Roles of Apicomplexan protein kinases at each life cycle stage

Parasitology International

Volumn 61, Issue 2, 2012, Pages 224-234

  Kato, Kentaro ^a   Sugi, Tatsuki ^a   Iwanaga, Tatsuya ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Apicomplexan protein kinase; Life cycle; Plasmodium; Protein kinase inhibitor; Toxoplasma

Indexed keywords

BENZAMIDE DERIVATIVE; BUTYROLACTONE; CALCIUM; CALMODULIN; CALMODULIN INHIBITOR; CYCLIC AMP; GENISTEIN; GLYCOGEN SYNTHASE KINASE 3; HYMENIALDISINE; INDIRUBIN; KENPAULLONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSIN LIGHT CHAIN; OLOMOUCINE; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE C INHIBITOR; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE; PURVALANOL A; PURVALANOL B; PYRIDINE DERIVATIVE; ROSCOVITINE; STAT3 PROTEIN; STAT6 PROTEIN; STAUROSPORINE; SULFONAMIDE; UNINDEXED DRUG; VIRULENCE FACTOR;

APICOMPLEXA; BRADYZOITE; CELL CYCLE REGULATION; CELL INVASION; CRYPTOSPORIDIUM PARVUM; ERYTHROCYTE; GAMETOGENESIS; LIFE CYCLE; MEROZOITE; NONHUMAN; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SCHIZONT; SPOROZOITE; STRESS; TACHYZOITE; TOXOPLASMA;

ANIMALS; APICOMPLEXA; LIFE CYCLE STAGES; PLASMODIUM; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTOZOAN PROTEINS; TOXOPLASMA;

PROTOZOA; TOXOPLASMA;

EID: 84857801309     PISSN: 13835769     EISSN: 18730329     Source Type: Journal    
DOI: 10.1016/j.parint.2011.12.002     Document Type: Review

References (84)

1. Dvorin J.D., Martyn D.C., Patel S.D., Grimley J.S., Collins C.R., Hopp C.S., et al. A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science 2010, 328:910-912.
2. Kato K., Sudo A., Kobayashi K., Tohya Y., Akashi H. Characterization of Plasmodium falciparum protein kinase 2. Mol Biochem Parasitol 2008, 162:87-95.
3. Jones M.L., Cottingham C., Rayner J.C. Effects of calcium signaling on Plasmodium falciparum erythrocyte invasion and post-translational modification of gliding-associated protein 45 (PfGAP45). Mol Biochem Parasitol 2009, 168:55-62.
4. Kumar A., Vaid A., Syin C., Sharma P. PfPKB, a novel protein kinase B-like enzyme from Plasmodium falciparum: I. Identification, characterization, and possible role in parasite development. J Biol Chem 2004, 279:24255-24264.
5. Vaid A., Sharma P. PfPKB, a protein kinase B-like enzyme from Plasmodium falciparum: II. Identification of calcium/calmodulin as its upstream activator and dissection of a novel signaling pathway. J Biol Chem 2006, 281:27126-27133.
6. Vaid A., Thomas D.C., Sharma P. Role of Ca2+/Calmodulin-PfPKB signaling pathway in erythrocyte invasion by Plasmodium falciparum. J Biol Chem 2008, 283:5589-5597.
7. Green J.L., Rees-Channer R.R., Howell S.A., Martin S.R., Knuepfer E., Taylor H.M., et al. The motor complex of Plasmodium falciparum: phosphorylation by a calcium-dependent protein kinase. J Biol Chem 2008, 283:30980-30989.
8. Leykauf K., Treeck M., Gilson P.R., Nebl T., Braulke T., Cowman A.F., et al. Protein kinase A dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite. PLoS Pathog 2010, 6:e1000941.
9. Ward G.E., Fujioka H., Aikawa M., Miller L.H. Staurosporine inhibits invasion of erythrocytes by malarial merozoites. Exp Parasitol 1994, 79:480-487.
10. Dluzewski A.R., Garcia C.R. Inhibition of invasion and intraerythrocytic development of Plasmodium falciparum by kinase inhibitors. Experientia 1996, 52:621-623.
11. Taylor H.M., McRobert L., Grainger M., Sicard A., Dluzewski A.R., Hopp C.S., et al. The malaria parasite cyclic GMP-dependent protein kinase plays a central role in blood-stage schizogony. Eukaryot Cell 2010, 9:37-45.
12. Diaz C.A., Allocco J., Powles M.A., Yeung L., Donald R.G.K., Anderson J.W., et al. Characterization of Plasmodium falciparum cGMP-dependent protein kinase (PfPKG): antiparasitic activity of a PKG inhibitor. Mol Biochem Parasitol 2006, 146:78-88.
13. Billker O., Lourido S., Sibley L.D. Calcium-dependent signaling and kinases in Apicomplexan parasites. Cell Host Microbe 2009, 5:612-622.
14. Siden-Kiamos I., Ecker A., Nyback S., Louis C., Sinden R.E., Billker O. Plasmodium berghei calcium-dependent protein kinase 3 is required for ookinete gliding motility and mosquito midgut invasion. Mol Microbiol 2006, 60:1355-1363.
15. Ishino T., Orito Y., Chinzei Y., Yuda M. A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Microbiol 2006, 59:1175-1184.
16. Coppi A., Tewari R., Bishop J.R., Bennett B.L., Lawrence R., Esko J.D., et al. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe 2007, 2:316-327.
17. Möskes C., Burghaus P.A., Wernli B., Sauder U., Dürrenberger M., Kappes B. Export of Plasmodium falciparum calcium-dependent protein kinase 1 to the parasitophorous vacuole is dependent on three N-terminal membrane anchor motifs. Mol Microbiol 2004, 54:676-691.
18. Droucheau E., Primot A., Thomas V., Mattei D., Knockaert M., Richardson C., et al. Plasmodium falciparum glycogen synthase kinase-3: molecular model, expression, intracellular localisation and selective inhibitors. Biochim Biophys Acta 2004, 1697:181-196.
19. Hotta C.T., Gazarini M.L., Beraldo F.H., Varotti F.P., Lopes C., Markus R.P., et al. Calcium-dependent modulation by melatonin of the circadian rhythm in malarial parasites. Nat Cell Biol 2000, 2:466-468.
20. Beraldo F.H., Almeida F.M., da Silva A.M., Garcia C.R. Cyclic AMP and calcium interplay as second messengers in melatonin-dependent regulation of Plasmodium falciparum cell cycle. J Cell Biol 2005, 170:551-557.
21. Syin C., Parzy D., Traincard F., Boccaccio I., Joshi M.B., Lin D.T., et al. The H89 cAMP-dependent protein kinase inhibitor blocks Plasmodium falciparum development in infected erythrocytes. Eur J Biochem 2001, 268:4842-4849.
22. Merckx A., Nivez M.P., Bouyer G., Alano P., Langsley G., Deitsch K., et al. Plasmodium falciparum regulatory subunit of cAMP-dependent PKA and anion channel conductance. PLoS Pathog 2008, 4:e19.
23. Dorin D., Semblat J.P., Poullet P., Alano P., Goldring J.P., Whittle C., et al. PfPK7, an atypical MEK-related protein kinase, reflects the absence of classical three-component MAPK pathways in the human malaria parasite Plasmodium falciparum. Mol Microbiol 2005, 55:184-196.
24. Merckx A., Echalier A., Langford K., Sicard A., Langsley G., Joore J., et al. Structures of P. falciparum protein kinase 7 identify an activation motif and leads for inhibitor design. Structure 2008, 16:228-238.
25. McRobert L., Taylor C.J., Deng W., Fivelman Q.L., Cummings R.M., Polley S.D., et al. Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. PLoS Biol 2008, 6:e139.
26. Laurent D., Jullian V., Parenty A., Knibiehler M., Dorin D., Schmitt S., et al. Antimalarial potential of xestoquinone, a protein kinase inhibitor isolated from a Vanuatu marine sponge Xestospongia sp. Bioorg Med Chem 2006, 14:4477-4482.
27. Sicard A., Semblat J.P., Doerig C., Hamelin R., Moniatte M., Dorin-Semblat D., et al. Activation of a PAK-MEK signalling pathway in malaria parasite-infected erythrocytes. Cell Microbiol 2011, 13:836-845.
28. Ward P., Equinet L., Packer J., Doerig C. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 2004, 5:79.
29. Woodard C.L., Li Z., Kathcart A.K., Terrell J., Gerena L., Lopez-Sanchez M., et al. Oxindole-based compounds are selective inhibitors of Plasmodium falciparum cyclin dependent protein kinases. J Med Chem 2003, 46:3877-3882.
30. Forney J.R., DeWald D.B., Yang S., Speer C.A., Healey M.C. A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection. Infect Immun 1999, 67:844-852.
31. Harmse L., van Zyl R., Gray N., Schultz P., Leclerc S., Meijer L., et al. Structure-activity relationships and inhibitory effects of various purine derivatives on the in vitro growth of Plasmodium falciparum. Biochem Pharmacol 2001, 62:341-348.
32. Graeser R., Wernli B., Franklin R.M., Kappes B. Plasmodium falciparum protein kinase 5 and the malarial nuclear division cycles. Mol Biochem Parasitol 1996, 82:37-49.
33. Caridha D., Kathcart A.K., Jirage D., Waters N.C. Activity of substituted thiophene sulfonamides against malarial and mammalian cyclin dependent protein kinases. Bioorg Med Chem Lett 2010, 20:3863-3867.
34. Lemercier G., Fernandez-Montalvan A., Shaw J.P., Kugelstadt D., Bomke J., Domostoj M., et al. Identification and characterization of novel small molecules as potent inhibitors of the plasmodial calcium-dependent protein kinase 1. Biochemistry 2009, 48:6379-6389.
35. Wu T., Nagle A., Sakata T., Henson K., Borboa R., Chen Z., et al. Cell-based optimization of novel benzamides as potential antimalarial leads. Bioorg Med Chem Lett 2009, 19:6970-6974.
36. Billker O., Dechamps S., Tewari R., Wenig G., Franke-Fayard B., Brinkmann V. Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 2004, 117:503-514.
37. Ranjan R., Ahmed A., Gourinath S., Sharma P. Dissection of mechanisms involved in the regulation of Plasmodium falciparum calcium-dependent protein kinase 4. J Biol Chem 2009, 284:15267-15276.
38. Kato K., Sudo A., Kobayashi K., Sugi T., Tohya Y., Akashi H. Characterization of Plasmodium falciparum calcium-dependent protein kinase 4. Parasitol Int 2009, 58:394-400.
39. Dorin D., Le Roch K., Sallicandro P., Alano P., Parzy D., Poullet P., et al. Pfnek-1, a NIMA-related kinase from the human malaria parasite Plasmodium falciparum Biochemical properties and possible involvement in MAPK regulation. Eur J Biochem 2001, 268:2600-2608.
40. Dorin D., Alano P., Boccaccio I., Cicéron L., Doerig C., Sulpice R., et al. An atypical mitogen-activated protein kinase (MAPK) homologue expressed in gametocytes of the human malaria parasite Plasmodium falciparum. Identification of a MAPK signature. J Biol Chem 1999, 274:29912-29920.
41. 2+/calmodulin-dependent protein kinase blocks morphological differentiation of Plasmodium gallinaceum zygotes to ookinetes. J Biol Chem 2002, 277:14085-14091.
42. 2+/calmodulin- and cGMP-dependent pathways in gametogenesis of a rodent malaria parasite, Plasmodium berghei. Eur J Cell Biol 1993, 60:101-107.
43. Peixoto L., Chen F., Harb O.S., Davis P.H., Beiting D.P., Brownback C.S., et al. Integrative genomic approaches highlight a family of parasite-specific kinases that regulate host responses. Cell Host Microbe 2010, 8:208-218.
44. Carruthers V.B., Giddings O.K., Sibley L.D. Secretion of micronemal proteins is associated with toxoplasma invasion of host cells. Cell Microbiol 1999, 1:225-235.
45. Caldas L.A., de Souza W., Attias M. Calcium ionophore-induced egress of Toxoplasma gondii shortly after host cell invasion. Vet Parasitol 2007, 147:210-220.
46. Kieschnick H., Wakefield T., Narducci C.A., Beckers C. Toxoplasma gondii attachment to host cells is regulated by a calmodulin-like domain protein kinase. J Biol Chem 2001, 276:12369-12377.
47. Dobrowolski J.M., Carruthers V.B., Sibley L.D. Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol Microbiol 1997, 26:163-173.
48. Donald R.G., Zhong T., Wiersma H., Nare B., Yao D., Lee A., et al. Anticoccidial kinase inhibitors: identification of protein kinase targets secondary to cGMP-dependent protein kinase. Mol Biochem Parasitol 2006, 149:86-98.
49. Wiersma H.I., Galuska S.E., Tomley F.M., Sibley L.D., Liberator P.A., Donald R.G.K. A role for coccidian cGMP-dependent protein kinase in motility and invasion. Int J Parasitol 2004, 34:369-380.
50. Pomel S., Luk F.C., Beckers C.J. Host cell egress and invasion induce marked relocations of glycolytic enzymes in Toxoplasma gondii tachyzoites. PLoS Pathog 2008, 4:e1000188.
51. Ojo K.K., Larson E.T., Keyloun K.R., Castaneda L.J., DeRocher A.E., Inampudi K.K., et al. Toxoplasma gondii calcium-dependent protein kinase 1 is a target for selective kinase inhibitors. Nat Struct Mol Biol 2010, 17:602-607.
52. Sugi T., Kato K., Kobayashi K., Watanabe S., Kurokawa H., Gong H., et al. Use of the kinase inhibitor analog 1NM-PP1 reveals a role for Toxoplasma gondii CDPK1 in the invasion step. Eukaryot Cell 2010, 9:667-670.
53. Lourido S., Shuman J., Zhang C., Shokat K.M., Hui R., Sibley L.D. Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma. Nature 2010, 465:359-362.
54. Sugi T., Kato K., Kobayashi K., Pandey K., Takemae H., Kurokawa H., et al. Molecular analyses of Toxoplasma gondii calmodulin-like domain protein kinase isoform 3. Parasitol Int 2009, 58:416-423.
55. Nagamune K., Sibley L.D. Comparative genomic and phylogenetic analyses of calcium ATPases and calcium-regulated proteins in the apicomplexa. Mol Biol Evol 2006, 23:1613-1627.
56. Robert-Gangneux F., Creuzet C., Dupouy-Camet J., Roisin M.P. Mitogen-activated protein kinases (MAPK) and Toxoplasma gondii host cell invasion. Ann Pharm Fr 2001, 59:297-304.
57. Robert-Gangneux F., Creuzet C., Dupouy-Camet J., Roisin M.P. Involvement of the Mitogen-Activated Protein (MAP) kinase signalling pathway in host cell invasion by Toxoplasma gondii. Parasite J Soc Fr Parasitol 2000, 7:95-101.
58. Gilk S.D., Gaskins E., Ward G.E., Beckers C.J.M. GAP45 phosphorylation controls assembly of the Toxoplasma myosin XIV complex. Eukaryot Cell 2009, 8:190-196.
59. Eaton M.S., Weiss L.M., Kim K. Cyclic nucleotide kinases and tachyzoite-bradyzoite transition in Toxoplasma gondii. Int J Parasitol 2006, 36:107-114.
60. Kurokawa H., Kato K., Iwanaga T., Sugi T., Sudo A., Kobayashi K., et al. Identification of Toxoplasma gondii cAMP dependent protein kinase and its role in the tachyzoite growth. PLoS One 2011, 6:e22492.
61. Donald R.G., Zhong T., Meijer L., Liberator P.A. Characterization of two T. gondii CK1 isoforms. Mol Biochem Parasitol 2005, 141:15-27.
62. Gubbels M.J., Lehmann M., Muthalagi M., Jerome M.E., Brooks C.F., Szatanek T., et al. Forward genetic analysis of the apicomplexan cell division cycle in Toxoplasma gondii. PLoS Pathog 2008, 4:e36.
63. Brumlik M.J., Wei S., Finstad K., Nesbit J., Hyman L.E., Lacey M., et al. Identification of a novel mitogen-activated protein kinase in Toxoplasma gondii. Int J Parasitol 2004, 34:1245-1254.
64. Brumlik M.J., Wei S., Lacey M., Curiel T.J. Toxoplasma gondii expresses two distinct mitogen-activated protein kinase genes that are differentially regulated. J Investig Med 2005, 53:S307.
65. Wei S., Marches F., Daniel B., Sonda S., Heidenreich K., Curiel T. Pyridinylimidazole p38 mitogen-activated protein kinase inhibitors block intracellular Toxoplasma gondii replication. Int J Parasitol 2002, 32:969-977.
66. Khan F., Tang J.Z., Qin C.L., Kim K. Cyclin-dependent kinase TPK2 is a critical cell cycle regulator in Toxoplasma gondii. Mol Microbiol 2002, 45:321-332.
67. Eaton M., Weiss L., Kim K. Cyclic nucleotide kinases and tachyzoite-bradyzoite transition in Toxoplasma gondii. Int J Parasitol 2006, 36:107-114.
68. Kim J.Y., Ahn M.H., Song H.O., Choi J.H., Ryu J.S., Min D.Y., et al. Involvement of MAPK activation in chemokine or COX-2 productions by Toxoplasma gondii. Korean J Parasitol 2006, 44:197-207.
69. Wei S., Daniel B.J., Brumlik M.J., Burow M.E., Zou W., Khan I.A., et al. Drugs designed to inhibit human p38 mitogen-activated protein kinase activation treat Toxoplasma gondii and Encephalitozoon cuniculi infection. Antimicrob Agents Chemother 2007, 51:4324-4328.
70. Radke J., Donald R., Eibs A., Jerome M., Behnke M., Liberator P., et al. Changes in the expression of human cell division autoantigen-1 influence Toxoplasma gondii growth and development. PLoS Pathog 2006, 2:e105.
71. Narasimhan J., Joyce B.R., Naguleswaran A., Smith A.T., Livingston M.R., Dixon S.E., et al. Translation regulation by eukaryotic initiation factor-2 kinases in the development of latent cysts in Toxoplasma gondii. J Biol Chem 2008, 283:16591-16601.
72. Sullivan W.J., Narasimhan J., Bhatti M.M., Wek R.C. Parasite-specific eIF2 (eukaryotic initiation factor-2) kinase required for stress-induced translation control. Biochem J 2004, 380:523-531.
73. Joyce B.R., Queener S.F., Wek R.C., Sullivan W.J. Phosphorylation of eukaryotic initiation factor-2 alpha promotes the extracellular survival of obligate intracellular parasite Toxoplasma gondii. Proc Natl Acad Sci USA 2010, 107:17200-17205.
74. Konrad C., Wek R.C., Sullivan W.J. A GCN2-like eukaryotic initiation factor-2 kinase increases the viability of extracellular Toxoplasma gondii parasites. Eukaryot Cell 2011, 10:1403-1412.
75. Saeij J.P.J., Boyle J.P., Coller S., Taylor S., Sibley L.D., Brooke-Powell E.T., et al. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 2006, 314:1780-1783.
76. Taylor S., Barragan A., Su C., Fux B., Fentress S.J., Tang K., et al. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 2006, 314:1776-1780.
77. Saeij J.P., Coller S., Boyle J.P., Jerome M.E., White M.W., Boothroyd J.C. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 2007, 445:324-327.
78. Yamamoto M., Standley D.M., Takashima S., Saiga H., Okuyama M., Kayama H., et al. A single polymorphic amino acid on Toxoplasma gondii kinase ROP16 determines the direct and strain-specific activation of Stat3. J Exp Med 2009, 206:2747-2760.
79. Ong Y.C., Reese M.L., Boothroyd J.C. Toxoplasma rhoptry protein 16 (ROP16) subverts host function by direct tyrosine phosphorylation of STAT6. J Biol Chem 2010, 285:28731-28740.
80. El Hajj H., Lebrun M., Arold S.T., Vial H., Labesse G., Dubremetz J.F. ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii. PLoS Pathog 2007, 3(e14).
81. Fentress S.J., Behnke M.S., Dunay I.R., Mashayekhi M., Rommereim L.M., Fox B.A., et al. Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Cell Host Microbe 2010, 8:484-495.
82. Yamamoto M., Ma J.S., Mueller C., Kamiyama N., Saiga H., Kubo E., et al. ATF6β is a host cellular target of the Toxoplasma gondii virulence factor ROP18. J Exp Med 2011, 208:1533-1546.
83. Nare B., Allocco J.J., Liberator P.A., Donald R.G.K. Evaluation of a cyclic GMP-dependent protein kinase inhibitor in treatment of murine toxoplasmosis: gamma interferon is required for efficacy. Antimicrob Agents Chemother 2002, 46:300-307.
84. Donald R.G.K., Allocco J., Singh S.B., Nare B., Salowe S.P., Wiltsie J., et al. Toxoplasma gondii cyclic GMP-dependent kinase: chemotherapeutic targeting of an essential parasite protein kinase. Eukaryot Cell 2002, 1:317-328.