ca2+ is essential for multiple steps in malaria parasite egress from infected erythrocytes. Malar J 12: 41.
33. Diaz CA, Allocco J, Powles MA, Yeung L, Donald RG, et al. (2006) Characterization of Plasmodium falciparum cGMP-dependent protein kinase (PfPKG): antiparasitic activity of a PKG inhibitor. Mol Biochem Parasitol 146: 78-88.
34. Alves E, Bartlett PJ, Garcia CR, Thomas AP, (2011) Melatonin and IP3-induced Ca2+ release from intracellular stores in the malaria parasite Plasmodium falciparum within infected red blood cells. J Biol Chem 286: 5905-5912.
35. Ishino T, Orito Y, Chinzei Y, Yuda M, (2006) A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Microbiol 59: 1175-1184.
36. Lourido S, Tang K, Sibley LD, (2012) Distinct signalling pathways control Toxoplasma egress and host-cell invasion. Embo J 31: 4524-4534.
37. Billker O, Lourido S, Sibley LD, (2009) Calcium-dependent signaling and kinases in apicomplexan parasites. Cell Host Microbe 5: 612-622.
38. Schlossmann J, Ammendola A, Ashman K, Zong X, Huber A, et al. (2000) Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Ibeta. Nature 404: 197-201.
39. Johnson JL, Leroux MR, (2010) cAMP and cGMP signaling: sensory systems with prokaryotic roots adopted by eukaryotic cilia. Trends Cell Biol 20: 435-444.
40. Kunz J, Fuelling A, Kolbe L, Anderson RA, (2002) Stereo-specific substrate recognition by phosphatidylinositol phosphate kinases is swapped by changing a single amino acid residue. J Biol Chem 277: 5611-5619.
41. Fik-Rymarkiewicz E, Duda T, Sharma RK, (2006) Novel frequenin-modulated Ca2+-signaling membrane guanylate cyclase (ROS-GC) transduction pathway in bovine hippocampus. Mol Cell Biochem 291: 187-204.
42. Taoufiq Z, Eguchi K, Takahashi T, (2013) Rho-kinase accelerates synaptic vesicle endocytosis by linking cyclic GMP-dependent protein kinase activity to phosphatidylinositol-4,5-bisphosphate synthesis. J Neurosci 33: 12099-12104.
43. Stewart MJ, Vanderberg JP, (1992) Electron microscopic analysis of circumsporozoite protein trail formation by gliding malaria sporozoites. J Protozool 39: 663-671.
44. Di Paolo G, De Camilli P, (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657.
45. Kremer K, Kamin D, Rittweger E, Wilkes J, Flammer H, et al. (2013) An overexpression screen of Toxoplasma gondii Rab-GTPases reveals distinct transport routes to the micronemes. PLoS Pathog 9: e1003213.
46. McNamara CW, Lee MCS, Lim CS, Lim SH, Roland J, et al. (2013) Targeting Plasmodium PI(4)K to eliminate malaria. Nature, Advance online publication.
47. Pfander C, Anar B, Schwach F, Otto TD, Brochet M, et al. (2011) A scalable pipeline for highly effective genetic modification of a malaria parasite. Nat Methods 8: 1078-1082.
48. Pino P, Sebastian S, Kim EunBin A, Bush E, Brochet M, et al. (2012) A tetracycline-repressible transactivator system to study essential genes in malaria parasites. Cell Host Microbe 12: 824-834.
49. Janse CJ, Ramesar J, Waters AP, (2006) High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1: 346-356.
50. Orr RY, Philip N, Waters AP, (2012) Improved negative selection protocol for Plasmodium berghei in the rodent malarial model. Malar J 11: 103.
51. Louise Meyer R, Zhou X, Tang L, Arpanaei A, Kingshott P, et al. (2010) Immobilisation of living bacteria for AFM imaging under physiological conditions. Ultramicroscopy 110: 1349-1357.
52. Volkmann K, Pfander C, Burstroem C, Ahras M, Goulding D, et al. (2012) The alveolin IMC1h is required for normal ookinete and sporozoite motility behaviour and host colonisation in Plasmodium berghei. PLoS One 7: e41409.
53. Otto TD, Wilinski D, Assefa S, Keane TM, Sarry LR, et al. (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol 76: 12-24.
54. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
55. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
56. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
57. Manza LL, Stamer SL, Ham AJ, Codreanu SG, Liebler DC, (2005) Sample preparation and digestion for proteomic analyses using spin filters. Proteomics 5: 1742-1745.
58. Wisniewski JR, Zougman A, Nagaraj N, Mann M, (2009) Universal sample preparation method for proteome analysis. Nat Methods 6: 359-362.
59. Kokubu M, Ishihama Y, Sato T, Nagasu T, Oda Y, (2005) Specificity of immobilized metal affinity-based IMAC/C18 tip enrichment of phosphopeptides for protein phosphorylation analysis. Anal Chem 77: 5144-5154.
60. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372.
61. Lundby A, Andersen MN, Steffensen AB, Horn H, Kelstrup CD, et al. (2013) In vivo phosphoproteomics analysis reveals the cardiac targets of beta-adrenergic receptor signaling. Sci Signal 6: rs11.
62. Richmond GS, Gibellini F, Young SA, Major L, Denton H, et al. (2010) Lipidomic analysis of bloodstream and procyclic form Trypanosoma brucei. Parasitology 137: 1357-1392.