Involvement of polyamines in apoptosis. Facts and controversies: Effectors or protectors?

Seminars in Cancer Biology

Volumn 10, Issue 1, 2000, Pages 55-68

  Schipper, Raymond G ^a   Penning, Louis C ^b   Verhofstad, Albert A J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Apoptosis; Neuronal cell death; Ornithine decarboxylase; Polyamine oxidation; Polyamines; Programmed cell death; Transglutaminase

Indexed keywords

ORNITHINE DECARBOXYLASE; POLYAMINE DERIVATIVE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

APOPTOSIS; CELL DEATH; CELL SURVIVAL; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVITY; HUMAN; NERVE CELL; NONHUMAN; OXIDATION; POLYAMINE METABOLISM; REVIEW;

EID: 0034045972     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1006/scbi.2000.0308     Document Type: Article

References (105)

1. Medina M A, Quesada A R, de-Castro I N, Sanchez J F. Histamine, polyamines, and cancer. Biochem Pharmacol. 57:1999;1341-1344.
2. Seiler N, Delcros J G, Moulinoux J P. Polyamine transport in mammalian cells. An update. Int J Biochem Cell Biol. 28:1996;843-861.
3. Persson L, Svensson F, Lovkist-Wallstrom E. Regulation of polyamine metabolism. Nishioka K. Polyamines in Cancer: Basic Mechanisms and Clinical Approaches. 1996;19-43 Landis, Austin.
4. Seiler N, Douaud F. Polyamine metabolism and transport in the mammalian organism. Bardocz S, White A, Hajos G. COST 917: Biogenically Active Amines in Food. 1998;19-38 European Commission, Luxembourg.
5. Marton L J, Pegg A E. Polyamines as targets for therapeutic intervention. Annu Rev Pharmacol Toxicol. 35:1995;55-91.
6. Fadeel B, Zhivotovsky B, Orrenius S. All along the watchtower: on the regulation of apoptosis regulators. FASEB J. 13:1999;1647-1657.
7. Bernstein H G, Muller M. The cellular localization of the l-ornithine decarboxylase/polyamine system in normal and diseased central nervous systems. Prog Neurobiol. 57:1999;485-505.
8. Packham G, Cleveland J L. Ornithine decarboxylase is a mediator of c-Myc-induced apoptosis. Mol Cell Biol. 14:1994;5741-5747.
9. Packham G, Porter C W, Cleveland J L. c-Myc induces apoptosis and cell cycle progression by separable, yet overlapping, pathways. Oncogene. 13:1996;461-469.
10. King K L, Cidlowski J A. Cell cycle regulation and apoptosis. Annu Rev Physiol. 60:1998;601-617.
11. Monti M G, Ghiaroni S, Pernecco L, Barbieri D, Marverti G, Franceschi C. Polyamine depletion protects HL-60 cells from 2-deoxy-d-ribose-induced apoptosis. Life Sci. 62:1998;799-806.
12. Monti M G, Ghiaroni S, Barbieri D, Franceschi C, Marverti G, Moruzzi M S. 2-deoxy-d-ribose-induced apoptosis in HL-60 cells is associated with the cell cycle progression by spermidine. Biochem Biophys Res Commun. 257:1999;460-465.
13. Kramer D L, Vujcic S, Diegelman P, White C, Black J D, Porter C W. Polyamine analogue-mediated cell cycle responses in human melanoma cells involves the p53, p21, Rb regulatory pathway. Biochem Soc Trans. 26:1998;609-614.
14. Tewari M, Hamid Q A, Tuncay O C, Tewari D S. Antizyme prevents ornithine decarboxylase-mediated cell death in human fibroblasts. Oral Oncol. 34:1998;538-542.
15. Lin C K, Zou H Y, Kaptein J S, Yen C F, Kalunta C I, Nguyen T T, Park E, Lad P M. Anti-IgM-induced growth inhibition and apoptosis are independent of ornithine decarboxylase in Ramos cells. Exp Cell Res. 237:1997;231-241.
16. Noda T, Iwakiri R, Fujimoto K, Matsuo S, Aw T Y. Programmed cell death induced by ischemia-reperfusion in rat intestinal mucosa. Am J Physiol. 274:1998;G270-G276.
17. Penning L C, Schipper R G, Vercammen D, Verhofstad A AJ, Denecker T, Beyaert R, Vandenabeele P. Sensitization of tnf-induced apoptosis with polyamine synthesis inhibitors in different human and murine tumour cell lines. Cytokine. 10:1998;423-431.
18. Gahl W A, Pitot H C. Putrescine-oxidase activity in adult bovine serum and fetal bovine serum. In Vitro. 15:1979;252-257.
19. Allen J C, Smith C J, Hussain J I, Thomas J M, Gaugas J M. Inhibition of lymphocyte proliferation by polyamines requires ruminant-plasma polyamine oxidase. Eur J Biochem. 102:1979;153-158.
20. Tabor C W, Tabor H. Polyamines. Annu Rev Biochem. 53:1984;749-790.
21. Seiler N. Functions of polyamine acetylation. Can J Physiol Pharmacol. 65:1987;2024-2035.
22. Van-den-Munckhof R J, Denyn M, Tigchelaar G W, Schipper R G, Verhofstad A AJ, Van-Noorden C J, Frederiks W M. In situ substrate specificity and ultrastructural localization of polyamine oxidase activity in unfixed rat tissues. J Histochem Cytochem. 43:1995;1155-1162.
23. Smith C J, Maschler R, Maurer H R, Allen J C. Inhibition of cells in culture by polyamines does not depend on the presence of ruminant serum. Cell Tissue Kinet. 16:1983;269-276.
24. Brunton V G, Grant M H, Wallace H M. Spermine toxicity and glutathione depletion in BHK-21/C13 cells. Biochem Pharmacol. 40:1990;1893-1900.
25. Brunton V G, Grant M H, Wallace H M. Mechanisms of spermine toxicity in baby-hamster kidney (BHK) cells. The role of amine oxidases and oxidative stress. Biochem J. 280:1991;193-198.
26. Mitchell J L, Diveley R RJ, Bareyal L A. Abnormal accumulation and toxicity of polyamines in a difluoromethylornithine-resistant HTC cell variant. Biochim Biophys Acta. 1136:1992;136-142.
27. Smith R C, Litwin M S, Lu Y, Zetter B R. Identification of an endogenous inhibitor of prostatic carcinoma cell growth. Nat Med. 1:1995;1040-1045.
28. Seiler N. Pharmacological properties of the natural polyamines and their depletion by biosynthesis inhibitors as a therapeutic approach. Prog Drug Res. 37:1991;107-159.
29. Kramer D L. Polyamine inhibitors and analogs. Nishioka K. Polyamines in Cancer: Basic Mechanisms and Clinical Approaches. 1996;151-189 Landis, Austin.
30. McCloskey D E, Yang J, Woster P M, Davidson N E, Casero R AJ. Polyamine analogue induction of programmed cell death in human lung tumor cells. Clin Cancer Res. 2:1996;441-446.
31. Ha H C, Woster P M, Casero R AJ. Unsymmetrically substituted polyamine analogue induces caspase-independent programmed cell death in Bcl-2-overexpressing cells. Cancer Res. 58:1998;2711-2714.
32. Eiseman J L, Rogers F A, Guo Y, Kauffman J, Sentz D L, Klinger M F, Callery P S, Kyprianou N. Tumor-targeted apoptosis by a novel spermine analogue, 1,12-diaziridinyl-4,9-diazadodecane, results in therapeutic efficacy and enhanced radiosensitivity of human prostate cancer. Cancer Res. 58:1998;4864-4870.
33. Zagaja G P, Shrivastav M, Fleig M J, Marton L J, Rinker S C, Dolan M E. Effects of polyamine analogues on prostatic adenocarcinoma cells in vitro and in vivo. Cancer Chemother Pharmacol. 41:1998;505-512.
34. Mi Z, Kramer D L, Miller J T, Bergeron R J, Bernacki R, Porter C W. Human prostatic carcinoma cell lines display altered regulation of polyamine transport in response to polyamine analogs and inhibitors. Prostate. 34:1998;51-60.
35. Schipper R G, Otten A E, Lange W P, De-Graaf M, Heerschap A, Romijn J, Schalken J A, Verhofstad A AJ. Polyamines and prostatic cancer. Bardocz S, White A, Hajos G. COST 917: Biogenically Active Amines in Food. 1998;71-78 European Commission, Luxembourg.
36. Poulin R, Pelletier G, Pegg A E. Induction of apoptosis by excessive polyamine accumulation in ornithine decarboxylase-overproducing L1210 cells. Biochem J. 311:1995;723-727.
37. Tobias K E, Kahana C. Exposure to ornithine results in excessive accumulation of putrescine and apoptotic cell death in ornithine decarboxylase overproducing mouse myeloma cells. Cell Growth Differ. 6:1995;1279-1285.
38. Tome M E, Fiser S M, Gerner E W. Consequences of aberrant ornithine decarboxylase regulation in rat hepatoma cells. J Cell Physiol. 158:1994;237-244.
39. Tome M E, Fiser S M, Payne C M, Gerner E W. Excess putrescine accumulation inhibits the formation of modified eukaryotic initiation factor 5A (eIF-5A) and induces apoptosis. Biochem J. 328:1997;847-854.
40. Xie X, Tome M E, Gerner E W. Loss of intracellular putrescine pool-size regulation induces apoptosis. Exp Cell Res. 230:1997;386-392.
41. Hu R H, Pegg A E. Rapid induction of apoptosis by deregulated uptake of polyamine analogues. Biochem J. 328:1997;307-316.
42. Tome M E, Gerner E W. Cellular eukaryotic initiation factor 5A content as a mediator of polyamine effects on growth and apoptosis. Biol Signals. 6:1997;150-156.
43. Stefanelli C, Bonavita F, Stanic ′ I, Mignani M, Facchini A, Pignatti C, Flamigni F, Caldarera C M. Spermine causes caspase activation in leukaemia cells. FEBS Lett. 437:1998;233-236.
44. Stefanelli C, Bonavita F, Stanic ′ I, Pignatti C, Flamigni F, Guarnieri C, Caldarera C M. Spermine triggers the activation of caspase-3 in a cell-free model of apoptosis. FEBS Lett. 451:1999;95-98.
45. Schipper R G, Otten A E, Verhofstad A AJ. Role of polyamine metabolism in programmed cell death. Bardocz S, White A. Polyamines in Health and Nutrition. 1999;77-84 Kluwer Academic Publishers, Dordrecht.
46. Hayashi S, Murakami Y. Rapid and regulated degradation of ornithine decarboxylase. Biochem J. 306:1995;1-10.
47. Grassilli E, Benatti F, Dansi P, Giammarioli A M, Malorni W, Franceschi C, Desiderio M A. Inhibition of proteasome function prevents thymocyte apoptosis: involvement of ornithine decarboxylase. Biochem Biophys Res Commun. 250:1998;293-297.
48. Iwata S, Sato Y, Asada M, Takagi M, Tsujimoto A, Inaba T, Yamada T, Sakamoto S, Yata J, Shimogori T, Igarashi K, Mizutani S. Anti-tumor activity of antizyme which targets the ornithine decarboxylase (ODC) required for cell growth and transformation. Oncogene. 18:1999;165-172.
49. Mitchell J L, Judd G G. Antizyme modifications affecting polyamine homoeostasis. Biochem Soc Trans. 26:1998;591-595.
50. Wilson M R. Apoptosis: unmasking the executioner. Cell Death Differ. 5:1998;646-652.
51. Susin S A, Zamzami N, Kroemer G. Mitochondria as regulators of apoptosis: doubt no more. Biochim Biophys Acta. 1366:1998;151-165.
52. 1-acetyltransferase. Casero R AJ. Polyamines: Regulation and Molecular Interaction. 1995;77-99 Landis, Austin.
53. Kramer D L, Fogel P M, Diegelman P, Cooley J M, Bernacki R J, McManis J S, Bergeron R J, Porter C W. Effects of novel spermine analogues on cell cycle progression and apoptosis in MALME-3M human melanoma cells. Cancer Res. 57:1997;5521-5527.
54. Desiderio M A, Grassilli E, Bellesia E, Salomoni P, Franceschi C. Involvement of ornithine decarboxylase and polyamines in glucocorticoid-induced apoptosis of rat thymocytes. Cell Growth Differ. 6:1995;505-513.
55. Ha H C, Woster P M, Yager J D, Casero R AJ. The role of polyamine catabolism in polyamine analogue-induced programmed cell death. Proc Natl Acad Sci. 94:1997;11557-11562.
56. Parchment R E, Pierce G B. Polyamine oxidation, programmed cell death, and regulation of melanoma in the murine embryonic limb. Cancer Res. 49:1989;6680-6686.
57. Parchment R E. An overview of the known and suspected mechanisms for control of apoptosis by polyamines and their metabolites. Nishioka K. Polyamines in Cancer: Basic Mechanisms and Clinical Approaches. 1996;99-150 Landis, Austin.
58. Clutton S. The importance of oxidative stress in apoptosis. Br Med Bull. 53:1997;662-668.
59. Lindsay G S, Wallace H M. Changes in polyamine catabolism in HL-60 human promyelogenous leukaemic cells in response to etoposide-induced apoptosis. Biochem J. 337:1999;83-87.
60. Fesus L, Madi A, Balajthy Z, Nemes Z, Szondy Z. Transglutaminase induction by various cell death and apoptosis pathways. Experientia. 52:1996;942-949.
61. Melino G, Piacentini M. 'Tissue' transglutaminase in cell death: a downstream or a multifunctional upstream effector? FEBS Lett. 430:1998;59-63.
62. Folk J E, Park M H, Chung S I, Schrode J, Lester E P, Cooper H L. Polyamines as physiological substrates for transglutaminases. J Biol Chem. 255:1980;3695-3700.
63. Piacentini M, Farrace M G, Imparato M, Piredda L, Autuori F. Polyamine-dependent post-translational modification of proteins in differentiating mouse epidermal cells. J Invest Dermatol. 94:1990;694-699.
64. Verrando P, Juhlin L, Lacour J P, Ortonne J P. Immunohistochemical localization of ornithine decarboxylase in human skin. J Dermatol. 14:1987;112-117.
65. Piacentini M, Martinet N, Beninati S, Folk J E. Free and protein-conjugated polyamines in mouse epidermal cells. Effect of high calcium and retinoic acid. J Biol Chem. 263:1988;3790-3794.
66. Beninati S, Folk J E. Covalent polyamine-protein conjugates: analysis and distribution. Adv Exp Med Biol. 250:1988;411-422.
67. Fesus L, Thomazy V, Autuori F, Ceru M P, Tarcsa E, Piacentini M. Apoptotic hepatocytes become insoluble in detergents and chaotropic agents as a result of transglutaminase action. FEBS Lett. 245:1989;150-154.
68. Piacentini M, Fesus L, Farrace M G, Ghibelli L, Piredda L, Melino G. The expression of "tissue" transglutaminase in two human cancer cell lines is related with the programmed cell death (apoptosis). Eur J Cell Biol. 54:1991;246-254.
69. Gilad G M, Dornay M, Gilad V H. Polyamine treatment in early development leads to increased numbers of rat sympathetic neurons. Brain Res. 348:1985;363-366.
70. Gilad G M, Gilad V H. Polyamines can protect against ischemia-induced nerve cell death in gerbil forebrain. Exp Neurol. 111:1991;349-355.
71. Harada J, Sugimoto M. Polyamines prevent apoptotic cell death in cultured cerebellar granule neurons. Brain Res. 753:1997;251-259.
72. Redman C, Xu M J, Peng Y M, Scott J A, Payne C, Clark L C, Nelson M A. Involvement of polyamines in selenomethionine induced apoptosis and mitotic alterations in human tumor cells. Carcinogenesis. 18:1997;1195-1202.
73. Kaneko H, Hibasami H, Mori K, Kawarada Y, Nakashima K. Apoptosis induction in human breast cancer MRK-nu-1 cells by a polyamine synthesis inhibitor, methylglyoxal bis(cyclopentylamidinohydrazone)(MGBCP). Anticancer Res. 18:1998;891-896.
74. Satoh N, Hibasami H, Mori K, Kaneko H, Wakabayashi H, Hirata K, Sonoda J, Nakashima K, Uchida A. Growth inhibition of human osteosarcoma HuO9 cells by methylglyoxal bis(cyclopentylamidinohydrazone)in vitro and in vivo. Oncol Rep. 6:1999;627-630.
75. Hashimoto Y, Hibasami H, Tamaki S, Kamei A, Ikoma J, Kaito M, Imoto I, Watanabe S, Nakashima K, Adachi Y. Induction of apoptotic cell death in human hepatocellular carcinoma SK-HEP-1 cells by a polyamine synthesis inhibitor, methylglyoxal bis(cyclopentylamidinohydrazone). Anticancer Drugs. 10:1999;323-327.
76. Davidson K, Petit T, Izbicka E, Koester S, Von-Hoff D D. Mitoguazone induces apoptosis via a p53-independent mechanism. Anticancer Drugs. 9:1998;635-640.
77. Brune B, Hartzell P, Nicotera P, Orrenius S. Spermine prevents endonuclease activation and apoptosis in thymocytes. Exp Cell Res. 195:1991;323-329.
78. (2+)- dependent endonuclease from human spleen: purification, properties, and role in apoptosis. Biochemistry. 32:1993;9129-9136.
79. Brooks W H. Polyamine involvement in the cell cycle, apoptosis, and autoimmunity. Med Hypotheses. 44:1995;331-338.
80. Basu H S, Smirnov I V, Peng H F, Tiffany K, Jackson V. Effects of spermine and its cytotoxic analogs on nucleosome formation on topologically stressed DNA in vitro. Eur J Biochem. 243:1997;247-258.
81. Khan A U, Di-Mascio P, Medeiros M H, Wilson T. Spermine and spermidine protection of plasmid DNA against single-strand breaks induced by singlet oxygen. Proc Natl Acad Sci. 89:1992;11428-11430.
82. Muscari C, Guarnieri C, Stefanelli C, Giaccari A, Caldarera C M. Protective effect of spermine on DNA exposed to oxidative stress. Mol Cell Biochem. 144:1995;125-129.
83. Dypbukt J M, Ankarcrona M, Burkitt M, Sjoholm A, Strom K, Orrenius S, Nicotera P. Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. J Biol Chem. 269:1994;30553-30560.
84. Ha H C, Sirisoma N S, Kuppusamy P, Zweier J L, Woster P M, Casero R AJ. The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA. 95:1998;11140-11145.
85. Snyder R D, Vogelpohl S J, Baldwin B L, Deaton E D, Bade E, Carter J D. Apparent inhibition of apoptosis by polyamines and aminothiols in DNA fragmentation assays is artificial. Cell Death Diff. 3:1996;323-330.
86. Williams K. Modulation and block of ion channels: a new biology of polyamines. Cell Signal. 9:1997;1-13.
87. Walev I, Reske K, Palmer M, Valeva A, Bhakdi S. Potassium-inhibited processing of IL-1 beta in human monocytes. EMBO J. 14:1995;1607-1614.
88. Perregaux D, Gabel C A. Interleukin-1 beta maturation and release in response to ATP and nigericin. Evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem. 269:1994;15195-15203.
89. +efflux in the activation of apoptosis. J Biol Chem. 272:1997;32436-32442.
90. Tanaka M, Sawada M, Miura M, Marunouchi T. Insulin-like growth factor-I analogue prevents apoptosis mediated through an interleukin-1 beta converting enzyme (caspase-1)-like protease of cerebellar external granular layer neurons: developmental stage-specific mechanisms of neuronal cell death. Neuroscience. 84:1998;89-100.
91. Miller T M, Moulder K L, Knudson C M, Creedon D J, Deshmukh M, Korsmeyer S J, Johnson E MJ. Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J Cell Biol. 139:1997;205-217.
92. L, C, Penning, G, Denecker, D, Vercammen, W, Declercq, R, G, Schipper, P, Vandenabeele.
93. Auvinen M, Laine A, Paasinen S A, Kangas A, Kangas L, Saksela O, Andersson L C, Holtta E. Human ornithine decarboxylase-overproducing NIH3T3 cells induce rapidly growing, highly vascularized tumors in nude mice. Cancer Res. 57:1997;3016-3025.
94. Shantz L M, Pegg A E. Ornithine decarboxylase induction in transformation by H-Ras and RhoA. Cancer Res. 58:1998;2748-2753.
95. Tabib A, Bachrach U. Polyamines induce malignant transformation in cultured NIH 3T3 fibroblasts. Int J Biochem Cell Biol. 30:1998;135-146.
96. Li L, Li J, Rao J N, Li M, Bass B L, Wang J Y. Inhibition of polyamine synthesis induces p53 gene expression but not apoptosis. Am J Physiol. 276:1999;C946-C954.
97. Ray R M, Zimmerman B J, McCormack S A, Patel T B, Johnson L R. Polyamine depletion arrests cell cycle and induces inhibitors p21(Waf1/Cip1), p27(Kip1), and p53 in IEC-6 cells. Am J Physiol. 276:1999;C684-C691.
98. Donato N J, Rotbein J, Rosenblum M G. Tumor necrosis factor stimulates ornithine decarboxylase activity in human fibroblasts and tumor target cells. J Cell Biochem. 46:1991;69-77.
99. Manchester K M, Heston W D, Donner D B. Tumour necrosis factor-induced cytotoxicity is accompanied by intracellular mitogenic signals in ME-180 human cervical carcinoma cells. Biochem J. 290:1993;185-190.
100. Grassilli E, Bettuzzi S, Monti D, Ingletti M C, Franceschi C, Corti A. Studies on the relationship between cell proliferation and cell death: opposite patterns of SGP-2 and ornithine decarboxylase mRNA accumulation in PHA-stimulated human lymphocytes. Biochem Biophys Res Commun. 180:1991;59-63.
101. Yanagawa K, Yamashita T, Yada K, Ohira M, Ishikawa T, Yano Y, Otani S, Sowa M. The antiproliferative effect of HGF on hepatoma cells involves induction of apoptosis with increase in intracellular polyamine concentration levels. Oncol Rep. 5:1998;185-190.
102. Schipper R G, Otten A E, Lange W P, Schalken J A, Verhofstad A AJ. Polyamine metabolism and programmed cell death in prostatic cancer cells. Urol Res. 23:1995;249.
103. Grassilli E, Desiderio M A, Bellesia E, Salomoni P, Benatti F, Franceschi C. Is polyamine decrease a common feature of apoptosis? Evidence from gamma rays- and heat shock-induced cell death. Biochem Biophys Res Commun. 216:1995;708-714.
104. Das B, Rao A R, Madhubala R. Difluoromethylornithine antagonizes taxol cytotoxicity in MCF-7 human breast cancer cells. Oncol Res. 9:1997;565-572.
105. Mori K, Hibasami H, Satoh N, Sonoda J, Yamasaki T, Tajima M, Higuchi S, Wakabayashi H, Kaneko H, Uchida A, Nakashima K. Induction of apoptotic cell death in three human osteosarcoma cell lines by a polyamine synthesis inhibitor, methylglyoxal bis(cyclopentylamidinohydrazone) (MGBCP). Anticancer Res. 17:1997;2385-2389.