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Reproduction (2005) 130 157-163
DOI: 10.1530/rep.1.00707
Copyright © 2005 Society for Reproduction and Fertility
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RESEARCH

Phospholipase C{zeta}, the trigger of egg activation in mammals, is present in a non-mammalian species

K Coward, C P Ponting1, H-Y Chang2, O Hibbitt, P Savolainen3, K T Jones2 and J Parrington

Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3QT, UK, 1 MRC Functional Genetics Unit, Department of Human Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, UK, 2 Cell and Developmental Physiology Research Group, Institute for Cell and Molecular Biosciences, The Medical School, Framlington Place, University of Newcastle NE2 4HH, UK and 3 Department of Biotechnology, Royal Institute of Technology, SE-10691 Stockholm, Sweden

Correspondence should be addressed to K Coward; Email: kevin.coward{at}pharm.ox.ac.uk


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
The activation of the egg to begin development into an embryo is triggered by a sperm-induced increase in intracellular egg Ca2+. There has been much controversy about how the sperm induces this fundamental developmental event, but recent studies suggest that, in mammals, egg activation is triggered by a testis-specific phospholipase C: PLC{zeta}. Since the discovery of PLC{zeta}, it has been unclear whether its role in triggering egg activation is common to all vertebrates, or is confined to mammals. Here, we demonstrate for the first time that PLC{zeta} is present in a non-mammalian vertebrate. Using genomic and cDNA databases, we have identified the cDNA encoding a PLC{zeta} orthologue in the domestic chicken that, like the mammalian isoforms, is a testis-specific gene. The chicken PLC{zeta} cDNA is 2152 bp in size and encodes an open reading frame of 639 amino acids. When injected into mouse oocytes, chicken PLC{zeta} cRNA triggers Ca2+ oscillations, indicating that it has functional properties similar to those of mammalian PLC{zeta}. Our findings suggest that PLC{zeta} may have a universal role in triggering egg activation in vertebrates.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
Activation of the egg by the sperm is a fundamental developmental event that frees the egg from its state of cell-cycle arrest, allows metabolism to resume, and acts as a block to polyspermy. In almost all species studied, egg activation is induced by an increase in the concentration of intracellular calcium ions (Ca2+) (Stricker 1999). However, the mechanism whereby the sperm triggers the release of Ca2+ in the egg has been a subject of controversy over recent decades, with opinion divided as to whether egg activation is initiated by a surface interaction between a sperm ligand and an egg receptor, or by a cytosolic ‘sperm factor’ that is released into the egg from the sperm during gamete fusion (Evans & Kopf 1998, Swann & Parrington 1999).

Recent studies suggest that the mammalian sperm factor is a sperm-specific phospholipase C, PLC{zeta}, that has the expected properties of the physiological agent of egg activation. For example, when injected into mouse oocytes, recombinant mouse PLC{zeta}, cRNA (Saunders et al. 2002) or protein (Kouchi et al. 2004), triggers Ca2+ oscillations identical to those seen at fertilization, whereas immunodepletion of endogenous PLC{zeta} from sperm extracts removes their ability to cause the release of Ca2+ (Saunders et al. 2002). PLC{zeta} also has other distinctive properties, such as its high Ca2+ sensitivity (Kouchi et al. 2004) and a propensity to accumulate in the pronucleus of the zygote (Larman et al. 2004, Yoda et al. 2004).

PLC{zeta} homologues have been identified in mice, humans and monkeys (Saunders et al. 2002, Cox et al. 2002). However, so far, PLC{zeta} has not been identified other than in eutherian mammals. Therefore, given the nearly universal conservation of a Ca2+ signal at fertilization, a major unanswered question is whether PLC{zeta} has a role only during egg activation in mammals or whether it has a more universal role. There is indirect evidence to suggest that the latter might be the case: when injected into mouse oocytes, sperm extracts from chicken and the clawed frog, Xenopus laevis, trigger Ca2+ oscillations similar to those seen at fertilization (Dong et al. 2000). We have shown further that a sperm protein extract from tilapia, a commercially important teleost (bony) fish, also triggers Ca2+ oscillations when injected into mouse oocytes (Coward et al. 2003). In addition, sperm factor activities have been identified in animals as diverse as marine worms (Stricker 1997) and sea squirts (Kyozuka et al. 1998), although to date there have been no reports that these invertebrate sperm factors can trigger Ca2+ oscillations in mouse oocytes. However, it remains far from clear whether such sperm factor activities are functions of a PLC{zeta} orthologue in these species, or are caused by some completely different signalling protein. In the current study, we demonstrate, for the first time, the existence of a PLC{zeta} orthologue in a non-mammalian vertebrate, the domestic chicken.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Acknowledgements
 References
 
Identification of a chicken PLC{zeta} orthologue in the chicken genome
Murine and human PLC{zeta} protein sequences were used to search the chicken genome database at Ensembl (http://www.ensembl.org/Gallus_gallus/) using BLAST (Altschul et al. 1997). The search identified a novel PLC-like sequence that exhibited strong sequence similarity to mammalian PLC{zeta} and had a similarly conserved syntenic location on the genome. The chicken PLC{zeta} gene was predicted using Genewise (Birney et al. 2004).

Cloning of chicken PLC{zeta}cDNA
A full-length clone (in pSPORT1 vector) was identified from a cDNA library constructed from testis (domestic White Leghorn cockerel, Gallus domesticus; Savolainen et al. 2005) and was fully sequenced by MWG Biotech Ltd (UK) to confirm its identity. The full-length nucleotide sequence was translated into a predicted amino acid sequence with the ExPaSy Molecular Biology Server (Swiss Institute of Bioinformatics; http://ca.expasy.org/). For purposes of comparison, the putative chicken PLC{zeta} was initially compared by constructing a multiple sequence alignment using CLUSTALW (Thompson et al. 1994), with the following sequences (accession numbers in parentheses): monkey PLC{zeta} (Macaca fascicularis; AB070108 [GenBank] ), human PLC{zeta} (NM_033123 [GenBank] ), mouse PLC{zeta} (NM_054066 [GenBank] ). A dendrogram of PLC{zeta} and PLC{delta}1 sequences was then constructed using CLUSTALW and unweighted pair-group method with arithmetic mean methodology. Sequences used in the dendrogram were as follows (accession numbers in parentheses): mouse PLC{zeta} (NM_054066 [GenBank] ), human PLC{zeta} (NM_033123 [GenBank] ), mouse PLC{delta}1 (AAH25798 [GenBank] , human PLC{delta}1 (AAH50382 [GenBank] , chicken PLC{delta}1 (XP_418522 [GenBank] ). The accession number for chicken PLC{zeta} is AY843531 [GenBank] . The domain structure of the putative chicken PLC{zeta} was investigated using SMART (Schultz et al. 1998).

Tissue expression of PLC {zeta}
A range of tissues (testis, heart, liver, kidney, brain, spleen, smooth muscle and gizzard) were collected from a freshly culled domestic White Leghorn (Gallus domesticus) cockerel and were immediately snap-frozen in liquid nitrogen. Total RNA was prepared from each tissue using an RNeasy Kit (Qiagen, UK) in accordance with the manufacturer’s instructions. For PCR analysis, total RNA (5 µg) from each of the harvested tissues was reverse-transcribed into singlestranded cDNA using a Cloned AMV First Strand Synthesis kit (Invitrogen, UK) and amplified with oligonucleotide primers designed to amplify the full-length chicken PLC {zeta} gene: CZ5 (5'-ATGGAGGAGAACAGATGGTTT-3') and CZ3 (5'-GTAGTACCAGACATACACAAA-3') using the Expand High Fidelity PCR System (Roche Diagnostics, UK). For northern blot analysis, 40µg total RNA from each harvested tissue were denatured and fractionated on a 1% formaldehyde RNA gel and blotted onto a Hybond-N+ membrane (Amersham Biosciences, UK) using a vacuum blotter (BioRad, UK). Membranes were subsequently stained with 0.03% methylene blue/0.2 mol/l sodium acetate to visualize RNA and provide a comparison of lane loading. Membranes were incubated for 20 min at 65 °C with Rapid-Hyb Buffer (Amersham Biosciences, UK) and then overnight at 65 °C with a 32P-dCTP-labelled probe (full-length cDNA, prepared using CZ5 and CZ3 oligonucleotides). The probe was labelled with a Megaprime II Labelling System (Amersham Biosciences, UK). After hybridization, the membrane was washed with 50 ml 2 x SSC 0.1% SDS at room temperature, followed by two 15-min washes in 50 ml 1.0–0.1% SSC/0.1% SDS at 65 °C as necessary. Hybridization signals were detected using a Typhoon Phosphor Imaging System (Amersham Biosciences, UK).

Injection of PLC {zeta}cRNA into mouse oocytes
cRNA was synthesized from linearized full-length chicken PLC{zeta} using the mMessage Machine kit (Ambion, Austin, TX, USA) in accordance with the Manufacturer’s instructions. Outbred MF1 mice (Harlan, Bicester, UK) were first super-ovulated with injections of pregnant mares serum gonadotropin and human chorionic gonadotropin and ovulated oocytes harvested. Microinjection of cRNA constructs and fura2 dextran were then carried out as described previously (Madgwick et al. 2004). Injected oocytes were imaged for resultant changes in intracellular Ca2+ on a heated stage fitted to a Nikon TE300 inverted microscope equipped for epi-fluorescence (Jones & Nixon 2000). Images were acquired using a Sony Interline CCD camera controlled by MetaFluor software (Universal Imaging Corp., Downington, PA, USA).


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Acknowledgements
 References
 
Identification of a chicken PLC {zeta} orthologue in the chicken genome
Searches of the chicken genome with murine and human PLC{zeta} protein sequences identified a novel PLC-like sequence that exhibited strong sequence similarity to mammalian PLC{zeta}. This novel chicken PLC was predicted to be a PLC{zeta} orthologue on the basis of its strong sequence similarity to mammalian PLC{zeta} and its conserved syntenic location on the genome. Despite extensive searches, no pleckstrin homology (PH) domain was discernible that was encoded within the chicken PLC{zeta} 5' sequence. The putative chicken PLC{zeta} shares between 55 and 58% amino acid identity and between 70 and 71% similarity to mammalian PLC{zeta} isoforms. A dendrogram was used to demonstrate monophyly among human, macaque, mouse and chicken PLC{zeta} isoforms, with PLC{delta}1 isoforms as outgroup sequences (Fig. 1AGo).



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  		Figure 1 Molecular identification of chicken PLC{zeta}. (A) Dendrogram illustrating monophyly among human, macaque, mouse and chicken PLC{zeta} isoforms, with PLC{delta}1 isoforms as outgroup sequences. The topology of this dendrogram is supported by bootstrap values of 100% at all internal nodes. (B) Conserved synteny for genes flanking chicken PLC{zeta} in chicken (chromosome 1 [chr 1]) and human (chromosome 12 [chr 12]). Gene abbreviations: PIK3C2G, phosphoinositide-3-kinase, class 2, gamma polypeptide; PLCZ1, phospholipase C, {zeta}1; CAPZA3, testis-specific capping protein (actin filament) muscle Z-line, {alpha}3: PEPP2, phosphatidylinositol 3-phosphate-binding PH domain protein 2; AEBP2, Adipocyte enhances (AE) binding protein 2.

 
Further evidence that the chicken gene is a PLC{zeta} orthologue is clearly demonstrated by its genomic location. In the chicken genome, PLC{zeta} is flanked by the same genes as those flanking PLC{zeta} in mammals (Fig. 1BGo). In mammals, PLC{zeta} is located back-to-back with another testis-specific gene, CAPZA3, with which it appears to share a bidirectional promoter containing a putative cAMP responsive element modulator protein recognition site (Hurst et al. 1998). In chickens, PLC{zeta} shares the same back-to-back arrangement with CAPZA3 (Fig. 1BGo), although a chicken sequence similar to the mammalian bidirectional promoter was not discernible.

Cloning of chicken PLC{zeta} cDNA
A full-length clone was identified from a cDNA library constructed from chicken testis tissue (Savolainen et al. 2005). Sequencing of the cDNA clone showed that it was 2152 bp in size and coded for an open reading frame of 639 amino acids. This cDNA sequence was identical to our prediction from the genome, and different in coding exons 1 and 7 compared with a RefSeq prediction (accession XM_416413 [GenBank] .1). Chicken PLC{zeta} has a predicted binding affinity (pI) of 8.53 and a molecular mass of 72.53 kDa. Phylogenetic analysis involving chicken, mouse and human PLC{zeta} isoforms demonstrated that the chicken isoform was the most divergent, as expected (Fig. 1AGo). The domain structure of chicken PLC{zeta} exhibits the same organization as mammalian PLC{zeta} isoforms: a catalytic X-Y domain and a C2 domain, but no PH domain (Fig. 2Go). Catalytically important residues and a putative phosphoinositide (PI) binding site are also shown in Fig. 2Go.



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  		Figure 2 Comparison of chicken PLC{zeta} with mammalian isoforms: multiple amino acid sequence alignment of chicken PLC{zeta} with monkey PLC{zeta}, human PLC{zeta} and mouse PLC{zeta}. Identical residues are indicated by black shading, conserved residues by dark grey shading, and similar residues by light grey shading. {dagger}Catalytically important residues; {ddagger}residues vital for Ca2+ binding; *residue mutated by Saunders et al.(2002) leading to an inability to release Ca2+; #residues forming a putative phosphoinositide binding site (residues 303–310). Sequences of closely spaced bold dots represent the following: EF-hand (residues 48–105), X domain (residues 163–308), Y domain (residues 392–508) and the C2 domain (residues: 528–653).

 
Tissue expression of PLC {zeta}
To investigate the tissue expression of chicken PLC{zeta}, we first searched chicken ‘expressed sequence tag’ (EST) cDNA databases. ESTs (e.g. accession numbers CN232708 [GenBank] , CN231906 [GenBank] ) corresponding to the chicken PLC{zeta} were identified as originating from testis, but were not identifiable from other tissues. This is consistent with a sperm-specific pattern of expression for chicken PLC{zeta}, as seen for mammalian PLC{zeta}. To confirm whether this were the case, we next analysed total RNA for PLC{zeta} transcripts in a panel of chicken tissues using RT-PCR and northern blot assays. Analysis of the RT-PCR product showed a band at the predicted size (2152 bp) only with testis cDNA and the positive control (Fig. 3AGo). Sequencing confirmed that the 2152 bp band was indeed chicken PLC{zeta}. Northern analysis further confirmed that chicken PLC{zeta} was present only in testis, and not in other tissues, and showed that the chicken PLC{zeta} mRNA conformed to its predicted size (Fig. 3BGo).



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  		Figure 3 Tissue expression of chicken PLC{zeta}. (A) Testis-specific expression of chicken PLC{zeta} as detected by RT-PCR. (B) Testis-specific expression of chicken PLC{zeta} as detected by northern blot analysis. Molecular weights are indicated on the vertical axes. T, testis; H, heart; Li, liver; B, brain; Sp, spleen; SM, smooth muscle; Gz, gizzard; (–ve, negative PCR control (distilled water); +ve, positive PCR control (chicken PLC{zeta} cDNA clone).

 
Injection of PLC{zeta} cRNA into mouse oocytes
A key question is whether chicken PLC{zeta} is functionally equivalent to its mammalian orthologue. Studying its ability to cause the release of Ca2+ after injection into a chicken oocyte is problematic, because imaging with fluorescent Ca2+-sensitive dyes in the thin layer of cytoplasm at the animal pole where the sperm fuses (Gilbert 2003) is technically challenging. Instead, we chose to assay the ability of chicken PLC{zeta} to cause the release of Ca2+ in a mouse oocyte, because previous studies had demonstrated that recombinant mouse, human and monkey PLC{zeta} cRNA triggered Ca2+ spiking in mouse oocytes (Cox et al. 2002, Saunders et al. 2002). Chicken PLC{zeta} cRNA (1.4–0.02 µg/µl, injected at 0.03–0.1% of oocyte volume) was microinjected into mature mouse oocytes to determine its ability to induce Ca2+ spiking. The procedure of injection into groups of oocytes lasted between 10 and 15 min. When injections were complete and imaging started, it was apparent that all oocytes had initiated Ca2+ spiking (Fig 4A Go,n = 17). The Ca2+ spiking frequency, expressed as the interspike interval at the lowest dose (0.02 µg/µl) was 3.75 ± 1.14 min (n = 5). This high frequency spiking is similar to that reported with human PLC{zeta} at the same dose (4.21 ± 1.79 min; Cox et al. 2002) and similar to that which we observed with 0.01 µg/µl human PLC{zeta} cRNA (Fig. 4BGo; n = 5). As a consequence of the Ca2+ spiking, which is the necessary and sufficient trigger for full oocyte activation (Hyslop et al. 2004), oocytes injected with chicken PLC{zeta} cRNA and monitored for several hours went on to extrude second polar bodies and form pronuclei (75%; n = 12).



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  		Figure 4 Ability of chicken PLC{zeta} to release Ca2+ in the mouse oocyte: Ca2+ oscillations in mouse oocytes microinjected with cRNA prepared from chicken or human PLC{zeta} cDNA clones. (A) 0.02 µg/µl chicken PLC{zeta} cRNA. (B) 0.01 µg/µl human PLC{zeta} cRNA. The volume microinjected was 0.03–0.1% of that of the oocyte.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Acknowledgements
 References
 
In the present study, our principal aim was to identify whether a PLC{zeta} orthologue was present in a non-mammalian species. Until now, PLC{zeta} has been identified only in mice (Saunders et al. 2002), monkeys and humans (Cox et al. 2002). We chose to investigate the chicken because it is one of the few non-mammalian vertebrate species to have had its genome fully sequenced and annotated, and also because birds are phylogenetically closer to mammals than are other vertebrate classes such as fish and amphibians (International Chicken Genome Sequencing Consortium 2004, Schmutz & Grimwood 2004).

The novel PLC-like molecule that we identified appears to be a chicken PLC{zeta} orthologue as judged by the following features. Firstly, it has discrete domains characteristic of a PLC such as an EF-hand domain, X and Y catalytic domains and a C2 domain, along with several catalytically important residues, but no PH domain that is discernible encoded within its genomic sequence. Sequence analysis of a full-length chicken PLC{zeta} clone also confirmed the absence of a PH domain. This supports its identification as a PLC{zeta} orthologue, as the lack of a PH domain distinguishes PLC{zeta} from PLC{delta} isoforms (Cox et al. 2002, Saunders et al. 2002). Secondly, in the chicken genome our PLC-like molecule is clearly flanked by the same genes as those flanking mammalian PLC{zeta} isoforms and thus also probably shares a bidirectional promoter with the testis-specific gene, CAPZA3 (Hurst et al. 1998, Yoshimura et al. 1999, Miyagawa et al. 2002), as is the case with mammalian PLC{zeta}. CAPZA3 appears to be a retrogene that has inserted into the genome next to PLC{zeta} and, presumably, in the process acquired the same testis-specific pattern of expression as PLC{zeta}. Thirdly, phylogenetic analysis showed that chicken PLC{zeta} is clearly more similar to mammalian PLC{zeta} isoforms than it is to chicken PLC{delta}1. Finally, chicken PLC{zeta} appears to have a testis-specific pattern of expression, and recombinant chicken PLC{zeta} cRNA is able to trigger Ca2+ oscillations in mouse oocytes and cause egg activation, just like the mammalian PLC{zeta} isoforms (Cox et al. 2002, Saunders et al. 2002).

The great commercial importance of chickens means there is great interest in identifying causes of subfertility in this species. Currently, very little is known about the mechanism of egg activation in chickens, despite the fact that defects in this process could be a cause of subfertility in cockerels. Our discovery of a PLC{zeta} orthologue in chickens, and the fact that it appears to have functional properties similar to those of mammalian PLC{zeta} and may thus have a similar role, not only is important as a step towards understanding the mechanism of egg activation in this species, but also has potential value as an important molecular marker of male fertility in cockerels.

These findings also have more general relevance for our understanding of the mechanism of egg activation in vertebrates as a whole. Previous studies have shown that an unidentified factor in chicken, frog and fish sperm can trigger Ca2+ oscillations when injected into mouse oocytes (Dong et al. 2000, Coward et al. 2003). However, it was not clear from those studies whether this ability to cause the release of Ca2+ was attributable to a PLC{zeta} orthologue or to a different signalling protein. Our identification of a chicken orthologue of PLC{zeta} with a pattern of expression and properties similar to those of mammalian PLC{zeta} suggests that PLC{zeta} may also be present in the sperm of fish and frogs, and may have a universal role during egg activation in vertebrates.


   Acknowledgements
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
References
 
This study was funded by a Medical Research Council (MRC) Non-Clinical Senior Fellowship awarded to JP and a Wellcome Trust project grant to KTJ. CPP is funded by the MRC. The author(s) declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.


   Footnotes
 
Received 23 February 2005
First decision 24 March 2005
Revised manuscript received 22 April 2005
Accepted 6 May 2005


   References
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 Introduction
 Materials and Methods
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 Discussion
 Acknowledgements
 References
 

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