Erythrocytes as a novel delivery vehicle for biologics: From enzymes to nucleic acid-based therapeutics

Therapeutic Delivery

Volumn 3, Issue 3, 2012, Pages 405-414

  Magnani, Mauro ^a   Pierig, Francesca ^a   Rossi, Luigia ^a  

^a UNIVERSITY OF URBINO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; ANTIGEN; BIOLOGICAL PRODUCT; CYCLOSPORIN; DIDANOSINE; DIPHTHERIA TOXIN; DRUG CARRIER; ENALAPRILAT; ENZYME; GLUTATHIONE; IMMUNOPHILIN; LIPOSOME; LISTERIOLYSIN; NUCLEIC ACID; PEPTIDE; PERTUSSIS TOXIN; TACROLIMUS; TETANUS TOXIN; TOXIN; ZIDOVUDINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADENOSINE DEAMINASE DEFICIENCY; ANTIBODY TITER; CELL COMPARTMENTALIZATION; CELL VIABILITY; CLINICAL EFFECTIVENESS; DOSE RESPONSE; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; ENCAPSULATION; ENZYME DEFICIENCY; ERYTHROCYTE; ERYTHROCYTE LIFESPAN; HUMAN; IMMUNOCOMPETENCE; IMMUNOMODULATION; IMMUNOREACTIVITY; IN VITRO STUDY; INTRACELLULAR SIGNALING; LIPOSOMAL DELIVERY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SLOW DRUG RELEASE;

EID: 84858120529     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.12.6     Document Type: Review

References (81)

1. Bax BE, Bain MD, Talbot PJ, Parker-Williams EJ, Chalmers RA. Survival of human carrier erythrocytes in vivo. Clin. Sci. (Lond.) 96(2), 171-178 (1999). (Pubitemid 29094936)
2. Anstee DJ. The functional importance of blood group-active molecules in human red blood cells. Vox Sang. 100(1), 140-149 (2011).
3. Hamidi M, Zarrin A, Foroozesh M, Mohammadi-Samani S. Applications of carrier erythrocytes in delivery of biopharmaceuticals. J. Control. Release 118(2), 145-160 (2007). (Pubitemid 46329734)
4. Pierige F, Serafini S, Rossi L, Magnani M. Cell-based drug delivery. Adv. Drug Deliv. Rev. 60(2), 286-295 (2008). (Pubitemid 350236405)
5. Patel PD, Dand N, Hirlekar RS, Kadam VJ. Drug loaded erythrocytes: as novel drug delivery system. Curr. Pharm. Des. 14(1), 63-70 (2008). (Pubitemid 351266985)
6. Rossi L, Serafini S, Pierige F et al. Erythrocyte-based drug delivery. Expert Opin. Drug Deliv. 2(2), 311-322 (2005). (Pubitemid 41130885)
7. Biagiotti S, Paoletti MF, Fraternale A, Rossi L, Magnani M. Drug delivery by red blood cells. IUBMB Life 63(8), 621-631 (2011).
8. Muzykantov VR. Drug delivery by red blood cells: vascular carriers designed by mother nature. Expert Opin. Drug Deliv. 7(4), 403-427 (2010).
9. Magnani M, Serafini S, Fraternale A et al. Red blood cell-based delivery of drugs and nanomaterials for therapeutic and diagnostic applications. In: Encyclopedia of Nanoscience and Nanotechnology (Volume 22). Nalwa SH (Ed.). American Scientific Publishers, Valencia, CA, USA, 309-354 (2011).
10. Millan CG, Marinero ML, Castaneda AZ, Lanao JM. Drug, enzyme and peptide delivery using erythrocytes as carriers. J. Control. Release 95(1), 27-49 (2004). (Pubitemid 38167677)
11. Godfrin Y, Horand F, Franco R et al. International seminar on the red blood cells as vehicles for drugs. Expert Opin. Biol. Ther. 12(1), 127-133 (2012).
12. Walsh G. Biopharmaceutical benchmarks 2010. Nat. Biotechnol. 28(9), 917-924 (2010).
13. Ihler GM, Glew RH, Schnure FW. Enzyme loading of erythrocytes. Proc. Natl Acad. Sci. USA 70(9), 2663-2666 (1973).
14. Hoffman JF. Physiological characteristics of human red blood cell ghosts. J. Gen. Physiol. 42(1), 9-28 (1958).
15. Seeman P. Transient holes in the erythrocyte membrane during hypotonic hemolysis and stable holes in the membrane after lysis by saponin and lysolecithin. J. Cell Biol. 32(1), 55-70 (1967).
16. Feero WG, Guttmacher AE, Collins FS. Genomic medicine-an updated primer. N. Engl. J. Med. 362(21), 2001-2011 (2010).
17. Benichou B, Goyal S, Sung C, Norfleet AM, O'Brien F. A retrospective analysis of the potential impact of IgG antibodies to agalsidase b on efficacy during enzyme replacement therapy for Fabry disease. Mol. Genet. Metab. 96(1), 4-12 (2009).
18. Pastores GM. Recombinant glucocerebrosidase (imiglucerase) as a therapy for Gaucher disease. BioDrugs 24(1), 41-47 (2010).
19. Ponder KP. Immune response hinders therapy for lysosomal storage diseases. J. Clin. Invest. 118(8), 2686-2689 (2008).
20. Thorpe SR, Fiddler MB, Desnick RJ. Enzyme therapy. V. In vivo fate of erythrocyte-entrapped b-glucuronidase in b-glucuronidase-deficient mice. Pediatr. Res. 9(12), 918-923 (1975).
21. Dale GL, Beutler E. Enzyme replacement therapy in Gaucher's disease: a rapid, high-yield method for purification of glucocerebrosidase. Proc. Natl Acad. Sci. USA 73(12), 4672-4674 (1976). (Pubitemid 8013583)
22. Deloach J, Peters S, Pinkard O, Glew R, Ihler G. Effect of glutaraldehyde treatment on enzyme-loaded erythrocytes. Biochim. Biophys. Acta 496(2), 507-515 (1977). (Pubitemid 8044899)
23. Dale GL, Kuhl W, Beutler E. Incorporation of glucocerebrosidase into Gaucher's disease monocytes in vitro. Proc. Natl Acad. Sci. USA 76(1), 473-475 (1979). (Pubitemid 9110220)
24. Sprandel U, Hubbard AR, Chalmers RA. In vitro studies on resealed erythrocyte ghosts as protein carriers. Res. Exp. Med. (Berl.) 175(3), 239-245 (1979). (Pubitemid 10171430)
25. Batlle AM, Bustos NL, Stella AM, Wider EA, Conti HA, Mendez A. Enzyme replacement therapy in porphyrias-IV. First successful human clinical trial of d-aminolevulinate dehydratase-loaded erythrocyte ghosts. Int. J. Biochem. 15(10), 1261-1265 (1983). (Pubitemid 13024837)
26. Alpar HO, Lewis DA. Therapeutic efficacy of asparaginase encapsulated in intact erythrocytes. Biochem. Pharmacol. 34(2), 257-261 (1985). (Pubitemid 15153420)
27. Bax BE, Bain MD, Fairbanks LD, Webster AD, Chalmers RA. In vitro and in vivo studies with human carrier erythrocytes loaded with polyethylene glycol-conjugated and native adenosine deaminase. Br. J. Haematol. 109(3), 549-554 (2000). (Pubitemid 30415181)
28. DeLoach JR, 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), 331-335 (1990). (Pubitemid 20305166)
29. Domenech C, Thomas X, Chabaud S et al. 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(1), 58-65 (2011).
30. Garin M, Rossi L, Luque J, Magnani M. Lactate catabolism by enzyme-loaded red blood cells. Biotechnol. Appl. Biochem. 22(Pt 3), 295-303 (1995).
31. Kravtzoff R, Ropars C, Laguerre M, Muh JP, Chassaigne M. Erythrocytes as carriers for l-asparaginase. Methodological and mouse in-vivo studies. J. Pharm. Pharmacol. 42(7), 473-476 (1990). (Pubitemid 20301482)
32. Kravtzoff R, Colombat PH, Desbois I et al. Tolerance evaluation of l-asparaginase loaded in red blood cells. Eur. J. Clin. Pharmacol. 51(3-4), 221-225 (1996). (Pubitemid 26422963)
33. Kwon YM, Chung HS, Moon C et al. l-Asparaginase encapsulated intact erythrocytes for treatment of acute lymphoblastic leukemia (ALL). J. Control. Release 139(3), 182-189 (2009).
34. Magnani M, Rossi L, Bianchi M et al. Improved metabolic properties of hexokinase-overloaded human erythrocytes. Biochim. Biophys. Acta 972(1), 1-8 (1988).
35. Magnani M, Laguerre M, Rossi L et al. Acetaldehyde dehydrogenase-loaded erythrocytes as bioreactors for the removal of blood acetaldehyde. Alcohol Clin. Exp. Res. 13(6), 849, (1989). (Pubitemid 20031170)
36. Magnani M, Laguerre M, Rossi L et al. In vivo accelerated acetaldehyde metabolism using acetaldehyde dehydrogenase-loaded erythrocytes. Alcohol Alcohol. 25(6), 627-637 (1990).
37. Magnani M, Fazi A, Mangani F, Rossi L, Mancini U. Methanol detoxification by enzyme-loaded erythrocytes. Biotechnol. Appl. Biochem. 18(Pt 3), 217-226 (1993). (Pubitemid 2022755)
38. Moran NF, Bain MD, Muqit MM, Bax BE. Carrier erythrocyte entrapped thymidine phosphorylase therapy for MNGIE. Neurology 71(9), 686-688 (2008).
39. 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), 207-216 (1992).
40. Sinauridze EI, Vitvitsky VM, Pichugin AV, Zhabotinsky AM, Ataullakhanov FI. A new chemotherapeutic agent: l-asparaginase entrapped in red blood cells. Adv. Exp. Med. Biol. 326, 203-206 (1992). (Pubitemid 23047342)
41. Updike SJ, Wakamiya RT. Infusion of red blood cell-loaded asparaginase in monkey. Immunologic, metabolic, and toxicologic consequences. J. Lab. Clin. Med. 101(5), 679-691 (1983). (Pubitemid 13090031)
42. Updike SJ. Entrapment of l-asparaginase in red blood cells. A strategy to improve treatment of acute lymphoblastic leukemia. Bibl. Haematol. (51), 65-74 (1985).
43. 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 Alcohol. 27(1), 19-23 (1992).
44. Benichou B, Goyal S, Sung C, Norfleet AM, O'Brien F. A retrospective analysis of the potential impact of IgG antibodies to agalsidase b on efficacy during enzyme replacement therapy for Fabry disease. Mol. Genet. Metab. 96(1), 4-12 (2009).
45. Samokhin GP, Smirnov MD, Muzykantov VR, Domogatsky SP, Smirnov VN. Red blood cell targeting to collagen-coated surfaces. FEBS Lett. 154(2), 257-261 (1983). (Pubitemid 13088362)
46. Murciano JC, Medinilla S, Eslin D, Atochina E, Cines DB, Muzykantov VR. Prophylactic fibrinolysis through selective dissolution of nascent clots by tPA-carrying erythrocytes. Nat. Biotechnol. 21(8), 891-896 (2003). (Pubitemid 36936194)
47. Xu L, Anchordoquy T. Drug delivery trends in clinical trials and translational medicine: challenges and opportunities in the delivery of nucleic acid-based therapeutics. J. Pharm. Sci. 100(1), 38-52 (2011).
48. Ringelhann B, Konotey-Ahulu FI. The removal of heat-damaged and 51Cr-labelled red cells in haemoglobinopathies. Br. J. Haematol. 21(1), 99-112 (1971).
49. Byun HM, Suh D, Yoon H et al. Erythrocyte ghost-mediated gene delivery for prolonged and blood-targeted expression. Gene Ther. 11(5), 492-496 (2004). (Pubitemid 38313170)
50. Grimaldi S, Lisi A, Pozzi D, Santoro N. Attempts to use liposomes and RBC ghosts as vectors in drug and antisense therapy of virus infection. Res. Virol. 148(2), 177-180 (1997). (Pubitemid 27162814)
51. Kim SH, Kim EJ, Hou JH et al. Opsonized erythrocyte ghosts for liver-targeted delivery of antisense oligodeoxynucleotides. Biomaterials 30(5), 959-967 (2009).
52. Fraternale A, Paoletti MF, Casabianca A et al. Erythrocytes as carriers of antisense PNA addressed against HIV-1 gag-pol transframe domain. J. Drug Target 17(4), 278-285 (2009).
53. Magnani M, Rossi L, Fraternale A et al. Erythrocyte-mediated delivery of drugs, peptides and modified oligonucleotides. Gene Ther. 9(11), 749-751 (2002). (Pubitemid 34591480)
54. Rossi L, Brandi G, Malatesta M et al. Effect of listeriolysin O-loaded erythrocytes on Mycobacterium avium replication within macrophages. J. Antimicrob. Chemother. 53(5), 863-866 (2004). (Pubitemid 38660293)
55. Hunt S, Green J, Artymiuk PJ. Hemolysin E (HlyE, ClyA, SheA) and related toxins. Adv. Exp. Med. Biol. 677, 116-126 (2010).
56. Schnupf P, Portnoy DA. Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 9(10), 1176-1187 (2007). (Pubitemid 47375145)
57. Giammarini C, Andreoni F, Amagliani G, Casiere A, Barocci S, Magnani M. High-level expression of the listeria monocytogenes listeriolysin O in Escherichia coli and preliminary characterization of the purified protein. Protein Expr. Purif. 28(1), 78-85 (2003). (Pubitemid 36453181)
58. Chestier N, Kravtzoff R, Canepa S, Chassaigne M, Ropars C. Erythrocytes as carriers of ricin A chain: effects on the erythrophagocytic cells. Adv. Exp. Med. Biol. 326, 279-289 (1992). (Pubitemid 23047351)
59. Lochs H, Morse EL, Adibi SA. Uptake and metabolism of dipeptides by human red blood cells. Biochem. J. 271(1), 133-137 (1990). (Pubitemid 20331208)
60. Hamidi M, Tajerzadeh H, Dehpour AR, Ejtemaee-Mehr S. Inhibition of serum angiotensin-converting enzyme in rabbits after intravenous administration of enalaprilat-loaded intact erythrocytes. J. Pharm. Pharmacol. 53(9), 1281-1286 (2001). (Pubitemid 32904023)
61. Antonelli A, Crinelli R, Bianchi M et al. Efficient inhibition of macrophage TNF-a production upon targeted delivery of K48R ubiquitin. Br. J. Haematol. 104(3), 475-481 (1999). (Pubitemid 29119269)
62. Chau V, Tobias JW, Bachmair A et al. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243(4898), 1576-1583 (1989). (Pubitemid 19090506)
63. Gregori L, Poosch MS, Cousins G, Chau V. A uniform isopeptide-linked multiubiquitin chain is sufficient to target substrate for degradation in ubiquitin-mediated proteolysis. J. Biol. Chem. 265(15), 8354-8357 (1990).
64. Magnani M, Fraternale A, Casabianca A et al. Antiretroviral effect of combined zidovudine and reduced glutathione therapy in murine AIDS. AIDS Res. Hum. Retroviruses 13(13), 1093-1099 (1997). (Pubitemid 27355739)
65. Murata Y, Shimamura T, Hamuro J. The polarization of T(h)1/T(h)2 balance is dependent on the intracellular thiol redox status of macrophages due to the distinctive cytokine production. Int. Immunol. 14(2), 201-212 (2002). (Pubitemid 34144744)
66. Fraternale A, Paoletti MF, Dominici S et al. The increase in intra-macrophage thiols induced by new pro-GSH molecules directs the Th1 skewing in ovalbumin immunized mice. Vaccine 28(48), 7676-7682 (2010).
67. Fraternale A, Paoletti MF, Dominici S et al. Modulation of Th1/Th2 immune responses to HIV-1 Tat by new pro-GSH molecules. Vaccine 29(40), 6823-6829 (2011).
68. Hamidi M, Zarei N, Zarrin AH, Mohammadi-Samani S. Preparation and in vitro characterization of carrier erythrocytes for vaccine delivery. Int. J. Pharm. 338(1-2), 70-78 (2007). (Pubitemid 46777221)
69. Polvani C, Gasparini A, Benatti U et al. Murine red blood cells as efficient carriers of three bacterial antigens for the production of specific and neutralizing antibodies. Biotechnol. Appl. Biochem. 14(3), 347-356 (1991).
70. Magnani M, Chiarantini L, Vittoria E, Mancini U, Rossi L, Fazi A. Red blood cells as an antigen-delivery system. Biotechnol. Appl. Biochem. 16(2), 188-194 (1992).
71. Chiarantini L, Argnani R, Zucchini S et al. Red blood cells as delivery system for recombinant HSV-1 glycoprotein B: immunogenicity and protection in mice. Vaccine 15(3), 276-280 (1997). (Pubitemid 27118570)
72. Corinti S, Chiarantini L, Dominici S, Laguardia ME, Magnani M, Girolomoni G. Erythrocytes deliver Tat to interferon-g-treated human dendritic cells for efficient initiation of specific Type 1 immune responses in vitro. J. Leukoc. Biol. 71(4), 652-658 (2002).
73. Dominici S, Laguardia ME, Serafini G et al. Red blood cell-mediated delivery of recombinant HIV-1 Tat protein in mice induces anti-Tat neutralizing antibodies and CTL. Vaccine 21(17-18), 2073-2081 (2003).
74. Banz A, Cremel M, Rembert A, Godfrin Y. In situ targeting of dendritic cells by antigen-loaded red blood cells: a novel approach to cancer immunotherapy. Vaccine 28(17), 2965-2972 (2010).
75. Murciano JC, Higazi AA, Cines DB, Muzykantov VR. Soluble urokinase receptor conjugated to carrier red blood cells binds latent pro-urokinase and alters its functional profile. J. Control. Release 139(3), 190-196 (2009).
76. Zaitsev S, Spitzer D, Murciano JC et al. Targeting of a mutant plasminogen activator to circulating red blood cells for prophylactic fibrinolysis. J. Pharmacol. Exp. Ther. 332(3), 1022-1031 (2010).
77. Hopkins AL, Groom CR. The druggable genome. Nat. Rev. Drug Discov. 1(9), 727-730 (2002). (Pubitemid 37361545)
78. Adriaenssens K, Karcher D, Lowenthal A, Terheggen HG. Use of enzyme-loaded erythrocytes in in vvitro correction of arginase-deficient erythrocytes in familial hyperargininemia. Clin. Chem. 22(3), 323-326 (1976).
79. Polmar SH, Stern RC, Schwartz AL, Wetzler EM, Chase PA, Hirschhorn R. Enzyme replacement therapy for adenosine deaminase deficiency and severe combined immunodeficiency. N. Engl. J. Med. 295(24), 1337-1343 (1976).
80. Beutler E, Dale GL, Guinto DE, Kuhl W. Enzyme replacement therapy in Gaucher's disease: preliminary clinical trial of a new enzyme preparation. Proc. Natl Acad. Sci. USA 74(10), 4620-4623 (1977). (Pubitemid 8225177)
81. Polmar SH. Enzyme replacement and other biochemical approaches to the therapy of adenosine deaminase deficiency. Ciba Found Symp. (68), 213-230 (1978).