Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> Venom

Animal venoms are small natural mixtures highly enriched in bioactive components. They are known to target at least two important pharmacological classes of cell surface receptors: ion channels and G protein coupled receptors. Since sperm cells express a wide variety of ion channels and membrane rec...

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Main Authors: Tarek Mohamed Abd El-Aziz, Lucie Jaquillard, Sandrine Bourgoin-Voillard, Guillaume Martinez, Mathilde Triquigneaux, Claude Zoukimian, Stéphanie Combemale, Jean-Pascal Hograindleur, Sawsan Al Khoury, Jessica Escoffier, Sylvie Michelland, Philippe Bulet, Rémy Beroud, Michel Seve, Christophe Arnoult, Michel De Waard
Format: Article
Language:English
Published: MDPI AG 2020-10-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/20/7786
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author Tarek Mohamed Abd El-Aziz
Lucie Jaquillard
Sandrine Bourgoin-Voillard
Guillaume Martinez
Mathilde Triquigneaux
Claude Zoukimian
Stéphanie Combemale
Jean-Pascal Hograindleur
Sawsan Al Khoury
Jessica Escoffier
Sylvie Michelland
Philippe Bulet
Rémy Beroud
Michel Seve
Christophe Arnoult
Michel De Waard
author_facet Tarek Mohamed Abd El-Aziz
Lucie Jaquillard
Sandrine Bourgoin-Voillard
Guillaume Martinez
Mathilde Triquigneaux
Claude Zoukimian
Stéphanie Combemale
Jean-Pascal Hograindleur
Sawsan Al Khoury
Jessica Escoffier
Sylvie Michelland
Philippe Bulet
Rémy Beroud
Michel Seve
Christophe Arnoult
Michel De Waard
author_sort Tarek Mohamed Abd El-Aziz
collection DOAJ
description Animal venoms are small natural mixtures highly enriched in bioactive components. They are known to target at least two important pharmacological classes of cell surface receptors: ion channels and G protein coupled receptors. Since sperm cells express a wide variety of ion channels and membrane receptors, required for the control of cell motility and acrosome reaction, two functions that are defective in infertility issues, animal venoms should contain interesting compounds capable of modulating these two essential physiological functions. Herein, we screened for bioactive compounds from the venom of the Egyptian black snake <i>Walterinnesia aegyptia</i> (Wa) that possess the property to activate sperm motility in vitro from male mice OF1. Using RP-HPLC and cation exchange chromatography, we identified a new toxin of 6389.89 Da (termed walterospermin) that activates sperm motility. Walterospermin was <i>de novo</i> sequenced using a combination of matrix assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF/TOF MS/MS) and liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry (LC-ESI-QTOF MS/MS) following reduction, alkylation, and enzymatic proteolytic digestion with trypsin, chymotrypsin or V8 protease. The peptide is 57 amino acid residues long and contains three disulfide bridges and was found to be identical to the previously cloned Wa Kunitz-type protease inhibitor II (Wa Kln-II) sequence. Moreover, it has strong homology with several other hitherto cloned Elapidae and Viperidae snake toxins suggesting that it belongs to a family of compounds able to regulate sperm function. The synthetic peptide shows promising activation of sperm motility from a variety of species, including humans. Its fluorescently-labelled analog predominantly marks the flagellum, a localization in agreement with a receptor that controls motility function.
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spelling doaj.art-d8e0f60767ef4ab48715eb0caa9c0cf32023-11-20T17:57:35ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-10-012120778610.3390/ijms21207786Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> VenomTarek Mohamed Abd El-Aziz0Lucie Jaquillard1Sandrine Bourgoin-Voillard2Guillaume Martinez3Mathilde Triquigneaux4Claude Zoukimian5Stéphanie Combemale6Jean-Pascal Hograindleur7Sawsan Al Khoury8Jessica Escoffier9Sylvie Michelland10Philippe Bulet11Rémy Beroud12Michel Seve13Christophe Arnoult14Michel De Waard15Department of Cellular and Integrative Physiology, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229-3900, USASmartox Biotechnology, 6 rue des Platanes, 38120 Saint-Egrève, FrancePROMETHEE Proteomic Platform, University Grenoble Alpes, LBFA et BEeSy, 38041 Grenoble, FranceInstitut Pour l’Avancée des Biosciences (IAB), INSERM U1209, CNRS UMR 5309, 38700 La Tronche, FranceSmartox Biotechnology, 6 rue des Platanes, 38120 Saint-Egrève, FranceSmartox Biotechnology, 6 rue des Platanes, 38120 Saint-Egrève, FranceSmartox Biotechnology, 6 rue des Platanes, 38120 Saint-Egrève, FranceInstitut Pour l’Avancée des Biosciences (IAB), INSERM U1209, CNRS UMR 5309, 38700 La Tronche, FranceL’institut du thorax, INSERM, CNRS, UNIV NANTES, F-44007 Nantes, FranceInstitut Pour l’Avancée des Biosciences (IAB), INSERM U1209, CNRS UMR 5309, 38700 La Tronche, FrancePROMETHEE Proteomic Platform, University Grenoble Alpes, LBFA et BEeSy, 38041 Grenoble, FranceInstitut Pour l’Avancée des Biosciences (IAB), INSERM U1209, CNRS UMR 5309, 38700 La Tronche, FranceSmartox Biotechnology, 6 rue des Platanes, 38120 Saint-Egrève, FrancePROMETHEE Proteomic Platform, University Grenoble Alpes, LBFA et BEeSy, 38041 Grenoble, FranceInstitut Pour l’Avancée des Biosciences (IAB), INSERM U1209, CNRS UMR 5309, 38700 La Tronche, FranceSmartox Biotechnology, 6 rue des Platanes, 38120 Saint-Egrève, FranceAnimal venoms are small natural mixtures highly enriched in bioactive components. They are known to target at least two important pharmacological classes of cell surface receptors: ion channels and G protein coupled receptors. Since sperm cells express a wide variety of ion channels and membrane receptors, required for the control of cell motility and acrosome reaction, two functions that are defective in infertility issues, animal venoms should contain interesting compounds capable of modulating these two essential physiological functions. Herein, we screened for bioactive compounds from the venom of the Egyptian black snake <i>Walterinnesia aegyptia</i> (Wa) that possess the property to activate sperm motility in vitro from male mice OF1. Using RP-HPLC and cation exchange chromatography, we identified a new toxin of 6389.89 Da (termed walterospermin) that activates sperm motility. Walterospermin was <i>de novo</i> sequenced using a combination of matrix assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF/TOF MS/MS) and liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry (LC-ESI-QTOF MS/MS) following reduction, alkylation, and enzymatic proteolytic digestion with trypsin, chymotrypsin or V8 protease. The peptide is 57 amino acid residues long and contains three disulfide bridges and was found to be identical to the previously cloned Wa Kunitz-type protease inhibitor II (Wa Kln-II) sequence. Moreover, it has strong homology with several other hitherto cloned Elapidae and Viperidae snake toxins suggesting that it belongs to a family of compounds able to regulate sperm function. The synthetic peptide shows promising activation of sperm motility from a variety of species, including humans. Its fluorescently-labelled analog predominantly marks the flagellum, a localization in agreement with a receptor that controls motility function.https://www.mdpi.com/1422-0067/21/20/7786Snake venom<i>Walterinnesia aegyptia</i>bioactive componentssperm motilityproteomicsmass spectrometry
spellingShingle Tarek Mohamed Abd El-Aziz
Lucie Jaquillard
Sandrine Bourgoin-Voillard
Guillaume Martinez
Mathilde Triquigneaux
Claude Zoukimian
Stéphanie Combemale
Jean-Pascal Hograindleur
Sawsan Al Khoury
Jessica Escoffier
Sylvie Michelland
Philippe Bulet
Rémy Beroud
Michel Seve
Christophe Arnoult
Michel De Waard
Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> Venom
International Journal of Molecular Sciences
Snake venom
<i>Walterinnesia aegyptia</i>
bioactive components
sperm motility
proteomics
mass spectrometry
title Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> Venom
title_full Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> Venom
title_fullStr Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> Venom
title_full_unstemmed Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> Venom
title_short Identification, Characterization and Synthesis of Walterospermin, a Sperm Motility Activator from the Egyptian Black Snake <i>Walterinnesia aegyptia</i> Venom
title_sort identification characterization and synthesis of walterospermin a sperm motility activator from the egyptian black snake i walterinnesia aegyptia i venom
topic Snake venom
<i>Walterinnesia aegyptia</i>
bioactive components
sperm motility
proteomics
mass spectrometry
url https://www.mdpi.com/1422-0067/21/20/7786
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