Ancestral Ca2+ Signaling Machinery in Early Animal and Fungal Evolution

Cai, Xinjiang; Clapham, David E.

doi:10.1093/molbev/msr149

Cited by 90 publications

(122 citation statements)

References 74 publications

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“…To further explore the origin of the Ca 2+ signaling machinery, we have more recently reported the examination of several genomes at the Origins of Multicellularity Database [14,15], the Broad Institute and the NCBI genomic databases including the genomes of three basal fungi Allomyces macrogynus, Spizellomyces punctatus, and Batrachochytrium dendrobatidis [16]. Surprisingly, our analysis revealed the presence of P2X receptor homologs in the three basal fungi (AmaP2X, SpuP2X, and BdeP2X) ( Fig.…”

mentioning

confidence: 87%

“…2). Fungal P2X receptor homologs also show sequence divergence, possibly reflecting lineage-specific adaptation [16]. For instance, as shown in Fig.…”

mentioning

confidence: 95%

“…For instance, as shown in Fig. 2, basal fungal P2X receptor homologs contain a Glu residue in the second transmembrane segment [16], which is conserved as an Asp residue in vertebrate P2X receptors [11].…”

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confidence: 99%

“…In conclusion, the identification of new P2X receptor homologs in basal fungi and primitive species in the animal lineage [16] sheds novel evolutionary and mechanistic insights into the purinergic signaling and provides new …”

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confidence: 99%

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P2X receptor homologs in basal fungi

Cai

2011

Purinergic Signalling

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P2X receptors are ligand-gated ion channels that induce the flux of cations across the membrane when activated by ATP, resulting in membrane depolarization and Ca 2+ entry [1][2][3][4]. In mammals, P2X receptors have been shown to play a critical role in regulating physiological processes in a wide range of cell types such as neurons, glial cells, muscle, endothelial and epithelial cells, osteoclasts, and hematopoietic cells [1,3]. The cloning of the first P2X receptor P2X 1 in 1994 revealed an unusual structure of P2X receptors containing two transmembrane segments [5,6], which is distinct from other ionotropic receptors such as glutamate receptors and acetylcholine receptors [3]. P2X receptors appear to be present in all vertebrate and many invertebrate genomes but are absent in some invertebrates such as Caenorhabditis elegans and Drosophila melanogaster [4,7,8]. It should be noted that C. elegans and D. melanogaster are also known to lack two other Ca 2+ -permeable channelsthe voltage-gated CatSper Ca 2+ channels at the plasma membrane [9] and the two-pore channels underlying NAADP-sensitive Ca 2+ release from acidic Ca 2+ stores [10].ATP is widely utilized as an energy source in many organisms, and so, ATP could serve as an evolutionarily conserved means to mediate cell-cell communications or intracellular signaling through P2X receptors. The emergence of purinergic signaling by P2X receptors is believed to have occurred in early evolution of eukaryotes [4,8], which is supported by the identification and characterization of P2X receptor homologs in non-metazoan organisms such as the dictyostelid social amoeba Dictyostelium discoideum [11], the green alga Ostreococcus tauri [12], and the choanoflagellate Monosiga brevicollis, one of the closet unicellular relatives of animals [12,13]. Interestingly, even though a P2X receptor homolog is characterized in D. discoideum [11], P2X receptor homologs have not been detected in known genomes of fungal species [4,8]. It is generally believed that P2X receptors had been lost in fungi [4,8].We have recently demonstrated in the choanoflagellate M. brevicollis the presence of extensive Ca 2+ signaling and amplification pathways, most of which are previously believed to be animal specific [13]. To further explore the origin of the Ca 2+ signaling machinery, we have more recently reported the examination of several genomes at the Origins of Multicellularity Database [14,15], the Broad Institute and the NCBI genomic databases including the genomes of three basal fungi Allomyces macrogynus, Spizellomyces punctatus, and Batrachochytrium dendrobatidis [16]. Surprisingly, our analysis revealed the presence of P2X receptor homologs in the three basal fungi (AmaP2X, SpuP2X, and BdeP2X) ( Fig. 1; Electronic supplementary Electronic supplementary material The online version of this article

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confidence: 87%

“…2). Fungal P2X receptor homologs also show sequence divergence, possibly reflecting lineage-specific adaptation [16]. For instance, as shown in Fig.…”

mentioning

confidence: 95%

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confidence: 99%

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confidence: 99%

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P2X receptor homologs in basal fungi

Cai

2011

Purinergic Signalling

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“…Cyclic ADPR and NAADP also influence TRPM2 function through synergistic facilitation (33). In metazoan phylogeny, the origins of the RyRs and TPCs date back at least to the urbilaterian (34), so that the signalling kit consisting of messengers, their biosynthetic enzymes and their calcium-releasing receptors, is found throughout invertebrate and vertebrate species, as is the InsP3-dependent signalling mechanism.…”

Section: Distinct Signalling Pathways Mediated By Cadpr and Naadpmentioning

confidence: 99%

The ADP-ribosyl cyclases - the current evolutionary state of the ARCs

et al. 2014

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The major ADP-ribosylating enzyme families are the focus of this special issue of Frontiers in Bioscience. However, there is room for another family of enzymes with the capacity to utilize nicotinamide adenine dinucleotide (NAD): the ADPribosyl cyclases (ARCs). These unique enzymes catalyse the cyclization of NAD to cyclic ADP ribose (cADPR), a widely distributed second messenger. However, the ARCs are versatile enzymes that can manipulate NAD, NAD phosphate (NADP) and other substrates to generate various bioactive molecules including nicotinic acid adenine dinucleotide diphosphate (NAADP) and ADP ribose (ADPR). This review will focus on the group of well-characterized ARCs identified in invertebrate and vertebrate animals, whose common gene structure allows us to trace their origin to the ancestor of bilaterian animals. Behind a façade of gene and protein homology lies a family with a disparate functional repertoire dictated by the animal model and the physical trait under investigation. Here we present a phylogenetic view of the ARCs to better understand the evolution of function in this family. Eggs, this "rich source for experimentation" have been a cornucopia for the ARCs. It was in the egg of the sea urchin Lytechinus pictus that cADPR was first identified as a mediator of stimulus-induced calcium release (2). It was another invertebrate egg, that of the sea slug Aplysia californica, that gave us the first enzyme capable of cADPR biosynthesis (3). Here is the story in brief. INTRODUCTIONThe excitement began just over 25 years ago when it first emerged that NAD, NADP and then cADPR could trigger Ca 2+ release in eggs of the sea urchin Lytechinus pictus (4), on a par with inositol-1,4,5-trisphosphate (InsP3) (5), until then one of the most potent intracellular messengers. Although the capacity to synthesize cADPR and mobilize Ca 2+ was shown to be quite broadly distributed in animal tissues (6), the enzyme responsible for converting NAD to cADPR remained unknown. By a classic 2 stroke of serendipity, the enzyme was detected by scientists studying ADP-ribosylation of G-proteins by the bacterial cholera and diptheria exotoxins in the marine gastropod mollusc Aplysia californica (7). ADP-ribosylation occurred in all examined tissues, except in the ovotestis. The unexpected finding was intelligently pursued until the 'inhibitory factor' was characterized as a NADsplitting protein capable of producing cADPR, similar to the enzymatic activity first identified in sea urchin eggs. This first ARC was molecularly cloned (8) and called 'ADP-ribosyl cyclase' in 1991 by Lee and Aarhus to avoid confusion with other NAD glycohydrolases (EC 3.2.2.5) (3). As will be discussed below, the antagonism between the mono-ADP-ribosyltransferases (mART) and the ARCs revealed in molluscan eggs is probably just the tip of the iceberg of this phenomenon. In the meantime, the availability of an amino acid sequence enabled the sequence homology-based identification of ARCs in other species, first amongst these, human CD38 (9). THE...

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Premammalian origin of the sperm‐specific Slo3 channel

Vicens¹,

Andrade-López²,

Cortez

et al. 2017

FEBS Open Bio

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Slo3 is a sperm‐specific potassium (K+) channel essential for male fertility. Slo3 channels have so far been considered to be specific to mammals. Through exploratory genomics, we identified the Slo3 gene in the genome of terrestrial (birds and reptiles) and aquatic (fish) vertebrates. In the case of fish, Slo3 has undergone several episodes of gene loss. Transcriptomic analysis showed that vertebrate Slo3 transcript orthologues are predominantly expressed in testis, in concordance with the mammalian Slo3. We conclude that the Slo3 gene arose during the radiation of early vertebrates, much earlier than previously thought. Our findings add to the growing evidence indicating that the phylogenetic profiles of sperm‐specific channels are intermittent throughout metazoan evolution, which probably reflects the adaptation of sperm to different ionic milieus and fertilization environments.

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Ancestral Ca2+ Signaling Machinery in Early Animal and Fungal Evolution

Cited by 90 publications

References 74 publications

P2X receptor homologs in basal fungi

P2X receptor homologs in basal fungi

The ADP-ribosyl cyclases - the current evolutionary state of the ARCs

Premammalian origin of the sperm‐specific Slo3 channel

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