journal article Nov 13, 2018

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

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.
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References
94
[1]
Abdulhussein "Polyamines and membrane transporters." Amino Acids (2014) 10.1007/s00726-013-1553-6
[2]
Agostinelli "Polyamines: fundamental characters in chemistry and biology." Amino Acids (2010) 10.1007/s00726-009-0396-7
[3]
Alexandre "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. (1979)
[4]
Alm "Cells and polyamines do it cyclically." Essays Biochem. (2009) 10.1042/bse0460005
[5]
Arruabarrena-Aristorena "Oil for the cancer engine: the cross-talk between oncogenic signaling and polyamine metabolism." Sci. Adv. (2018) 10.1126/sciadv.aar2606
[6]
The early history of polyamine research

Uriel Bachrach

Plant Physiology and Biochemistry 2010 10.1016/j.plaphy.2010.02.003
[7]
Bazer "Mechanistic mammalian target of rapamycin (MTOR) cell signaling: effects of select nutrients and secreted phosphoprotein 1 on development of mammalian conceptuses." Mol. Cell. Endocrinol. (2012) 10.1016/j.mce.2011.08.026
[8]
Bello-Fernandez "The ornithine decarboxylase gene is a transcriptional target of c-Myc." Proc. Natl Acad. Sci. USA (1993) 10.1073/pnas.90.16.7804
[9]
Belting "Glypican-1 is a vehicle for polyamine uptake in mammalian cells." J. Biol. Chem. (2003) 10.1074/jbc.m308325200
[10]
Bhurke "Progesterone-regulated endometrial factors controlling implantation." Am. J. Reprod. Immunol. (2016) 10.1111/aji.12473
[11]
Bulut-Karslioglu "Inhibition of mTOR induces a paused pluripotent state." Nature (2016) 10.1038/nature20578
[12]
Cui "Polyamines inhibit apoptosis in porcine parthenotes developing in vitro." Mol. Reprod. Dev. (2005) 10.1002/mrd.20228
[13]
D’Amico "Non-canonical hedgehog/AMPK-mediated control of polyamine metabolism supports neuronal and medulloblastoma cell growth." Dev. Cell (2015) 10.1016/j.devcel.2015.09.008
[14]
Domashenko "Expression of myc-family, myc-interacting, and myc-target genes during preimplantation mouse development." Mol. Reprod. Dev. (1997) 10.1002/(sici)1098-2795(199705)47:1<57::aid-mrd8>3.0.co;2-p
[15]
Elmetwally "Effects of catecholamines on secretion of interferon tau and expression of genes for synthesis of polyamines and apoptosis by ovine trophectoderm." Biol. Reprod. (2018) 10.1093/biolre/ioy085
[16]
Fenelon "Inhibition of polyamine synthesis causes entry of the mouse blastocyst into embryonic diapause." Biol. Reprod. (2017) 10.1093/biolre/iox060
[17]
Fenelon "Embryonic diapause: development on hold." Int. J. Dev. Biol. (2014) 10.1387/ijdb.140074bm
[18]
Fenelon "Polyamine-mediated effects of prolactin dictate emergence from mink obligate embryonic diapause." Biol. Reprod. (2016) 10.1095/biolreprod.116.139204
[19]
Flynn "Myc, oncogenic protein translation, and the role of polyamines." Med. Sci (Basel). (2018)
[20]
Fozard "l-Ornithine decarboxylase: an essential role in early mammalian embryogenesis." Science (1980) 10.1126/science.6768132
[21]
Fozard "Inhibition of murine embryonic development by alpha-difluromethylornithine, an irreversible inhibitor of ornithine decarboxylase." Eur. J. Pharmacol. (1980) 10.1016/0014-2999(80)90342-8
[22]
Fuell "Polyamine biosynthetic diversity in plants and algae." Plant Physiol. Biochem. (2010) 10.1016/j.plaphy.2010.02.008
[23]
Galliani "Contragestational effects of dl-a-difluoro-methylornithine, an irreversible inhibitor of ornithine decarboxylase, in the hamster." Contraception (1983) 10.1016/0010-7824(83)90015-x
[24]
González "Leucine and arginine regulate trophoblast motility through mTOR-dependent and independent pathways in the preimplantation mouse embryo." Dev. Biol. (2012) 10.1016/j.ydbio.2011.10.021
[25]
Gugliucci "Polyamines as clinical laboratory tools." Clin. Chim. Acta (2004) 10.1016/j.cccn.2004.02.022
[26]
Gwatkin "Defined media and development of mammalian eggs in vitro." Ann. N. Y. Acad. Sci. (1966) 10.1111/j.1749-6632.1966.tb41186.x
[27]
Handa "Polyamines: bio-molecules with diverse functions in plant and human health and disease." Front Chem. (2018) 10.3389/fchem.2018.00010
[28]
He "Analysis of gene expression identifies candidate markers and pathways in pre-eclampsia." J. Obstet. Gynaecol. (2015) 10.3109/01443615.2014.990430
[29]
Heby "DNA methylation and polyamines in embryonic development and cancer." Int. J. Dev. Biol. (1995) 10.1387/ijdb.8645558
[30]
Horyn "Biosynthesis of agmatine in isolated mitochondria and perfused rat liver: studies with 15N-labelled arginine." Biochem. J. (2005) 10.1042/bj20041260
[31]
Iyo "Expression of arginine decarboxylase in brain regions and neuronal cells." J. Neurochem. (2006) 10.1111/j.1471-4159.2005.03544.x
[32]
James "MINDY1 is a downstream target of the polyamines and promotes embryonic stem cell self-renewal." Stem Cells (2018) 10.1002/stem.2830
[33]
Kahana "Antizyme and antizyme inhibitor, a regulatory tango." Cell. Mol. Life Sci. (2009) 10.1007/s00018-009-0033-3
[34]
Kahana "Protein degradation, the main hub in the regulation of cellular polyamines." Biochem. J. (2016) 10.1042/bcj20160519c
[35]
Kim "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. (2011) 10.1095/biolreprod.110.088153
[36]
Kong "Putrescine stimulates the mTOR signaling pathway and protein synthesis in porcine trophectoderm cells." Biol. Reprod. (2014) 10.1095/biolreprod.113.113977
[37]
Kusunoki "Cyclic change in polyamine concentrations in sea urchin eggs related with cleavage cycle." Biochem. Biophys. Res. Commun. (1976) 10.1016/0006-291x(76)91227-4
[38]
Kusunoki "Inhibitory effect of alpha-hydrazinoornithine on egg cleavage in sea urchin eggs." Dev. Biol. (1978) 10.1016/0012-1606(78)90204-x
[39]
Kwon "Developmental changes in polyamine levels and synthesis in the ovine conceptus." Biol. Reprod. (2003) 10.1095/biolreprod.103.019067
[40]
Large "The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling." Mol. Cell. Endocrinol. (2012) 10.1016/j.mce.2011.07.027
[41]
Lefèvre "Uterine signaling at the emergence of the embryo from obligate diapause." Am. J. Physiol. Endocrinol. Metab. (2011) 10.1152/ajpendo.00702.2010
[42]
Lefèvre "Polyamines are implicated in the emergence of the embryo from obligate diapause." Endocrinology (2011) 10.1210/en.2010-0955
[43]
Polyamines on the Reproductive Landscape

Pavine L. C. Lefèvre, Marie-France Palin, Bruce D. Murphy

Endocrine Reviews 2011 10.1210/er.2011-0012
[44]
Lenis "Physiological importance of polyamines." Zygote (2017) 10.1017/s0967199417000120
[45]
Lenis "Functional roles of agmatinase during the peri-implantation period of pregnancy in sheep." Amino Acids (2018) 10.1007/s00726-017-2515-1
[46]
Lenis "Functional roles of ornithine decarboxylase and arginine decarboxylase during the peri-implantation period of pregnancy in sheep." J. Anim. Sci. Biotechnol. (2018) 10.1186/s40104-017-0225-x
[47]
Liang "Estrogen regulates amiloride-binding protein 1 through CCAAT/enhancer-binding protein-ß in mouse uterus during embryo implantation and decidualization." Endocrinology (2010) 10.1210/en.2010-0170
[48]
Liu "Ornithine decarboxylase prevents tumor necrosis factor alpha-induced apoptosis by decreasing intracellular reactive oxygen species." Apoptosis (2005) 10.1007/s10495-005-1891-2
[49]
López-Contreras "Antizyme inhibitor 2: molecular, cellular and physiological aspects." Amino Acids (2010) 10.1007/s00726-009-0419-4
[50]
López-Gárcia "Molecular and morphological changes in placenta and embryo-development associated with the inhibition of polyamine synthesis during midpregnancy in mice." Endocrinology (2008) 10.1210/en.2008-0084

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Published
Nov 13, 2018
Vol/Issue
31(7)
Pages
1228-1239
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Cite This Article
Jane C. Fenelon, Bruce D. Murphy (2018). New functions for old factors: the role of polyamines during the establishment of pregnancy. Reproduction, Fertility and Development, 31(7), 1228-1239. https://doi.org/10.1071/rd18235