A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa

Abstract

The primary task of a spermatozoon is to deliver its nuclear payload to the egg to form the next-generation zygote. With polyandry repeatedly evolving in the animal kingdom, however, sperm competition has become widespread, with the highest known intensities occurring in fish. Yet, the molecular controls regulating spermatozoon swimming performance in these organisms are largely unknown. Here, we show that the kinematic properties of postactivated piscine spermatozoa are regulated through a conserved trafficking mechanism whereby a peroxiporin ortholog of mammalian aquaporin-8 (Aqp8bb) is inserted into the inner mitochondrial membrane to facilitate H2O2 efflux in order to maintain ATP production. In teleosts from more ancestral lineages, such as the zebrafish (Danio rerio) and the Atlantic salmon (Salmo salar), in which spermatozoa are activated in freshwater, an intracellular Ca2+-signaling directly regulates this mechanism through monophosphorylation of the Aqp8bb N terminus. In contrast, in more recently evolved marine teleosts, such the gilthead seabream (Sparus aurata), in which spermatozoa activation occurs in seawater, a cross-talk between Ca2+- and oxidative stress-activated pathways generate a multiplier regulation of channel trafficking via dual N-terminal phosphorylation. These findings reveal that teleost spermatozoa evolved increasingly sophisticated detoxification pathways to maintain swimming performance under a high osmotic stress, and provide insight into molecular traits that are advantageous for postcopulatory sexual selection.

Reactive Oxygen Species: Not Omnipresent but Important in Many Locations

“…O 2 – quickly dismutates to H 2 O 2 , which is more, although not freely, diffusible for cellular membranes ( Bienert et al, 2006 ; Wang et al, 2020 ; Chauvigne et al, 2021 ), which questions saturation of the cell with H 2 O 2 to fulfill signaling functions in compartments, which are not in direct proximity to the ROS source ( Beretta et al, 2020 ; Sies, 2021 ). Communication between cellular compartments can be achieved by aquaporins, which facilitate a controlled passage of H 2 O 2 over membranes ( Bienert and Chaumont, 2014 ; Wang et al, 2020 ).…”

“…H 2 O 2 has a longer cellular half-life (∼1 ms) with concentrations of ∼10 –7 M under cellular homoeostatic conditions ( D’Autreaux and Toledano, 2007 ). Because of these properties, it functions as an important signaling molecule involved in many different cellular processes ( Kamata et al, 2005 ; Tonks, 2005 ; Rhee, 2006 ; Marinho et al, 2013 ; Holmstrom and Finkel, 2014 ; Romero et al, 2014 ; Jones et al, 2016 ; Short et al, 2016 ; Zhang et al, 2016 ; Herb et al, 2019b ; Sies and Jones, 2020 ; Chauvigne et al, 2021 ). H 2 O 2 -mediated signaling is mainly based on the oxidation of cysteine residues of proteins ( Chiarugi et al, 2001 ; Rhee, 2006 ; Herscovitch et al, 2008 ; Romero et al, 2014 ; Jones et al, 2016 ; Short et al, 2016 ; Herb et al, 2019b ).…”

“…Growing evidence indicates that the redox status in different cellular compartments varies greatly ( Fransen et al, 2017 ; Beretta et al, 2020 ; Chauvigne et al, 2021 ; Sies, 2021 ; Wang et al, 2021b ), is tightly regulated ( Nakamura, 2005 ; Kirkman and Gaetani, 2007 ; Kelley et al, 2010 ; Brigelius-Flohe and Maiorino, 2013 ; Poljsak et al, 2013 ; Couto et al, 2016 ; Jones et al, 2016 ; Chauvigne et al, 2021 ) and every elevation of ROS levels is controlled by the cell in various ways ( Babior, 2002 ; Bulua et al, 2011 ; Hoeven et al, 2011 ; West et al, 2011a ; Gluschko et al, 2018 ; Herb et al, 2019b ; Chauvigne et al, 2021 ). The condition of ROS levels exceeding the capacity of cellular antioxidant defense systems is termed oxidative stress ( Niki, 2016 ; Sies and Jones, 2020 ).…”

“…Of note, to reach levels at which the ROS can fulfill their important cellular roles, ROS production has to overcome the highly effective antioxidative defense systems of one or more cellular compartments ( Nakamura, 2005 ; Kirkman and Gaetani, 2007 ; Kelley et al, 2010 ; Brigelius-Flohe and Maiorino, 2013 ; Poljsak et al, 2013 ; Lismont et al, 2015 ; Couto et al, 2016 ; Jones et al, 2016 ; Shai et al, 2018 ; Chauvigne et al, 2021 ; Herb and Schramm, 2021 ). Also H 2 O 2 -detoxifying enzymes, such as glutathione peroxidases or catalase, which can quickly decrease cellular H 2 O 2 concentrations ( Winterbourn and Hampton, 2008 ) as well as the inactivation of these scavenger enzymes by H 2 O 2 itself broaden the regulatory potential of cells for selective and localized ROS signaling ( Wood et al, 2003 ; Woo et al, 2010 ).…”

Protamine lacking piscine spermatozoa are transcriptionally active

“…To investigate the transcription-dependent actions of sbGnRH and PDGF on the motility of SPZ ED , we employed a targeted approach by evaluating the hormone-induced changes in the expression levels of selected genes. This included genes that encode aquaporins and ion channels, receptors, components of the motile apparatus, and enzymes involved in respiratory pathways, most of them regulated in SPZ EJ as indicated by RNA-seq profiling (Figure 2 and 3), and which control or can potentially modulate sperm motility (Boj et al, 2015;Chauvigné et al, 2015;Alavi et al, 2019;Chauvigné et al, 2021). The data indicated that both sbGnRH and rPDGF-BB upregulated the expression of many of these genes in SPZ ED , but not all the same genes were affected by the two hormones (Figure 7F).…”