Human erythrocytes as drug carriers: Loading efficiency and side effects of hypotonic dialysis, chlorpromazine treatment and fusion with liposomes

Journal of Controlled Release

Volumn 170, Issue 3, 2013, Pages 343-351

  Favretto, M E ^a   Cluitmans, J C A ^a   Bosman, G J C G M ^a   Brock, R ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Chlorpromazine; Drug delivery; Hypotonic dialysis; Liposomes; Red blood cells; Spleen mimicking device

Indexed keywords

AMINO ACIDS; BIOCOMPATIBILITY; BIOMATERIALS; CELLS; DAMAGE DETECTION; DEFORMATION; DIALYSIS; DRUG DELIVERY; DRUG INTERACTIONS; EFFICIENCY; ENZYMES; LIPOSOMES; MOLECULAR WEIGHT; PHYSIOLOGY;

CHLORPROMAZINE; DRUG DELIVERY SYSTEM; HUMAN ERYTHROCYTES; HUMAN RED BLOOD CELL; MORPHOLOGICAL CHANGES; PHYSIOLOGICAL LEVELS; RED BLOOD CELL; SPLEEN-MIMICKING DEVICE;

BLOOD;

BETA GALACTOSIDASE; CHLORPROMAZINE; HORSERADISH PEROXIDASE; LIPOSOME; PHOSPHATIDYLSERINE; XANTHINE OXIDASE;

ARTICLE; CELL MATURATION; DIALYSIS; DRUG DELIVERY SYSTEM; DRUG EXPOSURE; ERYTHROCYTE; HEMOLYSIS; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; PRIORITY JOURNAL;

CHLORPROMAZINE; DRUG DELIVERY; HYPOTONIC DIALYSIS; LIPOSOMES; RED BLOOD CELLS; SPLEEN-MIMICKING DEVICE;

ANTIPSYCHOTIC AGENTS; BETA-GALACTOSIDASE; CHLORPROMAZINE; DIALYSIS; DRUG CARRIERS; ERYTHROCYTES; FLUORESCENT DYES; HEMOLYSIS; HORSERADISH PEROXIDASE; HUMANS; HYPOTONIC SOLUTIONS; PHOSPHATIDYLSERINES; RHODAMINES; XANTHINE OXIDASE;

EID: 84885124629     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.05.032     Document Type: Article

References (37)

1. J. Deloach, G. Ihler, A dialysis procedure for loading erythrocytes with enzymes and lipids, Biochim. Biophys. Acta 496 (1977) 136-145. (Pubitemid 8015396)
2. M. Delcea, N. Sternberg, A.M. Yashchenok, R. Georgieva, H. Baumler, H. Mohwald, A.G. Skirtach, Nanoplasmonics for dual-molecule release through nanopores in the membrane of red blood cells, ACS Nano 6 (2012) 4169-4180.
3. T.A. Kolesnikova, A.G. Skirtach, H. Mohwald, Red blood cells and polyelectrolyte multilayer capsules: natural carriers versus polymer-based drug delivery vehicles, Expert Opin. Drug Deliv. 10 (2013) 47-58.
4. V.R. Muzykantov, Drug delivery by red blood cells: vascular carriers designed by mother nature, Expert Opin. Drug Deliv. 7 (2010) 403-427.
5. L. Rossi, S. Serafini, F. Pierige, A. Antonelli, A. Cerasi, A. Fraternale, L. Chiarantini, M. Magnani, Erythrocyte-based drug delivery, Expert Opin. Drug Deliv. 2 (2005) 311-322. (Pubitemid 41130885)
6. Y. Godfrin, F. Horand, R. Franco, E. Dufour, E. Kosenko, B.E. Bax, A. Banz, O.A. Skorokhod, J.M. Lanao, V. Vitvitsky, E. Sinauridze, V. Bourgeaux, K.C. Gunter, International seminar on the red blood cells as vehicles for drugs, Expert. Opin. Biol. Ther. 12 (2012) 127-133.
7. C. Domenech, X. Thomas, S. Chabaud, A. Baruchel, F. Gueyffier, F. Mazingue, A. Auvrignon, S. Corm, H. Dombret, P. Chevallier, C. Galambrun, F. Huguet, F. Legrand, F. Mechinaud, N. Vey, I. Philip, D. Liens, Y. Godfrin, D. Rigal, Y. Bertrand, l-asparaginase loaded red blood cells in refractory or relapsing acute lymphoblastic leukaemia in children and adults: results of the GRASPALL 2005-01 randomized trial, Br. J. Haematol. 153 (2011) 58-65.
8. D. Shemin, D. Rittenberg, The life span of the human red blood cell, J. Biol. Chem. 166 (1946) 627-636.
9. A. Allen, E. Ponder, The measurement of the diameter of erythrocytes by the diffraction method, J. Physiol. 66 (1928) 37-48.
10. J.A. Chasis, M. Prenant, A. Leung, N. Mohandas, Membrane assembly and remodeling during reticulocyte maturation, Blood 74 (1989) 1112-1120. (Pubitemid 19210032)
11. F. Kamena,B. Monnanda,D. Makou, S. Capone,K. Patora-Komisarska,D. Seebach, On the mechanism of eukaryotic cell penetration by alpha- and beta-oligoarginines-targeting infected erythrocytes, Chem. Biodivers. 8 (2011) 1-12.
12. N. Sternberg, R. Georgieva, K. Duft, H. Baumler, Surface-modified loaded human red blood cells for targeting and delivery of drugs, J. Microencapsul. 29 (2012) 9-20.
13. N. Mohandas, J.A. Chasis, Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids, Semin. Hematol. 30 (1993) 171-192. (Pubitemid 23216313)
14. M.H.A.M. Fens, R. van Wijk, G. Andringa, K.L. van Rooijen, H.M. Dijstelbloem, J.T. Rasmussen, K.M.K. de Vooght, R.M. Schiffelers, C.A.J.M. Gaillard, W.W. van Solinge, A role for activated endothelial cells in red blood cell clearance: implications for vasopathology, Haematologica 97 (2012) 500-508.
15. M. Ghashghaeinia, J.C.A. Cluitmans, A. Akel, P. Dreischer, M. Toulany, M. Koberle, Y. Skabytska, M. Saki, T. Biedermann, M. Duszenko, F. Lang, T. Wieder, G.J.C.G.M. Bosman, The impact of erythrocyte age on eryptosis, Br. J. Haematol. 157 (2012) 606-614.
16. F.A. Kuypers, K.de Jong, The roleofphosphatidylserine in recognition and removal of erythrocytes, Cell Mol. Biol. (Noisy-le-grand) 50 (2004) 147-158.
17. A.J. Schroit, J.W. Madsen, Y. Tanaka, In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes, J. Biol. Chem. 260 (1985) 5131-5138. (Pubitemid 15031516)
18. A.S. Cornelius, M.P. Reilly, M. Suzuki, T. Asakura, K. Horiuchi, The mechanism of chlorpromazine-induced red blood cell swelling, Gen. Pharmacol. 25 (1994) 205-210. (Pubitemid 24055435)
19. S.L. Schrier, I. Junga, Entry and distribution of chlorpromazine and vinblastine into human erythrocytes during endocytosis, Proc. Soc. Exp. Biol. Med. 168 (1981) 159-167. (Pubitemid 12221468)
20. J. Hinton, Psychotropic drugs, Postgrad. Med. J. 44 (1968) 286-296.
21. L.H. Wang, K.G. Rothberg, R.G. Anderson, Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation, J. Cell Biol. 123 (1993) 1107-1117. (Pubitemid 23352421)
22. J.Y. Chen, W.H. Huestis, Role of membrane lipid distribution in chlorpromazine-induced shape change of human erythrocytes, Biochim. Biophys. Acta 1323 (1997) 299-309. (Pubitemid 27065377)
23. G. Lim, H.W.M. Wortis, R. Mukhopadhyay, Stomatocyte-discocyte-echinocyte sequence of the human red blood cell: evidence for the bilayer-couple hypothesis from membrane mechanics, Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 16766-16769. (Pubitemid 36034047)
24. J.L. Holovati, M.I.C. Gyongyossy-Issa, J.P. Acker, Effects of trehalose-loaded liposomes on red blood cell response to freezing and post-thaw membrane quality, Cryobiology 58 (2009) 75-83.
25. E. Ducat, J. Deprez, A. Gillet, A. Noel, B. Evrard, O. Peulen, G. Piel, Nuclear delivery of a therapeutic peptide by long circulating pH-sensitive liposomes: benefits over classical vesicles, Int. J. Pharm. 420 (2011) 319-332.
26. Z. Vanic, S. Barnert, R. Suss, R. Schubert, Fusogenic activity of PEGylated pH-sensitive liposomes, J. Liposome Res. 22 (2012) 148-157.
27. G.J.C.G.M. Bosman, J.C.A. Cluitmans, Y.A.M. Groenen, J.M. Werre, F.L.A. Willekens, V.M.J. Novotny, Susceptibility to hyperosmotic stress-induced phosphatidylserine exposure increases during red blood cell storage, Transfusion 51 (2011) 1072-1078.
28. G. Deplaine, I. Safeukui, F. Jeddi, F. Lacoste, V. Brousse, S. Perrot, S. Biligui, M. Guillotte, C. Guitton, S. Dokmak, B. Aussilhou, A. Sauvanet, D. Cazals Hatem, F. Paye, M. Thellier, D. Mazier, G. Milon, N. Mohandas, O. Mercereau-Puijalon, P.H. David, P.A. Buffet, The sensing of poorly deformable red blood cells by the human spleen can be mimicked in vitro, Blood 117 (2011) e88-e95.
29. C.C. Widmer, C.P. Pereira, P. Gehrig, F. Vallelian, G. Schoedon, P.W. Buehler, D.J. Schaer, Hemoglobin can attenuate hydrogen peroxide-induced oxidative stress by acting as an antioxidative peroxidase, Antioxid. Redox Signal. 12 (2010) 185-198.
30. G.J.C.G.M. Bosman, F.L.A. Willekens, J.M. Werre, Erythrocyte aging: a more than superficial resemblance to apoptosis? Cell. Physiol. Biochem. 16 (2005) 1-8. (Pubitemid 41197082)
31. F.K. Alanazi, G.E.-D.I. Harisa, A. Maqboul, M. Abdel-Hamid, S.H. Neau, I.A. Alsarra, Biochemically altered human erythrocytes as a carrier for targeted delivery of primaquine: an in vitro study, Arch. Pharm. Res. 34 (2011) 563-571.
32. G. Brecher, M. Bessis, Present status of spiculed red cells and their relationship to the discocyte-echinocyte transformation: a critical review, Blood 40 (1972) 333-344.
33. N.N. Barvitenko, N.C. Adragna, R.E. Weber, Erythrocyte signal transduction pathways, their oxygenation dependence and functional significance, Cell. Physiol. Biochem. 15 (2005) 1-18.
34. G.V. Born, G.M. Housley, Effects of modification of the membranes of intact erythro-cytes on the anti-haemolytic action of chlorpromazine, Br. J. Pharmacol. 79 (1983) 481-487. (Pubitemid 13055417)
35. M.R. Lieber, Y. Lange, R.S. Weinstein, T.L. Steck, Interaction of chlorpromazine with the human erythrocyte membrane, J. Biol. Chem. 259 (1984) 9225-9234. (Pubitemid 14098910)
36. A. Akel, T. Hermle, O.M. Niemoeller, D.S. Kempe, P.A. Lang, P. Attanasio, M. Podolski, T. Wieder, F. Lang, Stimulation of erythrocyte phosphatidylserine exposure by chlorpromazine, Eur. J. Pharmacol. 532 (2006) 11-17.
37. K. Stebelska, P.M. Dubielecka, A.F. Sikorski, The effect of PS content on the ability of natural membranes to fuse with positively charged liposomes and lipoplexes, J. Membr. Biol. 206 (2005) 203-214. (Pubitemid 43199138)