Drug delivery through phagocytosis of red blood cells

Transfusion Medicine and Hemotherapy

Volumn 31, Issue 2, 2004, Pages 92-101

  Serafini, S ^a   Rossi, L ^a   Antonelli, A ^a   Fraternale, A ^a   Cerasi, A ^a   Crinelli, R ^a   Chiarantini, L ^a   Schiavano, G F ^a   Magnani, M ^a  

^a UNIVERSITY OF URBINO   (Italy)

Author keywords

Drug targeting; Loaded erythrocytes; Macrophages

Indexed keywords

ACICLOVIR; ADEFOVIR; ADENINE DERIVATIVE; ANTIVIRUS AGENT; COMPLEMENT; COMPLEMENT COMPONENT C3B RECEPTOR; FC RECEPTOR; GLUCOCORTICOID; GLUTATHIONE; IMMUNOGLOBULIN G; NUCLEOTIDE DERIVATIVE; PEPTIDE; PROTEIN; RNA DIRECTED DNA POLYMERASE INHIBITOR; TENOFOVIR; ZIDOVUDINE;

CIRCULATION; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG HALF LIFE; DRUG TARGETING; ENDOCRINE DISEASE; ERYTHROCYTE; HUMAN; INFUSION; MACROPHAGE; MEMBRANE PERMEABILITY; METABOLIC DISORDER; MOLECULE; NONHUMAN; OPSONIZATION; PATHOGENESIS; PHAGOCYTOSIS; REVIEW; TOXICITY;

EID: 4444356205     PISSN: 16603796     EISSN: None     Source Type: Journal    
DOI: 10.1159/000078042     Document Type: Review

References (77)

1. Meijer DKF: Drug targeting with glycoproteins and other peptides carriers: An overview; in Gregoriadis G, McCormack B, Poste G (eds): Targeting of Drugs 4, Advances in System Constructs. New York, Plenum Press, 1994, pp 1-30.
2. Shastri VP: Non-degradable biocompatible polymers in medicine: Past, present and future. Curr Pharm Biotechnol 2003;4:331-337.
3. Dass CR: Liposome-mediated delivery of oligo-deoxynucleotides in vivo. Drug Deliv 2002;9:169-180.
4. Rossi L, Serafini S, Magnani M: Red blood cell loading: a selection of procedures; in Magnani M (ed): Erythrocyte Engineering for Drug Delivery and Targeting. New York, Landes Bioscience, 2003,pp 1-18.
5. De Loach JR: Encapsulation of exogenous agents in erythrocytes and the circulating survival of carrier erythrocytes. J Appl Biochem 1983;5:149-157.
6. De Loach JR, Sprandel U: Red Blood Cells as Carriers For Drugs. Basel, Karger, 1985.
7. De Flora A, Benatti U, Guida L, Zocchi E: Encapsulation of adriamycin in human erythrocytes. Proc Natl Acad Sci USA 1986;83:7029-7033.
8. Ropars C, Chassaigne M, Nicolau C: Red Blood Cells as Carriers for Drugs. Potential Therapeutic Applications. Oxford, Pergamon Press, 1987.
9. Rossi L, Brandi G, Schiavano GF, 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 Retroviruses 1999;15:345-353.
10. 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 1996;220:20-25.
11. 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 2001;33:85-89.
12. D'Ascenzo M, Antonelli A, Chiarantini L, Mancini U, Magnani M: Red blood cells as a glucocorticoids delivery system; in Sprandel U, Way JL (eds): Erythrocytes as Drug Carriers in Medicine. New York, Plenum Press, 1997, pp 81-88.
13. Magnani M, Rossi L, D'Ascenzo M, Panzani I, Bigi L, Zanella A: Erythrocyte engineering for drug delivery and targeting. Biotechnol Appl Biochem 1998;28:1-6.
14. Zimmermann U: Cellular drug-carrier system and their possible targeting: in Goldberg EP (ed): Targeted Drugs. New York, Wiley, 1983, pp 153-200.
15. Kay MM: Mechanism of removal of senescent cells by human macrophages in situ. Proc Natl Acad Sci USA 1975;72:3521-3525.
16. Kay MM, Tracey CM, Goodman JR, Cone JC, Bassel PS: Polypeptides immunologically related to band 3 are present in nucleated somatic cells. Proc Natl Acad Sci USA 1983;80:6882-6886.
17. Turrini F, Arese P, Yuan J, Low PS: Clustering of integral membrane proteins of the human erythrocyte membrane stimulates autologous IgG binding, complement deposition, and phagocytosis. J Biol Chem 1991;266:23611-23617.
18. Magnani M, Rossi L, Brandi G, Schiavano GF, Montoni M, Piedimonte G: Targeting antiretroviral nucleoside analogues in phosphorylated form to macrophages: In vitro and in vivo studies. Proc Natl Acad Sci USA 1992;89:6477-6481.
19. Chiarantini L, Rossi L, Fraternale A, Magnani M. Modulated red blood cell survival by membrane protein clustering. Mol Cell Biochem 1995;144:53-59.
20. Meltzer MS, Skillman DR, Gomatos PJ, Kalter DC, Gendelman HE: Role of mononuclear phagocytes in the pathogenesis of human immunodeficiency virus infection. Annu Rev Immunol 1990;8:169-194.
21. Meltzer MS, Nakamura M, Hansen BD, Turpin JA, Kalter DC, Gendelman HE: Macrophages as susceptible targets for HIV infection, persistent viral reservoirs in tissue, and key immunoregulatory cells that control levels of virus replication and extent of disease. AIDS Res Hum Retroviruses 1990;6:967-971.
22. Wu L, Morahan PS, Hendrzak JA, Eisenstein TK: Herpes simplex virus type 1 replication and IL-1 beta gene expression in mouse peritoneal macrophages activated in vivo by an attenuated Salmonella typhimurium vaccine or Corynebacterium parvum. Microb Pathog 1994;16:387-399.
23. Golden MP, Kim S, Hammer SM, Ladd EA, Schaffer PA, DeLuca N, Albrecht MA: Activation of human immunodeficiency virus by herpes simplex virus. J Infect Dis 1992;166:494-499.
24. Mitsuya H, Yarchoan R, Broder S: Molecular targets for AIDS therapy. Science 1990;249:1533-1544.
25. Mitsuya H, Yarchoan R, Kageyama S, Broder S: Targeted therapy of human immunodeficiency virus-related disease. FASEB J 1991;5:2369-2381.
26. Larder BA, Darby G, Richman DD: HIV with reduced sensitivity to zidovudine (AZT) isolated during prolonged therapy. Science 1989;243:1731-1734.
27. Gao Q, Gu ZX, Parniak MA, Li XG, Wainberg MA: In vitro selection of variants of human immunodeficiency virus type 1 resistant to 3′-azido-3′-deoxythymidine and 2′,3′-dideoxyinosine. J Virol 1992;66:12-19.
28. Perno CF, Yarchoan R, Cooney DA, Hartman NR, Gartner S, Popovic M, Hao Z, Gerrard TL, Wilson YA, Johns DG, Broder S: Inhibition of human immunodeficiency virus (HIV-1/HTLV-IIIBa-L) replication in fresh and cultured human peripheral blood monocytes/macrophages by azidothymidine and related 2',3'- dideoxynucleosides. J Exp Med 1988; 168:1111-1125.
29. Richman DD, Kornbluth RS, Carson DA: Failure of dideoxynucleosides to inhibit human immunodeficiency virus replication in cultured human macrophages. J Exp Med 1987;166:1144-1149.
30. Rossi L, Brandi G, Schiavano GF, Balestra E, Millo E, Scarfi S, Damonte G, Gasparini A, Magnani M, Perno CF, 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 Retroviruses 1998;14:435-444.
31. Rossi L, Serafini S, Cappellacci L, Balestra E, Brandi G, Schiavano GF, Franchetti P, Grifantini M, Perno CF, Magnani M: Erythrocyte-mediated delivery of a new homodinucleotide active against human immunodeficiency virus and herpes simplex virus. J Antimicrob Chemother 2001;47:819-827.
32. Franchetti P, Rossi L, Cappellacci L, Pasqualini M, Grifantini M, Balestra E, Forbici F, Perno CF, Serafini S, Magnani M: Inhibition of HIV-1 replication in macrophages by red blood cell-mediated delivery of a heterodinucleotide of azidothymidine and 9-(R)-2-(phosphono methoxypropyl) adenine. Antivir Chem Chemother 2001;12:151-159.
33. Franchetti P, Abu Sheikha G, Cappellacci L, Marchetti S, Grifantini M, Balestra E, Perno C, Benatti U, Brandi G, Rossi L, Magnani M: A new acyclic heterodinucleotide active against human immunodeficiency virus and herpes simplex virus. Antiviral Res 2000;47:149-158.
34. Magnani M, Casabianca A, Fraternale A, Brandi G, Gessani S, Williams R, Giovine M, Damonte G, De Flora A, Benatti U: Synthesis and targeted delivery of an azidothymidine homodinucleotide conferring protection to macrophages against retroviral infection. Proc Natl Acad Sci USA 1996;93:4403-4408.
35. Mulato AS, Cherrington JM: Anti-HIV activity of adefovir (PMEA) and PMPA in combination with antiretroviral compounds: In vitro analyses. Antiviral Res 1997;36:91-97.
36. Horton MA: Macrophages and related cells; in Horton MA (ed): Blood Cell Biochemistry. New York, Plenum Press, 1993, vol 5.
37. Beauparlant P, Hiscott J: Biological and biochemical inhibitors of the NF-kB/Rel proteins and cytokine synthesis. Cytokine Growth Factor Rev 1996;7:175-190.
38. Haskill S, Beg AA, Tompkins SM, Morris JS, Yurochko AD, Sampson-Johannes A, Mondal K, Ralph P, Baldwin AS Jr: Characterization of an immediate-early gene induced in adherent monocytes that encodes IkB-like activity. Cell 1991;65:1281-1289.
39. Peters, J: Proteasomes: Protein degradation machines of the cell. Trends Biochem Sci 1994;19:377-382.
40. Ciechanover A: The ubiquitin-proteasome proteolytic pathway. Cell 1994;79:13-21.
41. Barnes PJ, Karin M: Nuclear factor-kappaB: A pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 1997;336:1066-1071.
42. Tak PP, Firestein GS: NF-kB: A key role in inflammatory diseases. J Clin Invest 2001;107:7-11.
43. McEwan IJ, Wright AP, Gustafsson JA: Mechanism of gene expression by the glucocorticoid receptor: Role of protein-protein interactions. Bioessays 1997;19:153-160.
44. Ray A, Prefontaine KE: Physical association and functional antagonism between the p65 subunit of transcription factor NF-kb and the glucocorticoid receptor. Proc Natl Acad Sci USA 1994;91:752-756.
45. Crinelli R, Antonelli A, Bianchi M, Gentilini L, Scaramucci S, Magnani M: Selective Inhibition of NF-kb activation and TNF production in macrophages by red blood cell-mediated delivery of dexamethasone. Blood Cells Mol Dis 2000;26:211-222.
46. Dubiel W, Gordon C: Ubiquitin pathway: Another link in the polyubiquitin chain? Curr Biol 1999;9:R554-557.
47. Gregori L, Poosch MS, Cousins G, Chau V: A uniform isopeptide-linked multiubiquitin chain is sufficient to target substrates for degradation in ubiquitin-mediated proteolysis. J Biol Chem 1990;265:8354-8357.
48. Antonelli A, Crinelli R, Bianchi M, Cerasi A, Gentilini L, Serafini G, Magnani M: Efficient inhibition of macrophage TNF production upon targeted delivery of K48R ubiquitin. Br J Haematol 1999;104:475-481.
49. Nathan CF: Secretory products of macrophages. J Clin Invest 1987;79:319-326.
50. Bernard C, Szekely B, Philip I, Wollman E, Payen D, Tedgui A: Activated macrophages depress the contractility of rabbit carotids via an L-arginine/nitric oxide-dependent effector mechanism. Connection with amplified cytokine release. J Clin Invest 1992;89:851-860.
51. Goodwin DC, Landino LM, Marnett LJ: Effects of nitric oxide and nitric oxide-derived species on prostaglandin endoperoxide synthase and prostaglandin biosynthesis. FASEB J 1999;13:1121-1136.
52. Lyons CR, Orloff GJ, Cunningham JM: Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J Biol Chem 1992;267:6370-6374.
53. Nathan C: Nitric oxide as a secretory product of mammalian cells. FASEB J 1992;6:3051-3054.
54. Luss H, Nussler NC, Beger HG, Nussler AK: Expression and detection of inducible nitric oxide synthase in experimental models of inflammation. Methods 1996;10:51-60.
55. MacMicking J, Xie QW, Nathan C: Nitric oxide and macrophage function. Annu Rev Immunol 1997;15:323-350.
56. Miyasaka N, Hirata Y: Nitric oxide and inflammatory arthritides. Life Sci 1997;61:2073-2081.
57. Wilson KT, Ramanujam KS, Mobley HL, Musselman RF, James SP, Meltzer SJ: Helicobacter pylori stimulates inducible nitric oxide synthase expression and activity in a murine macrophage cell line. Gastroenterology 1996;111:1524-1533.
58. Giovine M, Gasparini A, Scarfì S, Damonte G, Sturla L, Millo E, Tonetti M, Benatti U: Synthesis and characterization of a specific peptide nucleic acid that inhibits expression of inducible NO synthase. FEBS Lett 1998;426:33-36.
59. Nielsen PE, Egholm M, Berg RH, Buchardt O: Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide. Science 1991;254:1497-1500.
60. Hanvey JC, Peffer NJ, Bisi JE, Thomson SA, Cadilla R, Josey JA, Ricca DJ, Hassman CF, Bonham MA, Au KG: Antisense and antigene properties of peptide nucleic acids. Science 1992;258: 1481-1485.
61. Nielsen PE: Peptide nucleic acids: On the road to new gene therapeutic drugs. Pharmacol Toxicol 2000;86:3-7.
62. Demidov VV, Potaman VN, Frank-Kamenetskii MD, Egholm M, Buchard O, Sonnichsen SH, Nielsen PE: Stability of peptide nucleic acids in human serum and cellular extracts. Biochem Pharmacol 1994;48:1309-1313.
63. Nielsen PE, Egholm M (eds): Peptide Nucleic Acids: Protocols and Applications. Wyrnondham, Horizon Scientific Press, 1999.
64. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the folin phenol agent. J Biol Chem 1951;193:265-275.
65. Mischiati C, Borgatti M, Bianchi N, Rutigliano C, Tomassetti M, Feriotto G, Gambari R: Interaction of the human NF-kappaB p52 transcription factor with DNA-PNA hybrids mimicking the NF-kappaB binding sites of the human immunodeficiency virus type 1 promoter. J Biol Chem 1999;274:33114-33122.
66. Wittung P, Kajanus J, Edwards K, Haima G, Nielsen PE, Norden B, Malmstrom BG: Phospholipid membrane permeability of peptide nucleic acid. FEBS Lett 1995;375:27-29.
67. Arima H, Sakamoto T, Aramaki Y, Ishidate K, Tsuchiya S: Specific inhibition of nitric oxide production in macrophages by phosphorothioate antisense oligonucleotides. J Pharm Sci 1997;86:1079-1084.
68. Buhl R, Holroyd KJ, Mastrangeli A, Cantin AM, Jaffe HA, Wells FB, Saltini C: Systemic glutathione deficiency in symptom-free HIV-seropositive individuals. Lancet 1989;ii:1294-1298.
69. Staal FJ, Roederer M, Israelski DM, Bubp J, Mole LA, McShane D, Deresinski SC, Ross W, Sussman H, Raju PA, et al: Intracellular glutathione levels in T-cell subsets decrease in HIV-infected individuals. AIDS Res Hum Retroviruses 1992;8:305-311.
70. Mihm S, Galter D, Dröge W: Modulation of transcription factor NFkB by intracellular glutathione levels and by variations of the extracellular cysteine supply. FASEB J 1995;9:246-252.
71. Garaci E, Palamara AT, Di Francesco P, Favalli C, Ciriolo MR, Rotilio G: Glutathione inhibits replication and expression of viral proteins in cultured cells infected with Sendai virus. Biochem Biophys Res Commun 1992;188:1090-1096.
72. Palamara AT, Perno CF, Ciriolo MR, Dini L, Balestra E, D'Agostini C, Di Francesco P, Favalli C, Rotilio G, Garaci E: Evidence for antiviral activity of glutathione: In vitro inhibition of herpes simplex virus type 1 replication. Antiviral Res 1995;27:237-253.
73. Palamara AT, Perno CF, Aquaro S, Buè MC, Dini L, Garaci E: Glutathione inhibits HIV replication by acting at late stages of the virus life cycle. AIDS Res Hum Retroviruses 1996;12:1537-1541.
74. Magnani M, Fraternale A, Casabianca A, Schiavano GF, Chiarantini L, Palamara AT, Ciriolo MR, Rotilio G, Garaci E: Antiretroviral effect of combined zidovudine and reduced glutathione therapy in murine AIDS. AIDS Res Hum Retroviruses 1997;13:1093-1099.
75. 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. Antiviral Res 2002;56:263-272.
76. Murata Y, Shimamura T, Hamura J: The polarizarion of Th1/Th2 balance is dependent on the intracellular thiol redox status of macrophages due to the distinctive cytokine production. Int Immunol 2002;14:201-212.
77. Murray HW: Survival of intracellular pathogens within human mononuclear phagocytes. Semin Hematol 1988;25:101-111.