Cellular efflux of cAMP and cGMP - A question about selectivity

Mini-Reviews in Medicinal Chemistry

Volumn 9, Issue 8, 2009, Pages 1009-1013

  Sager, Georg ^a   Ravna, Aina Westrheim ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

ABCC11; ABCC4; ABCC5; cAMP; cGMP; Transport selectivity

Indexed keywords

CARRIER PROTEIN; CYANIDE; CYCLIC AMP; CYCLIC GMP; CYCLIC NUCLEOTIDE GATED CHANNEL; ESTRADIOL; IODOACETIC ACID; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; MULTIDRUG RESISTANCE PROTEIN 8; NOCODAZOLE; OLIGOMYCIN; PAPAVERINE; PROBENECID; PROSTAGLANDIN; UNCLASSIFIED DRUG; VERAPAMIL; VINBLASTINE;

CELL TRANSPORT; CELL TYPE; DRUG SELECTIVITY; DRUG TARGETING; HUMAN; MEMBRANE TRANSPORT; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW;

EID: 70349089306     PISSN: 13895575     EISSN: None     Source Type: Journal    
DOI: 10.2174/138955709788681654     Document Type: Review

References (66)

1. Sutherland, E.W.; RALL, T.W. Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles. J. Biol. Chem., 1958, 232, 1077-91.
2. Ashman, D.F.; Lipton, R.; Melicow, M.M.; Price, T.D. Isolation of adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate from rat urine. Biochem. Biophys. Res. Commun., 1963, 11, 330-34.
3. Beavo, J.A.; Brunton, L.L. Cyclic nucleotide research - still expanding after half a century. Nat. Rev. Mol. Cell Biol., 2002, 3, 710-18.
4. Davoren, P.R.; Sutherland, E.W. The effect of l-epinephrine and other agents on the synthesis and release of adenosine 3′,5′-phosphate by whole pigeon erythrocytes. J. Biol. Chem., 1963, 238, 3009-15.
5. Barber, R.; Butcher, R.W. The egress of cyclic AMP from metazoan cells. Adv. Cycl. Nucleotide Res., 1983, 15, 119-38.
6. Penit, J.; Jard, S.; Benda, P. Probenecid sensitive 3′,5′-cyclic AMP secretion by isoproterenol stimulated glial cells in culture. FEBS Lett., 1974, 41, 156-60.
7. King,C.D. ; Mayer,S.E. Inhibition of egress of adenosine 3′,5′-monophosphate from pigeon erythrocytes. Mol. Pharmacol., 1974, 10, 941-53.
8. Doore, B.J.; Bashor, M.M.; Spitzer, N.; Mawe, R.C. Regulation of adenosine 3' :5'-monophosphate efflux from rat glioma cells in culture. J. Biol. Chem., 1975, 250, 4371-72.
9. Brunton, L.L.; Mayer, S.E. Extrusion of cyclic AMP from pigeon erythrocytes. J. Biol. Chem., 1979, 254, 9714-20.
10. Strewler, G.J. Release of cAMP from a renal epithelial cell line. Am. J. Physiol., 1984, 246, C224-C230.
11. Heasley, L.E.; Azari, J.; Brunton, L.L. Export of cyclic AMP from avian red cells. Independence from major membrane transporters and specific inhibition by prostaglandin A. Mol. Pharmacol., 1985, 27, 60-65.
12. Henderson, G.B.; Strauss, B.P. Evidence for cAMP and cholate extrusion in C6 rat glioma cells by a common anion efflux pump. J. Biol. Chem., 1991, 266, 1641-45.
13. Hamet, P.; Pang, S.C.; Tremblay, J. Atrial natriuretic factor-induced egression of cyclic guanosine 3′:5′-monophosphate in cultured vascular smooth muscle and endothelial cells. J. Biol. Chem., 1989, 264, 12364-69.
14. Marley, P.D.; Thomson, K.A. Regulation of cyclic AMP metabolism in bovine adrenal medullary cells. Biochem. Pharmacol., 1992, 44, 2105-10.
15. Ahlstrom, M. ; Lamberg-Allardt, C. Regulation of adenosine 3′,5′-cyclic monophosphate (cAMP) accumulation in UMR-106 osteoblast-like cells: role of cAMP-phosphodiesterase and cAMP efflux. Biochem. Pharmacol., 1999, 58, 1335-40.
16. Orlov, S.N.; Maksimova, N.V. Efflux of cyclic adenosine monophosphate from cells: mechanisms and physiological implications. Biochemistry (Moscow), 1999, 64, 127-35.
17. Kapoor, C.L.; Krishna, G. Hormone-induced cyclic guanosine monophosphate secretion from guinea pig pancreatic lobules. Science, 1977, 196, 1003-05.
18. Tjörnhammar, M.L.; Lazaridis, G.; Bartfai, T. Cyclic GMP efflux from liver slices. J. Biol. Chem., 1983, 258, 6882-86.
19. Tjörnhammar, M.L.; Lazaridis, G.; Bartfai, T. Efflux of cyclic guanosine 3′,5′-monophosphate from cerebellar slices stimulated by L-glutamate or high K+ or N-methyl-N'-nitro-N-nitrosguanidine. Neurosci. Lett., 1986, 68, 95-99.
20. Fiscus, R.R.; Robles, B.T.; Waldman, S.A.; Murad, F. Atrial natriuretic factors stimulate accumulation and efflux of cyclic GMP in C6-2B rat glioma and PC12 rat pheochromocytoma cell cultures. J. Neurochem., 1987, 48, 522-28.
21. Geary, C.A.; Goy, M.F.; Boucher, R.C. Synthesis and vectorial export of cGMP in airway epithelium: expression of soluble and CNP-specific guanylate cyclases. Am. J. Physiol., 1993, 265, L598-L605.
22. Wu, X.B.; Brune, B.; von Appen, F.; Ullrich, V. Efflux of cyclic GMP from activated human platelets. Mol. Pharmacol., 1993, 43, 564-68.
23. Radziszewski, W.; Chopra, M.; Zembowicz, A.; Gryglewski, R.; Ignarro, L.J.; Chaudhuri, G. Nitric oxide donors induce extrusion of cyclic GMP from isolated human blood platelets by a mechanism which may be modulated by prostaglandins. Int. J. Cardiol., 1995, 51, 211-20.
24. Sager, G.; Ørbo, A.; Pettersen, R.H.; Kjørstad, K.E. Export of guanosine 3′,5′-cyclic monophosphate (cGMP) from human erythrocytes characterized by inside-out membrane vesicles. Scand. J. Clin. Lab. Invest., 1996, 56, 289-93.
25. Schultz, C.; Vaskinn, S.; Kildalsen, H.; Sager, G. Cyclic AMP stimulates the cyclic GMP egression pump in human erythrocytes: effects of probenecid, verapamil, progesterone, theophylline, IBMX, forskolin, and cyclic AMP on cyclic GMP uptake and association to inside-out vesicles. Biochemistry, 1998, 37, 1161-66.
26. 4) does not share a cellular efflux mechanism with cGMP: characterisation of cGMP transport by uptake to inside-out vesicles from human erythrocytes. Biochem. Biophys. Acta, 2000, 1463, 121-30.
27. 3H]-cGMP to inside-out vesicles from human erythrocytes. Mol. Membr. Biol., 1999, 16, 181-88.
28. Pedersen, P.L. Multidrug resistance - a fascinating, clinically relevant problem in bioenergetics. J. Bioenerg. Biomembr., 1995, 27, 3-5.
29. Boadu, E.; Sager, G. ATPase activity and transport by a cGMP transporter in human erythrocyte ghosts and proteoliposome reconstituted membrane extracts. Biochim. Biophys. Acta, 2000, 1509, 467-74.
30. 3H]3′,5′-cGMP without stimulation of ATPase activity in human erythrocyte inside-out vesicles. Biochem. Pharmacol., 2001, 62, 425-29.
31. Sundkvist, E.; Jaeger, R.; Sager, G. Pharmacological characterization of the ATP-dependent low K(m) guanosine 3′,5′-cyclic monophosphate (cGMP) transporter in human erythrocytes. Biochem. Pharmacol., 2002, 63, 945-49.
32. Steiner, A.L.; Pagliara, A.S.; Chase, L.R.; Kipnis, D.M. Radioimmunoassay for cyclic nucleotides. II. Adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate in mammalian tissues and body fluids. J. Biol. Chem., 1972, 247, 1114-20.
33. Ardaillou, N.; Placier, S.; Ronco, P.; Ardaillou, R. Release of cyclic nucleotides from the apical and basolateral poles of cultured human glomerular epithelial cells. Exp. Nephrol., 1993, 1, 253-60.
34. Millul, V.; Prie, D.; GeniteauLegendre, M.; Verpont, M.C.; Baudouin, B.; Ronco, P.M. ANP-stimulated cGMP egression in renal principal cells: Abrogation of polarity by SV40 large T. Am. J. Physiol., 1996, 39, C1051-C1060.
35. Kool, M.; de Haas, M.; Scheffer, G.L.; Scheper, R.J.; van Eijk, M.J.; Juijn, J.A.; Baas, F.; Borst, P. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res., 1997, 57, 3537-47.
36. Lee, K.; Belinsky, M.G.; Bell, D.W.; Testa, J.R.; Kruh, G.D. Isolation of MOAT-B, a widely expressed multidrug resistance-associated protein/ canalicular multispecific organic anion transporter-related transporter. Cancer Res., 1998, 58, 2741-47.
37. McAleer, M.A.; Breen, M.A.; White, N.L.; Matthews, N. pABC11 (also known as MOAT-C and MRP5), a member of the ABC family of proteins, has anion transporter activity but does not confer multidrug resistance when overexpressed in human embryonic kidney 293 cells. J. Biol. Chem., 1999, 274, 23541-48.
38. Belinsky, M.G.; Bain, L.J.; Balsara, B.B.; Testa, J.R.; Kruh, G.D. Characterization of MOAT-C and MOAT-D, new members of the MRP/cMOAT subfamily of transporter proteins. J. Natl. Cancer Inst., 1998, 90, 1735-41.
39. Bera, T.K.; Lee, S.; Salvatore, G.; Lee, B.; Pastan, I. MRP8, a new member of ABC transporter superfamily, identified by EST database mining and gene prediction program, is highly expressed in breast cancer. Mol. Med., 2001, 7, 509-16.
40. Tammur, J.; Prades, C.; Arnould, I.; Rzhetsky, A.; Hutchinson, A.; Adachi, M.; Schuetz, J.D.; Swoboda, K.J.; Ptacek, L.J.; Rosier, M.; Dean, M.; Allikmets, R. Two new genes from the human ATP-binding cassette transporter superfamily, ABCC11 and ABCC12, tandemly duplicated on chromosome 16q12. Gene, 2001, 273, 89-96.
41. Yabuuchi, H.; Shimizu, H.; Takayanagi, S.; Ishikawa, T. Multiple splicing variants of two new human ATP-binding cassette transporters, ABCC11 and ABCC12. Biochem. Biophys. Res. Commun., 2001, 288, 933-39.
42. Klokouzas, A.; Wu, C.P.; van Veen, H.W.; Barrand, M.A.; Hladky, S.B. cGMP and glutathione-conjugate transport in human erythrocytes. Eur. J. Biochem., 2003, 270, 3696-708.
43. Wu, C.P.; Woodcock, H.; Hladky, S.B.; Barrand, M.A. cGMP (guanosine 3′,5′-cyclic monophosphate) transport across human erythrocyte membranes. Biochem. Pharmacol., 2005, 69, 1257-62.
44. Jedlitschky, G.; Burchell, B.; Keppler, D. The multidrug resistance protein 5 functions as an ATP-dependent export pump for cyclic nucleotides. J. Biol. Chem., 2000, 275, 30069-74.
45. Boadu, E.; Sager, G. Reconstitution of ATP-dependent cGMP transport into proteoliposomes by membrane proteins from human erythrocytes. Scand. J. Clin. Lab. Invest., 2004, 64, 41-48.
46. Xu, H.L.; Gavrilyuk, V.; Wolde, H.M.; Baughman, V.L.; Pelligrino, D.A. Regulation of rat pial arteriolar smooth muscle relaxation in vivo through multidrug resistance protein 5-mediated cGMP efflux. Am. J. Physiol. Heart Circ. Physiol., 2004, 286, H2020-H2027.
47. Andric, S.A.; Kostic, T.S.; Stojilkovic, S.S. Contribution of multidrug resistance protein MRP5 in control of cGMP intracellular signaling in anterior pituitary cells. Endocrinology, 2006, 147, 3435-45.
48. Wielinga, P.R.; van, d.H.I; Reid, G.; Beijnen, J.H.; Wijnholds, J.; Borst, P. Characterization of the MRP4-and MRP5-mediated transport of cyclic nucleotides from intact cells. J. Biol. Chem., 2003, 278, 17664-71.
49. van Aubel, R.A.; Smeets, P.H.; Van Den Heuvel, J.J.; Russel, F.G. Human organic anion transporter MRP4 (ABCC4) is an efflux pump for the purine end metabolite urate with multiple allosteric substrate binding sites. Am. J. Physiol., 2005, 288, F327-F333.
50. Chen, Z.S.; Lee, K.; Walther, S.; Raftogianis, R.B.; Kuwano, M.; Zeng, H.; Kruh, G.D. Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res., 2002, 62, 3144-50.
51. Sauna, Z.E.; Nandigama, K.; Ambudkar, S.V. Multidrug resistance protein 4 (ABCC4)-mediated ATP hydrolysis: effect of transport substrates and characterization of the post-hydrolysis transition state. J. Biol. Chem., 2004, 279, 49855-64.
52. Reid, G.; Wielinga, P.; Zelcer, N.; de Haas, M.; van Deemter, L.; Wijnholds, J.; Balzarini, J.; Borst, P. Characterization of the Transport of Nucleoside Analog Drugs by the Human Multidrug Resistance Proteins MRP4 and MRP5. Mol. Pharmacol., 2003, 63, 1094-103.
53. Chen, Z.S.; Lee, K.; Kruh, G.D. Transport of cyclic nucleotides and estradiol 17-beta -d-glucuronide by multidrug resistance protein 4. resistance to 6-mercaptopurine and 6-thioguanine. J. Biol. Chem., 2001, 276, 33747-54.
54. de Wolf, C.J.; Yamaguchi, H.; van der Heijden, I; Wielinga, P.R.; Hundscheid, S.L.; Ono, N.; Scheffer, G.L.; de, H.M.; Schuetz, J.D.; Wijnholds, J.; Borst, P. cGMP transport by vesicles from human and mouse erythrocytes. FEBS J., 2007, 274, 439-50.
55. Sassi, Y.; Lipskaia, L.; Vandecasteele, G.; Nikolaev, V.O.; Hatem, S.N.; Cohen, A.F.; Russel, F.G.; Mougenot, N.; Vrignaud, C.; Lechat, P.; Lompre, A.M.; Hulot, J.S. Multidrug resistance-associated protein 4 regulates cAMP-dependent signaling pathways and controls human and rat SMC proliferation. J. Clin. Invest., 2008, 118, 2747-57.
56. Guo, Y.; Kotova, E.; Chen, Z.S.; Lee, K.; Hopper-Borge, E.; Belinsky, M.G.; Kruh, G.D. MRP8 (ABCC11) is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines, 2′3′-dideoxycytidine and 9′-(2′-phosphonylmethoxyethyl)-adenine J. Biol. Chem., 2003, 278, 29509-14.
57. Chen, Z.S.; Guo, Y.; Belinsky, M.G.; Kotova, E.; Kruh, G.D. Transport of bile acids, sulfated steroids, estradiol 17-beta-D-glucuronide, and leukotriene C4 by human multidrug resistance protein 8 (ABCC11). Mol. Pharmacol., 2005, 67, 545-57.
58. Lai, L.; Tan, T.M. Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of cAMP and resistance to purine analogues. Biochem. J., 2002, 361, 497-503.
59. Reichel, V.; Masereeuw, R.; Van Den Heuvel, J.J.; Miller, D.S.; Fricker, G. Transport of a fluorescent cAMP analog in teleost proximal tubules. Am. J. Physiol. Regul., 2007, 293, R2382-R2389.
60. Reid, G.; Wielinga, P.; Zelcer, N.; van, d.H., I; Kuil, A.; de Haas, M.; Wijnholds, J.; Borst, P. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc. Natl. Acad. Sci. USA, 2003, 100, 9244-49.
61. Brunton, L.L.; Buss, J.E. Export of cyclic AMP by mammalian reticulocytes. J. Cycl. Nucleotide Res., 1980, 6, 369-77.
62. 1. Methods Enzymol., 1988, 159, 83-93.
63. Rindler, M.J.; Bashor, M.M.; Spitzer, N.; Saier jr, M.H. Regulation of adenosine 3′:5′-monophosphate efflux from animal cells. J. Biol. Chem., 1978, 253, 5431-36.
64. Francis, S.H.; Blount, M.A.; Zoraghi, R.; Corbin, J.D. Molecular properties of mammalian proteins that interact with cGMP: protein kinases, cation channels, phosphodiesterases, and multi-drug anion transporters. Front. Biosci., 2005, 10, 2097-117.
65. Clayton, G.M.; Silverman, W.R.; Heginbotham, L.; Morais-Cabral, J.H. Structural basis of ligand activation in a cyclic nucleotide regulated potassium channel. Cell, 2004, 119, 615-27.
66. Zagotta, W.N.; Olivier, N.B.; Black, K.D.; Young, E.C.; Olson, R.; Gouaux, E. Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature, 2003, 425, 200-05.