Inward translocation of the phospholipid analogue miltefosine across caco-2 cell membranes exhibits characteristics of a carrier-mediated process

Lipids

Volumn 42, Issue 3, 2007, Pages 229-240

  Ménez, Cécile ^a   Buyse, Marion ^b   Farinotti, Robert ^b   Barratt, Gillian ^a  

^a UNIV PARIS SUD   (France)

^b IPSIT   (France)

Author keywords

Caco 2; Cellular membrane incorporation; Hexadecylphosphocholine; Intestinal absorption; Miltefosine; Translocation

Indexed keywords

ADENOSINETRIPHOSPHATE; CELL MEMBRANES; DISEASE CONTROL; DRUG DELIVERY; ENZYME KINETICS; PROTEINS;

EPITHELIAL CELLS; MILTEFOSINE; ORAL ABSORPTION; TRANSLOCATION; VISCERAL LEISHMANIASIS;

PHOSPHOLIPIDS;

ADENOSINE TRIPHOSPHATE; ALBUMIN; MILTEFOSINE; PHOSPHOLIPID DERIVATIVE;

APICAL MEMBRANE; ARTICLE; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL STRAIN CACO 2; CONTROLLED STUDY; DRUG ABSORPTION; DRUG DIFFUSION; DRUG TRANSPORT; ENERGY; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID RAFT; MICHAELIS MENTEN KINETICS; TEMPERATURE DEPENDENCE; VISCERAL LEISHMANIASIS;

BIOLOGICAL TRANSPORT; CACO-2 CELLS; CELL MEMBRANE; ENDOCYTOSIS; HUMANS; PHOSPHORYLCHOLINE; SUBCELLULAR FRACTIONS;

EID: 34247547842     PISSN: 00244201     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11745-007-3026-8     Document Type: Article

References (54)

1. Sundar S, Makharia A, More DK, Agrawal G, Voss A, Fischer C, Bachmann P, Murray HW (2000) Short-course of oral miltefosine for treatment of visceral leishmaniasis. Clin Infect Dis 31:1110-1113
2. Sundar S, Jha TK, Thakur CP, Engel J, Sindermann H, Fischer C, Junge K, Bryceson A, Berman J (2002) Oral miltefosine for Indian visceral leishmaniasis. N Engl J Med 347:1739-1746
3. Arnold B, Reuther R, Weltzien HU (1978) Distribution and metabolism of synthetic alkyl analogs of lysophosphatidylcholine in mice. Biochim Biophys Acta 530:47-55
4. Geilen CC, Wieder T, Haase A, Reutter W, Morre DM, Morre DJ (1994) Uptake, subcellular distribution and metabolism of the phospholipid analogue hexadecylphosphocholine in MDCK cells. Biochim Biophys Acta 1211:14-22
5. Hoffman DR, Hoffman LH, Snyder F (1986) Cytotoxicity and metabolism of alkyl phospholipid analogues in neoplastic cells. Cancer Res 46:5803-5809
6. Van Blitterswijk WJ, Hilkmann H, Storme GA (1987) Accumulation of an alkyl lysophospholipid in tumor cell membranes affects membrane fluidity and tumor cell invasion. Lipids 22:P820-P823
7. Dive C, Watson JV, Workman P (1991) Multiparametric flow cytometry of the modulation of tumor cell membrane permeability by developmental antitumor ether lipid SRI 62-834 in EMT6 mouse mammary tumor and HL-60 human promyelocytic leukemia cells. Cancer Res 51:799-806
8. Grunicke HH (1991) The cell membrane as a target for cancer chemotherapy. Eur J Cancer 27:281-284
9. Modolell M, Andreesen R, Pahlke W, Brugger U, Munder PG (1979) Disturbance of phospholipid metabolism during the selective destruction of tumor cells induced by alkyllysophospholipids. Cancer Res 39:4681-4686
10. Uberall F, Oberhuber H, Maly K, Zaknun J, Demuth L, Grunicke HH (1991) Hexadecylphosphocholine inhibits inositol phosphate formation and protein kinase C activity. Cancer Res 51:807-812
11. Powis G, Seewald MJ, Gratas C, Melder D, Riebow J, Modest EJ (1992) Selective inhibition of phosphatidylinositol phospholipase C by cytotoxic ether lipid analogues. Cancer Res 52:2835-2840
12. Kelley EE, Modest EJ, Burns CP (1993) Unidirectional membrane uptake of the ether lipid antineoplastic agent edelfosine by L1210 cells. Biochem Pharmacol 45:2435-2439
13. Bazill GW, Dexter TM (1990) Role of endocytosis in the action of ether lipids on WEHI-3B, HL60, and FDCP-mix A4 cells. Cancer Res 50:7505-7512
14. Hanson PK, Malone L, Birchmore J, Nichols J (2003) Lem3p is essential for the uptake and potency of alkylphosphocholine drugs, edelfosine and miltefosine. J Biol Chem 278:36041-36050
15. Perez-Victoria FJ, Gamarro F, Ouellette M, Castanys S (2003) Functional cloning of the miltefosine transporter. A novel P-type phospholipid translocase from Leishmania involved in drug resistance. J Biol Chem 278:49965-49971
16. Perez-Victoria FJ, Castanys S, Gamarro F (2003) Leishmania donovani resistance to miltefosine involves a defective inward translocation of the drug. Antimicrob Agents Chemother 47:2397-2403
17. Hidalgo IJ, Raub TJ, Borchardt RT (1989) Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96:736-749
18. Geilen CC, Samson A, Wieder T, Wild H, Reutter W (1992) Synthesis of hexadecylphospho[methyl-14C]-choline. J Labelled Compd Radiopharm 31:1071-1076
19. Eibl H, Woolley P (1988) A general synthetic method for enantiomerically pure ester and ether lysophospholipids. Chem Phys Lipids 47:63-68
20. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63
21. Decker T, Lohmann-Matthes ML (1988) A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 115:61-69
22. Ménez C, Buyse M, Chacun H, Farinotti R, Barratt G (2006) Modulation of intestinal barrier properties by miltefosine. Biochem Pharmacol 71:486-496
23. Diomede L, Colotta F, Piovani B, Re F, Modest EJ, Salmona M (1993) Induction of apoptosis in human leukemic cells by the ether lipid 1-octadecyl-2-methyl-rac-glycero-3-phosphocholine. A possible basis for its selective action. Int J Cancer 53:124-130
24. Garcia-Garcia E, Andrieux K, Gil S, Kim HR, Le Doan T, Desmaele D, d'Angelo J, Taran F, Georgin D, Couvreur P (2005) A methodology to study intracellular distribution of nanoparticles in brain endothelial cells. Int J Pharm 298:310-314
25. Galdiero M, Vitiello M, D'Isanto M, Peluso L (2001) Induction of tyrosine phosphorylated proteins in THP-1 cells by Salmonella typhimurium, Pasteurella haemolytica and Haemophilus influenzae porins. FEMS Immunol Med Microbiol 31:121-130
26. LeDoan T, Etore F, Tenu JP, Letourneux Y, Agrawal S (1999) Cell binding, uptake and cytosolic partition of HIV anti-gag phosphodiester oligonucleotides 3′-linked to cholesterol derivatives in macrophages. Bioorg Med Chem 7:2263-2269
27. Clarke BL, Weigel PH (1985) Recycling of the asialoglycoprotein receptor in isolated rat hepatocytes. ATP depletion blocks receptor recycling but not a single round of endocytosis. J Biol Chem 260:128-133
28. Mohandas N, Wyatt J, Mel SF, Rossi ME, Shohet SB (1982) Lipid translocation across the human erythrocyte membrane. Regulatory factors. J Biol Chem 257:6537-6543
29. Ménez C, Buyse M, Dugave C, Farinotti R, Barratt G (2006) Intestinal absorption of miltefosine: contribution of passive paracellular transport. Pharm Res (in press). http://dx.doi.org/10.1007/s11095-006-9170-7
30. Berkovic D, Fleer EA, Eibl H, Unger C (1992) Effects of hexadecylphosphocholine on cellular function. Prog Exp Tumor Res 34:59-68
31. Wolkers WF, Looper SA, Fontanilla RA, Tsvetkova NM, Tablin F, Crowe JH (2003) Temperature dependence of fluid phase endocytosis coincides with membrane properties of pig platelets. Biochim Biophys Acta 1612:154-163
32. Steinman RM, Silver JM, Cohn ZA (1974) Pinocytosis in fibroblasts. Quantitative studies in vitro. J Cell Biol 63:949-969
33. Trotter PJ, Storch J (1991) Fatty acid uptake and metabolism in a human intestinal cell line (Caco-2): comparison of apical and basolateral incubation. J Lipid Res 32:293-304
34. Chabot MC, Wykle RL, Modest EJ, Daniel LW (1989) Correlation of ether lipid content of human leukemia cell lines and their susceptibility to 1-O-octadecyl-2-O-methyl-rac-glycero-3-phosphocholine. Cancer Res 49:4441-4445
35. Diomede L, Bizzi A, Magistrelli A, Modest EJ, Salmona M, Noseda A (1990) Role of cell cholesterol in modulating antineoplastic ether lipid uptake, membrane effects and cytotoxicity. Int J Cancer 46:341-346
36. Heesbeen EC, Rijksen G, van Heugten HG, Verdonck LF (1995) Influence of serum levels on leukemic cell destruction by the ether lipid ET-18-OCH3. Leuk Res 19:417-425
37. Heesbeen EC, Verdonck LF, Haagmans M, van Heugten HG, Staal GE, Rijksen G (1993) Adsorption and uptake of the alkyllysophospholipid ET-18-OCH3 by HL-60 cells during induction of differentiation by dimethylsulfoxide. Leuk Res 17:143-148
38. Sundar S, Rosenkaimer F, Makharia MK, Goyal AK, Mandal AK, Voss A, Hilgard P, Murray HW (1998) Trial of oral miltefosine for visceral leishmaniasis. Lancet 352:1821-1823
39. Murota K, Storch J (2005) Uptake of micellar long-chain fatty acid and sn-2-monoacylglycerol into human intestinal Caco-2 cells exhibits characteristics of protein-mediated transport. J Nutr 135:1626-1630
40. Trotter PJ, Ho SY, Storch J (1996) Fatty acid uptake by Caco-2 human intestinal cells. J Lipid Res 37:336-346
41. Fleer EA, Berkovic D, Eibl H, Unger C (1993) Investigations on the cellular uptake of hexadecylphosphocholine. Lipids 28:731-736
42. Small GW, Strum JC, Daniel LW (1997) Characterization of an HL-60 cell variant resistant to the antineoplastic ether lipid 1-O-octadecyl-2- O-methyl-rac-glycero-3-phosphocholine. Lipids 32:715-723
43. Vogel U, Sandvig K, van Deurs B (1998) Expression of caveolin-1 and polarized formation of invaginated caveolae in Caco-2 and MDCK II cells. J Cell Sci 111(Pt 6):825-832
44. Storch J, Munder PG (1987) Increased membrane permeability for an antitumoral alkyl lysophospholipid in sensitive tumor cells. Lipids 22:813-819
45. Mollinedo F, Fernandez-Luna JL, Gajate C, Martin-Martin B, Benito A, Martinez-Dalmau R, Modolell M (1997) Selective induction of apoptosis in cancer cells by the ether lipid ET-18-OCH3 (Edelfosine): molecular structure requirements, cellular uptake, and protection by Bcl-2 and Bcl-X(L). Cancer Res 57:1320-1328
46. Zoeller RA, Layne MD, Modest EJ (1995) Animal cell mutants unable to take up biologically active glycerophospholipids. J Lipid Res 36:1866-1875
47. Fleer EA, Berkovic D, Unger C, Eibl H (1992) Cellular uptake and metabolic fate of hexadecylphosphocholine. Prog Exp Tumor Res 34:33-46
48. Kotting J, Marschner NW, Neumuller W, Unger C, Eibl H (1992) Hexadecylphosphocholine and octadecyl-methyl-glycero-3-phosphocholine: a comparison of hemolytic activity, serum binding and tissue distribution. Prog Exp Tumor Res 34:131-142
49. Santa-Rita RM, Santos Barbosa H, Meirelles MN, de Castro SL (2000) Effect of the alkyl-lysophospholipids on the proliferation and differentiation of Trypanosoma cruzi. Acta Trop 75:219-228
50. Ho SY, Storch J (2001) Common mechanisms of monoacylglycerol and fatty acid uptake by human intestinal Caco-2 cells. Am J Physiol Cell Physiol 281:C1106-1117
51. Rey Gomez-Serranillos I, Minones J Jr, Dynarowicz-Latka P, Minones J, Iribarnegaray E (2004) Miltefosine-Cholesterol interactions: a monolayer study. Langmuir 20:928-933
52. Van der Luit AH, Budde M, Ruurs P, Verheij M, Van Blitterswijk WJ (2002) Alkyl-lysophospholipid accumulates in lipid rafts and induces apoptosis via raft-dependent endocytosis and inhibition of phosphatidylcholine synthesis. J Biol Chem 277:39541-39547
53. Voelker DR (1990) Lipid transport pathways in mammalian cells. Experientia 46:569-579
54. Pomorski T, Herrmann A, Muller P, van Meer G, Burger K (1999) Protein-mediated inward translocation of phospholipids occurs in both the apical and basolateral plasma membrane domains of epithelial cells. Biochemistry 38:142-150