The Absence of Mrp4 Has No Effect on the Recruitment of Neutrophils and Eosinophils into the Lung after LPS, Cigarette Smoke or Allergen Challenge

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Schymeinsky, Jürgen ^a   Mayer, Hannah ^a   Tomsic, Christopher ^a   Tilp, Cornelia ^a   Schuetz, John D ^b   Cui, Yunhai ^a   Wollin, Lutz ^a   Gantner, Florian ^a   Erb, Klaus J ^a  

^a BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,4,6,7,12,12A OCTAHYDRO 6 ISOBUTYL 9 METHOXY 1,4 DIOXOPYRAZINO[1',2':1,6]PYRIDO[3,4 B]INDOLE 3 PROPANOIC ACID TERT BUTYL ESTER; ABC TRANSPORTER; ALLERGEN; BREAST CANCER RESISTANCE PROTEIN; CYCLIC AMP; DEXAMETHASONE; INTERLEUKIN 4; INTERLEUKIN 5; LIPOPOLYSACCHARIDE; MULTIDRUG RESISTANCE PROTEIN 4; ROFLUMILAST; TUMOR NECROSIS FACTOR ALPHA; VERLUKAST; 3-(6-ISOBUTYL-9-METHOXY-1,4-DIOXO-1,2,3,4,6,7,12,12A-OCTAHYDROPYRAZINO(1',2'-1,6)PYRIDO(3,4-B)INDOL-3-YL)PROPIONIC ACID TERT-BUTYL ESTER; ABCC4 PROTEIN, MOUSE; ABCG2 PROTEIN, MOUSE; ADENOSINE; CYTOKINE; MULTIDRUG RESISTANCE PROTEIN; OVALBUMIN; PHOSPHODIESTERASE IV INHIBITOR; PROPIONIC ACID DERIVATIVE; QUINOLINE DERIVATIVE; ROLIPRAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTHMA; CELL TRANSPORT; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CYTOKINE RELEASE; DOSE RESPONSE; DRUG EFFICACY; ENZYME INHIBITION; EOSINOPHIL; EX VIVO STUDY; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PNEUMONIA; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; PROTEIN FUNCTION; SMOKING; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; DEFICIENCY; DRUG EFFECTS; IMMUNOLOGY; LUNG; LUNG LAVAGE; METABOLISM; NEUTROPHIL; TH2 CELL; TIME;

ANIMALIA; MURINAE; MUS;

ADENOSINE; ALLERGENS; ANIMALS; ASTHMA; ATP-BINDING CASSETTE TRANSPORTERS; BRONCHOALVEOLAR LAVAGE FLUID; CYCLIC AMP; CYTOKINES; EOSINOPHILS; LIPOPOLYSACCHARIDES; LUNG; MICE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEUTROPHILS; OVALBUMIN; PHOSPHODIESTERASE 4 INHIBITORS; PROPIONATES; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; QUINOLINES; ROLIPRAM; SMOKING; TH2 CELLS; TIME FACTORS;

EID: 84876424127     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061193     Document Type: Article

References (46)

1. Rees DC, Johnson E, Lewinson O, (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10: 218-227.
2. Russel FG, Koenderink JB, Masereeuw R, (2008) Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 29: 200-207.
3. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, et al. (2004) Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 24: 7612-7621.
4. van Aubel RA, Smeets PH, Peters JG, Bindels RJ, 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.
5. Chen ZS, Lee K, Kruh GD, (2001) 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 276: 33747-33754.
6. Ci L, Kusuhara H, Adachi M, Schuetz JD, Takeuchi K, et al. (2007) Involvement of MRP4 (ABCC4) in the luminal efflux of ceftizoxime and cefazolin in the kidney. Mol Pharmacol 71: 1591-1597.
7. Beavo JA, Brunton LL, (2002) Cyclic nucleotide research - still expanding after half a century. Nat Rev Mol Cell Biol 3: 710-718.
8. Gloerich M, Bos JL, (2010) Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50: 355-375.
9. Peters-Golden M, (2009) Putting on the brakes: cyclic AMP as a multipronged controller of macrophage function. Sci Signal 2: e37.
10. Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, et al. (2007) Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131: 940-951.
11. Sassi Y, Lipskaia L, Vandecasteele G, Nikolaev VO, Hatem SN, 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.
12. Pierre S, Eschenhagen T, Geisslinger G, Scholich K, (2009) Capturing adenylyl cyclases as potential drug targets. Nat Rev Drug Discov 8: 321-335.
13. Kamenetsky M, Middelhaufe S, Bank EM, Levin LR, Buck J, et al. (2006) Molecular details of cAMP generation in mammalian cells: a tale of two systems. J Mol Biol 362: 623-639.
14. Hatzelmann A, Morcillo EJ, Lungarella G, Adnot S, Sanjar S, et al. (2010) The preclinical pharmacology of roflumilast- A selective, oral phosphodiesterase 4 inhibitor in development for chronic obstructive pulmonary disease. Pulm Pharmacol Ther 23: 235-256.
15. Barnette MS, Christensen SB, Essayan DM, Grous M, Prabhakar U, et al. (1998) SB 207499 (Ariflo), a potent and selective second-generation phosphodiesterase 4 inhibitor: in vitro anti-inflammatory actions. J Pharmacol Exp Ther 284: 420-426.
16. Essayan DM, (1999) Cyclic nucleotide phosphodiesterase (PDE) inhibitors and immunomodulation. Biochem Pharmacol 57: 965-973.
17. Proskocil BJ, Fryer AD, (2005) Beta2-agonist and anticholinergic drugs in the treatment of lung disease. Proc Am Thorac Soc 2: 305-310.
18. Duplantier AJ, Biggers MS, Chambers RJ, Cheng JB, Cooper K, et al. (1996) Biarylcarboxylic acids and-amides: inhibition of phosphodiesterase type IV versus [3H]rolipram binding activity and their relationship to emetic behavior in the ferret. J Med Chem 39: 120-125.
19. Davis TG, Peterson JJ, Kou JP, Capper-Spudich EA, Ball D, et al. (2009) The identification of a novel phosphodiesterase 4 inhibitor, 1-ethyl-5-{5-[(4-methyl-1-piperazinyl)methyl]-1,3,4-oxadiazol-2-yl}-N-(tet rahydro-2H-pyran-4-yl)-1H-pyrazolo[3,4-b]pyridin-4-amine (EPPA-1), with improved therapeutic index using pica feeding in rats as a measure of emetogenicity. J Pharmacol Exp Ther 330: 922-931.
20. Lipworth BJ, (2005) Phosphodiesterase-4 inhibitors for asthma and chronic obstructive pulmonary disease. Lancet 365: 167-175.
21. Pick A, Klinkhammer W, Wiese M, (2010) Specific inhibitors of the breast cancer resistance protein (BCRP). ChemMedChem 5: 1498-1505.
22. Allen JD, van LA, Lakhai JM, van d, V, van TO, et al. (2002) Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol Cancer Ther 1: 417-425.
23. Reid G, Wielinga P, Zelcer N, de HM, Van DL, et al. (2003) Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63: 1094-1103.
24. Borst P, Evers R, Kool M, Wijnholds J, (2000) A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 92: 1295-1302.
25. Bickert T, Trujillo-Vargas CM, Duechs M, Wohlleben G, Polte T, et al. (2009) Probiotic Escherichia coli Nissle 1917 suppresses allergen-induced Th2 responses in the airways. Int Arch Allergy Immunol 149: 219-230.
26. Wollin L, Pieper MP, (2010) Tiotropium bromide exerts anti-inflammatory activity in a cigarette smoke mouse model of COPD. Pulm Pharmacol Ther 23: 345-354.
27. Barnes PJ, (2008) Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 8: 183-192.
28. Beck-Schimmer B, Schwendener R, Pasch T, Reyes L, Booy C, et al. (2005) Alveolar macrophages regulate neutrophil recruitment in endotoxin-induced lung injury. Respir Res 6: 61.
29. Andonegui G, Bonder CS, Green F, Mullaly SC, Zbytnuik L, et al. (2003) Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 111: 1011-1020.
30. Hara Y, Sassi Y, Guibert C, Gambaryan N, Dorfmuller P, et al. (2011) Inhibition of MRP4 prevents and reverses pulmonary hypertension in mice. J Clin Invest 121: 2888-2897.
31. Page CP, Spina D, (2011) Phosphodiesterase inhibitors in the treatment of inflammatory diseases. Handb Exp Pharmacol pp. 391-414.
32. Peter D, Goggel R, Colbatzky F, Nickolaus P, (2011) Inhibition of cyclooxygenase-2 prevents adverse effects induced by phosphodiesterase type 4 inhibitors in rats. Br J Pharmacol 162: 415-427.
33. Herbert C, Hettiaratchi A, Webb DC, Thomas PS, Foster PS, et al. (2008) Suppression of cytokine expression by roflumilast and dexamethasone in a model of chronic asthma. Clin Exp Allergy 38: 847-856.
34. de Wolf CJ, Yamaguchi H, van dH, I, Wielinga PR, Hundscheid SL, et al. (2007) cGMP transport by vesicles from human and mouse erythrocytes. FEBS J 274: 439-450.
35. Takenaka K, Morgan JA, Scheffer GL, Adachi M, Stewart CF, et al. (2007) Substrate overlap between Mrp4 and Abcg2/Bcrp affects purine analogue drug cytotoxicity and tissue distribution. Cancer Res 67: 6965-6972.
36. Cheng JB, Watson JW, Pazoles CJ, Eskra JD, Griffiths RJ, et al. (1997) The phosphodiesterase type 4 (PDE4) inhibitor CP-80,633 elevates plasma cyclic AMP levels and decreases tumor necrosis factor-α (TNFα) production in mice: effect of adrenalectomy. J Pharmacol Exp Ther 280: 621-626.
37. van de Ven R, de GJ, Reurs AW, Wijnands PG, van de WK, et al. (2009) Unimpaired immune functions in the absence of Mrp4 (Abcc4). Immunol Lett 124: 81-87.
38. van de Ven R, Scheffer GL, Reurs AW, Lindenberg JJ, Oerlemans R, et al. (2008) A role for multidrug resistance protein 4 (MRP4; ABCC4) in human dendritic cell migration. Blood 112: 2353-2359.
39. Lee RJ, Foskett JK, (2010) cAMP-activated Ca2+ signaling is required for CFTR-mediated serous cell fluid secretion in porcine and human airways. J Clin Invest 120: 3137-3148.
40. Sayner SL, (2011) Emerging themes of cAMP regulation of the pulmonary endothelial barrier. Am J Physiol Lung Cell Mol Physiol 300: L667-L678.
41. Chen C, Slitt AL, Dieter MZ, Tanaka Y, Scheffer GL, et al. (2005) Up-regulation of Mrp4 expression in kidney of Mrp2-deficient TR- rats. Biochem Pharmacol 70: 1088-1095.
42. Seldon PM, Barnes PJ, Meja K, Giembycz MA, (1995) Suppression of lipopolysaccharide-induced tumor necrosis factor-alpha generation from human peripheral blood monocytes by inhibitors of phosphodiesterase 4: interaction with stimulants of adenylyl cyclase. Mol Pharmacol 48: 747-757.
43. Prabhakar U, Lipshutz D, Bartus JO, Slivjak MJ, Smith EF, et al. (1994) Characterization of cAMP-dependent inhibition of LPS-induced TNF alpha production by rolipram, a specific phosphodiesterase IV (PDE IV) inhibitor. Int J Immunopharmacol 16: 805-816.
44. Wollin L, Bundschuh DS, Wohlsen A, Marx D, Beume R, (2006) Inhibition of airway hyperresponsiveness and pulmonary inflammation by roflumilast and other PDE4 inhibitors. Pulm Pharmacol Ther 19: 343-352.
45. Kanehiro A, Ikemura T, Makela MJ, Lahn M, Joetham A, et al. (2001) Inhibition of Phosphodiesterase 4 Attenuates Airway Hyperresponsiveness and Airway Inflammation in a Model of Secondary Allergen Challenge. Am J Respir Crit Care Med 163: 173-184.
46. Nies AT, Jedlitschky G, Konig J, Herold-Mende C, Steiner HH, et al. (2004) Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129: 349-360.