Positive Selection in the Evolution of Mammalian CRISPs

Vicens, Alberto; Treviño, Claudia L.

doi:10.1007/s00239-018-9872-6

Cited by 9 publications

(12 citation statements)

References 62 publications

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“…They are not required for male fertility, yet they are incorporated into sperm, and bathe, sperm at high concentrations across mammalian species ( Gaikwad et al, 2020a ). As indicated here, and as posited previously ( Hu et al, 2018 ; Vicens and Treviño, 2018 ), we hypothesize this is due to the competitive advantage CRISPs confer upon sperm in situations of competition. While not normally the case in research facilities, mice are polyandrous in the wild.…”

Section: Discussionsupporting

confidence: 81%

“…Such rapidly evolving genes are thought to play key roles in optimizing sperm motility, in conspecific compatibility in key fertilization proteins and ultimately speciation ( Swanson et al, 2001 ; Vicens et al, 2014a ). Studies have shown that mammalian CRISP genes have experienced positive evolution in both the CAP and CRISP domains ( Vicens and Treviño, 2018 ; Arévalo et al, 2020 ). Cross-species sequence comparison indicate that Crisp2 is likely the ancestral gene from which Crisp1 was derived ( Arévalo et al, 2020 ; Gaikwad et al, 2020a ).…”

Section: Discussionmentioning

confidence: 99%

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CRISPs Function to Boost Sperm Power Output and Motility

Gaikwad

Nandagiri

Potter

et al. 2021

Front. Cell Dev. Biol.

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Fertilization requires sperm to travel long distances through the complex environment of the female reproductive tract. Despite the strong association between poor motility and infertility, the kinetics of sperm tail movement and the role individual proteins play in this process is poorly understood. Here, we use a high spatiotemporal sperm imaging system and an analysis protocol to define the role of CRISPs in the mechanobiology of sperm function. Each of CRISP1, CRISP2, and CRISP4 is required to optimize sperm flagellum waveform. Each plays an autonomous role in defining beat frequency, flexibility, and power dissipation. We thus posit that the expansion of the CRISP family from one member in basal vertebrates, to three in most mammals, and four in numerous rodents, represents an example of neofunctionalization wherein proteins with a common core function, boosting power output, have evolved to optimize different aspects of sperm tail performance.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

CRISPs Function to Boost Sperm Power Output and Motility

Gaikwad

Nandagiri

Potter

et al. 2021

Front. Cell Dev. Biol.

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“…(2000) studied 18 genes directly involved in male reproduction in primates and found that five of these genes (28%) had dN/dS values >1. Other studies of specific gene families involved in male reproduction, such as the CRISP (cysteine‐rich secretory proteins) genes and Adam (a disintegrin and metalloprotease) genes in rodents, also found evidence of positive selection, in some cases with very large dN/dS values (Grayson and Civetta 2013; Vicens and Treviño 2018). However, the study of CRISP genes, like ours, found multiple genes with evidence of positive selection despite having dN/dS values <1.…”

Section: Discussionmentioning

confidence: 95%

The evolution of the testis transcriptome in pregnant male pipefishes and seahorses

et al. 2022

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In many animals, sperm competition and sexual conflict are thought to drive the rapid evolution of male‐specific genes, especially those expressed in the testes. A potential exception occurs in the male pregnant pipefishes, where females transfer eggs to the males, eliminating testes from participating in these processes. Here, we show that testis‐related genes differ dramatically in their rates of molecular evolution and expression patterns in pipefishes and seahorses (Syngnathidae) compared to other fish. Genes involved in testis or sperm function within syngnathids experience weaker selection in comparison to their orthologs in spawning and livebearing fishes. An assessment of gene turnover and expression in the testis transcriptome suggests that syngnathids have lost (or significantly reduced expression of) important classes of genes from their testis transcriptomes compared to other fish. Our results indicate that more than 50 million years of male pregnancy have removed syngnathid testes from the molecular arms race that drives the rapid evolution of male reproductive genes in other taxa.

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“…In mammals, three paralogues of four CRISP members have been described: CRISP1, CRISP2, CRISP3 and CRISP4, with CRISP4 only found in some rodent species [6]. These proteins are 20-30 kDa in size, and share an N-terminal CAP domain containing four conserved motifs and a C-terminal cysteine-rich domain connected with a hinge [1,7].…”

Section: Introductionmentioning

confidence: 99%

Characterization of different oligomeric forms of CRISP2 in the perinuclear theca versus the fibrous tail structures of boar spermatozoa†

Zhang

Bromfield

Veenendaal

et al. 2021

Biology of Reproduction

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Mammalian sperm carry a variety of highly condensed insoluble protein structures such as the perinuclear theca, the fibrous sheath and the outer dense fibers, which are essential to sperm function. We studied the role of cysteine rich secretory protein 2 (CRISP2); a known inducer of non-pathological protein amyloids, in pig sperm with a variety of techniques. CRISP2, which is synthesized during spermatogenesis, was localized by confocal immunofluorescent imaging in the tail and in the post-acrosomal region of the sperm head. High resolution localization by immunogold labeling electron microscopy (EM) of ultrathin cryosections revealed that CRISP2 was present in the perinuclear theca and neck region of the sperm head, as well as in the outer dense fibers and the fibrous sheath of the sperm tail. Interestingly, we found that under native, non-reducing conditions CRISP2 formed oligomers both in the tail and the head but with different molecular weights and different biochemical properties. The tail oligomers were insensitive to reducing conditions but nearly complete dissociated into monomers under 8 M urea treatment, while the head 250 kDa CRISP2 positive oligomer completely dissociated into CRISP2 monomers under reducing conditions. The head specific dissociation of CRISP2 oligomer is likely a result of the reduction of various sulfhydryl groups in the cysteine rich domain of this protein. The sperm head CRISP2 shared typical solubilization characteristics with other perinuclear theca proteins as was shown with sequential detergent and salt treatments. Thus, CRISP2 is likely to participate in the formation of functional protein complexes in both the sperm tail and sperm head, but with differing oligomeric organization and biochemical properties. Future studies will be devoted to the understand the role of CRISP2 in sperm protein complexes formation and how this contributes to the fertilization processes.

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Positive Selection in the Evolution of Mammalian CRISPs

Cited by 9 publications

References 62 publications

CRISPs Function to Boost Sperm Power Output and Motility

CRISPs Function to Boost Sperm Power Output and Motility

The evolution of the testis transcriptome in pregnant male pipefishes and seahorses

Characterization of different oligomeric forms of CRISP2 in the perinuclear theca versus the fibrous tail structures of boar spermatozoa†

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