Drug, enzyme and peptide delivery using erythrocytes as carriers

Journal of Controlled Release

Volumn 95, Issue 1, 2004, Pages 27-49

  Millán, Carmen Gutiérrez ^a   Marinero, María Luisa Sayalero ^a   Castañeda, Aránzazu Zarzuelo ^a   Lanao, José M ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Applications; Carrier erythrocytes; Drugs; Enzymes; Peptides

Indexed keywords

ALCOHOLS; ANTIBIOTICS; CONTAMINATION; DIALYSIS; ENCAPSULATION; ENZYMES;

RETICULO-ENDOTHELIAL SYSTEMS (RES);

DRUG INFUSION;

AMINOGLYCOSIDE ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; ANTINEOPLASTIC AGENT; ANTIOXIDANT; ANTISENSE OLIGONUCLEOTIDE; BLEOMYCIN; CARBOPLATIN; CORTICOSTEROID; DACTINOMYCIN; DAUNORUBICIN; DEXAMETHASONE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DOXORUBICIN; DRUG CARRIER; ENALAPRILAT; ENZYME; ETOPOSIDE; FLUDARABINE; GENTAMICIN; GLUTARALDEHYDE; IMIDAZOLE DERIVATIVE; IMIDOCARB DIPROPIONATE; METHOTREXATE; METRONIDAZOLE; NALOXONE; NALTREXONE; NUCLEOSIDE ANALOG; PRIMAQUINE; UNINDEXED DRUG; ZIDOVUDINE;

ANTINEOPLASTIC ACTIVITY; CELL COUNT; DIALYSIS; DRUG DELIVERY SYSTEM; DRUG RELEASE; DRUG TARGETING; DRUG TOXICITY; ELECTROPORATION; ENDOCYTOSIS; ERYTHROCYTE; HEMATOLOGICAL PARAMETERS; HUMAN; LIVER FUNCTION; MACROPHAGE; MORPHOLOGY; NONHUMAN; OSMOTIC FRAGILITY; PRIORITY JOURNAL; RETICULOENDOTHELIAL SYSTEM; REVIEW; SIDE EFFECT; SPLEEN FUNCTION;

EID: 0842309173     PISSN: 01683659     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jconrel.2003.11.018     Document Type: Review

References (174)

1. Hillman R.S., Finch C.A. Red Cell Manual. 1996;F. A. Davis, Philadelphia.
2. West J.B. Physiological Basis of Medicine Practice. 1995;Panamericana, Buenos Aires.
3. Guyton A.C., Hall J.E., Saunders W.B. Red blood cells, anemia and polycitemia. 1996;Textbook of Medical Physiology, Philadelphia.
4. Bunn H.F. Erythrocyte destruction and hemoglobin catabolism. Semin. Hematol. 9:1972;317.
5. Sprandel U., Way L. Erythrocytes as Drug Carriers in Medicine. 1997;Plenum Press, New York and London.
6. Deloach J.R., Way J.L. Carrier and Bioreactor Red Blood Cells for Drug Delivery and Targeting. 1994;Elsevier, Tarry-town, NY.
7. Magnani M., Deloach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. 1992;Plenum, New York.
8. Talwar N., Jain N.K. Erythrocytes as carriers of metronidazole: in vitro characterization. Drug Dev. Ind. Pharm. 18(16):1992;1799-1812.
9. Grimaldi S., Lisi A., Pozzi D., Santoro N. Attempts to use liposomes and RBC ghosts as vectors and antisense therapy of virus infection. Res. Virol. 148:1997;177-180.
10. Chiarantini L., Droleskey R.E., DeLoach J.R. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;269-277.
11. Magnani M., Rossi L., Fraternale A., Bianchi M., Antonelli A., Crinelli R., Chiarantini L. Erythrocyte-mediated delivery of drugs, peptides and modified oligonucleotides. Gene Ther. 9(11):2002;749-751.
12. Hamidi M., Tajerzadeh H. Carrier erythrocytes: an overview. Drug Deliv. 10:2003;9-20.
13. Zocchi E., Tonetti M., Polvani C., Guida L., Benatti U., De Flora A. Encapsulation of doxorubicin in liver-targeted erythrocytes increases the therapeutic index of the drug in a murine metastitic model. Proc. Natl. Acad. Sci. U. S. A. 86:1989;2040-2044.
14. Gasparini A., Chiarantini L., Kirch H., DeLoach J.R. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;291-297.
15. Eichler H.G., Gasic S., Bauer K., Korn A., Bacher S. In vivo clearance of antibody-sensitized human drug carrier erythrocytes. Clin. Pharmacol. Ther. 40(3):1986;300-303.
16. Noel-Hocquet S., Jabbouri S., Lazar S., Maunier J.C., Guillaumet G., Ropars C. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;215-221.
17. Bax B.E., Bain M.D., Talbot P.J., Parker-Williams E.J., Chalmers R.A. Survival of human carrier erythrocytes in vivo. Clin. Sci. (Lond.). 96(2):1999;171-178.
18. Lynch W.E., Sartiano G.P., Chaffar A. Erytrocytes as carriers of chemotherapeutic agents for targeting the reticuloendothelial system. Am. J. Hematol. 9(3):1980;249-259.
19. Jain S., Jain N.K. Engineered erythrocytes as a drug delivery system. Indian J. Pharm. Sci. 59:1997;275-281.
20. Moss H.A., Tebbs S.E., Faroqui M.H., Herbst T., Isaac J.L., Brown J., Elliott T.S. A central venous catheter coated with benzalkonium chloride for the prevention of catheter-related microbial colonozation. Eur. J. Anaesthesiol. 17(11):2000;680-687.
21. Valbonesi M., Bruni R., Florio G., Zanella A., Bunkens H. Cellular contamination of plasma collected with various apheresis systems. Transfus. Apher. Sci. 24:2001;91-94.
22. Sugai Y., Sugai K., Fuse A. Current status of bacterial contamination of autologous blood for transfusion. Transfus. Apher. Sci. 24:2001;255-259.
23. Álvarez F.E., Lichtiger B. Bacterial contamination of cellular blood components. Curr. Issues Transfus. Med. 3(3):1995;. http://www.mdacc.tmc. edu/~citm/.
24. Magnani M., Rossi L., D'ascenzo M., Panzani I., Bigi L., Zanella A. Erythrocyte engineering for drug delivery and targeting. Biotechnol. Appl. Biochem. 28:1998;1-6.
25. Mishra P.R., Jain N.K. Biotinylated methotrexate loaded erythrocytes for enhanced liver uptake. "A study on the rat" Int. J. Pharm. 231(2):2002;145-153.
26. Kravtzoff R., Ropars C., Laguerre M., Muh J.P., Chassaigne M. Erythrocytes as carriers for L-asparaginase. Methodological and mouse in-vivo studies. J. Pharm. Pharmacol. 42(7):1990;473-476.
27. Hamidi M., Tajerzadeh H., Dehpour A.R., Ejtemaee-Mehr S. Inhibition of serum angiotensin-converting enzyme in rabbits after intravenous administration of enalaprilat-loaded intact erythrocytes. J. Pharm. Pharmacol. 53(9):2001;1281-1286.
28. Tonetti M., Astroff A.B., Satterfield W., De Flora A., Benatti U., DeLoach J.R. Pharmacokinetic properties of doxorubicin encapsulated in glutaraldehyde-treated canine erythrocytes. Am. J. Vet. Res. 52:1991;1630-1635.
29. Green R., Widder K.J. Methods in Enzymology. vol. 149:1987;221-229 Academic Press, San Diego.
30. DeLoach J.R., Ihler G. A dyalisis procedure for loading erythrocytes with enzymes and lipids. Biochim. Biophys. Acta. 496:1977;136-145.
31. el-Kalay M.A., Koochaki Z., Schutz P.W., Gaylor J.D. Efficient continuous flow washing of red blood cells for exogenous agent loading using a hollow fiber plasma separator. Artif. Organs. 13(6):1989;515-524.
32. Ihler G.M., Glew R.H., Schunure F.W. Enzyme loading of erythrocytes. Proc. Natl. Acad. Sci. U. S. A. 70:1973;2663-2666.
33. Dale G. Green R., Widder K.J. Methods in Enzymology. vol. 149:1987;229-234 Academic Press, San Diego.
34. Magnani M., Rossi L., Brandi G., Schiavano G.F., Montroni M., Piedimonte G. Targeting antiretroviral nucleoside analogues in phosphorylated form to macrophages: in vitro and in vivo studies. Proc. Natl. Acad. Sci. U. S. A. 89(14):1992;6477-6481.
35. Dale G., Villacorte D., Beutler E. High-yield entrapment of proteins into erythrocytes. Biochem. Med. 18:1977;220-225.
36. Tamura A., Tominaga N., Sato T., Fujii T. Preparation of human erythrocyte ghost having the membrane structure and properties similar to those of the intact cell. Yakuzaigaku. 48:1988;86-91.
37. Ito Y., Ogiso T., Iwaki M., Yoneda I., Okuda Y. In vitro stability of insulin-loaded erythrocytes after freezing storage. J. Pharmacobio-Dyn. 12:1989;201-207.
38. Jenner D.J., Lewis D.A., Pitt E., Offord R.A. The effect of intravenous administration of corticosteroids encapsulated in intact erythrocytes on adyuvant arthritis in the rat. Br. J. Pharmacol. 73:1981;212-213.
39. Franco R., Barker R., Weiner M. The nature and kinetics of red cell membrane changes during the osmotic pulse method of incorporating xenobiotics into viable red cells. Adv. Biosci. 67:1987;63-72. (series).
40. Mosca A., Paleari R., Russo V., Rosti E., Nano R., Boicelli A., Villa S., Zanella A. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;19-26.
41. Ropars C., Chassaigne M., Villereal M.C., Avenard G., Hurel C., Nicolau C. DeLoach J.R., Sprandel U. Red Blood Cells as Carriers for Drugs. 1985;82-91 Karger, Basel.
42. Green R., Miller J., Crosby W. Enhancement of iron chelation by desferrioxamine entrapped in red blood cell ghosts. Blood. 57(5):1981;866-872.
43. Ihler M.G., Chi-Wan Tsang H. Green R., Widder K.J. Methods in Enzymology. vol. 149:1987;221-229 Academic Press, San Diego.
44. Álvarez F.J., Jordan J.A., Herráez A., Díez J.C., Tejedor M.C. Hypotonically loaded rat erythrocytes deliver encapsulated substances into peritoneal macrophages. J. Biochem. 123:1998;233-239.
45. DeLoach J.R. Green R., Widder K.J. Methods in Enzymology. vol. 149:1987;235-242 Academic Press, San Diego.
46. DeLoach J.R., Peters S., Pinkard O., Glew R., Ihler G. Effect of glutaraldehyde on enzyme-loaded erythrocytes. Biochim. Biophys. Acta. 496:1977;507-515.
47. Sanz S., Lizano C., Luque J., Pinilla M. In vitro and in vivo study of glutamate dehydrogenase encapsulated into mouse erythrocytes by hypotonic dialysis procedure. Life Sci. 65(26):1999;2781-2789.
48. Franchetti P., Sheikha G.A., Cappellacci L., Marchetti S., Grifantini M., Balestra E., Perno C.F., Benatti U., Brandi G., Rossi L., Magnani M. A new acyclic heterodinucleotide active against Human Immunodeficiency Virus and Herpes Simplex Virus. Antivir. Res. 47:2000;149-158.
49. Rossi L., Serafini S., Cappellacci L., Balestra E., Brandi G., Schiviano G.F., Franchetti P., Grifantini M., Perno C.F., Magnani M. Erythrocyte-mediated delivery of a new homodinucleotide active against human immunodeficiency virus and herpes simplex virus. J. Antimicrob. Chemother. 47:2001;819-827.
50. Perno C.F., Santoro N., Balestra E., Aquaro S., Cenci A., Lazzarino G., Di Pierro D., Tavazzi B., Balzarini J., Garaci E., Grimaldi S., Calio R. Red blood cells mediated delivery of 9-(2-phosphonylmethoxyethyl)adenine to primary macrophages: efficiency metabolism and activity against human immunodeficiency virus or herpes simplex virus. Antivir. Res. 33(3):1997;153-164.
51. Ropars C., Avenard G., Chassaigne M. Green R., Widder K.J. Methods in Enzymology. vol. 149:1987;242-248 Academic Press, San Diego.
52. Corsi D., Galluzzi L., Crinelli R., Magnani M. Ubiquitin is conjugated to the cytoeskeletal protein α-spectrin in matures erythrocytes. J. Biol. Chem. 270(15):1995;8928-8935.
53. Sinauridze E.I., Vitvitsky V.M., Pichugin A.V., Zhabotinsky A.M., Ataullakhanov F.I. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;203-206.
54. Luque J., Garín M.I., Sanz S., Ropero P., Pinilla M. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;81-89.
55. Tonetti M., Zocchi E., Guida L., Polvani C., Benatti U., Biassoni P., Romei F., Guglielmi A., Aschele C., Sobrero A., De Flora A. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;307-317.
56. Franco R.S., Weiner M., Wagner K., Martelo O.J. Incorporation of inositol hexaphosphate into red blood cells mediated by dimethyl sulfoxide. Life Sci. 32:1983;2763-2768.
57. Santos N.C., Figueira-Coelho J., Saldanha C., Martins-Silva J. Biochemical, biophysical and haemorheological effects of dimethylsulphoxide on human erythrocyte calcium loading. Cell Calcium. 31(4):2002;183-188.
58. Garin M.I., López R.M., Sanz S., Pinilla M., Luque J. Erythrocytes as carriers for recombinant human erythropoietin. Pharm. Res. 13(6):1996;869-874.
59. DeLoach J.R., Sprandel U. Red Blood Cells as Carriers for Drugs. 1985;Karger, Basel.
60. Tsong T.Y. Electroporation of cell membranes. Biophys. J. 60:1991;297-306.
61. Lizano C., Sanz S., Luque J., Pinilla M. In vitro study of alcohol dehydrogenase and acetaldehyde dehydrogenase encapsulated into human erythrocytes by an electroporation procedure. Biochim. Biophys. Acta. 1425(2):1998;328-336.
62. Lizano C., Perez M.T., Pinilla M. Mouse erythrocytes as carriers for coencapsulated alcohol and aldehyde dehydrogenase obtained by electroporation in vivo survival rate in circulation, organ distribution and ethanol degradation. Life Sci. 68:2001;2001-2016.
63. Dong Q., Jin W. Monitoring diclofenac sodium in single human erythrocytes introduced by electroporation using capillary zone electrophoresis with electrochemical detection. Electrophoresis. 22(13):2001;2786-2792.
64. Haritou M., Yova D., Koutsouris D., Loukas S. Loading of intact rabbit erythrocytes with fluorophores and the enzyme pronase by means of electroporation. Clin. Hemorheol. Microcirc. 19(3):1988;205-217.
65. Mangal P.C., Kaur A. Electroporation of red blood cell membrane and its use as a drug carrier system. Indian J. Biochem. Biophys. 28(3):1991;219-221.
66. Ben-Bassat I., Bensch K.G., Schrier S.L. Drug-induced erythrocyte membrane internalization. J. Clin. Invest. 51(7):1972;1833-1844.
67. Matovcik L.M., Junga I.G., Schrier S.L. Drug-induced endocytosis of neonatal erythrocytes. Blood. 65(5):1985;1056-1063.
68. Schrier S.L., Zachowski A., Devaux P.F. Mechanisms of amphipath-induced stomatocytosis in human erythrocytes. Blood. 79(3):1992;782-786.
69. Tonetti M., Polvani C., Zocchi E., Guida L., Benatti U., Biassoni P., Romei F., Guglielmi A., Aschele C., Sobrero A.et al. Liver targeting of autologous erythrocytes loaded with doxorubicin. Eur. J. Cancer. 27(7):1991;947-948.
70. Ataullakhanov F.I., Vitvitsky V.M., Kovaleva V.L., Mironova S.B. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;209-213.
71. Gasparini A., Tonetti M., Astroff B., Rowe L., Satterfield W., Schmidt R., DeLoach J.R. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;299-304.
72. Jordan J.A., Álvarez F.J., Lotero L.A., Herráez A., Díez J.C., Tejedor M.C. In vitro phagocytosis of carrier mouse red blood cells is increased by Band 3 cross-linking or diamide treatment. Biotechnol. Appl. Biochem. 34(3):2001;143-149.
73. Lotero L.A., Jordan J.A., Olmos G., Álvarez F.J., Tejedor M.C., Díez J.C. Differential in vitro and in vivo behaviour of mouse ascorbate/Fe3+ and diamide oxidized erythrocytes. Biosci. Rep. 21(6):2001;857-871.
74. Mishra P.R., Jain N.K. Surface modified methotrexate loaded erythrocytes for enhanced macrophage uptake. J. Drug Target. 8(4):2000;217-224.
75. Murciano J.C., Muzykantov V.R., Hernández A. Sprandel U., Way J.L. Erythrocytes as drug carriers in medicine. 1997;93-99 Plenum Press, New York.
76. Castellana M.A., De Renzis M.R., Piccinini G., Mianetti G., Seppi C., Balduini C., Brovelli A. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;91-99.
77. De Flora A., Benatti U., Guida L., Zocchi E. Encapsulation of Adriamycin in human erythrocytes. Proc. Natl. Acad. Sci. 83:1986;7029-7033.
78. Pitt E., Johnson C.M., Lewis D.A. Encapsulation of drugs in intact erythrocytes: an intravenous delivery system. Biochem. Pharmacol. 32(22):1983;3359-3368.
79. Eichler H.C., Gasic S., Daum B., Bacher S., Steger G. In vitro drug release from human carrier erythrocytes. Adv. Biosci. 67:1987;11-15. (series).
80. Krantz A. Red-cell mediated therapy: opportunities and challenges. Blood Cells Mol. Diseases. 23(3):1997;58-68.
81. Hamidi M., Tajerzadeh H., Dehpour A.R., Rouini M.R., Ejtemaee-Mehr S. In vitro characterization of human intact erythrocytes loaded by enalaprilat. Drug Deliv. 8(4):2001;223-230.
82. Tonetti M., Gasparini A., Giovine M., Bini D., Mazzucotelli A., De Paz F., Benatti U., De Flora A. Interaction of carboplatin with carrier human erythrocytes. Biotechnol. Appl. Biochem. 15(3):1992;267-277.
83. Álvarez F.J., Herráez A., Murciano J.C., Jordan J.A., Díez J.C., Tejedor M.C. In vivo survival and organ uptake of loaded carrier rat erythrocytes. J. Biochem. (Tokyo). 120(2):1996;286-291.
84. Ogiso T., Iwaki M., Ohtori A. Encapsulation of dexamethasone in rabbit erythrocytes, the disposition in circulation and anti-inflammatory effect. J. Pharmacobio-dyn. 8(12):1985;1032-1040.
85. Magnani M., Bianchi M., Rossi L., Stocchi V. Human red blood cells as bioreactors for the release of 2′,3′-dideoxycytidine, an inhibitor of HIV infectivity. Biochem. Biophys. Res. Commun. 164(1):1989;446-452.
86. Tonetti M., Astroff B., Satterfield W., De Flora A., Benatti U., DeLoach J.R. Construction and characterization of adriamycin-loaded canine red blood cells as a potential slow delivery system. Biotechnol. Appl. Biochem. 12(6):1990;621-629.
87. Benatti U., Giovine M., Damonte G., Gasparini A., Scarfi S., De Flora A., Fraternale A., Rossi L., Magnani M. Azidothymidine homodinucleotide-loaded erythrocytes and bioreactors for slow delivery of the antiretroviral drug azidothymidine. Biochem. Biophys. Res. Commun. 220(1):1996;20-25.
88. Ihler G.M., Tsang H.C. Erythrocyte carriers. Crit. Rev. Ther. Drug Carr. Syst. 1(2):1985;155-187.
89. Leung P., Davis R.W., Yao C.C., Cannon E.P., Way J.L. Rhodanese and sodium thiosulfate encapsulated in mouse carrier erythrocytes: II. In vivo survivability and alterations in physiologic and morphologic characteristics. Fundam. Appl. Toxicol. 16(3):1991;559-566.
90. Houck K.S., Huang L. The role of multivalency in antibody mediated liposome targeting. Biochem. Biophys. Res. Commun. 145:1987;1205-1210.
91. Beretta E., Bischi G.I., Solimano F. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;247-253.
92. Beretta E., Solimano F. An optimal time control problem for the administration of 2′,3′-dideoxycytidine by using red blood cells as bioreactors. Bull. Math. Biol. 55(4):1993;715-730.
93. Beretta E., Solimano F., Takeuchi Y. A mathematical model for drug administration by using the phagocytosis of red blood cells. J. Math. Biol. 35(1):1996;1-19.
94. Kruse C.A., Freehauf C.L., Patel K.R., Baldeschwieler J.D. Mouse erythrocyte carriers osmotically loaded with methotrexate. Biotechnol. Appl. Biochem. 9(2):1987;123-140.
95. Zocchi E., Tonetti M., Polvani C., Guida L., Benatti U., De Flora A. In vivo liver and lung targeting of adriamycin encapsulated in glutaraldehyde- treated murine erythrocytes. Biotechnol. Appl. Biochem. 10(6):1988;555-562.
96. DeLoach J.R., Barton C. Glutaraldehyde-treated carrier erythrocytes for organ targeting of methotrexate in dogs. Am. J. Vet. Res. 42(11):1981;1971-1974.
97. Lynch W.E., Sartiano G.P., Rosenblum S.L., Calkins J.H., Ramsey C.B. The use of erythrocytes for delivery of chemotherapeutic agents to the reticuloendothelial system. Bibl. Haematol. (51):1985;42-49.
98. Mishra P.R., Jain N.K. Reverse biomembrane vesicles for effective controlled delivery of doxorubicin HCl. Drug Deliv. 7(3):2000;155-159.
99. Benatti U., Zocchi E., Tonetti M., Guida L., Polvani C., De Flora A. Enhanced antitumor activity of adriamycin by encapsulation in mouse erythrocytes targeted to liver and lungs. Pharmacol. Res. 21(2):1989;27-33.
100. Kitao T., Hattori K. Erythrocyte entrapment of daunomycin by amphotericin B without hemolysis. Cancer Res. 40(4):1980;1351-1353.
101. Lotero L.A., Olmos G., Díez J.C. Delivery to macrophages and toxic action of etoposide carried in mouse red blood cells. Biochim. Biophys. Acta. 17(1-3):2003;160-166.
102. Tajerzadeh H., Hamidi M. Evaluation of hypotonic preswelling method for encapsulation of enalaprilat in intact human erythrocytes. Drug Dev. Ind. Pharm. 26(12):2000;1247-1257.
103. Eichler H.G., Rameis H., Bauer K., Korn A., Bacher S., Gasic S. Survival of gentamicin-loaded carrier erythrocytes in healthy human volunteers. Eur. J. Clin. Investig. 16(1):1986;39-42.
104. Talwar N., Jain N.K. Erythrocyte based delivery system of primaquine: in vitro characterization. J. Microencapsul. 9(3):1992;357-364.
105. DeLoach J.R. Encapsulation potential of a trypanocidal drug homidium bromide in bovine carrier erythrocytes. Res. Exp. Med. (Berl.). 185(5):1985;345-353.
106. DeLoach J.R., Wagner G.G., Corrier D.E. Pharmacokinetics of imidocarb dipropionate encapsulated in carrier erythrocytes and use of carrier cells for babesiosis chemotherapy. J. Control. Release. 9(3):1989;243-248.
107. Rossi L., Serafini S., Cenerini L., Picardi F., Bigi L., Panzani I., Magnani M. Erythrocyte-mediated delivery of dexamethasone in patients with chronic obstructive pulmonary disease. Biotechnol. Appl. Biochem. 33(2):2001;85-89.
108. Bonomo R.P., De Flora A., Rizzarelli E., Santoro A.M., Tabbi G., Tonetti M. Copper (II) complexes encapsulated in human red blood cells. J. Inorg. Biochem. 59(4):1995;773-784.
109. Magnani M., Laguerre M., Rossi L., Bianchi M., Ninfali P., Mangani F., Ropars C. Acetaldehyde dehydrogenase-loaded erythrocytes as bioreactors for the removal of blood acetaldehyde. Alcohol., Clin. Exp. Res. 13(6):1989;849-852.
110. Magnani M., Laguerre M., Rossi L., Bianchi M., Ninfali P., Mangani F., Ropars C. In vivo accelerated acetaldehyde metabolism using acetaldehyde dehydrogenase-loaded erythrocytes. Alcohol. 25(6):1990;627-637.
111. Ninfali P., Rossi L., Baronciani L., Ropars C., Magnani M. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;165-173.
112. Ninfali P., Rossi L., Baronciani L., Tirillini B., Ropars C., Magnani M. Acetaldehyde, ethanol and acetone concentrations in blood of alcohol-treated mice receiving aldehyde dehydrogenase-loaded erythrocytes. Alcohol. 27(1):1992;19-23.
113. Magnani M., Fazi A., Magnani F., Rossi L., Mancini U. Methanol detoxification by enzyme-loaded erythrocytes. Biotechnol. Appl. Biochem. 18:1993;217-226.
114. Oettgen H.F., Old L.J., Boyse E.A., Campbell H.A., Philips F.S., Clarkson B.D., Tallal L., Leeper R.D., Schwartz M.K., Kim J.H. Inhibition of leukaemia in man by L-asparaginase. Cancer Res. 27(12):1967;2619-2631.
115. Oettgen H.F., Stephenson P.A., Schwartz M.K., Leeper R.D., Tallai L., Tan C.C., Clarkson B.D., Golbey R.B., Krakoff I.H., Karnofsky D.A., Murphy M.L., Burchenal J.H. Toxicity of E. coli L-asparaginase in man. Cancer. 25(2):1970;253-278.
116. Updike S.J., Wakamiya R.T. Infusion of red blood cell-loaded asparaginase in monkey. Immunologic, metabolic and toxicologic consequences. J. Lab. Clin. Med. 101(5):1983;679-691.
117. Updike S.J. Entrapment of L-asparaginase in red blood cells. A strategy to improve treatment of acute lymphoblastic leukaemia. Bibl. Haematol. (51):1985;65-74.
118. Alpar H.O., Lewis D.A. Therapeutic efficacy of asparaginase encapsulated in intact erythrocytes. Biochem. Pharmacol. 34(2):1985;257-261.
119. Naqi A., DeLoach J.R., Andrews K., Satterfield W., Keeling M. Determination of parameters for enzyme therapy using L-asparaginase entrapped in canine erythrocytes. Biotechnol. Appl. Biochem. 10(4):1988;365-372.
120. DeLoach J.R., Andrews K., Satterfield W., Keeling M. Intraperitoneal administration of carrier erythrocytes in dogs: an improved method for delivery of L-asparaginase. Biotechnol. Appl. Biochem. 12(3):1990;331-335.
121. Kravtzoff R., Desbois I., Lamagnere J.P., Muh J.P., Valat C., Chassaigne M., Colombat P., Ropars C. Improved pharmacodynamics of L-asparaginase-loaded in human red blood cells. Eur. J. Clin. Pharmacol. 49(6):1996;465-470.
122. Ihler G., Lantzy A., Purpura J., Glew R.H. Enzymatic degradation of uric acid by uricase-loaded human erythrocytes. J. Clin. Invest. 56(3):1975;595-602.
123. Magnani M., Mancini U., Bianchi M., Fazi A. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;189-194.
124. Ito Y., Ogiso T., Iwaki M., Atago H. Encapsulation of human urokinase in rabbit erythrocytes and its disposition in the circulation system in rabbits. J. Pharmacobio-dyn. 10:1987;550-556.
125. Rossi L., Bianchi M., Magnani M. Increased glucose metabolism by enzyme-loaded erythrocytes in vitro and in vivo normalization of hyperglycemia in diabetic mice. Biotechnol. Appl. Biochem. 15(2):1992;207-216.
126. Garin M., Rossi L., Luque J., Magnani M. Lactate catabolism by enzyme-loaded red blood cells. Biotechnol. Appl. Biochem. 22(3):1995;295-303.
127. Adriaenssens K., Karcher D., Lowenthal A., Terheggen H.G. Use of enzyme-loaded erythrocytes in in-vitro correction of arginase-deficient erythrocytes in familial hyperargininemia. Clin. Chem. 22(3):1976;323-326.
128. Adriaenssens K., Karcher D., Marescau B., Van Broeckhoven A., Terheggen H.C. Hyperargininemia: the rat as a model for the human disease and the comparative response to enzyme replacement therapy with free arginase and arginase loaded erythrocytes in vivo. Int. J. Biochem. 16(7):1984;779-786.
129. Petrikovics I., Pei L., McGuinn W.D., Cannon E.P., Way J.L. Encapsulation of rhodanese and organic thiosulfonates by mouse erythrocytes. Fundam. Appl. Toxicol. 23(1):1994;70-75.
130. Pei L., McGuinn W.D., Omburo G., Zitzer A.H., Petrikovics I., Way J.L. Spectrophotometric determination of paraoxonase within mouse carrier red blood cells. Biotechnol. Appl. Biochem. 20(1):1994;35-41.
131. Pei L., Omburo G., McGuinn W.D., Petrikovics I., Dave K., Raushel F.M., Wild J.R., DeLoach J.R., Way J.L. Encapsulation of phosphotriesterase within murine erythrocytes. Toxicol. Appl. Pharmacol. 124(2):1994;296-301.
132. Bustos N.L., Batlle A.M. Enzyme replacement therapy in porphyrias: V. In vivo correction of delta-aminolaevulinate dehydratase defective in erythrocytes in lead intoxicated animals by enzyme-loaded red blood cell ghosts. Drug Des. Deliv. 5(2):1989;125-131.
133. Hamarat Baysal S., Uslan A.H. Encapsulation of PEG-urease/PEG-AlaDH enzyme system in erythrocyte. Artif. Cells Blood Substit. Immobil. Biotechnol. 29(5):2001;405-412.
134. Hamarat Baysal S., Uslan A.H. In vitro study of urease/AlaDH enzyme system encapsulated into human erythrocytes and research into its medical applications. Artif. Cells Blood Substit. Immobil. Biotechnol. 30(1):2002;71-77.
135. Bax B.E., Bain M.D., Fairbanks L.D., Webster A.D., Chalmers R.A. In vitro and in vivo studies with human carrier erythrocytes loaded with polyethylene glycol-conjugated and native adenosine deaminase. Br. J. Haematol. 109(3):2000;549-554.
136. Bax B.E., Bain M.D., Fairbanks L.D., Simmonds H.A., Webster A.D., Chalmers R.A. Carrier erythrocyte entrapped adenosine deaminase therapy in adenosine deaminase deficiency. Adv. Exp. Med. Biol. 486:2000;47-50.
137. Flynn G., Hackett T.J., McHale L., McHale A.P. Encapsulation of the thrombolytic enzyme, brinase, in photosensitized erythrocytes: a novel thrombolytic system based on photodynamic activation. J. Photochem. Photobiol., B Biol. 26(2):1994;193-196.
138. Humphreys J.D., Ihler G. Enhanced stability of erythrocyte-entrapped glucocerebrosidase activity. J. Lab. Clin. Med. 96(4):1980;682-692.
139. Bax B.E., Bain M.D., Ward C.P., Fensom A.H., Chalmers R.A. The entrapment of mannose-terminated glucocerebrosidase (alglucerase) in human carrier erythrocytes. Biochem. Soc. Trans. 24(3):1996;441S.
140. Fraternale A., Casabianca A., Orlandi C., Cerasi A., Chiarantini L., Brandi G., Magnani M. Macrophage protection by addition of glutathione (GSH)-loaded erythrocytes to AZT and DDI in a murine AIDS model. Antivir. Res. 56(3):2002;263-272.
141. Fraternale A., Casabianca A., Tonelli A., Chiarantini L., Brandi G., Magnani M. New drug combinations for the treatment of murine AIDS and macrophage protection. Eur. J. Clin. Investig. 31(3):2001;248-252.
142. Fraternale A., Tonelli A., Casabianca A., Vallanti G., Chiarantini L., Schiavano G.F., Benatti U., De Flora A., Magnani M. Role of macrophage protection in the development of murine AIDS. J. Acquir. Immune Defic. Syndr. 21(2):1999;81-89.
143. Rossi L., Brandi G., Schiavano G.F., Balestra E., Millo E., Scarfi S., Damonte G., Gasparini A., Magnani M., Perno C.F., Benatti U., De Flora A. Macrophage protection against human immunodeficiency virus or herpes simplex virus by red blood cell-mediated delivery of a heterodinucleotide of azidothymidine and acyclovir. AIDS Res. Hum. Retrovir. 14(5):1998;435-444.
144. Fraternale A., Casabianca A., Rossi L., Chiarantini L., Schiavano G.F., Palamara A.T., Garaci E., Magnani M. Erythrocytes as carriers of reduced glutathione (GSH) in the treatment of retroviral infections. J. Antimicrob. Chemother. 52(4):2003;551-554.
145. Rossi L., Brandi G., Schiavano G.F., Scarfi S., Millo E., Damonte G., Benatti U., De Flora A., Magnani M. Heterodimer-loaded erythrocytes as bioreactors for slow delivery of the antiviral drug azidothymidine and the antimycobacterial drug ethambutol. AIDS Res. Hum. Retrovir. 15(4):1999;345-353.
146. Magnani M., Rossi L., Fraternale A., Silvotti L., Quintavalla F., Piedimonte G., Matteucci D., Baldinotti F., Bendinelli M. FIV infection of macrophages: in vitro and in vivo inhibition by dideoxycytidine 5′-triphosphate. Vet. Immunol. Immunopathol. 46(1-2):1995;151-158.
147. Nielsen P.E. Antisense peptide nucleic acids. Curr. Opin. Mol. Ther. 2(3):2000;282-287.
148. Chiarantini L., Cerasi A., Fraternale A., Andreoni F., Scari S., Giovine M., Clavarino E., Magnani M. Inhibition of macrophage iNOS by selective targeting of antisense PNA. Biochemistry. 41(26):2002;8471-8477.
149. Fraternale A., Rossi L., Magnani M. Encapsulation, metabolism and release of 2-fluoro-ara-AMP from human erythrocytes. Biochim. Biophys. Acta. 1291(2):1996;149-154.
150. De Flora A., Zocchi E., Guida L., Polvani C., Benatti U. Conversion of encapsulated 5-fluoro-2′-deoxyuridine 5′-monophosphate to the antineoplastic drug 5-fluoro-2′-deoxyuridine in human erythrocytes. Proc. Natl. Acad. Sci. U. S. A. 85(9):1988;3145-3149.
151. Garin M.I., López R.M., Luque J. Pharmacokinetic properties and in-vivo biological activity of recombinant human erythropoietin encapsulated in red blood cells. Cytokine. 9(1):1997;66-71.
152. Eichler H.G., Schneider W., Raberger G., Bacher S., Pabinger I. Erythrocytes as carriers for heparin. Preliminary in vitro and animal studies. Res. Exp. Med. (Berl.). 186(6):1986;407-412.
153. Feder R., Nehushtai R., Mor A. Affinity driven molecular transfer from erythrocyte membrane to target cells. Peptides. 22(10):2001;1683-1690.
154. Olmos G., Lotero L.A., Tejedor M.C., Díez J.C. Delivery to macrophages of interleukin 3 loaded in mouse erythrocytes. Biosci. Rep. 20(5):2000;399-410.
155. Polvani C., Gasparini A., Benatti U., De Flora A., Silvestri S., Volpini G., Nencioni L. Murine red blood cells as efficient carriers of three bacterial antigens for the production of specific and neutralizing antibodies. Biotechnol. Appl. Biochem. 14(3):1991;347-356.
156. Franco R.S., Weiner M., Wagner K., Martelo O.J. Incorporation of inositol hexaphosphate into red blood cells mediated by dimethyl sulfoxide. Life Sci. 32(24):1983;2763-2768.
157. Teisseire B., Ropars C., Villereal M.C., Nicolau C. Long-term physiological effects of enhanced O2 release by inositol hexaphosphate-loaded erythrocytes. Proc. Natl. Acad. Sci. U. S. A. 84(19):1987;6894-6898.
158. Bailleul C., Borrelly-Villereal M.C., Chassaigne M., Ropars C. Modification of partial pressure of oxygen (P50) in mammalian red blood cells by incorporation of an allosteric effector of haemoglobin. Biotechnol. Appl. Biochem. 11:1989;31-40.
159. Al-Achi A., Greenwood R., Walker B. Buccal administration of erythrocyte-ghosts-insulin in rats. J. Control. Release. 28(1-3):1994;267-268.
160. Vyas S.P., Talwar N., Karajgi J.S., Jain N.K. An erythrocyte based bioadhesive system for nasal delivery of propranolol. J. Control. Release. 23(3):1993;231-237.
161. Vyas S.P., Jain S.K. Preparation and in vitro characterization of a magnetically responsive ibuprofen-loaded erythrocytes carrier. J. Microencapsul. 11(1):1994;19-29.
162. Johnson K.M., Tao J.Z., Kennan R.P., Gore J.C. Gadolinium-bearing red cells as blood pool MRI contrast agents. Magn. Reson. Med. 40(1):1998;133-142.
163. Kravtzoff R., Urvoase E., Chambon C., Ropars C. Magnani M., DeLoach J.R. The Use of Resealed Erythrocytes as Carriers and Bioreactors. Advances in Experimental Medicine and Biology. vol. 326:1992;347-354.
164. Piatti E., Accorsi A., Piacentini M.P., Fazi A. Glucose 1,6-bisphosphate-overloaded erythrocytes: a strategy to investigate the metabolic role of the bisphosphate in red blood cells. Arch. Biochem. Biophys. 293(1):1992;117-121.
165. Magnani M., Rossi L., Bianchi M., Serafini G., Stocchi V. Red blood cell loading with hexokinase and hexokinase-inactivating antibodies. A new strategy for studying the role of enzymes in red cell metabolism and removal. Biomed. Biochim. Acta. 49(2-3):1990;S149-S153.
166. Miwa I., Fukatsu H., Toyoda Y., Okuda J. Anomeric preference of glucose utilization in human erythrocytes loaded with glucokinase. Biochem. Biophys. Res. Commun. 173(1):1990;201-207.
167. Magnani M., Rossi L., Bianchi M., Serafini G., Stocchi V. Human red blood cell loading with hexokinase-inactivating antibodies. An in vitro model for enzyme deficiencies. Acta Haematol. 82(1):1989;27-34.
168. Magnani M., Rossi L., Bianchi M., Fornaini G., Benatti U., Guida L., Zocchi E., De Flora A. Improved metabolic properties of hexokinase-overloaded human erythrocytes. Biochim. Biophys. Acta. 972(1):1988;1-8.
169. Fiorelli G., Ploner T., Berardi W., Manoussakis C. G6PD encapsulation and metabolic properties of loaded erythrocytes. Bibl. Haematol. 51:1985;57-64.
170. De Flora A., Guida L., Zocchi E., Tonetti M., Benatti U. Construction of glucose oxidase-loaded human erythrocytes: a model of oxidative cytotoxicity. Ital. J. Biochem. 35(5):1986;361-367.
171. Doxsey S.J., Sambrook J., Helenius A., White J. An efficient method for introducing macromolecules into living cells. J. Cell Biol. 101(1):1985;19-27.
172. Schlegel R.A., McEvoy L. Green R., Widder K.J. Methods in Enzymology. vol. 149:1987;293-300 Academic Press, San Diego.
173. Kruse C.A., Spector E.B., Cederbaum S.D., Wisnieski B.J., Popjak G. Microinjection of arginase into enzyme-deficient cells with the isolated glycoprotein of sendai virus as fusogen. Biochim. Biophys. Acta. 645:1981;339-345.
174. Wille W., Willecke K. Retention of purified proteins in resealed human erythrocyte ghosts and transfer by fusion into cultured murine cells. FEBS Lett. 65:1976;59-62.