Comparative genomic analysis suggests that the sperm-specific sodium/proton exchanger and soluble adenylyl cyclase are key regulators of CatSper among the Metazoa

Abstract

Background CatSper is a sperm-specific calcium ion (Ca 2+ ) channel, which regulates sperm flagellar beating by tuning cytoplasmic Ca 2+ concentrations. Although this Ca 2+ channel is essential for mammalian fertilization, recent bioinformatics analyses have revealed that genes encoding CatSper are heterogeneously distributed throughout the eukaryotes, including vertebrates. As this channel is activated by cytoplasmic alkalization in mammals and sea urchins, it has been proposed that the sperm-specific Na + /H + exchanger (sNHE, a product of the SLC9C gene family) positively regulates its activity. In mouse, sNHE is functionally coupled to soluble adenylyl cyclase (sAC). CatSper, sNHE, and sAC have thus been considered functionally interconnected in the control of sperm motility, at least in mouse and sea urchin. Results We carried out a comparative genomic analysis to explore phylogenetic relationships among CatSper, sNHE and sAC in eukaryotes. We found that sNHE occurs only in Metazoa, although sAC occurs widely across eukaryotes. In animals, we found correlated and restricted distribution patterns of the three proteins, suggesting coevolution among them in the Metazoa. Namely, nearly all species in which CatSper is conserved also preserve sNHE and sAC. In contrast, in species without sAC, neither CatSper nor sNHE is conserved. On the other hand, the distribution of another testis-specific NHE (NHA, a product of the SLC9B gene family) does not show any apparent association with that of CatSper. Conclusions Our results suggest that CatSper, sNHE and sAC form prototypical machinery that functions in regulating sperm flagellar beating in Metazoa. In non-metazoan species, CatSper may be regulated by other H + transporters, or its activity might be independent of cytoplasmic pH. Electronic supplementary material The online version of this article (10.1186/s40851-019-0141-3) contains supplementary material, which is available to authorized users.

De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: molecular mechanisms underlying scleractinian gametogenesis

“…5, Table 5). These findings support the hypothesis of Romero and Nishigaki that CatSper3, sNHE, and sAC form prototypical machinery for sperm flagellar beating in metazoans [87]. This study further identified the gene encoding creatine kinase, flagellar, which was first identified from flagella of sea urchin sperm, participating in energy transport from sperm heads to the flagella during sperm motility [89].…”

“…Spermiogenesis is a process by which haploid spermatids undergo a complex series of morphological changes, and eventually become elongated functional sperm. The Testis-specific serine/threonine-protein kinase 1 CL2440.Contig1_All [78,79] Testis-specific serine/threonine-protein kinase 2 Unigene8363_All [78,79] Outer dense fiber protein 2 CL11766.Contig4_All [80] Alstrom syndrome protein 1 CL2440.Contig1_All [81] Radial spoke head 1 homolog CL2440.Contig1_All [82] Dynein regulatory complex protein 9 CL4871.Contig6_All [83] Sperm motility/capacitation Dynein regulatory complex subunit 7 CL8060.Contig33_All [86] Sodium/hydrogen exchanger 10 CL11505.Contig1_All [87] Creatine kinase, flagellar CL12240.Contig1_All [88] Adenylate cyclase type 10 CL1089.Contig3_All [87] Cation channel sperm-associated protein 3 Unigene27629_All [87] Cyclin-F Unigene55093_All [89] Dynein regulatory complex subunit 4 Unigene7541_All [90] Chromosome structure Histone H2A CL4659.Contig4_All [120] Fertilization process Hapless 2 CL1879.Contig3_All [109,110] Receptor guanylate cyclases CL4659.Contig4_All [22] Cyclic nucleotide-gated channel cone photoreceptor subunit alpha CL3457.Contig2_All [153] Steroidogenesis Steroid 17-alpha-hydroxylase/17,20 lyase Unigene38823_All [104] presence of spermaries having both round spermatids and mature sperm in testes collected in June 2017 suggested that spermiogenesis was occurring in the testes at the time of collection, and that genes involved in regulation of spermiogenesis were being expressed in testes.…”

“…Molecules regulating flagellar motility still remain largely unexplored in scleractinians. This study identified a number of important genes encoding proteins involved in sperm motility and/or capacitation in mammals and sea urchins, such as cation channel spermassociated protein 3 (CatSper3), sodium/hydrogen exchanger (sNHE), and adenylate cyclase type 10 (sAC) [86][87][88][89][90] (Fig. 5, Table 5).…”

De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: Molecular mechanisms underlying scleractinian gametogenesis

“…5, Table 5). These ndings support the hypothesis of Romero and Nishigaki that CatSper3, sNHE, and sAC form prototypical machinery for sperm agellar beating in metazoans [76]. This study further identi ed the gene encoding creatine kinase, agellar, which was rst identi ed from agella of sea urchin sperm, participating in energy transport from sperm heads to the agella during sperm motility [77].…”

Bisphenol A Diglycidyl Ether (BADGE) and Progesterone Do Not Induce Ca2+ Signals in Boar Sperm Cells

“…The CatSper Ca 2+ channel is a sperm specific Ca 2+ channel highly conserved in mammals (Cai and Clapham, 2008), but also present in a wide range of other species (Romero and Nishigaki, 2019). Ca 2+ signaling is a key regulator of sperm function and CatSper thus controls important sperm functions (Lishko et al, 2012).…”