ATP-binding cassette (ABC) transporters in normal and pathological lung

Respiratory Research

Volumn 6, Issue , 2005, Pages

  van der Deen, Margaretha ^a   de Vries, Elisabeth G E ^a   Timens, Wim ^c   Scheper, Rik J ^d   Timmer Bosscha, Hetty ^a   Postma, Dirkje S ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b Department of Pulmonary Medicine ^*  (Netherlands)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A1; ABC TRANSPORTER A3; BREAST CANCER RESISTANCE PROTEIN; GENE PRODUCT; GLYCOPROTEIN P; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG;

ASTHMA; BRONCHUS MUCOSA; CELL MEMBRANE TRANSPORT; CELL TYPE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CYSTIC FIBROSIS; GENE MUTATION; GENETIC POLYMORPHISM; HUMAN; KNOCKOUT MOUSE; LUNG ALVEOLUS SURFACE TENSION; LUNG DISEASE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; TANGIER DISEASE; ANIMAL; LUNG; METABOLISM;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; HUMANS; LUNG; LUNG DISEASES;

EID: 26244431743     PISSN: 1465993X     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-6-59     Document Type: Review

References (155)

1. Crapo JD, Barry BE, Gehr P, Bachofen M, Weibel ER: Cell number and cell characteristics of the normal human lung. Am Rev Respir Dis 1982, 125:740-745.
2. Dean M, Hamon Y, Chimini G: The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 2001, 42:1007-1017.
3. Muller M: Human ABC-transporters. [http://nutrigene.4t.com/humanabc.htm].
4. Scheffer GL, Pijnenborg AC, Smit EF, Muller M, Postma DS, Timens W, van der Valk P, de Vries EG, Scheper RJ: Multidrug resistance related molecules in human and murine lung. J Clin Pathol 2002, 55:332-339.
5. Hamilton KO, Yazdanian MA, Audus KL: Contribution of efflux pump activity to the delivery of pulmonary therapeutics. Curr Drug Metab 2002, 3:1-12.
6. Langmann T, Mauerer R, Zahn A, Moehle C, Probst M, Stremmel W, Schmitz G: Real-time reverse transcription-PCR expression profiling of the complete human ATP-binding cassette transporter superfamily in various tissues. Clin Chem 2003, 49:230-238.
7. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, Chou JL: Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245:1066-1073.
8. Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, Yu L, Brewer C, Collins JA, Molhuizen HO, Loubser O, Ouelette BF, Fichter K, Ashbourne-Excoffon KJ, Sensen CW, Scherer S, Mott S, Denis M, Martindale D, Frohlich J, Morgan K, Koop B, Pimstone S, Kastelein JJ, Hayden MR: Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 1999, 22:336-345.
9. Shulenin S, Nogee LM, Annilo T, Wert SE, Whitsett JA, Dean M: ABCA3 gene mutations in newborns with fatal surfactant deficiency. N Engl J Med 2004, 350:1296-1303.
10. Van der Deen M, Marks H, Muller M, Pijnenborg AC, Postma DS, Scheffer G, Scheper RJ, Smit EF, Timens W, de Vries EG: Diminished expression of Multidrug Resistance-associated Protein 1 (MRP1) in bronchial epithelium of COPD patients [abstract]. Am J Respir Crit Care Med 2003, 167:A397.
11. Gottesman MM, Fojo T, Bates SE: Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002, 2:48-58.
12. Lechapt-Zalcman E, Hurbain I, Lacave R, Commo F, Urban T, Antoine M, Milleron B, Bernaudin JF: MDR1-Pgp 170 expression in human bronchus. Eur Respir J 1997, 10:1837-1843.
13. Wioland MA, Fleury-Feith J, Corlieu P, Commo F, Monceaux G, Lacau-St-Guily J, Bernaudin JF: CFTR, MDR1, and MRP1 immunolocalization in normal human nasal respiratory mucosa. J Histochem Cytochem 2000, 48:1215-1222.
14. Campbell L, Abulrob AN, Kandalaft LE, Plummer S, Hollins AJ, Gibbs A, Gumbleton M: Constitutive expression of p-glycoprotein in normal lung alveolar epithelium and functionality in primary alveolar epithelial cultures. J Pharmacol Exp Ther 2003, 304:441-452.
15. Cordon-Cardo C, O'Brien JP, Boccia J, Casals D, Bertino JR, Melamed MR: Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues. J Histochem Cytochem 1990, 38:1277-1287.
16. Van der Valk P, van Kalken CK, Ketelaars H, Broxterman HJ, Scheffer G, Kuiper CM, Tsuruo T, Lankelma J, Meijer CJ, Pinedo HM: Distribution of multi-drug resistance-associated P-glycoprotein in normal and neoplastic human tissues. Analysis with 3 monoclonal antibodies recognizing different epitopes of the Pglycoprotein molecule. Ann Oncol 1990, 1:56-64.
17. Puddu P, Fais S, Luciani F, Gherardi G, Dupuis ML, Romagnoli G, Ramoni C, Cianfriglia M, Gessani S: Interferon-gamma up-regulates expression and activity of P-glycoprotein in human peripheral blood monocyte-derived macrophages. Lab Invest 1999, 79:1299-1309.
18. Valverde MA, Diaz M, Sepulveda FV, Gill DR, Hyde SC, Higgins CF: Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein. Nature 1992, 355:830-833.
19. Gill DR, Hyde SC, Higgins CF, Valverde MA, Mintenig GM, Sepulveda FV: Separation of drug transport and chloride channel functions of the human multidrug resistance P-glycoprotein. Cell 1992, 71:23-32.
20. Higgins CF: P-glycoprotein and cell volume-activated chloride channels. J Bioenerg Biomembr 1995, 27:63-70.
21. Kunzelmann K, Slotki IN, Klein P, Koslowsky T, Ausiello DA, Greger R, Cabantchik ZI: Effects of P-glycoprotein expression on cyclic AMP and volume-activated ion fluxes and conductances in HT-29 colon adenocarcinoma cells. J Cell Physiol 1994, 161:393-406.
22. De Greef C, Sehrer J, Viana F, van Acker K, Eggermont J, Mertens L, Raeymaekers L, Droogmans G, Nilius B: Volume-activated chloride currents are not correlated with P-glycoprotein expression. Biochem J 1995, 307:713-718.
23. Waters CM, Krejcie TC, Avram MJ: Facilitated uptake of fentanyl, but not alfentanil, by human pulmonary endothelial cells. Anesthesiology 2000, 93:825-831.
24. Wood L, Palmer M, Hewitt J, Urtasun R, Bruera E, Rapp E, Thaell JF: Results of a phase III, double-blind, placebo-controlled trial of megestrol acetate modulation of P-glycoprotein-mediated drug resistance in the first-line management of small-cell lung carcinoma. Br J Cancer 1998, 77:627-631.
25. Beer TW, Rowlands DC, Crocker J: Detection of the multidrug resistance marker P-glycoprotein by immunohistochemistry in malignant lung tumours. Thorax 1996, 51:526-529.
26. Volm M, Mattern J, Samsel B: Relationship of inherent resistance to doxorubicin, proliferative activity and expression of Pglycoprotein 170, and glutathione S-transferase-pi in human lung tumors. Cancer 1992, 70:764-769.
27. Volm M, Mattern J, Samsel B: Overexpression of P-glycoprotein and glutathione S-transferase-pi in resistant non-small cell lung carcinomas of smokers. Br J Cancer 1991, 64:700-704.
28. Hoffmeyer S, Burk O, von Richter O, Arnold HP, Brockmoller J, Johne A, Cascorbi I, Gerloff T, Roots I, Eichelbaum M, Brinkmann U: Functional polymorphisms of the human multidrug-resistance gene: multiple sequence variations and correlation of one allele with P-glycoprotein expression and activity in vivo. Proc Natl Acad Sci U S A 2000, 97:3473-3478.
29. Eichelbaum M, Fromm MF, Schwab M: Clinical aspects of the MDR1 (ABCB1) gene polymorphism. Ther Drug Monit 2004, 26:180-185.
30. Johannesson M, Nordqvist AC, Bogdanovic N, Hjelte L, Schalling M: Polymorphic expression of multidrug resistance mRNA in lung parenchyma of nonpregnant and pregnant rats: a comparison to cystic fibrosis mRNA expression. Biochem Biophys Res Commun 1997, 239:606-611.
31. Sinues B, Fanlo A, Bernal ML, Mayayo E, Bello S, Rubio E, Isla D: MDR-1 C3435T genetic polymorphism and tobacco-related lung cancer. Oncology 2003, 64:183-185.
32. Isla D, Sarries C, Rosell R, Alonso G, Domine M, Taron M, Lopez-Vivanco G, Camps C, Botia M, Nunez L, Sanchez-Ronco M, Sanchez JJ, Lopez-Brea M, Barneto I, Paredes A, Medina B, Artal A, Lianes P: Single nucleotide polymorphisms and outcome in docetaxel-cisplatin-treated advanced non-small-cell lung cancer. Ann Oncol 2004, 15:1194-1203.
33. Zheng H, Zeevi A, Schuetz E, Lamba J, McCurry K, Griffith BP, Webber S, Ristich J, Dauber J, Iacono A, Grgurich W, Zaldonis D, McDade K, Zhang J, Burckart GJ: Tacrolimus dosing in adult lung transplant patients is related to cytochrome P4503A5 gene polymorphism. J Clin Pharmacol 2004, 44:135-140.
34. Brady JM, Cherrington NJ, Hartley DP, Buist SC, Li N, Klaassen CD: Tissue distribution and chemical induction of multiple drug resistance genes in rats. Drug Metab Dispos 2002, 30:838-844.
35. Seree E, Villard PH, Hever A, Guigal N, Puyoou F, Charvet B, Point-Scomma H, Lechevalier E, Lacarelle B, Barra Y: Modulation of MDR1 and CYP3A expression by dexamethasone: evidence for an inverse regulation in adrenals. Biochem Biophys Res Commun 1998, 252:392-395.
36. Hendrikse NH, de Vries EG, Eriks-Fluks L, van der Graaf WT, Hospers GA, Willemsen AT, Vaalburg W, Franssen EJ: A new in vivo method to study P-glycoprotein transport in tumors and the blood-brain barrier. Cancer Res 1999, 59:2411-2416.
37. Roerig DL, Audi SH, Ahlf SB: Kinetic characterization of p-glycoprotein-mediated efflux of rhodamine 6g in the intact rabbit lung. Drug Metab Dispos 2004, 32:953-958.
38. Booth CL, Brouwer KR, Brouwer KL: Effect of multidrug resistance modulators on the hepatobiliary disposition of doxorubicin in the isolated perfused rat liver. Cancer Res 1998, 58:3641-3648.
39. Schinkel AH, Mayer U, Wagenaar E, Mol CA, van Deemter L, Smit JJ, van der Valk MA, Voordouw AC, Spits H, van Tellingen O, Zijlmans JM, Fibbe WE, Borst P: Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) Pglycoproteins. Proc Natl Acad Sci U S A 1997, 94:4028-4033.
40. Grauer MT, Uhr M: P-glycoprotein reduces the ability of amitriptyline metabolites to cross the blood brain barrier in mice after a 10-day administration of amitriptyline. J Psychopharmacol 2004, 18:66-74.
41. Forbes II: Human airway epithelial cell lines for in vitro drug transport and metabolism studies. Pharm Sci Technol Today 2000, 3:18-27.
42. Ehrhardt C, Kneuer C, Laue M, Schaefer UF, Kim KJ, Lehr CM: 16HBE14o- human bronchial epithelial cell layers express P-glycoprotein, lung resistance-related protein, and caveolin-1. Pharm Res 2003, 20:545-551.
43. Hamilton KO, Yazdanian MA, Audus KL: Modulation of P-glycoprotein activity in Calu-3 cells using steroids and beta-ligands. Int J Pharm 2001, 228:171-179.
44. Hamilton KO, Topp E, Makagiansar I, Siahaan T, Yazdanian M, Audus KL: Multidrug resistance-associated protein-1 functional activity in Calu-3 cells. J Pharmacol Exp Ther 2001, 298:1199-1205.
45. Lehmann T, Kohler C, Weidauer E, Taege C, Foth H: Expression of MRP1 and related transporters in human lung cells in culture. Toxicology 2001, 167:59-72.
46. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, Deeley RG: Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258:1650-1654.
47. Muller M, Meijer C, Zaman GJ, Borst P, Scheper RJ, Mulder NH, de Vries EG, Jansen PL: Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci U S A 1994, 91:13033-13037.
48. Hipfner DR, Deeley RG, Cole SP: Structural, mechanistic and clinical aspects of MRP1. Biochim Biophys Acta 1999, 1461:359-376.
49. Loe DW, Deeley RG, Cole SP: Characterization of vincristine transport by the M(r) 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 1998, 58:5130-5136.
50. Renes J, de Vries EG, Nienhuis EF, Jansen PL, Muller M: ATP- and glutathione-dependent transport of chemotherapeutic drugs by the multidrug resistance protein MRP1. Br J Pharmacol 1999, 126:681-688.
51. Hooijberg JH, Broxterman HJ, Kool M, Assaraf YG, Peters GJ, Noordhuis P, Scheper RJ, Borst P, Pinedo HM, Jansen G: Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res 1999, 59:2532-2535.
52. Leier I, Jedlitschky G, Buchholz U, Keppler D: Characterization of the ATP-dependent leukotriene C4 export carrier in mastocytoma cells. Eur J Biochem 1994, 220:599-606.
53. Brechot JM, Hurbain I, Fajac A, Daty N, Bernaudin JF: Different pattern of MRP localization in ciliated and basal cells from human bronchial epithelium. J Histochem Cytochem 1998, 46:513-517.
54. Flens MJ, Zaman GJ, van der Valk P, Izquierdo MA, Schroeijers AB, Scheffer GL, van der Groep P, de Haas M, Meijer CJ, Scheper RJ: Tissue distribution of the multidrug resistance protein. Am J Pathol 1996, 148:1237-1247.
55. Kool M, de Haas M, Scheffer GL, Scheper RJ, van Eijk MJ, Juijn JA, 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, 57:3537-3547.
56. Wijnholds J, Scheffer GL, van der Valk M, van der Valk P, Beijnen JH, Scheper RJ, Borst P: Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J Exp Med 1998, 188:797-808.
57. Thomas GA, Barrand MA, Stewart S, Rabbitts PH, Williams ED, Twentyman PR: Expression of the multidrug resistance-associated protein (MRP) gene in human lung tumours and normal tissue as determined by in situ hybridisation. Eur J Cancer 1994, 30A:1705-1709.
58. Doubre H, Cesari D, Mairovitz A, Benac C, Chantot-Bastaraud S, Dagnon K, Antoine M, Danel C, Bernaudin JF, Fleury-Feith J: Multidrug resistance-associated protein (MRP1) is overexpressed in DNA aneuploid carcinomatous cells in non-small cell lung cancer (NSCLC). Int J Cancer 2005, 113:568-574.
59. Trompier D, Chang XB, Barattin R, du Moulinet d'Hardemare A, Di Pietro A, Baubichon-Cortay H: Verapamil and its derivative trigger apoptosis through glutathione extrusion by multidrug resistance protein MRP1. Cancer Res 2004, 64:4950-4956.
60. Leslie EM, Ito K, Upadhyaya P, Hecht SS, Deeley RG, Cole SP: Transport of the beta -O-glucuronide conjugate of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1- butanol (NNAL) by the multidrug resistance protein 1 (MRP1). Requirement for glutathione or a non-sulfur-containing analog. J Biol Chem 2001, 276:27846-27854.
61. Kerb R, Hoffmeyer S, Brinkmann U: ABC drug transporters: hereditary polymorphisms and pharmacological impact in MDR1, MRP1 and MRP2. Pharmacogenomics 2001, 2:51-64.
62. Saito S, Iida A, Sekine A, Miura Y, Ogawa C, Kawauchi S, Higuchi S, Nakamura Y: Identification of 779 genetic variations in eight genes encoding members of the ATP-binding cassette, subfamily C (ABCC/MRP/CFTR. J Hum Genet 2002, 47:147-171.
63. Oselin K, Mrozikiewicz PM, Gaikovitch E, Pahkla R, Roots I: Frequency of MRP1 genetic polymorphisms and their functional significance in Caucasians: detection of a novel mutation G816A in the human MRP1 gene. Eur J Clin Pharmacol 2003, 59:347-350.
64. Ito S, Ieiri I, Tanabe M, Suzuki A, Higuchi S, Otsubo K: Polymorphism of the ABC transporter genes, MDR1, MRP1 and MRP2/cMOAT, in healthy Japanese subjects. Pharmacogenetics 2001, 11:175-184.
65. Ito K, Olsen SL, Qiu W, Deeley RG, Cole SP: Mutation of a single conserved tryptophan in multidrug resistance protein 1 (MRP1/ABCC1) results in loss of drug resistance and selective loss of organic anion transport. J Biol Chem 2001, 276:15616-15624.
66. Conrad S, Kauffmann HM, Ito K, Leslie EM, Deeley RG, Schrenk D, Cole SP: A naturally occurring mutation in MRP1 results in a selective decrease in organic anion transport and in increased doxorubicin resistance. Pharmacogenetics 2002, 12:321-330.
67. Lorico A, Rappa G, Finch RA, Yang D, Flavell RA, Sartorelli AC: Disruption of the murine MRP (multidrug resistance protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res 1997, 57:5238-5242.
68. Wijnholds J, Evers R, van Leusden MR, Mol CA, Zaman GJ, Mayer U, Beijnen JH, van der Valk M, Krimpenfort P, Borst P: Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking the multidrug resistance-associated protein. Nat Med 1997, 3:1275-1279.
69. Bain LJ, Feldman RA: Altered expression of sulfotransferases, glucuronosyltransferases and mrp transporters in FVB/mrp1-/- mice. Xenobiotica 2003, 33:1173-1183.
70. Verbon A, Leemans JC, Weijer S, Florquin S, van der PT: Mice lacking the multidrug resistance protein 1 have a transiently impaired immune response during tuberculosis. Clin Exp Immunol 2002, 130:32-36.
71. Schultz MJ, Wijnholds J, Peppelenbosch MP, Vervoordeldonk MJ, Speelman P, van Deventer SJ, Borst P, van der Poll T: Mice lacking the multidrug resistance protein 1 are resistant to Streptococcus pneumoniae-induced pneumonia. J Immunol 2001, 166:4059-4064.
72. Crooks SW, Bayley DL, Hill SL, Stockley RA: Bronchial inflammation in acute bacterial exacerbations of chronic bronchitis: the role of leukotriene B4. Eur Respir J 2000, 15:274-280.
73. Biernacki WA, Kharitonov SA, Barnes PJ: Increased leukotriene B4 and 8-isoprostane in exhaled breath condensate of patients with exacerbations of COPD. Thorax 2003, 58:294-298.
74. Loe DW, Stewart RK, Massey TE, Deeley RG, Cole SP: ATP-dependent transport of aflatoxin B1 and its glutathione conjugates by the product of the multidrug resistance protein (MRP) gene. Mol Pharmacol 1997, 51:1034-1041.
75. Lorico A, Nesland J, Emilsen E, Fodstad O, Rappa G: Role of the multidrug resistance protein 1 gene in the carcinogenicity of aflatoxin B1: investigations using mrp1-null mice. Toxicology 2002, 171:201-205.
76. Hayashi A, Suzuki H, Itoh K, Yamamoto M, Sugiyama Y: Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem Biophys Res Commun 2003, 310:824-829.
77. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S: Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 2004, 114:1248-1259.
78. Yamamoto T, Yoh K, Kobayashi A, Ishii Y, Kure S, Koyama A, Sakamoto T, Sekizawa K, Motohashi H, Yamamoto M: Identification of polymorphisms in the promoter region of the human NRF2 gene. Biochem Biophys Res Commun 2004, 321:72-79.
79. Wijnholds J, deLange EC, Scheffer GL, van den Berg DJ, Mol CA, van der Valk M, Schinkel AH, Scheper RJ, Breimer DD, Borst P: Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J Clin Invest 2000, 105:279-285.
80. Johnson DR, Finch RA, Lin ZP, Zeiss CJ, Sartorelli AC: The pharmacological phenotype of combined multidrug-resistance mdr1a/1b- and mrp1-deficient mice. Cancer Res 2001, 61:1469-1476.
81. Muramatsu T, Johnson DR, Finch RA, Johnson LK, Leffert JJ, Lin ZP, Pizzorno G, Sartorelli AC: Age-related differences in vincristine toxicity and biodistribution in wild-type and transporter-deficient mice. Oncol Res 2004, 14:331-343.
82. Bandi N, Kompella UB: Budesonide reduces multidrug resistance-associated protein 1 expression in an airway epithelial cell line (Calu-1). Eur J Pharmacol 2002, 437:9-17.
83. Van der Deen M, Timmer-Bosscha H, Timens W, Postma DS, de Vries EG: Effect of cigarette smoke extract on MRP1 function in bronchial epithelial cells [abstract]. Proc Amer Assoc Cancer Res 2004, 45:A508.
84. Nagayoshi K, Nemoto T, Yokoyama S, Yamashita F, Hashida M: Effect of polycyclic aromatic hydrocarbons on generation and efflux of glutathione conjugates in primary cultured alveolar epithelial cells. Drug Metab Pharmacokinet 2004, 19:407-412.
85. Torky AR, Stehfest E, Viehweger K, Taege C, Foth H: Immuno-histochemical detection of MRPs in human lung cells in culture. Toxicology 2005, 207:437-450.
86. Buchler M, Konig J, Brom M, Kartenbeck J, Spring H, Horie T, Keppler D: cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J Biol Chem 1996, 271:15091-15098.
87. Cui Y, Konig J, Buchholz JK, Spring H, Leier I, Keppler D: Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol Pharmacol 1999, 55:929-937.
88. Leier I, Jedlitschky G, Buchholz U, Cole SP, Deeley RG, Keppler D: The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem 1994, 269:27807-27810.
89. Kamisako T, Leier I, Cui Y, Konig J, Buchholz U, Hummel-Eisenbeiss J, Keppler D: Transport of monoglucuronosyl and bisglucuronosyl bilirubin by recombinant human and rat multidrug resistance protein 2. Hepatology 1999, 30:485-490.
90. Holland IB, Cole SP, Kuchler K, Higgins CF: ABC proteins, from bacteria to men. London: Elsevier Sci Ltd; 2003:p427.
91. Paulusma CC, Bosma PJ, Zaman GJ, Bakker CT, Otter M, Scheffer GL, Scheper RJ, Borst P, Oude Elferink RP: Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 1996, 271:1126-1128.
92. Hosokawa S, Tagaya O, Mikami T, Nozaki Y, Kawaguchi A, Yamatsu K, Shamoto M: A new rat mutant with chronic conjugated hyperbilirubinemia and renal glomerular lesions. Lab Anim Sci 1992, 42:27-34.
93. Kuroda M, Kobayashi Y, Tanaka Y, Itani T, Mifuji R, Araki J, Kaito M, Adachi Y: Increased hepatic and renal expressions of multidrug resistance-associated protein 3 in Eisai hyperbilirubinuria rats. J Gastroenterol Hepatol 2004, 19:146-153.
94. Kiuchi Y, Suzuki H, Hirohashi T, Tyson CA, Sugiyama Y: cDNA cloning and inducible expression of human multidrug resistance associated protein 3 (MRP3). FEBS Lett 1998, 433:149-152.
95. Kool M, van der Linden M, de Haas M, Scheffer GL, de Vree JM, Smith AJ, Jansen G, Peters GJ, Ponne N, Scheper RJ, Elferink RP, Baas F, Borst P: MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci U S A 1999, 96:6914-6919.
96. Scheffer GL, Kool M, de Haas M, de Vree JM, Pijnenborg AC, Bosman DK, Elferink RP, van der Valk P, Borst P, Scheper RJ: Tissue distribution and induction of human multidrug resistant protein 3. Lab Invest 2002, 82:193-201.
97. Oguri T, Isobe T, Fujitaka K, Ishikawa N, Kohno N: Association between expression of the MRP3 gene and exposure to platinum drugs in lung cancer. Int J Cancer 2001, 93:584-589.
98. Young LC, Campling BG, Voskoglou-Nomikos T, Cole SP, Deeley RG, Gerlach JH: Expression of multidrug resistance protein-related genes in lung cancer: correlation with drug response. Clin Cancer Res 1999, 5:673-680.
99. Borst P, Evers R, Kool M, Wijnholds J: A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 2000, 92:1295-1302.
100. Wielinga PR, van der Heijden I, Reid G, Beijnen JH, Wijnholds J, Borst P: Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J Biol Chem 2003, 278:17664-17671.
101. 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, 275:30069-30074.
102. Chen ZS, Lee K, Kruh GD: 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, 276:33747-33754.
103. Van Aubel RA, Smeets PH, Peters JG, Bindels RJ, Russel FG: 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 2002, 13:595-603.
104. Van den Berge M, Polosa R, Kerstjens HA, Postma DS: The role of endogenous and exogenous AMP in asthma and chronic obstructive pulmonary disease. J Allergy Clin Immunol 2004, 114:737-746.
105. Reid G, Wielinga P, Zelcer N, van der Heijden 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.
106. Zelcer N, Reid G, Wielinga P, Kuil A, van der Heijden I, Schuetz JD, Borst P: Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem J 2003, 371:361-367.
107. Prehm P, Schumacher U: Inhibition of hyaluronan export from human fibroblasts by inhibitors of multidrug resistance transporters. Biochem Pharmacol 2004, 68:1401-1410.
108. Szakacs G, Annereau JP, Lababidi S, Shankavaram U, Arciello A, Bussey KJ, Reinhold W, Guo Y, Kruh GD, Reimers M, Weinstein JN, Gottesman MM: Predicting drug sensitivity and resistance; Profiling ABC transporter genes in cancer cells. Cancer Cell 2004, 6:129-137.
109. Savaraj N, Wu C, Wangpaichitr M, Kuo MT, Lampidis T, Robles C, Furst AJ, Feun L: Overexpression of mutated MRP4 in cisplatin resistant small cell lung cancer cell line: collateral sensitivity to azidothymidine. Int J Oncol 2003, 23:173-179.
110. Suzuki T, Nishio K, Tanabe S: The MRP family and anticancer drug metabolism. Curr Drug Metab 2001, 2:367-377.
111. Scheffer GL, Hu X, Pijnenborg AC, Wijnholds J, Bergen AA, Scheper RJ: MRP6 (ABCC6) detection in normal human tissues and tumors. Lab Invest 2002, 82:515-518.
112. Hu X, Plomp AS, van Soest S, Wijnholds J, de Jong PT, Bergen AA: Pseudoxanthoma elasticum: a clinical, histopathological, and molecular update. Surv Ophthalmol 2003, 48:424-438.
113. Jackson A, Loh CL: Pulmonary calcification and elastic tissue damage in pseudoxanthoma elasticum. Histopathology 1980, 4:607-611.
114. Beck K, Hayashi K, Nishiguchi B, Le Saux O, Hayashi M, Boyd CD: The distribution of Abcc6 in normal mouse tissues suggests multiple functions for this ABC transporter. J Histochem Cytochem 2003, 51:887-902.
115. Hopper-Borge E, Chen ZS, Shchaveleva I, Belinsky MG, Kruh GD: Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res 2004, 64:4927-4930.
116. Chen ZS, Guo Y, Belinsky MG, Kotova E, Kruh GD: Transport of bile acids, sulfated steroids, estradiol 17-beta-D-glucuronide, and leukotriene C4 by human multidrug resistance protein 8 (ABCC11). Mol Pharmacol 2005, 67:545-557.
117. Denning GM, Ostedgaard LS, Welsh MJ: Abnormal localization of cystic fibrosis transmembrane conductance regulator in primary cultures of cystic fibrosis airway epithelia. J Cell Biol 1992, 118:551-559.
118. Engelhardt JF, Zepeda M, Cohn JA, Yankaskas JR, Wilson JM: Expression of the cystic fibrosis gene in adult human lung. J Clin Invest 1994, 93:737-749.
119. Puchelle E, Gaillard D, Ploton D, Hinnrasky J, Fuchey C, Boutterin MC, Jacquot J, Dreyer D, Pavirani A, Dalemans W: Differential localization of the cystic fibrosis transmembrane conductance regulator in normal and cystic fibrosis airway epithelium. Am J Respir Cell Mol Biol 1992, 7:485-491.
120. Kalin N, Claass A, Sommer M, Puchelle E, Tummler B: DeltaF508 CFTR protein expression in tissues from patients with cystic fibrosis. J Clin Invest 1999, 103:1379-1389.
121. Pilewski JM, Frizzell RA: Role of CFTR in airway disease. Physiol Rev 1999, 79:S215-S255.
122. Brezillon S, Dupuit F, Hinnrasky J, Marchand V, Kalin N, Tummler B, Puchelle E: Decreased expression of the CFTR protein in remodeled human nasal epithelium from non-cystic fibrosis patients. Lab Invest 1995, 72:191-200.
123. Brezillon S, Hamm H, Heilmann M, Schafers HJ, Hinnrasky J, Wagner TO, Puchelle E, Tummler B: Decreased expression of the cystic fibrosis transmembrane conductance regulator protein in remodeled airway epithelium from lung transplanted patients. Hum Pathol 1997, 28:944-952.
124. Penque D, Mendes F, Beck S, Farinha C, Pacheco P, Nogueira P, Lavinha J, Malho R, Amaral MD: Cystic fibrosis F508del patients have apically localized CFTR in a reduced number of airway cells. Lab Invest 2000, 80:857-868.
125. Morris AP, Cunningham SA, Benos DJ, Frizzell RA: Cellular differentiation is required for cAMP but not Ca(2+)-dependent Cl-secretion in colonic epithelial cells expressing high levels of cystic fibrosis transmembrane conductance regulator. J Biol Chem 1992, 267:5575-5583.
126. Hollande E, Fanjul M, Chemin-Thomas C, Devaux C, Demolombe S, Van Rietschoten J, Guy-Crotte O, Figarella C: Targeting of CFTR protein is linked to the polarization of human pancreatic duct cells in culture. Eur J Cell Biol 1998, 76:220-227.
127. Hurbain I, Sermet-Gaudelus I, Vallee B, Feuillet MN, Lenoir G, Bernaudin JF, Edelman A, Fajac A: Evaluation of MRP1-5 gene expression in cystic fibrosis patients homozygous for the delta F508 mutation. Pediatr Res 2003, 54:627-634.
128. Linsdell P, Hanrahan JW: Substrates of multidrug resistance-associated proteins block the cystic fibrosis transmembrane conductance regulator chloride channel. Br J Pharmacol 1999, 126:1471-1477.
129. Bebok Z, Varga K, Hicks JK, Venglarik CJ, Kovacs T, Chen L, Hardiman KM, Collawn JF, Sorscher EJ, Matalon S: Reactive oxygen nitrogen species decrease cystic fibrosis transmembrane conductance regulator expression and cAMP-mediated Cl-secretion in airway epithelia. J Biol Chem 2002, 277:43041-43049.
130. Hickman-Davis J, Gibbs-Erwin J, Lindsey JR, Matalon S: Surfactant protein A mediates mycoplasmacidal activity of alveolar macrophages by production of peroxynitrite. Proc Natl Acad Sci U S A 1999, 96:4953-4958.
131. Hickman-Davis JM, O'Reilly P, Davis IC, Peti-Peterdi J, Davis G, Young KR, Devlin RB, Matalon S: Killing of Klebsiella pneumoniae by human alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 2002, 282:L944-L956.
132. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, van der Vliet A: Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 1998, 391:393-397.
133. Punjabi CJ, Laskin JD, Pendino KJ, Goller NL, Durham SK, Laskin DL: Production of nitric oxide by rat type II pneumocytes: increased expression of inducible nitric oxide synthase following inhalation of a pulmonary irritant. Am J Respir Cell Mol Biol 1994, 11:165-172.
134. Weinberger B, Heck DE, Laskin DL, Laskin JD: Nitric oxide in the lung: therapeutic and cellular mechanisms of action. Pharmacol Ther 1999, 84:401-411.
135. Meng QH, Polak JM, Edgar AJ, Chacon MR, Evans TJ, Gruenert DC, Bishop AE: Neutrophils enhance expression of inducible nitric oxide synthase in human normal but not cystic fibrosis bronchial epithelial cells. J Pathol 2000, 190:126-132.
136. Trezise AE, Ratcliff R, Hawkins TE, Evans MJ, Freeman TC, Romano PR, Higgins CF, Colledge WH: Co-ordinate regulation of the cystic fibrosis and multidrug resistance genes in cystic fibrosis knockout mice. Hum Mol Genet 1997, 6:527-537.
137. Ratcliff R, Evans MJ, Cuthbert AW, MacVinish LJ, Foster D, Anderson JR, Colledge WH: Production of a severe cystic fibrosis mutation in mice by gene targeting. Nat Genet 1993, 4:35-41.
138. Shen BQ, Finkbeiner WE, Wine JJ, Mrsny RJ, Widdicombe JH: Calu-3: a human airway epithelial cell line that shows cAMP-dependent Cl- secretion. Am J Physiol 1994, 266:L493-L501.
139. Baudouin-Legros M, Brouillard F, Tondelier D, Hinzpeter A, Edelman A: Effect of ouabain on CFTR gene expression in human Calu-3 cells. Am J Physiol Cell Physiol 2003, 284:C620-C626.
140. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC: CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 1994, 10:38-47.
141. Kogan I, Ramjeesingh M, Li C, Kidd JF, Wang Y, Leslie EM, Cole SP, Bear CE: CFTR directly mediates nucleotide-regulated glutathione flux. EMBO J 2003, 22:1981-1989.
142. Croop JM, Tiller GE, Fletcher JA, Lux ML, Raab E, Goldenson D, Son D, Arciniegas S, Wu RL: Isolation and characterization of a mammalian homolog of the Drosophila white gene. Gene 1997, 185:77-85.
143. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK, Ross DD: A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci U S A 1998, 95:15665-15670.
144. Komatani H, Kotani H, Hara Y, Nakagawa R, Matsumoto M, Arakawa H, Nishimura S: Identification of breast cancer resistant protein/mitoxantrone resistance/placenta-specific, ATP-binding cassette transporter as a transporter of NB-506 and J-10 topoisomerase I inhibitors with an indolocarbazole structure. Cancer Res 7088, 61:2827-2832.
145. Diestra JE, Scheffer GL, Catala II, Maliepaard M, Schellens JH, Scheper RJ, Germa-Lluch JR, Izquierdo MA: Frequent expression of the multi-drug resistance-associated protein BCRP/MXR/ABCP/ABCG2 in human tumours detected by the BXP-21 monoclonal antibody in paraffin-embedded material. J Pathol 2002, 198:213-219.
146. Yoh K, Ishii G, Yokose T, Minegishi Y, Tsuta K, Goto K, Nishiwaki Y, Kodama T, Suga M, Ochiai A: Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin Cancer Res 2004, 10:1691-1697.
147. Jonker JW, Buitelaar M, Wagenaar E, van der Valk MA, Scheffer GL, Scheper RJ, Plosch T, Kuipers F, Elferink RP, Rosing H, Beijnen JH, Schinkel AH: The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci U S A 2002, 99:15649-15654.
148. Summer R, Kotton DN, Sun X, Ma B, Fitzsimmons K, Fine A: Side population cells and Bcrp1 expression in lung. Am J Physiol Lung Cell Mol Physiol 2003, 285:L97-104.
149. Giangreco A, Shen H, Reynolds SD, Stripp BR: Molecular Phenotype of Airway Side Population Cells. Am J Physiol Lung Cell Mol Physiol 2003.
150. Neuringer IP, Randell SH: Stem cells and repair of lung injuries. Respir Res 2004, 5:6.
151. Agassandian M, Mathur SN, Zhou J, Field FJ, Mallampalli RK: Oxysterols trigger ABCA1-mediated basolateral surfactant efflux. Am J Respir Cell Mol Biol 2004, 31:227-233.
152. Drobnik W, Lindenthal B, Lieser B, Ritter M, Christiansen WT, Liebisch G, Giesa U, Igel M, Borsukova H, Buchler C, Fung-Leung WP, Von Bergmann K, Schmitz G: ATP-binding cassette transporter A1 (ABCA1) affects total body sterol metabolism. Gastroenterology 2001, 120:1203-1211.
153. McNeish J, Aiello RJ, Guyot D, Turi T, Gabel C, Aldinger C, Hoppe KL, Roach ML, Royer LJ, de Wet J, Broccardo C, Chimini G, Francone OL: High density lipoprotein deficiency and foam cell accumulation in mice with targeted disruption of ATP-binding cassette transporter-1. Proc Natl Acad Sci U S A 2000, 97:4245-4250.
154. Wang N, Lan D, Gerbod-Giannone M, Linsel-Nitschke P, Jehle AW, Chen W, Martinez LO, Tall AR: ATP-binding cassette transporter A7 (ABCA7) binds apolipoprotein A-I and mediates cellular phospholipid but not cholesterol efflux. J Biol Chem 2003, 278:42906-42912.
155. Yamano G, Funahashi H, Kawanami O, Zhao LX, Ban N, Uchida Y, Morohoshi T, Ogawa J, Shioda S, Inagaki N: ABCA3 is a lamellar body membrane protein in human lung alveolar type II cells. FEBS Lett 2001, 508:221-225.