. 2016 May 24;18(7):905–918. doi: 10.1111/cmi.12604

Table 1.

Summary of published data on proteins involved in malaria parasite development in the mosquito midgut

Protein	Function	Species	Gender^*	Reference
Actin 2	Male gametogenesis; ookinete formation	P. berghei	M	Deligianni et al., 2011; Andreadaki et al., 2014
Calcineurin	Male gametogenesis; fertilization	P. berghei	M	Philip and Waters, 2015
CDC20	Chromatin condensation; axoneme motility; cytokinesis (M)	P. berghei		Guttery et al., 2012a
CDPK1	Essential in ABS; P. berghei: ookinete development; release of translational repression of mRNAs (F); exflagellation (M)	P. falciparum		Sebastian et al., 2012
CDPK1		P. berghei		Sebastian et al., 2012
CDPK3	Ookinete motility; mosquito midgut invasion	P. berghei		Ishino et al., 2006; Siden‐Kiamos et al., 2006
CDPK4	P. falciparum: microgamete egress; P. berghei: DNA synthesis; transmission to the mosquito	P. falciparum	M	Billker et al., 2004; Ojo et al., 2012, 2014
CDPK4		P. berghei	M	Billker et al., 2004; Ojo et al., 2012, 2014
CelTOS	Ookinete midgut traversal	P. berghei		Kariu et al., 2006
Chitinase	Hydrolysis of peritrophic membrane during ookinete midgut traversal	P. falciparum		Vinetz et al., 1999, 2000; Langer et al., 2000; Dessens et al., 2001; Tsai et al., 2001
		P. berghei
		P. gallinaceum
CITH	Translational repression of mRNAs	P. berghei	F	Mair et al., 2006, 2009
CTRP	Ookinete motility	P. falciparum		Trottein et al., 1995; Dessens et al., 1999; Yuda et al., 1999; Templeton et al., 2000; Li et al., 2004
CTRP	Ookinete motility	P. berghei
DHHC2	Lipidation modification during zygote‐to‐ookinete conversion	P. berghei		Santos et al., 2015
DOZI	Translational repression of mRNAs	P. berghei	F	Mair et al., 2006, 2010
FACT‐L	Essential in ABS; DNA replication (M)	P. berghei		Laurentino et al., 2011
GAK	Phosphate group transfer during ookinete formation	P. berghei		Tewari et al., 2010
GAP45	Ookinete development	P. berghei		Sebastian et al., 2012
GAP50	Part of the IMC; relocalization to the plasmalemma during gametogenesis; receptor of factor H in gametes	P. falciparum		Simon et al., 2013
GCα	Essential in ABS; signalling during GC activation; cGMP synthesis	P. falciparum		Carucci et al., 2000; Muhia et al., 2001
GCα		P. berghei		Carucci et al., 2000; Muhia et al., 2001
GCβ	Ookinete motility	P. berghei		Hirai et al., 2006
GCS1 (HAP2)	Gamete fusion	P. berghei		Hirai et al., 2008; Liu et al., 2008
GEST	Osmiophilic body protein; GC egress; PV rupture	P. berghei		Talman et al., 2011
IMC1a, b, h	Alveolins important for mechanical strength of ookinete	P. berghei		Volkmann et al., 2012
ISP1 and 3	Association with apical complex in retorts	P. berghei		Poulin et al., 2013
LCCL‐domain proteins	Microgamete‐macrogamete attachment	P. falciparum	F	Pradel et al., 2004; Simon et al., 2009, 2016
LCCL‐domain proteins	Microgamete‐macrogamete attachment	P. berghei	F	Pradel et al., 2004; Simon et al., 2009, 2016
Map‐2	Chromatin condensation; axoneme motility; cytokinesis	P. berghei	M	Rangarajan et al., 2005; Tewari et al., 2005
MDV‐1/Peg3	Osmiophilic body protein; GC egress; PV rupture	P. falciparum		Furuya et al., 2005; Silvestrini et al., 2005; Lanfrancotti et al., 2007; Ponzi et al., 2009; Olivieri et al., 2015
MDV‐1/Peg3	Osmiophilic body protein; GC egress; PV rupture	P. berghei
Nek‐2 and Nek‐4	Genome replication	P. falciparum	Nek‐4: F	Reininger et al., 2005, 2009
Nek‐2 and Nek‐4	Genome replication	P. berghei	Nek‐4: F	Reininger et al., 2005, 2009
P25	Ookinete surface protein; ookinete survival in the mosquito midgut, traversal of the epithelium; ookinete–oocyst transformation	P. berghei	F	Tomas et al., 2001
P28	Ookinete surface protein; ookinete survival in the mosquito midgut, traversal of the epithelium; ookinete–oocyst transformation	P. berghei	F	Tomas et al., 2001
PDEδ	Hydrolysis of cGMP; rounding up of activated GC	P. falciparum		McRobert et al., 2008
PF16	Axoneme motility	P. berghei		Straschil et al., 2010
Pg377	Osmiophilic body protein; GC egress	P. falciparum	F (P. f.)	Alano et al., 1995; Severini et al., 1999; Olivieri et al., 2015
Pg377	Osmiophilic body protein; GC egress	P. berghei	F (P. f.)
PI4K	Essential in ABS; phosphorylation of PI during GC activation	P. berghei		Brochet et al., 2014
PIP5K	P. berghei: essential in ABS; phosphorylation of PI4P during GC activation	P. falciparum		Leber et al., 2009; Brochet et al., 2014
PIP5K		P. berghei		Leber et al., 2009; Brochet et al., 2014
PI‐PLC	PIP₂ degradation into DAG and IP₃ during GC activation	P. falciparum		Martin et al., 1994; Raabe et al., 2011
PI‐PLC	PIP₂ degradation into DAG and IP₃ during GC activation	P. berghei		Martin et al., 1994; Raabe et al., 2011
PK7	Phosphate group transfer during ookinete formation	P. berghei		Tewari et al., 2010
PKG	Gametogenesis; regulation of Ca²⁺ levels; P. berghei: ookinete gliding	P. falciparum		McRobert et al., 2008; Moon et al., 2009; Brochet et al., 2014
PKG		P. berghei
POS1‐10	Ookinete surface protein	P. berghei		Kaneko et al., 2015
PPKL	Ookinete development and motility	P. berghei	F	Guttery et al., 2012b
PPLP2	GC egress; EM perforation	P. falciparum		Deligianni et al., 2013; Wirth et al., 2014
PPLP2	GC egress; EM perforation	P. berghei		Deligianni et al., 2013; Wirth et al., 2014
PPLP3‐5	Ookinete midgut traversal	P. falciparum	PPLP4: F	Kadota et al., 2004; Ecker et al., 2007, 2008; Kaneko et al., 2015; Wirth et al., 2015
PPLP3‐5	Ookinete midgut traversal	P. berghei	PPLP4: F
PPM1	Exflagellation	P. berghei		Guttery et al., 2014
PPM2	Ookinete development	P. berghei		Guttery et al., 2014
Ps230	Rosetting; microgamete‐macrogamete attachment	P. falciparum		Eksi et al., 2006
Ps47	Microgamete‐macrogamete attachment; evasion of TEP1‐related killing in the mosquito midgut	P. falciparum	F	van Schaijk et al., 2006; Molina‐Cruz et al., 2013
Ps47		P. berghei	F	van Schaijk et al., 2006; Molina‐Cruz et al., 2013
Ps48/45	Microgamete–macrogamete attachment	P. falciparum		van Dijk et al., 2001
Ps48/45	Microgamete–macrogamete attachment	P. berghei		van Dijk et al., 2001
PSOP1, 2, 6, 7, 12	Ookinete‐secreted proteins	P. berghei		Kaneko et al., 2015
Puf2	Translational repression of mRNAs	P. falciparum		Miao et al., 2013
SAS‐6	Flagellum formation	P. berghei	M	Marques et al., 2015
SHLP1	Ookinete development	P. berghei	F	Patzewitz et al., 2013
SOAP	Ookinete midgut traversal	P. berghei		Dessens et al., 2003
WARP	Ookinete midgut traversal	P. berghei		Yuda et al., 2001; Li et al., 2004

Proteins specifically expressed in male (M) or female (F) sexual stages. ABS, asexual blood stages; Ca²⁺, calcium ion; CDC20, cell division cycle protein 20; CDPK, calcium‐dependent protein kinase; CelTOS, cell‐traversal protein for ookinetes and sporozoites; cGMP, cyclic guanosine monophosphate; CITH, homolog of worm CAR‐I and fly Trailer Hitch; CTRP, circumsporozoite and thrombospondin‐related adhesive protein‐related protein; DAG, diacylglycerol; DHHC2, palmitoyl‐S‐acyl‐transferase; DOZI, development of zygote inhibited; EM, erythrocyte membrane; FACT‐L, facilitates chromatin transcription protein L; GAK, cyclin G‐associated kinase; GAP, glideosome‐associated protein; GC, gametocyte; GCα/β, guanylyl cyclase; GCS1/HAP2, generative cell specific 1; GEST, gamete egress and sporozoite traversal; IMC, inner membrane complex; IP₃, inositol triphosphate; ISP, IMC sub‐compartment proteins; LCCL, Limulus coagulation factor C; Map‐2, Mitogen‐activated protein kinase 2; MDV‐1/Peg3, male development‐1/protein of early gametocyte 3; Nek, NIMA‐related kinase; PDE, phosphodiesterase; P. f., Plasmodium falciparum; PI, phosphatidyl‐1D‐myo‐inositol; PI4K, phosphatidylinositol 4‐kinase; PI4P, phosphatidylinositol 4‐phosphate; PIP₂, phosphatidylinositol‐4,5‐bisphosphate; PIP5K, phosphatidylinositol 4‐phosphate 5‐kinase; PI‐PLC, phosphoinositide‐specific phospholipase C; PK7, protein kinase 7; PKG, cGMP‐dependent protein kinase; POS, putative ookinete surface‐associated protein; PPKL, kelch‐like domain‐containing phosphatase; PPLP, plasmodial perforin‐like protein; PPM, metallo‐dependent protein phosphatase; PSOP, putative secreted ookinete protein; Puf2, Pumilio/FBF (fem‐3 binding factor) family protein 2; PV, parasitophorous vacuole; SAS‐6; centriole/basal body protein; SHLP1; Shewanella‐like protein phosphatase 1; SOAP, secreted ookinete adhesive protein; TEP1, thioesther‐containing protein 1; WARP, von Willebrand factor A domain‐related protein.