2,092
Views
10
CrossRef citations to date
0
Altmetric
Review

Preclinical developments of enzyme-loaded red blood cells

, , &
Pages 43-54 | Received 08 Jul 2020, Accepted 08 Sep 2020, Published online: 23 Dec 2020

References

  • Ihler GM, Glew RH, Schnure FW. Enzyme loading of erythrocytes. Proc Natl Acad Sci USA. 1973;70(9):2663–2666. DOI:10.1073/pnas.70.9.2663.
  • Magnani M, Laguerre M, Rossi L, et al. In vivo accelerated acetaldehyde metabolism using acetaldehyde dehydrogenase-loaded erythrocytes. Alcohol Alcohol. 1990;25(6):627–637.
  • Bourgeaux V, Aufradet E, Campion Y, et al. Efficacy of homologous inositol hexaphosphate-loaded red blood cells in sickle transgenic mice. Br J Haematol. 2012;157:357–369.
  • Bax BE, Bain MD, Talbot PJ, et al. Survival of human carrier erythrocytes in vivo. Clin Sci. 1999;96(2):171–178.
  • Coker SA, Szczepiorkowski ZM, Siegel AH, et al. A study of the pharmacokinetic properties and the in vivo kinetics of erythrocytes loaded with dexamethasone sodium phosphate in healthy volunteers. Transfus Med Rev. 2018;32(2):102–110.
  • Rossi L, Pierigè F, Aliano MP, et al. Ongoing developments and clinical progress in drug-loaded red blood cell technologies. BioDrugs. 2020;34:265–272.
  • DeLoach JR. Hypotonic dialysis encapsulation in erythrocytes of mammalian species. Bibl Haematol. 1985;51:1–6.
  • Pierigè F, Bigini N, Rossi L, et al. Reengineering red blood cells for cellular therapeutics and diagnostics. WIREs Nanomed Nanobiotechnol. 2017;9:e1454.
  • Bax EB. Erythrocytes as carriers of therapeutic enzymes. Pharmaceutics. 2020;12:435–455. .
  • Pei L, Omburo G, McGuinn WD, et al. Encapsulation of phosphotriesterase within murine erythrocytes. Toxicol Appl Pharmacol. 1994;124:296–301.
  • Leung P, Cannon EP, Petrikovics I, et al. In vivo studies on rhodanese encapsulation in mouse carrier erythrocytes. Toxicol Appl Pharmacol. 1991;110:268–274.
  • Pei L, McGuinn WD, Omburo G, et al. Spectrophotometric determination of paraoxonase within mouse carrier red blood cells. Biotechnol Appl Biochem. 1994;20(Pt1):35–41.
  • Bustos NL, Batlle AM. 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. 1989;5:125–131.
  • Ito Y, Ogiso T, Iwaki M, et al. Encapsulation of human urokinase in rabbit erythrocytes and its disposition in the circulation system in rabbits. J Pharmacobiodyn. 1987;10:550–556.
  • Flynn G, Hackett TJ, McHale L, et al. Encapsulation of the thrombolytic enzyme, brinase, in photosensitized erythrocytes: a novel thrombolytic system based on photodynamic activation. J Photochem Photobiol B Biol. 1994;26:193–196.
  • Muzykantov VR, Sakharov DV, Smirnov MD, et al. Immunotargeting of erythrocytes-bound streptokinase provides local lysis of a fibrin clot. BBA Gen Subj. 1986;884:355–362.
  • Murciano JC, Medinilla S, Eslin D, et al. Prophylactic fibrinolysis through selective dissolution of nascent clots by tPA-carrying erythrocytes. Nat Biotechnol. 2003;21:891–896.
  • Adriaenssens K, Karcher D, Marescau B, et al. Hyper-argininemia: 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. 1984;16:779–786.
  • Thorpe SR, Fiddler MB, Desnick RJ, et al. In Vivo Fate of Erythrocyte-Entrapped β-Glucuronidase in β- Glucuronidase-Deficient Mice. Pediatr Res. 1975;9:918–923.
  • Magnani M, Mancini U, Bianchi M, et al. Comparison of uricase-bound and uricase-loaded erythrocytes as bioreactors for uric acid degradation. Adv Exp Med Biol. 1992;326:189–194.
  • Zocchi E, Benatti U, Guida L, et al. Encapsulation of glucose oxidase in mouse erythrocytes: an experimental model of oxidant-induced cytotoxicity and a means for splenic targeting of carrier erythrocytes. In: Ropars C, Chassaigne M, Nicolau C, editors. Red blood cells as carriers for drugs. Oxford (UK): Pergamon Press; 1987:95–101.
  • 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. 1992;15:207–216.
  • Garin M, Rossi L, Luque J, et al. Lactate catabolism by enzyme-loaded red blood cells. Biotechnol Appl Biochem. 1995;22:295–303.
  • Naqi A, DeLoach JR, Andrews K, et al. Determination of parameters for enzyme therapy using L-asparaginase entrapped in canine erythrocytes. Biotechnol Appl Biochem. 1988;10:365–372.
  • Moran NF, Bain MD, Muqit MM, et al. Carrier erythrocyte entrapped thymidine phosphorylase therapy for MNGIE. Neurology. 2008;71:686–688.
  • Bax BE, Bain MD, Scarpelli M, et al. Clinical and biochemical improvements in a patient with MNGIE following enzyme replacement. Neurology. 2013;81:1269–1271.
  • Levene M, Bain MD, Moran NF, et al. Safety and efficacy of erythrocyte encapsulated thymidine phosphorylase in mitochondrial neurogastrointestinal encephalomyopathy. J Clin Med. 2019;8(4):457.
  • Bax BE, Levene M, Bain MD, et al. Erythrocyte encapsulated thymidine phosphorylase for the treatment of patients with mitochondrial neurogastrointestinal encephalomyopathy: study protocol for a multi-centre, multiple dose, open label trial. J Clin Med. 2019;8(8):1096.
  • Levene M, Coleman DG, Kilpatrick HC, et al. Preclinical toxicity evaluation of erythrocyte-encapsulated thymidine phosphorylase in BALB/c mice and beagle dogs: an enzyme-replacement therapy for mitochondrial neurogastrointestinal encephalomyopathy. Toxicol Sci. 2013;131:311–324.
  • Wanders D, Hobson K, Ji X. Methionine restriction and cancer biology. Nutrients. 2020;12(3):684.
  • Kang JS. Dietary restriction of amino acids for Cancer therapy. Nutr Metab. 2020;17(1):1–12.
  • Poirson-Bichat F, Goņalves RAB, Miccoli L, et al. Methionine depletion enhances the antitumoral efficacy of cytotoxic agents in drug-resistant human tumor xenografts. Clin Cancer Res. 2000;6(2):643–653.
  • Kokkinakis DM, Hoffman RM, Frenkel EP, et al. Synergy between methionine stress and chemotherapy in the treatment of brain tumor xenografts in athymic mice. Cancer Res. 2001;61(10):4017–4023.
  • Gao X, Sanderson SM, Dai Z, et al. Dietary methionine links nutrition and metabolism to the efficacy of cancer therapies. Nature. 2019;572:397–401.
  • Thivat E, Durando X, Demidem A, et al. A methionine-free diet associated with nitrosourea treatment down-regulates methylguanine-DNA methyl transferase activity in patients with metastatic cancer. Anticancer Res. 2007;27(4 C):2779–2783.
  • Durando X, Farges MC, Buc E, et al. Dietary methionine restriction with FOLFOX regimen as first line therapy of metastatic colorectal cancer: a feasibility study. Oncology. 2010;78:205–209.
  • Thivat E, Farges MC, Bacin F, et al. Phase II trial of the association of a methionine-free diet with cystemustine therapy in melanoma and glioma. Anticancer Res. 2009;29(12):5235–5240.
  • Epner DE, Morrow S, Wilcox M, et al. Nutrient intake and nutritional indexes in adults with metastatic cancer on a phase I clinical trial of dietary methionine restriction. Nutr Cancer. 2002;42(2):158‐166.
  • Machover D, Zittoun J, Broët P, et al. Cytotoxic synergism of methioninase in combination with 5-fluorouracil and folinic acid. Biochem Pharmacol. 2001;61(7):867–876.
  • Hoffman RM. Development of recombinant methioninase to target the general cancer-specific metabolic defect of methionine dependence: a 40-year odyssey. Expert Opin Biol Ther. 2015;15(1):21–31.
  • Sun X, Yang Z, Li S, et al. In vivo efficacy of recombinant methioninase is enhanced by the combination of polyethylene glycol conjugation and Pyridoxal 5′-phosphate supplementation. Cancer Res. 2003;63(23):8377–8383.
  • Yang Z, Sun X, Li S, et al. Circulating half-life of PEGylated recombinant methioninase holoenzyme is highly dose dependent on cofactor pyridoxal-5′-phosphate. Cancer Res. 2004;64(16):5775–5778.
  • Gay F, Aguera K, Sénéchal K, et al. Methionine tumor starvation by erythrocyte-encapsulated methionine gamma-lyase activity controlled with per Os Vitamin B6. Cancer Med. 2017;6:1437–1452.
  • Anderson BB, Fulford-Jones CE, Child JA, et al. Conversion of vitamin B6 compounds to active forms in the red blood cell. J Clin Invest. 1971;50(9):1901–1909.
  • Sénéchal K, Maubant S, Leblanc M, et al. Abstract 2258: erymethionase (Methionine-Gamma-Lyase Encapsulated into Red Blood Cells) Potentiates Anti-PD-1 therapy in TNBC syngeneic mouse model. In Cancer Research. Vol. 79. American Association for Cancer Research (AACR): Philadelphia (PA); 2019. p. 2258.
  • Machover D, Bonnarme P. Polypeptides isolated from Brevibacterium aurantiacum and their use for the treatment of cancer. WO Patent App. PCT/EP2012/061,497; 2012.
  • Machover D, Rossi L, Hamelin J, et al. Effects in cancer cells of the recombinant l-methionine gamma-lyase from brevibacterium aurantiacum. Encapsulation in human erythrocytes for sustained l-methionine elimination. J Pharmacol Exp Ther. 2019;369(3):489–502.
  • Wriston JC, Yellin TO. L-Asparaginase: A review. Advances in enzymology and related areas of molecular biology. Vol. 39. Hoboken (NJ): Wiley; 2006. p. 185–248.
  • Heo YA, Syed YY, Keam SJ. Pegaspargase: A review in acute lymphoblastic leukaemia. Drugs. 2019;79:767–777.
  • Updike SJ, Wakamiya RT. Infusion of red blood cell-loaded asparaginase in monkey. Immunologic, metabolic, and toxicologic consequences. J Lab Clin Med. 1983;101(5):679–691.
  • Kravtzoff R, Colombat PH, Desbois I, et al. Tolerance evaluation of L-asparaginase loaded in red blood cells. Eur J Clin Pharmacol. 1996;51(3–4):221–225.
  • Kravtzoff R, Ropars C, Laguerre M, et al. Erythrocytes as carriers for L-asparaginase. Methodological and mouse in-vivo studies. J Pharm Pharmacol. 1990;42(7):473–476.
  • Kwon YM, Chung HS, Moon C, et al. L-asparaginase encapsulated intact erythrocytes for treatment of acute lymphoblastic leukemia (ALL). J Control Release. 2009;139:182–189.
  • Hunault-Berger M, Leguay T, Huguet F, et al. Group for Research on Adult Acute Lymphoblastic Leukemia (GRAALL). A Phase 2 Study of L-Asparaginase Encapsulated in erythrocytes in elderly patients with philadelphia chromosome negative acute lymphoblastic leukemia: the GRASPALL/GRAALLSA2-2008 study. Am J Hematol. 2015;90::811–818.
  • Patil MD, Bhaumik J, Banerjee UC, et al. Arginine dependence of tumor cells: targeting a chink in cancer’s armor. Oncogene. 2016;35:4957–4972.
  • Xiong L, Teng JLL, Botelho MG, et al. Arginine metabolism in bacterial pathogenesis and cancer therapy. Int J Mol Sci. 2016;17:363–381.
  • Kuo MT, Savaraj N, Feun LG. Targeted cellular metabolism for cancer chemotherapy with recombinant arginine-degrading enzymes. Oncotarget. 2010;1(4):246–251.
  • Szlosarek PW, Luong P, Phillips MM, et al. Metabolic response to pegylated arginine deiminase in mesothelioma with promoter methylation of argininosuccinate synthetase. J Clin Oncol. 2013;31(7):e111–e113.
  • Gay F, Aguera K, Senechal K, et al. Abstract 4812: arginine deiminase loaded in erythrocytes: a promising formulation for L-Arginine deprivation therapy in cancers. In Cancer Research. Vol 6. American Association for Cancer Research (AACR): Philadelphia (PA); 2016. p. 4812.
  • Dhankhar R, Gupta V, Kumar S, et al. Microbial enzymes for deprivation of amino acids metabolism in malignant cells: biological strategy for cancer treatment. Appl Microbiol Biotechnol. 2020;104:2857–2869.
  • Palermo L, Geberhiwot T, MacDonald A, et al. Cognitive outcomes in early-treated adults with phenylketonuria (PKU): a comprehensive picture across domains. Neuropsychology. 2017;31(3):255–267.
  • Manti F, Nardecchia F, Chiarotti F, et al. Psychiatric disorders in adolescent and young adult patients with phenylketonuria. Mol Genet Metab. 2016;117(1):12–18.
  • Brown CS, Lichter-Konecki U. Phenylketonuria (PKU): A problem solved?. Mol Genet Metab Rep. 2015;6:8–12.
  • Gupta S, Lau K, Harding CO, et al. Association of immune response with efficacy and safety outcomes in adults with phenylketonuria administered pegvaliase in phase 3 clinical trials. EBioMedicine. 2018;37:366–373.
  • Yew NS, Dufour E, Przybylska M, et al. Erythrocytes encapsulated with phenylalanine hydroxylase exhibit improved pharmacokinetics and lowered plasma phenylalanine levels in normal mice. Mol Genet Metab. 2013;109:339–344.
  • Rossi L, Pierigè F, Carducci C, et al. Erythrocyte-mediated delivery of phenylalanine ammonia lyase for the treatment of phenylketonuria in BTBR-Pahenu2mice. J Control Release. 2014;194:37–44.
  • Pascucci T, Rossi L, Colamartino M, et al. A new therapy prevents intellectual disability in mouse with phenylketonuria. Mol Genet Metab. 2018;124(1):39–49.
  • Griswold MG, Fullman N, Hawley C, et al. Alcohol use and burden for 195 countries and territories, 1990-2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2018;392(10152):1015–1035.
  • Julien J, Ayer T, Bethea ED, et al. Projected prevalence and mortality associated with alcohol-related liver disease in the USA, 2019-40: a modelling study. Lancet Public Health. 2020;5(6):e316–e323.
  • Shield K, Manthey J, Rylett M, et al. National, regional, and global burdens of disease from 2000 to 2016 attributable to alcohol use: a comparative risk assessment study. Lancet Public Heal. 2020;5(1):e51–e61.
  • Flor LS, Gakidou E. The burden of alcohol use: better data and strong policies towards a sustainable development. Lancet Public Heal. 2020;5(1):e10–e11.
  • Zhou H, Sealock JM, Sanchez-Roige S, et al. Genome-wide meta-analysis of problematic alcohol use in 435,563 individuals yields insights into biology and relationships with other traits. Nat Neurosci. 2020;23:809–818.
  • Fairbanks J, Umbreit A, Prakash Kolla B, et al. Evidenced-based pharmacotherapies for alcohol use disorder: clinical pearls. Mayo Clin Proc. 2020;95(9):1964–1977.
  • Lizano C, Pérez MT, 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. 2001;68:2001–2016.
  • Lizano C, Sanz S, Luque J, et al. In vitro study of alcohol dehydrogenase and acetaldehyde dehydrogenase encapsulated into human erythrocytes by an electroporation procedure. Biochim Biophys Acta. 1998;1425(2):328–336.
  • Alexandrovich YG, Kosenko EA, Sinauridze EI, et al. Rapid elimination of blood alcohol using erythrocytes: mathematical modeling and in vitro study. Biomed Res Int. 2017;2017:1–14.
  • Magnani M, Fazi A, Mangani F, et al. Methanol detoxification by enzyme-loaded erythrocytes. Biotechnol Appl Biochem. 1993;18(3):217–226.
  • Muthuvel A, Rajamani R, Manikandan S, et al. Detoxification of formate by formate dehydrogenase-loaded erythrocytes and carbicarb in folate-deficient methanol-intoxicated rats. Clin Chim Acta. 2006;367:162–169.
  • Felipo V, Butterworth RF. Neurobiology of ammonia. Prog Neurobiol. 2002;67:259–279.
  • Picca S, Dionisi-Vici C, Abeni D, et al. Extracorporeal dialysis in neonatal hyperammonemia: modalities and prognostic indicators. Ped Nephrol. 2001;16(11):862–867.
  • Häberle J, Burlina A, Chakrapani A, et al. Suggested guidelines for the diagnosis and management of urea cycle disorder: first revision. J Inherit Metab Dis. 2019;42(86):1192–1230.
  • Ames EG, Luckritz KE, Ahmad A. A retrospective review of outcomes in the treatment of hyperammonemia with renal replacement therapy due to inborn errors of metabolism. Pediatr Nephrol. 2020;35(9):1761–1769.
  • Sharma BC, Sharma P, Lunia MK, et al. A randomized, double-blind, controlled trial comparing rifaximin plus lactulose with lactulose alone in treatment of overt hepatic encephalopathy. Am J Gastroenterol. 2013;108(9):1458–1463.
  • Sushma S, Dasarathy S, Tandon RK, et al. Sodium benzoate in the treatment of acute hepatic encephalopathy: a double-blind randomized trial. Hepatology. 1992;16(1):138–144.
  • Honda S, Yamamoto K, Sekizuka M, et al. Successful treatment of severe hyperammonemia using sodium phenylacetate powder prepared in hospital pharmacy. Biol Pharm Bull. 2002;25(9):1244–1246.
  • Mizutani N, Kato T, Maehara M, et al. Oral administration of arginine and citrulline in the treatment of lysinuric protein intolerance. Tohoku J Exp Med. 1984;142(1):15–24.
  • Sanz S, Lizano C, Luque J, et al. In vitro and in vivo study of glutamate dehydrogenase encapsulated into mouse erythrocytes by a hypotonic dialysis procedure. Life Sci. 1999;65:2781–2789.
  • Kosenko EA, Venediktova NI, Kudryavtsev AA, et al. Encapsulation of glutamine synthetase in mouse erythrocytes: a new procedure for ammonia detoxification. Biochem Cell Biol. 2008;86:469–476.
  • Protasov ES, Borsakova DV, Alexandrovich YG, et al. Erythrocytes as bioreactors to decrease excess ammonium concentration in blood. Sci Rep. 2019;9:1455.
  • Glassman PM, Villa CH, Ukidve A, et al. Vascular drug delivery using carrier red blood cells: focus on RBC surface loading and pharmacokinetics. Pharmaceutics. 2020;12(5):440.