Advertisement

Amino Acids

, Volume 42, Issue 2–3, pp 411–426 | Cite as

Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants

  • Paraskevi Tavladoraki
  • Alessandra Cona
  • Rodolfo Federico
  • Giampiero Tempera
  • Nikenza Viceconte
  • Stefania Saccoccio
  • Valentina Battaglia
  • Antonio Toninello
  • Enzo Agostinelli
Minireview Article

Abstract

Metabolism of polyamines spermidine and spermine, and their diamine precursor, putrescine, has been a target for antineoplastic therapy since these naturally occurring alkyl amines were found essential for normal mammalian cell growth. Intracellular polyamine concentrations are maintained at a cell type-specific set point through the coordinated and highly regulated interplay between biosynthesis, transport, and catabolism. A correlation between regulation of cell proliferation and polyamine metabolism is described. In particular, polyamine catabolism involves copper-containing amine oxidases and FAD-dependent polyamine oxidases. Several studies showed an important role of these enzymes in several developmental and disease-related processes in both animals and plants through a control on polyamine homeostasis in response to normal cellular signals, drug treatment, environmental and/or cellular stressors. The production of toxic aldehydes and reactive oxygen species, H2O2 in particular, by these oxidases using extracellular and intracellular polyamines as substrates, suggests a mechanism by which the oxidases can be exploited as antineoplastic drug targets. This minireview summarizes recent advances on the physiological roles of polyamine catabolism in animals and plants in an attempt to highlight differences and similarities that may contribute to determine in detail the underlined mechanisms involved. This information could be useful in evaluating the possibility of this metabolic pathway as a target for new antiproliferative therapies in animals and stress tolerance strategies in plants.

Keywords

Polyamines Polyamine oxidase Amine oxidase Tumor cells Reactive oxygen species Plants 

Abbreviations

ABA

Abscisic acid

ADC

Arginine decarboxylase

ALDH

Aldehyde dehydrogenase

AMADH

Aminoaldehyde dehydrogenase

APAO

N 1 -acetylpolyamine oxidase

ATAO

Arabidopsis thaliana CuAO

AtPAO

Arabidopsis thaliana PAO

BENSpm

Bis(ethyl)norspermine

BSAO

Bovine serum amine oxidase

CHO

Chinese hamster ovary

CPENSpm

N 1-ethyl-N 11-[(cyclopropyl)methyl]-4,8-diazaundecane

CuAO

Copper amine oxidase

Dap

1,3-diaminopropane

DFMO

Difluoromethylornithine

DX

Doxorubicin-resistant

eIF5A

Eukaryotic translation initiation factor 5A

FBS

Fetal bovine serum

GABA

γ-aminobutyric acid

HO·

Hydroxyl radical

HR

Hypersensitive response

JA

Jasmonic acid

MDR

Multidrug-resistant

NSAIDS

Non-steroidal anti-inflammatory drugs

ODC

Ornithine decarboxylase

PAO

Polyamine oxidase

PBS-BSA

Phosphate buffered saline-bovin serum albumin

PC-Acro

Protein conjugated acrolein

PCD

Programmed cell death

P-gp

P-glycoprotein

Put

Putrescine

ROS

Reactive oxygen species

SA

Salicylic acid

SAMDC

S-adenosylmethionine decarboxylase

SMO

Spermine oxidase

Spd

Spermidine

SPDS

Spd synthase

Spm

Spermine

SPMS

Spm synthase

SSAT

Spd/Spm N 1-acetyltransferase

Ther-Spm

Thermospermine

TMV

Tobacco mosaic virus

TNFα

Tumor-necrosis factor α

TPQ

2,4,5-trihydroxyphenylalaninequinone

ZmPAO

Maize PAO

Notes

Acknowledgments

This work was partially supported by the Italian MIUR (Ministero dell’Istruzione, dell’Università e della Ricerca), by Istituto Superiore di Sanità “Project Italy-USA”, by Istituto Pasteur-Fondazione Cenci Bolognetti and by funds MIUR-PRIN (Cofin). Thanks are due to Fondazione ‘Enrico ed Enrica Sovena’ for the scholarships given to Nikenza Viceconte and Stefania Saccoccio for supporting their Ph.D.

References

  1. Agostinelli E, Arancia G, Dalla Vedova L, Belli F, Marra M, Salvi M, Toninello A (2004) The biological function of polyamine oxidation products by amine oxidases: perspectives of clinical applications. Amino Acids 2:347–358CrossRefGoogle Scholar
  2. Agostinelli E, Belli F, Molinari A, Condello M, Palmigiani P, Dalla Vedova L, Marra M, Seiler N, Arancia G (2006a) Toxicity of enzymatic oxidation products of spermine to human melanoma cells (M14): sensitisation by heat and MDL 72527. Biochim Biophys Acta 1763:1040–1050PubMedCrossRefGoogle Scholar
  3. Agostinelli E, Dalla Vedova L, Belli F, Condello M, Arancia G, Seiler N (2006b) Sensitization of human colon adenocarcinoma cells (LoVo) to reactive oxygen species by a lysosomotropic compound. Int J Oncol 29:947–955PubMedGoogle Scholar
  4. Agostinelli E, Belli F, Dalla Vedova L, Marra M, Crateri P, Arancia G (2006c) Hyperthermia enhances cytotoxicity of amine oxidase and spermine on drug-resistant LoVo colon adenocarcinoma cells. Int J Oncol 28:1543–1553PubMedGoogle Scholar
  5. Agostinelli E, Condello M, Molinari A, Tempera G, Viceconte N, Arancia G (2009) Cytotoxicity of spermine oxidation products to multidrug resistant melanoma M14 ADR2 cells: sensitization by MDL 72527 lysosomotropic compound. Int J Oncol 35:485–498PubMedCrossRefGoogle Scholar
  6. Agostinelli E, Seiler N (2006) Non-irradiation-derived reactive oxygen species (ROS) and cancer: therapeutic implications. Amino Acids 31:341–355PubMedCrossRefGoogle Scholar
  7. Agostinelli E, Tempera G, Dalla Vedova L, Condello M, Arancia G (2007) MDL 72527 and spermine oxidation products induce a lysosomotropic effect and mitochondrial alterations in tumor effect. Biochem Soc Trans 35:343–348PubMedCrossRefGoogle Scholar
  8. Agostinelli E, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Grancara S, Toninello A, Stevanato R (2010) Potential anticancer application of polyamine oxidation products formed by amine oxidase: a new therapeutic approach. Amino Acids 38:353–368PubMedCrossRefGoogle Scholar
  9. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249PubMedCrossRefGoogle Scholar
  10. Amendola R, Bellini A, Cervelli M, Degan P, Marcocci L, Martini F, Mariottini P (2005) Direct oxidative DNA damage, apoptosis and radio sensitivity by spermine oxidase activities in mouse neuroblastoma cells. Biochim Biophys Acta Rev Cancer 1775:15–24Google Scholar
  11. Amendola R, Cervelli M, Fratini E, Polticelli F, Sallustio DE, Mariottini P (2009) Spermine metabolism and anticancer therapy. Curr Cancer Drug Targets 9:118–130PubMedCrossRefGoogle Scholar
  12. An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825PubMedCrossRefGoogle Scholar
  13. Angelini R, Tisi A, Rea G, Chen MM, Botta M, Federico R, Cona A (2008) Involvement of polyamine oxidase in wound healing. Plant Physiol 146:162–177PubMedCrossRefGoogle Scholar
  14. Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases “on the move”: an update. Plant Physiol Biochem 48:560–564PubMedCrossRefGoogle Scholar
  15. Arancia G, Calcabrini A, Marra M, Crateri P, Artico M, Martone A, Martelli F, Agostinelli E (2004) Mitochondrial alterations induced by serum amine oxidase and spermine on human multidrug resistant tumor cells. Amino Acids 26:273–282PubMedCrossRefGoogle Scholar
  16. Averill-Bates DA, Cherif A, Agostinelli E, Tanel A, Fortier G (2005) Anti-tumoral effect of native and immobilized bovine serum amine oxidase in a mouse melanoma model. Biochem Pharmacol 69:1693–1704PubMedCrossRefGoogle Scholar
  17. Averill-Bates DA, Ke Q, Tanel A, Roy J, Fortier G, Agostinelli E (2008) Mechanism of cell death induced by spermine and amine oxidase in mouse melanoma cells. Int J Oncol 32:79–88PubMedGoogle Scholar
  18. Babbar N, Casero RA Jr (2006) Tumor necrosis factor-alpha increases reactive oxygen species by inducing spermine oxidase in human lung epithelial cells: a potential mechanism for inflammation-induced carcinogenesis. Cancer Res 66:11125–11130PubMedCrossRefGoogle Scholar
  19. Babbar N, Hacker A, Huang Y, Casero RA Jr (2006) Tumor necrosis factor α induces spermidine/spermine N1-acetyltransferase through nuclear factor κB in non-small cell lung cancer cells. J Biol Chem 281:24182–24192PubMedCrossRefGoogle Scholar
  20. Babbar N, Murray-Stewart T, Casero RA Jr (2007) Inflammation and polyamine catabolism: the good, the bad and the ugly. Biochem Soc Trans 35:300–304PubMedCrossRefGoogle Scholar
  21. Bachrach U, Ash I, Rahamanin E (1987) Effect of microinjected amine and diamine oxidases on the ultrastructure of eukaryotic cultured cells. Tissue Cell 19:39–50PubMedCrossRefGoogle Scholar
  22. Bachrach U (2004) Polyamines and cancer: minireview article. Amino Acids 26:307–309PubMedCrossRefGoogle Scholar
  23. Bachrach U, Wang YC, Tabib A (2001) Polyamines: new cues in cellular signal transduction. News Physiol Sci 16:106–109PubMedGoogle Scholar
  24. Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317PubMedCrossRefGoogle Scholar
  25. Bhatnagar P, Minocha R, Minocha S (2002) Genetic manipulation of the metabolism of polyamines in poplar cells: the regulation of putrescine catabolism. Plant Physiol 128:1455–1469PubMedCrossRefGoogle Scholar
  26. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125CrossRefGoogle Scholar
  27. Calcabrini A, Arancia G, Marra M, Crateri P, Befani O, Martone A, Agostinelli E (2002) Enzymatic oxidation products of spermine induce greater cytotoxic effects on human multidrug-resistant colon carcinoma cells (LoVo) than on their wild type counterparts. Int J Cancer 99:43–52PubMedCrossRefGoogle Scholar
  28. Campestre MP, Bordenave CD, Origone AC, Menéndez AB, Ruiz OA, Rodríguez AA, Maiale SJ (2011) Polyamine catabolism is involved in response to salt stress in soybean hypocotyls. J Plant Physiol (in press). doi: 10.1016/j.jplph.2011.01.007
  29. Casero RA, Pegg AE (2009) Polyamine catabolism and disease. Biochem J 421:323–338PubMedCrossRefGoogle Scholar
  30. Casero RA Jr, Woster PM (2009) Recent advances in the development of polyamine analogues as antitumor agents. J Med Chem 52:4551–4573PubMedCrossRefGoogle Scholar
  31. Casero RA Jr, Wang Y, Stewart TM, Devereux W, Hacker A, Wang Y, Smith R, Woster PM (2003) The role of polyamine catabolism in anti-tumor drug response. Biochem Soc Trans 31:361–365PubMedCrossRefGoogle Scholar
  32. Cervelli M, Polticelli F, Federico R, Mariottini P (2003) Heterologous expression and characterization of mouse spermine oxidase. J Biol Chem 278:5271–5276PubMedCrossRefGoogle Scholar
  33. Cervelli M, Bellini A, Bianchi M, Marcocci L, Nocera S, Polticelli F, Federico R, Amendola R, Mariottini P (2004) Mouse spermine oxidase gene splice variants: nuclear subcellular localization of a novel active isoform. Eur J Biochem 271:760–770PubMedCrossRefGoogle Scholar
  34. Cervelli M, Fratini E, Amendola R, Bianchi M, Signori E, Ferraro E, Lisi A, Federico R, Marcocci L, Mariottini P (2009) Increased spermine oxidase (SMO) activity as a novel differentiation marker of myogenic C2C12 cells. Int J Biochem Cell Biol 41:934–944PubMedCrossRefGoogle Scholar
  35. Cervelli M, Bellavia G, Fratini E, Amendola R, Polticelli F, Barba M, Federico R, Signore F, Gucciardo G, Grillo R, Woster PM, Casero RA Jr, Mariottini P (2010) Spermine oxidase (SMO) activity in breast tumor tissues and biochemical analysis of the anticancer spermine analogues BENSpm and CPENSpm. BMC Cancer 10:555. doi: 10.1186/1471-2407-10-555 PubMedCrossRefGoogle Scholar
  36. Childs AC, Mehta DJ, Gerner EW (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60:1394–1406PubMedCrossRefGoogle Scholar
  37. Cohen SS (1998) A guide to the polyamines. Oxford University Press, New YorkGoogle Scholar
  38. Cona A, Manetti F, Leone R, Corelli F, Tavladoraki P, Polticelli F, Botta M (2004) Molecular basis for the binding of competitive inhibitors of maize polyamine oxidase. Biochemistry 43:3426–3435PubMedCrossRefGoogle Scholar
  39. Cona A, Rea G, Botta M, Corelli F, Federico R, Angelini R (2006) Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. J Exp Bot 57:2277–2289PubMedCrossRefGoogle Scholar
  40. Dittami SM, Gravot A, Renault D, Goulitquer S, Eggert A, Bouchereau A, Boyen C, Tonon T (2011) Integrative analysis of metabolite and transcript abundance during the short-term response to saline and oxidative stress in the brown alga Ectocarpus siliculosus. Plant Cell Environ (in press). doi: 10.1111/j.1365-3040.2010.02268.x
  41. Eisenberg T, Knauer H, Schauer A, Büttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, Fussi H, Deszcz L, Hartl R, Schraml E, Criollo A, Megalou E, Weiskopf D, Laun P, Heeren G, Breitenbach M, Grubeck-Loebenstein B, Herker E, Fahrenkrog B, Fröhlich KU, Sinner F, Tavernarakis N, Minois N, Kroemer G, Madeo F (2009) Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 11:1305–1314PubMedCrossRefGoogle Scholar
  42. Fellenberg C, Böttcher C, Vogt T (2009) Phenylpropanoid polyamine conjugate biosynthesis in Arabidopsis thaliana flower buds. Phytochemistry 70:1392–1400PubMedCrossRefGoogle Scholar
  43. Fincato P, Moschou PN, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis-Angelakis KA, Tavladoraki P (2011) Functional diversity inside the Arabidopsis polyamine oxidase gene family. J Exp Bot 62:1155–1168PubMedCrossRefGoogle Scholar
  44. Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48:513–520PubMedCrossRefGoogle Scholar
  45. Gerner EW, Meyskens FL Jr, Goldschmid S, Lance P, Pelot D (2007) Rationale for, and design of, a clinical trial targeting polyamine metabolism for colon cancer chemoprevention. Amino Acids 33:189–195PubMedCrossRefGoogle Scholar
  46. Goodwin AC, Jadallah S, Toubaji A, Lecksell K, Hicks JL, Kowalski J, Bova GS, De Marzo AM, Netto GJ, Casero RA Jr (2008) Increased spermine oxidase expression in human prostate cancer and prostatic intraepithelial neoplasia tissues. Prostate 68:766–772PubMedCrossRefGoogle Scholar
  47. Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45PubMedCrossRefGoogle Scholar
  48. Häkkinen MR, Hyvönen MT, Auriola S, Casero RA Jr, Vepsäläinen J, Khomutov AR, Alhonen L, Keinänen TA (2010) Metabolism of N-alkylated spermine analogues by polyamine and spermine oxidases. Amino Acids 38:369–381PubMedCrossRefGoogle Scholar
  49. Hahm HA, Ettinger DS, Bowling K, Hoker B, Chen TL, Zabelina Y, Casero RA Jr (2002) Phase I study of N 1 , N 11-diethylnorspermine in patients with non-small cell lung cancer. Clin Cancer Res 8:684–690PubMedGoogle Scholar
  50. Heby O, Persson L (1990) Molecular genetics of polyamine synthesis in eukaryotic cells. Trends Biochem Sci 15:153–158PubMedCrossRefGoogle Scholar
  51. Heim WG, Sykes KA, Hildreth SB, Sun J, Lu R-H, Jelesko JG (2006) Cloning and characterization of a Nicotiana tabacum methylputrescine oxidase transcript. Phytochemistry 68:454–463PubMedCrossRefGoogle Scholar
  52. Hewezi T, Howe PJ, Maier TR, Hessey RS, Mitchum MG, Davis EL, Baum TJ (2010) Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol 152:968–984PubMedCrossRefGoogle Scholar
  53. Igarashi K, Kashiwagi K (2010) Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42:39–51PubMedCrossRefGoogle Scholar
  54. Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004a) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573PubMedCrossRefGoogle Scholar
  55. Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T (2004b) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152PubMedCrossRefGoogle Scholar
  56. Jänne J, Alhonen L, Keinänen TA, Pietilä M, Uimari A, Pirinen E, Hyvönen MT, Järvinen A (2005) Animal disease models generated by genetic engineering of polyamine metabolism. J Cell Mol Med 9:865–882PubMedCrossRefGoogle Scholar
  57. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282PubMedCrossRefGoogle Scholar
  58. Katoh A, Shoji T, Hashimoto T (2007) Molecular cloning of N-methylputrescine oxidase from tobacco. Plant Cell Physiol 48:550–554PubMedCrossRefGoogle Scholar
  59. Kaur H, Heinzel N, Schöttner M, Baldwin IT, Gális I (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 152:1731–1747PubMedCrossRefGoogle Scholar
  60. Kee K, Foster BA, Merali S, Kramer DL, Hensen ML, Diegelman P, Kisiel N, Vujcic S, Mazurchuk RV, Porter CW (2004) Activated polyamine catabolism depletes acetyl-CoA pools and suppresses prostate tumor growth in TRAMP mice. J Biol Chem 279:40076–40083PubMedCrossRefGoogle Scholar
  61. Keskinege A, Elgun S, Yilmaz E (2001) Possible implications of arginase and diamine oxidase in prostatic carcinoma. Cancer Detect Prev 25:76–79PubMedGoogle Scholar
  62. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381PubMedCrossRefGoogle Scholar
  63. Lord-Fontaine S, Agostinelli E, Przybytkowski E, Averill-Bates DA (2001) Amine oxidase, spermine, and hyperthermia induce cytotoxicity in P-glycoprotein overexpressing multidrug resistant Chinese Hamster ovary cells. Biochem Cell Biol 79:165–175PubMedCrossRefGoogle Scholar
  64. Maiale SJ, Marina M, Sánchez DH, Pieckenstain FL, Ruiz OA (2008) In vitro and in vivo inhibition of plant polyamine oxidase activity by polyamine analogues. Phytochemistry 69:2552–2558PubMedCrossRefGoogle Scholar
  65. Marina M, Maiale SJ, Rossi FR, Romero MF, Rivas EI, Gárriz A, Ruiz OA, Pieckenstain FL (2008) Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava. Plant Physiol 147:2164–2178PubMedCrossRefGoogle Scholar
  66. Masini E, Pierpaoli S, Marzocca C, Mannaioni PF, Pietrangeli P, Mateescu MA, Zelli M, Federico R, Mondovì B (2003) Protective effects of a plant histaminase in myocardial ischaemia and reperfusion injury in vivo. Biochem Biophys Res Commun 309:432–439PubMedCrossRefGoogle Scholar
  67. Mateescu MA, Dumoulin M-J, Wang XT, Nadeau R, Mondovi B (1997) A new physiological role of copper amine oxidases: cardioprotection against reactive oxygen intermediates. J Physiol Pharmacol 48:110–121Google Scholar
  68. Mattoo AK, Minocha SC, Minocha R, Handa AK (2010) Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38:405–413PubMedCrossRefGoogle Scholar
  69. Minguet EG, Vera-Sirera F, Marina A, Carbonell J, Blázquez MA (2008) Evolutionary diversification in polyamine biosynthesis. Mol Biol Evol 25:2119–2128PubMedCrossRefGoogle Scholar
  70. Minocha R, Long S, Thangavel P, Minocha SC, Eagar C, Driscoll CT (2010) Elevation dependent sensitivity of northern hardwoods to Ca-addition at Hubbard Brook Experimental Forest, NH, USA. For Ecol Manag 260:2115–2124CrossRefGoogle Scholar
  71. Mitchell Guss J, Zanotti G, Salminen TA (2009) Copper amine oxidases crystal structures. In: Floris G, Mondovı` B (eds) Copper amine oxidases. CRC press, Boca Raton, pp 119–142Google Scholar
  72. Mitsuya Y, Takahashi Y, Uehara Y, Berberich T, Miyazaki A, Takahashi H, Kusano T (2007) Identification of a novel Cys2/His2-type zinc finger protein as a component of a spermine-signaling pathway in tobacco. J Plant Physiol 164:785–793PubMedCrossRefGoogle Scholar
  73. Mohapatra S, Minocha R, Long S, Minocha SC (2010) Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids. Amino Acids 38:1117–1129PubMedCrossRefGoogle Scholar
  74. Møller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis atao1 gene encoding an H2O2-generating diamine oxidase. Plant J 13:781–791PubMedCrossRefGoogle Scholar
  75. Møller SG, Urwin PE, Atkinson HJ, McPherson MJ (1998) Nematode-induced expression of atao1, a gene encoding an extracellular diamine oxidase associated with developing vascular tissue. Physiol Mol Plant Pathol 53:73–79CrossRefGoogle Scholar
  76. Mondovì B, Pietrangeli P, Morpurgo L, Masini E, Federico R, Mateescu MA, Befani O, Agostinelli E (2003) Some new functions of amine oxidases. Inflammopharmacology 11:155–163PubMedCrossRefGoogle Scholar
  77. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008a) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147:1845–1857PubMedCrossRefGoogle Scholar
  78. Moschou PN, Delis ID, Paschalidis KA, Roubelakis-Angelakis KA (2008b) Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiol Plant 133:140–156PubMedCrossRefGoogle Scholar
  79. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008c) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724PubMedCrossRefGoogle Scholar
  80. Moschou PN, Sarris PF, Skandalis N, Andriopoulou AH, Paschalidis KA, Panopoulos NJ, Roubelakis-Angelakis KA (2009) Engineered polyamine catabolism preinduces tolerance of tobacco to bacteria and oomycetes. Plant Physiol 149:1970–1981PubMedCrossRefGoogle Scholar
  81. Mu D, Janes SM, Smith AJ, Brown DE, Dooley DM, Klinman JP (1992) Tyrosine codon corresponds to topaquinone at the active site of copper amine oxidases. J Biol Chem 267:7979–7982PubMedGoogle Scholar
  82. Murray-Stewart T, Wang Y, Goodwin A, Hacker A, Meeker A, Casero RA Jr (2008) Nuclear localization of human spermine oxidase isoforms—possible implications in drug response and disease etiology. FEBS J 275:2795–2806PubMedCrossRefGoogle Scholar
  83. Nocera S, Marcocci L, Pietrangeli P, Mondovì B (2003) New perspectives on the role of amine oxidases in physiopathology. Amino Acids 24:13–17PubMedGoogle Scholar
  84. Park JH, Aravind L, Wolff EC, Kaevel J, Kim YS, Park MH (2006) Molecular cloning, expression, and structural prediction of deoxyhypusine hydroxylase: a HEAT-repeat-containing metalloenzyme. Proc Natl Acad Sci USA 103:51–56PubMedCrossRefGoogle Scholar
  85. Pegg AE (1986) Recent advances in the biochemistry of polyamines in eukaryotes. Biochem J 234:249–262PubMedGoogle Scholar
  86. Pegg AE (1988) Polyamine metabolism and its importance in neoplastic growth and a target for chemotherapy. Cancer Res 48:759–774PubMedGoogle Scholar
  87. Pegg AE (2009) Mammalian polyamine metabolism and function. IUBMB Life 61:880–894PubMedCrossRefGoogle Scholar
  88. Pegg AE, Feith DJ (2007) Polyamines and neoplastic growth. Biochem Soc Trans 35:295–299PubMedCrossRefGoogle Scholar
  89. Pegg AE, Michael AJ (2010) Spermine synthase. Cell Mol Life Sci 67:113–121PubMedCrossRefGoogle Scholar
  90. Petřivalský M, Brauner F, Luhová L, Gagneul D, Šebela M (2007) Aminoaldehyde dehydrogenase activity during wound healing of mechanically injured pea seedlings. J Plant Physiol 164:1410–1418PubMedCrossRefGoogle Scholar
  91. Pledgie A, Huang Y, Hacker A, Zhang Z, Woster PM, Davidson NE, Casero RA Jr (2005) Spermine oxidase SMO (PAOh1), not N1-acetylpolyamine oxidase PAO, is the primary source of cytotoxic H2O2 in polyamine analog-treated human breast cancer cell lines. J Biol Chem 280:39843–39851PubMedCrossRefGoogle Scholar
  92. Pledgie-Tracy A, Billam M, Hacker A, Sobolewski MD, Woster PM, Zhang Z, Casero RA, Davidson NE (2010) The role of the polyamine catabolic enzymes SSAT and SMO in the synergistic effects of standard chemotherapeutic agents with a polyamine analogue in human breast cancer cell lines. Cancer Chemother Pharmacol 65:1067–1081PubMedCrossRefGoogle Scholar
  93. Quinet M, Ndayiragije A, Lefèvre I, Lambillotte B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733PubMedCrossRefGoogle Scholar
  94. Rodríguez AA, Maiale SJ, Menéndez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J Exp Bot 60:4249–4262PubMedCrossRefGoogle Scholar
  95. Saiki R, Park H, Ishii I, Yoshida M, Nishimura K, Toida T, Tatsukawa H, Kojima S, Ikeguchi Y, Pegg AE, Kashiwagi K, Igarashi K (2011) Brain infarction correlates more closely with acrolein that with reactive oxygen species. Biochem Biophys Res Commun 404:1044–1049PubMedCrossRefGoogle Scholar
  96. Seiler N (2000) Oxidation of polyamines and brain injury. Neurochem Res 25:471–490PubMedCrossRefGoogle Scholar
  97. Seiler N (2004) Catabolism of polyamines. Amino Acids 26:217–233PubMedGoogle Scholar
  98. Serafini-Fracassini D, Della Mea M, Tasco G, Casadio R, Del Duca S (2009) Plant and animal transglutaminases: do similar functions imply similar structures? Amino Acids 36:643–657PubMedCrossRefGoogle Scholar
  99. Sharmin S, Sakata K, Kashiwagi K, Ueda S, Iwasaki S, Shirahata A, Igarashi K (2001) Polyamine cytotoxicity in the presence of bovine serum amine oxidase. Biochem Biophys Res Commun 282:228–235PubMedCrossRefGoogle Scholar
  100. Srivastava A, Chung SH, Fatima T, Datsenka T, Handa AK, Mattoo AK (2007) Polyamines as anabolic growth regulators revealed by transcriptome analysis and metabolite profiles of tomato fruits engineered to accumulate spermidine and spermine. Plant Biotechnol 24:57–70CrossRefGoogle Scholar
  101. Takahashi Y, Cong R, Sagor GH, Niitsu M, Berberich T, Kusano T (2010) Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep 29:955–965PubMedCrossRefGoogle Scholar
  102. Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Federico R (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141:1519–1532PubMedCrossRefGoogle Scholar
  103. Taylor CA, Sun Z, Cliche DO, Ming H, Eshaque B, Jin S, Hopkins MT, Thai B, Thompson JE (2007) Eukaryotic translation initiation factor 5A induces apoptosis in colon cancer cells and associates with the nucleus in response to tumor necrosis factor alpha signaling. Exp Cell Res 313:437–449PubMedCrossRefGoogle Scholar
  104. Toninello A, Pietrangeli P, De Marchi U, Salvi M, Mondovì B (2006) Amine oxidases in apoptosis and cancer. Biochim Biophys Acta 1765:1–13PubMedGoogle Scholar
  105. Toumi I, Moschou PN, Paschalidis KA, Daldoul S, Bouamama B, Chenennaoui S, Ghorbel A, Mliki A, Roubelakis-Angelakis KA (2010) Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine. J Plant Physiol 167:519–525PubMedCrossRefGoogle Scholar
  106. Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Letters 579:1557–1564PubMedCrossRefGoogle Scholar
  107. Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blázquez MA, Carbonell J (2010) Role of polyamines in plant vascular development. Plant Physiol Biochem 48:534–539PubMedCrossRefGoogle Scholar
  108. Vujcic S, Diegelman P, Bacchi CJ, Kramer DL, Porter CW (2002) Identification and characterization of a novel flavin-containing spermine oxidase of mammalian cell origin. Biochem J 367:665–675PubMedCrossRefGoogle Scholar
  109. Wallace HM, Duthie J, Evans DM, Lamond S, Nicoll KM, Heys SD (2000) Alterations in polyamine catabolic enzymes in human breast cancer tissue. Clin Cancer Res 6:3657–3661PubMedGoogle Scholar
  110. Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14PubMedCrossRefGoogle Scholar
  111. Wallace HM, Niiranen K (2007) Polyamine analogues: an update. Amino Acids 33:261–265PubMedCrossRefGoogle Scholar
  112. Walters DR (2003) Polyamines and plant disease. Phytochemistry 64:97–107PubMedCrossRefGoogle Scholar
  113. Wang Y, Devereux W, Woster PM, Stewart TM, Hacker A, Casero RA Jr (2001) Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 61:5370–5373PubMedGoogle Scholar
  114. Wang TW, Lu L, Zhang CG, Taylor CA, Thompson JE (2003) Pleiotropic effects of suppressing deoxyhypusine synthase expression in Arabidopsis thaliana. Plant Mol Biol 52:1223–1235PubMedCrossRefGoogle Scholar
  115. Wang Y, Hacker A, Murray-Stewart T, Frydman B, Valasinas A, Fraser AV, Woster PM, Casero RA Jr (2005) Properties of recombinant human N1-acetylpolyamine oxidase (hPAO): potential role in determining drug sensitivity. Cancer Chemother Pharmacol 56:83–90PubMedCrossRefGoogle Scholar
  116. Wang Y, Casero RA Jr (2006) Mammalian polyamine catabolism: a therapeutic target, a pathological problem, or both? Biochem J 139:17–25CrossRefGoogle Scholar
  117. Wargo PM, Minocha R, Wong BL, Long RP, Horsley SB, Hall TJ (2002) Measuring changes in stress and vitality indicators in limed sugar maple on the Allegheny Plateau in north-central Pennsylvania. Can J For Res 32:629–641CrossRefGoogle Scholar
  118. Wolff AC, Armstrong DK, Fetting JH, Carducci MK, Riley CD, Bender JF, Casero RA Jr, Davidson NE (2003) A Phase II study of the polyamine analog N 1 , N 11-diethylnorspermine (DENSpm) daily for five days every 21 days in patients with previously treated metastatic breast cancer. Clin Cancer Res 9:5922–5928PubMedGoogle Scholar
  119. Wu J, Qu H, Shang Z, Jiang X, Moschou PN, Roubelakis-Angelakis KA, Zhang S (2010) Spermidine oxidase derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca2+-permeable channels and pollen tube growth. Plant J 63:1042–1053PubMedCrossRefGoogle Scholar
  120. Wu L, Mateescu MA, Wang XT, Mondovi B, Wang R (1996) Modulation of K+ channel currents by serum amineoxidase in neurons. Biochem Biophys Res Commun 220:47–52PubMedCrossRefGoogle Scholar
  121. Xing SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45:560–566PubMedCrossRefGoogle Scholar
  122. Xue B, Zhang A, Jiang M (2009) Involvement of polyamine oxidase in abscisic acid-induced cytosolic antioxidant defense in leaves of maize. J Integr Plant Biol 51:225–234PubMedCrossRefGoogle Scholar
  123. Yamakawa H, Kamada H, Satoh M, Ohashi Y (1998) Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against Tobacco mosaic virus infection. Plant Physiol 118:1213–1222PubMedCrossRefGoogle Scholar
  124. Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol 132:1973–1981PubMedCrossRefGoogle Scholar
  125. Yoda H, Hiroi Y, Sano H (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142:193–206PubMedCrossRefGoogle Scholar
  126. Yoda H, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H (2009) Polyamines as a common source of hydrogen peroxide in host- and non-host hypersensitive response during pathogen infection. Plant Mol Biol 70:103–112PubMedCrossRefGoogle Scholar
  127. Yu GH, Sun MX (2007) Deciphering the possible mechanism of GABA in tobacco pollen tube growth and guidance. Plant Signal Behav 2:393–395PubMedCrossRefGoogle Scholar
  128. Zahedi K, Bissler JJ, Wang Z, Josyula A, Lu L, Diegelman P, Kisiel N, Porter CW, Soleimani M (2007) Spermidine/spermine N 1-acetyltransferase overexpression in kidney epithelial cells disrupts polyamine homeostasis, leads to DNA damage, and causes G2 arrest. Am J Physiol Cell Physiol 292:1204–1215CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Paraskevi Tavladoraki
    • 1
  • Alessandra Cona
    • 1
  • Rodolfo Federico
    • 1
  • Giampiero Tempera
    • 2
  • Nikenza Viceconte
    • 2
  • Stefania Saccoccio
    • 2
  • Valentina Battaglia
    • 3
  • Antonio Toninello
    • 3
  • Enzo Agostinelli
    • 2
  1. 1.Department of BiologyUniversity ‘Roma Tre’RomeItaly
  2. 2.Department of Biochemical Sciences, Istituto Pasteur-Fondazione Cenci BolognettiSAPIENZA University of Rome and CNR, Institute Biology and Molecular PathologyRomeItaly
  3. 3.Department of Biological ChemistryUniversity of PaduaPaduaItaly

Personalised recommendations