Intense pseudotransport of a cationic drug mediated by vacuolar ATPase: Procainamide-induced autophagic cell vacuolization

Toxicology and Applied Pharmacology

Volumn 228, Issue 3, 2008, Pages 364-377

  Morissette, Guillaume ^a,b   Lodge, Robert ^b,c   Marceau, François ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

Autophagy; Bafilomycin A1; Drug transport; Procainamide; Smooth muscle cell; V ATPase

Indexed keywords

2,6 DICHLORO N [3 (1 HYDROXY 1 METHYLETHYL) 2 METHYL 7 BENZOFRUANYL]BENZAMIDE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE INHIBITOR; BAFILOMYCIN A1; CATION; FR 167356; PROCAINAMIDE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CELL ORGANELLE; CELL PH; CELL STRUCTURE; CELL VACUOLE; CHEMICAL LABELING; CONTROLLED STUDY; CYTOPATHOLOGY; DRUG DISTRIBUTION; DRUG TRANSPORT; ENDOCYTOSIS; ENZYME INHIBITION; FLUOROMETRY; HUMAN; HUMAN CELL; MITOCHONDRION; OSMOSIS; PHARMACOLOGICAL BLOCKING; PROTEIN TRANSPORT; SMOOTH MUSCLE FIBER;

AUTOPHAGY; BIOLOGICAL TRANSPORT; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MACROLIDES; MUSCLE, SMOOTH, VASCULAR; PROCAINAMIDE; PROTEIN FOLDING; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES;

BOVINAE;

EID: 41949116716     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2007.12.031     Document Type: Article

References (40)

1. Allen D.D., and Lockman R.R. The blood-brain barrier choline transporter as a brain drug delivery vector. Life Sci. 73 (2003) 1609-1615
2. Anderson N., and Borlak J. Drug-induced phospholipidosis. FEBS Lett. 580 (2006) 5533-5540
3. Belkin M., Hardy W.G., Orr H.C., and Lachman A.B. Induction in vitro by autonomic drugs of cytoplasmic vacuoles in ascites tumor cells. J. Natl. Cancer Inst. 28 (1962) 187-201
4. Boger D.L., Fink B.E., Brunette S.R., Tse W.C., and Hendrick M.P. A simple, high-resolution method for establishing DNA binding affinity and sequence selectivity. J. Am. Chem. Soc. 123 (2001) 5878-5891
5. Boya P., Gonzales-Polo R.A., Poncet D., Andreau K., La Vieira H., Roumier T., Perfettini J.L., and Kroemer G. Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine. Oncogene 22 (2003) 3927-3936
6. Boya P., Gonzalez-Polo R.A., Casares N., Perfettini J.L., Dessen P., Larochette N., Métivier D., Meley D., Souquere S., Yoshimori T., Pierron G., Codogno P., and Kroemer G. Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25 (2005) 1025-1040
7. Bunting J.R. Influx and efflux kinetics of cationic dye binding to respiring mitochondria. Biophys. Chem. 42 (1992) 163-175
8. Casartelli A., Bonato M., Cristofori P., Crivellente F., Dal Negro G., Masotto I., Mutinelli C., Valko K., and Bonfante V. A cell-based approach for the early assessment of the phospholipidogenic potential in pharmaceutical research and drug development. Cell Biol. Toxicol. 19 (2003) 161-176
9. 2+ release is inhibited by mitochondrial depolarization. Biochem. J. 347 (2000) 593-600
10. Dudley A.J., and Brown C.D. pH-dependent transport of procainamide in cultured renal epithelial monolayers of OK cells: consistent with nonionic diffusion. Br. J. Pharmacol. 116 (1995) 1685-1691
11. Eskelinen E.L., Tanaka Y., and Saftig P. At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13 (2003) 137-145
12. Fan C., Wang W., Zhao B., Zhang S., and Miao J. Chloroquine inhibits cell growth and induces cell death in A549 lung cancer cells. Bioorg. Med. Chem. 14 (2006) 3218-3222
13. Fedorko M.E., Hirsch J.G., and Cohn Z.A. Autophagic vacuoles produced in vitro. II. Studies on the mechanism of formation of autophagic vacuoles produced by chloroquine. J. Cell Biol. 38 (1968) 392-402
14. Finnin B.C., Reed B.L., and Ruffin N.E. The effects of osmotic pressure on procaine-induced vacuolation in cell culture. J. Pharm. Pharmacol. 21 (1969) 114-117
15. Hu D., Ran Y.-L., Zhong X., Hu H., Yu L., Lou J.-N., Sun L.-X., and Yang Z.-H. Overexpressed Derlin-1 inhibits ER expansion in the endothelial cells derived from human hepatic cavernous hemangioma. J. Biochem. Mol. Biol. 39 (2006) 677-685
16. 1 angiotensin receptor. J. Cell Biol. 157 (2002) 1211-1222
17. Hurtado-Lorenzo A., Skinner M., El Annan J., Futai M., Sun-Wada G.H., Bourgoin S., Casanova J., Wildeman A., Bechoua S., Ausiello D.A., Brown D., and Marshansky V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell Biol. 8 (2006) 124-136
18. Jäger S., Bucci C., Tanida I., Ueno T., Kominami E., Saftig P., and Eskelinen E.L. Role of Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117 (2004) 4837-4848
19. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., and Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19 (2000) 5720-5728
20. +/tertiary amine antiport system in rabbit interstitial brush-border membrane. Am. J. Physiol. Gastrointest. Liver Physiol. 279 (2000) G799-G805
21. Kaufmann A.M., and Krise J.P. Lysosomal sequestration of amine-containing drugs: analysis and therapeutic implications. J. Pharm. Sci. 96 (2006) 729-746
22. Kawasaki-Nishi S., Nishi T., and Forgac M. Proton translocation driven by ATP hydrolysis in V-ATPases. FEBS Lett. 545 (2003) 76-85
23. Kjer-Nielsen L., van Vliet C., Erlich R., Toh B.H., and Gleeson P.A. The Golgi-targeting sequence of the peripheral membrane protein p230. J. Cell Sci. 112 (1999) 1645-1654
24. +-ATPase is essential for the assembly and activity of the proton pump. J. Biol. Chem. 282 (2007) 24495-24503
25. Modica-Napolitano J.S., and Aprille J.R. Delocalized lipophilic cations selectively target the mitochondria of carcinoma cells. Adv. Drug Deliv. Rev. 49 (2001) 63-70
26. Morissette G., Moreau E., C.-Gaudreault R., and Marceau F. Massive cell vacuolization induced by organic amines such as procainamide. J. Pharmacol. Exp. Ther. 310 (2004) 395-406
27. Morissette G., Moreau E., C.-Gaudreault R., and Marceau F. N-substituted 4-aminobenzamides (procainamide analogs): an assessment of multiple cellular effects concerning ion trapping. Mol. Pharmacol. 68 (2005) 1576-1589
28. Morissette G., Bouthillier J., and Marceau F. Trapping of adrenergic decongestant drugs into cellular endomembrane compartments: toxicological and pharmacological consequences. Int. Immunopharmacol. 7 (2007) 1869-1879
29. Morissette G., Germain L., and Marceau F. The anti-wrinkle effect of topical concentrated 2-dimethylaminoethanol involves a vacuolar cytopathology. Br. J. Dermatol. 156 (2007) 433-439
30. Moriyama Y. Membrane energization by proton pumps is important for compartmentalization of drugs and toxins: a new type of active transport. J. Exp. Biol. 199 (1996) 1447-1454
31. Murphy M.P., and Smith R.A.J. Drug delivery to mitochondria: the key to mitochondrial medicine. Adv. Drug Deliv. Rev. 41 (2000) 235-250
32. Niikura K., Takano M., and Sawada M. A novel inhibitor of vacuolar ATPase, FR167356, which can discriminate between osteoclast vacuolar ATPase and lysosomal vacuolar ATPase. Br. J. Pharmacol. 142 (2004) 558-566
33. Piccotti J.R., LaGattuta M.S., Knight S.A., Gonzales A.J., and Bleavins M.R. Induction of apoptosis by cationic amphiphilic drugs amiodarone and imipramine. Drugs Chem. Toxicol. 28 (2005) 117-133
34. Rous B.A., Reaves B.J., Ihrke G., Briggs J.A., Gray S.R., Stephens D.J., Banting G., and Luzio J.P. Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Mol. Biol. Cell 13 (2002) 1071-1082
35. Shacka J.J., Klocke B.J., Shibata M., Uchiyama Y., Datta G., Schmidt R.E., and Roth K.A. Bafilomycin A1 inhibits chloroquine-induced death of cerebellar granule neurons. Mol. Pharmacol. 69 (2006) 1125-1136
36. +-ATPase interacts with phosphofructokinase-1 in humans. J. Biol. Chem. 278 (2003) 20013-20018
37. Szegezdi E., Logue S.E., Gorman A.M., and Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7 (2006) 880-885
38. Tse W.C., and Boger D.L. Sequence-selective DNA recognition: natural products and nature's lessons. Chem. Biol. 11 (2004) 1607-1617
39. Weiss M.J., Wong J.R., Ha C.S., Bleday R., Salem R.R., Steele Jr. G.D., and Chen L.B. Dequalinium, a topical antimicrobial agent, displays anticarcinoma activity based on selective mitochondrial accumulation. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 5444-5448
40. Zhang L., Strong J.M., Qiu W., Lesko L.J., and Huang S.M. Scientific perspectives on drug transporters and their role in drug interaction. Mol. Pharm. 3 (2006) 62-69