Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
REVIEW

New functions for old factors: the role of polyamines during the establishment of pregnancy

Jane C. Fenelon https://orcid.org/0000-0001-8771-5196 A C and Bruce D. Murphy B
+ Author Affiliations
- Author Affiliations

A School of BioSciences, The University of Melbourne, Parkville, Vic. 3010, Australia.

B Centre de recherché en reproduction et fertilité, Faculté de médicine vétérinaire, Université de Montréal, 3200 Rue Sicotte, Saint-Hyacinthe, Quebec J2S 2M2, Canada.

C Corresponding author. Email: fenelonj@unimelb.edu.au

Reproduction, Fertility and Development 31(7) 1228-1239 https://doi.org/10.1071/RD18235
Submitted: 21 June 2018  Accepted: 1 October 2018   Published: 13 November 2018

Abstract

Implantation is essential for the establishment of a successful pregnancy, and the preimplantation period plays a significant role in ensuring implantation occurs in a timely and coordinated manner. This requires effective maternal–embryonic signalling, established during the preimplantation period, to synchronise development. Although multiple factors have been identified as present during this time, the exact molecular mechanisms involved are unknown. Polyamines are small cationic molecules that are ubiquitously expressed from prokaryotes to eukaryotes. Despite being first identified over 300 years ago, their essential roles in cell proliferation and growth, including cancer, have only been recently recognised, with new technologies and interest resulting in rapid expansion of the polyamine field. This review provides a summary of our current understanding of polyamine synthesis, regulation and function with a focus on recent developments demonstrating the requirements for polyamines during the establishment of pregnancy up to the implantation stage, in particular the role of polyamines in the control of embryonic diapause and the identification of an alternative pathway for their synthesis in sheep pregnancy. This, along with other novel discoveries, provides new insights into the control of the peri-implantation period in mammals and highlights the complexities that exist in regulating this critical period of pregnancy.

Additional keywords: blastocyst, comparative reproduction, diapause, implantation, uterus.


References

Abdulhussein, A. A., and Wallace, H. M. (2014). Polyamines and membrane transporters. Amino Acids 46, 655–660.
Polyamines and membrane transporters.Crossref | GoogleScholarGoogle Scholar |

Agostinelli, E., Marques, M. P. M., Calheiros, R., Gil, F. P. S. C., Tempera, G., Viceconte, N., Battaglia, V., Grancara, S., and Toninello, A. (2010). Polyamines: fundamental characters in chemistry and biology. Amino Acids 38, 393–403.
Polyamines: fundamental characters in chemistry and biology.Crossref | GoogleScholarGoogle Scholar |

Alexandre, H. (1979). The utilization of an inhibitor of spermidine and spermine synthesis as a tool for the study of the determination of cavitation in the preimplantation mouse embryo. J. Embryol. Exp. Morphol. 53, 145–162.

Alm, K., and Oredsson, S. (2009). Cells and polyamines do it cyclically. Essays Biochem. 46, 63–76.
Cells and polyamines do it cyclically.Crossref | GoogleScholarGoogle Scholar |

Arruabarrena-Aristorena, A., Zabala-Letona, A., and Carracedo, A. (2018). Oil for the cancer engine: the cross-talk between oncogenic signaling and polyamine metabolism. Sci. Adv. 4, eaar2606.
Oil for the cancer engine: the cross-talk between oncogenic signaling and polyamine metabolism.Crossref | GoogleScholarGoogle Scholar |

Bachrach, U. (2010). The early history of polyamine research. Plant Physiol. Biochem. 48, 490–495.
The early history of polyamine research.Crossref | GoogleScholarGoogle Scholar |

Bazer, F. W., Song, G., Kim, J., Erikson, D. W., Johnson, G. A., Burghardt, R. C., Gao, H., Satterfield, M. C., Spencer, T. E., and Wu, G. (2012). Mechanistic mammalian target of rapamycin (MTOR) cell signaling: effects of select nutrients and secreted phosphoprotein 1 on development of mammalian conceptuses. Mol. Cell. Endocrinol. 354, 22–33.
Mechanistic mammalian target of rapamycin (MTOR) cell signaling: effects of select nutrients and secreted phosphoprotein 1 on development of mammalian conceptuses.Crossref | GoogleScholarGoogle Scholar |

Bello-Fernandez, C., Packham, G., and Cleveland, J. L. (1993). The ornithine decarboxylase gene is a transcriptional target of c-Myc. Proc. Natl Acad. Sci. USA 90, 7804–7808.
The ornithine decarboxylase gene is a transcriptional target of c-Myc.Crossref | GoogleScholarGoogle Scholar |

Belting, M., Mani, K., Jönsson, M., Cheng, F., Sandgren, S., Jonsson, S., Ding, K., Delcros, J.-G., and Fransson, L.-Å. (2003). Glypican-1 is a vehicle for polyamine uptake in mammalian cells. J. Biol. Chem. 278, 47181–47189.
Glypican-1 is a vehicle for polyamine uptake in mammalian cells.Crossref | GoogleScholarGoogle Scholar |

Bhurke, A. S., Bagchi, I. C., and Bagchi, M. K. (2016). Progesterone-regulated endometrial factors controlling implantation. Am. J. Reprod. Immunol. 75, 237–245.
Progesterone-regulated endometrial factors controlling implantation.Crossref | GoogleScholarGoogle Scholar |

Bulut-Karslioglu, A., Biechele, S., Jin, H., Macrae, T. A., Hejna, M., Gertsenstein, M., Song, J. S., and Ramalho-Santos, M. (2016). Inhibition of mTOR induces a paused pluripotent state. Nature 540, 119–123.
Inhibition of mTOR induces a paused pluripotent state.Crossref | GoogleScholarGoogle Scholar |

Cui, X.-S., and Kim, N.-H. (2005). Polyamines inhibit apoptosis in porcine parthenotes developing in vitro. Mol. Reprod. Dev. 70, 471–477.
Polyamines inhibit apoptosis in porcine parthenotes developing in vitro.Crossref | GoogleScholarGoogle Scholar |

D’Amico, D., Antonucci, L., Magno, L. D., Coni, S., Sdruscia, G., Macone, A., Miele, E., Infante, P., Marcotullio, L. D., Smaele, E. D., Ferretti, E., Ciapponi, L., Giangaspero, F., Yates, J. R., Agostinelli, E., Cardinali, B., Screpanti, I., Gulino, A., and Canettieri, G. (2015). Non-canonical hedgehog/AMPK-mediated control of polyamine metabolism supports neuronal and medulloblastoma cell growth. Dev. Cell 35, 21–35.
Non-canonical hedgehog/AMPK-mediated control of polyamine metabolism supports neuronal and medulloblastoma cell growth.Crossref | GoogleScholarGoogle Scholar |

Domashenko, A. D., Latham, K. E., and Hatton, K. S. (1997). Expression of myc-family, myc-interacting, and myc-target genes during preimplantation mouse development. Mol. Reprod. Dev. 47, 57–65.
Expression of myc-family, myc-interacting, and myc-target genes during preimplantation mouse development.Crossref | GoogleScholarGoogle Scholar |

Elmetwally, M. A., Lenis, Y., Tang, W., Wu, G., and Bazer, F. W. (2018). Effects of catecholamines on secretion of interferon tau and expression of genes for synthesis of polyamines and apoptosis by ovine trophectoderm. Biol. Reprod. 99, 611–628.
Effects of catecholamines on secretion of interferon tau and expression of genes for synthesis of polyamines and apoptosis by ovine trophectoderm.Crossref | GoogleScholarGoogle Scholar |

Fenelon, J. C., and Murphy, B. D. (2017). Inhibition of polyamine synthesis causes entry of the mouse blastocyst into embryonic diapause. Biol. Reprod. 97, 119–132.
Inhibition of polyamine synthesis causes entry of the mouse blastocyst into embryonic diapause.Crossref | GoogleScholarGoogle Scholar |

Fenelon, J. C., Banerjee, A., and Murphy, B. D. (2014). Embryonic diapause: development on hold. Int. J. Dev. Biol. 58, 163–174.
Embryonic diapause: development on hold.Crossref | GoogleScholarGoogle Scholar |

Fenelon, J. C., Banerjee, A., Lefèvre, P., Gratin, F., and Murphy, B. D. (2016). Polyamine-mediated effects of prolactin dictate emergence from mink obligate embryonic diapause. Biol. Reprod. 95, 6.
Polyamine-mediated effects of prolactin dictate emergence from mink obligate embryonic diapause.Crossref | GoogleScholarGoogle Scholar |

Flynn, A. T., and Hogarty, M. D. (2018). Myc, oncogenic protein translation, and the role of polyamines. Med. Sci (Basel). 6, 41.

Fozard, J. R., Part, M.-L., Prakash, N. J., Grove, J., Schechter, P. J., Sjoerdsma, A., and Koch-Weser, J. (1980a). l-Ornithine decarboxylase: an essential role in early mammalian embryogenesis. Science 208, 505–508.
l-Ornithine decarboxylase: an essential role in early mammalian embryogenesis.Crossref | GoogleScholarGoogle Scholar |

Fozard, J. R., Part, M.-L., Prakash, N. J., and Grove, J. (1980b). Inhibition of murine embryonic development by alpha-difluromethylornithine, an irreversible inhibitor of ornithine decarboxylase. Eur. J. Pharmacol. 65, 379–391.
Inhibition of murine embryonic development by alpha-difluromethylornithine, an irreversible inhibitor of ornithine decarboxylase.Crossref | GoogleScholarGoogle Scholar |

Fuell, C., Elliott, K. A., Hanfrey, C. C., Franceschetti, M., and Michael, A. J. (2010). Polyamine biosynthetic diversity in plants and algae. Plant Physiol. Biochem. 48, 513–520.
Polyamine biosynthetic diversity in plants and algae.Crossref | GoogleScholarGoogle Scholar |

Galliani, G., Colombo, G., and Luzzani, F. (1983). Contragestational effects of dl-α-difluoro-methylornithine, an irreversible inhibitor of ornithine decarboxylase, in the hamster. Contraception 28, 159–170.
Contragestational effects of dl-α-difluoro-methylornithine, an irreversible inhibitor of ornithine decarboxylase, in the hamster.Crossref | GoogleScholarGoogle Scholar |

González, I. M., Martin, P. M., Burdsal, C., Sloan, J. L., Mager, S., Harris, T., and Sutherland, A. E. (2012). Leucine and arginine regulate trophoblast motility through mTOR-dependent and independent pathways in the preimplantation mouse embryo. Dev. Biol. 361, 286–300.
Leucine and arginine regulate trophoblast motility through mTOR-dependent and independent pathways in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar |

Gugliucci, A. (2004). Polyamines as clinical laboratory tools. Clin. Chim. Acta 344, 23–35.
Polyamines as clinical laboratory tools.Crossref | GoogleScholarGoogle Scholar |

Gwatkin, R. B. L. (1966). Defined media and development of mammalian eggs in vitro. Ann. N. Y. Acad. Sci. 139, 79–90.
Defined media and development of mammalian eggs in vitro.Crossref | GoogleScholarGoogle Scholar |

Handa, A. K., Fatima, T., and Mattoo, A. K. (2018). Polyamines: bio-molecules with diverse functions in plant and human health and disease. Front Chem. 6, 10.
Polyamines: bio-molecules with diverse functions in plant and human health and disease.Crossref | GoogleScholarGoogle Scholar |

He, P., Shao, D., Ye, M., and Zhang, G. (2015). Analysis of gene expression identifies candidate markers and pathways in pre-eclampsia. J. Obstet. Gynaecol. 35, 578–584.
Analysis of gene expression identifies candidate markers and pathways in pre-eclampsia.Crossref | GoogleScholarGoogle Scholar |

Heby, O. (1995). DNA methylation and polyamines in embryonic development and cancer. Int. J. Dev. Biol. 39, 737–757.

Horyn, O., Luhovyy, B., Lazarow, A., Daikhin, Y., Nissim, I., Yudkoff, M., and Nissim, I. (2005). Biosynthesis of agmatine in isolated mitochondria and perfused rat liver: studies with 15N-labelled arginine. Biochem. J. 388, 419–425.
Biosynthesis of agmatine in isolated mitochondria and perfused rat liver: studies with 15N-labelled arginine.Crossref | GoogleScholarGoogle Scholar |

Iyo, A. H., Zhu, M.-Y., Ordway, G. A., and Regunathan, S. (2006). Expression of arginine decarboxylase in brain regions and neuronal cells. J. Neurochem. 96, 1042–1050.
Expression of arginine decarboxylase in brain regions and neuronal cells.Crossref | GoogleScholarGoogle Scholar |

James, C., Zhao, T. Y., Rahim, A., Saxena, P., Muthalif, N. A., Uemura, T., Tsuneyoshi, N., Ong, S., Igarashi, K., Lim, C. Y., Dunn, N. R., and Vardy, L. A. (2018). MINDY1 is a downstream target of the polyamines and promotes embryonic stem cell self-renewal. Stem Cells 36, 1170–1178.
MINDY1 is a downstream target of the polyamines and promotes embryonic stem cell self-renewal.Crossref | GoogleScholarGoogle Scholar |

Kahana, C. (2009). Antizyme and antizyme inhibitor, a regulatory tango. Cell. Mol. Life Sci. 66, 2479–2488.
Antizyme and antizyme inhibitor, a regulatory tango.Crossref | GoogleScholarGoogle Scholar |

Kahana, C. (2016). Protein degradation, the main hub in the regulation of cellular polyamines. Biochem. J. 473, 4551–4558.
Protein degradation, the main hub in the regulation of cellular polyamines.Crossref | GoogleScholarGoogle Scholar |

Kim, J., Burghardt, R. C., Wu, G., Johnson, G. A., Spencer, T. E., and Bazer, F. W. (2011). Select nutrients in the ovine uterine lumen. IX. Differential effects of arginine, leucine, glutamine and glucose on interferon tau, ornithine decarboxylase, and nitric oxide synthase in the ovine conceptus. Biol. Reprod. 84, 1139–1147.
Select nutrients in the ovine uterine lumen. IX. Differential effects of arginine, leucine, glutamine and glucose on interferon tau, ornithine decarboxylase, and nitric oxide synthase in the ovine conceptus.Crossref | GoogleScholarGoogle Scholar |

Kong, X., Wang, X., Yin, Y., Li, X., Gao, H., Bazer, F. W., and Wu, G. (2014). Putrescine stimulates the mTOR signaling pathway and protein synthesis in porcine trophectoderm cells. Biol. Reprod. 91, 106.
Putrescine stimulates the mTOR signaling pathway and protein synthesis in porcine trophectoderm cells.Crossref | GoogleScholarGoogle Scholar |

Kusunoki, S., and Yasumasu, I. (1976). Cyclic change in polyamine concentrations in sea urchin eggs related with cleavage cycle. Biochem. Biophys. Res. Commun. 68, 881–885.
Cyclic change in polyamine concentrations in sea urchin eggs related with cleavage cycle.Crossref | GoogleScholarGoogle Scholar |

Kusunoki, S., and Yasumasu, I. (1978). Inhibitory effect of alpha-hydrazinoornithine on egg cleavage in sea urchin eggs. Dev. Biol. 67, 336–345.
Inhibitory effect of alpha-hydrazinoornithine on egg cleavage in sea urchin eggs.Crossref | GoogleScholarGoogle Scholar |

Kwon, H., Wu, G., Bazer, F. W., and Spencer, T. E. (2003). Developmental changes in polyamine levels and synthesis in the ovine conceptus. Biol. Reprod. 69, 1626–1634.
Developmental changes in polyamine levels and synthesis in the ovine conceptus.Crossref | GoogleScholarGoogle Scholar |

Large, M. J., and DeMayo, F. J. (2012). The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling. Mol. Cell. Endocrinol. 358, 155–165.
The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling.Crossref | GoogleScholarGoogle Scholar |

Lefèvre, P. L. C., Palin, M.-F., Beaudry, D., Dobias-Goff, M., Desmarais, J., Llerena, E. M., and Murphy, B. D. (2011a). Uterine signaling at the emergence of the embryo from obligate diapause. Am. J. Physiol. Endocrinol. Metab. 300, E800–E808.
Uterine signaling at the emergence of the embryo from obligate diapause.Crossref | GoogleScholarGoogle Scholar |

Lefèvre, P. L. C., Palin, M.-F., Chen, G., Turecki, G., and Murphy, B. D. (2011b). Polyamines are implicated in the emergence of the embryo from obligate diapause. Endocrinology 152, 1627–1639.
Polyamines are implicated in the emergence of the embryo from obligate diapause.Crossref | GoogleScholarGoogle Scholar |

Lefèvre, P. L. C., Palin, M.-F., and Murphy, B. D. (2011c). Polyamines on the reproductive landscape. Endocr. Rev. 32, 694–712.
Polyamines on the reproductive landscape.Crossref | GoogleScholarGoogle Scholar |

Lenis, Y. Y., Elmetwally, M. A., Maldonado-Estrada, J. G., and Bazer, F. W. (2017). Physiological importance of polyamines. Zygote 25, 244–255.
Physiological importance of polyamines.Crossref | GoogleScholarGoogle Scholar |

Lenis, Y. Y., Elmetwally, M. A., Tang, W., Satterfield, C., Dunlap, K., Wu, G., and Bazer, F. W. (2018a). Functional roles of agmatinase during the peri-implantation period of pregnancy in sheep. Amino Acids 50, 293–308.
Functional roles of agmatinase during the peri-implantation period of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |

Lenis, Y. Y., Johnson, G. A., Wang, X., Tang, W. W., Dunlap, K. A., Satterfield, M. C., Wu, G., Hansen, T. R., and Bazer, F. W. (2018b). Functional roles of ornithine decarboxylase and arginine decarboxylase during the peri-implantation period of pregnancy in sheep. J. Anim. Sci. Biotechnol. 9, 10.
Functional roles of ornithine decarboxylase and arginine decarboxylase during the peri-implantation period of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |

Liang, X.-H., Zhao, Z.-A., Deng, W.-B., Tian, Z., Lei, W., Xu, X., Zhang, X.-H., Su, R.-W., and Yang, Z.-M. (2010). Estrogen regulates amiloride-binding protein 1 through CCAAT/enhancer-binding protein-β in mouse uterus during embryo implantation and decidualization. Endocrinology 151, 5007–5016.
Estrogen regulates amiloride-binding protein 1 through CCAAT/enhancer-binding protein-β in mouse uterus during embryo implantation and decidualization.Crossref | GoogleScholarGoogle Scholar |

Liu, G.-Y., Hung, Y.-C., Hsu, P.-C., Liao, Y.-F., Chang, W.-H., Tsay, G. J., and Hung, H.-C. (2005). Ornithine decarboxylase prevents tumor necrosis factor alpha-induced apoptosis by decreasing intracellular reactive oxygen species. Apoptosis 10, 569–581.
Ornithine decarboxylase prevents tumor necrosis factor alpha-induced apoptosis by decreasing intracellular reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |

López-Contreras, A. J., Ramos-Molina, B., Cremades, A., and Peñafiel, R. (2010). Antizyme inhibitor 2: molecular, cellular and physiological aspects. Amino Acids 38, 603–611.
Antizyme inhibitor 2: molecular, cellular and physiological aspects.Crossref | GoogleScholarGoogle Scholar |

López-Gárcia, C., López-Contreras, A. J., Cremades, A., Castells, M. T., Marín, F., Shreiber, F., and Peñafiel, R. (2008). Molecular and morphological changes in placenta and embryo-development associated with the inhibition of polyamine synthesis during midpregnancy in mice. Endocrinology 149, 5012–5023.
Molecular and morphological changes in placenta and embryo-development associated with the inhibition of polyamine synthesis during midpregnancy in mice.Crossref | GoogleScholarGoogle Scholar |

Löwkvist, B., Heby, O., and Emanuelsson, H. (1980). Essential role of the polyamines in early chick embryo development. J. Embryol. Exp. Morphol. 60, 83–92.

Mamont, P. S., Duchesne, M.-C., Grove, J., and Bey, P. (1978). Anti-proliferative properties of dl-α-difluromethyl ornithine in cultured cells. A consequence of the irreversible inhibition of ornithine decarboxylase. Biochem. Biophys. Res. Commun. 81, 58–66.
Anti-proliferative properties of dl-α-difluromethyl ornithine in cultured cells. A consequence of the irreversible inhibition of ornithine decarboxylase.Crossref | GoogleScholarGoogle Scholar |

Marcho, C., Cui, W., and Mager, J. (2015). Epigenetic dynamics during preimplantation development. Reproduction 150, R109–R120.
Epigenetic dynamics during preimplantation development.Crossref | GoogleScholarGoogle Scholar |

Martin, P. M., and Sutherland, A. E. (2001). Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway. Dev. Biol. 240, 182–193.
Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway.Crossref | GoogleScholarGoogle Scholar |

Mehrotra, P. K., Kitchlu, S., and Farheen, S. (1998). Effect of inhibitors of enzymes involved in polyamine biosynthesis pathway on pregnancy in mouse and hamster. Contraception 57, 55–60.
Effect of inhibitors of enzymes involved in polyamine biosynthesis pathway on pregnancy in mouse and hamster.Crossref | GoogleScholarGoogle Scholar |

Michael, A. J. (2016a). Biosynthesis of polyamines and polyamine-containing molecules. Biochem. J. 473, 2315–2329.
Biosynthesis of polyamines and polyamine-containing molecules.Crossref | GoogleScholarGoogle Scholar |

Michael, A. J. (2016b). Polyamines in eukaryotes, bacteria, and archaea. J. Biol. Chem. 291, 14896–14903.
Polyamines in eukaryotes, bacteria, and archaea.Crossref | GoogleScholarGoogle Scholar |

Miller-Fleming, L., Olin-Sandoval, V., Campbell, K., and Ralser, M. (2015). Remaining mysteries of molecular biology: the role of polyamines in the cell. J. Mol. Biol. 427, 3389–3406.
Remaining mysteries of molecular biology: the role of polyamines in the cell.Crossref | GoogleScholarGoogle Scholar |

Nishimura, K., Nakatsu, F., Kashiwagi, K., Ohno, H., Saito, T., and Igarashi, K. (2002). Essential role of S-adenosylmethionine decarboxylase in mouse embryonic development. Genes Cells 7, 41–47.
Essential role of S-adenosylmethionine decarboxylase in mouse embryonic development.Crossref | GoogleScholarGoogle Scholar |

Novotny, W. F., Chassande, O., Baker, M., Lazdunski, M., and Barbry, P. (1994). Diamine oxidase is the amiloride-binding protein and is inhibited by amiloride analogues. J. Biol. Chem. 269, 9921–9925.

Paria, B. C., Ma, W.-g., Tan, J., Raja, S., Das, S. K., Dey, S. K., and Hogan, B. L. M. (2001). Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc. Natl Acad. Sci. USA 98, 1047–1052.
Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors.Crossref | GoogleScholarGoogle Scholar |

Park, M. H., and Nishimura, K. (2010). Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38, 491–500.
Functional significance of eIF5A and its hypusine modification in eukaryotes.Crossref | GoogleScholarGoogle Scholar |

Pegg, A. E. (1984). The role of polyamine depletion and accumulation of decarboxylated S-adenosylmethionine in the inhibition of growth of SV-3T3 cells treated with α-difluormethylornithine. Biochem. J. 224, 29–38.
The role of polyamine depletion and accumulation of decarboxylated S-adenosylmethionine in the inhibition of growth of SV-3T3 cells treated with α-difluormethylornithine.Crossref | GoogleScholarGoogle Scholar |

Pegg, A. E. (2009). S-Adenosylmethionine decarboxylase. Essays Biochem. 46, 25–46.
S-Adenosylmethionine decarboxylase.Crossref | GoogleScholarGoogle Scholar |

Pegg, A. E., and Casero, R. A. (2011). Current status of the polyamine research field. Methods Mol. Biol. 720, 3–35.
Current status of the polyamine research field.Crossref | GoogleScholarGoogle Scholar |

Peña, A., Wu, S., Hickok, N. J., Soprano, D. R., and Soprano, K. J. (1995). Regulation of human ornithine decarboxylase expression following prolonged quiescence: expression following prolonged quiescence: role for the c-Myc/Max protein complex. J. Cell. Physiol. 162, 234–245.
Regulation of human ornithine decarboxylase expression following prolonged quiescence: expression following prolonged quiescence: role for the c-Myc/Max protein complex.Crossref | GoogleScholarGoogle Scholar |

Pendeville, H., Carpino, N., Marine, J.-C., Takahasi, Y., Muller, M., Martial, J. A., and Cleveland, J. L. (2001). The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol. Cell. Biol. 21, 6549–6558.
The ornithine decarboxylase gene is essential for cell survival during early murine development.Crossref | GoogleScholarGoogle Scholar |

Perez-Leal, O., and Merali, S. (2012). Regulation of polyamine metabolism by translational control. Amino Acids 42, 611–617.
Regulation of polyamine metabolism by translational control.Crossref | GoogleScholarGoogle Scholar |

Perez-Leal, O., Barrero, C. A., Clarkson, A. B., Casero, R. A., and Merali, S. (2012). Polyamine-regulated translation of spermidine/spermine-N1-acetyltransferase. Mol. Cell. Biol. 32, 1453–1467.
Polyamine-regulated translation of spermidine/spermine-N1-acetyltransferase.Crossref | GoogleScholarGoogle Scholar |

Poulin, R. (2012). Recent advances in the molecular biology of metazoan polyamine transport. Amino Acids 42, 711–723.
Recent advances in the molecular biology of metazoan polyamine transport.Crossref | GoogleScholarGoogle Scholar |

Ramani, D., Bandt, J. P. D., and Cynober, L. (2014). Aliphatic polyamines in physiology and diseases. Clin. Nutr. 33, 14–22.
Aliphatic polyamines in physiology and diseases.Crossref | GoogleScholarGoogle Scholar |

Ray, R. M., Bhattacharya, S., Bavaria, M. N., Viar, M. J., and Johnson, L. R. (2014). Spermidine, a sensor for antizyme 1 expression regulates intracellular polyamine homeostasis. Amino Acids 46, 2005–2013.
Spermidine, a sensor for antizyme 1 expression regulates intracellular polyamine homeostasis.Crossref | GoogleScholarGoogle Scholar |

Reddy, P. R. K., and Rukmini, V. (1981). α-Difluormethylornithine as a postcoitally effective antifertility agent in female rats. Contraception 24, 215–221.
α-Difluormethylornithine as a postcoitally effective antifertility agent in female rats.Crossref | GoogleScholarGoogle Scholar |

Renfree, M. B., and Fenelon, J. C. (2017). The enigma of embryonic diapause. Development 144, 3199–3210.
The enigma of embryonic diapause.Crossref | GoogleScholarGoogle Scholar |

Rider, J. E., Hacker, A., Mackintosh, C. A., Pegg, A. E., Woster, P. M., and Casero, R. A. (2007). Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33, 231–240.
Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar |

Russell, D. H. (1971). Putrescine and spermidine biosynthesis in the development of normal and anucleolate mutants of Xenopus laevis. Proc. Natl Acad. Sci. USA 68, 523–527.
Putrescine and spermidine biosynthesis in the development of normal and anucleolate mutants of Xenopus laevis.Crossref | GoogleScholarGoogle Scholar |

Saunderson, R., and Heald, P. J. (1974). Ornithine decarboxylase activity in the uterus of the rat during early pregnancy. J. Reprod. Fertil. 39, 141–143.
Ornithine decarboxylase activity in the uterus of the rat during early pregnancy.Crossref | GoogleScholarGoogle Scholar |

Scognamiglio, R., Cabezas-Wallscheid, N., Thier, M. C., Altamura, S., Reyes, A., Prendergast, A. M., Baumgartner, D., Carnevalli, L. S., Atzberger, A., Haas, S., van Paleske, L., Boroviak, T., Worsdorfer, P., Essers, M. A. G., Kloz, U., Eisenman, R. N., Edenhofer, F., Bertone, P., Huber, W., Hoeven, F. d., Smith, A., and Trumpp, A. (2016). Myc depletion induces a pluripotent dormant state mimicking diapause. Cell 164, 668–680.
Myc depletion induces a pluripotent dormant state mimicking diapause.Crossref | GoogleScholarGoogle Scholar |

Seiler, N. (1987). Functions of polyamine acetylation. Can. J. Physiol. Pharmacol. 65, 2024–2035.
Functions of polyamine acetylation.Crossref | GoogleScholarGoogle Scholar |

Seiler, N. (2004). Catabolism of polyamines. Amino Acids 26, 217–233.
Catabolism of polyamines.Crossref | GoogleScholarGoogle Scholar |

Shantz, L. M., and Pegg, A. E. (1999). Translational regulation of ornithine decarboxylase and other enzymes of the polyamine pathway. Int. J. Biochem. Cell Biol. 31, 107–122.
Translational regulation of ornithine decarboxylase and other enzymes of the polyamine pathway.Crossref | GoogleScholarGoogle Scholar |

Silva, T. M., Cirenajwis, H., Wallace, H. M., Oredsson, S., and Persson, L. (2015). A role for antizyme inhibitor in cell proliferation. Amino Acids 47, 1341–1352.
A role for antizyme inhibitor in cell proliferation.Crossref | GoogleScholarGoogle Scholar |

Soprano, K. J. (1994). WI-38 cell long-term quiescence model system: a valuable tool to study molecular events that regulate growth. J. Cell. Biochem. 54, 405–414.
WI-38 cell long-term quiescence model system: a valuable tool to study molecular events that regulate growth.Crossref | GoogleScholarGoogle Scholar |

Thomas, T., and Thomas, T. J. (2001). Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell. Mol. Life Sci. 58, 244–258.
Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications.Crossref | GoogleScholarGoogle Scholar |

Van Winkle, L. J., and Campione, A. L. (1983). Effect of inhibitors of polyamine synthesis on activation of diapausing mouse blastocyst in vitro. J. Reprod. Fertil. 68, 437–444.
Effect of inhibitors of polyamine synthesis on activation of diapausing mouse blastocyst in vitro.Crossref | GoogleScholarGoogle Scholar |

Van Winkle, L. J., Tesch, J. K., Shah, A., and Campione, A. L. (2006). System B0,+ amino acid transport regulates the penetration stage of blastocyst implantation with possible long-term developmental consequences through adulthood. Hum. Reprod. Update 12, 145–157.
System B0,+ amino acid transport regulates the penetration stage of blastocyst implantation with possible long-term developmental consequences through adulthood.Crossref | GoogleScholarGoogle Scholar |

Wallace, H. M., Fraser, A. V., and Hughes, A. (2003). A perspective of polyamine metabolism. Biochem. J. 376, 1–14.
A perspective of polyamine metabolism.Crossref | GoogleScholarGoogle Scholar |

Wang, X., Ying, W., Dunlap, K. A., Lin, G., Satterfield, M. C., Burghardt, R. C., Wu, G., and Bazer, F. W. (2014). Arginine decarboxylase and agmatinase: an alternative pathway for de novo biosynthesis of polyamines for development of mammalian conceptuses. Biol. Reprod. 90, 84.
Arginine decarboxylase and agmatinase: an alternative pathway for de novo biosynthesis of polyamines for development of mammalian conceptuses.Crossref | GoogleScholarGoogle Scholar |

Wang, X., Burghardt, R. C., Romero, J. J., Hansen, T. R., Wu, G., and Bazer, F. W. (2015). Functional roles of arginine during the peri-implantation period of pregnancy. III. Arginine stimulates proliferation and interferon tau production by ovine trophectoderm cells via nitric oxide and polyamine–TSC2–MTOR signaling pathways. Biol. Reprod. 92, 75.
Functional roles of arginine during the peri-implantation period of pregnancy. III. Arginine stimulates proliferation and interferon tau production by ovine trophectoderm cells via nitric oxide and polyamine–TSC2–MTOR signaling pathways.Crossref | GoogleScholarGoogle Scholar |

Zeng, X., Mao, X., Huang, Z., Wang, F., Wu, G., and Qiao, S. (2013). Arginine enhances embryo implantation in rats through PI3K/PKB/mTOR/NO signaling pathway during early pregnancy. Reproduction 145, 1–7.
Arginine enhances embryo implantation in rats through PI3K/PKB/mTOR/NO signaling pathway during early pregnancy.Crossref | GoogleScholarGoogle Scholar |

Zhang, D., Zhao, T., Ang, H. S., Chong, P., Saiki, R., Igarashi, K., Yang, H., and Vardy, L. A. (2012). AMD1 is essential for ESC self-renewal and is translationally down-regulated on differentiation to neural precursor cells. Genes Dev. 26, 461–473.
AMD1 is essential for ESC self-renewal and is translationally down-regulated on differentiation to neural precursor cells.Crossref | GoogleScholarGoogle Scholar |

Zhao, Y.-C., Chi, Y.-J., Yu, Y.-S., Liu, J.-L., Su, R.-W., Ma, X.-H., Shan, C.-H., and Yang, Z.-M. (2008). Polyamines are essential in embryo implantation: expression and function of polyamine-related genes in mouse uterus during peri-implantation period. Endocrinology 149, 2325–2332.
Polyamines are essential in embryo implantation: expression and function of polyamine-related genes in mouse uterus during peri-implantation period.Crossref | GoogleScholarGoogle Scholar |

Zhao, T., Goh, K. J., Ng, H. H., and Vardy, L. A. (2012). A role for polyamine regulators in ESC self-renewal. Cell Cycle 11, 4517–4523.
A role for polyamine regulators in ESC self-renewal.Crossref | GoogleScholarGoogle Scholar |

Zwierzchowski, L., Czlonkowska, M., and Guszkiewicz, A. (1986). Effect of polyamine limitiation on DNA synthesis and development of mouse preimplantation embryos in vitro. J. Reprod. Fertil. 76, 115–121.
Effect of polyamine limitiation on DNA synthesis and development of mouse preimplantation embryos in vitro.Crossref | GoogleScholarGoogle Scholar |