Inhibition of cation channels in human erythrocytes by spermine

Journal of Membrane Biology

Volumn 237, Issue 2-3, 2010, Pages 93-106

  Kucherenko, Yuliya V ^a,b   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b INSTITUTE FOR PROBLEMS OF CRYOBIOLOGY AND CRYOMEDICINE   (Ukraine)

Author keywords

Aging; Ca2+; Cell volume; Channel; NASPM; Phosphatidylserine exposure; Red blood cell; Spermine

Indexed keywords

CALCIUM ION; CATION CHANNEL; CHLORIDE ION; LIPOCORTIN 5; MONOVALENT CATION; NAPHTHYL GROUP; POTASSIUM ION; SODIUM CHLORIDE; SODIUM ION; SPERMINE;

ARTICLE; BATH; CALCIUM CELL LEVEL; CATION TRANSPORT; CELL MEMBRANE; CELL SURVIVAL; CELL VOLUME; CONDUCTANCE; CYTOSOL; ELECTRIC POTENTIAL; ERYTHROCYTE; ERYTHROCYTE LIFESPAN; FLUORESCENCE; HUMAN; PATCH CLAMP; SPERMATOZOON DENSITY; STATISTICAL SIGNIFICANCE; WHOLE CELL;

CALCIUM; CELLS, CULTURED; ELECTROPHYSIOLOGY; ERYTHROCYTES; HUMANS; ION CHANNELS; PATCH-CLAMP TECHNIQUES; SPERMINE;

EID: 78649935627     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00232-010-9310-1     Document Type: Article

References (85)

1. E Agostinelli G Tempera N Viceconte, et al. 2010 Potential anticancer application of polyamine oxidation products formed by amine oxidase: a new therapeutic approach Amino Acids 38 353 368 1:CAS:528:DC%2BC3cXhs1Ojsr4%3D 10.1007/s00726-009-0431-8 20012114
2. 19F-NMR spectroscopy Biochim Biophys Acta 1136 155 160 1:CAS:528:DyaK38Xls1ygt7c%3D 10.1016/0167-4889(92)90251-6 1504100
3. U Bachrach 1970 Metabolism and function of spermine and related polyamines Annu Rev Microbiol 24 109 134 1:CAS:528:DyaE3MXhvFansw%3D%3D 10.1146/annurev.mi.24.100170.000545 4927131
4. Bachrach U (1973) Function of naturally occurring polyamines. Academic Press, New York
5. SK Ballas MR Clark N Mohandas, et al. 1983 Polyamines do not inhibit erythrocyte ATPase activities Clin Chim Acta 129 287 293 1:CAS:528: DyaL3sXktVersLg%3D 10.1016/0009-8981(83)90031-1 6303631 (Pubitemid 13117653)
6. SK Ballas N Mohandas LJ Marton, et al. 1983 Stabilization of erythrocyte membranes by polyamines Proc Natl Acad Sci USA 80 1942 1946 1:CAS:528: DyaL3sXhslGhtr4%3D 10.1073/pnas.80.7.1942 6572953
7. PH Barry JW Lynch 1991 Liquid junction potentials and small cell effects in patch-clamp analysis J Membr Biol 121 101 117 1:STN:280:DyaK3MzltVWlsQ%3D%3D 10.1007/BF01870526 1715403
8. 2+ into human red cells Bioelectrochemistry 73 145 150 1:CAS:528: DC%2BD1cXhtVSjs7zK 10.1016/j.bioelechem.2008.04.006 18534924
9. SB Baylin BJ Rosenstein LJ Marton, et al. 1980 Age-related abnormalities of circulating polyamines and diamine oxidase activity in cystic fibrosis heterozygotes and homozygotes Pediatr Res 14 921 925 1:STN:280: DyaL3M%2FjtFynsQ%3D%3D 10.1203/00006450-198008000-00005 6775274
10. P Bennekou 1993 The voltage-gated nonselective cation channel from human red cells is sensitive to acetylcholine Biochim Biophys Acta 1147 165 167 1:CAS:528:DyaK3sXit1Kgsr8%3D 10.1016/0005-2736(93)90328-W 7682111 (Pubitemid 23104901)
11. P Bennekou TL Barksmann LR Jensen, et al. 2004 Voltage activation and hysteresis of the nonselective voltage-dependent channel in the intact human red cell Bioelectrochemistry 62 181 185 1:CAS:528:DC%2BD2cXisVartrY%3D 10.1016/j.bioelechem.2003.08.006 15039024 (Pubitemid 38376161)
12. L Bordin F Cattapan G Clari, et al. 1994 Spermine-mediated casein kinase II-uptake by rat liver mitochondria Biochim Biophys Acta 1199 266 270 1:CAS:528:DyaK2cXksFantL0%3D 7718030
13. GJ Bosman FL Willekens JM Werre 2005 Erythrocyte aging: a more than superficial resemblance to apoptosis? Cell Physiol Biochem 16 1 8 1:CAS:528:DC%2BD2MXos1ChsrY%3D 10.1159/000087725 16121027 (Pubitemid 41197082)
14. V Brand S Koka C Lang, et al. 2008 Influence of amitriptyline on eryptosis, parasitemia and survival of Plasmodium berghei-infected mice Cell Physiol Biochem 22 405 412 1:CAS:528:DC%2BD1cXhsV2lt7bM 10.1159/000185482 19088422
15. JA Browning HM Staines HC Robinson, et al. 2007 The effect of deoxygenation on whole-cell conductance of red blood cells from healthy individuals and patients with sickle cell disease Blood 109 2622 2629 1:CAS:528:DC%2BD2sXnslygtrY%3D 10.1182/blood-2006-03-001404 17138828 (Pubitemid 46425912)
16. R Bucki C Bachelot-Loza A Zachowski, et al. 1998 Calcium induces phospholipid redistribution and microvesicle release in human erythrocyte membranes by independent pathways Biochemistry 37 15383 15391 1:CAS:528:DyaK1cXmsF2it7s%3D 10.1021/bi9805238 9799499 (Pubitemid 28515999)
17. PM Cala JG Norby DC Tosteson 1982 Effects of the plant alkaloid sanguinarine on cation transport by human red blood cells and lipid bilayer membranes J Membr Biol 64 23 31 1:CAS:528:DyaL38XpvFSrtg%3D%3D 10.1007/BF01870765 7057451
18. I Cino A Formenti 2008 Spermine biphasically affects N-type calcium channel currents in adult dorsal root ganglion neurons of the rat Biochim Biophys Acta 1778 2437 2443 1:CAS:528:DC%2BD1cXhtFCktbvL 10.1016/j.bbamem.2008. 07.006 18675782
19. G Clari A Toninello L Bordin, et al. 1994 Spermine effect on the binding of casein kinase I to the rat liver mitochondrial structures Biochem Biophys Res Commun 205 389 395 1:CAS:528:DyaK2MXis1alsLs%3D 10.1006/bbrc.1994.2677 7999054 (Pubitemid 24381638)
20. LF Cohen DW Lundgren PM Farrell 1976 Distribution of spermidine and spermine in blood from cystic fibrosis patients and control subjects Blood 48 469 475 1:CAS:528:DyaE28XkvFWlsb4%3D 953366
21. KD Cooper JB Shukla OM Rennert 1976 Polyamine distribution in cellular compartments of blood and in aging erythrocytes Clin Chim Acta 73 71 88 1:CAS:528:DyaE2sXktVymug%3D%3D 10.1016/0009-8981(76)90307-7 1000842
22. B Corry TW Allen S Kuyucak, et al. 2001 Mechanisms of permeation and selectivity in calcium channels Biophys J 80 195 214 1:CAS:528: DC%2BD3MXkvFWjsr8%3D 10.1016/S0006-3495(01)76007-9 11159395
23. VL Dalla NV Di D Siliprandi, et al. 1996 Spermine binding to liver mitochondria Biochim Biophys Acta 1284 247 252 10.1016/S0005-2736(96)00140-X (Pubitemid 26356161)
24. VL Dalla NV Di A Toninello 1998 Spermine binding to liver mitochondria deenergized by ruthenium red plus either FCCP or antimycin A FEBS Lett 422 36 42 10.1016/S0014-5793(97)01594-9 (Pubitemid 28052861)
25. --dependent cation conductance in human red blood cells J Physiol 539 847 855 1:CAS:528:DC%2BD38Xjt1ejs7o%3D 10.1113/jphysiol.2001.013040 11897854 (Pubitemid 35175434)
26. S Egee O Mignen BJ Harvey, et al. 1998 Chloride and nonselective cation channels in unstimulated trout red blood cells J Physiol 511 Pt 1 213 224 1:CAS:528:DyaK1cXmtlCqt7k%3D 10.1111/j.1469-7793.1998.213bi.x 9679175 (Pubitemid 28421324)
27. 2+ conductance in C. elegans intestinal cells J Physiol 567 239 251 1:CAS:528:DC%2BD2MXps1Omsbk%3D 10.1113/jphysiol.2005.091900 15961418 (Pubitemid 41167318)
28. A Ferrante CM Rzepczyk AC Allison 1983 Polyamine oxidase mediates intra-erythrocytic death of Plasmodium falciparum Trans R Soc Trop Med Hyg 77 789 791 1:CAS:528:DyaL2cXosVSrtw%3D%3D 10.1016/0035-9203(83)90290-0 6364468
29. 2+ leak of human erythrocytes Cell Physiol Biochem 21 183 192 10.1159/000113760 18209485
30. M Foller D Bobbala S Koka, et al. 2009 Suicide for survival-death of infected erythrocytes as a host mechanism to survive malaria Cell Physiol Biochem 24 133 140 10.1159/000233238 19710527
31. M Foller H Mahmud S Gu, et al. 2009 Modulation of suicidal erythrocyte cation channels by an AMPA antagonist J Cell Mol Med 13 3680 3686 10.1111/j.1582-4934.2009.00745.x 19320779
32. + channel for the short-term survival of injured erythrocytes Pflugers Arch 460 1029 10.1007/s00424-010-0878-1 20857305
33. SM Huber N Gamper F Lang 2001 Chloride conductance and volume-regulatory nonselective cation conductance in human red blood cell ghosts Pflugers Arch 441 551 558 1:CAS:528:DC%2BD3MXlt1Ogtw%3D%3D 10.1007/s004240000456 11212220 (Pubitemid 32128152)
34. 2+-ATPase by spermine and other polycationic compounds Biochemistry 33 4745 4754 1:CAS:528:DyaK2cXis1CgtLc%3D 10.1021/bi00182a001 8161533 (Pubitemid 24158422)
35. L Kaestner I Bernhardt 2002 Ion channels in the human red blood cell membrane: their further investigation and physiological relevance Bioelectrochemistry 55 71 74 1:CAS:528:DC%2BD38Xls1enug%3D%3D 10.1016/S1567-5394(01)00164-5 11786344 (Pubitemid 34084755)
36. L Kaestner C Bollensdorff I Bernhardt 1999 Nonselective voltage-activated cation channel in the human red blood cell membrane Biochim Biophys Acta 1417 9 15 1:CAS:528:DyaK1MXhsVynsbs%3D 10.1016/S0005-2736(98)00240-5 10076030 (Pubitemid 29078581)
37. L Kaestner P Christophersen I Bernhardt, et al. 2000 The nonselective voltage-activated cation channel in the human red blood cell membrane: reconciliation between two conflicting reports and further characterisation Bioelectrochemistry 52 117 125 1:CAS:528:DC%2BD3cXot1yls7g%3D 10.1016/S0302-4598(00)00110-0 11129235
38. DS Kempe PA Lang C Duranton, et al. 2006 Enhanced programmed cell death of iron-deficient erythrocytes FASEB J 20 368 370 1:CAS:528:DC%2BD28XhsFOksLs%3D 16371427
39. DS Kempe A Akel PA Lang, et al. 2007 Suicidal erythrocyte death in sepsis J Mol Med 85 273 281 1:CAS:528:DC%2BD2sXhvVehs78%3D 10.1007/s00109-006-0123-8 17180345 (Pubitemid 46295242)
40. HH Kerschbaum JA Kozak MD Cahalan 2003 Polyvalent cations as permeant probes of MIC and TRPM7 pores Biophys J 84 2293 2305 1:CAS:528: DC%2BD3sXivVent7Y%3D 10.1016/S0006-3495(03)75035-8 12668438
41. NA Khan V Quemener P Moulinoux 1990 Inhibition of adenylate cyclase activity by polyamines in human erythrocyte plasma membranes Life Sci 46 43 47 1:CAS:528:DyaK3cXnt1ygsQ%3D%3D 10.1016/0024-3205(90)90055-V 2105420 (Pubitemid 20019512)
42. CR Kiefer LM Snyder 2000 Oxidation and erythrocyte senescence Curr Opin Hematol 7 113 116 1:STN:280:DC%2BD3c7mt1Whtg%3D%3D 10.1097/00062752-200003000- 00007 10698298 (Pubitemid 30106543)
43. +/spermine antiporter in the rat renal brush-border membrane J Pharm Pharmacol 51 279 284 1:CAS:528:DyaK1MXislGhsLg%3D 10.1211/0022357991772457 10344628
44. H Koenig A Goldstone CY Lu 1983 Polyamines regulate calcium fluxes in a rapid plasma membrane response Nature 305 530 534 1:CAS:528:DyaL3sXls12qsbg%3D 10.1038/305530a0 6413866 (Pubitemid 13009093)
45. 2+-permeable AMPA receptors in cultured rat hippocampal neurons Neurosci Res 29 27 36 1:CAS:528:DyaK2sXmtF2qt7s%3D 10.1016/S0168-0102(97)00067- 9 9293490 (Pubitemid 27365675)
46. S Koka C Lang KM Boini, et al. 2008 Influence of chlorpromazine on eryptosis, parasitemia and survival of Plasmodium berghe infected mice Cell Physiol Biochem 22 261 268 1:CAS:528:DC%2BD1cXhtVKlsL7L 10.1159/000149804 18769053
47. S Koka C Lang OM Niemoeller, et al. 2008 Influence of NO synthase inhibitor l-NAME on parasitemia and survival of Plasmodium berghei infected mice Cell Physiol Biochem 21 481 488 1:CAS:528:DC%2BD1cXltFOrtL4%3D 10.1159/000129641 18453756 (Pubitemid 351620302)
48. S Koka D Bobbala C Lang, et al. 2009 Influence of paclitaxel on parasitemia and survival of Plasmodium berghei infected mice Cell Physiol Biochem 23 191 198 1:CAS:528:DC%2BD1MXitVGjtbY%3D 10.1159/000204107 19255513
49. A Kossorotow HU Wolf N Seiler 1974 Regulatory effects of polyamines on membrane-bound acetylcholinesterase Biochem J 144 21 27 1:CAS:528: DyaE2MXhtVyjtbw%3D 4462573
50. Y Kucherenko SK Bhavsar VI Grischenko, et al. 2010 Increased cation conductance in human erythrocytes artificially aged by glycation J Membr Biol 235 177 1:CAS:528:DC%2BC3cXotVajsb8%3D 10.1007/s00232-010-9265-2 20526772
51. FA Kuypers 2007 Membrane lipid alterations in hemoglobinopathies Hematology Am Soc Hematol Educ Program 2007 68 73
52. PA Lang O Beringer JP Nicolay, et al. 2006 Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome J Mol Med 84 378 388 10.1007/s00109-006-0058-0 16622713 (Pubitemid 43673612)
53. PA Lang M Schenck JP Nicolay, et al. 2007 Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide Nat Med 13 164 170 1:CAS:528:DC%2BD2sXhsVyktbc%3D 10.1038/nm1539 17259995
54. F Lang E Gulbins H Lerche, et al. 2008 Eryptosis, a window to systemic disease Cell Physiol Biochem 22 373 380 1:CAS:528:DC%2BD1cXhsV2lt7nK 10.1159/000185448 19088418
55. PA Lang RS Kasinathan VB Brand, et al. 2009 Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and Annexin-A7 deficiency Cell Physiol Biochem 24 415 428 1:CAS:528:DC%2BD1MXhsVSktrzE 10.1159/000257529 19910682
56. F Lapaix G Bouyer S Thomas, et al. 2008 Further characterization of cation channels present in the chicken red blood cell membrane Bioelectrochemistry 73 129 136 1:CAS:528:DC%2BD1cXhtVSjs7%2FE 10.1016/j.bioelechem.2008.04.003 18534923
57. 2+ transport Biochem J 286 Pt 2 597 602 1:CAS:528:DyaK38XlsVGnu78%3D 1530590
58. VL Lew N Daw Z Etzion, et al. 2007 Effects of age-dependent membrane transport changes on the homeostasis of senescent human red blood cells Blood 110 1334 1342 1:CAS:528:DC%2BD2sXptFKls7Y%3D 10.1182/blood-2006-11-057232 17456724 (Pubitemid 47281434)
59. X Lin E Fenn RD Veenstra 2006 An amino-terminal lysine residue of rat connexin40 that is required for spermine block J Physiol 570 251 269 1:CAS:528:DC%2BD28XmtV2isw%3D%3D 16284078
60. 2+-dependent pathway without caspase-3 activation Arch Toxicol 81 859 865 1:CAS:528:DC%2BD2sXhsVOqsLfO 10.1007/s00204-007-0214-5 17541556 (Pubitemid 350198003)
61. H Mahmud D Mauro SM Qadri, et al. 2009 Triggering of suicidal erythrocyte death by amphotericin B Cell Physiol Biochem 24 263 270 1:CAS:528: DC%2BD1MXpsVaks7s%3D 10.1159/000233251 19710541
62. A Makhro J Wang J Vogel, et al. 2010 Functional NMDA receptors in rat erythrocytes Am J Physiol Cell Physiol 298 C1315 C1325 1:CAS:528: DC%2BC3cXnvFanu7o%3D 10.1152/ajpcell.00407.2009 20457837
63. J Molgo E del Pozo JE Banos, et al. 1991 Changes of quantal transmitter release caused by gadolinium ions at the frog neuromuscular junction Br J Pharmacol 104 133 138 1:CAS:528:DyaK3MXmtVequrc%3D 1686201
64. OM Niemoeller M Foller C Lang, et al. 2008 Retinoic acid induced suicidal erythrocyte death Cell Physiol Biochem 21 193 202 1:CAS:528: DC%2BD1cXps1ajtQ%3D%3D 10.1159/000113761 18209486
65. OM Niemoeller H Mahmud M Foller, et al. 2008 Ciglitazone and 15d-PGJ2 induced suicidal erythrocyte death Cell Physiol Biochem 22 237 244 1:CAS:528:DC%2BD1cXhtVKlsL7I 10.1159/000149801 18769050
66. 2+-activated cation channel TRPM4b Pflugers Arch 448 70 75 1:CAS:528:DC%2BD2cXitFehtb4%3D 10.1007/s00424-003-1221-x 14758478 (Pubitemid 38657207)
67. M Orta E Ordoqui A Aranzabal, et al. 2003 Anaphylactic reaction after artificial insemination Ann Allergy Asthma Immunol 90 446 451 10.1016/S1081-1206(10)61831-5 12722969
68. MS Proctor HV Fletcher Jr JB Shukla, et al. 1975 Elevated spermidine and spermine levels in the blood of psoriasis patients J Invest Dermatol 65 409 411 1:STN:280:DyaE28%2Fis1Sgtg%3D%3D 10.1111/1523-1747.ep12607659 1176793
69. O Rennert T Miale J Shukla, et al. 1976 Polyamine concentrations in bone marrow aspirates of children with leukemia and other malignancies Blood 47 695 701 1:STN:280:DyaE287mtFyqsQ%3D%3D 1260130
70. PJ Romero EA Romero D Mateu, et al. 2006 Voltage-dependent calcium channels in young and old human red cells Cell Biochem Biophys 46 265 276 1:CAS:528:DC%2BD2sXhvFWms7c%3D 10.1385/CBB:46:3:265 17272852 (Pubitemid 46202580)
71. DH Russell 1971 Increased polyamine concentrations in the urine of human cancer patients Nat New Biol 233 144 145 1:STN:280:DyaE38%2FjtlSjuw%3D%3D 5286749
72. CM Rzepczyk AJ Saul A Ferrante 1984 Polyamine oxidase-mediated intraerythrocytic killing of Plasmodium falciparum: evidence against the role of reactive oxygen metabolites Infect Immun 43 238 244 1:CAS:528: DyaL2cXms1Cksg%3D%3D 6360897
73. JR Sachs 1994 Soluble polycations and cationic amphiphiles inhibit volume-sensitive K-Cl cotransport in human red cell ghosts Am J Physiol Cell Physiol 266 C997 C1005 1:CAS:528:DyaK2cXlsFWnsr4%3D
74. JA Sanchez-Chapula MC Sanguinetti 2000 Altered gating of HERG potassium channels by cobalt and lanthanum Pflugers Arch 440 264 274 1:CAS:528: DC%2BD3cXjs1Cnu7c%3D 10898527
75. Shaw GG (1994) Polyamines as neurotransmitters or modulators. In: Carter C (ed) Neuropharmacology of polyamines. Academic Press, London, pp 61-80
76. J Shi E Mori Y Mori, et al. 2004 Multiple regulation by calcium of murine homologues of transient receptor potential proteins TRPC6 and TRPC7 expressed in HEK293 cells J Physiol 561 415 432 1:CAS:528:DC%2BD2cXhtFait73P 10.1113/jphysiol.2004.075051 15579537 (Pubitemid 39646532)
77. M Sopjani M Foller P Dreischer, et al. 2008 Stimulation of eryptosis by cadmium ions Cell Physiol Biochem 22 245 252 1:CAS:528:DC%2BD1cXhtVKlsL7J 10.1159/000149802 18769051
78. M Sopjani M Foller E Gulbins, et al. 2008 Suicidal death of erythrocytes due to selenium-compounds Cell Physiol Biochem 22 387 394 1:CAS:528: DC%2BD1cXhsV2lt7nE 10.1159/000185452 19088420
79. AV Starushchenko I Neguliaev EZ Morachevskaia 2002 Inhibiting and stimulating effect of amiloride on potential-dependent cation channels in K562 cells [in Russian] Tsitologiia 44 676 680 1:STN:280:DC%2BD38npsVKhtA%3D%3D 12455378
80. A Tassoni F Antognoni N Bagni 1996 Polyamine binding to plasma membrane vesicles isolated from zucchini hypocotyls Plant Physiol 110 817 824 1:CAS:528:DyaK28Xhs1GisLo%3D 12226221
81. M Toner G Vaio A McLaughlin, et al. 1988 Adsorption of cations to phosphatidylinositol 4,5-bisphosphate Biochemistry 27 7435 7443 1:CAS:528:DyaL1cXlt12msLo%3D 10.1021/bi00419a039 2849993
82. 2+-activated cation channels TRPM4 and TRPM5 from mice Cell Calcium 37 267 278 1:CAS:528:DC%2BD2MXms1GjsA%3D%3D 10.1016/j.ceca.2004.11.001 15670874
83. 2+-permeable cation conductance sensitive to carbon monoxide and to GsMTx-4 in human and mouse sickle erythrocytes PLoS One 5 e8732 10.1371/journal.pone.0008732 20090940
84. K Wang H Mahmud M Foller, et al. 2008 Lipopeptides in the triggering of erythrocyte cell membrane scrambling Cell Physiol Biochem 22 381 386 1:CAS:528:DC%2BD1cXhsV2lt7nL 10.1159/000187116 19088419
85. S Zhu M Ashok J Li, et al. 2009 Spermine protects mice against lethal sepsis partly by attenuating surrogate inflammatory markers Mol Med 15 275 282 1:CAS:528:DC%2BD1MXotlajtb4%3D 19593412