Inactivation of multidrug resistance proteins disrupts both cellular extrusion and intracellular degradation of cAMP

Molecular Pharmacology

Volumn 80, Issue 2, 2011, Pages 281-293

  Xie, Moses ^a   Rich, Thomas C ^b   Scheitrum, Colleen ^a   Conti, Marco ^a   Richter, Wito ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; MULTIDRUG RESISTANCE PROTEIN; PHOSPHODIESTERASE; PROBENECID; VERLUKAST;

ANIMAL CELL; ARTICLE; CELL COMPOSITION; CELL LEVEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; EMBRYO; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; INTRACELLULAR MEMBRANE; INTRACELLULAR SIGNALING; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; EXTRACELLULAR FLUID; HEK293 CELLS; HUMANS; INTRACELLULAR FLUID; MICE; MICE, KNOCKOUT; P-GLYCOPROTEINS;

EID: 79960282793     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.111.071134     Document Type: Article

References (42)

1. Andric SA, Kostic TS, and Stojilkovic SS (2006) Contribution of multidrug resistance protein MRP5 in control of cyclic guanosine 5′-monophosphate intracellular signaling in anterior pituitary cells. Endocrinology 147:3435-3445. (Pubitemid 43901134)
2. Bankir L, Ahloulay M, Devreotes PN, and Parent CA (2002) Extracellular cAMP inhibits proximal reabsorption: are plasma membrane cAMP receptors involved? Am J Physiol Renal Physiol 282:F376-F392. (Pubitemid 34654526)
3. Barnes AP, Livera G, Huang P, Sun C, O'Neal WK, Conti M, Stutts MJ, and Milgram SL (2005) Phosphodiesterase 4D forms a cAMP diffusion barrier at the apical membrane of the airway epithelium. J Biol Chem 280:7997-8003. (Pubitemid 40349697)
4. Biondi C, Ferretti ME, Lunghi L, Medici S, Cervellati F, Pavan B, Vesce F, Morano D, Adinolfi E, Bertoni F, et al. (2010) cAMP efflux from human trophoblast cell lines: a role for multidrug resistance protein (MRP)1 transporter. Mol Hum Reprod 16:481-491.
5. Blackman BE, Horner K, Heidmann J, Wang D, Richter W, Rich TC, and Conti M (2011) PDE4D and PDE4B function in distinct subcellular compartments in mouse embryonic fibroblasts. J Biol Chem 286:12590-12601.
6. Brunton LL and Mayer SE (1979) Extrusion of cyclic AMP from pigeon erythrocytes. J Biol Chem 254:9714-9720. (Pubitemid 10248736)
7. Conti M and Beavo J (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76:481-511.
8. Cui L, Aleksandrov L, Chang XB, Hou YX, He L, Hegedus T, Gentzsch M, Aleksandrov A, Balch WE, and Riordan JR (2007) Domain interdependence in the biosynthetic assembly of CFTR. J Mol Biol 365:981-994. (Pubitemid 46014191)
9. Davoren PR and Sutherland EW (1963) 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 238:3009-3015.
10. de Wolf CJ, Yamaguchi H, van der Heijden I, Wielinga PR, Hundscheid SL, Ono N, Scheffer GL, de Haas M, Schuetz JD, Wijnholds J, et al. (2007) cGMP transport by vesicles from human and mouse erythrocytes. FEBS J 274:439-450. (Pubitemid 46046653)
11. Doore BJ, Bashor MM, Spitzer N, Mawe RC, and Saier MH Jr (1975) Regulation of adenosine 3′:5′-monophosphate efflux from rat glioma cells in culture*. J Biol Chem 250:4371-4372.
12. Hamet P, Pang SC, and Tremblay J (1989) Atrial natriuretic factor-induced egression of cyclic guanosine 3′:5′-monophosphate in cultured vascular smooth muscle and endothelial cells. J Biol Chem 264:12364-12369. (Pubitemid 19191126)
13. Hofer AM and Lefkimmiatis K (2007) Extracellular calcium and cAMP: second messengers as "third messengers"? Physiology 22:320-327.
14. Huang P, Lazarowski ER, Tarran R, Milgram SL, Boucher RC, and Stutts MJ (2001) Compartmentalized autocrine signaling to cystic fibrosis transmembrane conductance regulator at the apical membrane of airway epithelial cells. Proc Natl Acad Sci USA 98:14120-14125. (Pubitemid 33116034)
15. Jackson EK and Raghvendra DK (2004) The extracellular cyclic AMP-adenosine pathway in renal physiology. Annu Rev Physiol 66:571-599. (Pubitemid 40614455)
16. Jaiswal BS and Conti M (2001) Identification and functional analysis of splice variants of the germ cell soluble adenylyl cyclase. J Biol Chem 276:31698-31708.
17. Jedlitschky G, Burchell B, and Keppler D (2000) The multidrug resistance protein 5 functions as an ATP-dependent export pump for cyclic nucleotides. J Biol Chem 275:30069-30074.
18. Kessin RH (2001) Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity. Cambridge University Press.
19. Knecht M, Ranta T, and Catt KJ(1983) Hormonal regulation of a plasma membrane phosphodiesterase in differentiating granulosa cells. Reciprocal actions of follicle-stimulating hormone and a gonadotropin-releasing hormone agonist on cAMP degradation. J Biol Chem 258:12420-12426. (Pubitemid 14231164)
20. Lee JH, Richter W, Namkung W, Kim KH, Kim E, Conti M, and Lee MG(2007) Dynamic regulation of cystic fibrosis transmembrane conductance regulator by competitive interactions of molecular adaptors. J Biol Chem 282:10414-10422. (Pubitemid 47093434)
21. Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, Zaccolo M, Jalink K, Li M, Nelson DJ, Schuetz JD, et al. (2007) Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131:940-951. (Pubitemid 350138082)
22. Li C and Naren AP (2005) Macromolecular complexes of cystic fibrosis transmembrane conductance regulator and its interacting partners. Pharmacol Ther 108:208-223. (Pubitemid 41527085)
23. Lin ZP, Zhu YL, Johnson DR, Rice KP, Nottoli T, Hains BC, McGrath J, Waxman SG, and Sartorelli AC (2008) Disruption of cAMP and prostaglandin E2 transport by multidrug resistance protein 4 deficiency alters cAMP-mediated signaling and nociceptive response. Mol Pharmacol 73:243-251. (Pubitemid 350294215)
24. Ma T, Thiagarajah JR, Yang H, Sonawane ND, Folli C, Galietta LJ, and Verkman AS(2002) Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest 110:1651-1658. (Pubitemid 35424243)
25. Penit J, Jard S, and Benda P (1974) Probenecide sensitive 3′-5′-cyclic AMP secretion by isoproterenol stimulated glial cells in culture. FEBS Lett 41:156-160.
26. Penmatsa H, Zhang W, Yarlagadda S, Li C, Conoley VG, Yue J, Bahouth SW, Buddington RK, Zhang G, Nelson DJ, et al. (2010) Compartmentalized cyclic adenosine 3′,5′-monophosphate at the plasma membrane clusters PDE3A and cystic fibrosis transmembrane conductance regulator into microdomains. Mol Biol Cell 21:1097-1110.
27. Poschet JF, Timmins GS, Taylor-Cousar JL, Ornatowski W, Fazio J, Perkett E, Wilson KR, Yu HD, de Jonge HR, and Deretic V (2007) Pharmacological modulation of cGMP levels by phosphodiesterase 5 inhibitors as a therapeutic strategy for treatment of respiratory pathology in cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 293:L712-L719. (Pubitemid 47358834)
28. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, Balzarini J, and Borst P (2003a) Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63:1094-1103. (Pubitemid 36529928)
29. Reid G, Wielinga P, Zelcer N, van der Heijden I, Kuil A, de Haas M, Wijnholds J, and Borst P(2003b) The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc Natl Acad Sci USA 100:9244-9249. (Pubitemid 37033914)
30. Rich TC, Fagan KA, Tse TE, Schaack J, Cooper DM, and Karpen JW (2001) A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc Natl Acad Sci USA 98:13049-13054. (Pubitemid 33051315)
31. Richter W and Conti M(2002) Dimerization of the type 4 cAMP-specific phosphodiesterases is mediated by the upstream conserved regions (UCRs). J Biol Chem 277:40212-40221. (Pubitemid 35215591)
32. Richter W, Day P, Agrawal R, Bruss MD, Granier S, Wang YL, Rasmussen SG, Horner K, Wang P, Lei T, et al. (2008) Signaling from beta1- and beta2-adrenergic receptors is defined by differential interactions with PDE4. EMBO J 27:384-393. (Pubitemid 351161657)
33. Russel FG, Koenderink JB, and Masereeuw R (2008) Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 29:200-207.
34. Sager G (2004) Cyclic GMP transporters. Neurochem Int 45:865-873.
35. Sampath J, Adachi M, Hatse S, Naesens L, Balzarini J, Flatley RM, Matherly LH, and Schuetz JD (2002) Role of MRP4 and MRP5 in biology and chemotherapy. AAPS PharmSci 4:E14.
36. Sassi Y, Lipskaia L, Vandecasteele G, Nikolaev VO, Hatem SN, Cohen Aubart F, Russel FG, Mougenot N, Vrignaud C, Lechat P, et al. (2008) Multidrug resistance-associated protein 4 regulates cAMP-dependent signaling pathways and controls human and rat SMC proliferation. J Clin Invest 118:2747-2757.
37. Smolenski A, Bachmann C, Reinhard K, Hönig-Liedl P, Jarchau T, Hoschuetzky H, and Walter U (1998) Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J Biol Chem 273:20029-20035. (Pubitemid 28377554)
38. Terrin A, Di Benedetto G, Pertegato V, Cheung YF, Baillie G, Lynch MJ, Elvassore N, Prinz A, Herberg FW, Houslay MD, et al. (2006) PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J Cell Biol 175:441-451. (Pubitemid 44708068)
39. Thiagarajah JR, Song Y, Derichs N, and Verkman AS (2010) Airway surface liquid depth imaged by surface laser reflectance microscopy. J Gen Physiol 136:353-362.
40. van Aubel RA, Smeets PH, Peters JG, Bindels RJ, and Russel FG (2002) The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J Am Soc Nephrol 13:595-603. (Pubitemid 34183923)
41. Wachten S, Masada N, Ayling LJ, Ciruela A, Nikolaev VO, Lohse MJ, and Cooper DM (2010) Distinct pools of cAMP centre on different isoforms of adenylyl cyclase in pituitary-derived GH3B6 cells. J Cell Sci 123:95-106.
42. Wielinga PR, van der Heijden I, Reid G, Beijnen JH, Wijnholds J, and Borst P (2003) Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J Biol Chem 278:17664-17671. (Pubitemid 36799368)