Comparative binding, endocytosis, and biodistribution of antibodies and antibody-coated carriers for targeted delivery of lysosomal enzymes to ICAM-1 versus transferrin receptor

Journal of Inherited Metabolic Disease

Volumn 36, Issue 3, 2013, Pages 467-477

  Papademetriou, Jason ^a   Garnacho, Carmen ^b   Serrano, Daniel ^c   Bhowmick, Tridib ^d   Schuchman, Edward H ^e   Muro, Silvia ^a,d  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF SEVILLE   (Spain)

^c University of Maryland   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; IODINE 125; MONOCLONAL ANTIBODY; POLYSTYRENE; SPHINGOMYELIN PHOSPHODIESTERASE; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG DOSAGE FORM COMPARISON; DRUG FORMULATION; ENDOCYTOSIS; ENDOTHELIUM CELL; ENZYME REPLACEMENT; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG PARENCHYMA; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PROTEIN BINDING; PROTEIN TARGETING; RECEPTOR BINDING; TISSUE DISTRIBUTION;

ANIMALS; ANTIBODIES; CELLS, CULTURED; CHO CELLS; COATED MATERIALS, BIOCOMPATIBLE; CRICETINAE; CRICETULUS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; ENZYME REPLACEMENT THERAPY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; INTERCELLULAR ADHESION MOLECULE-1; LYSOSOMAL STORAGE DISEASES; LYSOSOMES; MICE; MICE, INBRED C57BL; MOLECULAR TARGETED THERAPY; PROTEIN BINDING; RECEPTORS, TRANSFERRIN; TISSUE DISTRIBUTION;

EID: 84877776316     PISSN: 01418955     EISSN: 15732665     Source Type: Journal    
DOI: 10.1007/s10545-012-9534-6     Document Type: Article

References (78)

1. Altieri DC, Duperray A, Plescia J, Thornton GB, Languino LR (1995) Structural recognition of a novel fibrinogen gamma chain sequence (117-133) by intercellular adhesion molecule-1 mediates leukocyte-endothelium interaction. J Biol Chem 270(2):696-699
2. Balyasnikova IV, Metzger R, Visintine DJ et al (2005) Selective rat lung endothelial targeting with a new set of monoclonal antibodies to angiotensin I-converting enzyme. Pulm Pharmacol Ther 18(4):251-267
3. Banks WA (2009) Blood-brain barrier as a regulatory interface. Forum Nutr 63:102-110
4. Barreiro O, Zamai M, Yáñez-Mó M et al (2008) Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. J Cell Biol 183(3):527-542
5. Begley DJ, Pontikis CC, Scarpa M (2008) Lysosomal storage diseases and the blood-brain barrier. Curr Pharm Des 14(16):1566-1580
6. Boado RJ, Zhang Y, Xia CF, Wang Y, Pardridge WM (2008) Genetic engineering of a lysosomal enzyme fusion protein for targeted delivery across the human blood brain barrier. Biotechnol Bioeng 99(2):475-484
7. Boado RJ, Zhang Y, Wang Y, Pardridge WM (2009) Engineering and expression of a chimeric transferrin receptor monoclonal antibody for blood-brain barrier delivery in the mouse. Biotechnol Bioeng 102(4):1251-1258
8. Boado RJ, Hui EK, Lu JZ, Zhou Q, Pardridge WM (2011) Reversal of lysosomal storage in brain of adult MPS-I mice with intravenous Trojan horse-iduronidase fusion protein. Mol Pharm 8(4):1342-1350
9. Brady RO (2003) Enzyme replacement therapy: conception, chaos and culmination. Philos Trans R Soc Lond B Biol Sci 358(1433):915-919
10. Calderon AJ, Bhowmick T, Leferovich J et al (2011) Optimizing endothelial targeting by modulating the antibody density and particle concentration of anti-ICAM coated carriers. J Control Release 150(1):37-44
11. Cardone M, Porto C, Tarallo A et al (2008) Abnormal mannose-6-phosphate receptor trafficking impairs recombinant alpha-glucosidase uptake in Pompe disease fibroblasts. Pathogenetics 1(1):6
12. Carman CV, Springer TA (2004) A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol 167(2):377-388
13. Carman CV, Sage PT, Sciuto TE et al (2007) Transcellular diapedesis is initiated by invasive podosomes. Immunity 26(6):784-797
14. Carpén O, Pallai P, Staunton DE, Springer TA (1992) Association of intercellular adhesion molecule-1 (ICAM-1) with actin-containing cytoskeleton and alpha-actinin. J Cell Biol 118(5):1223-1234
15. Chen CH, Dellamaggiore KR, Ouellette CP et al (2008) Aptamer-based endocytosis of a lysosomal enzyme. Proc Natl Acad Sci U S A 105(41):15908-15913
16. Conrad ME, Umbreit JN (2000) Iron absorption and transport - an update. Am J Hematol 64(4):287-298
17. Dautry-Varsat A (1986) Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor. Biochimie 68(3):375-381
18. DeGraba T, Azhar S, Dignat-George F et al (2000) Profile of endothelial and leukocyte activation in Fabry patients. Ann Neurol 47(2):229-233
19. Desnick RJ, Schuchman EH (2002) Enzyme replacement and enhancement therapies: lessons from lysosomal disorders. Nat Rev Genet 3(12):954-966
20. Dhami R, Schuchman EH (2004) Mannose 6-phosphate receptor-mediated uptake is defective in acid sphingomyelinase-deficient macrophages: implications for Niemann-Pick disease enzyme replacement therapy. J Biol Chem 279(2):1526-1532
21. Dvorak AM, Feng D (2001) The vesiculo-vacuolar organelle (VVO). A new endothelial cell permeability organelle. J Histochem Cytochem 49(4):419-432
22. Fishman JB, Rubin JB, Handrahan JV, Connor JR, Fine RE (1987) Receptor-mediated transcytosis of transferrin across the blood-brain barrier. J Neurosci Res 18(2):299-304
23. Frey A, Giannasca KT, Weltzin R et al (1996) Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells: implications for microbial attachment and oral vaccine targeting. J Exp Med 184(3):1045-1059
24. Fuchs H, Lucken U et al (1998) Structural model of phospholipid- reconstituted human transferrin receptor derived by electron microscopy. Structure 6(10):1235-1243
25. Futerman AH, van Meer G (2004) The cell biology of lysosomal storage disorders. Nat Rev Mol Cell Biol 5(7):554-565
26. Garnacho C, Dhami R, Simone E et al (2008a) Delivery of acid sphingomyelinase in normal and niemann-pick disease mice using intercellular adhesion molecule-1-targeted polymer nanocarriers. J Pharmacol Exp Ther 325(2):400-408
27. Garnacho C, Albelda SM, Muzykantov VR, Muro S (2008b) Differential intra-endothelial delivery of polymer nanocarriers targeted to distinct PECAM-1 epitopes. J Control Release 130(3):226-233
28. Garnacho C, Serrano D, Muro S (2012) A fibrinogen-derived peptide provides ICAM-1-specific targeting and intra-endothelial transport of polymer nanocarriers in human cell cultures and mice. J Pharmacol Exp Ther 340(3):638-647
29. Ghaffarian R, Bhowmick T, Muro S (2012) Transport of nanocarriers across gastrointestinal epithelial cells by a new transcellular route induced by targeting ICAM-1. J Control Release June 12 (Epub ahead of print)
30. Hatakeyama H, Akita H, Maruyama K et al (2004) Factors governing the in vivo tissue uptake of transferrin-coupled polyethylene glycol liposomes in vivo. Int J Pharm 281(1-2):25-33
31. He X, Miranda SR, Xiong X, Dagan A, Gatt S, Schuchman EH (1999) Characterization of human acid sphingomyelinase purified from the media of overexpressing Chinese hamster ovary cells. Biochim Biophys Acta 1432(2):251-264
32. Hillebrand U, Hausberg M, Stock C et al (2006) 17beta-estradiol increases volume, apical surface and elasticity of human endothelium mediated by Na+/H+ exchange. Cardiovasc Res 69(4):916-924
33. Hirst J, Robinson MS (1998) Clathrin and adaptors. Biochim Biophys Acta 1404(1-2):173-193
34. Hsu J, Serrano D, Bhowmick T, Muro S (2011) Enhanced endothelial delivery and biochemical effects of alpha-galactosidase by ICAM-1-targeted nanocarriers for Fabry disease. J Control Release 149(3):323-331
35. Hsu J, Northrup L, Bhowmick T, Muro S (2012) Enhanced delivery of alpha-glucosidase for Pompe disease by ICAM-1-targeted nanocarriers: comparative performance of a strategy for three distinct lysosomal storage disorders. Nanomedicine 8(5):731-739
36. Jefferies WA, Brandon MR, Hunt SV, Williams AF, Gatter KS, Mason DY (1984) Transferrin receptor on endothelium of brain capillaries. Nature 312(5990):162-163
37. Jevnikar AM, Wuthrich RP, Takei F et al (1990) Differing regulation and function of ICAM-1 and class II antigens on renal tubular cells. Kidney Int 38(3):417-425
38. Jin M, Snider MD (1993) Role of microtubules in transferrin receptor transport from the cell surface to endosomes and the Golgi complex. J Biol Chem 268(24):18390-18397
39. Jun CD, Carman CV, Redick SD, Shimaoka M, Erickson HP, Springer TA (2001) Ultrastructure and function of dimeric, soluble intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 276(31):29019-29027
40. Kissel K, Hamm S et al (1998) Immunohistochemical localization of the murine transferrin receptor (TfR) on blood-tissue barriers using a novel anti-TfR monoclonal antibody. Histochem Cell Biol 110(1):63-72
41. Ko YT, Bhattacharya R, Bickel U (2009) Liposome encapsulated polyethylenimine/ODN polyplexes for brain targeting. J Control Release 133(3):230-237
42. LeBowitz JH, Grubb JH, Maga JA, Schmiel DH, Vogler C, Sly WS (2004) Glycosylation-independent targeting enhances enzyme delivery to lysosomes and decreases storage in mucopolysaccharidosis type VII mice. Proc Natl Acad Sci U S A 101(9):3083-3088
43. Lossinsky AS, Mossakowski MJ, Pluta R, Wisniewski HM (1995) Intercellular adhesion molecule-1 (ICAM-1) upregulation in human brain tumors as an expression of increased blood-brain barrier permeability. Brain Pathol 5(4):339-344
44. Lu JZ, Boado RJ, Hui EK, Zhou QH, Pardridge WM (2011) Expression in CHO cells and pharmacokinetics and brain uptake in the Rhesus monkey of an IgG-iduronate-2-sulfatase fusion protein. Biotechnol Bioeng 108(8):1954-1964
45. Marlin SD, Springer TA (1987) Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell 51(5):813-819
46. Matzner U, Matthes F, Weigelt C et al (2008) Non-inhibitory antibodies impede lysosomal storage reduction during enzyme replacement therapy of a lysosomal storage disease. J Mol Med 86(4):433-442
47. Millán J, Hewlett L, Glyn M, Toomre D, Clark P, Ridley AJ (2006) Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat Cell Biol 8(2):113-123
48. Mistry PK, Wraight EP, Cox TM (1996) Therapeutic delivery of proteins to macrophages: implications for treatment of Gaucher's disease. Lancet 348(9041):1555-1559
49. Moghimi SM, Hunter AC, Murray JC (2001) Long circulating and target-specific nanoparticles: theory to practice. Pharmacol Rev 53(2):283-318
50. Murciano JC, Muro S, Koniaris L et al (2003) ICAM-directed vascular immunotargeting of antithrombotic agents to the endothelial luminal surface. Blood 101(10):3977-3984
51. Muro S (2010) New biotechnological and nanomedicine strategies for treatment of lysosomal storage disorders. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2(2):189-204
52. Muro S, Wiewrodt R, Thomas A et al (2003) A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J Cell Sci 116(Pt 8):1599-1609
53. Muro S, Gajewski C, Koval M, Muzykantov VR (2005) ICAM-1 recycling in endothelial cells: a novel pathway for sustained intracellular delivery and prolonged effects of drugs. Blood 105(2):650-658
54. Muro S, Schuchman EH, Muzykantov VR (2006a) Lysosomal enzyme delivery by ICAM-1-targeted nanocarriers bypassing glycosylation- and clathrin-dependent endocytosis. Mol Ther 13(1):135-141
55. Muro S, Mateescu M, Gajewski C et al (2006b) Control of intracellular trafficking of ICAM-1-targeted nanocarriers by endothelial Na+/H+ exchanger proteins. Am J Physiol Lung Cell Mol Physiol 290(5):L809-L817
56. Muro S, Garnacho C, Champion JA et al (2008) Control of endothelial targeting and intracellular delivery of therapeutic enzymes by modulating the size and shape of ICAM-1-targeted carriers. Mol Ther 16(8):1450-1458
57. Nanami M, Ookawara T, Otaki Y et al (2005) Tumor necrosis factor-alpha-induced iron sequestration and oxidative stress in human endothelial cells. Arterioscler Thromb Vasc Biol 25(12):2495-2501
58. Ohashi T, Iizuka S, Ida H, Eto Y (2008) Reduced alpha-Gal A enzyme activity in Fabry fibroblast cells and Fabry mice tissues induced by serum from antibody positive patients with Fabry disease. Mol Genet Metab 94(3):313-318
59. Osborn MJ, McElmurry RT, Peacock B, Tolar J, Blazar BR (2008) Targeting of the CNS in MPS-IH using anonviral transferrin-alpha-L-iduronidase fusion gene product. Mol Ther 16(8):1459-1466
60. Pang Z, Gao H, Yu Y et al (2011) Brain delivery and cellular internalization mechanisms for transferrin conjugated biodegradable polymersomes. Int J Pharm 415(1-2):284-292
61. Pardridge WM (2010) Biopharmaceutical drug targeting to the brain. J Drug Target 18(3):157-167
62. Pardridge WM, Boado RJ (2012) Reengineering biopharmaceuticals for targeted delivery across the blood-brain barrier. Methods Enzymol 503:269-292
63. Prince WS, McCormick LM, Wendt DJ et al (2004) Lipoprotein receptor binding, cellular uptake, and lysosomal delivery of fusions between the receptor-associated protein (RAP) and alpha-L-iduronidase or acid alpha-glucosidase. J Biol Chem 279(33):35037-35046
64. Rothlein R, Dustin ML, Marlin SD, Springer TA (1986) A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J Immunol 137(4):1270-1274
65. Schnitzer JE (2001) Caveolae: from basic trafficking mechanisms to targeting transcytosis for tissue-specific drug and gene delivery in vivo. Adv Drug Deliv Rev 49(3):265-280
66. Serrano D, Bhowmick T, Chadha R, Garnacho C, Muro S (2012) Intercellular adhesion molecule 1 engagement modulates sphingomyelinase and ceramide, supporting uptake of drug carriers by the vascular endothelium. Arterioscler Thromb Vasc Biol 32(5):1178-1185
67. Shen JS, Meng XL, Moore DF, Quirk JM, Shayman JA, Schiffmann R, Kaneski CR (2008) Globotriaosylceramide induces oxidative stress and up-regulates cell adhesion molecule expression in Fabry disease endothelial cells. Mol Genet Metab 95(3):163-168
68. Shi N, Boado RJ, Pardridge WM (2001) Receptor-mediated gene targeting to tissues in vivo following intravenous administration of pegylated immunoliposomes. Pharm Res 18(8):1091-1095
69. Steven AC, Hainfeld JF, Wall JS, Steer CJ (1983) Mass distributions of coated vesicles isolated from liver and brain: analysis by scanning transmission electron microscopy. J Cell Biol 97(6):1714-1723
70. Torchilin VP (2006) Multifunctional nanocarriers. Adv Drug Deliv Rev 58(14):1532-1555
71. Urayama A, Grubb JH, Sly WS, Banks WA (2004) Developmentally regulated mannose 6-phosphate receptor-mediated transport of a lysosomal enzyme across the blood-brain barrier. Proc Natl Acad Sci U S A 101(34):12658-12663
72. Vaags AK, Campbell TN, Choy FY (2005) HIV TAT variants differentially influence the production of glucocerebrosidase in Sf9 cells. Genet Mol Res 4(3):491-495
73. van Rooy I, Mastrobattista E, Storm G, Hennink WE, Schiffelers RM (2011) Comparison of five different targeting ligands to enhance accumulation of liposomes into the brain. J Control Release 150(1):30-36
74. Visser CC, Voorwinden LH, Crommelin DJ, Danhof M, de Boer AG (2004) Characterization and modulation of the transferrin receptor on brain capillary endothelial cells. Pharm Res 21(5):761-769
75. Xia H, Anderson B, Mao Q, Davidson BL (2000) Recombinant human adenovirus: targeting to the human transferrin receptor improves gene transfer to brain microcapillary endothelium. J Virol 74(23):11359-11366
76. Xia H, Mao Q, Davidson BL (2001) The HIV Tat protein transduction domain improves the biodistribution of beta-glucuronidase expressed from recombinant viral vectors. Nat Biotechnol 19(7):640-644
77. Zhang XY, Dinh A, Cronin J, Li SC, Reiser J (2008) Cellular uptake and lysosomal delivery of galactocerebrosidase tagged with the HIV Tat protein transduction domain. J Neurochem 104(4):1055-1064
78. Zhou QH, Boado RJ, Lu JZ, Hui EK, Pardridge WM (2012) Brain-penetrating IgG-iduronate 2-sulfatase fusion protein for the mouse. Drug Metab Dispos 40(2):329-335