Literature DB >> 25160621

Nucleoside triphosphate diphosphohydrolase-1 ectonucleotidase is required for normal vas deferens contraction and male fertility through maintaining P2X1 receptor function.

Gilles Kauffenstein1, Julie Pelletier2, Elise G Lavoie3, Filip Kukulski3, Mireia Martín-Satué4, Sébastien S Dufresne5, Jérôme Frenette5, Cristina Ribas Fürstenau3, Michal J Sereda6, Bertrand Toutain7, Daniel Henrion7, Robert Sullivan8, Catherine Vial6, Jean Sévigny9.   

Abstract

In this work, we report that Entpd1(-/-) mice, deficient for the ectonucleotidase nucleoside triphosphate diphosphohydrolase-1 (NTPDase1), produce smaller litters (27% reduction) compared with wild-type C57BL6 animals. This deficit is linked to reduced in vivo oocyte fertilization by Entpd1(-/-) males (61 ± 11% versus 88 ± 7% for Entpd1(+/+)). Normal epididymal sperm count, spermatozoa morphology, capacitation, and motility and reduced ejaculated sperm number (2.4 ± 0.5 versus 3.7 ± 0.4 million for Entpd1(+/+)) pointed to vas deferens dysfunction. NTPDase1 was localized by immunofluorescence in the tunica muscularis of the vas deferens. Its absence resulted in a major ATP hydrolysis deficiency, as observed in situ by histochemistry and in primary smooth muscle cell cultures. In vitro, Entpd1(-/-) vas deferens displayed an exacerbated contraction to ATP, a diminished response to its non-hydrolysable analog αβMeATP, and a reduced contraction to electrical field stimulation, suggesting altered P2X1 receptor function with a propensity to desensitize. This functional alteration was accompanied by a 3-fold decrease in P2X1 protein expression in Entpd1(-/-) vas deferens with no variation in mRNA levels. Accordingly, exogenous nucleotidase activity was required to fully preserve P2X1 receptor activation by ATP in vitro. Our study demonstrates that NTPDase1 is required to maintain normal P2X1 receptor functionality in the vas deferens and that its absence leads to impaired peristalsis, reduced spermatozoa concentration in the semen, and, eventually, reduced fertility. This suggests that alteration of NTPDase1 activity affects ejaculation efficacy and male fertility. This work may contribute to unveil a cause of infertility and open new therapeutic potentials.
© 2014 by The American Society for Biochemistry and Molecular Biology, Inc.

Entities:  

Keywords:  ATP; ATPase; Male Fertility; Mouse; NTPDase1/CD39; Nucleotide; P2X1; Reproduction; Smooth Muscle Cells; Vas Deferens

Mesh:

Substances:

Year:  2014        PMID: 25160621      PMCID: PMC4192512          DOI: 10.1074/jbc.M114.604082

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  45 in total

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Journal:  FEBS Lett       Date:  2001-02-02       Impact factor: 4.124

Review 2.  Pathophysiology and therapeutic potential of purinergic signaling.

Authors:  Geoffrey Burnstock
Journal:  Pharmacol Rev       Date:  2006-03       Impact factor: 25.468

Review 3.  Impact of ectoenzymes on p2 and p1 receptor signaling.

Authors:  Filip Kukulski; Sébastien A Lévesque; Jean Sévigny
Journal:  Adv Pharmacol       Date:  2011

4.  Selective enhancement by an adenosine A1 receptor agonist of agents inducing contraction of the rat vas deferens.

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Journal:  Naunyn Schmiedebergs Arch Pharmacol       Date:  1996-04       Impact factor: 3.000

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Authors:  A M French; N C Scott
Journal:  Experientia       Date:  1983-03-15

6.  Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculature of the brain.

Authors:  N Braun; J Sévigny; S C Robson; K Enjyoji; O Guckelberger; K Hammer; F Di Virgilio; H Zimmermann
Journal:  Eur J Neurosci       Date:  2000-12       Impact factor: 3.386

7.  Inhibition of excitatory junction potentials in guinea-pig vas deferens by alpha, beta-methylene-ATP: further evidence for ATP and noradrenaline as cotransmitters.

Authors:  P Sneddon; G Burnstock
Journal:  Eur J Pharmacol       Date:  1984-04-13       Impact factor: 4.432

8.  NTPDase1 (CD39) controls nucleotide-dependent vasoconstriction in mouse.

Authors:  Gilles Kauffenstein; Annick Drouin; Nathalie Thorin-Trescases; Hélène Bachelard; Bernard Robaye; Pedro D'Orléans-Juste; François Marceau; Eric Thorin; Jean Sévigny
Journal:  Cardiovasc Res       Date:  2010-01-01       Impact factor: 10.787

Review 9.  Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade.

Authors:  Gennady G Yegutkin
Journal:  Biochim Biophys Acta       Date:  2008-02-12

10.  Hydrolysis of P2-purinoceptor agonists by a purified ectonucleotidase from the bovine aorta, the ATP-diphosphohydrolase.

Authors:  M Picher; J Sévigny; P D'Orléans-Juste; A R Beaudoin
Journal:  Biochem Pharmacol       Date:  1996-06-14       Impact factor: 5.858

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  7 in total

1.  Unravelling purinergic regulation in the epididymis: activation of V-ATPase-dependent acidification by luminal ATP and adenosine.

Authors:  Maria A Battistone; Maria Merkulova; Yoo-Jin Park; Maria A Peralta; Flavia Gombar; Dennis Brown; Sylvie Breton
Journal:  J Physiol       Date:  2019-02-28       Impact factor: 5.182

Review 2.  Epithelial dynamics in the epididymis: role in the maturation, protection, and storage of spermatozoa.

Authors:  S Breton; A V Nair; M A Battistone
Journal:  Andrology       Date:  2019-05-01       Impact factor: 3.842

3.  Distinct roles of ecto-nucleoside triphosphate diphosphohydrolase-2 (NTPDase2) in liver regeneration and fibrosis.

Authors:  Linda Feldbrügge; Z Gordon Jiang; Eva Csizmadia; Shuji Mitsuhashi; Stephanie Tran; Eric U Yee; Sonja Rothweiler; Kahini A Vaid; Jean Sévigny; Moritz Schmelzle; Yury V Popov; Simon C Robson
Journal:  Purinergic Signal       Date:  2017-11-13       Impact factor: 3.765

Review 4.  P2 purinergic receptor dysregulation in urologic disease.

Authors:  Janielle P Maynard; Karen S Sfanos
Journal:  Purinergic Signal       Date:  2022-06-10       Impact factor: 3.950

Review 5.  To Inhibit or Enhance? Is There a Benefit to Positive Allosteric Modulation of P2X Receptors?

Authors:  Leanne Stokes; Stefan Bidula; Lučka Bibič; Elizabeth Allum
Journal:  Front Pharmacol       Date:  2020-05-12       Impact factor: 5.810

6.  NTPDase1 Modulates Smooth Muscle Contraction in Mice Bladder by Regulating Nucleotide Receptor Activation Distinctly in Male and Female.

Authors:  Romuald Brice Babou Kammoe; Gilles Kauffenstein; Julie Pelletier; Bernard Robaye; Jean Sévigny
Journal:  Biomolecules       Date:  2021-01-23

Review 7.  Purinergic Signaling in Endometriosis-Associated Pain.

Authors:  Carla Trapero; Mireia Martín-Satué
Journal:  Int J Mol Sci       Date:  2020-11-12       Impact factor: 5.923

  7 in total

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