Polyamine biosynthesis in Xenopus laevis: the xlAZIN2/xlODC2 gene encodes a lysine/ornithine decarboxylase
Autoři:
Ana Lambertos aff001; Rafael Peñafiel aff001
Působiště autorů:
Department of Biochemistry and Molecular Biology B and Immunology, Faculty of Medicine, University of Murcia, Murcia, Spain
aff001; Biomedical Research Institute of Murcia (IMIB), Murcia, Spain
aff002
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0218500
Souhrn
Ornithine decarboxylase (ODC) is a key enzyme in the biosynthesis of polyamines, organic cations that are implicated in many cellular processes. The enzyme is regulated at the post-translational level by an unusual system that includes antizymes (AZs) and antizyme inhibitors (AZINs). Most studies on this complex regulatory mechanism have been focused on human and rodent cells, showing that AZINs (AZIN1 and AZIN2) are homologues of ODC but devoid of enzymatic activity. Little is known about Xenopus ODC and its paralogues, in spite of the relevance of Xenopus as a model organism for biomedical research. We have used the information existing in different genomic databases to compare the functional properties of the amphibian ODC1, AZIN1 and AZIN2/ODC2, by means of transient transfection experiments of HEK293T cells. Whereas the properties of xlODC1 and xlAZIN1 were similar to those reported for their mammalian orthologues, the former catalyzing the decarboxylation of L-ornithine preferentially to that of L-lysine, xlAZIN2/xlODC2 showed important differences with respect to human and mouse AZIN2. xlAZIN2 did not behave as an antizyme inhibitor, but it rather acts as an authentic decarboxylase forming cadaverine, due to its higher affinity to L-lysine than to L-ornithine as substrate; so, in accordance with this, it should be named as lysine decarboxylase (LDC) or lysine/ornithine decarboxylase (LODC). In addition, AZ1 stimulated the degradation of xlAZIN2 by the proteasome, but the removal of the 21 amino acid C-terminal tail, with a sequence quite different to that of mouse or human ODC, made the protein resistant to degradation. Collectively, our results indicate that in Xenopus there is only one antizyme inhibitor (xlAZIN1) and two decarboxylases, xlODC1 and xlLDC, with clear preferences for L-ornithine and L-lysine, respectively.
Klíčová slova:
Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Animal models – Sequencing techniques – Protein sequencing – Biological cultures – Culture media – Database and informatics methods – Bioinformatics – Sequence analysis – Sequence alignment – Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Amphibians – Frogs – Xenopus – Molecular biology – Molecular biology techniques – Transfection – Biochemistry – Proteins – Protein complexes – Proteasomes – Amino acids – Basic amino acids – Lysine – Engineering and technology – Equipment – Laboratory equipment – Physical sciences – Chemistry – Chemical compounds – Organic compounds – Organic chemistry
Zdroje
1. Pegg AE. Regulation of ornithine decarboxylase. J Biol Chem. 2006; 281(21): 14529–14532. doi: 10.1074/jbc.R500031200 16459331
2. Cohen S. A Guide to the Polyamines. 1997. Oxford, UK: Oxford University Press.
3. Igarashi K, Kashiwagi K. Polyamines: Mysterious modulators of cellular functions. Biochem Biophys Res Commun. 2000; 271(3): 559–564. doi: 10.1006/bbrc.2000.2601 10814501
4. Gerner EW, Meyskens FL. Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer. 2004; 4(10): 781–792. doi: 10.1038/nrc1454 15510159
5. Igarashi K, Kashiwagi K. Modulation of cellular function by polyamines. Int J Biochem Cell Biol. 2010; 42(1): 39–51. doi: 10.1016/j.biocel.2009.07.009 19643201
6. Minois N. Molecular basis of the “anti-aging” effect of spermidine and other natural polyamines—A mini-review. Gerontology. 2014; 60(4): 319–326. doi: 10.1159/000356748
7. Pegg AE. Functions of polyamines in mammals. J Biol Chem. 2016; 291(29): 14904–14912. doi: 10.1074/jbc.R116.731661 27268251
8. Bae DH, Lane DJR, Jansson PJ, Richardson DR. The old and new biochemistry of polyamines. Biochim Biophys Acta Gen Subj. 2018; 1862(9): 2053–2068. doi: 10.1016/j.bbagen.2018.06.004 29890242
9. Coffino P. Regulation of cellular polyamines by antizyme. Nat Rev Mol Cell Biol. 2001; 2: 188–194. 11265248
10. Kahana C. Antizyme and antizyme inhibitor, a regulatory tango. Cell Mol Life Sci. 2009; 66(15): 2479–88. doi: 10.1007/s00018-009-0033-3 19399584
11. Miller-Fleming L, Olin-Sandoval V, Campbell K, Ralser M. Remaining Mysteries of Molecular Biology: The Role of Polyamines in the Cell. J Mol Biol. 2015; 427(21): 3389–3406. doi: 10.1016/j.jmb.2015.06.020 26156863
12. Murakami Y, Matsufuji S, Kameji T, Hayashi SI, Igarashi K, Tamura T, et al. Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature. 1992; 360(6404), 597–599. doi: 10.1038/360597a0 1334232
13. Erales J, Coffino P. Ubiquitin-independent proteasomal degradation. Biochim Biophys Acta—Mol Cell Res. 2014; 1843(1): 216–221
14. Murakami Y, Matsufuji S, Hayashi SI, Tanahashi N, Tanaka K. Degradation of ornithine decarboxylase by the 26S proteasome. Biochem Biophys Res Commun. 2000; 267(1):1–6. 10623564
15. Mangold U. The antizyme family: Polyamines and beyond. IUBMB Life. 2005; 57(10): 671–676. doi: 10.1080/15216540500307031 16223706
16. Kahana C. The antizyme family for regulating polyamines. J Biol Chem. 2018; 293(48):18730–18735. doi: 10.1074/jbc.TM118.003339 30355739
17. Rom E, Kahana C. Polyamines regulate the expression of ornithine decarboxylase antizyme in vitro by inducing ribosomal frame-shifting. Proc Natl Acad Sci. 2006; 91(9), 3959–3963.
18. Matsufuji S, Matsufuji T, Miyazaki Y, Murakami Y, Atkins JF, Gesteland RF, et al. Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell. 1995; 80(1): 51–60. 7813017
19. Wu H-Y, Chen S-F, Hsieh J-Y, Chou F, Wang Y-H, Lin W-T, et al. Structural basis of antizyme-mediated regulation of polyamine homeostasis. Proc Natl Acad Sci USA. 2015; 112(36):11229–11234. doi: 10.1073/pnas.1508187112 26305948
20. Mangold U. Antizyme inhibitor: Mysterious modulator of cell proliferation. Cell Mol Life Sci. 2006; 63(18):2095–2101. doi: 10.1007/s00018-005-5583-4 16847581
21. López-Contreras AJ, Ramos-Molina B, Cremades A, Peñafiel R. Antizyme inhibitor 2: Molecular, cellular and physiological aspects. Amino Acids. 2010; 38: 603–611. doi: 10.1007/s00726-009-0419-4 19956990
22. Ramos-Molina B, Lambertos A, Peñafiel R. Antizyme Inhibitors in Polyamine Metabolism and Beyond: Physiopathological Implications. Med Sci. 2018. doi: 10.3390/medsci6040089 30304856
23. Tang H, Ariki K, Ohkido M, Murakami Y, Matsufuji S, Li Z, et al. Role of ornithine decarboxylase antizyme inhibitor in vivo. Genes to Cells. 2009; 14: 79–87. doi: 10.1111/j.1365-2443.2008.01249.x 19077035
24. Ramos-Molina B, López-Contreras AJ, Cremades A, Peñafiel R. Differential expression of ornithine decarboxylase antizyme inhibitors and antizymes in rodent tissues and human cell lines. Amino Acids. 2012; 42: 539–547. doi: 10.1007/s00726-011-1031-y 21814789
25. Rasila T, Lehtonen A, Kanerva K, Mäkitie LT, Haglund C, Andersson LC. Expression of ODC Antizyme Inhibitor 2 (AZIN2) in Human Secretory Cells and Tissues. PLoS One. 2016; 11: e0151175. doi: 10.1371/journal.pone.0151175 26963840
26. Bercovich Z, Kahana C. Degradation of antizyme inhibitor, an ornithine decarboxylase homologous protein, is ubiquitin-dependent and is inhibited by antizyme. J Biol Chem. 2004; 279(52): 54097–54102. doi: 10.1074/jbc.M410234200 15491992
27. Snapir Z, Keren-Paz A, Bercovich Z, Kahana C. ODCp, a brain- and testis-specific ornithine decarboxylase paralogue, functions as an antizyme inhibitor, although less efficiently than AzI1. Biochem J. 2008; 410: 613–619. 18062773
28. Ghoda L, Phillips MA, Bass KE, Wang CC, Coffino P. Trypanosome ornithine decarboxylase is stable because it lacks sequences found in the carboxyl terminus of the mouse enzyme which target the latter for intracellualr degradation. J Biol Chem. 1990; 265(20):11823–11826.
29. Gupta R, Hamasaki-Katagiri N, Tabor CW, Tabor H. Effect of spermidine on the in vivo degradation of ornithine decarboxylase in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 2002; 98(19):10620–10623.
30. Porat Z, Landau G, Bercovich Z, Krutauz D, Glickman M, Kahana C. Yeast antizyme mediates degradation of yeast ornithine decarboxylase by yeast but not by mammalian proteasome: New insights on yeast antizyme. J Biol Chem. 2008; 283: 4528–4534. doi: 10.1074/jbc.M708088200 18089576
31. Gödderz D, Schäfer E, Palanimurugan R, Dohmen RJ. The N-terminal unstructured domain of yeast odc functions as a transplantable and replaceable ubiquitin-independent degron. J Mol Biol. 2011; 407(3): 354–367. doi: 10.1016/j.jmb.2011.01.051 21295581
32. Osborne HB, Mulner-Lorillon O, Marot J, Belle R. Polyamine levels during Xenopus laevis oogenesis: A role in oocyte competence to meiotic resumption. Biochem Biophys Res Commun. 1989; 158: 520–526. 2917000
33. Osborne HB, Duval C, Ghoda L, Omilli F, Bassez T, Coffino P. Expression and post‐transcriptional regulation of ornithine decarboxylase during early Xenopus development. Eur J Biochem. 1991; 202: 575–581.
34. Osborne HB, Cormier P, Lorillon O, Maniey D, Belle R. An appraisal of the developmental importance of polyamine changes in early Xenopus embryos. Int J Dev Biol. 1993; 37: 615–618. 8180006
35. Bassez T, Paris J, Omilli F, Dorel C, Osborne HB. Post-transcriptional regulation of ornithine decarboxylase in Xenopus laevis oocytes. Development. 1990; 110: 955–962. 2088731
36. Cao Y, Zhao H, Hollemann T, Chen Y, Grunz H. Tissue-specific expression of an Ornithine decarboxylase paralogue, XODC2, in Xenopus laevis. Mech Dev. 2001; 102: 243–246. 11287202
37. López-Contreras AJ, López-Garcia C, Jiménez-Cervantes C, Cremades A, Peñafiel R. Mouse ornithine decarboxylase-like gene encodes an antizyme inhibitor devoid of ornithine and arginine decarboxylating activity. J Biol Chem. 2006; 281(41): 30896–30906. doi: 10.1074/jbc.M602840200 16916800
38. López-Contreras AJ, Ramos-Molina B, Martínez-de-la-Torre M, Peñafiel-Verdú C, Puelles L, Cremades A, et al. Expression of antizyme inhibitor 2 in male haploid germinal cells suggests a role in spermiogenesis. Int J Biochem Cell Biol. 2009; 41(5): 1070–1078. doi: 10.1016/j.biocel.2008.09.029 18973822
39. López-Garcia C, Ramos-Molina B, Lambertos A, López-Contreras AJ, Cremades A, Peñafiel R. Antizyme Inhibitor 2 Hypomorphic Mice. New Patterns of Expression in Pancreas and Adrenal Glands Suggest a Role in Secretory Processes. PLoS One. 2013; 8(7): e69188. doi: 10.1371/journal.pone.0069188 23874910
40. Ramos-Molina B, Lambertos A, López-Contreras AJ, Peñafiel R. Mutational analysis of the antizyme-binding element reveals critical residues for the function of ornithine decarboxylase. Biochim Biophys Acta—Gen Subj. 2013; 1830(11):5157–5165. doi: 10.1016/j.bbagen.2013.07.003
41. Ramos-Molina B, Lambertos A, Lopez-Contreras AJ, Kasprzak JM, Czerwoniec A, Bujnicki JM, et al. Structural and degradative aspects of ornithine decarboxylase antizyme inhibitor 2. FEBS Open Bio. 2014; 4: 510–521. doi: 10.1016/j.fob.2014.05.004 24967154
42. Lambertos A, Ramos-Molina B, López-Contreras AJ, Cremades A, Peñafiel R. New insights of polyamine metabolism in testicular physiology: A role of ornithine decarboxylase antizyme inhibitor 2 (AZIN2) in the modulation of testosterone levels and sperm motility. PLoS One. 2018; 13(12): e0209202. doi: 10.1371/journal.pone.0209202 30566531
43. Seiler N. Liquid Chromatographic Methods for Assaying Polyamines Using Prechromatographic Derivatization. Methods Enzymol. 1983; 94:10–2. 6621380
44. Tsirka S, Coffino P. Dominant negative mutants of ornithine decarboxylase. J Biol Chem. 1992; 267: 23057–23062 1429654
45. Coleman CS, Stanley BA, Pegg AE. Effect of mutations at active site residues on the activity of ornithine decarboxylase and its inhibition by active site-directed irreversible inhibitors. J Biol Chem. 1993; 268: 24572–24579. 8227016
46. Tobias KE, Kahana C. Intersubunit Location of the Active Site of Mammalian Ornithine Decarboxylase As Determined by Hybridization of Site-Directed Mutants. Biochemistry. 1993; 32: 5842–5847. 8504104
47. Kidron H, Repo S, Johnson MS, Salminen TA. Functional classification of amino acid decarboxylases from the alanine racemase structural family by phylogenetic studies. Mol Biol Evol. 2007; 24: 79–89. 16997906
48. Ivanov IP, Firth AE, Atkins JF. Recurrent emergence of catalytically inactive ornithine decarboxylase homologous forms that likely have regulatory function. J Mol Evol. 2010; 70(3): 289–302. doi: 10.1007/s00239-010-9331-5 20217058
49. Pegg AE, McGill S. Decarboxylation of ornithine and lysine in rat tissues. BBA—Enzymol. 1979; 568(2): 416–427.
50. Ghoda L, Van Daalen Wetters T, Macrae M, Ascherman D, Coffino P. Prevention of rapid intracellular degradation of ODC by a carboxyl-terminal truncation. Science. 1989; 243: 1493–1495. 2928784
51. Rosenberg-Hasson Y, Bercovich Z, Kahana C. Characterization of sequences involved in mediating degradation of ornithine decarboxylase in cells and in reticulocyte lysate. Eur J Biochem. 1991; 196: 647–651. 2013288
52. Li X, Coffino P. Regulated degradation of ornithine decarboxylase requires interaction with the polyamine-inducible protein antizyme. Mol Cell Biol. 1992; 12: 3556–3562. 1630460
53. Hamana K, Matsuzaki S. Occurrence of sym-homosphermidine in the Japanese newt, Cynops pyrrhogaster pyrrhogaster. FEBS Lett. 1979; 99: 325–328.
54. Matsuzaki S, Tanaka S, Suzuki M, Hamana K. A possible role of cadaverine in the biosynthesis of polyamines in the japanese newt testis. Endocrinol Jpn. 2011; 28 (3): 305–312.
55. Kurabuchi S, Matsuzaki S, Inoue S. Changes in polyamine content during limb regeneration in adult Xenopus laevis. J Exp Zool. 1983; 227(1): 121–126. 6619761
56. Baby G, Hayashi S. Presence of ornithine decarboxylase antizyme in primary cultured hepatocytes of the frog Xenopus laevis. Biochim Biophys Acta. 1991; 1092 161–164. 2018782
57. López-Contreras AJ, Sánchez-Laorden BL, Ramos-Molina B, De La Morena ME, Cremades A, Peñafiel R. Subcellular localization of antizyme inhibitor 2 in mammalian cells: Influence of intrinsic sequences and interaction with antizymes. J Cell Biochem. 2009; 107(4):732–740. doi: 10.1002/jcb.22168 19449338
58. Kanerva K, Mäkitie LT, Pelander A, Heiskala M, Andersson LC. Human ornithine decarboxylase paralogue (ODCp) is an antizyme inhibitor but not an arginine decarboxylase. Biochem J. 2007; 409(1): 187–192. doi: 10.1042/BJ20071004
59. Kahana C. Protein degradation, the main hub in the regulation of cellular polyamines. Biochem J. 2016; 473(24): 4551–4558. doi: 10.1042/BCJ20160519C 27941031
60. Ghoda L, Sidney D, Macrae M, Coffino P. Structural elements of ornithine decarboxylase required for intracellular degradation and polyamine-dependent regulation. Mol Cell Biol. 1992; 12: 2178–2185. 1569947
61. Li X, Coffino P. Degradation of Ornithine Decarboxylase: Exposure of the C-Terminal Target by a Polyamine-Inducible Inhibitory Protein Downloaded from. Mol Cell Biol. 1993; 13: 2377–2383.
62. Zhang M, Pickart CM, Coffino P. Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate. EMBO J. 2003; 22: 1488–1496. doi: 10.1093/emboj/cdg158 12660156
63. Prakash S, Tian L, Ratliff KS, Lehotzky RE, Matouschek A. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat Struct Mol Biol. 2004; 11: 830–837. 15311270
64. Berko D, Tabachnick-Cherny S, Shental-Bechor D, Cascio P, Mioletti S, Levy Y, et al. The Direction of Protein Entry into the Proteasome Determines the Variety of Products and Depends on the Force Needed to Unfold Its Two Termini. Mol Cell. 2012; 48(4): 601–611. doi: 10.1016/j.molcel.2012.08.029 23041283
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