Ca²⁺-regulated exocytosis is ubiquitous among eukaryotes. This signaling paradigm regulates an array of processes such as neurotransmitter release in neurons, hormone secretion in endocrine cells, and histamine secretion in mast cells (Pang and Südhof, 2010). Ca²⁺-regulated exocytosis is also critical for apicomplexan parasites that are the causative agents of rampant, life-threatening diseases, including malaria, toxoplasmosis, and cryptosporidiosis (Havelaar et al., 2015). Central to their pathogenesis is their ability to transition from intracellular replicative stages to extracellular motile stages, which involves a unique form of cellular movement called gliding, egress from the primary host cell, and invasion into a new host. These processes are driven by the Ca²⁺-regulated exocytosis of apicomplexan-specific membrane-bound organelles called micronemes and rhoptries.

The sequential exocytosis of micronemes and rhoptries is required to promote extracellular motile stages of the parasite (Blader et al., 2016; Carruthers and Sibley, 1997). Micronemes are localized to the parasite apex and their positioning is dependent on cortical microtubules, ultrastable filaments that polymerize down the length of the parasite (Chen et al., 2015; Leung et al., 2017; Wang et al., 2021). Exocytosis of microneme cargo enables host cell rupture by releasing perforin-like proteins during egress and translocation of exposed adhesins required for gliding and attachment to new host cells (Carruthers and Sibley, 1997; Carruthers and Tomley, 2008; Kafsack et al., 2009). Multiple microneme proteins, including the associated cysteine repeat modular proteins (CRMP) complex, are also required to trigger the exocytosis of rhoptries upon host cell contact (Kessler et al., 2008; Sidik et al., 2023; Singer et al., 2023; Sparvoli et al., 2022). Rhoptry proteins include effectors that modulate host responses and transmembrane proteins that are embedded into the host plasma membrane to enable active invasion (Bradley and Sibley, 2007; Lamarque et al., 2011; Lamarque et al., 2014; Ong et al., 2010; Tyler et al., 2011). Intracellular Ca²⁺ release is necessary and sufficient to trigger the rapid trafficking and exocytosis of micronemes (Carruthers et al., 1999a; Carruthers et al., 1999b; Endo et al., 1982; Sidik et al., 2016b). While Ca²⁺ is also necessary for rhoptry discharge, discharge relies on additional cellular processes such as microneme exocytosis (Coleman et al., 2018; Segev-Zarko et al., 2022). While the exocytosis of micronemes and rhoptries is known to be critical for parasite motility, the mechanisms linking Ca²⁺ signaling to their trafficking and fusion to the plasma membrane are still unclear.

Ca²⁺ signals in apicomplexans are primarily transduced by Ca²⁺-dependent protein kinases (CDPKs) (Billker et al., 2009; Farrell et al., 2012; Garrison et al., 2012; Kumar et al., 2017; Lourido et al., 2012; Lourido et al., 2010; Lourido and Moreno, 2015; Luo et al., 2005; Márquez-Nogueras et al., 2021; McCoy et al., 2012; Sebastian et al., 2012). CDPKs are serine/threonine protein kinases that are unique to apicomplexans and plants. CDPKs are activated by directly binding to Ca²⁺, in contrast to Ca²⁺/calmodulin-dependent protein kinases (CaMKs) found in animals, which are indirectly regulated by Ca²⁺-bound calmodulin (CaM) (Ojo et al., 2010; Wernimont et al., 2010). CDPKs are crucial for apicomplexan infection—yet are absent from mammals—making them attractive drug targets; however, their mechanisms of action are still not well understood at a cellular and molecular level. In Toxoplasma gondii, Ca²⁺-dependent protein kinase 1 (CDPK1) is required for the Ca²⁺-regulated exocytosis of micronemes, impacting all steps of parasite motility, including egress, gliding, and invasion (Lourido et al., 2010). Small-molecule competitive inhibitors of CDPK1 have been identified and have shown some activity against T. gondii (Doggett et al., 2014; Johnson et al., 2012; Lourido et al., 2013b; Lourido et al., 2010; Winzer et al., 2015). Identifying the signaling pathways regulated by CDPK1 could reveal the pathways controlling microneme and rhoptry exocytosis.

The Ca²⁺ that activates CDPK1 and other cellular processes is released from intracellular stores following cyclic nucleotide–mediated activation of protein kinase G (PKG) (Bisio and Soldati-Favre, 2019; Brown et al., 2017; Sidik et al., 2016a). This process can be artificially induced by treating parasites with cGMP specific phosphodiesterase (PDE) inhibitors zaprinast or BIPPO that indirectly activate PKG (Figure 1A; Lourido et al., 2012; Nofal et al., 2022; Sidik et al., 2016a; Yuasa et al., 2005). PDE inhibition activates PKG within seconds and triggers the Ca²⁺ and lipid signaling nodes controlling parasite motility, including the exocytosis of micronemes (Figure 1A; Lourido et al., 2012; Yuasa et al., 2005). The identity of the CDPK1 substrates that contribute to the regulation of microneme exocytosis remains unknown. Determining CDPK1-dependent phosphorylation is challenging because the signaling pathways controlling parasite motility are rapid and integrate signals from multiple kinases.

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Global phosphoproteomic studies of apicomplexans found that Ca²⁺-dependent phosphorylation encapsulated proteins involved in signal transduction, motility, exocytosis, and the cytoskeleton, as well as those with unknown functions; however, the functional relevance and organization of these proteins—especially CDPK1—in regulating exocytosis remain unclear (Herneisen et al., 2022; Invergo et al., 2017; McCoy et al., 2012; Nofal et al., 2022; Treeck et al., 2014). Here, we utilized time-resolved phosphoproteomics and chemical genetics to identify 163 proteins phosphorylated by CDPK1. Our comprehensive analysis of CDPK1 not only identified phosphoregulation of known factors involved in parasite motility, but also revealed new regulators of exocytosis. We identified a conserved HOOK complex that is phosphorylated by CDPK1 and is required for microneme exocytosis by mediating the rapid trafficking of micronemes during parasite motility.

In this study, we sought to identify new regulators of Ca²⁺-mediated exocytosis in T. gondii by studying the targets of a key regulator, the kinase CDPK1. We identified 163 proteins phosphorylated in a CDPK1-dependent manner using sub-minute resolution phosphoproteomics and thiophosphorylation for direct substrate capture. We determined that myristoylation of CDPK1 contributes to the kinase’s function during the lytic cycle. Thirteen of the identified CDPK1 targets have previously described functions in parasite motility, revealing possible points of regulation within relevant signaling pathways. Furthermore, we characterized a new regulator of microneme exocytosis called HOOK, which forms a stable complex with FTS and two other proteins. Homologs of HOOK and FTS participate in dynein-mediated vesicular trafficking in other organisms. In T. gondii, knockdown of HOOK or FTS blocked invasion of host cells and altered rapid microneme trafficking during Ca²⁺-regulated motility. Overall, we show how studying parasite signaling pathways can illuminate the cellular adaptations that support parasitism.

Over the past decade, several efforts have sought to characterize phosphorylation within apicomplexans. Improvements in phosphopeptide enrichment and mass spectrometry have enabled global characterization of the phosphoproteomes from T. gondii tachyzoites and Plasmodium falciparum schizonts, trophozoites, and ring-stages (Lasonder et al., 2012; Pease et al., 2013; Solyakov et al., 2011; Treeck et al., 2011). Coupling such approaches with genetic and pharmacological tools has enabled the deconvolution of kinase-specific effects from the vast global phosphorylation program (Bhappu et al., 2020; Fang et al., 2017; Invergo et al., 2017; Nofal et al., 2022; Pease et al., 2018; Treeck et al., 2014), revealing the activation of MyoA-mediated gliding by TgCDPK3, the roles of PbCDPK4 and PbSRPK1 during male gametogenesis, and the erythrocytic-stage effects of PfCDPK1, PfPK7, and PfCDPK5 (Bhappu et al., 2020; Fang et al., 2017; Gaji et al., 2015; Invergo et al., 2017; Pease et al., 2018; Tang et al., 2014). Attributing individual phosphorylation events to specific kinases can be complicated by cumulative changes or adaptation of the signaling networks in knockouts. Chemical-genetic approaches can more precisely inhibit the activity of a given kinase at the time of the assay, while controlling for off-target effects, and have been used to characterize PfPKG-dependent phosphorylation (Alam et al., 2015; Brochet et al., 2014). Kinetically resolved phosphoproteomics has enabled a more nuanced understanding of signaling cascades during parasite motility (Herneisen et al., 2022; Invergo et al., 2017; Nofal et al., 2022). While such technical advances have led to more in-depth phosphoproteome mapping, identifying the direct targets of a given kinase remains a key challenge to structuring the observed changes into signaling pathways.

To resolve direct and indirect effects on the phosphoproteome for T. gondii CDPK1, we combined two complementary approaches: temporally resolved phosphoproteomics and bio-orthogonal labeling of direct substrates. We implemented several methodological advances. Conditional knockdown using the auxin-inducible degron system (Brown et al., 2018a) resulted in rapid and specific depletion of the kinase of interest for the phosphoproteomic studies (Brown et al., 2018a). Additionally, quantification and coverage by mass spectrometry were improved through TMTpro multiplexing and ion mobility spectrometry (FAIMS) (Bekker-Jensen et al., 2020; Li et al., 2020). We also improved on the low coverage observed in previous thiophosphorylation experiments with parasite lysates (Fang et al., 2017; Lourido et al., 2013a) by maintaining a more native signaling environment using aerolysin semi-permeabilization, SILAC-based peptide quantification, and shortened labeling times (Rothenberg et al., 2016). These approaches characterize proteome-wide phosphorylation kinetics in live parasites and reveal direct kinase–substrate relationships for CDPK1.

We observed that myristoylation of CDPK1 contributes to its function. Contrary to previous reports describing the kinase as cytosolic or nuclear (Ojo et al., 2010; Pomel et al., 2008), we demonstrate that myristoylated CDPK1 is at least partially associated with structures that can be fractionated from the cytoplasm by differential centrifugation. Loss of myristoylation led to CDPK1 release from the insoluble fraction. The ortholog of CDPK1 in Plasmodium berghei, PbCDPK4, also displays myristoylation-specific functions during male gametogenesis: myristoylated PbCDPK4 is critical for the first genome replication, whereas the non-myristoylated PbCDPK4 is important for the completion of gametogenesis (Fang et al., 2017). Myristoylation could impact CDPK1’s ability to access certain targets efficiently. However, such interactions appear to be too weak or transient to be captured by immunoprecipitation. Mutating the myristoylation site of CDPK1 only modestly affected ionophore-induced egress. However, minor effects in these key transitions may be magnified over repeated lytic cycles, which could explain the more substantial impact of losing CDPK1 myristoylation on plaque formation. Alternatively, other kinases may compensate for decreased CDPK1 activity, particularly under hyperactivated conditions like stimulated egress. A plausible candidate for compensation is CDPK2A, which also appears to be myristoylated and was recently shown to display epistatic interactions with CDPK1 (Broncel et al., 2020; Shortt et al., 2022).

CDPK1 plays a critical role in the transition from the replicative intracellular stages to motile extracellular stages (Lourido et al., 2010; Shortt et al., 2022). During this transition, parasites must execute rapid cellular changes that involve the exocytosis of micronemes and rhoptries, reorganization of the cytoskeleton, gliding motility, and maintenance of ion homeostasis (Blader et al., 2016). CDPK1 has also been suggested to control the actomyosin system and extrusion of the conoid (Tosetti et al., 2019). Our detailed target analysis suggests CDPK1 regulates—and possibly helps coordinate—multiple pathways. We revealed over a hundred CDPK1 targets with diverse predicted functions, including many relevant to phenotypes dependent on CDPK1. In addition to the effects on microneme trafficking, our results point to a direct link between CDPK1 and rhoptry exocytosis. Ca²⁺ has been implicated in rhoptry discharge, as the rhoptry-localized Ca²⁺-binding FER2 is required for rhoptry exocytosis (Coleman et al., 2018). We observed a preponderance of CDPK1-dependent phosphorylation on proteins regulating rhoptry exocytosis, including DHHC7, ARO, and AIP. Phosphorylation on ARO was observed near the N-terminal acylation sites required for rhoptry targeting and may regulate the bundling and positioning of mature rhoptries during motile stages (Mueller et al., 2016). However, formally demonstrating the relationship between Ca²⁺/CDPK1 and rhoptry discharge is complicated by the dependency of the latter on the secretion of certain microneme proteins (Ben Chaabene et al., 2021; Carruthers and Sibley, 1997). T. gondii tachyzoites have several rhoptries, yet only two are docked for exocytosis at a given time (Aquilini et al., 2021; Mageswaran et al., 2021; Segev-Zarko et al., 2022). Regulating the activity of ARO during motile stages may influence the ability to mobilize and re-dock rhoptries in preparation for invasion. Considering how different CDPK1 substrates function, we expect the various phenotypes associated with CDPK1 will depend on distinct sets of substrates.

Although CDPK1 is known to mediate microneme exocytosis (Lourido et al., 2010), the precise molecular events controlling this process have remained elusive. In this study, we determined that CDPK1 activity is required for the Ca²⁺-stimulated trafficking of micronemes to the apical end. This phenotype depends on HOOK, one of the CDPK1 targets uncovered by both global phosphoproteomics and thiophosphorylation studies. Despite prior annotation as a microneme protein (Butler et al., 2014), HOOK likely functions as an activating adaptor in T. gondii based on homology to other Hook proteins and the functional characterization we have performed. Phosphorylation has been reported to regulate the function of activating adaptors. In HeLa cells, phosphorylation of BICD2 facilitates recruitment of dynein and dynactin (Gallisà-Suñé et al. 2023). Analogously, phosphorylation of JIP1 mediates the switch between kinesin and dynein motility of autophagosomes in murine neurons (Fu et al., 2014). We therefore speculate that phosphorylation of HOOK by CDPK1 may activate the adaptor by promoting its interaction with dynein and dynactin to initiate trafficking of micronemes.

Immunoprecipitation of HOOK identified three interacting proteins: FTS, TGGT_316650, and TGGT1_306920. In Homo sapiens, Aspergillus nidulans, and D. melanogaster, Hook proteins complex with FTS and FHIP (the FHF complex), to link cargo to the dynein machinery for trafficking along microtubules (Bielska et al., 2014; Gillingham et al., 2014; Guo et al., 2016; Xu et al., 2008; Yao et al., 2014). FHF complexes have been shown to recognize early endosomes via FHIP binding to RAB5 (Bielska et al., 2014; Guo et al., 2016; Zhang et al., 2014). Homology to FHIP was lacking in TGGT1_316650 and TGGT1_306920. However, genome-wide knockout screens indicate TGGT1_306920 is critical for parasite fitness, leading us to speculate that it may mediate cargo binding in a manner structurally distinct from known adaptors. Additional work will be needed to elucidate the function of the HOOK complex and to understand how it mediates trafficking of apicomplexan-specific organelles.

Our results place the HOOK complex downstream of CDPK1, regulating the stimulated relocalization of micronemes to the apical end of parasites. However, the HOOK complex only partially explains CDPK1’s role during egress. Whereas CDPK1 depletion blocks egress entirely, parasites depleted of HOOK or FTS exit host cells, despite subsequent defects in microneme secretion and invasion. Microneme discharge is required for egress, supplying adhesins for gliding motility and the perforin PLP1 to rupture the parasitophorous vacuole membrane (Kafsack et al., 2009). It therefore appears that the initial round of microneme discharge during egress depends on CDPK1, and only subsequent rounds require the HOOK complex. Indeed, a fraction of micronemes are already found docked at the apical complex prior to the transition from the replicative to the motile stages, and may constitute the first round of microneme exocytosis (Mageswaran et al., 2021; Sun et al., 2022). Ferlin 1 (FER1) was recently shown to be involved in microneme positioning and overexpression of FER1 was sufficient to initiate an initial round of microneme exocytosis and induce egress (Tagoe et al., 2020). Dynein-mediated trafficking might become important immediately following egress when continuous microneme discharge is necessary, as is the case during gliding motility and invasion. Consistent with this hypothesis, depletion of the dynein light chain 8a (DLC8a) yielded similar phenotypes to HOOK and FTS knockdown: intact egress but dysfunctional microneme protein secretion, gliding motility, and invasion (Lentini et al., 2019). Loss of DLC8a also led to defects in rhoptry positioning, which were not observed in HOOK knockdowns (Lentini et al., 2019), so other activating adaptors may be involved in rhoptry trafficking. Our results suggest that the HOOK complex has been specifically adapted for microneme trafficking in T. gondii.

Several aspects of microneme trafficking remain to be determined. The precise nature of the dynein complex is poorly understood. Eukaryotes typically express a single cytoplasmic dynein heavy chain. In T. gondii, TGGT1_294550 is the top candidate for the cytoplasmic dynein heavy chain (DHC) as it contains the necessary domains, is conserved among apicomplexans, and is required for parasite fitness (Lentini et al., 2019; Sidik et al., 2016b). Other putative DHCs in the T. gondii genome are likely axonemal dyneins required for flagellar function in sexual-stage parasites. Two putative plus-end motors have been characterized in T. gondii. KinesinA localizes to the apical polar ring where cortical microtubules emanate from and is required for ring stability and parasite motility (Leung et al., 2017). In contrast, KinesinB localizes to the distal two-thirds of the cortical microtubules but is dispensable for the lytic cycle (Leung et al., 2017). Motile parasites depleted of HOOK mislocalized micronemes to the distal two-thirds of the cortical microtubules. We hypothesize that KinesinB, which is also a target of CDPK1, may maintain the association between micronemes and microtubules in the absence of HOOK. It also remains unknown how the HOOK complex binds to micronemes. In H. sapiens and D. melanogaster, RAB5 on vesicles interacts with FHIP in the HOOK complex (Bielska et al., 2014; Gillingham et al., 2014; Guo et al., 2016; Xu et al., 2008; Yao et al., 2014). We speculate that TGGT1_306920 may serve the role of FHIP within the HOOK complex as it is fitness conferring, whereas TGGT1_316650 appears dispensable but the complex’s binding partner on micronemes remains unknown. RAB5A and RAB5C have been implicated in the biogenesis of micronemes, but their roles during exocytosis have not been explored (Kremer et al., 2013). Understanding how micronemes are recognized may elucidate how cargo specificity is achieved and regulated.

Ca²⁺ signaling has been tuned to support apicomplexan-specific cellular processes but identifying and integrating effectors within the pathway has remained a major bottleneck. Signaling effectors conserved amongst eukaryotes are often integrated into apicomplexan cellular pathways in novel or unusual ways. Here, we identified candidate downstream effectors of the Ca²⁺-regulated kinase CDPK1 by monitoring proteome-wide protein phosphorylation. In addition to creating a catalog of candidates for future characterization, we identified, characterized, and integrated the HOOK complex downstream of CDPK1 within the Ca²⁺ signaling network controlling microneme exocytosis. Lastly, our results are the first to implicate activating adaptors as critical factors for the pathogenesis of an apicomplexan organism by promoting exocytic trafficking.

All mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository. Accession numbers are listed in the appropriate ‘Materials and methods’ sections and here: Sub-minute resolution phosphoproteomics (PXD039426), Immunoprecipitation of cWT and cMut (PXD044081), Thiophosphorylation of CDPK1 substrates (PXD039431), Immunoprecipitation of HOOK and FTS (PXD039432), Immunoprecipitation of TGGT1_306920 (PXD044080), and Proximity labeling FTS-TurboID (PXD039434). Most sequences of cloning vectors generated for this study have been deposited in GenBank, as listed in Supplementary file 10. Custom analysis scripts in the R computing language are available in Supplementary file 11 (Sub-minute resolution phosphoproteomics) and Supplementary file 12 (Thiophosphorylation of CDPK1 substrates). Strains and plasmids generated for this study can be obtained by emailing the corresponding author.

1. 1. Chan AW

   (2023) PRIDE

   ID PXD039426. Analysis of CDPK1 targets identifies a trafficking adaptor complex that regulates microneme exocytosis in Toxoplasma.

   https://www.ebi.ac.uk/pride/archive/projects/PXD039426
2. 1. Chan AW

   (2023) PRIDE

   ID PXD044081. Analysis of CDPK1 targets identifies a trafficking adaptor complex that regulates microneme exocytosis in Toxoplasma - cWT and cMut IPs.

   https://www.ebi.ac.uk/pride/archive/projects/PXD044081
3. 1. Chan AW

   (2023) PRIDE

   ID PXD039431. Analysis of CDPK1 targets identifies a trafficking adaptor complex that regulates microneme exocytosis in Toxoplasma - Thiophosphorylation.

   https://www.ebi.ac.uk/pride/archive/projects/PXD039431
4. 1. Chan AW

   (2023) PRIDE

   ID PXD039432. Analysis of CDPK1 targets identifies a trafficking adaptor complex that regulates microneme exocytosis in Toxoplasma - HOOK and FTS IPs.

   https://www.ebi.ac.uk/pride/archive/projects/PXD039432
5. 1. Chan AW

   (2023) PRIDE

   ID PXD044080. Analysis of CDPK1 targets identifies a trafficking adaptor complex that regulates microneme exocytosis in Toxoplasma - TGGT1_306920 IPs.

   https://www.ebi.ac.uk/pride/archive/projects/PXD044080
6. 1. Chan AW

   (2023) PRIDE

   ID PXD039434. Analysis of CDPK1 targets identifies a trafficking adaptor complex that regulates microneme exocytosis in Toxoplasma - FTS TurboID.

   https://www.ebi.ac.uk/pride/archive/projects/PXD039434

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Author details

1. Alex W Chan

   1. Whitehead Institute for Biomedical Research, Cambridge, United States
   2. Biology Department, Massachusetts Institute of Technology, Cambridge, United States

   Contribution

   Conceptualization, Formal analysis, Validation, Investigation, Methodology, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5444-5756

2. Malgorzata Broncel

   Signaling in Apicomplexan Parasites Laboratory, The Francis Crick Institute, London, United Kingdom

   Contribution

   Formal analysis, Validation, Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2991-3500

3. Eden Yifrach

   Whitehead Institute for Biomedical Research, Cambridge, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5074-0048

4. Nicole R Haseley

   Whitehead Institute for Biomedical Research, Cambridge, United States

   Contribution

   Formal analysis, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9346-2161

5. Sundeep Chakladar

   Whitehead Institute for Biomedical Research, Cambridge, United States

   Contribution

   Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

6. Elena Andree

   Whitehead Institute for Biomedical Research, Cambridge, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

7. Alice L Herneisen

   1. Whitehead Institute for Biomedical Research, Cambridge, United States
   2. Biology Department, Massachusetts Institute of Technology, Cambridge, United States

   Contribution

   Resources, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3368-0893

8. Emily Shortt

   Whitehead Institute for Biomedical Research, Cambridge, United States

   Contribution

   Resources

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0009-7625-4772

9. Moritz Treeck

   Signaling in Apicomplexan Parasites Laboratory, The Francis Crick Institute, London, United Kingdom

   Contribution

   Resources, Supervision, Funding acquisition, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9727-6657

10. Sebastian Lourido

    1. Whitehead Institute for Biomedical Research, Cambridge, United States
    2. Biology Department, Massachusetts Institute of Technology, Cambridge, United States

    Contribution

    Conceptualization, Resources, Supervision, Funding acquisition, Methodology, Writing - review and editing

    For correspondence

    lourido@wi.mit.edu

    Competing interests

    Reviewing editor, eLife

    "This ORCID iD identifies the author of this article:" 0000-0002-5237-1095

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