Bottom-up approach to deciphering the targets of the ubiquitin-proteasome system in porcine sperm capacitation
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
PubMed
39215164
PubMed Central
PMC11364869
DOI
10.1038/s41598-024-71056-4
PII: 10.1038/s41598-024-71056-4
Knihovny.cz E-zdroje
- Klíčová slova
- Pig, Sperm capacitation, Sperm proteomics, Ubiquitin-proteasome system,
- MeSH
- kapacitace spermií * fyziologie MeSH
- prasata MeSH
- proteasomový endopeptidasový komplex * metabolismus MeSH
- proteom metabolismus MeSH
- proteomika * metody MeSH
- spermie * metabolismus fyziologie MeSH
- ubikvitin * metabolismus MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- proteasomový endopeptidasový komplex * MeSH
- proteom MeSH
- ubikvitin * MeSH
Capacitation is an essential post-testicular maturation event endowing spermatozoa with fertilizing capacity within the female reproductive tract, significant for fertility, reproductive health, and contraception. By using a human-relevant large animal model, the domestic boar, this study focuses on furthering our understanding of the involvement of the ubiquitin-proteasome system (UPS) in sperm capacitation. The UPS is a universal, evolutionarily conserved, cellular proteome-wide degradation and recycling machinery, that has been shown to play a significant role in reproduction during the past two decades. Herein, we have used a bottom-up proteomic approach to (i) monitor the capacitation-related changes in the sperm protein levels, and (ii) identify the targets of UPS regulation during sperm capacitation. Spermatozoa were capacitated under proteasomal activity-permissive and inhibiting conditions and extracted sperm proteins were subjected to high-resolution mass spectrometry. We report that 401 individual proteins differed at least two-fold in abundance (P < 0.05) after in vitro capacitation (IVC) and 13 proteins were found significantly different (P < 0.05) between capacitated spermatozoa with proteasomal inhibition compared to the vehicle control. These proteins were associated with biological processes including sperm capacitation, sperm motility, metabolism, binding to zona pellucida, and proteasome-mediated catabolism. Changes in RAB2A, CFAP161, and TTR during IVC were phenotyped by immunocytochemistry, image-based flow cytometry, and Western blotting. We conclude that (i) the sperm proteome is subjected to extensive remodeling during sperm capacitation, and (ii) the UPS has a narrow range of distinct protein substrates during capacitation. This knowledge highlights the importance of the UPS in sperm capacitation and offers opportunities to identify novel pharmacological targets to modulate sperm fertilizing ability for the benefit of human reproductive health, assisted reproductive therapy, and contraception, as well as reproductive management in food animal agriculture.
Department of Animal Science Iowa State University Ames IA 50011 USA
Department of Obstetrics Gynecology and Women's Health University of Missouri Columbia MO 65211 USA
Division of Animal Sciences University of Missouri Columbia MO 65211 5300 USA
HMRI Infertility and Reproduction Research Program University of Newcastle Callaghan NSW Australia
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Austin, C. R. Observations on the penetration of the sperm in the mammalian egg. PubMed
Chang, M. C. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. PubMed DOI
Suarez, S. S. The oviductal sperm reservoir in mammals: Mechanisms of formation. PubMed DOI
Florman, H. M. & Ducibella, T. Fertilization in Mammals. In
Florman, H. M. & Fissore, R. A. Fertilization in Mammals. In
Yanagimachi, R. in
Guidobaldi, H. A., Teves, M. E., Uñates, D. R., Anastasía, A. & Giojalas, L. C. Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PubMed DOI PMC
Oren-Benaroya, R., Orvieto, R., Gakamsky, A., Pinchasov, M. & Eisenbach, M. The sperm chemoattractant secreted from human cumulus cells is progesterone. PubMed DOI
Pérez-Cerezales, S., López-Cardona, A. P. & Gutiérrez-Adán, A. Progesterone effects on mouse sperm kinetics in conditions of viscosity. PubMed DOI
Villanueva-Díaz, C., Arias-Martínez, J., Bermejo-Martínez, L. & Vadillo-Ortega, F. Progesterone induces human sperm chemotaxis. PubMed DOI
Kerns, K., Zigo, M., Drobnis, E. Z., Sutovsky, M. & Sutovsky, P. Zinc ion flux during mammalian sperm capacitation. PubMed DOI PMC
Kerns, K., Zigo, M. & Sutovsky, P. Zinc: A necessary ion for mammalian sperm fertilization competency. PubMed DOI PMC
Bhakta, H. H., Refai, F. H. & Avella, M. A. The molecular mechanisms mediating mammalian fertilization. PubMed DOI
Siu, K. K., Serrão, V. H. B., Ziyyat, A. & Lee, J. E. The cell biology of fertilization: Gamete attachment and fusion. PubMed DOI PMC
Tumova, L., Zigo, M., Sutovsky, P., Sedmikova, M. & Postlerova, P. Ligands and receptors involved in the sperm-zona pellucida interactions in mammals. PubMed DOI PMC
Bailey, J. L. Factors regulating sperm capacitation. PubMed DOI
Hunt, L. T. & Dayhoff, M. O. Amino-terminal sequence identity of ubiquitin and the nonhistone component of nuclear protein A24. PubMed DOI
Hershko, A. & Heller, H. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. PubMed DOI
Hough, R., Pratt, G. & Rechsteiner, M. Ubiquitin-lysozyme conjugates. Identification and characterization of an ATP-dependent protease from rabbit reticulocyte lysates. PubMed DOI
Waxman, L., Fagan, J. M. & Goldberg, A. L. Demonstration of two distinct high molecular weight proteases in rabbit reticulocytes, one of which degrades ubiquitin conjugates. PubMed DOI
Ciechanover, A., Elias, S., Heller, H. & Hershko, A. “Covalent affinity” purification of ubiquitin-activating enzyme. PubMed DOI
Hershko, A., Heller, H., Elias, S. & Ciechanover, A. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. PubMed DOI
Ciechanover, A. Intracellular protein degradation: From a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. PubMed DOI
Sutovsky, P. Sperm proteasome and fertilization. PubMed DOI
Glickman, M. H. & Ciechanover, A. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. PubMed DOI
Pickart, C. M. & Cohen, R. E. Proteasomes and their kin: Proteases in the machine age. PubMed DOI
Ciechanover, A. Proteolysis: From the lysosome to ubiquitin and the proteasome. PubMed DOI
Manandhar, G., Schatten, H. & Sutovsky, P. Centrosome reduction during gametogenesis and its significance. PubMed DOI
Mtango, N. R., Latham, K. E. & Sutovsky, P. Deubiquitinating enzymes in oocyte maturation, fertilization and preimplantation embryo development. PubMed DOI
Sutovsky, P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: Killing three birds with one stone. PubMed DOI
Kerns, K., Morales, P. & Sutovsky, P. Regulation of sperm capacitation by the 26S proteasome: An emerging new paradigm in spermatology. PubMed DOI
Song, W. H., Ballard, J. W., Yi, Y. J. & Sutovsky, P. Regulation of mitochondrial genome inheritance by autophagy and ubiquitin-proteasome system: implications for health, fitness, and fertility. PubMed DOI PMC
Sutovsky, P. Sperm-egg adhesion and fusion in mammals. PubMed DOI
Sutovsky, P. & Song, W. H. Post-fertilisation sperm mitophagy: the tale of Mitochondrial Eve and Steve. PubMed DOI
Sutovsky, P., Van Leyen, K., McCauley, T., Day, B. N. & Sutovsky, M. Degradation of paternal mitochondria after fertilization: Implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. PubMed DOI
Yi, Y. J., Manandhar, G., Oko, R. J., Breed, W. G. & Sutovsky, P. Mechanism of sperm-zona pellucida penetration during mammalian fertilization: 26S proteasome as a candidate egg coat lysin. PubMed
Zimmerman, S. & Sutovsky, P. The sperm proteasome during sperm capacitation and fertilization. PubMed DOI
Sharif, M., Kerns, K., Sutovsky, P., Bovin, N. & Miller, D. J. Progesterone induces porcine sperm release from oviduct glycans in a proteasome-dependent manner. PubMed DOI PMC
Zigo, M., Jonakova, V., Manaskova-Postlerova, P., Kerns, K. & Sutovsky, P. Ubiquitin-proteasome system participates in the de-aggregation of spermadhesin and DQH protein during boar sperm capacitation. PubMed DOI
Zigo, M., Kerns, K., Sutovsky, M. & Sutovsky, P. Modifications of the 26S proteasome during boar sperm capacitation. PubMed DOI PMC
Zigo, M., Kerns, K. & Sutovsky, P. The ubiquitin-proteasome system participates in sperm surface subproteome remodeling during boar sperm capacitation. PubMed DOI PMC
Zigo, M., Manaskova-Postlerova, P., Jonakova, V., Kerns, K. & Sutovsky, P. Compartmentalization of the proteasome-interacting proteins during sperm capacitation. PubMed DOI PMC
Song, W. H. & Sutovsky, P. Porcine cell-free system to study mammalian sperm mitophagy. PubMed DOI
Song, W. H., Yi, Y. J., Sutovsky, M., Meyers, S. & Sutovsky, P. The ART and science of sperm mitophagy. PubMed DOI PMC
Song, W. H., Yi, Y. J., Sutovsky, M., Meyers, S. & Sutovsky, P. Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization. PubMed DOI PMC
Zuidema, D., Jones, A., Song, W. H., Zigo, M. & Sutovsky, P. Identification of candidate mitochondrial inheritance determinants using the mammalian cell-free system. PubMed DOI PMC
Benesova, V., Kinterova, V., Kanka, J. & Toralova, T. Potential involvement of SCF-complex in zygotic genome activation during early bovine embryo development. PubMed DOI
Hillman, P., Ickowicz, D., Vizel, R. & Breitbart, H. Dissociation between AKAP3 and PKARII promotes AKAP3 degradation in sperm capacitation. PubMed DOI PMC
Zapata-Carmona, H., Barón, L., Kong, M. & Morales, P. Protein kinase a (PRKA) activity is regulated by the proteasome at the onset of human sperm capacitation. PubMed DOI PMC
Yi, Y. J., Sutovsky, M., Kennedy, C. & Sutovsky, P. Identification of the inorganic pyrophosphate metabolizing, ATP substituting pathway in mammalian spermatozoa. PubMed DOI PMC
Kong, M., Diaz, E. S. & Morales, P. Participation of the human sperm proteasome in the capacitation process and its regulation by protein kinase A and tyrosine kinase. PubMed DOI
Zapata-Carmona, H. PubMed DOI PMC
Blighe, K., Rana, S. & Lewis, M.
Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. PubMed DOI PMC
Kanehisa, M. Toward understanding the origin and evolution of cellular organisms. PubMed DOI PMC
Kanehisa, M., Furumichi, M., Sato, Y., Kawashima, M. & Ishiguro-Watanabe, M. KEGG for taxonomy-based analysis of pathways and genomes. PubMed DOI PMC
Arroteia, K. F. PubMed DOI PMC
Strittmatter, L. PubMed DOI PMC
Tovich, P. R. & Oko, R. J. Somatic histones are components of the perinuclear theca in bovine spermatozoa. PubMed DOI
Hamilton, L. E. PubMed DOI PMC
Torres-Flores, U. & Hernández-Hernández, A. The interplay between replacement and retention of histones in the sperm genome. PubMed DOI PMC
Hirst, J. Mitochondrial complex I. PubMed DOI
Mountjoy, J. R., Xu, W., McLeod, D., Hyndman, D. & Oko, R. RAB2A: A major subacrosomal protein of bovine spermatozoa implicated in acrosomal biogenesis. PubMed DOI
Kisselev, A. F. & Goldberg, A. L. Proteasome inhibitors: From research tools to drug candidates. PubMed DOI
Tanphaichitr, N. PubMed DOI PMC
Asano, A., Nelson, J. L., Zhang, S. & Travis, A. J. Characterization of the proteomes associating with three distinct membrane raft sub-types in murine sperm. PubMed DOI PMC
Nixon, B. & Aitken, R. J. The biological significance of detergent-resistant membranes in spermatozoa. PubMed DOI
Yunes, R., Michaut, M., Tomes, C. & Mayorga, L. S. Rab3A triggers the acrosome reaction in permeabilized human spermatozoa. PubMed DOI
Lopez, C. I., Belmonte, S. A., De Blas, G. A. & Mayorga, L. S. Membrane-permeant Rab3A triggers acrosomal exocytosis in living human sperm. PubMed DOI
Kwon, W. S., Rahman, M. S., Ryu, D. Y., Park, Y. J. & Pang, M. G. Increased male fertility using fertility-related biomarkers. PubMed DOI PMC
Kwon, W. S., Rahman, M. S., Ryu, D. Y., Khatun, A. & Pang, M. G. Comparison of markers predicting litter size in different pig breeds. PubMed DOI
Zoca, S. M., Northrop-Albrecht, E. J., Walker, J. A., Cushman, R. A. & Perry, G. A. Proteomic analyses identify differences between bovine epididymal and ejaculated spermatozoa that contribute to longevity. PubMed DOI
Magalhães, J., Eira, J. & Liz, M. A. The role of transthyretin in cell biology: Impact on human pathophysiology. PubMed DOI PMC
Wang, Q., Liu, C. & Zhang, Z. Transthyretin and normal human pregnancy: Mini review. PubMed DOI
Zigo, M., Jonakova, V. & Manaskova-Postlerova, P. Electrophoretic and zymographic characterization of proteins isolated by various extraction methods from ejaculated and capacitated boar sperms. PubMed DOI
Zigo, M., Jonakova, V., Sulc, M. & Manaskova-Postlerova, P. Characterization of sperm surface protein patterns of ejaculated and capacitated boar sperm, with the detection of ZP binding candidates. PubMed DOI