Vitamin e TPGS P-glycoprotein inhibition mechanism: Influence on conformational flexibility, intracellular ATP levels, and role of time and site of access

Molecular Pharmaceutics

Volumn 7, Issue 3, 2010, Pages 642-651

  Collnot, Eva Maria ^a   Baldes, Christiane ^a   Schaefer, Ulrich F ^a   Edgar, Kevin J ^b,c   Wempe, Michael F ^b,d   Lehr, Claus Michael ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b EASTMAN CHEMICAL COMPANY   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

ATP; Conformation; Efflux transporter; Inhibition; P glycoprotein; Vitamin E TPGS

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN 1; NUCLEOTIDE BINDING PROTEIN; ORTHOVANADIC ACID; TOCOFERSOLAN;

ARTICLE; CELL STRAIN CACO 2; CONFORMATIONAL TRANSITION; DRUG INHIBITION; DRUG SYNTHESIS; DRUG TRANSPORT; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN BINDING;

ADENOSINE TRIPHOSPHATE; CACO-2 CELLS; HUMANS; P-GLYCOPROTEIN; POLYETHYLENE GLYCOLS; PROTEIN CONFORMATION; VITAMIN E;

EID: 77953235847     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp900191s     Document Type: Article

References (39)

1. Ueda, K.; Cornwell, M. M.; Gottesman, M. M.; Pastan, I.; Roninson, I. B.; Ling, V.; Riordan, J. R. The mdr1 gene, responsible for multidrug-resistance, codes for P-glycoprotein Biochem. Biophys. Res. Commun. 1986, 141 (3) 956-962
2. Higgins, C. F. ABC transporters: from microorganisms to man Annu. Rev. Cell Biol. 1992, 8, 67-113
3. Thiebaut, F.; Tsuruo, T.; Hamada, H.; Gottesman, M. M.; Pastan, I.; Willingham, M. C. Cellular Localization of the Multidrug-Resistance Gene Product P-glycoprotein in Normal Human Tissues Proc. Natl. Acad. Sci. U.S.A. 1987, 84 (21) 7735-7738
4. Fromm, M. F. Importance of P-glycoprotein at blood-tissue barriers Trends Pharmacol. Sci. 2004, 25 (8) 423-429
5. Mizuno, N.; Niwa, T.; Yotsumoto, Y.; Sugiyama, Y. Impact of drug transporter studies on drug discovery and development Pharmacol. Rev. 2003, 55 (3) 425-461
6. Lankas, G. R.; Wise, L. D.; Cartwright, M. E.; Pippert, T.; Umbenhauer, D. R. Placental P-glycoprotein deficiency enhances susceptibility to chemically induced birth defects in mice Reprod. Toxicol. 1998, 12 (4) 457-463
7. van der Valk, P.; van Kalken, C. K.; Ketelaars, H.; Broxterman, H. J.; Scheffer, G.; Kuiper, C. M.; Tsuruo, T.; Lankelma, J.; Meijer, C. J.; Pinedo, H. M. Distribution of multi-drug resistance-associated P-glycoprotein in normal and neoplastic human tissues. Analysis with 3 monoclonal antibodies recognizing different epitopes of the P-glycoprotein molecule Ann. Oncol. 1990, 1 (1) 56-64
8. Roninson, I. B. Molecular mechanism of multidrug resistance in tumor cells Clin. Physiol. Biochem. 1987, 5 (3-4) 140-151
9. Suzuki, H.; Sugiyama, Y. Role of metabolic enzymes and efflux transporters in the absorption of drugs from the small intestine Eur. J. Pharm. Sci. 2000, 12 (1) 3-12
10. Malingre, M. M.; Beijnen, J. H.; Rosing, H.; Koopman, F. J.; Jewell, R. C.; Paul, E. M.; Ten Bokkel Huinink, W. W.; Schellens, J. H. Co-administration of GF120918 significantly increases the systemic exposure to oral paclitaxel in cancer patients Br. J. Cancer 2001, 84 (1) 42-47
11. Cagliero, E.; Ferracini, R.; Morello, E.; Scotlandi, K.; Manara, M. C.; Buracco, P.; Comandone, A.; Baroetto Parisi, R.; Baldini, N. Reversal of multidrug-resistance using Valspodar (PSC 833) and doxorubicin in osteosarcoma Oncol. Rep. 2004, 12 (5) 1023-1031
12. Kitagawa, S.; Nabekura, T.; Takahashi, T.; Nakamura, Y.; Sakamoto, H.; Tano, H.; Hirai, M.; Tsukahara, G. Structure-activity relationships of the inhibitory effects of flavonoids on P-glycoprotein-mediated transport in KB-C2 cells Biol. Pharm. Bull. 2005, 28 (12) 2274-2278
13. Schuldes, H.; Dolderer, J. H.; Zimmer, G.; Knobloch, J.; Bickeboller, R.; Jonas, D.; Woodcock, B. G. Reversal of multidrug resistance and increase in plasma membrane fluidity in CHO cells with R-verapamil and bile salts Eur. J. Cancer 2001, 37 (5) 660-667
14. Dintaman, J. M.; Silverman, J. A. Inhibition of P-glycoprotein by D-alpha-tocopheryl polyethylene glycol 1000 succinate (TPGS) Pharm. Res. 1999, 16 (10) 1550-1556
15. Shono, Y.; Nishihara, H.; Matsuda, Y.; Furukawa, S.; Okada, N.; Fujita, T.; Yamamoto, A. Modulation of intestinal P-glycoprotein function by cremophor EL and other surfactants by an in vitro diffusion chamber method using the isolated rat intestinal membranes J. Pharm. Sci. 2004, 93 (4) 877-885
16. Collnot, E. M.; Baldes, C.; Wempe, M. F.; Hyatt, J.; Navarro, L.; Edgar, K. J.; Schaefer, U. F.; Lehr, C. M. Influence of vitamin E TPGS poly(ethylene glycol) chain length on apical efflux transporters in Caco-2 cell monolayers J. Controlled Release 2006, 111 (1-2) 35-40
17. Bogman, K.; Erne-Brand, F.; Alsenz, J.; Drewe, J. The role of surfactants in the reversal of active transport mediated by multidrug resistance proteins J. Pharm. Sci. 2003, 92 (6) 1250-1261
18. Cornaire, G.; Woodley, J.; Hermann, P.; Cloarec, A.; Arellano, C.; Houin, G. Impact of excipients on the absorption of P-glycoprotein substrates in vitro and in vivo Int. J. Pharm. 2004, 278 (1) 119-131
19. Johnson, B. M.; Charman, W. N.; Porter, C. J. An in vitro examination of the impact of polyethylene glycol 400, Pluronic P85, and vitamin E d-alpha-tocopheryl polyethylene glycol 1000 succinate on P-glycoprotein efflux and enterocyte-based metabolism in excised rat intestine AAPS PharmSci 2002, 4 (4 E40
20. Rege, B. D.; Kao, J. P.; Polli, J. E. Effects of nonionic surfactants on membrane transporters in Caco-2 cell monolayers Eur. J. Pharm. Sci. 2002, 16 (4-5) 237-246
21. Collnot, E. M.; Baldes, C.; Wempe, M. F.; Kappl, R.; Huttermann, J.; Hyatt, J. A.; Edgar, K. J.; Schaefer, U. F.; Lehr, C. M. Mechanism of Inhibition of P-Glycoprotein Mediated Efflux by Vitamin E TPGS: Influence on ATPase Activity and Membrane Fluidity Mol. Pharmaceutics 2007, 4 (3) 465-474
22. Orlowski, S.; Selosse, M. A.; Boudon, C.; Micoud, C.; Mir, L. M.; Belehradek, J., Jr.; Garrigos, M. Effects of detergents on P-glycoprotein atpase activity: differences in perturbations of basal and verapamil-dependent activities Cancer Biochem. Biophys. 1998, 16 (1-2) 85-110
23. Batrakova, E. V.; Li, S.; Li, Y.; Alakhov, V. Y.; Kabanov, A. V. Effect of pluronic P85 on ATPase activity of drug efflux transporters Pharm. Res. 2004, 21 (12) 2226-2233
24. Batrakova, E. V.; Li, S.; Vinogradov, S. V.; Alakhov, V. Y.; Miller, D. W.; Kabanov, A. V. Mechanism of pluronic effect on P-glycoprotein efflux system in blood-brain barrier: Contributions of energy depletion and membrane fluidization J. Pharmacol. Exp. Ther. 2001, 299 (2) 483-493
25. Mechetner, E.; Roninson, I. Efficient Inhibition of P-Glycoprotein- Mediated Multidrug Resistance with a Monoclonal Antibody Proc. Natl. Acad. Sci. U.S.A. 1992, 89 (13) 5824-5828
26. Mechetner, E. B.; Schott, B.; Morse, B. S.; Stein, W. D.; Druley, T.; Davis, K. A.; Tsuruo, T.; Roninson, I. B. P-glycoprotein function involves conformational transitions detectable by differential immunoreactivity Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (24) 12908-12913
27. Urbatsch, I. L.; Sankaran, B.; Weber, J.; Senior, A. E. P-glycoprotein Is Stably Inhibited by Vanadate-induced Trapping of Nucleotide at a Single Catalytic Site J. Biol. Chem. 1995, 270 (33) 19383-19390
28. Druley, T. E.; Stein, W. D.; Roninson, I. B. Analysis of MDR1 P-Glycoprotein Conformational Changes in Permeabilized Cells Using Differential Immunoreactivity Biochemistry 2001, 40 (14) 4312-4322
29. Zhou, Y.; Gottesman, M. M.; Pastan, I. The extracellular loop between TM5 and TM6 of P-glycoprotein is required for reactivity with monoclonal antibody UIC2 Arch. Biochem. Biophys. 1999, 367 (1) 74-80
30. Maki, N.; Hafkemeyer, P.; Dey, S. Allosteric modulation of human P-glycoprotein. Inhibition of transport by preventing substrate translocation and dissociation J. Biol. Chem. 2003, 278 (20) 18132-18139
31. Rapoport, N.; Marin, A. P.; Timoshin, A. A. Effect of a Polymeric Surfactant on Electron Transport in HL-60 Cells Arch. Biochem. Biophys. 2000, 384 (1) 100-108
32. Batrakova, E. V.; Li, S.; Elmquist, W. F.; Miller, D. W.; Alakhov, V. Y.; Kabanov, A. V. Mechanism of sensitization of MDR cancer cells by Pluronic block copolymers: Selective energy depletion Br. J. Cancer 2001, 85 (12) 1987-1997
33. Zhu, S.; Huang, R.; Hong, M.; Jiang, Y.; Hu, Z.; Liu, C.; Pei, Y. Effects of polyoxyethylene (40) stearate on the activity of P-glycoprotein and cytochrome P450 Eur. J. Pharm. Sci. 2009, 37 (5) 573-580
34. Wempe, M. F.; Wright, C.; Little, J. L.; Lightner, J. W.; Large, S. E.; Caflisch, G. B.; Buchanan, C. M.; Rice, P. J.; Wacher, V. J.; Ruble, K. M.; Edgar, K. J. Inhibiting efflux with novel non-ionic surfactants: Rational design based on vitamin E TPGS Int. J. Pharm. 2009, 370 (1-2) 93-102
35. Troutman, M. D.; Thakker, D. R. Rhodamine 123 requires carrier-mediated influx for its activity as a P-glycoprotein substrate in Caco-2 cells Pharm. Res. 2003, 20 (8) 1192-1199
36. Bogman, K.; Zysset, Y.; Degen, L.; Hopfgartner, G.; Gutmann, H.; Alsenz, J.; Drewe, J. P-glycoprotein and surfactants: effect on intestinal talinolol absorption Clin. Pharmacol. Ther. 2005, 77 (1) 24-32
37. Yu, L.; Bridgers, A.; Polli, J.; Vickers, A.; Long, S.; Roy, A.; Winnike, R.; Coffin, M. Vitamin E-TPGS increases absorption flux of an HIV protease inhibitor by enhancing its solubility and permeability Pharm. Res. 1999, 16 (12) 1812-1817
38. Varma, M. V.; Panchagnula, R. Enhanced oral paclitaxel absorption with vitamin E-TPGS: effect on solubility and permeability in vitro, in situ and in vivo Eur. J. Pharm. Sci. 2005, 25 (4-5) 445-453
39. Troutman, M.; Thakker, D. Efflux ratio cannot assess P-glycoprotein- mediated attenuation of absorptive transport: asymmetric effect of P-glycoprotein on absorptive and secretory transport across Caco-2 cell monolayers Pharm. Res. 2003, 20 (8) 1200-1209