Table 1.
Kinases secreted by protozoan parasites.
| Organism | Kinase Name | Kinase Class | References | Stages |
|---|---|---|---|---|
| Leishmania | 6-phospho-1-fructokinase, putative | carbohydrate | Silverman et al., 2008; Silverman et al., 2010a; Douanne et al., 2020 | Stationary-phase promastigotes, logarithmic promastigotes |
| adenosine kinase, putative | nucleoside | Silverman et al., 2008 | Stationary-phase promastigotes | |
| adenylate kinase, putative | nucleoside | Silverman et al., 2008; Silverman et al., 2010a; Hassani et al., 2011; Douanne et al., 2020 | Stationary-phase promastigotes, logarithmic promastigotes and axenic amastigotes | |
| casein kinase I, putative CK1.2 | protein | Silverman et al., 2008; Silverman et al., 2010a | Stationary-phase promastigotes | |
| casein kinase II, alpha chain, Putative LmjF.02.0360 | protein | Douanne et al., 2020 | Logarithmic promastigotes | |
| mevalonate kinase | lipid | Bamra et al., 2021 | Promastigotes and amastigotes | |
| cdc2-related kinase 9 | protein | Silverman et al., 2008 | Stationary-phase promastigotes | |
| glycogen synthase kinase3-putative | protein | Douanne et al., 2020 | Logarithmic promastigotes | |
| glycosomal phosphoenolpyruvate carboxykinase, putative | other | Silverman et al., 2008; Hassani et al., 2011; Douanne et al., 2020 | Stationary-phase promastigotes and logarithmic promastigotes | |
| hexokinase, putative | carbohydrate | Silverman et al., 2008; Hassani et al., 2011 | Stationary-phase promastigotes | |
| mitogen activated protein kinase, putative,map kinase, putative | protein | Silverman et al., 2008 | Stationary-phase promastigotes | |
| mitogen-activated protein kinase 3, putative,map kinase 3, putative | protein | Silverman et al., 2008 | Stationary-phase promastigotes | |
| nucleoside diphosphate kinase b | nucleoside | Silverman et al., 2008; Silverman et al., 2010a; Hassani et al., 2011; Douanne et al., 2020 | Stationary-phase promastigotes, logarithmic promastigotes and axenic amastigotes. | |
| phosphoglycerate kinase | other | Douanne et al., 2020; Mandacaru et al., 2019; Ribeiro et al., 2018; Brossas et al., 2017; Queiroz et al., 2016; Bayer-Santos et al., 2013; Hassani et al., 2011 | Logarithmic promastigotes, stationary-phase promastigotes and Epimastigotes, Vero cells infected with trypomastigotes, Trypomastigotes, Tissue culture-derived trypomastigotes and trypomastigotes. | |
| protein kinase, putative LmjF34.0030 | protein | Silverman et al., 2008 | Stationary-phase promastigotes | |
| pyruvate dehydrogenase lipoamide kinase, putative | other | Silverman et al., 2008 | Stationary-phase promastigotes | |
| pyruvate kinase, putative | other | Silverman et al., 2008; Silverman et al., 2010a; Douanne et al., 2020; Ribeiro et al., 2018 | Stationary-phase promastigotes and logarithmic promastigotes, Tissue culture-derived trypomastigotes. | |
| pyruvate phosphate dikinase, putative | other | Silverman et al., 2008; Silverman et al., 2010a; Douanne et al., 2020 | Stationary-phase promastigotes and logarithmic promastigotes | |
| serine/threonine-protein kinase, putative LINF_290033500/LmjF29.2570 identity to human Nek1 | protein | Douanne et al., 2020 | Logarithmic promastigotes | |
| serine/threonine-protein kinase, putative LmjF25.2340 identity to human AKT1 | protein | Silverman et al., 2010a | Stationary-phase promastigotes | |
| tagatose-6-phosphate kinase-like protein | carbohydrate | Silverman et al., 2008 | Stationary-phase promastigotes | |
| Trypanosoma cruzi | adenosine kinase, putative | nucleoside | Brossas et al., 2017 | Trypomastigotes |
| mevalonate kinase | lipid | Ferreira et al., 2016 | Metacyclic trypomastigote and extracellular amastigote cultures | |
| adenylate kinase, putative | nucleoside | Queiroz et al., 2016; Ribeiro et al., 2018 | Trypomastigotes, Tissue culture-derived trypomastigotes | |
| arginine kinase | other | Bayer-Santos et al., 2013; Queiroz et al., 2016; Brossas et al., 2017; Ribeiro et al., 2018; Mandacaru et al., 2019 | Epimastigotes, Vero cells infected with trypomastigotes, Trypomastigotes, Tissue culture-derived trypomastigotes and trypomastigotes. | |
| fucose kinase | carbohydrate | Ribeiro et al., 2018 | Tissue culture-derived trypomastigotes | |
| galactokinase | carbohydrate | Ribeiro et al., 2018 | Tissue culture-derived trypomastigotes | |
| glycosomal phosphoenolpyruvate carboxykinase, putative | other | Queiroz et al., 2016; Ribeiro et al., 2018; Mandacaru et al., 2019 | Trypomastigotes, Tissue culture-derived trypomastigotes and trypomastigotes. | |
| hexokinase | carbohydrate | Bayer-Santos et al., 2013, Mandacaru et al., 2019 | Epimastigotes and trypomastigotes. | |
| mitogen-activated protein kinase, putative | protein | Bayer-Santos et al., 2013; Brossas et al., 2017; Ribeiro et al., 2018 | Epimastigotes, Vero cells infected with trypomastigotes, Tissue culture-derived trypomastigotes | |
| NIMA-related kinase, putative | protein | Queiroz et al., 2016 | Trypomastigotes | |
| nucleoside diphosphate kinase B | nucleoside | Bayer-Santos et al., 2013; Brossas et al., 2017; Queiroz et al., 2016; Ribeiro et al., 2018; Mandacaru et al., 2019 | Epimastigotes, Vero cells infected with trypomastigotes, Trypomastigotes, Tissue culture-derived trypomastigotes and trypomastigotes. | |
| phosphatidylinositol-3-Kinase | lipid | Bayer-Santos et al., 2013 | Epimastigotes | |
| Protein kinase Tc00.1047053506211.210 MAPKKK identity to human PAK1/PAK3 | protein | Ribeiro et al., 2018 | Tissue culture-derived trypomastigotes | |
| Protein kinase, putative TcCLB.508641.170 identity to human PKC theta | protein | Brossas et al., 2017 | Vero cells infected with trypomastigotes | |
| protein kinase-A catalytic subunit | protein | Queiroz et al., 2016 | Trypomastigotes | |
| pyridoxal kinase, putative | other | Queiroz et al., 2016; Ribeiro et al., 2018 | Trypomastigotes, Tissue culture-derived trypomastigotes | |
| pyruvate kinase 2, putative | other | Queiroz et al., 2016 | Trypomastigotes | |
| pyruvate phosphate dikinase 2 | other | Queiroz et al., 2016 | Trypomastigotes | |
| pyruvate phosphate dikinase 1 | other | Bayer-Santos et al., 2013; Ribeiro et al., 2018 | Epimastigotes, Tissue culture-derived trypomastigotes | |
| serine/threonine protein kinase TcCLB.508153.400/TCSYLVIO_004423 identity to human Nek1 | protein | Bayer-Santos et al., 2013; Ribeiro et al., 2018 | Epimastigotes, Tissue culture-derived trypomastigotes | |
| serine/threonine-protein kinase 10, putative TcCLB.506401.110 identity to human STK10 | protein | Queiroz et al., 2016 | Trypomastigotes | |
| Plasmodium | Camk2d calcium/calmodulin_dependent protein kinase II_ delta isoform 1 | protein | Martin-Jaular et al., 2011 | Trophozoite P. yoelii infected reticulocyte |
| Camk2d Isoform 1 of Calcium/calmodulin_dependent protein kinase type II delta chain | protein | Martin-Jaular et al., 2011 | Trophozoite P. yoelii infected reticulocyte | |
| Camk2d Isoform 2 of Calcium/calmodulin_dependent protein kinase type II delta chain | protein | Martin-Jaular et al., 2011 | Trophozoite P. yoelii infected reticulocyte | |
| Camk2d Isoform 3 of Calcium/calmodulin_dependent protein kinase type II delta chain | protein | Martin-Jaular et al., 2011 | Trophozoite P. yoelii infected reticulocyte | |
| Camk2d Isoform 4 of Calcium/calmodulin_dependent protein kinase type II delta chain | protein | Martin-Jaular et al., 2011 | Trophozoite P. yoelii infected reticulocyte | |
| casein kinase 2, alpha subunit | protein | Abdi et al., 2017 | Trophozoite P. falciparum infected erythrocyte | |
| diacyl glycerol kinase | lipid | Gualdron-Lopez et al., 2018 | Trophozoite P. vivax infected erythrocyte | |
| FIKK10.1 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK13 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK14 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK1 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK4.1 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK4.2 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK7.1 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK9.1 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK9.3 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK9.6 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK10.2 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK11 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| FIKK12 | protein | Hiller et al., 2004 | Trophozoite P. falciparum infected erythrocyte | |
| pacsin2 Protein kinase C and casein kinase substrate in neurons protein 2 | protein | Martin-Jaular et al., 2011 | Trophozoite P. yoelii infected reticulocyte | |
| phosphatidylinositol 4-kinase, putative | lipid | Abdi et al., 2017 | Trophozoite P. falciparum infected erythrocyte | |
| phosphoglycerate kinase | other | Mantel et al., 2013; Abdi et al., 2017 | Trophozoite P. falciparum infected erythrocyte | |
| pseudo protein kinase 1, putative PF3D7_0321400 | protein | Abdi et al., 2017 | Trophozoite P. falciparum infected erythrocyte | |
| pyruvate kinase | other | Vincensini et al., 2005; Mantel et al., 2013 | Trophozoite P. falciparum infected erythrocyte | |
| serine/threonine protein kinase, putative PF3D7_1441300 | protein | Abdi et al., 2017 | Trophozoite P. falciparum infected erythrocyte | |
| calcium-dependent protein kinase CDPK1 | protein | Lal et al., 2009 | Purified microneme organelle | |
| calcium-dependent protein kinase CDPK4 | protein | Lal et al., 2009 | Purified microneme organelle | |
| adenylate kinase | nucleoside | Vincensini et al., 2005 | Trophozoite P. falciparum infected erythrocyte | |
| Toxoplasma | calcium-dependent protein kinase CDPK1 | protein | Wowk et al., 2017; Ramirez-Flores et al., 2019 | Tachyzoite T. gondii infected human foreskin fibroblast, Acellular tachyzoites |
| calcium-dependent protein kinase CDPK2A | protein | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| calcium-dependent protein kinase CDPK3 | protein | Wowk et al., 2017; Ramirez-Flores et al., 2019 | Tachyzoite T. gondii infected human foreskin fibroblast, Acellular tachyzoites | |
| casein kinase I | protein | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| CMGC kinase, CK2 family | protein | Wowk et al., 2017; Ramirez-Flores et al., 2019 | Tachyzoite T. gondii infected human foreskin fibroblast, Acellular tachyzoites | |
| hexokinase | carbohydrate | Wowk et al., 2017; Ramirez-Flores et al., 2019 | Tachyzoite T. gondii infected human foreskin fibroblast, Acellular tachyzoites | |
| nucleoside diphosphate kinase | nucleoside | Lee et al., 2014 | Acellular tachyzoites | |
| phosphoenolpyruvate-carboxykinase I | other | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| phosphofructokinase PFKII | carbohydrate | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| phosphoglycerate kinase | other | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| pyruvate kinase | other | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| rhoptry kinase family protein ROP39 | protein | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| selenide, water dikinase | other | Wowk et al., 2017 | Tachyzoite T. gondii infected human foreskin fibroblast | |
| ROP2 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP4 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP5 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP8 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP11 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP16 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP17 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP18 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| ROP38 - PK-like | protein | Bradley et al., 2005 | Purified rhoptry organelle | |
| WNG1 (With-No-Gly-Loop) | protein | Beraki et al., 2019 | Bradyzoite | |
| WNG2 | protein | Beraki et al., 2019 | Bradyzoite | |
| WNG3 | protein | Beraki et al., 2019 | Bradyzoite | |
| BPK1 bradyzoite pseudokinase 1 | protein | Buchholz et al., 2013 | Bradyzoite | |
| Eimeria a | pyruvate kinase | other | Labbé et al., 2006 | Schizont from in vitro infected cells |
| hexokinase | carbohydrate | Sun et al., 2016 | Sporozoite from in vitro infected cells | |
| calcium-dependent protein kinase CDPK1 | protein | Dunn et al., 1996 | Sporozoite from in vitro infected cells | |
| calcium-dependent protein kinase CDPK2 | protein | Dunn et al., 1996 | Sporozoite from in vitro infected cells | |
| calcium-dependent protein kinase CDPK3 | protein | Han et al., 2013 | Sporozoite and schizont from in vitro infected cells | |
| calcium-dependent protein kinase CDPK4 | protein | Wang et al., 2016a | Sporozoite and merozoite from in vitro infected cells | |
| ETH_00000075 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00005190 - EtROP1 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00005400 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00005840 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00005905 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00020620 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00026495 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00027695 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00027700 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00027855 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| ETH_00028765 | protein | Oakes et al., 2013 | Purified rhoptry organelle | |
| WNG1, predicted | protein | Beraki et al., 2019 | ND b | |
| WNG4, predicted | protein | Beraki et al., 2019 | ND b |
a
Secreted kinases listed for Eimeria are underestimated, due to a lack of datasets. Eimeria pyruvate kinase (Labbé et al., 2006), hexokinase (Sun et al., 2016) and CDPK (Dunn et al., 1996; Han et al., 2013; Wang et al., 2016a) are secreted by an unknown mechanism.
b
Not determined.
Kinase class refers to the kinase substrate. Kinases common to kinetoplastids and Apicomplexa are indicated in bold, kinases specific to kinetoplastids or to Apicomplexa are indicated in italic or underlined, respectively. Based on experimental procedures of cited references for Apicomplexa, kinases from organelles are secreted in the host cell cytoplasm, not in the extracellular medium. To the author knowledge, only P. falciparum TKL2 and PfCK1 were detected in extracellular medium and at the erythrocyte membrane (Abdi et al., 2013) and maybe associated to immunomodulatory functions. Most of the secreted proteins of Kinetoplastids are released inside the host cell. Ndk and AK seem to be secreted in the extracellular environment of the host cell due to their role. Limitations concerning secretome preparation and characterization have been reviewed (Severino et al., 2013).