Recent advances in the molecular biology of metazoan polyamine transport

Amino Acids

Volumn 42, Issue 2-3, 2012, Pages 711-723

  Poulin, R ^a,b   Casero, R A ^c   Soulet, D ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

DNA cloning; Membrane transport; Permeases; Polyamines; Vesicular transport

Indexed keywords

BLEOMYCIN; DOXORUBICIN; PERMEASE; POLYAMINE; PUTRESCINE; SPERMIDINE; SPERMINE;

AMINE TRANSPORT; ANIMAL; BIOACCUMULATION; BIOCHEMISTRY; CELL VACUOLE; CELLULAR DISTRIBUTION; DRUG MECHANISM; ENDOCYTOSIS; ENZYME LOCALIZATION; ENZYME SPECIFICITY; HUMAN; INTERNALIZATION; LEUKEMIA; MAMMAL CELL; MOLECULAR BIOLOGY; MOLECULAR CLONING; NONHUMAN; POLYAMINE METABOLISM; PRIORITY JOURNAL; REVIEW; TESTIS CANCER; TRANSPORT KINETICS; METABOLISM;

ANIMALIA; MAMMALIA; METAZOA;

ANIMALS; BIOGENIC POLYAMINES; SUBSTRATE SPECIFICITY;

EID: 84861677889     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-011-0987-y     Document Type: Review

References (93)

1. Adair GM, Siciliano MJ (1985) Linkage of the MBG locus to another functionally hemizygous gene locus (IDH2) on chromosome Z3 in Chinese hamster ovary cells. Mol Cell Biol 5:109-113 (Pubitemid 15164276)
2. Aouida M, Ramotar D (2010) A new twist in cellular resistance to the anticancer drug bleomycin-A5. Curr Drug Metab 11:595-602. pii:BSP/CDM/E-Pub/ 00088
3. Aouida M, Leduc A, Poulin R, Ramotar D (2005) AGP2 encodes the major permease for high affinity polyamine import in Saccharomyces cerevisiae. J Biol Chem 280:24267-24276. doi: 10.1074/jbc.M503071200 (Pubitemid 40884917)
4. Aouida M, Poulin R, Ramotar D (2010) The human carnitine transporter SLC22A16 mediates high affinity uptake of the anticancer polyamine analogue bleomycin-A5. J Biol Chem 285:6275-6284. doi:10.1074/jbc.M109.046151
5. Aziz SM, Yatin M, Worthen DR, Lipke DW, Crooks PA (1998) A novel technique for visualizing the intracellular localization and distribution of transported polyamines in cultured pulmonary artery smooth muscle cells. J Pharm Biomed Anal 17:307-320. pii:S0731-7085(98)00016-8 (Pubitemid 28261483)
6. Belting M, Havsmark B, Jönsson M, Persson S, Fransson Lå (1996) Heparan sulphate/heparin glycosaminoglycans with strong affinity for the growth-promoter spermine have high antiproliferative activity. Glycobiology 6:121-129 (Pubitemid 26139055)
7. Belting M, Mani K, Jönsson M, Cheng F, Sandgren S, Jonsson S, Ding K, Delcros JG, Fransson L-å (2003) Glypican-1 is a vehicle for polyamine uptake in mammalian cells. A pivotal role for nitrosothiol-derived nitric oxide. J Biol Chem 278:47181-47189. doi:10.1074/jbc.M308325200 (Pubitemid 37455394)
8. Bergeron RJ, Seligsohn HW (1986) Hexahydropyrimidines as masked spermidine vectors in drug delivery. Bioorg Chem 14:345-355 (Pubitemid 17225819)
9. Bergeron RJ, Hawthorne TR, Vinson JRT, Beck DE Jr, Ingeno MJ (1989) Role of the methylene backbone in the antiproliferative activity of polyamine analogues on L1210 cells. Cancer Res 49:2959-2964 (Pubitemid 19148633)
10. Blais Y, Zhao C, Huber M, Audette M, Labrie F, Poulin R (1996) Growth-independent induction of spermidine transport by IL-4 and IL-13 in ZR-75-1 human breast cancer cells. Int J Cancer 67:532-538. doi:10.1002/(SICI) 1097-0215(19960807)67:4\532: AID-IJC12[3.0.CO;2-9 (Pubitemid 26274111)
11. Brachet P, Tome D (1992) Putrescine uptake by rabbit intestinal brush-border membrane vesicles. Biochem Int 27:465-475
12. Brachet P, Debbabi H, Tomé D (1995) Transport and steady-state accumulation of putrescine in brush-border membrane vesicles of rabbit small intestine. Am J Physiol 32:G754-G762 (Pubitemid 3005932)
13. Burns MR, Carlson CL, Vanderwerf SM, Ziemer JR, Weeks RS, Cai F, Webb HK, Graminski GF (2001) Amino acid/spermine conjugates: polyamine amides as potent spermidine uptake inhibitors. J Med Chem 44:3632-3644. pii:jm0101040 (Pubitemid 33026671)
14. Busch AE, Quester S, Ulzheimer JC, Waldegger S, Gorboulev V, Arndt P, Lang F, Koepsell H (1996) Electrogenic properties and substrate specificity of the polyspecific rat cation transporter rOCT1. J Biol Chem 271:32599-32604 (Pubitemid 27008679)
15. Byers TL, Pegg AE (1989) Properties and physiological function of the polyamine transport system. Am J Physiol 257:C545-C553
16. Byers TL, Pegg AE (1990) Regulation of polyamine transport in Chinese hamster ovary cells. J Cell Physiol 143:460-467. doi: 10.1002/jcp.1041430309 (Pubitemid 20201661)
17. Byers TL, Kameji R, Rannels DE, Pegg AE (1987) Multiple pathways for uptake of paraquat, methylglyoxal bis(guanylhydrazone), and polyamines. Am J Physiol 252:C663-C669
18. Byers TL, Wechter R, Nuttall ME, Pegg AE (1989) Expression of a human gene for polyamine transport in Chinese-hamster ovary cells. Biochem J 263:745-752 (Pubitemid 19276453)
19. Casero RA Jr, Woster PM (2009) Recent advances in the development of polyamine analogues as antitumor agents. J Med Chem 52:4551-4573. doi:10.1021/jm900187v
20. Chaney JE, Kobayashi K, Goto R, Digenis GA (1983) Tumor selective enhancement of radioactivity uptake in mice treated with a- difluoromethylornithine prior to administration of 14Cputrescine. Life Sci 32:1237-1241 (Pubitemid 13117967)
21. Coffino P (2001) Regulation of cellular polyamines by antizyme. Nat Rev Mol Cell Biol 2:188-194. doi:10.1038/35056508 (Pubitemid 33675743)
22. Covassin L, Desjardins M, Soulet D, Charest-Gaudreault R, Audette M, Poulin R (2003) Xylylated dimers of putrescine and polyamines: influence of the polyamine backbone on spermidine transport inhibition. Bioorg Med Chem Lett 13:3267-3271. pii:S0960894X03006681 (Pubitemid 37093841)
23. Cullis PM, Green RE, Merson-Davies L, Travis N (1999) Probing the mechanism of transport and compartmentalisation of polyamines in mammalian cells. Chem Biol 6:717-729. pii:S1074-5521(00)80019-8 (Pubitemid 29485534)
24. Daigle ND, Carpentier GA, Frenette-Cotton R, Simard MG, Lefoll MH, Noel M, Caron L, Noel J, Isenring P (2009) Molecular characterization of a human cation-Cl- cotransporter (SLC12A8A, CCC9A) that promotes polyamine and amino acid transport. J Cell Physiol 220:680-689. doi:10.1002/jcp.21814
25. De Smedt H, Van den Bosch L, Geuns J, Borghgraef R (1989) Polyamine transport systems in the LLC-PK1 renal epithelial established cell line. Biochim Biophys Acta 1012:171-177. pii:0167-4889(89)90092-X (Pubitemid 19181750)
26. Delcros JG, Tomasi S, Duhieu S, Foucault M, Martin B, Le Roch M, Eifler-Lima V, Renault J, Uriac P (2006) Effect of polyamine homologation on the transport and biological properties of heterocyclic amidines. J Med Chem 49:232-245. doi:10.1021/ jm050018q (Pubitemid 43078592)
27. Delpire E, Gagnon KB (2008) SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem J 409:321-331. doi:10.1042/ BJ20071324 (Pubitemid 351184951)
28. Dot J, Lluch M, Blanco I, Rodriguez-Alvarez J (2000) Polyamine uptake in cultured astrocytes: characterization and modulation by protein kinases. J Neurochem 75:1917-1926
29. Feige JJ, Chambaz EM (1985) Polyamine uptake by bovine adrenocortical cells. Biochim Biophys Acta 846:93-100. pii:0167-4889(85)90114-4 (Pubitemid 15012800)
30. Garcia-Faroldi G, Rodriguez CE, Urdiales JL, Perez-Pomares JM, Davila JC, Pejler G, Sanchez-Jimenez F, Fajardo I (2010) Polyamines are present in mast cell secretory granules and are important for granule homeostasis. PLoS ONE 5:e15071. doi: 10.1371/journal.pone.0015071
31. Gardner RA, Delcros JG, Konate F, Breitbeil F 3rd, Martin B, Sigman M, Huang M, Phanstiel Ot (2004) N1-substituent effects in the selective delivery of polyamine conjugates into cells containing active polyamine transporters. J Med Chem 47:6055-6069. doi: 10.1021/jm0497040 (Pubitemid 39507347)
32. Gawel-Thompson K, Greene RM (1988) Characterization of a polyamine transport system in murine embryonic palate mesenchymal cells. J Cell Physiol 136:237-246. doi:10.1002/jcp.1041360205
33. Gawel-Thompson KJ, Greene RM (1989) Epidermal growth factor: modulator of murine embryonic palate mesenchymal cell proliferation, polyamine biosynthesis, and polyamine transport. J Cell Physiol 140:359-370. doi:10.1002/jcp.1041400222 (Pubitemid 19186001)
34. Gordonsmith RH, Brooke-Taylor S, Smith LL, Cohen GM (1983) Structural requirements of compounds to inhibit pulmonary diamine accumulation. Biochem Pharmacol 32:3701-3709. pii:0006-2952(83)90138-7 (Pubitemid 14212194)
35. Graminski GF, Carlson CL, Ziemer JR, Cai F, Vermeulen NM, Vanderwerf SM, Burns MR (2002) Synthesis of bis-spermine dimers that are potent polyamine transport inhibitors. Bioorg Med Chem Lett 12:35-40. pii:S0960894X0100659X (Pubitemid 34008564)
36. Groblewski GE, Hargittai PT, Seidel ER (1992) Ca2+/calmodulin regulation of putrescine uptake in cultured gastrointestinal epithelial cells. Am J Physiol 262:C1356-C1363
37. Hasne MP, Ullman B (2011) Genetic and biochemical analysis of protozoal polyamine transporters. Methods Mol Biol 720:309-326. doi:10.1007/978-1-61779- 034-8-19
38. Heinick A, Urban K, Roth S, Spies D, Nunes F, Phanstiel Ot, Liebau E, Luersen K (2010) Caenorhabditis elegans P5B-type ATPase CATP-5 operates in polyamine transport and is crucial for norspermidine-mediated suppression of RNA interference. FASEB J 24:206-217. doi:10.1096/fj.09-135889
39. Huber M, Pelletier J, Torossian K, Dionne P, Gamache I, Charest- Gaudreault R, Audette M, Poulin R (1996) 2, 20-Dithiobis (N-ethyl-spermine-5- carboxamide) is a high affinity, membraneimpermeant antagonist of the mammalian polyamine transport system. J Biol Chem 271:27556-27563 (Pubitemid 26367319)
40. Hurley JH, Hanson PI (2010) Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat Rev Mol Cell Biol 11:556-566. doi:10.1038/nrm2937
41. Igarashi K, Kashiwagi K (2010) Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 48:506-512. doi:10.1016/j.plaphy.2010.01.017
42. Kahana C (2009) Regulation of cellular polyamine levels and cellular proliferation by antizyme and antizyme inhibitor. Essays Biochem 46:47-61. doi:10.1042/bse0460004
43. Kakinuma Y, Hoshino K, Igarashi K (1988) Characterization of the inducible polyamine transporter in bovine lymphocytes. Eur J Biochem 176:409-414
44. Kano K, Oka T (1976) Polyamine transport and metabolism in mouse mammary gland. General properties and hormonal regulation. J Biol Chem 251:2795-2800
45. Käpyaho K, Jänne J (1982) Regulation of putrescine metabolism in Ehrlich ascites carcinoma cells exposed to hypotonic medium. Biochim Biophys Acta 714:93-100 (Pubitemid 12140148)
46. KashiwagiK, Pistocchi R, Shibuya S, Sugiyama S,MorikawaK, Igarashi K (1996) Spermidine-preferential uptake system in Escherichia coli. Identification of amino acids involved in polyamine binding in PotD protein. J Biol Chem 271:12205-12208 (Pubitemid 26160880)
47. Kavanaugh MP (1993) Voltage dependence of facilitated arginine flux mediated by the system y? basic amino acid transporter. Biochemistry 32:5781-5785 (Pubitemid 23175679)
48. Koepsell H, Lips K, Volk C (2007) Polyspecific organic cation transporters: structure, function, physiological roles, and biopharmaceutical implications. Pharm Res 24:1227-1251. doi: 10.1007/s11095-007-9254-z (Pubitemid 46876495)
49. Kumagai J, Johnson LR (1988) Characteristics of putrescine uptake in isolated rat enterocytes. Am J Physiol 254:G81-G86
50. Lessard M, Zhao C, Singh SM, Poulin R (1995) Hormonal and feedback regulation of putrescine and spermidine transport in human breast cancer cells. J Biol Chem 270:1685-1694
51. Li Y, MacKerell AD Jr, Egorin MJ, Ballesteros MF, Rosen DM, Wu YY, Blamble DA, Callery PS (1997) Comparative molecular field analysis-based predictive model of structure-function relationships of polyamine transport inhibitors in L1210 cells. Cancer Res 57:234-239 (Pubitemid 27036599)
52. Lopez-Contreras AJ, Ramos-Molina B, Martinez-de-la-Torre M, Penafiel-Verdu C, Puelles L, Cremades A, Penafiel R (2008) Expression of antizyme inhibitor 2 in male haploid germinal cells suggests a role in spermiogenesis. Int J Biochem Cell Biol 41:1070-1078. doi:10.1016/j.biocel.2008. 09.029
53. Masuko T, Kusama-Eguchi K, Sakata K, Kusama T, Chaki S, Okuyama S, Williams K, Kashiwagi K, Igarashi K (2003) Polyamine transport, accumulation, and release in brain. J Neurochem 84:610-617 (Pubitemid 36182260)
54. McCormack SA, Johnson LR (1989) Putrescine uptake and release by colon cancer cells. Am J Physiol 256:G868-G877
55. Minchin RF, Martin RL (1997) Extracellular calcium stimulates Na+-dependent putrescine uptake in B16 melanoma cells. Int J Biochem Cell Biol 29:447-454. pii:S1357-2725(96)00145-8 (Pubitemid 27230997)
56. Mitchell JL, Judd GG, Bareyal-Leyser A, Ling SY (1994) Feedback repression of polyamine transport is mediated by antizyme in mammalian tissue-culture cells. Biochem J 299:19-22 (Pubitemid 24106282)
57. Mitchell JL, Judd GG, Leyser A, Choe C (1998) Osmotic stress induces variation in cellular levels of ornithine decarboxylaseantizyme. Biochem J 329:453-459 (Pubitemid 28055165)
58. Munro GF, Hercules K, Morgan J, Sauerbier W (1972) Dependence of the putrescine content of Escherichia coli on the osmotic strength of the medium. J Biol Chem 247:1272-1280
59. Munro GF, Miller RA, Bell CA, Verderber EL (1975) Effects of external osmolality on polyamine metabolism in HeLa cells. Biochim Biophys Acta 411:263-281. pii:0304-4165(75)90306-2
60. Nicolet TG, Scemama JL, Pradayrol L, Seva C, Vaysse N (1990) Characterization of putrescine- and spermidine-transport systems of a rat pancreatic acinar tumoral cell line (AR4-2J). Biochem J 269:629-632 (Pubitemid 20236069)
61. Nicolet T, Scemama JL, Pradayrol L, Berthelemy P, Seva C, Vaysse N (1991) Putrescine and spermidine uptake is regulated by proliferation and dexamethasone treatment in AR4-2J cells. Int J Cancer 49:577-581
62. Osborne DL, Seidel ER (1990) Gastrointestinal luminal polyamines: cellular accumulation and enterohepatic circulation. Am J Physiol 258:G576-G584 (Pubitemid 20144078)
63. Parys JB, De Smedt H, Van Den Bosch L, Geuns J, Borghgraef R (1990) Regulation of the Na+-dependent and the Na+-independent polyamine transporters in renal epithelial cells (LLC-PK1). J Cell Physiol 144:365-375. doi:10.1002/jcp.1041440302 (Pubitemid 20263812)
64. Perry JW, Oka T (1980) Regulation of ornithine decarboxylase in cultured mouse mammary gland by the osmolarity in the cellular environment. Biochim Biophys Acta 629:24-35. pii:0304-4165(80)90261-5 (Pubitemid 10033509)
65. Phanstiel Ot, Kaur N, Delcros JG (2007) Structure-activity investigations of polyamine-anthracene conjugates and their uptake via the polyamine transporter. Amino Acids 33:305-313. doi: 10.1007/s00726-007-0527-y (Pubitemid 47222973)
66. Pohjanpelto P (1976) Putrescine transport is greatly increased in human fibroblasts initiated to proliferate. J Cell Biol 68:512-520
67. Porter CW, Bergeron RJ (1983) Spermidine requirement for cell proliferation in eukaryotic cells: structural specificity and quantitation. Science 219:1083-1085
68. Poulin R, Pegg AE (1990) Regulation of ornithine decarboxylase expression by anisosmotic shock in a-difluoromethylornithineresistant L1210 cells. J Biol Chem 265:4025-4032
69. Poulin R, Wechter RS, Pegg AE (1991) An early enlargement of the putrescine pool is required for growth in L1210 mouse leukemia cells under hyposmotic stress. J Biol Chem 266:6142-6151 (Pubitemid 21906196)
70. Poulin R, Coward JK, Lakanen JR, PeggAE(1993) Enhancement of the spermidine uptake system and lethal effects of spermidine overaccumulation in ornithine decarboxylase-overproducing L1210 cells under hyposmotic stress. J Biol Chem 268:4690-4698 (Pubitemid 23081580)
71. Poulin R, Pelletier G, Pegg AE (1995a) Induction of apoptosis by excessive polyamine accumulation in ornithine decarboxylaseoverproducing L1210 cells. Biochem J 311:723-727
72. Poulin R, Lessard M, Zhao C (1995b) Inorganic cation dependence of putrescine and spermidine transport in human breast cancer cells. J Biol Chem 270:1695-1704
73. Poulin R, Zhao C, Verma S, Charest-Gaudreault R, Audette M (1998) Dependence of mammalian putrescine and spermidine transport on plasma- membrane potential: identification of an amiloride binding site on the putrescine carrier. Biochem J 330:1283-1291 (Pubitemid 28162007)
74. Rannels DE, Kameji R, Pegg AE, Rannels SR (1989) Spermidine uptake by type II pneumocytes: interactions of amine uptake pathways. Am J Physiol 257:L346-L353
75. Redgate ES, Grudziak AG, Deutsch M, Boggs SS (1997) Difluoromethylornithine enhanced uptake of tritiated putrescine in 9L rat brain tumors. Int J Radiat Oncol Biol Phys 38:169-174. pii:S0360-3016(97)00243-5 (Pubitemid 27270958)
76. Rinehart CA Jr, Chen KY (1984) Characterization of the polyamine transport system in mouse neuroblastoma cells. Effects of sodium and system A amino acids. J Biol Chem 259:4750-4756 (Pubitemid 14144194)
77. Roy UK, Rial NS, Kachel KL, Gerner EW (2008) Activated K-RAS increases polyamine uptake in human colon cancer cells through modulation of caveolar endocytosis. Mol Carcinog 47:538-553. doi:10.1002/mc.20414 (Pubitemid 351898584)
78. Seiler N (2003) Thirty years of polyamine-related approaches to cancer therapy. Retrospect and prospect. Part 2. Structural analogues and derivatives. Curr Drug Targets 4:565-585 (Pubitemid 37139050)
79. Seiler N, Dezeure F (1990) Polyamine transport in mammalian cells. Int J Biochem 22:211-218 (Pubitemid 20199939)
80. Seiler N, Delcros JG, Moulinoux JP (1996) Polyamine transport in mammalian cells. An update. Int J Biochem Cell Biol 28:843-861 (Pubitemid 26284212)
81. Sharpe JG, Seidel ER (2005) Polyamines are absorbed through a y? amino acid carrier in rat intestinal epithelial cells. Amino Acids 29:245-253. doi:10.1007/s00726-005-0234-5 (Pubitemid 41752087)
82. Soulet D, Covassin L, Kaouass M, Charest-Gaudreault R, Audette M, Poulin R (2002) Role of endocytosis in the internalization of spermidine-C2-BODIPY, a highly fluorescent probe of polyamine transport. Biochem J 367:347-357. doi:10.1042/BJ200 20764 (Pubitemid 35216809)
83. Soulet D, Gagnon B, Rivest S, Audette M, Poulin R (2004) A fluorescent probe of polyamine transport accumulates into intracellular acidic vesicles via a two-step mechanism. J Biol Chem 279:49355-49366. doi:10.1074/jbc.M401287200 (Pubitemid 39642166)
84. Torossian K, Audette M, Poulin R (1996) Substrate protection against inactivation of the mammalian polyamine- transport system by 1-ethyl-3-(3-dimethylaminopropyl)carbodi-imide. Biochem J 319:21-26 (Pubitemid 26394734)
85. Uemura T, Yerushalmi HF, Tsaprailis G, Stringer DE, Pastorian KE, Hawel L 3rd, Byus CV, Gerner EW (2008) Identification and characterization of a diamine exporter in colon epithelial cells. J Biol Chem 283:26428-26435. doi:10.1074/jbc.M804714200
86. Uemura T, Stringer DE, Blohm-Mangone KA, Gerner EW (2010) Polyamine transport is mediated by both endocytic and solute carrier transport mechanisms in the gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 299:G517-G522. doi: 10.1152/ajpgi.00169.2010
87. Volkow N, Goldman SS, Flamm ES, Cravioto H, Wolf AP, Brodie JD (1983) Labeled putrescine as a probe in brain tumors. Science 221:673-675 (Pubitemid 13026088)
88. Wang JT, Kerr MC, Karunaratne S, Jeanes A, Yap AS, Teasdale RD (2010) The SNX-PX-BAR family in macropinocytosis: the regulation of macropinosome formation by SNX-PX-BAR proteins. PLoS ONE 5:e13763. doi:10.1371/journal.pone. 0013763
89. Wassmer T, Attar N, Harterink M, van Weering JR, Traer CJ, Oakley J, Goud B, Stephens DJ, Verkade P, Korswagen HC, Cullen PJ (2009) The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev Cell 17:110-122. doi:10.1016/ j.devcel.2009.04.016
90. Wehner F (2006) Cell volume-regulated cation channels. Contrib Nephrol 152:25-53. doi:10.1159/000096315 (Pubitemid 44672102)
91. Wilson L, Gage P, Ewart G (2006) Hexamethylene amiloride blocks E protein ion channels and inhibits coronavirus replication. Virology 353:294-306. doi:10.1016/j.virol.2006.05.028 (Pubitemid 44397131)
92. Winter TN, Elmquist WF, Fairbanks CA (2011) OCT2 and MATE1 provide bidirectional agmatine transport. Mol Pharm 8:133-142. doi:10.1021/mp100180a
93. Wu X, Davis MJ (2001) Characterization of stretch-activated cation current in coronary smooth muscle cells. Am J Physiol Heart Circ Physiol 280:H1751-H1761