Journal of Cystic Fibrosis
Volume 4, Issue 3 , Pages 157-168 , September 2005

P-glycoprotein expression increases ATP release in respiratory cystic fibrosis cells

Received 16 February 2005 ,Revised 1 May 2005 ,Accepted 11 May 2005.

References 

  1. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science. 1989;245:1066–1073
  2. Rommens JM, Iannuzzi MC, Kerem B, Drumm ML, Melmer G, Dean M, et al. Identification of the cystic fibrosis gene: chromosome walking and jumping. Science. 1989;245:1059–1065
  3. Akabas MH. Cystic fibrosis transmembrane conductance regulator. Structure and function of an epithelial chloride channel. J Biol Chem. 2000;275:3729–3732
  4. Sheppard DN, Welsh MJ. Structure and function of the CFTR chloride channel. Physiol Rev. 1999;79:S23–S45
  5. Mall M, Bleich M, Greger R, Schreiber R, Kunzelmann K. The amiloride-inhibitable Na+ conductance is reduced by the cystic fibrosis transmembrane conductance regulator in normal but not in cystic fibrosis airways. J Clin Invest. 1998;102:15–21
  6. Stutts MJ, Canessa CM, Olsen JC, Hamrick M, Cohn JA, Rossier BC, et al. CFTR as a cAMP-dependent regulator of sodium channels. Science. 1995;269:847–850
  7. Kunzelmann K, Schreiber R. CFTR, a regulator of channels. J Membr Biol. 1999;168:1–8
  8. Schwiebert EM, Benos DJ, Egan ME, Stutts MJ, Guggino WB. CFTR is a conductance regulator as well as a chloride channel. Physiol Rev. 1999;79:S145–S166
  9. Prat AG, Reisin IL, Ausiello DA, Cantiello HF. Cellular ATP release by the cystic fibrosis transmembrane conductance regulator. Am J Physiol. 1996;270:C538–C545
  10. Braunstein GM, Roman RM, Clancy JP, Kudlow BA, Taylor AL, Shylonsky VG, et al. Cystic fibrosis transmembrane conductance regulator facilitates ATP release by stimulating a separate ATP release channel for autocrine control of cell volume regulation. J Biol Chem. 2001;276:6621–6630
  11. Taylor AL, Kudlow BA, Marrs KL, Gruenert DC, Guggino WB, Schwiebert EM. Bioluminescence detection of ATP release mechanisms in epithelia. Am J Physiol. 1998;275:C1391–C1406
  12. Cantiello HF. Electrodiffusional ATP movement through CFTR and other ABC transporters. Pflugers Arch. 2001;443(Suppl 1):S22–S27
  13. Schwiebert EM, Egan ME, Guggino WB. Assays of dynamics, mechanisms, and regulation of ATP transport and release: implications for study of ABC transporter function. Methods Enzymol. 1998;292:664–675
  14. Huang P, Lazarowski ER, Tarran R, Milgram SL, Boucher RC, Stutts MJ. Compartmentalized autocrine signaling to cystic fibrosis transmembrane conductance regulator at the apical membrane of airway epithelial cells. Proc Natl Acad Sci U S A. 2001;98:14120–14125
  15. Schwiebert EM. ABC transporter-facilitated ATP conductive transport. Am J Physiol. 1999;276:C1–C8
  16. Walsh DE, Harvey BJ, Urbach V. CFTR regulation of intracellular calcium in normal and cystic fibrosis human airway epithelia. J Membr Biol. 2000;177:209–219
  17. Tarasiuk A, Bar-Shimon M, Gheber L, Korngreen A, Grossman Y, Priel Z. Extracellular ATP induces hyperpolarization and motility stimulation of ciliary cells. Biophys J. 1995;68:1163–1169
  18. Korngreen A, Ma W, Priel Z, Silberberg SD. Extracellular ATP directly gates a cation-selective channel in rabbit airway ciliated epithelial cells. J Physiol. 1998;508(Pt 3):703–720
  19. Zsembery A, Boyce AT, Liang L, Peti-Peterdi J, Bell PD, Schwiebert EM. Sustained calcium entry through P2X nucleotide receptor channels in human airway epithelial cells. J Biol Chem. 2003;278:13398–13408
  20. Lallemand JY, Stoven V, Annereau JP, Boucher J, Blanquet S, Barthe J, et al. Induction by antitumoral drugs of proteins that functionally complement CFTR: a novel therapy for cystic fibrosis?. Lancet. 1997;350:711–712
  21. Ambudkar SV, Dey S, Hrycyna CA, Ramachandra M, Pastan I, Gottesman MM. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol. 1999;39:361–398
  22. Bremer S, Hoof T, Wilke M, Busche R, Scholte B, Riordan JR, et al. Quantitative expression patterns of multidrug-resistance P-glycoprotein (MDR1) and differentially spliced cystic-fibrosis transmembrane-conductance regulator mRNA transcripts in human epithelia. Eur J Biochem. 1992;206:137–149
  23. Abraham EH, Prat AG, Gerweck L, Seneveratne T, Arceci RJ, Kramer R, et al. The multidrug resistance (mdr1) gene product functions as an ATP channel. Proc Natl Acad Sci U S A. 1993;90:312–316
  24. Roman RM, Wang Y, Lidofsky SD, Feranchak AP, Lomri N, Scharschmidt BF, et al. Hepatocellular ATP-binding cassette protein expression enhances ATP release and autocrine regulation of cell volume. J Biol Chem. 1997;272:21970–21976
  25. Roman RM, Lomri N, Braunstein G, Feranchak AP, Simeoni LA, Davison AK, et al. Evidence for multidrug resistance-1 P-glycoprotein-dependent regulation of cellular ATP permeability. J Membr Biol. 2001;183:165–173
  26. Grygorczyk R, Hanrahan JW. Cystic fibrosis transmembrane conductance regulator and adenosine triphosphate. Science. 1997;275:1324–1326
  27. Haws C, Krouse ME, Xia Y, Gruenert DC, Wine JJ. CFTR channels in immortalized human airway cells. Am J Physiol. 1992;263:L692–L707
  28. Baum C, Hegewisch-Becker S, Eckert HG, Stocking C, Ostertag W. Novel retroviral vectors for efficient expression of the multidrug resistance (mdr-1) gene in early hematopoietic cells. J Virol. 1995;69:7541–7547
  29. Bosch I, Croop J. P-glycoprotein multidrug resistance and cancer. Biochim Biophys Acta. 1996;1288:F37–F54
  30. Nooter K, Sonneveld P, Oostrum R, Herweijer H, Hagenbeek T, Valerio D. Overexpression of the mdr1 gene in blast cells from patients with acute myelocytic leukemia is associated with decreased anthracycline accumulation that can be restored by cyclosporin-A. Int J Cancer. 1990;45:263–268
  31. Stanley PE. Extraction of adenosine triphosphate from microbial and somatic cells. Methods Enzymol. 1986;133:14–22
  32. Lundin A, Hasenson M, Persson J, Pousette A. Estimation of biomass in growing cell lines by adenosine triphosphate assay. Methods Enzymol. 1986;133:27–42
  33. Johnstone RW, Ruefli AA, Smyth MJ. Multiple physiological functions for multidrug transporter P-glycoprotein?. Trends Biochem Sci. 2000;25:1–6
  34. Bosch I, Jackson GR, Croop JM, Cantiello HF. Expression of Drosophila melanogaster P-glycoproteins is associated with ATP channel activity. Am J Physiol. 1996;271:C1527–C1538
  35. Wei LY, Stutts MJ, Hoffman MM, Roepe PD. Overexpression of the cystic fibrosis transmembrane conductance regulator in NIH 3T3 cells lowers membrane potential and intracellular pH and confers a multidrug resistance phenotype. Biophys J. 1995;69:883–895
  36. Altschuler EL. Azithromycin, the multidrug-resistant protein, and cystic fibrosis. Lancet. 1998;351:1286
  37. Breuer W, Slotki IN, Ausiello DA, Cabantchik IZ. Induction of multidrug resistance downregulates the expression of CFTR in colon epithelial cells. Am J Physiol. 1993;265:C1711–C1715
  38. Trezise AE, Ratcliff R, Hawkins TE, Evans MJ, Freeman TC, Romano PR, et al. Co-ordinate regulation of the cystic fibrosis and multidrug resistance genes in cystic fibrosis knockout mice. Hum Mol Genet. 1997;6:527–537
  39. Trezise AE, Romano PR, Gill DR, Hyde SC, Sepulveda FV, Buchwald M, et al. The multidrug resistance and cystic fibrosis genes have complementary patterns of epithelial expression. EMBO J. 1992;11:4291–4303
  40. 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
  41. Marcet B, Chappe V, Delmas P, Gola M, Verrier B. Negative regulation of CFTR activity by extracellular ATP involves P2Y2 receptors in CFTR-expressing CHO cells. J Membr Biol. 2003;194:21–32
  42. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta. 1976;455:152–162
  43. Sabouraud A, Rochdi M, Urtizberea M, Christen MO, Achtert G, Scherrmann JM. Pharmacokinetics of colchicine: a review of experimental and clinical data. Z Gastroenterol. 1992;1(30 Suppl.):35–39
  44. Rochdi M, Sabouraud A, Baud FJ, Bismuth C, Scherrmann JM. Toxicokinetics of colchicine in humans: analysis of tissue, plasma and urine data in ten cases. Hum Exp Toxicol. 1992;11:510–516
  45. Witko-Sarsat V, Sermet-Gaudelus I, Lenoir G, Descamps-Latscha B. Inflammation and CFTR: might neutrophils be the key in cystic fibrosis?. Mediators Inflamm. 1999;8:7–11
  46. Entzian P, Schlaak M, Seitzer U, Bufe A, Acil Y, Zabel P. Antiinflammatory and antifibrotic properties of colchicine: implications for idiopathic pulmonary fibrosis. Lung. 1997;175:41–51
  47. Sermet-Gaudelus I, Stoven V, Annereau JP, Witko-Sarsat V, Reinert P, Guyot M, et al. Interest of colchicine for the treatment of cystic fibrosis patients. Preliminary report. Mediators Inflamm. 1999;8:13–15
  48. Sugita M, Yue Y, Foskett JK. CFTR Cl− channel and CFTR-associated ATP channel: distinct pores regulated by common gates. EMBO J. 1998;17:898–908
  49. Pasyk EA, Foskett JK. Cystic fibrosis transmembrane conductance regulator-associated ATP and adenosine 3′-phosphate 5′-phosphosulfate channels in endoplasmic reticulum and plasma membranes. J Biol Chem. 1997;272:7746–7751
  50. Abraham EH, Okunieff P, Scala S, Vos P, Oosterveld MJ, Chen AY, et al. Cystic fibrosis transmembrane conductance regulator and adenosine triphosphate. Science. 1997;275:1324–1326
  51. Li C, Ramjeesingh M, Bear CE. Purified cystic fibrosis transmembrane conductance regulator (CFTR) does not function as an ATP channel. J Biol Chem. 1996;271:11623–11626
  52. Reddy MM, Quinton PM, Haws C, Wine JJ, Grygorczyk R, Tabcharani JA, et al. Failure of the cystic fibrosis transmembrane conductance regulator to conduct ATP. Science. 1996;271:1876–1879
  53. Konig J, Schreiber R, Mall M, Kunzelmann K. No evidence for inhibition of ENaC through CFTR-mediated release of ATP. Biochim Biophys Acta. 2002;1565:17–28
  54. Ito Y, Son M, Sato S, Ishikawa T, Kondo M, Nakayama S, et al. ATP release triggered by activation of the Ca2+-activated K+ channel in human airway Calu-3 cells. Am J Respir Cell Mol Biol. 2004;30:388–395
  55. Boudreault F, Grygorczyk R. Cell swelling-induced ATP release and gadolinium-sensitive channels. Am J Physiol Cell Physiol. 2002;282:C219–C226
  56. Grygorczyk R, Guyot A. Osmotic swelling-induced ATP release: a new role for tyrosine and Rho-kinases?. J Physiol. 2001;532:582
  57. Aleu J, Martin-Satue M, Navarro P, Perez dL I, Bahima L, Marsal J, et al. Release of ATP induced by hypertonic solutions in Xenopus oocytes. J Physiol. 2003;547:209–219
  58. Schreiber R, Konig J, Sun J, Markovich D, Kunzelmann K. Effects of purinergic stimulation, CFTR and osmotic stress on amiloride-sensitive Na+ transport in epithelia and Xenopus oocytes. J Membr Biol. 2003;192:101–110
  59. Valverde MA, Bond TD, Hardy SP, Taylor JC, Higgins CF, Altamirano J, et al. The multidrug resistance P-glycoprotein modulates cell regulatory volume decrease. EMBO J. 1996;15:4460–4468
  60. Cheng VC, Wu AK, Hung IF, Tang BS, Lee RA, Lau SK, et al. Clinical deterioration in community acquired infections associated with lymphocyte upsurge in immunocompetent hosts. Scand J Infect Dis. 2004;36:743–751
  61. Iwase N, Sasaki T, Shimura S, Yamamoto M, Suzuki S, Shirato K. ATP-induced Cl− secretion with suppressed Na+ absorption in rabbit tracheal epithelium. Respir Physiol. 1997;107:173–180
  62. McCoy DE, Taylor AL, Kudlow BA, Karlson K, Slattery MJ, Schwiebert LM, et al. Nucleotides regulate NaCl transport in mIMCD-K2 cells via P2X and P2Y purinergic receptors. Am J Physiol. 1999;277:F552–F559
  63. Wang Y, Roman R, Lidofsky SD, Fitz JG. Autocrine signaling through ATP release represents a novel mechanism for cell volume regulation. Proc Natl Acad Sci U S A. 1996;93:12020–12025
  64. Kellerman DJ. P2Y(2) receptor agonists: a new class of medication targeted at improved mucociliary clearance. Chest. 2002;121:201S–205S

PII: S1569-1993(05)00049-4

doi: 10.1016/j.jcf.2005.05.003

Journal of Cystic Fibrosis
Volume 4, Issue 3 , Pages 157-168 , September 2005