The function of spermine

IUBMB Life

Volumn 66, Issue 1, 2014, Pages 8-18

  Pegg, Anthony E ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

polyamines; Snyder Robinson syndrome; spermine; spermine synthase

Indexed keywords

POLYAMINES; SNYDER-ROBINSON SYNDROME; SPERMINE; SPERMINE SYNTHASE;

ANIMALS; HUMANS; MENTAL RETARDATION, X-LINKED; MICE; SPERMINE; SPERMINE SYNTHASE;

EID: 84893714418     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1237     Document Type: Review

References (67)

1. Leeuwenhoek, A., (1678) Observationes D. Antonii Lewenhoeck, de Natis e semine genitali Animalculis. Phil. Trans. Roy. Soc. 12, 1040-1048.
2. Pegg, A. E., (2009) Mammalian polyamine metabolism and function. IUBMB Life 61, 880-894.
3. Park, M. H., Nishimura, K., Zanelli, C. F., and, Valentini, S. R., (2010) Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 41, 2538-2545.
4. Igarashi, K., and, Kashiwagi, K., (2010) Modulation of cellular function by polyamines. Int. J. Biochem. Cell Biol. 42, 39-51.
5. Nowotarski, S. L., Woster, P. M., and, Casero, R. A. Jr,. (2013) Polyamines and cancer: implications for chemotherapy and chemoprevention. Expert Rev. Mol. Med. 15, e3.
6. Gutierrez, E., Shin, B. S., Woolstenhulme, C. J., Kim, J. R., Saini, P., et al. (2013) eIF5A promotes translation of polyproline motifs. Mol. Cell. 51, 35-45.
7. Pendeville, H., Carpino, N., Marine, J. C., Takahashi, Y., Muller, M., et al. (2001) The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol. Cell. Biol. 21, 6459-6558.
8. Nishimura, K., Nakatsu, F., Kashiwagi, K., Ohno, H., Saito, H., et al. (2002) Essential role of S-adenosylmethionine decarboxylase in mouse embryonic development. Genes Cells 7, 41-47.
9. Pegg, A. E., and, Michael, A. J., (2010) Spermine synthase. Cell. Mol. Life Sci. 67, 113-121.
10. Wu, H., Min, J., Zeng, H., McCloskey, D. E., Ikeguchi, Y., et al. (2008) Crystal structure of human spermine synthase: implications of substrate binding and catalytic mechanism. J. Biol. Chem. 283, 16135-16146.
11. Zhang, Z., Zheng, Y., Petukh, M., Pegg, A., Ikeguchi, Y., et al. (2013) Enhancing human spermine synthase activity by engineered mutations. PLoS Comput. Biol. 9, e1002924.
12. Korhonen, V. P., Niiranen, K., Halmekyto, M., Pietila, M., Diegelman, P., et al. (2001) Spermine deficiency resulting from targeted disruption of the spermine synthase gene in embryonic stem cells leads to enhanced sensitivity to antiproliferative drugs. Mol. Pharmacol. 59, 231-238.
13. Nilsson, J., Gritli-Linde, A., and, Heby, O., (2000) Skin fibroblasts from spermine synthase-deficient hemizygous gryo male (Gy/Y) mice overproduce spermidine and exhibit increased resistance to oxidative stress but decreased resistance to UV irradiation. Biochem. J. 352, 381-387.
14. Mackintosh, C. A., and, Pegg, A. E., (2000) Effect of spermine synthase deficiency on polyamine biosynthesis and content in mice and embryonic fibroblasts and the sensitivity of fibroblasts to 1,3-bis(2-chloroethyl)-N- nitrosourea. Biochem. J. 351, 439-447.
15. Huber, M., and, Poulin, R., (1995) Antiproliferative effect of spermine depletion by N-cyclohexyl-1,3-diaminopropane in human breast cancer cells. Cancer Res. 55, 934-943.
16. Ikeguchi, Y., Mackintosh, C. A., McCloskey, D. E., and, Pegg, A. E., (2003) Effect of spermine synthase on the sensitivity of cells to antitumor agents. Biochem. J. 373, 885-892.
17. Cason, A. L., Ikeguchi, Y., Skinner, C., Wood, T. C., Lubs, H. A., et al. (2003) X-Linked spermine synthase gene (SMS) defect: the first polyamine deficiency syndrome. Eur. J. Hum. Genet. 11, 937-944.
18. Albert, J., Schwartz, C., Boerkoel, C., and, Stevenson, R., (2013) Snyder-Robinson Syndrome, in GeneReviews™ [Internet]. 2013/06/28 ed., University of Washington, Seattle, Seattle (WA).
19. Meyer, R. A. Jr,., Henley, C. M., Meyer, M. H., Morgan, P. L., McDonald, A. G., et al. (1998) Partial deletion of both the spermine synthase gene and the Pex gene in the x-linked hypophosphatemic, Gyro (Gy) mouse. Genomics 48, 289-295.
20. Pegg, A. E., and, Wang, X., (2009) Mouse models to investigate the function of spermine. Commun. Integr. Biol. 2, 271-274.
21. Lyon, M. F., Scriver, C. R., Baker, L. R., Tenenhouse, H. S., Kronick, J., et al. (1986) The Gy mutation: another cause of X-linked hypophosphatemia in mouse. Proc. Natl. Acad. Sci. USA 83, 4899-4903.
22. Lorenz, B., Francis, F., Gempel, J., Böddrich, A. J. M., Schmahl, W., et al. (1998) Spermine deficiency in Gy mice caused by deletion of the spermine synthase gene. Hum. Mol. Genet. 7, 541-547.
23. Wang, X., Ikeguchi, Y., McCloskey, D. E., Nelson, P., and, Pegg, A. E., (2004) Spermine synthesis is required for normal viability, growth and fertility in the mouse. J. Biol. Chem. 49, 51370-51375.
24. Meyer, R. A. Jr,., Meyer, M. H., Gray, R. W., and, Bruns, M. E., (1995) Femoral abnormalities and vitamin D metabolism in X-linked hypophosphatemic (Hyp and Gy) mice. J. Orthop. Res. 13, 30-40.
25. Ikeguchi, Y., Wang, X., McCloskey, D. E., Coleman, C. S., Nelson, P., et al. (2004) Characterization of transgenic mice with widespread overexpression of spermine synthase. Biochem. J. 381, 701-707.
26. Wang, X., Levic, S., Gratton, M. A., Doyle, K. J., Yamoah, E. N., et al. (2009) Spermine synthase deficiency leads to deafness and a profound sensitivity to alpha-difluoromethylornithine. J. Biol. Chem. 284, 930-937.
27. Abdulhussein, A. A., and, Wallace, H. M., Polyamines and membrane transporters. Amino Acids, in press.
28. Poulin, R., Casero, R. A., and, Soulet, D., (2012) Recent advances in the molecular biology of metazoan polyamine transport. Amino Acids 42, 711-723.
29. Pegg, A. E., Wang, X., Schwartz, C. E., and, McCloskey, D. E., (2011) Spermine synthase activity affects the content of decarboxylated S-adenosylmethionine. Biochem. J. 433, 139-144.
30. Sowell, J., Norris, J., Jones, K., Schwartz, C., and, Wood, T., (2011) Diagnostic screening for spermine synthase deficiency by liquid chromatography tandem mass spectrometry. Clin. Chim. Acta 412, 655-660.
31. de Alencastro, G., McCloskey, D. E., Kliemann, S. E., Maranduba, C. M., Pegg, A. E., et al. (2008) New SMS mutation leads to a striking reduction in spermine synthase protein function and a severe form of Snyder-Robinson X-linked recessive mental retardation syndrome. J. Med. Genet. 45, 539-543.
32. Becerra-Solano, L. E., Butler, J., Castañeda-Cisneros, G., McCloskey, D. E., Wang, X., et al. (2009) A missense mutation, p.V132G, in the X-linked spermine synthase gene (SMS) causes Snyder-Robinson syndrome. Am. J. Med. Genet. A 149, 328-335.
33. Schwartz, C. E., Wang, X., Stevenson, R. E., and, Pegg, A. E., (2011) Spermine synthase deficiency resulting in X-linked intellectual disability (Snyder-Robinson syndrome). Methods Mol. Biol. 720, 437-445.
34. Zhang, Z., Norris, J., Schwartz, C., and, Alexov, E., (2011) In silico and in vitro investigations of the mutability of disease-causing missense mutation sites in spermine synthase. PLoS One 6, e20373.
35. Zhang, Z., Norris, J., Kalscheuer, V., Wood, T., Wang, L., et al. (2013) A Y328C missense mutation in spermine synthase causes a mild form of Snyder-Robinson syndrome. Hum. Mol. Genet. 22, 3789-3797.
36. Peron, A., Spaccini, L., Norris, J., Bova, S. M., Selicorni, A., et al. (2013) Snyder-Robinson syndrome: a novel nonsense mutation in spermine synthase and expansion of the phenotype. Am. J. Med. Genet. A 161, 2316-2320.
37. 1-acetyltransferase: a key metabolic regulator. Am. J. Physiol. Endocrinol. Metab. 294, E995-E1010.
38. Casero, R. A. Jr,. and, Pegg, A. E., (2009) Polyamine catabolism and disease. Biochem. J. 421, 323-338.
39. Pegg, A. E., Toxicity of polyamines and their metabolic products. Chem. Res. Toxicol. 26, 1782-1800.
40. Chattopadhyay, M. K., Tabor, C. W., and, Tabor, H., (2006) Polyamine deficiency leads to accumulation of reactive oxygen species in a spe2Delta mutant of Saccharomyces cerevisiae. Yeast 23, 751-761.
41. Rider, J. E., Hacker, A., Mackintosh, C. A., Pegg, A. E., Woster, P. M., et al. (2007) Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33, 231-240.
42. Khan, A. U., Mei, Y. H., and, Wilson, T., (1992) A proposed function for spermine and spermidine: protection of replicating DNA against damage by singlet oxygen. Proc. Natl. Acad. Sci. USA 89, 11426-11427.
43. Ha, H. C., Sirisoma, N. S., Kuppusamy, P., Zweier, J. L., Woster, P. M., et al. (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proc. Natl. Acad. Sci. USA 95, 11140-11145.
44. Tkachenko, A. G., and, Fedotova, M. V., (2007) Dependence of protective functions of Escherichia coli polyamines on strength of stress caused by superoxide radicals. Biochemistry (Mosc) 72, 109-116.
45. Kruger, A., Vowinckel, J., Mulleder, M., Grote, P., Capuano, F., et al. (2013) Tpo1-mediated spermine and spermidine export controls cell cycle delay and times antioxidant protein expression during the oxidative stress response. EMBO Rep. 14, 1113-1119.
46. Sagor, G. H., Berberich, T., Takahashi, Y., Niitsu, M., and, Kusano, T., (2013) The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res. 22, 595-605.
47. Alet, A. I., Sanchez, D. H., Cuevas, J. C., Marina, M., Carrasco, P., et al. (2012) New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci. 182, 94-100.
48. Do, P. T., Degenkolbe, T., Erban, A., Heyer, A. G., Kopka, J., et al. (2013) Dissecting rice polyamine metabolism under controlled long-term drought stress. PLoS One 8, e60325.
49. + channels. J. Gen. Physiol. 127, 467-480.
50. Benedikt, J., Inyushin, M., Kucheryavykh, Y. V., Rivera, Y., Kucheryavykh, L. Y., et al. (2012) Intracellular polyamines enhance astrocytic coupling. Neuroreport 23, 1021-1025.
51. Lopatin, A. N., Shantz, L. M., Mackintosh, C. A., Nichols, C. G., and, Pegg, A. E., (2000) Modulation of potassium channels in the hearts of transgenic and mutant mice with altered polyamine biosynthesis. J. Mol. Cell. Cardiol. 32, 2007-2024.
52. Tjabringa, G. S., Zandieh-Doulabi, B., Helder, M. N., Knippenberg, M., Wuisman, P. I., et al. (2008) The polymine spermine regulates osteogenic differentiation in adipose stem cells. J. Cell. Mol. Med. 12, 1710-1717.
53. Guidotti, S., Facchini, A., Platano, D., Olivotto, E., Minguzzi, M., et al. (2013) Enhanced osteoblastogenesis of adipose-derived stem cells on spermine delivery via beta-catenin activation. Stem Cells Dev. 22, 1588-1601.
54. Lee, M. J., Chen, Y., Huang, Y. P., Hsu, Y. C., Chiang, L. H., et al. (2013) Exogenous polyamines promote osteogenic differentiation by reciprocally regulating osteogenic and adipogenic gene expression. J. Cell. Biochem. 114, 2718-2728.
55. Bethell, D. R., and, Pegg, A. E., (1981) Polyamines are needed for the differentiation of 3T3-L1 fibroblasts into adipose cells. Biochem. Biophys. Res. Commun. 102, 272-278.
56. Ishii, I., Ikeguchi, Y., Mano, H., Wada, M., Pegg, A. E., et al. (2012) Polyamine metabolism is involved in adipogenesis of 3T3-L1 cells. Amino Acids 42, 619-626.
57. Hyvonen, M. T., Koponen, T., Weisell, J., Pietila, M., Khomutov, A. R., et al. (2013) Spermidine promotes adipogenesis of 3T3-L1 cells by preventing interaction of ANP32 with HuR and PP2A. Biochem. J. 453, 467-474.
58. Halmekyto, M., Hyttinen, J. M., Sinervirta, R., Urtrainen, M., Myöhänen, S., et al. (1991) Transgenic mice aberrantly expressing human ornithine decarboxylase gene. J. Biol. Chem. 266, 19746-19751.
59. Ruan, Y., Cheng, M., Ou, Y., Oko, R., and, van der Hoorn, F. A., (2011) Antizyme OAZ3 modulates protein phosphatase activity. J. Biol. Chem. 286, 29417-29427.
60. Deloyer, P., Peulen, O., and, Dandrifosse, G., (2005) Intestinal effects of long-lasting spermine ingestion by suckling rats. Exp. Physiol. 90, 901-908.
61. Perez-Cano, F. J., Gonzalez-Castro, A., Castellote, C., Franch, A., and, Castell, M., (2009) Influence of breast milk polyamines on suckling rat immune system maturation. Dev. Comp. Immunol. 34, 210-218.
62. Plaza-Zamora, J., Sabater-Molina, M., Rodriguez-Palmero, M., Rivero, M., Bosch, V., et al. (2013) Polyamines in human breast milk for preterm and term infants. Br. J. Nutr. 110, 524-528.
63. Wu, H., Min, J., Ikeguchi, Y., Zeng, H., Dong, A., et al. (2007) Structure and mechanism of spermidine synthases. Biochemistry 46, 8331-8339.
64. Shi, C., Welsh, P. A., Sass-Kuhn, S., Wang, X., McCloskey, D. E., et al. (2012) Characterization of transgenic mice with overexpression of spermidine synthase. Amino Acids 42, 495-505.
65. Zhang, Z., Witham, S., Petukh, M., Moroy, G., Miteva, M., et al. (2013) A rational free energy-based approach to understanding and targeting disease-causing missense mutations. J. Am. Med. Inform. Assoc. 20, 643-651.
66. Novoyatleva, T., Tang, Y., Rafalska, I., and, Stamm, S., (2006) Pre-mRNA missplicing as a cause of human disease. Prog. Mol. Subcell. Biol. 44, 27-46.
67. Perez, B., Rodriguez-Pombo, P., Ugarte, M., and, Desviat, L. R., (2012) Readthrough strategies for therapeutic suppression of nonsense mutations in inherited metabolic disease. Mol. Syndromol. 3, 230-236.