Tobacco carcinogen NNK transporter MRP2 regulates CFTR function in lung epithelia: Implications for lung cancer

Cancer Letters

Volumn 292, Issue 2, 2010, Pages 246-253

  Li, Chunying ^a   Schuetz, John D ^b   Naren, Anjaparavanda P ^c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

CFTR; Lung cancer; MRP2; NNK; Protein interaction; Tobacco specific carcinogen

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ABC TRANSPORTER; MULTIDRUG RESISTANCE PROTEIN 2; PDZ PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR; 4-(N-METHYL-N-NITROSAMINO)-1-(3-PYRIDYL)-1-BUTANONE; CARCINOGEN; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN 2; NITROSAMINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CELLULAR DISTRIBUTION; CIGARETTE SMOKING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; LUNG CANCER; LUNG CARCINOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; TOBACCO; UPREGULATION; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; DOG; EPITHELIUM CELL; HAMSTER; HUMAN; LUNG; LUNG TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY;

NICOTIANA TABACUM;

ANIMALS; CARCINOGENS; CELL LINE; CRICETINAE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DOGS; EPITHELIAL CELLS; HUMANS; LUNG; LUNG NEOPLASMS; MICROSCOPY, FLUORESCENCE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NITROSAMINES; TOBACCO;

EID: 77951884691     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.12.009     Document Type: Article

References (39)

1. Nelson D.E., Kirkendall R.S., Lawton R.L., Chrismon J.H., Merritt R.K., Arday D.A., Giovino G.A. Surveillance for smoking-attributable mortality and years of potential life lost; by state - United States. MMWR CDC 1994, 43:1-8.
2. Ockene I.S., Miller N.H. Cigarette smoking, cardiovascular disease, and stroke: a statement for healthcare professionals from the American Heart Association. Circulation 1997, 96:3243-3247.
3. Centers for Disease Control and Prevention. Smoking-attributable mortality and years of potential life lost - United States, Morbidity Mortality Weekly Rep. 42 (1993) 645-648.
4. Hecht S.S. Tobacco smoke carcinogens and lung cancer. J. Natl. Cancer Inst. 1999, 91:1194-1210.
5. Proulx L.-I., Castonguay A., Bissonnette E.Y. Cytokine production by alveolar macrophages is down regulated by the a-methylhydroxylation pathway of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK). Carcinogenesis 2004, 25:997-1003.
6. Dean M., Rzhetsky A., Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001, 11:1156-1166.
7. 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.
8. Gerk P.M., Vore M. Regulation of expression of the multidrug resistance-associated protein 2 (MRP2) and its role in drug disposition. J. Pharmacol. Exp. Ther. 2002, 302:407-415.
9. Leslie E.M., Ito K.-I., Upadhyaya P., Hecht S.S., Deeley R.G., Cole S.P.C. Transport of the β-O-glucuronide conjugate of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) by the multidrug resistance protein 1 (MRP1). J. Biol. Chem. 2001, 276:27846-27854.
10. Leslie E.M., Ghibellini G., Nezasa K., Brouwer K.L. Biotransformation and transport of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) in bile duct-cannulated wild-type and Mrp2/Abcc2-deficient (TR) Wistar rats. Carcinogenesis 2007, 28:2650-2656.
11. Hegedus T., Sessler T., Scott R., Thelin W., Bakos E., Varadi A., Szabo K., Homolya L., Milgram S.L., Sarkadi B. C-terminal phosphorylation of MRP2 modulates its interaction with PDZ proteins. Biochem. Biophys. Res. Commun. 2003, 302:454-461.
12. Kocher O., Comella N., Gilchrist A., Pal R., Tognazzi K., Brown L.F., Knoll J.H. PDZK1, a novel PDZ domain-containing protein up-regulated in carcinomas and mapped to chromosome 1q21, interacts with cMOAT (MRP2), the multidrug resistance-associated protein. Lab. Invest. 1999, 79:1161-1170.
13. Fanning A.S., Anderson J.M. PDZ domains: fundamental building blocks in the organization of protein complexes at the plasma membrane. J. Clin. Invest. 1999, 103:767-772.
14. Hung A.Y., Sheng M. PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 2002, 277:5699-5702.
15. Bezprozvanny I., Maximov A. PDZ domains: more than just a glue. Proc. Natl. Acad. Sci. USA 2001, 98:787-789.
16. Altschuler Y., Hodson C., Milgram S.L. The apical compartment: trafficking pathways, regulators and scaffolding proteins. Curr. Opin. Cell Biol. 2003, 15:423-429.
17. Wang S., Yue H., Derin R.B., Guggino W.B., Li M. Accessory protein facilitated CFTR-CFTR interaction, a molecular mechanism to potentiate the chloride channel activity. Cell 2000, 103:169-179.
18. Hall R.A., Ostedgaard L.S., Premont R.T., Blitzer J.T., Rahman N., Welsh M.J., Lefkowitz R.J. A C-terminal motif found in the beta2-adrenergic receptor P2Y1 receptor, and cystic fibrosis transmembrane conductance regulator determines binding to the Na+/H+ exchanger regulatory factor family of PDZ proteins. Proc. Natl. Acad. Sci. USA 1998, 95:8496-8501.
19. Short D.B., Trotter K.W., Reczek D., Kreda S.M., Bretscher A., Boucher R.C., Stutts M.J., Milgram S.L. An apical PDZ protein anchors the cystic fibrosis transmembrane conductance regulator to the cytoskeleton. J. Biol. Chem. 1998, 273:19797-19801.
20. Welsh M.J., Tsui L.C., Boat T.F., Beaudet A.L. Cystic fibrosis. The Metabolic and Molecular Basis of Inherited Diseases: Membrane Transport Systems 1995, 3799-3876. McGraw-Hill, New York. C. Scriver, A.L. Beaudet, W.S. Sly, D. Valle (Eds.).
21. Naren A.P., Cobb B., Li C., Roy K., Nelson D., Heda G.D., Liao J., Kirk K.L., Sorscher E.J., Hanrahan J., Clancy J.P. A macromolecular complex of beta 2 adrenergic, receptor CFTR, and ezrin/radixin/moesin-binding phosphoprotein 50 is regulated by PKA. Proc. Natl. Acad. Sci. USA 2003, 100:342-346.
22. Li C., Dandridge K.S., Di A., Marrs K.L., Harris E.L., Roy K., Jackson J.S., Makarova N.V., Fujiwara Y., Farrar P.L., Nelson D.J., Tigyi G.J., Naren A.P. Lysophosphatidic acid inhibits cholera toxin-induced secretory diarrhea through CFTR-dependent protein interactions. J Exp. Med. 2005, 202:975-986.
23. Li C., Krishnamurthy P.C., Penmatsa H., Marrs K.L., Wang X.Q., Zaccolo M., Jalink K., Li M., Nelson D.J., Schuetz J.D., Naren A.P. Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 2007, 131:940-951.
24. Li X., Weinman S.A. Mrp2 modulates the activity of chloride channels in isolated hepatocytes. Hepatology 2002, 36:65-71.
25. Li C., Roy K., Dandridge K., Naren A.P. Molecular assembly of cystic fibrosis transmembrane conductance regulator in plasma membrane. J. Biol. Chem. 2004, 279:24673-24684.
26. Rubenstein R.C., Zeitlin P.L. Sodium 4-phenylbutyrate downregulates Hsc70: implications for intracellular trafficking of ΔF508-CFTR. Am. J. Physiol. Cell Physiol. 2000, 278:C259-C267.
27. Naren A.P. Methods for the study of intermolecular and intramolecular interactions regulating CFTR function. Methods Mol. Med. 2002, 70:175-186.
28. Ryu S., Kawabe T., Nada S., Yamaguchi A. Identification of basic residues involved in drug export function of human multidrug resistance-associated protein 2. J. Biol. Chem. 2000, 275:39617-39624.
29. Roelofsen H., Soroka C.J., Keppler D., Boyer J.L. Cyclic AMP stimulates sorting of the canalicular organic anion transporter (Mrp2/cMoat) to the apical domain in hepatocyte couplets. J. Cell Sci. 1998, 111:1137-1145.
30. Chang X.B., Tabcharani J.A., Hou Y.X., Jensen T.J., Kartner N., Alon N., Hanrahan J.W., Riordan J.R. Protein kinase A (PKA) still activates CFTR chloride channel after mutagenesis of all 10 PKA consensus phosphorylation sites. J. Biol. Chem. 1993, 268:11304-11311.
31. Kruh G.D., Belinsky M.G. The MRP family of drug efflux pumps. Oncogene 2003, 22:7537-7552.
32. Sheth P., Basuroy S., Li C., Naren A.P., Rao R.K. Role of phosphatidylinositol in oxidative stress-induced disruption of tight junction. J. Biol. Chem. 2003, 278:49239-49245.
33. Proulx L.I., Gaudreault M., Turmel V., Augusto L.A., Castonguay A., Bissonnette E.Y. 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone a, component of tobacco smoke, modulates mediator release from human bronchial and alveolar epithelial cells. Clin. Exp. Immunol. 2005, 140(1):46-53.
34. Therriault M.J., Proulx L.I., Castonguay A., Bissonnette E.Y. Immunomodulatory effects of the tobacco-specific carcinogen, NNK, on alveolar macrophages. Clin. Exp. Immunol. 2003, 132(2):232-238.
35. Schuller H.M., Tithof P.K., Williams M., Plummer H. The tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone is a β-adrenergic agonist and stimulates DNA synthesis in lung adenocarcinoma via β-adrenergic receptor-mediated release of arachidonic acid. Cancer Res. 1999, 59:4510-4515.
36. Zeitlin P.L., Lu L., Rhim J., Cutting G., Stetten G., Kieffer K.A., Craig R., Guggino W.B. A cystic fibrosis bronchial epithelial cell line: immortalization by adeno-12-SV40 infection. Am. J. Respir. Cell Mol. Biol. 1991, 4:313-319.
37. Li C., Naren A.P. Macromolecular complexes of cystic fibrosis transmembrane conductance regulator and its interacting partners. Pharmacol. Ther. 2005, 108:208-223.
38. Kreindler J.L., Jackson A.D., Kemp P.A., Bridges R.J., Danahay H. Inhibition of chloride secretion in human bronchial epithelial cells by cigarette smoke extract. Am. J. Physiol. Lung Cell Mol. Physiol. 2005, 288:L894-L902.
39. Cantin A.M., Hanrahan J.W., Bilodeau G., Ellis L., Dupuis A., Liao J., Zielenski J., Durie P. Cystic fibrosis transmembrane conductance regulator function is suppressed in cigarette smokers. Am. J. Respir. Crit. Care Med. 2006, 173:1139-1144.