Thermosensitive ion channel TRPV1 is endogenously expressed in the sperm of a fresh water teleost fish (<i>Labeo rohita</i>) and regulates sperm motility

Majhi, Rakesh Kumar; Kumar, Ashutosh; Yadav, Manoj Kumar; Swain, Nirlipta; Kumari, Shikha; Saha, Ashish Kumar; Pradhan, Avinash; Goswami, Luna; Saha, S. K.; Samanta, Luna; Maity, Apratim; Nayak, Tapas Kumar; Chattopadhyay, Subhasis; Rajakuberan, Chitra; Kumar, Abhishek; Goswami, Chandan

doi:10.4161/chan.25793

Cited by 44 publications

(39 citation statements)

References 58 publications

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“…This is especially relevant in salmonids, where sperm movement duration and the associated window for fertilization are extremely short (Kime et al, 2001). In the freshwater teleost Labeo rohita, Ca 2+ influx and consequentially the activation and preservation of sperm movement are regulated by thermosensitive ion channels [vanilloid transient receptor potential (TRPV) channels; Majhi et al, 2013], which may confer heat resistance to the sperm cells, as previously shown for germ cells in mouse testes (Mizrak and van DisselEmiliani, 2008). Changes in heat sensitivity of sperm over the breeding season could be a result of the expression of TRPV channels in sperm cell membranes with advanced maturation of the male trout in our study.…”

Section: Discussionmentioning

confidence: 86%

Sperm in hot water: Direct and indirect thermal challenges interact to impact on brown trout sperm quality

Fenkes

Fitzpatrick

Ozolina

et al. 2017

Journal of Experimental Biology

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Climate change alters the thermal habitat of aquatic species on a global scale, generating novel environmental challenges during all life stages, including reproduction. Changes in water temperature profoundly influence the performance of ectothermic aquatic organisms. This is an especially crucial issue for migratory fish, because they traverse multiple environments in order to reproduce. In externally fertilizing migratory fish, gametes are affected by water temperature indirectly, within the reproductive organ in which they are produced during migration, as well as directly, upon release into the surrounding medium at the spawning grounds. Both direct (after release) and indirect (during production) thermal impacts on gamete quality have been investigated, but never in conjunction. Here, we assessed the cumulative influence of temperature on brown trout, Salmo trutta, sperm quality during sperm production (male acclimation temperature) as well as upon release (sperm activation water temperature) on two consecutive dates during the brown trout spawning season. Early in the season, warm acclimation of males reduced their fertilization probability (lower sperm velocity) when compared with cold-acclimated males, especially when the activation water temperature was also increased beyond the thermal optimum (resulting in a lower proportion of motile sperm with lower velocity). Later in the season, sperm quality was unaffected by acclimation temperature and thermal sensitivity of sperm was reduced. These results give novel insights into the complex impacts of climate change on fish sperm, with implications for the reproduction and management of hatchery and wild trout populations in future climate scenarios.

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Section: Discussionmentioning

confidence: 86%

Sperm in hot water: Direct and indirect thermal challenges interact to impact on brown trout sperm quality

Fenkes

Fitzpatrick

Ozolina

et al. 2017

Journal of Experimental Biology

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“…This hypothesis, while not yet demonstrated, is supported by the finding that AQP4 or -5 can interact with the volume sensitive calcium channel transient receptor potential vanalloid 4 (TRPV4) to regulate cell volume under hypotonic stimulation in mouse astrocytes and salivary glands [50,51], and by the direct interaction of AQP2 with actin described in rat kidney cells [52]. In addition, TRP channels have been shown to play functions during sperm capacitation, acrosome reaction motility and fertilization in mammals [53][54][55], as well as to regulate sperm motility in freshwater teleosts [56].…”

Section: Discussionmentioning

confidence: 99%

Coordinated Action of Aquaporins Regulates Sperm Motility in a Marine Teleost1

Boj

Chauvigné

Cerdà

2015

Biology of Reproduction

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In marine teleosts, such as the gilthead seabream, several aquaporin paralogs are known to be expressed during the hyperosmotic induction of spermatozoon motility in seawater. Here, we used immunological inhibition of channel function to investigate the physiological roles of Aqp1aa, Aqp1ab, and Aqp7 during seabream sperm activation. Double immunofluorescence microscopy of SW-activated sperm showed that Aqp1aa and Aqp7 were respectively distributed along the flagellum and the head, whereas Aqp1ab accumulated in the head and in discrete areas toward the anterior tail. Inhibition of Aqp1aa reduced the rise of intracellular Ca(2+), which is independent of external Ca(2+) and normally occurs upon activation, and strongly inhibited sperm motility. Impaired Aqp1aa function also prevented the intracellular trafficking of Aqp8b to the mitochondrion, where it acts as a peroxiporin allowing H2O2 efflux and ATP production during activation. However, restoring the Ca(2+) levels with a Ca(2+) ionophore in spermatozoa with immunosuppressed Aqp1aa function fully rescued mitochondrial Aqp8b accumulation and sperm motility. In contrast, exposure of sperm to Aqp1ab and Aqp7 antibodies did not affect motility during the initial phase of activation, but latently compromised the trajectory and the pattern of movement. These data reveal the coordinated action of spatially segregated aquaporins during sperm motility activation in a marine teleost, where flagellar-localized Aqp1aa plays a dual Ca(2+)-dependent role controlling the initiation of sperm motility and the activation of mitochondrial detoxification mechanisms, while Aqp1ab and Aqp7 in the head and anterior tail direct the motion pattern.

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“…44,45 Two possible candidates are the nonspecific cation channels TRPV1 and TRPV4 (Transient Receptor Potential Vanilloid types 1 and 4, respectively), which have been linked to sperm capacitation, motility, and the AR. [46][47][48][49][50] TRPV1 and TRPV4 have an important physical and functional interaction with TMEM16A, 45,51 in such a way that TMEM16A inhibition produces an important reduction of TRPV1 activation by capsaicin, 45 and TRPV4 activation induces Cl − currents that depend on TMEM16A. 51 In conclusion, this is the first instance of a report of TMEM16A expression in guinea pig sperm.…”

Section: Discussionmentioning

confidence: 63%

TMEM16A inhibition impedes capacitation and acquisition of hyperactivated motility in guinea pig sperm

Cordero-Martínez

Reyes-Miguel

Rodrı́guez-Páez

et al. 2018

J of Cellular Biochemistry

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Ca -activated Cl channels (CaCCs) are anionic channels that regulate many important physiological functions associated with chloride and calcium flux in some somatic cells. The molecular identity of CaCCs was revealed to be TMEM16A and TMEM16B (also known as Anoctamin or ANO1 and ANO2, respectively) in all eukaryotes. A recent study suggests the presence of TMEM16A in human sperm and a relationship with the rhZP-induced acrosome reaction. However, to the best of our knowledge, little is known about the role of TMEM16A in other spermatic processes such as capacitation or motility. In this study, we evaluated the effects of two TMEM16A antagonists on capacitation, acrosome reaction, and motility in guinea pig sperm; these antagonists were T16Ainh-A01, belonging to a second generation of potent antagonists of TMEM16A, and niflumic acid (NFA), a well-known antagonist of TMEM16A (CaCCs). First of all, we confirmed that the absence of Cl in the capacitation medium changes motility parameters, capacitation, and the progesterone-induced acrosome reaction. Using a specific antibody, TMEM16A was found as a protein band of ∼120 kDa, which localization was in the apical crest of the acrosome and the middle piece of the flagellum. Inhibition of TMEM16A by T16Ainh-A01 affected sperm physiology by reducing capacitation, blocking the progesterone-induced acrosome reaction under optimal capacitation conditions, inhibiting progressive motility, and the acquisition of hyperactivated motility, diminishing [Ca ]i, and increasing [Cl ]i. These changes in sperm kinematic parameters provide new evidence of the important role played by TMEM16A in the production of sperm capable of fertilizing oocytes.

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Thermosensitive ion channel TRPV1 is endogenously expressed in the sperm of a fresh water teleost fish (Labeo rohita) and regulates sperm motility

Abstract: (2013) Thermosensitive ion channel TRPV1 is endogenously expressed in the sperm of a fresh water teleost fish (Labeorohita) and regulates sperm motility, Channels, 7:6, 483-492,

Cited by 44 publications

References 58 publications

Sperm in hot water: Direct and indirect thermal challenges interact to impact on brown trout sperm quality

Sperm in hot water: Direct and indirect thermal challenges interact to impact on brown trout sperm quality

Coordinated Action of Aquaporins Regulates Sperm Motility in a Marine Teleost1

TMEM16A inhibition impedes capacitation and acquisition of hyperactivated motility in guinea pig sperm

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