Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T07:51:01.322Z Has data issue: false hasContentIssue false

Physiological importance of polyamines

Published online by Cambridge University Press:  07 June 2017

Yasser Y. Lenis*
Affiliation:
Research Group in Animal Science, Faculty of Agricultural Sciences, University of Applied and Environmental Sciences, Calle 222 #55–37, Bogota, Colombia. Department of Animal Science, Texas A&M University, College Station, TX 77843, USA. Center for Animal Biotechnology and Genomics, Texas A&M University, College Station, TX 77843, USA. OHVRI-Group (One Health and Veterinary Innovative Research and Development) School of Veterinary Medicine, Faculty of Agrarian Science, University of Antioquia, Calle 70 # 52-21, Medellin, Colombia.
Mohammed A. Elmetwally
Affiliation:
Department of Animal Science, Texas A&M University, College Station, TX 77843, USA. Center for Animal Biotechnology and Genomics, Texas A&M University, College Station, TX 77843, USA. Department of Theriogenology, Faculty of Veterinary Medicine, University of Mansoura, Mansoura, 35516, Egypt.
Juan G. Maldonado-Estrada
Affiliation:
Center for Animal Biotechnology and Genomics, Texas A&M University, College Station, TX 77843, USA.
Fuller W. Bazer
Affiliation:
Department of Animal Science, Texas A&M University, College Station, TX 77843, USA. Center for Animal Biotechnology and Genomics, Texas A&M University, College Station, TX 77843, USA.
*
All correspondence to: Yasser Y. Lenis. Research Group in Animal Science, Faculty of Agricultural Sciences, University of Applied and Environmental Sciences, Calle 222 #55–37, Bogota, Colombia. E-mail: yasser.lenis@udea.edu.co

Summary

Polyamines are polycationic molecules that contain two or more amino groups (–NH3+) and are present in all eukaryotic and prokaryotic cells. Polyamines are synthesized from arginine, ornithine, and proline, and from methionine as the methyl-group donor. In the traditional pathway for polyamine synthesis, arginase converts arginine into ornithine, which is decarboxylated by ornithine decarboxylase (ODC1) to generate putrescine. The latter is converted to spermidine and spermine. Recent studies have indicated the existence of ‘non-classical pathways’ for the generation of putrescine from arginine and proline in animal cells. Specifically, arginine decarboxylase (ADC) catalyzes the conversion of arginine into agmatine, which is hydrolyzed by agmatinase (AGMAT) to form putrescine. Additionally, proline is oxidized by proline oxidase to yield pyrroline-5-carboxylate, which undergoes transamination with glutamate to produce ornithine for decarboxylation by ODC1. Intracellular production of polyamines is controlled by antizymes binding to and inactivating ODC1. Polyamines exert effects that include stimulation of cell division and proliferation, gene expression for the survival of cells, DNA and protein synthesis, regulation of apoptosis, oxidative stress, angiogenesis, and cell–cell communication activity. Accordingly, polyamines are essential for early embryonic development and successful pregnancy outcome in mammals. In this paper the main concepts on the history, structure and molecular pathways of polyamines as well as their physiological role on angiogenesis, and reproductive physiology are reviewed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, R.G. & Tresini, M. (2000). Oxidative stress and gene regulation. Free Radic. Biol. Med. 28, 463–99.Google Scholar
Ames, B.N., Donald, T.D. & Sanford, M.R. (1958). Presence of polyamines in certain bacterial viruses. Science 127, 814.CrossRefGoogle ScholarPubMed
Arısan, E.D., Ajda, Ç. & Narçin, P.Ü. (2012). Polyamine depletion enhances the roscovitine-induced apoptosis through the activation of mitochondria in HCT116 colon carcinoma cells. Amino Acids 42, 655–65.Google Scholar
Bachrach, U. (2010). The early history of polyamine research. Plant Physiol. Biochem. 48, 490–5.CrossRefGoogle ScholarPubMed
Bazer, F.W., Wu, G., Johnson, G.A., Kim, J. & Song, G. (2011). Uterine histotroph and conceptus development: select nutrients and secreted phosphoprotein 1 affect mechanistic target of rapamycin cell signaling in ewes. Biol. Reprod. 85, 1094–107.Google Scholar
Billington, D.C. (1991). Angiogenesis and its inhibition: potential new therapies in oncology and non-neoplastic diseases. Drug Des. Discov. 8, 335.Google ScholarPubMed
Boettcher, A. (1865). Farblose Krystalle eines eiweissartigen Korpers aus dem menschlichen Sperma dargestellt. Virchows Arch. Pathol. Anat. Physiol. Klin. Med. 32, 525–35.CrossRefGoogle Scholar
Codoñer, F.P., Valls, B.V., Codoñer, A.A. & Eulalia, A.I. (2011). Oxidant mechanisms in childhood obesity: the link between inflammation and oxidative stress. Transl. Res. 158, 369–84.Google Scholar
Coffino, P. (2001). Regulation of cellular polyamines by antizyme. Nat. Rev. Mol. Cell. Biol. 2,188–94.Google Scholar
Conway, E.M., Désiré, C. & Peter, C. (2001). Molecular mechanisms of blood vessel growth. Cardiovasc. Res. 49, 507–21.Google Scholar
Demircan, S.S., Küçük, M., Nergiz Avcıoğlu, S., Zafer, E., Altınkaya, S.Ö., Bıçakçı, B. & Kurt, Ö. (2015). Comparison of maternal and umbilical cord blood HIF-1α and nitric oxide levels in early and late onset preeclamptic pregnancies. Gynecol. Endocrinol. 25,14.Google Scholar
Drolet, G., Dumbroff, E.B., Legge, R.L. & Thompson, J.E. (1986). Radical scavenging properties of polyamines. Phytochemistry 25, 367–71.Google Scholar
Dudley, H.W., Rosenheim, M.C. & Rosenheim, O. (1924). The chemical constitution of spermine. I. The isolation of spermine from animal tissues, and the preparation of its salts. Biochem. J. 18, 1263–72.Google Scholar
Finkel, T. & Nikki, J.H. (2000). Oxidants, oxidative stress and the biology of ageing. Nature 408, 239–47.Google Scholar
Grancara, S., Zonta, F., Ohkubo, S., Brunati, A.M., Agostinelli, E. & Toninello, A. (2015). Pathophysiological implications of mitochondrial oxidative stress mediated by mitochondriotropic agents and polyamines: the role of tyrosine phosphorylation. Amino Acids 47, 869–83.Google Scholar
Gray, C.A., Taylor, K.M., Ramsey, W.S. Hill, J.R., Bazer, F.W., Bartol, F.F. & Spencer, T.E. (2001). Endometrial glands are required for preimplantation conceptus elongation and survival. Biol. Reprod. 1, 1608–13.Google Scholar
Grillo, M.A. & Colombatto, S. (2004). Arginine revisited: minireview article. Amino Acids 26, 345–51.Google Scholar
Harari, P.M., Fuller, D.J. & Eugene, W.G. (1989). Heat shock stimulates polyamine oxidation by two distinct mechanisms in mammalian cell cultures. Int. J. Radiat. Oncol. Biol. Phys. 16, 451–7.Google Scholar
Herbst, E.J. & Esmond, E. S. (1948). Putrescine as a growth factor for Hemophilus parainfluenzae . J. Biol. Chem. 176, 989–90.Google Scholar
Hirst, D.G. & Flitney, F.W. (1997). The physiological importance and therapeutic potential of nitric oxide in the tumour-associated vasculature. In Bicknell, R., Lewis, C.E. & Ferrara, N. (eds), Tumor Angiogenesis. vol. 153–7, Oxford University Press.CrossRefGoogle Scholar
Igarashi, K. & Kashiwagi, K. (2000). Polyamines: mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun. 271, 559–64.Google Scholar
Igarashi, K. & Kashiwagi, K. (2015). Modulation of protein synthesis by polyamines. IUBMB Life 67, 160–9.Google Scholar
Jasnis, M.A., Klein, S., Monte, M., Davel, L., de Lustig, E.S. & Algranati, I.D. (1994). Polyamines prevent DFMO-mediated inhibition of angiogenesis. Cancer Lett. 79, 3943.Google Scholar
Joshi, M. (1997). The importance of l-arginine metabolism in melanoma: an hypothesis for the role of nitric oxide and polyamines in tumor angiogenesis. Free Radic. Biol. Med. 22, 573–8.CrossRefGoogle ScholarPubMed
Kalač, P. (2013). Health effects and occurrence of dietary polyamines: a review for the period 2005–mid 2013. Food Chem. 161, 2739.CrossRefGoogle Scholar
Kim, J.Y., Burghardt, R.C., Wu, G., Johnson, G.A., Spencer, T.E. & Bazer, F.W. (2011). Select nutrients in the ovine uterine lumen. VIII. Arginine stimulates proliferation of ovine trophectoderm cells through MTOR–RPS6K–RPS6 signaling cascade and synthesis of nitric oxide and polyamines. Biol. Reprod. 84, 70–8.Google Scholar
Knowles, R.G. & Salvador, M. (1994). Nitric oxide synthases in mammals. Biochem. J. 298, 249–58.Google Scholar
Kwon, H, Wu, G., Bazer, F.W. & Spencer, T.E. (2003). Developmental changes in polyamine levels and synthesis in the ovine conceptus. Biol. Reprod. 69, 16261634.Google Scholar
Ladenburg, A. & Abel, J. (1888). Ueber das Aethylenimin (Spermin?). Ber Deutsch Chem. Ges. 21, 758–66.Google Scholar
Lefèvre, P.L., Palin, M.F. & Murphy, B.D. (2011). Polyamines on the reproductive landscape. Endocr. Rev. 32, 694712.Google Scholar
Lenis, Y.Y., Olivera, M.A. & Tarazona, A.M. (2010). Molecular signals affecting PGF2α and PGE2 synthesis in bovine endometrium. Rev. Colomb. Cienc. Pecu. 23, 377–89.Google Scholar
Li, H., Meininger, C.J., Kelly, K.A., Hawker, J.R., Morris, S.M. & Wu, G. (2002). Activities of arginase I and II are limiting for endothelial cell proliferation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, 64–9.Google Scholar
Li, X., Fan, X., Zheng, Z.H., Yang, X., Liu, Z., Gong, J.P. & Liang, H.P. (2013). [Protective effects of agmatine on lipopolysaccharide-induced acute hepatic injury in mice]. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue [In Chinese] 25, 720–4.Google Scholar
Liu, Z., Hou, F., Jin, H., Xiao, Y., Fan, X., Yang, X., Yan, J. & Liang, H. (2015). [Effects of agmatine on excessive inflammatory reaction and proliferation of splenic cells in mice with trauma]. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue [In Chinese] 27,110–4.Google Scholar
Medina, M.A., Quesada, A.R., de Castro, I.N. & Sánchez, J.F. (1999). Histamine, polyamines, and cancer. Biochem. Pharmacol. 57, 1341–4.Google Scholar
Moinard, C., Cynober, L. & de Bandt, J.P. (2005). Polyamines: metabolism and implications in human diseases. Clin. Nutr. 24, 184–97.Google Scholar
Morbidelli, L.U., Chang, C.H., Douglas, J.G., Granger, H.J., Ledda, F.A. & Ziche, M.A. (1996). Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. Heart Circ. Physiol. 270, 411–5.Google Scholar
Neufeld, G., Cohen, T., Gengrinovitch, S. & Poltorak, Z. (1999). Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 922.Google Scholar
Papapetropoulos, A., García, C.G., Madri, J.A. & Sessa, W.C. (1997). Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100, 3131–9.Google Scholar
Pegg, A.E. (2009). Mammalian polyamine metabolism and function. IUBMB Life 61, 880–94.Google Scholar
Pipili, S.E., Sakkoula, E., Haralabopoulos, G., Andriopoulou, P., Peristeris, P. & Maragoudakis, M.E. (1994). Evidence that nitric oxide is an endogenous antiangiogenic mediator. Br. J. Pharmacol. 111, 894902.Google Scholar
Rhee, H.J., Kim, E.J. & Lee, J.K. (2007). Physiological polyamines: simple primordial stress molecules. J. Cell. Mol. Med. 11, 685703.Google Scholar
Rider, J.E., Hacker, A., Mackintosh, C.A., Pegg, A.E., Woster, P.M. & Casero, J.R. (2007). Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33, 231–40.Google Scholar
Tabor, H., Celia, W. & Sanford, M. (1961). Rosenthal. The biochemistry of the polyamines: spermidine and spermine. Annu. Rev. Biochem. 30, 579604.Google Scholar
Tadolini, B., Cabrini, L., Landi, L., Varani, E. & Pasquali, P. (1984). Polyamine binding to phospholipid vesicles and inhibition of lipid peroxidation. Biochem. Biophys. Res. Commun. 122, 550–5.Google Scholar
Takahashi, Y., Mai, M. & Nishioka, K. (2000). α-Difluoromethylornithine induces apoptosis as well as anti-angiogenesis in the inhibition of tumor growth and metastasis in a human gastric cancer model. Int. J. Cancer 85, 243–7.Google Scholar
Takigawa, M., Enomoto, M., Nishida, Y., Pan, H.O., Kinoshita, A. & Suzuki, F. (1990a). Tumor angiogenesis and polyamines: α-difluoromethylornithine, an irreversible inhibitor of ornithine decarboxylase, inhibits B16 melanoma-induced angiogenesis in ovo and the proliferation of vascular endothelial cells in vitro . Cancer Res. 50, 4131–8.Google Scholar
Takigawa, M., Nishida, Y., Suzuki, F., Kishi, J.I., Yamashita, K. & Hayakawa, T. (1990b). Induction of angiogenesis in chick yolk-sac membrane by polyamines and its inhibition by tissue inhibitors of metalloproteinases (TIMP and TIMP-2). Biochem. Biophys. Res. Commun. 171, 1264–71.Google Scholar
Tarazona, A.M., Olivera, M.A., Lenis, Y.Y. (2010). Rol de la mitocondria y el estrés oxidativo en el bloqueo del desarrollo de embriones bovinos producidos in vitro . Arch. Med. Vet. 42, 125–33.Google Scholar
Tiburcio, A.F., Altabella, T., Bitrián, M., Alcázar, R. (2014). The roles of polyamines during the lifespan of plants: from development to stress. Planta 240, 118.Google Scholar
Tkachenko, A., Nesterova, L. & Pshenichnov, M. (2001). The role of the natural polyamine putrescine in defense against oxidative stress in Escherichia coli . Arch. Microbiol. 176, 155–7.Google Scholar
Vauquelin, L.N. (1791). Experiences sur le sperme humain. Ann. Chim. 9, 6480.Google Scholar
Venuti, A., Paolini, F., Nasir, L., Corteggio, A., Roperto, S., Campo, M.S. & Borzacchiello, G. (2011). Papillomavirus E5: the smallest oncoprotein with many functions. Mol. Cancer 10, 140.CrossRefGoogle ScholarPubMed
Wang, X., Ikeguchi, Y., McCloskey, D.E., Nelson, P. & Pegg, A.E. (2004). Spermine synthesis is required for normal viability, growth, and fertility in the mouse. J. Biol. Chem. 279, 51370–5.Google Scholar
Wang, J.F., Su, R.B., Wu, N., Xu, B., Lu, X.Q., Liu, Y. & Li, J. (2005). Inhibitory effect of agmatine on proliferation of tumor cells by modulation of polyamine metabolism. Acta Pharmacol. Sin. 26, 616–22.Google Scholar
Wang, X., Wei, Y., Dunlap, K.A., Lin, G., Satterfield, M.C., Burghardt, R.C., Wu, G. & 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.Google Scholar
Weis, S.M. & Cheresh, D.A. (2011). Tumor angiogenesis: molecular pathways and therapeutic targets. Nature Med. 17, 1359–70.Google Scholar
Wu, G., Pond, W.G., Flynn, S.P., Ott, T.L. & Bazer, F.W. (1998). Maternal dietary protein deficiency decreases nitric oxide synthase and ornithine decarboxylase activities in placenta and endometrium of pigs during early gestation. J. Nutr. 128, 2395–402.Google Scholar
Zauberman, H., Michaelson, I.C., Bergmann, F. & Maurice, D.M. (1969). Stimulation of neovascularization of the cornea by biogenic amines. Exp. Eye Res. 8, 7783.Google Scholar
Ziche, M., Morbidelli, L., Masini, E., Amerini, S., Granger, H.J., Maggi, C.A., Geppetti, P. & Ledda, F. (1994). Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest. 94, 2036–44.Google Scholar