Coupling of the polyamine and iron metabolism pathways in the regulation of proliferation: Mechanistic links to alterations in key polyamine biosynthetic and catabolic enzymes

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1864, Issue 9, 2018, Pages 2793-2813

  Lane, Darius J R ^d   Bae, Dong Hun ^a   Siafakas, Aritee R ^a   Suryo Rahmanto, Yohan ^e   Al Akra, Lina ^a   Jansson, Patric J ^a   Casero, Robert A ^b   Richardson, Des R ^a,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Acireductone dioxygenase 1 (ADI1); Iron; Ornithine decarboxylase; Polyamines; S adenosylmethionine (AdoMet); Spermidine spermine N1 acetyltransferase 1 (SAT1)

Indexed keywords

ACIREDUCTONE DIOXYGENASE 1; ADENOSYLMETHIONINE DECARBOXYLASE; ANTIZYME; ANTIZYME INHIBITOR 1; ENZYME; IRON; METHIONINE ADENOSYLTRANSFERASE; METHIONINE ADENOSYLTRANSFERASE 2ALPHA; ORGANIC CATION TRANSPORTER 6; POLYAMINE; POLYAMINE OXIDASE; SPERMIDINE; SPERMINE; SPERMINE N ACETYLTRANSFERASE 1; UNCLASSIFIED DRUG; CHELATING AGENT;

ARTICLE; BIOSYNTHESIS; CATABOLISM; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IRON DEPLETION; IRON METABOLISM; POLYAMINE METABOLISM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; CELL PROLIFERATION; DRUG EFFECT; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; CHELATING AGENTS; DOWN-REGULATION; ENZYMES; HUMANS; IRON; METABOLIC NETWORKS AND PATHWAYS; POLYAMINES; UP-REGULATION;

EID: 85047961643     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2018.05.007     Document Type: Article

References (96)

1. Pegg, A.E., Mammalian polyamine metabolism and function. IUBMB Life 61 (2009), 880–894.
2. Chattopadhyay, M.K., Tabor, C.W., Tabor, H., Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 2261–2265.
3. Bae, D.H., Lane, D.J.R., Jansson, P.J., Richardson, D.R., The old and new biochemistry of polyamines. Biochim. Biophys. Acta, 2018 (In Press).
4. Chattopadhyay, M.K., Tabor, C.W., Tabor, H., Spermidine but not spermine is essential for hypusine biosynthesis and growth in Saccharomyces cerevisiae: spermine is converted to spermidine in vivo by the FMS1-amine oxidase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 13869–13874.
5. Yu, Y., Kovacevic, Z., Richardson, D.R., Tuning cell cycle regulation with an iron key. Cell Cycle 6 (2007), 1982–1994.
6. Oredsson, S.M., Polyamine dependence of normal cell-cycle progression. Biochem. Soc. Trans. 31 (2003), 366–370.
7. Chattopadhyay, M.K., Tabor, C.W., Tabor, H., Absolute requirement of spermidine for growth and cell cycle progression of fission yeast (Schizosaccharomyces pombe). Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 10330–10334.
8. Murray-Stewart, T.R., Woster, P.M., Casero, R.A. Jr., Targeting polyamine metabolism for cancer therapy and prevention. Biochem. J. 473 (2016), 2937–2953.
9. Thomas, T., Thomas, T.J., Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell. Mol. Life Sci. 58 (2001), 244–258.
10. Thomas, T., Thomas, T.J., Polyamine metabolism and cancer. J. Cell. Mol. Med. 7 (2003), 113–126.
11. Chantrel-Groussard, K., Gaboriau, F., Pasdeloup, N., Havouis, R., Nick, H., Pierre, J.L., Brissot, P., Lescoat, G., The new orally active iron chelator ICL670A exhibits a higher antiproliferative effect in human hepatocyte cultures than O-trensox. Eur. J. Pharmacol. 541 (2006), 129–137.
12. Gaboriau, F., Laupen-Chassay, C., Pasdeloup, N., Pierre, J.L., Brissot, P., Lescoat, G., Modulation of cell proliferation and polyamine metabolism in rat liver cell cultures by the iron chelator O-trensox. Biometals 19 (2006), 623–632.
13. Lescoat, G., Chantrel-Groussard, K., Pasdeloup, N., Nick, H., Brissot, P., Gaboriau, F., Antiproliferative and apoptotic effects in rat and human hepatoma cell cultures of the orally active iron chelator ICL670 compared to CP20: a possible relationship with polyamine metabolism. Cell Prolif. 40 (2007), 755–767.
14. Saletta, F., Suryo Rahmanto, Y., Noulsri, E., Richardson, D.R., Iron chelator-mediated alterations in gene expression: identification of novel iron-regulated molecules that are molecular targets of hypoxia-inducible factor-1 alpha and p53. Mol. Pharmacol. 77 (2010), 443–458.
15. Richardson, D.R., Tran, E.H., Ponka, P., The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents. Blood 86 (1995), 4295–4306.
16. Kalinowski, D.S., Richardson, D.R., The evolution of iron chelators for the treatment of iron overload disease and cancer. Pharmacol. Rev. 57 (2005), 547–583.
17. Wagner, A.J., Meyers, C., Laimins, L.A., Hay, N., c-Myc induces the expression and activity of ornithine decarboxylase. Cell Growth Differ. 4 (1993), 879–883.
18. Packham, G., Bello-Fernandez, C., Cleveland, J.L., Position and orientation independent transactivation by c-Myc. Cell. Mol. Biol. Res. 40 (1994), 699–706.
19. Bello-Fernandez, C., Packham, G., Cleveland, J.L., The ornithine decarboxylase gene is a transcriptional target of c-Myc. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 7804–7808.
20. Pegg, A.E., Regulation of ornithine decarboxylase. J. Biol. Chem. 281 (2006), 14529–14532.
21. Kurian, L., Palanimurugan, R., Godderz, D., Dohmen, R.J., Polyamine sensing by nascent ornithine decarboxylase antizyme stimulates decoding of its mRNA. Nature 477 (2011), 490–494.
22. Coffino, P., Regulation of cellular polyamines by antizyme. Nat. Rev. Mol. Cell Biol. 2 (2001), 188–194.
23. Albers, E., Metabolic characteristics and importance of the universal methionine salvage pathway recycling methionine from 5′-methylthioadenosine. IUBMB Life 61 (2009), 1132–1142.
24. Casero, R.A., Pegg, A.E., Polyamine catabolism and disease. Biochem. J. 421 (2009), 323–338.
25. 1-acetyltransferase: a key metabolic regulator. Am. J. Physiol. Endocrinol. Metab. 294 (2008), E995–1010.
26. Pegg, A.E., Casero, R.A. Jr., Current status of the polyamine research field. Methods Mol. Biol. 720 (2011), 3–35.
27. Uemura, T., Yerushalmi, H.F., Tsaprailis, G., Stringer, D.E., Pastorian, K.E., Hawel, L. 3rd, Byus, C.V., Gerner, E.W., Identification and characterization of a diamine exporter in colon epithelial cells. J. Biol. Chem. 283 (2008), 26428–26435.
28. Uemura, T., Stringer, D.E., Blohm-Mangone, K.A., Gerner, E.W., Polyamine transport is mediated by both endocytic and solute carrier transport mechanisms in the gastrointestinal tract. Am. J. Physiol. Gastrointest. Liver Physiol. 299 (2010), G517–522.
29. Lane, D.J.R., Mills, T.M., Shafie, N.H., Merlot, A.M., Saleh Moussa, R., Kalinowski, D.S., Kovacevic, Z., Richardson, D.R., Expanding horizons in iron chelation and the treatment of cancer: role of iron in the regulation of ER stress and the epithelial-mesenchymal transition. Biochim. Biophys. Acta 1845 (2014), 166–181.
30. Le, N.T., Richardson, D.R., Iron chelators with high antiproliferative activity up-regulate the expression of a growth inhibitory and metastasis suppressor gene: a link between iron metabolism and proliferation. Blood 104 (2004), 2967–2975.
31. Liang, S.X., Richardson, D.R., The effect of potent iron chelators on the regulation of p53: examination of the expression, localization and DNA-binding activity of p53 and the transactivation of WAF1. Carcinogenesis 24 (2003), 1601–1614.
32. Fu, D., Richardson, D.R., Iron chelation and regulation of the cell cycle: 2 mechanisms of posttranscriptional regulation of the universal cyclin-dependent kinase inhibitor p21CIP1/WAF1 by iron depletion. Blood 110 (2007), 752–761.
33. Nurtjahja-Tjendraputra, E., Fu, D., Phang, J.M., Richardson, D.R., Iron chelation regulates cyclin D1 expression via the proteasome: a link to iron deficiency-mediated growth suppression. Blood 109 (2007), 4045–4054.
34. Fukuchi, K., Tomoyasu, S., Watanabe, H., Kaetsu, S., Tsuruoka, N., Gomi, K., Iron deprivation results in an increase in p53 expression. Biol. Chem. Hoppe Seyler 376 (1995), 627–630.
35. Lane, D.J.R., Saletta, F., Suryo Rahmanto, Y., Kovacevic, Z., Richardson, D.R., N-myc downstream regulated 1 (NDRG1) is regulated by eukaryotic initiation factor 3a (eIF3a) during cellular stress caused by iron depletion. PLoS One, 8, 2013, e57273.
36. Richardson, D.R., Molecular mechanisms of iron uptake by cells and the use of iron chelators for the treatment of cancer. Curr. Med. Chem. 12 (2005), 2711–2729.
37. Yuan, J., Lovejoy, D.B., Richardson, D.R., Novel di-2-pyridyl-derived iron chelators with marked and selective antitumor activity: in vitro and in vivo assessment. Blood 104 (2004), 1450–1458.
38. Greene, B.T., Thorburn, J., Willingham, M.C., Thorburn, A., Planalp, R.P., Brechbiel, M.W., Jennings-Gee, J., Wilkinson, J.T., Torti, F.M., Torti, S.V., Activation of caspase pathways during iron chelator-mediated apoptosis. J. Biol. Chem. 277 (2002), 25568–25575.
39. Saletta, F., Suryo Rahmanto, Y., Siafakas, A.R., Richardson, D.R., Cellular iron depletion and the mechanisms involved in the iron-dependent regulation of the growth arrest and DNA damage family of genes. J. Biol. Chem. 286 (2011), 35396–35406.
40. Richardson, D.R., Bernhardt, P.V., Crystal and molecular structure of 2-hydroxy-1-naphthaldehyde isonicotinoyl hydrazone (NIH) and its iron(III) complex: an iron chelator with anti-tumour activity. J. Biol. Inorg. Chem. 4 (1999), 266–273.
41. Jansson, P.J., Kalinowski, D.S., Lane, D.J., Kovacevic, Z., Seebacher, N.A., Fouani, L., Sahni, S., Merlot, A.M., Richardson, D.R., The renaissance of polypharmacology in the development of anti-cancer therapeutics: inhibition of the “triad of death” in cancer by Di-2-pyridylketone thiosemicarbazones. Pharmacol. Res. 100 (2015), 255–260.
42. Kalinowski, D.S., Stefani, C., Toyokuni, S., Ganz, T., Anderson, G.J., Subramaniam, N.V., Trinder, D., Olynyk, J.K., Chua, A., Jansson, P.J., Sahni, S., Lane, D.J.R., Merlot, A.M., Kovacevic, Z., Huang, M.L., Lee, C.S., Richardson, D.R., Redox cycling metals: pedaling their roles in metabolism and their use in the development of novel therapeutics. Biochim. Biophys. Acta 1863 (2016), 727–748.
43. Torti, S.V., Torti, F.M., Iron and cancer: more ore to be mined. Nat. Rev. Cancer 13 (2013), 342–355.
44. Richardson, D.R., Iron chelators as therapeutic agents for the treatment of cancer. Crit. Rev. Oncol. Hematol. 42 (2002), 267–281.
45. Ducros, V., Ruffieux, D., Belva-Besnet, H., de Fraipont, F., Berger, F., Favier, A., Determination of dansylated polyamines in red blood cells by liquid chromatography-tandem mass spectrometry. Anal. Biochem. 390 (2009), 46–51.
46. Richardson, D., Baker, E., Two mechanisms of iron uptake from transferrin by melanoma cells. The effect of desferrioxamine and ferric ammonium citrate. J. Biol. Chem. 267 (1992), 13972–13979.
47. Richardson, D.R., Baker, E., The uptake of iron and transferrin by the human malignant melanoma cell. Biochim. Biophys. Acta 1053 (1990), 1–12.
48. Lane, D.J.R., Chikhani, S., Richardson, V., Richardson, D.R., Transferrin iron uptake is stimulated by ascorbate via an intracellular reductive mechanism. Biochim. Biophys. Acta 1833 (2013), 1527–1541.
49. Mosmann, T., Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983), 55–63.
50. Darnell, G., Richardson, D.R., The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents III: the effect of the ligands on molecular targets involved in proliferation. Blood 94 (1999), 781–792.
51. Gao, J., Richardson, D.R., The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents, IV: the mechanisms involved in inhibiting cell-cycle progression. Blood 98 (2001), 842–850.
52. Richardson, D.R., Milnes, K., The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents II: the mechanism of action of ligands derived from salicylaldehyde benzoyl hydrazone and 2-hydroxy-1-naphthylaldehyde benzoyl hydrazone. Blood 89 (1997), 3025–3038.
53. Gutierrez, E.M., Seebacher, N.A., Arzuman, L., Kovacevic, Z., Lane, D.J., Richardson, V., Merlot, A.M., Lok, H., Kalinowski, D.S., Sahni, S., Jansson, P.J., Richardson, D.R., Lysosomal membrane stability plays a major role in the cytotoxic activity of the anti-proliferative agent, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT). Biochim. Biophys. Acta 1863 (2016), 1665–1681.
54. Richardson, D., Baker, E., The uptake of inorganic iron complexes by human melanoma cells. Biochim. Biophys. Acta 1093 (1991), 20–28.
55. Richardson, D., Ponka, P., Baker, E., The effect of the iron(III) chelator, desferrioxamine, on iron and transferrin uptake by the human malignant melanoma cell. Cancer Res. 54 (1994), 685–689.
56. Kaplan, J., Jordan, I., Sturrock, A., Regulation of the transferrin-independent iron transport system in cultured cells. J. Biol. Chem. 266 (1991), 2997–3004.
57. Ward, J.H., Jordan, I., Kushner, J.P., Kaplan, J., Heme regulation of HeLa cell transferrin receptor number. J. Biol. Chem. 259 (1984), 13235–13240.
58. Wardrop, S.L., Watts, R.N., Richardson, D.R., Nitrogen monoxide activates iron regulatory protein 1 RNA-binding activity by two possible mechanisms: effect on the [4Fe-4S] cluster and iron mobilization from cells. Biochemistry 39 (2000), 2748–2758.
59. Wardrop, S.L., Richardson, D.R., The effect of intracellular iron concentration and nitrogen monoxide on Nramp2 expression and non-transferrin-bound iron uptake. Eur. J. Biochem. 263 (1999), 41–49.
60. Ward, J.H., Kushner, J.P., Kaplan, J., Regulation of HeLa cell transferrin receptors. J. Biol. Chem. 257 (1982), 10317–10323.
61. Hentze, M.W., Kuhn, L.C., Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 8175–8182.
62. Richardson, D.R., Ponka, P., The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim. Biophys. Acta 1331 (1997), 1–40.
63. Pegg, A.E., S-Adenosylmethionine decarboxylase. Essays Biochem. 46 (2009), 25–45.
64. Raney, A., Law, G.L., Mize, G.J., Morris, D.R., Regulated translation termination at the upstream open reading frame in s-adenosylmethionine decarboxylase mRNA. J. Biol. Chem. 277 (2002), 5988–5994.
65. Kahana, C., Regulation of cellular polyamine levels and cellular proliferation by antizyme and antizyme inhibitor. Essays Biochem. 46 (2009), 47–61.
66. Heiskala, M., Zhang, J., Hayashi, S., Holtta, E., Andersson, L.C., Translocation of ornithine decarboxylase to the surface membrane during cell activation and transformation. EMBO J. 18 (1999), 1214–1222.
67. Cervelli, M., Amendola, R., Polticelli, F., Mariottini, P., Spermine oxidase: ten years after. Amino Acids 42 (2012), 441–450.
68. Gamble, L.D., Hogarty, M.D., Liu, X., Ziegler, D.S., Marshall, G., Norris, M.D., Haber, M., Polyamine pathway inhibition as a novel therapeutic approach to treating neuroblastoma. Front. Oncol., 2, 2012, 162.
69. Aouida, M., Poulin, R., Ramotar, D., The human carnitine transporter SLC22A16 mediates high affinity uptake of the anticancer polyamine analogue bleomycin-A5. J. Biol. Chem. 285 (2010), 6275–6284.
70. Chen, Y., Kramer, D.L., Li, F., Porter, C.W., Loss of inhibitor of apoptosis proteins as a determinant of polyamine analog-induced apoptosis in human melanoma cells. Oncogene 22 (2003), 4964–4972.
71. Hahm, H.A., Dunn, V.R., Butash, K.A., Deveraux, W.L., Woster, P.M., Casero, R.A. Jr., Davidson, N.E., Combination of standard cytotoxic agents with polyamine analogues in the treatment of breast cancer cell lines. Clin. Cancer Res. 7 (2001), 391–399.
72. Pegg, A.E., Shantz, L.M., Coleman, C.S., Ornithine decarboxylase as a target for chemoprevention. J. Cell. Biochem. Suppl. 22 (1995), 132–138.
73. Raul, F., Revival of 2-(difluoromethyl)ornithine (DFMO), an inhibitor of polyamine biosynthesis, as a cancer chemopreventive agent. Biochem. Soc. Trans. 35 (2007), 353–355.
74. Mirza, A., Wu, Q., Wang, L., McClanahan, T., Bishop, W.R., Gheyas, F., Ding, W., Hutchins, B., Hockenberry, T., Kirschmeier, P., Greene, J.R., Liu, S., Global transcriptional program of p53 target genes during the process of apoptosis and cell cycle progression. Oncogene 22 (2003), 3645–3654.
75. Ou, Y., Wang, S.J., Li, D., Chu, B., Gu, W., Activation of SAT1 engages polyamine metabolism with p53-mediated ferroptotic responses. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E6806–E6812.
76. Sabo, A., Kress, T.R., Pelizzola, M., de Pretis, S., Gorski, M.M., Tesi, A., Morelli, M.J., Bora, P., Doni, M., Verrecchia, A., Tonelli, C., Faga, G., Bianchi, V., Ronchi, A., Low, D., Muller, H., Guccione, E., Campaner, S., Amati, B., Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis. Nature 511 (2014), 488–492.
77. Zeller, K.I., Jegga, A.G., Aronow, B.J., O'Donnell, K.A., Dang, C.V., An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol., 4, 2003, R69.
78. Zhang, A.H., Rao, J.N., Zou, T., Liu, L., Marasa, B.S., Xiao, L., Chen, J., Turner, D.J., Wang, J.Y., p53-dependent NDRG1 expression induces inhibition of intestinal epithelial cell proliferation but not apoptosis after polyamine depletion. Am. J. Physiol. Cell Physiol. 293 (2007), C379–389.
79. Lui, G.Y., Kovacevic, Z., V Menezes, S., Kalinowski, D.S., Merlot, A.M., Sahni, S., Richardson, D.R., Novel thiosemicarbazones regulate the signal transducer and activator of transcription 3 (STAT3) pathway: inhibition of constitutive and interleukin 6-induced activation by iron depletion. Mol. Pharmacol. 87 (2015), 543–560.
80. Li, Q., Kluz, T., Sun, H., Costa, M., Mechanisms of c-myc degradation by nickel compounds and hypoxia. PLoS One, 4, 2009, e8531.
81. An, W.G., Kanekal, M., Simon, M.C., Maltepe, E., Blagosklonny, M.V., Neckers, L.M., Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature 392 (1998), 405–408.
82. Kamada, R., Toguchi, Y., Nomura, T., Imagawa, T., Sakaguchi, K., Tetramer formation of tumor suppressor protein p53: structure, function, and applications. Biopolymers 106 (2016), 598–612.
83. Forbes, S., Clements, J., Dawson, E., Bamford, S., Webb, T., Dogan, A., Flanagan, A., Teague, J., Wooster, R., Futreal, P.A., Stratton, M.R., Cosmic 2005. Br. J. Cancer 94 (2006), 318–322.
84. Avery-Kiejda, K.A., Bowden, N.A., Croft, A.J., Scurr, L.L., Kairupan, C.F., Ashton, K.A., Talseth-Palmer, B.A., Rizos, H., Zhang, X.D., Scott, R.J., Hersey, P., P53 in human melanoma fails to regulate target genes associated with apoptosis and the cell cycle and may contribute to proliferation. BMC Cancer, 11, 2011, 203.
85. Rider, J.E., Hacker, A., Mackintosh, C.A., Pegg, A.E., Woster, P.M., Casero, R.A. Jr., Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33 (2007), 231–240.
86. Sharmin, S., Sakata, K., Kashiwagi, K., Ueda, S., Iwasaki, S., Shirahata, A., Igarashi, K., Polyamine cytotoxicity in the presence of bovine serum amine oxidase. Biochem. Biophys. Res. Commun. 282 (2001), 228–235.
87. Shephard, G.S., Katzhendler, J., Gean, K.F., Kreisel, M., Bachrach, U., Inhibition of bovine serum amine oxidase activity by aminoalkylaminoanthraquinones. Biochem. Pharmacol. 37 (1988), 4780–4783.
88. Tabor, C.W., Tabor, H., Bachrach, U., Identification of the aminoaldehydes produced by the oxidation of spermine and spermidine with purified plasma amine oxidase. J. Biol. Chem. 239 (1964), 2194–2203.
89. Sugiyama, T., Shimada, H., Nomura, M., Miyamoto, K., Aminoguanidine inhibits cell proliferation by prolongation of the mitotic phase. Toxicol. Lett. 69 (1993), 273–278.
90. Pledgie, A., Huang, Y., Hacker, A., Zhang, Z., Woster, P.M., Davidson, N.E., Casero, R.A. Jr., Spermine oxidase SMO(PAOh1), not N1-acetylpolyamine oxidase PAO, is the primary source of cytotoxic H2O2 in polyamine analogue-treated human breast cancer cell lines. J. Biol. Chem. 280 (2005), 39843–39851.
91. Lane, D.J., Merlot, A.M., Huang, M.L., Bae, D.H., Jansson, P.J., Sahni, S., Kalinowski, D.S., Richardson, D.R., Cellular iron uptake, trafficking and metabolism: key molecules and mechanisms and their roles in disease. Biochim. Biophys. Acta 1853 (2015), 1130–1144.
92. Walerych, D., Lisek, K., Sommaggio, R., Piazza, S., Ciani, Y., Dalla, E., Rajkowska, K., Gaweda-Walerych, K., Ingallina, E., Tonelli, C., Morelli, M.J., Amato, A., Eterno, V., Zambelli, A., Rosato, A., Amati, B., Wisniewski, J.R., Del Sal, G., Proteasome machinery is instrumental in a common gain-of-function program of the p53 missense mutants in cancer. Nat. Cell Biol. 18 (2016), 897–909.
93. Pegg, A.E., Functions of polyamines in mammals. J. Biol. Chem. 291 (2016), 14904–14912.
94. Park, M.H., Nishimura, K., Zanelli, C.F., Valentini, S.R., Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38 (2010), 491–500.
95. Clement, P.M., Hanauske-Abel, H.M., Wolff, E.C., Kleinman, H.K., Park, M.H., The antifungal drug ciclopirox inhibits deoxyhypusine and proline hydroxylation, endothelial cell growth and angiogenesis in vitro. Int. J. Cancer 100 (2002), 491–498.
96. Saini, P., Eyler, D.E., Green, R., Dever, T.E., Hypusine-containing protein eIF5A promotes translation elongation. Nature 459 (2009), 118–121.