Cocaine induces a mixed lysosomal lipidosis in cultured fibroblasts, by inactivation of acid sphingomyelinase and inhibition of phospholipase A1

Toxicology and Applied Pharmacology

Volumn 194, Issue 2, 2004, Pages 101-110

  Nassogne, Marie Cécile ^a   Lizarraga, Chantal ^a   N'Kuli, Francisca ^a   Van Bambeke, Françoise ^b   Van Binst, Roger ^c   Wallemacq, Pierre ^c   Tulkens, Paul M ^b   Mingeot Leclercq, Marie Paule ^b   Levade, Thierry ^d   Courtoy, Pierre J ^a  

^a DE DUVE INSTITUTE   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^d CHU RANGUEIL   (France)

Author keywords

Cocaine; DMEM; Dulbecco's modified Eagle's medium; FCS; Fetal calf serum; Lysosomes; Phospholipidosis

Indexed keywords

ADENOSINE TRIPHOSPHATASE INHIBITOR; BAFILOMYCIN A1; BENZOYLECGONINE; COCAINE; CYSTEINE PROTEINASE INHIBITOR; LEUPEPTIN; LYSOSOME ENZYME; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; PHOSPHOLIPASE A1; PHOSPHOLIPID; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE;

ANIMAL CELL; ARTICLE; CELL LEVEL; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME INHIBITION; FIBROBLAST; LIPIDOSIS; LYSOSOME; LYSOSOME STORAGE DISEASE; NONHUMAN; RAT;

CICONIIFORMES;

EID: 9144258195     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.taap.2003.09.026     Document Type: Article

References (58)

1. Aubert-Tulkens G., Van Hoof F., Tulkens P. Gentamicin-induced lysosomal phospholipidosis in cultured rat fibroblasts. Lab. Invest. 40:1979;481-491.
2. Bailey D.N. Cocaine and cocaethylene binding to human milk. Am. J. Clin. Pathol. 110:1998;491-494.
3. Bartlett G.R. Phosphorus assay in column chromatography. J. Biol. Chem. 234:1959;466-468.
4. Bowman E.J., Siebers A., Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. U.S.A. 85:1988;7972-7976.
5. Catravas J.D., Waters I.W., Walz M.A., Davis W.M. Acute cocaine intoxication in the conscious dog: pathophysiologic profile of acute lethality. Arch. Int. Phamacodyn. Ther. 235:1978;328-340.
6. Cornillie F., Brosens I., Belsey E.M., Marbaix E., Baudhuin P., Courtoy P.J. Lysosomal enzymes in the human endometrium: a biochemical study in untreated and levonorgestrel-treated women. Contraception. 43:1991;387-400.
7. de Duve C., de Barsy T., Poole B., Trouet A., Tulkens P., Van Hoof F. Lysosomotropic agents. Biochem. Pharmacol. 23:1974;2495-2531.
8. Draye J.P., Courtoy P.J., Quintart J., Baudhuin P. Relations between plasma membrane and lysosomal membrane. 2. Quantitative evaluation of plasma membrane marker enzymes in the lysosomes. Eur. J. Biochem. 170:1987;405-411.
9. Draye J.P., Courtoy P.J., Quintart J., Baudhuin P. A quantitative model of traffic between plasma membrane and secondary lysosomes: evaluation of inflow, lateral diffusion, and degradation. J. Cell Biol. 107:1988;2109-2115.
10. El Mouedden M., Laurent G., Mingeot-Leclercq M.P., Tulkens P.M. Gentamicin-induced apoptosis in renal cell lines and embryonic rat fibroblasts. Toxicol. Sci. 56:2000;229-239.
11. El-Mouedden M., Laurent G., Mingeot-Leclercq M.P., Taper H.S., Cumps J., Tulkens P.M. Apoptosis in renal proximal tubules of rats treated with low doses of aminoglycosides. Antimicrob. Agents Chemother. 44:2000;665-675.
12. Enari M., Sakahira H., Yokoyama H., Okawa K., Iwamatsu A., Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature. 391:1998;43-50.
13. Folch J., Lees M., Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226:1957;497-509.
14. Fowler S., de Duve C. Digestive activity of lysosomes. III. The digestion of lipids by extracts of rat liver lysosomes. J. Biol. Chem. 244:1969;471-481.
15. Gerbaux C., Van Bambeke F., Montenez J.P., Piret J., Morlighem G., Tulkens P.M. Hyperactivity of cathepsin B and other lysosomal enzymes in fibroblasts exposed to azithromycin, a dicationic antibiotic with exceptional tissue accumulation. FEBS Lett. 394:1996;307-310.
16. Giurgea-Marion L., Toubeau G., Laurent G., Heuson-Stiennon J.A., Tulkens P.M. Impairment of lysosome-pinocytic vesicle fusion in rat kidney proximal tubules after treatment with gentamicin at low doses. Toxicol. Appl. Pharmacol. 86:1986;271-285.
17. Halliwell W.H. Cationic amphiphilic drug-induced phospholipidosis. Toxicol. Pathol. 25:1997;53-60.
18. He J., Xiao Y., Casiano C.A., Zhang L. Role of mitochondrial cytochrome c in cocaine-induced apoptosis in coronary artery endothelial cells. J. Pharmacol. Exp. Ther. 295:2000;896-903.
19. Hostetler K.Y., Jellison E.J. Inhibition of kidney lysosomal phospholipase A1 by aminoglycosides is a novel variant of substrate depletion inhibition. J. Pharmacol. Exp. Ther. 254:1990;188-191.
20. Huang J.Q., Trasier J.M., Igdoura S., Michaud J., Hanai N., Gravel R.A. Apoptotic cell death in mouse models of GM2 gangliosidosis and observations on human Tay-Sachs and Sandhoff diseases. Hum. Mol. Genet. 6:1997;1879-1885.
21. Hurwitz R., Ferlinz K., Sandhoff K. The tricyclic antidepressant desipramine causes proteolytic degradation of lysosomal sphingomyelinase in human fibroblasts. Biol. Chem. Hoppe-Seyler. 375:1994;447-450.
22. Ishisaka R., Utsumi T., Yabuki M., Kanno T., Furuno T., Inoue M., Utsumi K. Activation of caspase-3-like protease by digitonin-treated lysosomes. FEBS Lett. 435:1998;233-236.
23. Ishisaka R., Kanno T., Akiyama J., Yoshioka T., Utsumi K., Utsumi T. Activation of caspase-3 by lysosomal cysteine proteases and its role in 2,2′-azobis-(2-amidinopropane)dihydrochloride (AAPH)-induced apoptosis in HL-60 cells. J. Biochem. 129:2001;35-41.
24. Jägel M., Lüllmann-Rauch R. Lipidosis-like alterations in cultured macrophages exposed to local anesthetics. Arch. Toxicol. 55:1984;229-232.
25. Joshi U.M., Rao P., Kodavanti S., Lockard V.G., Mehendale H.M. Fluorescence studies on binding of amphiphilic drugs to isolated lamellar bodies: relevance to phospholipidosis. Biochim. Biophys. Acta. 1004:1989;309-320.
26. Just M., Habermann E. The renal handling of polybasic drugs. 2. In vitro studies with brush border and lysosomal preparations. Arch. Pharmacol. 25:1977;67-76.
27. Kint J.A., Dacremont G., Carton D., Orye E., Hooft C. Mucopolysaccharidosis: secondarily-induced abnormal distribution of lysosomal isoenzymes. Science. 181:1973;352-354.
28. Kishore B.K., Fuming L., Maldague P., Tulkens P.M., Courtoy P.J. Mechanisms of the thesaurismosis and altered lysosomal dynamics induced by poly-D-glutamic acid in kidney proximal tubular cells. Lab. Invest. 74:1996;1025-1037.
29. Kodavanti U.P., Mehendale H.M. Cationic amphiphilic drugs and phospholipid storage disorder. Pharmacol. Rev. 42:1990;327-353.
30. Lau C.E., Sun L. The pharmacokinetic determinants of the frequency and pattern of intravenous cocaine self-administration in rats by pharmacokinetic modeling. Drug Metab. Dispos. 30:2002;2524-2561.
31. Laurent G., Carlier M.B., Rollman B., Van Hoof F., Tulkens P.M. Mechanism of aminoglycoside-induced lysosomal phospholipidosis: in vitro and in vivo studies with gentamycin and amikacin. Biochem. Pharmacol. 31:1982;3861-3870.
32. Leighton F., Poole B., Beaufay H., Baudhuin P., Coffey J.W., Fowler S., de Duve C. The large-scale separation of peroxisomes, mitochondria, and lysosomes from the livers of rats injected with triton WR-1339. Improved isolation procedures, automated analysis, biochemical and morphological properties of fractions. J. Cell Biol. 37:1968;482-513.
33. Levade T., Salvayre R., Douste-Blazy L. Comparative hydrolysis of sphingomyelin and 2-N-(hexadecanoyl)-amino-4-nitrophenyl-phosphorylcholine by normal human brain homogenate at acid and neutral pH. J. Neurochem. 40:1983;1762-1764.
34. Li H., Jiang Y., Rajpurkar A., Dunbar J.C., Dhabuwala C.B. Cocaine induced apoptosis in rat testes. J. Urol. 162:1999;213-216.
35. Limet J.N., Quintart J., Schneider Y.-J., Courtoy P.J. Receptor-mediated endocytosis of polymeric IgA and galactosylated serum albumin in rat liver. Evidence for intracellular ligand sorting and identification of distinct endosomal compartments. Eur. J. Biochem. 146:1985;539-548.
36. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:1951;265-275.
37. Lüllmann-Rauch R. Drug-induced lysosomal storage disorders. Dingle J.T., Jacques P.J., Shaw L.H. Lysosomes in Applied Biology and Therapeutics. 1979;49-130 North-Holland Publ. Co, Amsterdam.
38. Maxfield F.R. Weak bases and ionophores rapidly and reversibly raise the pH of endocytic vesicles in cultured mouse fibroblasts. J. Cell Biol. 95:1982;676-681.
39. Mingeot-Leclercq M.P., Laurent G., Tulkens P. Biochemical mechanism of aminoglycoside-induced inhibition of phosphatidylcholine hydrolysis by lysosomal phospholipases. Biochem. Pharmacol. 37:1988;591-599.
40. Moestrup S.K., Cui S., Vorum H., Bregengard C., Bjorn S.E., Norris K., Gliemann J., Christensen E.I. Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs. J. Clin. Invest. 96:1995;1404-1413.
41. Montenez J.P., Kishore B.K., Maldague P., Tulkens P.M. Leupeptin and E-64, inhibitors of cysteine proteinases, prevent gentamicin-induced lysosomal phospholipidosis in cultured rat fibroblasts. Toxicol. Lett. 73:1994;201-208.
42. Montenez J.P., Delaissé J.M., Tulkens P.M., Koshore B.K. Increased activities of cathepsin B and other lysosomal hydrolases in fibroblasts and bone tissue cultured in the presence of cysteine proteinase inhibitors. Life Sci. 55:1994;1199-1208.
43. Montenez J.P., Van Bambeke F., Piret J., Brasseur R., Tulkens P.M., Mingeot-Leclercq M.P. Interactions of macrolide antibiotics (erythromycin A, roxithromycin, erythromycylamine [dirithromycin], and azithromycin) with phospholipids: computer-aided conformational analysis and studies on acellular and cell culture models. Toxicol. Appl. Pharmacol. 156:1999;129-140.
44. Nassogne M.C., Evrard P., Courtoy P.J. Selective neuronal toxicity of cocaine in embryonic mouse brain cocultures. Proc. Natl. Acad. Sci. U.S.A. 92:1995;11029-11033.
45. Nassogne M.C., Louahed J., Evrard P., Courtoy P.J. Cocaine induces apoptosis in cortical neurons of fetal mice. J. Neurochem. 58:1997;2442-2450.
46. Neufeld E.F., Sando G.N., Garvin A.J., Rome L.H. The transport of lysosomal enzymes. J. Supramol. Struct. 6:1977;95-101.
47. Ohkuma S., Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. U.S.A. 75:1978;3327-3331.
48. Reasor M.J., Kacew S. Drug-induced phospholipidosis: are there functional consequences? Proc. Soc. Exp. Biol. Med. 226:2001;825-830.
49. Rouser G., Fleischer S., Yamamoto A. Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids. 5:1970;494-496.
50. Ruben Z., Anderson S.N., Kacew S. Changes in saccharide and phospholipid content associated with drug storage in cultured rabbit aorta muscle cells. Lab. Invest. 64:1991;574-584.
51. Sun L., Lau C.E. Simultaneous pharmacokinetic modeling of cocaine and its metabolites, norcocaine and benzoylecgonine, after intravenous and oral administration in rats. Drug Metab. Dispos. 29:2001;1183-1189.
52. Tartakoff A.M. Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell. 32:1983;1026-1028.
53. Tulkens P., Beaufay H., Trouet A. Analytical fractionation of homogenates from cultured rat embryo fibroblasts. J. Cell Biol. 63:1974;383-401.
54. Veithen A., Cupers P., Baudhuin P., Courtoy P.J. v-Src induces constitutive macropinocytosis in rat fibroblasts. J. Cell Sci. 109:1996;2005-2012.
55. Wibo M., Poole B. Protein degradation in cultured cells. II. The uptake of chloroquine by rat fibroblasts and the inhibition of cellular protein degradation and cathepsin B1. J. Cell Biol. 63:1974;430-440.
56. Wu Y.B., Shen M.L., Gu G.G., Anderson K.M., Ou D.W. The effects of cocaine injections on mouse thymocytes population. Proc. Soc. Exp. Biol. Med. 214:1997;173-179.
57. Xia Z., Ying G., Hansson A.L., Karlsson H., Xie Y., Bergstrand A., DePierre J.W., Nässberger L. Antidepressant-induced lipidosis with special reference to tricyclic compounds. Prog. Neurobiol. 60:2000;501-512.
58. Zaragoza A., Diez-Fernandez C., Alvarez A.M., Andres D., Cascales M. Effect of N-acetylcysteine and deferoxamine on endogenous antioxidant defense system gene expression in a rat hepatocytes model of cocaine cytotoxicity. Biochim. Biophys. Acta. 1496:2000;183-195.