Polyamine catabolism in carcinogenesis: Potential targets for chemotherapy and chemoprevention

Amino Acids

Volumn 46, Issue 3, 2014, Pages 511-519

  Battaglia, Valentina ^a,b   DeStefano Shields, Christina ^a,c   Murray Stewart, Tracy ^a   Casero, Robert A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF PADOVA   (Italy)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Polyamines; Reactive oxygen species; Spermidine; Spermine; Spermine oxidase

Indexed keywords

ACETYLPOLYAMINE OXIDASE; ACYLTRANSFERASE; ALDEHYDE; CELECOXIB; DIAMINE; EFLORNITHINE; HYDROGEN PEROXIDE; N,N' BIS(2,3 BUTADIENYL)PUTRESCINE; NAPHTHALIMIDE DERIVATIVE; OXIDOREDUCTASE INHIBITOR; POLYAMINE DERIVATIVE; POLYAMINE OXIDASE; POLYAMINE OXIDASE INHIBITOR; PUTRESCINE; SPERMIDINE; SPERMIDINE ACETYLTRANSFERASE; SPERMINE; SPERMINE ACETYLTRANSFERASE; SPERMINE OXIDASE; SULINDAC; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; POLYAMINE;

ACUTE KIDNEY FAILURE; ANTIINFLAMMATORY ACTIVITY; BIOLOGICAL ACTIVITY; CANCER CHEMOTHERAPY; CARCINOGENESIS; CATABOLISM; CELL DIFFERENTIATION; CELL GROWTH; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CHEMOPROPHYLAXIS; COLORECTAL CANCER; DNA DAMAGE; DRUG POTENTIATION; DRUG TARGETING; ENZYME ACTIVITY; HUMAN; INFLAMMATION; INTESTINE CANCER; MOLECULAR INTERACTION; NONHUMAN; OXIDATIVE STRESS; POLYAMINE DEPLETION; POLYAMINE METABOLISM; POLYAMINE SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; SIGNAL TRANSDUCTION; SKIN CANCER; ANIMAL; METABOLISM; NEOPLASMS; PATHOLOGY;

EUKARYOTA;

ALDEHYDES; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARCINOGENESIS; HUMANS; HYDROGEN PEROXIDE; NEOPLASMS; POLYAMINES;

EID: 84896316188     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-013-1529-6     Document Type: Short Survey

References (75)

1. Atiya Ali M, Poortvliet E, Strömberg R, Yngve A (2011) Polyamines in foods: development of a food database. Food Nutr Res 55:424-429
2. 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(23):11125-11130 (Pubitemid 46009938)
3. Babbar N, Hacker A, Huang Y, Casero RA Jr (2006a) Tumor necrosis factor alpha induces spermidine/spermine N1-acetyltransferase through nuclear factor kappaB in non-small cell lung cancer cells. J Biol Chem 281(34):24182-24192 (Pubitemid 44274192)
4. Babbar N, Gerner EW, Casero RA Jr (2006c) Induction of spermidine/spermine N1-acetyltransferase (SSAT) by aspirin in Caco-2 colon cancer cells. Biochem J 394(Pt1):317-324 (Pubitemid 43259681)
5. Bardia A, Platz EA, Yegnasubramanian S, De Marzo AM, Nelson WG (2009) Anti-inflammatory drugs, antioxidants, and prostate cancer prevention. Curr Opin Pharmacol 9(4):419-426
6. Bianchi M, Polticelli F, Ascenzi P, Botta M, Federico R, Mariottini P, Cona A (2006) Inhibition of polyamine and spermine oxidases by polyamine analogues. FEBS J 273(6):1115-1123 (Pubitemid 43345033)
7. Burn J, Mathers J, Bishop DT (2013) Genetics, inheritance and strategies for prevention in populations at high risk of colorectal cancer (CRC). Recent Results Cancer Res 191:157-183
8. Casero RA Jr, Marton LJ (2007) Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 6(5):373-390
9. Casero RA Jr, Pegg AE (2009) Polyamine catabolism and disease. Biochem J 421(3):323-338
10. Casero RA Jr, Ervin SJ, Celano P, Baylin SB, Bergeron RJ (1989) Differential response to treatment with the bis(ethyl)polyamine analogues between human small cell lung carcinoma and undifferentiated large cell lung carcinoma in culture. Cancer Res 49(3):639-643 (Pubitemid 19050329)
11. Chaturvedi R, Cheng Y, Asim M, Bussiere FI, Xu H, Gobert AP, Hacker A, Casero RA Jr, Wilson KT (2004) Induction of polyamine oxidase 1 by Helicobacter pylori causes macrophage apoptosis by hydrogen peroxide release and mitochondrial membrane depolarization. J Biol Chem 279(38):40161-40173 (Pubitemid 39258292)
12. Chaturvedi R, de Sablet T, Peek RM, Wilson KT (2012) Spermine oxidase, a polyamine catabolic enzyme that links Helicobacter pylori CagA and gastric cancer cells. Gut Microbes 3(1):48-56
13. Chu FF, Esworthy RS, Chu PG, Longmate JA, Huycke MM, Wilczynski S, Doroshow JH (2004) Bacteria-induced intestinal cancer in mice with disrupted Gpx1 and Gpx2 genes. Cancer Res 64(3):962-968 (Pubitemid 38176898)
14. De Marzo AM, Marchi VL, Epstein JI, Nelson WG (1999) Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol 155(6):1985-1992
15. Goel A, Chang DK, Ricciardiello L, Gasche C, Boland CR (2003) A novel mechanism for aspirin-mediated growth inhibition of human colon cancer cells. Clin Cancer Res 9(1):383-390 (Pubitemid 36109756)
16. 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(7):766-772 (Pubitemid 351632948)
17. Goodwin AC, Destefano Shields CE, Wu S, Huso DL, Wu X, Murray-Stewart TR, Hacker-Prietz A, Rabizadeh S, Woster PM, Sears CL, Casero RA Jr (2011) Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA 108(37):15354-15359
18. Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM, Casero RA Jr (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 95(19):11140-11145 (Pubitemid 28450095)
19. Hong SK, Chaturvedi R, Piazuelo MB, Coburn LA, Williams CS, Delgado AG, Casero RA Jr, Schwartz DA, Wilson KT (2010) Increased expression and cellular localization of spermine oxidase in ulcerative colitis and relationship to disease activity. Inflamm Bowel Dis 16(9):1557-1566
20. Hughes A, Smith NI, Wallace HM (2003) Polyamines reverse non-steroidal anti-inflammatory drug-induced toxicity in human colorectal cancer cells. Biochem J 374(Pt 2):481-488 (Pubitemid 37094107)
21. Igarashi K, Kashiwagi K (2010) Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42(1):39-51
22. Igarashi K, Kashiwagi K (2011) Protein-conjugated acrolein as a biochemical marker of brain infarction. Mol Nutr Food Res 55(9):1332-1341
23. Ignatenko NA, Besselsen DG, Roy UK, Stringer DE, Blohm-Mangone KA, Padilla-Torres JL, Guillen-R JM, Gerner EW (2006) Dietary putrescine reduces the intestinal anticarcinogenic activity of sulindac in a murine model of familial adenomatous polyposis. Nutr Cancer 56(2):172-181 (Pubitemid 46417677)
24. 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(38):40076-40083 (Pubitemid 39258282)
25. Kobayashi M, Iseki K, Saitoh H, Miyazaki K (1992) Uptake characteristics of polyamines into rat intestinal brush-border membrane. Biochim Biophys Acta 1105(1):177-183
26. Kurata HT, Marton LJ, Nichols CG (2006) The polyamine binding site in inward rectifier K+ channels. J Gen Physiol 127(5):467-480
27. Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372(6504):366-369 (Pubitemid 24363439)
28. Löser C, Eisel A, Harms D, Fölsch UR (1999) Dietary polyamines are essential luminal growth factors for small intestinal and colonic mucosal growth and development. Gut 44(1):12-16
29. Luk GD, Goodwin G, Marton LJ, Baylin SB (1981) Polyamines are necessary for the survival of human small-cell lung carcinoma in culture. Proc Natl Acad Sci USA 78(4):2355-2358 (Pubitemid 11119828)
30. Luk GD, Goodwin G, Gazdar AF, Baylin SB (1982) Growth-inhibitory effects of DL-alpha-difluoromethylornithine in the spectrum of human lung carcinoma cells in culture. Cancer Res 42(8):3070-3073 (Pubitemid 12041055)
31. Macarthur M, Hold GL, El-Omar EM (2004) Inflammation and Cancer II. Role of chronic inflammation and cytokine gene polymorphisms in the pathogenesis of gastrointestinal malignancy. Am J Physiol Gastrointest Liver Physiol 286(4):G515-G520 (Pubitemid 38374969)
32. Mandal S, Mandal A, Johansson HE, Orjalo AV, Park MH (2013) Depletion of cellular polyamines, spermidine and spermine, causes a total arrest in translation and growth in mammalian cells. Proc Natl Acad Sci USA 110(6):2169-2174
33. Merentie M, Uimari A, Pietilä M, Sinervirta R, Keinänen TA, Vepsäläinen J, Khomutov A, Grigorenko N, Herzig KH, Jänne J, Alhonen L (2007) Oxidative stress and inflammation in the pathogenesis of activated polyamine catabolism-induced acute pancreatitis. Amino Acids 33(2):323-330 (Pubitemid 47222968)
34. Murray-Stewart T, Wang Y, Devereux W, Casero RA Jr (2002) Cloning and characterization of multiple human polyamine oxidase splice variants that code for isoenzymes with different biochemical characteristics. Biochem J 368(Pt3):673-677 (Pubitemid 36042668)
35. 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(11):2795-2806 (Pubitemid 351678666)
36. Obayashi M, Matsui-Yuasa I, Matsumoto T, Kitano A, Kobayashi K, Otani S (1992) Polyamine metabolism in colonic mucosa from patients with ulcerative colitis. Am J Gastroenterol 87(6):736-740
37. O'Hagan HM, Wang W, Sen S, Destefano Shields C, Lee SS, Zhang YW, Clements EG, Cai Y, Van Neste L, Easwaran H, Casero RA Jr, Sears CL, Baylin SB (2011) Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell 20(5):606-619
38. Park MH, Nishimura K, Zanelli CF, Valentini SR (2010) Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38(2):491-500
39. Pegg AE (2006) Regulation of ornithine decarboxylase. J Biol Chem 281(21):14529-14532
40. Pegg AE (2008) Spermidine/spermine-N(1)-acetyltransferase: a key metabolic regulator. Am J Physiol Endocrinol Metab 294(6):E995-E1010
41. Pegg AE (2009) S-Adenosylmethionine decarboxylase. Essays Biochem 46:25-45
42. Pegg AE, Casero RA Jr (2011) Current status of the polyamine research field. Methods Mol Biol 720:3-35
43. Pledgie-Tracy A, Billam M, Hacker A, Sobolewski MD, Woster PM, Zhang Z, Casero RA Jr, 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(6):1067-1081
44. Poulin R, Casero RA Jr, Soulet D (2012) Recent advances in the molecular biology of metazoan polyamine transport. Amino Acids 42(2-3):711-723
45. Raj KP, Zell JA, Rock CL, McLaren CE, Zoumas-Morse C, Gerner EW, Meyskens FL (2013) Role of dietary polyamines in a phase III clinical trial of difluoromethylornithine (DFMO) and sulindac for prevention of sporadic colorectal adenomas. Br J Cancer 108(3):512-518
46. Ray RM, Zimmerman BJ, McCormack SA, Patel TB, Johnson LR (1999) Polyamine depletion arrests cell cycle and induces inhibitors p21(Waf1/Cip1), p27(Kip1), and p53 in IEC-6 cells. Am J Physiol 276(3 Pt 1):C684-C691 (Pubitemid 29157385)
47. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49(11):1603-1616
48. Riddell RH, Goldman H, Ransohoff DF, Appelman HD, Fenoglio CM, Haggitt RC, Ahren C, Correa P, Hamilton SR, Morson BC et al (1983) Dysplasia in inflammatory bowel disease: standardized classification with provisional clinical applications. Hum Pathol 14(11):931-968
49. Ruschoff J, Wallinger S, Dietmaier W et al (1998) Aspirin suppresses the mutator phenotype associated with hereditary nonpolyposis colorectal cancer by genetic selection. Proc Natl Acad Sci USA 95:11301-11306 (Pubitemid 28450123)
50. Schipper RG, Penning LC, Verhofstad AA (2000) Involvement of polyamines in apoptosis. Facts and controversies: effectors or protectors? Semin Cancer Biol 10(1):55-68 (Pubitemid 30391957)
51. Schreck R, Rieber P, Baeuerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10(8):2247-2258 (Pubitemid 21905698)
52. 1-acetyltransferase in human hepatoma HUH7 cells. Biochimie 94(9):1876-1883
53. ter Steege JC, Forget PP, Buurman WA (1999) Oral spermine administration inhibits nitric oxide-mediated intestinal damage and levels of systemic inflammatory mediators in a mouse endotoxin model. Shock 11(2):115-119
54. Tucker JM, Murphy JT, Kisiel N, Diegelman P, Barbour KW, Davis C, Medda M, Alhonen L, Jänne J, Kramer DL, Porter CW, Berger FG (2005) Potent modulation of intestinal tumorigenesis in Apcmin/+mice by the polyamine catabolic enzyme spermidine/spermine N1-acetyltransferase. Cancer Res 65(12):5390-5398 (Pubitemid 40827352)
55. Turchanowa L, Dauletbaev N, Milovic V, Stein J (2001) Nonsteroidal anti-inflammatory drugs stimulate spermidine/spermine acetyltransferase and deplete polyamine content in colon cancer cells. Eur J Clin Invest 31(10):887-893 (Pubitemid 34592089)
56. Wang Y, Devereux W, Woster P, Stewart T, Hacker A, Casero RA Jr (2001) Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 61(14):5370-5373 (Pubitemid 32694912)
57. Wang Y, Murray-Stewart T, Devereux W, Hacker A, Frydman B, Woster PM, Casero RA Jr (2003) Properties of purified recombinant human polyamine oxidase, PAOh1/SMO. Biochem Biophys Res Commun 304(4):605-611 (Pubitemid 36513529)
58. Wang Y, Hacker A, Murray-Stewart T, Fleischer JG, Woster PM, Casero RA Jr (2005) Induction of human spermine oxidase SMO(PAOh1) is regulated at the levels of new mRNA synthesis, mRNA stabilization and newly synthesized protein. Biochem J 386(Pt 3):543-547 (Pubitemid 40445879)
59. Wang X, Feith DJ, Welsh P, Coleman CS, Lopez C, Woster PM, O'Brien TG, Pegg AE (2007) Studies of the mechanism by which increased spermidine/spermine N1-acetyltransferase activity increases susceptibility to skin carcinogenesis. Carcinogenesis 28(11):2404-2411 (Pubitemid 350111601)
60. Weinberg F, Chandel NS (2009) Reactive oxygen species-dependent signaling regulates cancer. Cell Mol Life Sci 66(23):3663-3673
61. Weiss TS, Herfarth H, Obermeier F, Ouart J, Vogl D, Schölmerich J, Jauch KW, Rogler G (2004) Intracellular polyamine levels of intestinal epithelial cells in inflammatory bowel disease. Inflamm Bowel Dis 10(5):529-535 (Pubitemid 39276459)
62. Williams K (1997) Modulation and block of ion channels: a new biology of polyamines. Cell Signal 9(1):1-13
63. Wu T, Ling KQ, Sayre LM, McIntire WS (2005) Inhibition of murine N1-acetylated polyamine oxidase by an acetylenic amine and the allenic amine, MDL 72527. Biochem Biophys Res Commun 326(2):483-490 (Pubitemid 39593572)
64. Xie SQ, Zhang YH, Li Q, Wang JH, Li JH, Zhao J, Wang CJ (2011) COX-2-independent induction of apoptosis by celecoxib and polyamine naphthalimide conjugate mediated by polyamine depression in colorectal cancer cell lines. Int J Colorectal Dis 27(7):861-868
65. Xu H, Chaturvedi R, Cheng Y, Bussiere FI, Asim M, Yao MD, Potosky D, Meltzer SJ, Rhee JG, Kim SS, Moss SF, Hacker A, Wang Y, Casero RA Jr, Wilson KT (2004) Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res 64(23):8521-8525 (Pubitemid 39552063)
66. Yao Y, Fan Y, Wu J, Wan H, Wang J, Lam S, Lam WL, Girard L, Gazdar AF, Wu Z, Zhou Q (2012) Potential application of non-small cell lung cancer-associated autoantibodies to early cancer diagnosis. Biochem Biophys Res Commun 423(3):613-619
67. Yoshida M, Kashiwagi K, Shigemasa A, Taniguchi S, Yamamoto K, Makinoshima H, Ishihama A, Igarashi K (2004) A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J Biol Chem 279(44):46008-46013 (Pubitemid 39491594)
68. Yuan Q, Ray RM, Johnson LR (2002) Polyamine depletion prevents camptothecin-induced apoptosis by inhibiting the release of cytochrome c. Am J Physiol Cell Physiol 282(6):C1290-C1297 (Pubitemid 34663077)
69. Zahedi K, Wang Z, Barone S, Prada AE, Kelly CN, Casero RA Jr, Yokota N, Porter CW, Rabb H, Soleimani M (2003) Expression of SSAT, a novel biomarker of tubular cell damage, increases in kidney ischemia-reperfusion injury. Am J Physiol Renal Physiol 284(5):F1046-F1055 (Pubitemid 36443590)
70. Zahedi K, Lentsch AB, Okaya T, Barone S, Sakai N, Witte DP, Arend LJ, Alhonen L, Jell J, Jänne J, Porter CW, Soleimani M (2009) Spermidine/spermine-N1-acetyltransferase ablation protects against liver and kidney ischemia-reperfusion injury in mice. Am J Physiol Gastrointest Liver Physiol 296(4):G899-G909
71. Zahedi K, Barone S, Kramer DL, Amlal H, Alhonen L, Jänne J, Porter CW, Soleimani M (2010a) The role of spermidine/spermine N1-acetyltransferase in endotoxin-induced acute kidney injury. Am J Physiol Cell Physiol 299(1):C164-C174
72. Zahedi K, Huttinger F, Morrison R, Murray-Stewart T, Casero RA Jr, Strauss KI (2010b) Polyamine catabolism is enhanced after traumatic brain injury. J Neurotrauma 27(3):515-525
73. Zahedi K, Barone SL, Xu J, Steinbergs N, Schuster R, Lentsch AB, Amlal H, Wang J, Casero RA Jr, Soleimani M (2012) Hepatocyte-specific ablation of spermine/spermidine-N1-acetyltransferase gene reduces the severity of CCl4-induced acute liver injury. Am J Physiol Gastrointest Liver Physiol 303(5):G546-G560
74. Zell JA, McLaren CE, Chen WP, Thompson PA, Gerner EW, Meyskens FL (2010) Ornithine decarboxylase-1 polymorphism, chemoprevention with eflornithine and sulindac, and outcomes among colorectal adenoma patients. J Natl Cancer Inst 102(19):1513-1516
75. Zhang M, Caragine T, Wang H, Cohen PS, Botchkina G, Soda K, Bianchi M, Ulrich P, Cerami A, Sherry B, Tracey KJ (1997) Spermine inhibits proinflammatory cytokine synthesis in human mononuclear cells: a counterregulatory mechanism that restrains the immune response. J Exp Med 185(10):1759-1768 (Pubitemid 27242197)