The 14-3-3 (YWHA) Proteins in Mammalian Reproduction

Authors

  • Santanu De Department of Biological Sciences, Halmos College of Arts and Sciences, Nova Southeastern University, 3301 College Avenue, Fort Lauderdale, Florida 33314, United States of America http://orcid.org/0000-0002-9739-4039

DOI:

https://doi.org/10.21467/ias.10.1.52-59

Abstract

The 14-3-3 (YWHA or Tyrosine 3-Monooxygenase/Tryptophan 5-Monooxygenase Activation protein) is an acidic and homologous protein family involved in regulation of key biological events including cell cycle, signal transduction and development.  They are highly conserved and are expressed ubiquitously across a wide variety of species ranging from plants to animals.  Seven isoforms of 14-3-3 exist in mammals, which are encoded by separate genes, have tissue-specific, developmental stage-specific as well as isoform-specific presence and consequences.  It is known that these proteins play significant roles in mitosis of mammalian cells and meiosis of amphibians.  However, their effects on development and functioning of mammalian gonads and germ cells are not entirely delineated.  This paper, for the first time, provides a comprehensive review of the comparative expression, localization/distribution, binding interactions, and importance of the 14-3-3 proteins in gametogenesis and reproduction among multiple female and male mammalian species.  Thorough understanding of these proteins in oogenesis and spermatogenesis would help elucidate the physiological basis of fertility in mammals, including humans.

Keywords:

14-3-3 proteins, 14-3-3 isoforms, YWHA, mammalan reproduction, gametogenesis

Downloads

Download data is not yet available.

References

M. B. Yaffe, "How do 14-3-3 proteins work?-- Gatekeeper phosphorylation and the molecular anvil hypothesis," FEBS Lett, vol. 513, no. 1, pp. 53-7, Feb 20 2002.

S. E. Meek, W. S. Lane, and H. Piwnica-Worms, "Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins," J Biol Chem, vol. 279, no. 31, pp. 32046-54, Jul 30 2004.

X. Yang et al., "Structural basis for protein-protein interactions in the 14-3-3 protein family," Proc Natl Acad Sci U S A, vol. 103, no. 46, pp. 17237-42, Nov 14 2006.

S. De, "The 14-3-3 (YWHA) Proteins in Signalling and Development of the Fruit Fly, Drosophila melanogaster," International Annals of Science, vol. 9, no. 1, pp. 80-85, 2020.

S. De, J. L. Marcinkiewicz, S. Vijayaraghavan, and D. Kline, "Expression of 14-3-3 protein isoforms in mouse oocytes, eggs and ovarian follicular development," BMC Res Notes, vol. 5, p. 57, Jan 23 2012.

A. A. Eisa et al., "YWHA (14-3-3) protein isoforms and their interactions with CDC25B phosphatase in mouse oogenesis and oocyte maturation," BMC Developmental Biology, vol. 19, no. 1, p. 20, 2019/10/22 2019.

Z. Huang, K. Myers, B. Khatra, and S. Vijayaraghavan, "Protein 14-3-3zeta binds to protein phosphatase PP1gamma2 in bovine epididymal spermatozoa," Biol Reprod, vol. 71, no. 1, pp. 177-84, Jul 2004.

T. Ichimura et al., "Molecular cloning of cDNA coding for brain-specific 14-3-3 protein, a protein kinase-dependent activator of tyrosine and tryptophan hydroxylases," Proc Natl Acad Sci U S A, vol. 85, no. 19, pp. 7084-8, Oct 1988.

A. Aitken, S. Howell, D. Jones, J. Madrazo, and Y. Patel, "14-3-3 alpha and delta are the phosphorylated forms of raf-activating 14-3-3 beta and zeta. In vivo stoichiometric phosphorylation in brain at a Ser-Pro-Glu-Lys MOTIF," J Biol Chem, vol. 270, no. 11, pp. 5706-9, Mar 17 1995.

A. Aitken, "Functional specificity in 14-3-3 isoform interactions through dimer formation and phosphorylation. Chromosome location of mammalian isoforms and variants," Plant Mol Biol, vol. 50, no. 6, pp. 993-1010, Dec 2002.

A. K. Gardino, S. J. Smerdon, and M. B. Yaffe, "Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the X-ray crystal structures of all human 14-3-3 isoforms," Semin Cancer Biol, vol. 16, no. 3, pp. 173-82, Jun 2006.

C. M. Cahill et al., "Phosphatidylinositol 3-kinase signaling inhibits DAF-16 DNA binding and function via 14-3-3-dependent and 14-3-3-independent pathways," J Biol Chem, vol. 276, no. 16, pp. 13402-10, Apr 20 2001.

C. Mackintosh, "Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes," Biochem J, vol. 381, no. Pt 2, pp. 329-42, Jul 15 2004.

K. Rittinger et al., "Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding," Mol Cell, vol. 4, no. 2, pp. 153-66, Aug 1999.

S. De, "Protein 14-3-3 (YWHA) isoforms and their roles in regulating mouse oocyte maturation," Kent State University, 2014.

S. De, J. Marcinkiewicz, and D. Kline, "Expression of 14-3-3 Protein Isoforms in Different Stages of Follicular Development in Adult Mouse Ovaries," Biology of Reproduction, vol. 85, no. Suppl_1, p. 639, 2011.

S. De and D. Kline, "The importance of 14-3-3 (YWHA) proteins in mammalian reproduction and fertility," Conference Presentation, 29th Annual Graduate Research Symposium, Kent State University 2014.

S. De, B. F. Villarreal, S. Vijayaraghavan, and D. Kline, "Identification of 14-3-3 Protein Isoforms and their Differential Subcellular Distribution in Mouse Oocytes and Eggs," Mol Biol Cell #381 vol. 22, 2011.

W. Zhang et al., "The role of 14-3-3 proteins in gynecological tumors," Front Biosci (Landmark Ed), vol. 20, pp. 934-45, Jun 1 2015.

J. Akahira et al., "Decreased expression of 14-3-3 sigma is associated with advanced disease in human epithelial ovarian cancer: its correlation with aberrant DNA methylation," Clin Cancer Res, vol. 10, no. 8, pp. 2687-93, Apr 15 2004.

H. J. Kim et al., "14-3-3zeta Overexpression is Associated with Poor Prognosis in Ovarian Cancer," Yonsei Med J, vol. 59, no. 1, pp. 51-56, Jan 2018.

D. Peddinti, E. Memili, and S. C. Burgess, "Proteomics-based systems biology modeling of bovine germinal vesicle stage oocyte and cumulus cell interaction," PLoS One, vol. 5, no. 6, p. e11240, Jun 21 2010.

A. J. Snow, P. Puri, A. Acker-Palmer, T. Bouwmeester, S. Vijayaraghavan, and D. Kline, "Phosphorylation-dependent interaction of tyrosine 3-monooxygenase/tryptophan 5-monooxygenase activation protein (YWHA) with PADI6 following oocyte maturation in mice," Biol Reprod, vol. 79, no. 2, pp. 337-47, Aug 2008.

Y. Kohama, M. Saito, M. Yada, and H. Sakurai, "Regulation of the stability and activity of CDC25A and CDC25B by protein phosphatase PP2A and 14-3-3 binding," Cell Signal, vol. 54, pp. 10-16, Feb 2019.

M. Conti et al., "Role of cyclic nucleotide signaling in oocyte maturation," vol. 187, no. 1-2, pp. 153-159, 2002.

L. M. Mehlmann, T. L. Jones, and L. A. Jaffe, "Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte," Science, vol. 297, no. 5585, pp. 1343-5, Aug 23 2002.

L. M. Mehlmann, "Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation," Reproduction, vol. 130, no. 6, pp. 791-9, Dec 2005.

B. C. Duckworth, J. S. Weaver, and J. V. Ruderman, "G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A," Proc Natl Acad Sci U S A, vol. 99, no. 26, pp. 16794-9, Dec 24 2002.

G. Pirino, M. P. Wescott, and P. J. Donovan, "Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes," Cell Cycle, vol. 8, no. 4, pp. 665-70, Feb 15 2009.

C. Cui et al., "CDC25B acts as a potential target of PRKACA in fertilized mouse eggs," Biol Reprod, vol. 79, no. 5, pp. 991-8, Nov 2008.

A. J. Lincoln et al., "Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation," Nat Genet, vol. 30, no. 4, pp. 446-9, Apr 2002.

J. Meng et al., "The Role of 14-3-3ε Interaction with Phosphorylated Cdc25B at Its Ser321 in the Release of the Mouse Oocyte from Prophase I Arrest," PLoS One, vol. 8, no. 1, p. e53633, 2013.

S. De and D. Kline, "Interactions of 14-3-3 proteins with CDC25B phosphatase in ovaries and oocytes of adult mice," Conference Presentation, 26th Annual Graduate Research Symposium, Kent State University 2011.

S. De, A. Reese, and D. Kline, "Interactions of 14-3-3 (YWHA) protein isoforms with CDC25B phosphatase in mouse oocytes," Mol Biol Cell, #1571 vol. 23, 2012.

S. De, A. Reese, and D. Kline, "Interactions of 14-3-3 protein isoforms with CDC25B phosphatase in mouse oocyte maturation," Conference Presentation, Duolink User Meeting 2011.

S. De, A. Reese, and D. Kline, "Duolink in situ proximity ligation assays reveal interactions of 14-3-3 protein isoforms with CDC25B phosphatase in mouse oocyte maturation," Conference Presentation, 27th Annual Graduate Research Symposium, Kent State University 2012.

A. C. Detwiler, S. De, and D. Kline, "Interactions of YWHA (14-3-3) protein isoforms with CDC25B phosphatase in regulating mouse oocyte maturation," Conference Presentation, 48th Annual Meeting of the Society for the Study of Reproduction 2015.

S. De and D. Kline, "Evidence for the requirement of 14-3-3eta (YWHAH) in meiotic spindle assembly during mouse oocyte maturation," (in eng), BMC Dev Biol, vol. 13, p. 10, Apr 1 2013.

S. De and D. Kline, "Erratum to: evidence for the requirement of 14-3-3eta (YWHAH) in meiotic spindle assembly during mouse oocyte maturation," BMC developmental biology, vol. 14, no. 1, p. 20, 2014.

S. De, S. Davis, D. Letwin, C. Mozena, and D. Kline, "Protein 14-3-3 eta (YWHAH) is essential for normal meiotic spindle assembly during in vitro maturation of mouse oocytes," Mol Biol Cell, #1967 vol. 23, 2012.

J. Chaudhary and M. Skinner, "Characterization of a Novel Transcript of 14–3‐3 Theta in Sertoli Cells," Journal of andrology, vol. 21, pp. 730-8, 09/10 2000.

Q. Q. He, X. Wu, X. P. Liu, X. J. Yang, Z. M. Yuan, and Y. Zhang, "14‐3‐3 epsilon plays an important role in testicular germ cell apoptosis: A functional proteomic study of experimental varicocele," Andrologia, vol. 51, no. 6, p. e13275, 2019.

G. Berruti, "A novel rap1/B-Raf/14-3-3 theta protein complex is formed in vivo during the morphogenetic differentiation of postmeiotic male germ cells," Exp Cell Res, vol. 257, no. 1, pp. 172-9, May 25 2000.

E. Aivatiadou, E. Mattei, M. Ceriani, L. Tilia, and G. Berruti, "Impaired fertility and spermiogenetic disorders with loss of cell adhesion in male mice expressing an interfering Rap1 mutant," Mol Biol Cell, vol. 18, no. 4, pp. 1530-42, Apr 2007.

P. Puri, A. Acker-Palmer, R. Stahler, Y. Chen, D. Kline, and S. Vijayaraghavan, "Identification of testis 14-3-3 binding proteins by tandem affinity purification," Spermatogenesis, vol. 1, no. 4, pp. 354-365, Oct 2011.

P. Puri, K. Myers, D. Kline, and S. Vijayaraghavan, "Proteomic analysis of bovine sperm YWHA binding partners identify proteins involved in signaling and metabolism," Biol Reprod, vol. 79, no. 6, pp. 1183-91, Dec 2008.

S. Sun, E. W. Wong, M. W. Li, W. M. Lee, and C. Y. Cheng, "14-3-3 and its binding partners are regulators of protein-protein interactions during spermatogenesis," J Endocrinol, vol. 202, no. 3, pp. 327-36, Sep 2009.

E. W. Wong, D. D. Mruk, W. M. Lee, and C. Y. Cheng, "Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis," Proc Natl Acad Sci U S A, vol. 105, no. 28, pp. 9657-62, Jul 15 2008.

M. Graf, A. Brobeil, K. Sturm, K. Steger, and M. Wimmer, "14-3-3 beta in the healthy and diseased male reproductive system," Hum Reprod, vol. 26, no. 1, pp. 59-66, Jan 2011.

S. Fan et al., "Polarity proteins control ciliogenesis via kinesin motor interactions," Curr Biol, vol. 14, no. 16, pp. 1451-61, Aug 24 2004.

A. A. Eisa, "Role of 14-3-3 eta and epsilon in gametogenesis," Kent State Unversity, 2019.

A. Eisa et al., "The protein YWHAE (14-3-3 epsilon) in spermatozoa is essential for male fertility," Andrology, Jul 13 2020.

Downloads

Published

2020-09-04

Issue

Section

Short Review

How to Cite

[1]
S. . De, “The 14-3-3 (YWHA) Proteins in Mammalian Reproduction”, Int. Ann. Sci., vol. 10, no. 1, pp. 52-59, Sep. 2020.