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Identification and characterization of RING-finger ubiquitin ligase UBR7 in mammalian spermatozoa

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Abstract

The ubiquitin-proteasome system (UPS) controls intracellular protein turnover in a substrate-specific manner via E3-type ubiquitin ligases. Mammalian fertilization and particularly sperm penetration through the oocyte vitelline coat, the zona pellucida (ZP), is regulated by UPS. We use an extrinsic substrate of the proteasome-dependent ubiquitin-fusion degradation pathway, the mutant ubiquitin UBB+1, to provide evidence that an E3-type ligase activity exists in sperm-acrosomal fractions. Protein electrophoresis gels from such de novo ubiquitination experiments contained a unique protein band identified by tandem mass spectrometry as being similar to ubiquitin ligase UBR7 (alternative name: C14ORF130). Corresponding mRNA was amplified from boar testis and several variants of the UBR7 protein were detected in boar, mouse and human sperm extracts by Western blotting. Genomic analysis indicated a high degree of evolutionary conservation, remarkably constant purifying selection and conserved testis expression of the UBR7 gene. By immunofluorescence, UBR7 was localized to the spermatid acrosomal cap and sperm acrosome, in addition to hotspots of proteasomal activity in spermatids, such as the cytoplasmic lobe, caudal manchette, nucleus and centrosome. During fertilization, UBR7 remained with the ZP-bound acrosomal shroud following acrosomal exocytosis. Thus, UBR7 is present in the acrosomal cap of round spermatids and within the acrosomal matrix of mature boar spermatozoa. These data provide the first evidence of ubiquitin ligase activity in mammalian spermatozoa and indicate UBR7 involvement in spermiogenesis.

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Abbreviations

aa:

Amino acid

ATP:

Adenosine triphosphate

CLBL:

Clasto-lactacystin-β-lactone (specific proteasomal inhibitor)

DMSO:

Dimethyl sulfoxide (vehicle solution)

Epox:

Epoxomicin (specific proteasomal inhibitor)

EtOH:

Ethyl alcohol, ethanol (vehicle solution)

EST:

Expressed sequence tag

GST tag:

Glutathione S-transferase tag

LCAP:

Linear combination of amino acid properties

LRT:

Likelihood ratio test

MG132:

N-(benzyloxycarbonyl)leucinylleucinylleucinal ( Z-Leu-Leu-Leu-al;specific proteasomal inhibitor)

MS/MS:

Tandem mass spectrometry

PCR:

Polymerase chain reaction

UBA1:

Ubiquitin-activating enzyme E1

UBAL:

Ubiquitin-aldehyde (specific inhibitor of ubiquitin-C-terminal hydrolases)

UBB:

Ubiquitin B

UBB+1 :

Mutant frame-shifted ubiquitin B protein

UPS:

Ubiquitin-proteasome system

VC:

Vitelline coat

ZP:

Zona pellucida

ZPP:

Zona pellucida protein (solubilized)

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Acknowledgments

We thank Dr. Kiho Lee and Dr. Randall Prather for providing the mRNA samples for PCR analysis from boar testis.

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Authors and Affiliations

  1. Division of Animal Sciences, University of Missouri, Columbia, MO, 65211-5300, USA

    Shawn W. Zimmerman, Young-Joo Yi, Miriam Sutovsky, Gavin Conant & Peter Sutovsky

  2. Departments of Obstetrics, Gynecology and Women’s Health, University of Missouri, Columbia, MO, 65211-5300, USA

    Peter Sutovsky

  3. Department of Neuroscience, School for Mental Health and Neuroscience, Maastricht University, Universiteitssingel 50, 6229 ER, Maastricht, The Netherlands

    Fred W. van Leeuwen

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  1. Shawn W. Zimmerman
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  2. Young-Joo Yi
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  3. Miriam Sutovsky
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  4. Fred W. van Leeuwen
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  5. Gavin Conant
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  6. Peter Sutovsky
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Correspondence to Peter Sutovsky.

Additional information

This work was supported by National Research Initiative Competitive Grant no. 2011-67015-20025 from the USDA National Institute of Food and Agriculture and by the Food for the 21st Century Program of the University of Missouri-Columbia (to P.S.). F.W.V.L. was supported by ISAO (grant nos. 06502 and 09514).

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Zimmerman, S.W., Yi, YJ., Sutovsky, M. et al. Identification and characterization of RING-finger ubiquitin ligase UBR7 in mammalian spermatozoa. Cell Tissue Res 356, 261–278 (2014). https://doi.org/10.1007/s00441-014-1808-x

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