Pervasive Adaptive Evolution in Mammalian Fertilization Proteins

Swanson, Willie J.; Nielsen, Rasmus; Yang, Qiaofeng

doi:10.1093/oxfordjournals.molbev.a004233

Cited by 438 publications

(430 citation statements)

References 18 publications

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“…Human ZP1 and ZP4 are paralogues that may have arisen from a common ancestral gene either by gene duplication or exon swapping. 11,78,79 The aa sequence identity of human ZP1 and ZP4 is 47%, which further supports the notion that AR induction mediated by ZP1/ZP4 is likely to follow similar downstream signalling events. Murine models Chemically deglycosylated forms of mouse ZP3 fail to induce the AR, suggesting that glycosylation of ZP3 is critical for its functional activity.…”

Section: Zp4supporting

confidence: 72%

“…77 The region of ZP3 encoded by exon 7 has undergone a relatively large number of changes during evolution compared with the remainder of the polypeptide and is a proposed site of positive Darwinian selection. 78,79 Human ZP3 has a polypeptide backbone of 424 aa, with a signal peptide (SP) at 1-22 aa that facilitates its secretion (Figure 2a). A tetra basic consensus furin cleavage site (349-352 aa) is present upstream of a hydrophobic transmembrane-like domain (387-409 aa).…”

Section: Zp3mentioning

confidence: 99%

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Acrosome reaction: relevance of zona pellucida glycoproteins

Gupta

Bhandari²

2010

Asian J Androl

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During mammalian fertilisation, the zona pellucida (ZP) matrix surrounding the oocyte is responsible for the binding of the spermatozoa to the oocyte and induction of the acrosome reaction (AR) in the ZP-bound spermatozoon. The AR is crucial for the penetration of the ZP matrix by spermatozoa. The ZP matrix in mice is composed of three glycoproteins designated ZP1, ZP2 and ZP3, whereas in humans, it is composed of four (ZP1, ZP2, ZP3 and ZP4). ZP3 acts as the putative primary sperm receptor and is responsible for AR induction in mice, whereas in humans (in addition to ZP3), ZP1 and ZP4 also induce the AR. The ability of ZP3 to induce the AR resides in its C-terminal fragment. O-linked glycans are critical for the murine ZP3-mediated AR. However, N-linked glycans of human ZP1, ZP3 and ZP4 have important roles in the induction of the AR. Studies with pharmacological inhibitors showed that the ZP3-induced AR involves the activation of the G i -coupled receptor pathway, whereas ZP1-and ZP4-mediated ARs are independent of this pathway. The ZP3-induced AR involves the activation of T-type voltage-operated calcium channels (VOCCs), whereas ZP1-and ZP4-induced ARs involve both T-and L-type VOCCs. To conclude, in mice, ZP3 is primarily responsible for the binding of capacitated spermatozoa to the ZP matrix and induction of the AR, whereas in humans (in addition to ZP3), ZP1 and ZP4 also participate in these stages of fertilisation. Keywords: acrosome reaction; fertilisation; oocyte; signalling pathways; spermatozoa; zona pellucida glycoproteins INTRODUCTION Mammalian fertilisation is a highly synchronized process that involves a complex series of interactions between the spermatozoon and the egg, culminating in their unison. The initial steps in fertilisation involves the binding of the spermatozoon to the zona pellucida (ZP) matrix surrounding the egg, followed by induction of the acrosome reaction (AR) in the zona-bound spermatozoon, a pre-requisite for penetration of the ZP matrix by the spermatozoon. The spermatozoon acrosome is a Golgi-derived organelle that forms a cap over the anterior two-thirds of its nucleus. The AR involves the fusion of the sperm membrane with the outer acrosomal membrane, resulting in release of the acrosomal contents and exposure of the inner acrosomal membrane on the anterior head of the spermatozoon. Various physiological agents, such as progesterone, serum albumin, follicular fluid, hormones (including biogenic amines), hydrolytic enzymes (particularly proteases), hyaluronic acid and ZP glycoproteins, have been implicated in the induction of the AR. [1][2][3] In the present paper, we review the role of the ZP matrix and its constituents in AR induction. Various downstream signalling pathways involved in the ZP glycoprotein-induced AR will also be discussed. On the basis of the current literature and studies from our group, the salient differences in the ZP glycoprotein-mediated induction of the AR in mouse versus human will be highlighted.

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Section: Zp4supporting

confidence: 72%

Section: Zp3mentioning

confidence: 99%

Acrosome reaction: relevance of zona pellucida glycoproteins

Gupta

Bhandari²

2010

Asian J Androl

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“…4,22,23 Positive selection is pervasive among mammalian reproductive proteins, especially several sperm proteins that have been implicated in binding the egg promoting fertilization. 24 The rapid evolution of reproductive proteins may be driven by the selective forces of sperm competition, sexual selection and sexual conflict, individually, or in combination. 20 Previously, we identified the novel epididymal spermbinding protein DEFB118 25 and recently showed that DEFB118 has potent antibacterial activity.…”

Section: Introductionmentioning

confidence: 99%

Identification, characterization, and evolution of a primate β-defensin gene cluster

et al. 2005

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Defensins are members of a large diverse family of cationic antimicrobial peptides that share a signature pattern consisting of six conserved cysteine residues. Defensins have a wide variety of functions and their disruption has been implicated in various human diseases. Here we report the characterization of DEFB119-DEFB123, five genes in the human b-defensin cluster locus on chromosome 20q11.1. The genomic structures of DEFB121 and DEFB122 were determined in silico. Sequences of the five macaque orthologs were obtained and expression patterns of the genes were analyzed in humans and macaque by semiquantitative reverse transcription polymerase chain reaction. Expression was restricted to the male reproductive tract. The genes in this cluster are differentially regulated by androgens. Evolutionary analyses suggest that this cluster originated by a series of duplication events and by positive selection. The evolutionary forces driving the proliferation and diversification of these defensins may be related to reproductive specialization and/or the host-parasite coevolutionary process.

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“…LRTs were used to compare models that assume no positive selection (u < 1) with those that assume positive selection (u > 1). The seven codon substitution models are: M0 (one-ratio), M1a [34] and M8a (b þ u ¼ 1) [51]. The M1a model estimates a single parameter p 0 , the frequency of conserved sites with u 0 ¼ 0 and the remaining sites with frequency p 1 (p 1 ¼ 1 À p 0 ) assuming u 1 ¼ 1.…”

mentioning

confidence: 99%

“…The fourth comparison was between a model of beta-distributed selective pressures, that allows for 10 site classes, each with u < 1 and M8, which has 11 site classes, one of them allowed for u > 1. The last comparison was between M8 and M8a, in which an additional parameter was constrained to have u ¼ 1 [51]. In all LRTs good evidence for positive selection is found if the LRT indicates that models that allow for selection (i.e.…”

mentioning

confidence: 99%

Adaptive evolution after duplication of penaeidin antimicrobial peptides

Padhi

Verghese

Otta

et al. 2007

Fish & Shellfish Immunology

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Penaeidin antimicrobial peptides in penaeid shrimps are an important component of their innate immune system that provides immunity against infection caused by several gram-positive bacteria and filamentous fungal species. Despite the knowledge on the identification and characterization of these peptides in penaeid shrimps, little is known about the evolutionary pattern of these peptides and the underlying genetic mechanisms that maintain high sequence diversities in the penaeidin gene family. Based on the phylogenetic analyses and maximum likelihood-based codon substitution analyses, here we present the convincing evidence that multiple copies of penaeidins have evolved by gene duplication, and positive Darwinian selection (adaptive evolution) is the likely cause of accelerated rate of amino acid substitutions among these duplicated genes.While the average ratio of non-synonymous to synonymous substitutions (u) for the entire coding region of both active domains is 0.9805, few codon sites showed significantly higher u (3.73). The likelihood ratio tests that compare models incorporating positive selection (u > 1) at certain codon sites with models not incorporating positive selection (u < 1), failed to reject (p ¼ 0) the evidence of positive Darwinian selection. The rapid adaptive evolution of this gene family might be directed by the pathogens and the faster rate of amino acid substitutions in the N-terminal proline-rich and C-terminal cysteine-rich domains could be due to their direct involvement in the protection against pathogens. When the host expose to different habitats/environment an accelerated rate of amino acid substitutions in both the active domains may also be expected.

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Pervasive Adaptive Evolution in Mammalian Fertilization Proteins

Cited by 438 publications

References 18 publications

Acrosome reaction: relevance of zona pellucida glycoproteins

Acrosome reaction: relevance of zona pellucida glycoproteins

Identification, characterization, and evolution of a primate β-defensin gene cluster

Adaptive evolution after duplication of penaeidin antimicrobial peptides

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