Bottom-up approach to deciphering the targets of the ubiquitin-proteasome system in porcine sperm capacitation

. 2024 Aug 29 ; 14 (1) : 20159. [epub] 20240829

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39215164
Odkazy

PubMed 39215164
PubMed Central PMC11364869
DOI 10.1038/s41598-024-71056-4
PII: 10.1038/s41598-024-71056-4
Knihovny.cz E-zdroje

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.

Zobrazit více v PubMed

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

Teves, M. E. 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

Zigo, M. PubMed DOI

Zimmerman, S. & Sutovsky, P. The sperm proteasome during sperm capacitation and fertilization. PubMed DOI

Sutovsky, P. PubMed DOI

Baska, K. M. PubMed DOI

Sharif, M. PubMed DOI PMC

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

Mao, J. 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

Qu, X. PubMed DOI

Sanchez, R. PubMed DOI

Yi, Y. J., Sutovsky, M., Kennedy, C. & Sutovsky, P. Identification of the inorganic pyrophosphate metabolizing, ATP substituting pathway in mammalian spermatozoa. PubMed DOI PMC

Hackerova, L. PubMed DOI PMC

Taraschi, A. 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

He, M. PubMed DOI PMC

Arroteia, K. F. PubMed DOI PMC

Beckers, A. PubMed DOI PMC

Strittmatter, L. PubMed DOI PMC

Lee, R. K. PubMed DOI PMC

Eckhardt, K. PubMed DOI

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

Morohoshi, A. PubMed DOI PMC

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

Zhang, M. PubMed DOI PMC

Zigo, M. PubMed DOI

Miles, E. L. PubMed DOI PMC

Kisselev, A. F. & Goldberg, A. L. Proteasome inhibitors: From research tools to drug candidates. PubMed DOI

Kongmanas, K. PubMed DOI

Tanphaichitr, N. PubMed DOI PMC

Nixon, B. PubMed DOI

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

van Gestel, R. A. PubMed DOI

Sleight, S. B. PubMed DOI

Bou Khalil, M. PubMed DOI

Nixon, B. & Aitken, R. J. The biological significance of detergent-resistant membranes in spermatozoa. PubMed DOI

Nixon, B. PubMed DOI

Zigo, M. PubMed DOI PMC

Bae, J. W. PubMed DOI

Kwon, W. S. PubMed DOI PMC

Yunes, R., Michaut, M., Tomes, C. & Mayorga, L. S. Rab3A triggers the acrosome reaction in permeabilized human spermatozoa. PubMed DOI

Belmonte, S. A. 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

Choi, Y. J. 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

Kennedy, C. E. PubMed DOI

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...