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International Journal of Cell Biology
Volume 2013, Article ID 703545, 14 pages
http://dx.doi.org/10.1155/2013/703545
Review Article

Receptor-Mediated Endocytosis and Brain Delivery of Therapeutic Biologics

Drug Metabolism and Pharmacokinetics, Biogen Idec, 14 Cambridge Center, Cambridge, MA 02142, USA

Received 23 January 2013; Accepted 13 May 2013

Academic Editor: Afshin Samali

Copyright © 2013 Guangqing Xiao and Liang-Shang Gan. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. P. Blumling III and G. A. Silva, “Targeting the brain: advances in drug delivery,” Current Pharmaceutical Biotechnology, vol. 13, pp. 2417–2426, 2012. View at Publisher · View at Google Scholar
  2. R. Gabathuler, “Approaches to transport therapeutic drugs across the blood-brain barrier to treat brain diseases,” Neurobiology of Disease, vol. 37, no. 1, pp. 48–57, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Demeule, J. Currie, Y. Bertrand et al., “Involvement of the low-density lipoprotein receptor-related protein in the transcytosis of the brain delivery vector Angiopep-2,” Journal of Neurochemistry, vol. 106, no. 4, pp. 1534–1544, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Demeule, A. Regina, C. Ché et al., “Identification and design of peptides as a new drug delivery system for the brain,” Journal of Pharmacology and Experimental Therapeutics, vol. 324, no. 3, pp. 1064–1072, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Guo, X. Gao, L. Su et al., “Aptamer-functionalized PEG-PLGA nanoparticles for enhanced anti-glioma drug delivery,” Biomaterials, vol. 32, no. 31, pp. 8010–8020, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Huile, P. Shuaiqi, Y. Zhi et al., “A cascade targeting strategy for brain neuroglial cells employing nanoparticles modified with angiopep-2 peptide and EGFP-EGF1 protein,” Biomaterials, vol. 32, no. 33, pp. 8669–8675, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Muruganandam, J. Tanha, S. Narang, and D. Stanimirovic, “Selection of phage-displayed llama single-domain antibodies that transmigrate across human blood-brain barrier endothelium,” The FASEB Journal, vol. 16, no. 2, pp. 240–242, 2002. View at Google Scholar · View at Scopus
  8. J. Tanha, A. Muruganandam, and D. Stanimirovic, “Phage display technology for identifying specific antigens on brain endothelial cells,” Methods in Molecular Medicine, vol. 89, pp. 435–449, 2003. View at Google Scholar · View at Scopus
  9. A. S. Haqqani, N. Caram-Salas, W. Ding et al., “Multiplexed Evaluation of Serum and CSF Pharmacokinetics of Brain-Targeting Single-Domain Antibodies Using a NanoLC-SRM-ILIS Method,” Molecular Pharmaceutics, vol. 10, no. 5, pp. 1542–1556, 2013. View at Publisher · View at Google Scholar
  10. R. J. Boado, E. K. Hui, J. Z. Lu, and W. M. Pardridge, “Glycemic control and chronic dosing of rhesus monkeys with a fusion protein of iduronidase and a monoclonal antibody against the human insulin receptor,” Drug Metabolism and Disposition, vol. 40, pp. 2021–2025, 2012. View at Publisher · View at Google Scholar
  11. W. M. Pardridge and R. J. Boado, “Reengineering biopharmaceuticals for targeted delivery across the blood-brain barrier,” Methods in Enzymology, vol. 503, pp. 269–292, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. W. M. Pardridge, “Re-engineering biopharmaceuticals for delivery to brain with molecular Trojan horses,” Bioconjugate Chemistry, vol. 19, no. 7, pp. 1327–1338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. J. A. Dumont, T. Liu, S. C. Low et al., “Prolonged activity of a recombinant factor VIII-Fc fusion protein in hemophiliaA mice and dogs,” Blood, vol. 119, no. 13, pp. 3024–3030, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. A. Yeung, M. K. Leabman, J. S. Marvin et al., “Engineering human IgG1 affinity to human neonatal Fc receptor: impact of affinity improvement on pharmacokinetics in primates,” Journal of Immunology, vol. 182, no. 12, pp. 7663–7671, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Caram-Salas, E. Boileau, G. K. Farrington et al., “In vitro and in vivo methods for assessing fcrn-mediated reverse transcytosis across the blood-brain barrier,” Methods in Molecular Biology, vol. 763, pp. 383–401, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Zhang and W. M. Pardridge, “Mediated efflux of IgG molecules from brain to blood across the blood-brain barrier,” Journal of Neuroimmunology, vol. 114, no. 1-2, pp. 168–172, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Abuqayyas and J. P. Balthasar, “Investigation of the role of FcγR and FcRn in mAb distribution to the brain,” Molecular Pharmaceutics, vol. 10, no. 5, pp. 1505–1513, 2013. View at Google Scholar
  18. A. Garg and J. P. Balthasar, “Investigation of the influence of FcRn on the distribution of IgG to the brain,” AAPS Journal, vol. 11, no. 3, pp. 553–557, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. S. D. Conner and S. L. Schmid, “Regulated portals of entry into the cell,” Nature, vol. 422, no. 6927, pp. 37–44, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. J. H. Lin, “Pharmacokinetics of biotech drugs: peptides, proteins and monoclonal antibodies,” Current Drug Metabolism, vol. 10, no. 7, pp. 661–691, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. D. M. Underhill and H. S. Goodridge, “Information processing during phagocytosis,” Nature Reviews Immunology, vol. 12, pp. 492–502, 2012. View at Publisher · View at Google Scholar
  22. S. Mayor and R. E. Pagano, “Pathways of clathrin-independent endocytosis,” Nature Reviews Molecular Cell Biology, vol. 8, no. 8, pp. 603–612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. H. T. McMahon and E. Boucrot, “Molecular mechanism and physiological functions of clathrin-mediated endocytosis,” Nature Reviews Molecular Cell Biology, vol. 12, no. 8, pp. 517–533, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. I. R. Nabi and P. U. Le, “Caveolae/raft-dependent endocytosis,” Journal of Cell Biology, vol. 161, no. 4, pp. 673–677, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. A. L. Kiss, “Caveolae and the regulation of endocytosis,” Advances in Experimental Medicine and Biology, vol. 729, pp. 14–28, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Sato, J. Nagai, N. Mitsui, R. Y. Ryoko Yumoto, and M. Takano, “Effects of endocytosis inhibitors on internalization of human IgG by Caco-2 human intestinal epithelial cells,” Life Sciences, vol. 85, no. 23–26, pp. 800–807, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. H. S. Kruth, “Receptor-independent fluid-phase pinocytosis mechanisms for induction of foam cell formation with native low-density lipoprotein particles,” Current Opinion in Lipidology, vol. 22, no. 5, pp. 386–393, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. H. S. Kruth, N. L. Jones, W. Huang et al., “Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein,” Journal of Biological Chemistry, vol. 280, no. 3, pp. 2352–2360, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. M. R. Jahn, T. Nawroth, S. Futterer, U. Wolfrum, U. Kolb, and P. Langguth, “Iron oxide/hydroxide nanoparticles with negatively charged shells show increased uptake in Caco-2 cells,” Molecular Pharmaceutics, vol. 9, pp. 1628–1637, 2012. View at Publisher · View at Google Scholar
  30. F. Hervé, N. Ghinea, and J. M. Scherrmann, “CNS delivery via adsorptive transcytosis,” AAPS Journal, vol. 10, no. 3, pp. 455–472, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Kato, H. Kamiyama, A. Okazaki, K. Kumaki, Y. Kato, and Y. Sugiyama, “Mechanism for the nonlinear pharmacokinetics of erythropoietin in rats,” Journal of Pharmacology and Experimental Therapeutics, vol. 283, no. 2, pp. 520–527, 1997. View at Google Scholar · View at Scopus
  32. J. J. van Lammerts Bueren, W. K. Bleeker, H. O. Bøgh et al., “Effect of target dynamics on pharmacokinetics of a novel therapeutic antibody against the epidermal growth factor receptor: implications for the mechanisms of action,” Cancer Research, vol. 66, no. 15, pp. 7630–7638, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. O. Khorev, D. Stokmaier, O. Schwardt, B. Cutting, and B. Ernst, “Trivalent, Gal/GalNAc-containing ligands designed for the asialoglycoprotein receptor,” Bioorganic and Medicinal Chemistry, vol. 16, no. 9, pp. 5216–5231, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Macedo-Ramos, F. S. O. Campos, L. A. Carvalho et al., “Olfactory ensheathing cells as putative host cells for Streptococcus pneumoniae: evidence of bacterial invasion via mannose receptor-mediated endocytosis,” Neuroscience Research, vol. 69, no. 4, pp. 308–313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. M. E. Taylor, “Structure and function of the macrophage mannose receptor,” Results and Problems in Cell Differentiation, vol. 33, pp. 105–121, 2001. View at Google Scholar · View at Scopus
  36. E. A. L. Biessen, M. van Teijlingen, H. Vietsch et al., “Antagonists of the mannose receptor and the LDL receptor-related protein dramatically delay the clearance of tissue plasminogen activator,” Circulation, vol. 95, no. 1, pp. 46–52, 1997. View at Google Scholar · View at Scopus
  37. T. R. Daniels, T. Delgado, G. Helguera, and M. L. Penichet, “The transferrin receptor part II: targeted delivery of therapeutic agents into cancer cells,” Clinical Immunology, vol. 121, no. 2, pp. 159–176, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Anabousi, U. Bakowsky, M. Schneider, H. Huwer, C. Lehr, and C. Ehrhardt, “In vitro assessment of transferrin-conjugated liposomes as drug delivery systems for inhalation therapy of lung cancer,” European Journal of Pharmaceutical Sciences, vol. 29, no. 5, pp. 367–374, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Singh, H. Atwal, and R. Micetich, “Transferrin directed delivery of adriamycin to human cells,” Anticancer Research, vol. 18, no. 3, pp. 1423–1427, 1998. View at Google Scholar · View at Scopus
  40. A. den Broeder, L. B. A. van de Putte, R. Rau et al., “A single dose, placebo controlled study of the fully human anti-tumor necrosis factor-α antibody adalimumab (D2E7) in patients with rheumatoid arthritis,” Journal of Rheumatology, vol. 29, no. 11, pp. 2288–2298, 2002. View at Google Scholar · View at Scopus
  41. R. D. Bell, A. P. Sagare, A. E. Friedman et al., “Transport pathways for clearance of human Alzheimer's amyloid β-peptide and apolipoproteins E and J in the mouse central nervous system,” Journal of Cerebral Blood Flow and Metabolism, vol. 27, no. 5, pp. 909–918, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Ito, S. Ohtsuki, and T. Terasaki, “Functional characterization of the brain-to-blood efflux clearance of human amyloid-β peptide (1-40) across the rat blood-brain barrier,” Neuroscience Research, vol. 56, no. 3, pp. 246–252, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Shibata, S. Yamada, S. R. Kumar et al., “Clearance of Alzheimer's amyloid-β1-40 peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier,” Journal of Clinical Investigation, vol. 106, no. 12, pp. 1489–1499, 2000. View at Google Scholar · View at Scopus
  44. M. M. Hussain, D. K. Strickland, and A. Bakillah, “The mammalian low-density lipoprotein receptor family,” Annual Review of Nutrition, vol. 19, pp. 141–172, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. S. K. Moestrup, S. Cui, H. Vorum et al., “Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs,” Journal of Clinical Investigation, vol. 96, no. 3, pp. 1404–1413, 1995. View at Google Scholar · View at Scopus
  46. M. P. Dehouck, P. Jolliet-Riant, F. Bree, J. C. Fruchart, R. Cecchelli, and J. P. Tillement, “Drug transfer across the blood-brain barrier: correlation between in vitro and in vivo models,” Journal of Neurochemistry, vol. 58, no. 5, pp. 1790–1797, 1992. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Ren, S. Shen, D. Wang et al., “The targeted delivery of anticancer drugs to brain glioma by PEGylated oxidized multi-walled carbon nanotubes modified with angiopep-2,” Biomaterials, vol. 33, no. 11, pp. 3324–3333, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Kurzrock, N. Gabrail, C. Chandhasin et al., “Safety, pharmacokinetics, and activity of GRN1005, a novel conjugate of angiopep-2, a peptide facilitating brain penetration, and paclitaxel, in patients with advanced solid tumors,” Molecular Cancer Therapeutics, vol. 11, no. 2, pp. 308–316, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Huang, J. Li, L. Han et al., “Dual targeting effect of Angiopep-2-modified, DNA-loaded nanoparticles for glioma,” Biomaterials, vol. 32, no. 28, pp. 6832–6838, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Gao, J. Qian, S. Cao et al., “Precise glioma targeting of and penetration by aptamer and peptide dual-functioned nanoparticles,” Biomaterials, vol. 33, no. 20, pp. 5115–5123, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Xin, X. Sha, X. Jiang et al., “The brain targeting mechanism of Angiopep-conjugated poly(ethylene glycol)-co-poly(ɛ-caprolactone) nanoparticles,” Biomaterials, vol. 33, no. 5, pp. 1673–1681, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. R. J. Boado, Q. Zhou, J. Z. Lu, E. K. Hui, and W. M. Pardridge, “Pharmacokinetics and brain uptake of a genetically engineered bifunctional fusion antibody targeting the mouse transferrin receptor,” Molecular Pharmaceutics, vol. 7, no. 1, pp. 237–244, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Huwyler and W. M. Pardridge, “Examination of blood-brain barrier transferrin receptor by confocal fluorescent microscopy of unfixed isolated rat brain capillaries,” Journal of Neurochemistry, vol. 70, no. 2, pp. 883–886, 1998. View at Google Scholar · View at Scopus
  54. W. M. Pardridge, Y. S. Kang, J. L. Buciak, and J. Yang, “Human insulin receptor monoclonal antibody undergoes high affinity binding to human brain capillaries in vitro and rapid transcytosis through the blood-brain barrier in vivo in the primate,” Pharmaceutical Research, vol. 12, no. 6, pp. 807–816, 1995. View at Google Scholar · View at Scopus
  55. W. M. Pardridge, J. L. Buciak, and P. M. Friden, “Selective transport of an anti-transferrin receptor antibody through the blood-brain barrier in vivo,” Journal of Pharmacology and Experimental Therapeutics, vol. 259, no. 1, pp. 66–70, 1991. View at Google Scholar · View at Scopus
  56. R. D. Broadwell, B. J. Baker-Cairns, P. M. Friden, C. Oliver, and J. C. Villegas, “Transcytosis of protein through the mammalian cerebral epithelium and endothelium. III. Receptor-mediated transcytosis through the blood-brain barrier of blood-borne transferrin and antibody against the transferrin receptor,” Experimental Neurology, vol. 142, no. 1, pp. 47–65, 1996. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Zhang and W. M. Pardridge, “Rapid transferrin efflux from brain to blood across the blood-brain barrier,” Journal of Neurochemistry, vol. 76, no. 5, pp. 1597–1600, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. H. J. Lee, B. Engelhardt, J. Lesley, U. Bickel, and W. M. Pardridge, “Targeting rat anti-mouse transferrin receptor monoclonal antibodies through blood-brain barrier in mouse,” Journal of Pharmacology and Experimental Therapeutics, vol. 292, no. 3, pp. 1048–1052, 2000. View at Google Scholar · View at Scopus
  59. R. Fleischmann, S. W. Baumgartner, M. H. Weisman, T. Liu, B. White, and P. Peloso, “Long term safety of etanercept in elderly subjects with rheumatic diseases,” Annals of the Rheumatic Diseases, vol. 65, no. 3, pp. 379–384, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. R. K. Sumbria, R. J. Boado, and W. M. Pardridge, “Brain protection from stroke with intravenous TNFalpha decoy receptor-Trojan horse fusion protein,” Journal of Cerebral Blood Flow & Metabolism, vol. 32, pp. 1933–1938, 2012. View at Google Scholar
  61. R. J. Boado, E. K. Hui, J. Z. Lu, Q. Zhou, and W. M. Pardridge, “Selective targeting of a TNFR decoy receptor pharmaceutical to the primate brain as a receptor-specific IgG fusion protein,” Journal of Biotechnology, vol. 146, no. 1-2, pp. 84–91, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. B. Ferger, A. Leng, A. Mura, B. Hengerer, and J. Feldon, “Genetic ablation of tumor necrosis factor-alpha (TNF-α) and pharmacological inhibition of TNF-synthesis attenuates MPTP toxicity in mouse striatum,” Journal of Neurochemistry, vol. 89, no. 4, pp. 822–833, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. Q. Zhou, A. Fu, R. J. Boado, E. K. Hui, J. Z. Lu, and W. M. Pardridge, “Receptor-mediated abeta amyloid antibody targeting to Alzheimer's disease mouse brain,” Molecular Pharmaceutics, vol. 8, no. 1, pp. 280–285, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. J. K. Atwal, Y. Chen, C. Chiu et al., “A therapeutic antibody targeting BACE1 inhibits amyloid-β production in vivo,” Science Translational Medicine, vol. 3, no. 84, Article ID 84ra43, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. J. Yu, Y. Zhang, M. Kenrick et al., “Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target,” Science Translational Medicine, vol. 3, no. 84, Article ID 84ra44, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. D. M. Gash, Z. Zhang, A. Ovadia et al., “Functional recovery in parkinsonian monkeys treated with GDNF,” Nature, vol. 380, no. 6571, pp. 252–255, 1996. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Kirik, B. Georgievska, and A. Björklund, “Localized striatal delivery of GDNF as a treatment for Parkinson disease,” Nature Neuroscience, vol. 7, no. 2, pp. 105–110, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Fu, Q. Zhou, E. K. Hui, J. Z. Lu, R. J. Boado, and W. M. Pardridge, “Intravenous treatment of experimental Parkinson's disease in the mouse with an IgG-GDNF fusion protein that penetrates the blood-brain barrier,” Brain Research, vol. 1352, pp. 208–213, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Abulrob, H. Sprong, P. van Bergen en Henegouwen, and D. Stanimirovic, “The blood-brain barrier transmigrating single domain antibody: mechanisms of transport and antigenic epitopes in human brain endothelial cells,” Journal of Neurochemistry, vol. 95, no. 4, pp. 1201–1214, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. R. J. Boado, E. K. Hui, J. Zhiqiang Lu, and W. M. Pardridge, “Drug targeting of erythropoietin across the primate blood-brain barrier with an IgG molecular trojan horse,” Journal of Pharmacology and Experimental Therapeutics, vol. 333, no. 3, pp. 961–969, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Al Sawaf, E. Mayatepek, and B. Hoffmann, “Neurological findings in Hunter disease: pathology and possible therapeutic effects reviewed,” Journal of Inherited Metabolic Disease, vol. 31, no. 4, pp. 473–480, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. J. E. Wraith, M. Scarpa, M. Beck et al., “Mucopolysaccharidosis type II (Hunter syndrome): a clinical review and recommendations for treatment in the era of enzyme replacement therapy,” European Journal of Pediatrics, vol. 167, no. 3, pp. 267–277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. J. Z. Lu, E. K. Hui, R. J. Boado, and W. M. Pardridge, “Genetic engineering of a bifunctional IgG fusion protein with iduronate-2-sulfatase,” Bioconjugate Chemistry, vol. 21, no. 1, pp. 151–156, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. R. J. Boado and W. M. Pardridge, “Genetic engineering of IgG-glucuronidase fusion proteins,” Journal of Drug Targeting, vol. 18, no. 3, pp. 205–211, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Muyldermans and M. Lauwereys, “Unique single-domain antigen binding fragments derived from naturally occurring camel heavy-chain antibodies,” Journal of Molecular Recognition, vol. 12, pp. 131–140, 1999. View at Google Scholar
  76. A. S. Haqqani, C. E. Delaney, T. L. Tremblay, C. Sodja, J. K. Sandhu, and D. B. Stanimirovic, “Method for isolation and molecular characterization of extracellular microvesicles released from brain endothelial cells,” Barriers CNS, vol. 10, no. 1, article 4, 2013. View at Google Scholar
  77. R. H. J. van der Linden, L. G. J. Frenken, B. de Geus et al., “Comparison of physical chemical properties of llama V(HH) antibody fragments and mouse monoclonal antibodies,” Biochimica et Biophysica Acta, vol. 1431, no. 1, pp. 37–46, 1999. View at Publisher · View at Google Scholar · View at Scopus
  78. F. W. R. Brambell, W. A. Hemmings, and I. G. Morris, “A theoretical model of γ-globulin catabolism,” Nature, vol. 203, no. 4952, pp. 1352–1355, 1964. View at Publisher · View at Google Scholar · View at Scopus
  79. E. A. Jones and T. A. Waldmann, “The mechanism of intestinal uptake and transcellular transport of IgG in the neonatal rat,” Journal of Clinical Investigation, vol. 51, no. 11, pp. 2916–2927, 1972. View at Google Scholar · View at Scopus
  80. E. J. Israel, V. K. Patel, S. F. Taylor, A. Marshak-Rothstein, and N. E. Sinister, “Requirement for a β2-microglobulin-associated Fc receptor for acquisition of maternal IgG by fetal and neonatal mice,” Journal of Immunology, vol. 154, no. 12, pp. 6246–6251, 1995. View at Google Scholar · View at Scopus
  81. N. E. Simister and K. E. Mostov, “An Fc receptor structurally related to MHC class I antigens,” Nature, vol. 337, no. 6203, pp. 184–187, 1989. View at Google Scholar · View at Scopus
  82. E. J. Israel, S. Taylor, Z. Wu et al., “Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells,” Immunology, vol. 92, no. 1, pp. 69–74, 1997. View at Google Scholar · View at Scopus
  83. F. Schlachetzki, C. Zhu, and W. M. Pardridge, “Expression of the neonatal Fc receptor (FcRn) at the blood-brain barrier,” Journal of Neurochemistry, vol. 81, no. 1, pp. 203–206, 2002. View at Publisher · View at Google Scholar · View at Scopus
  84. U. Shah, B. L. Dickinson, R. S. Blumberg, N. E. Simister, W. I. Lencer, and W. A. Walker, “Distribution of the IgG Fc receptor, FcRn, in the human fetal intestine,” Pediatric Research, vol. 53, no. 2, pp. 295–301, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. M. Yoshida, A. Masuda, T. T. Kuo et al., “IgG transport across mucosal barriers by neonatal Fc receptor for IgG and mucosal immunity,” Springer Seminars in Immunopathology, vol. 28, no. 4, pp. 397–403, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Akilesh, G. J. Christianson, D. C. Roopenian, and A. S. Shaw, “Neonatal FcR expression in bone marrow-derived cells functions to protect serum IgG from catabolism,” Journal of Immunology, vol. 179, no. 7, pp. 4580–4588, 2007. View at Google Scholar · View at Scopus
  87. D. C. Roopenian and S. Akilesh, “FcRn: the neonatal Fc receptor comes of age,” Nature Reviews Immunology, vol. 7, no. 9, pp. 715–725, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. K. M. McCarthy, Y. Yoong, and N. E. Simister, “Bidirectional transcytosis of IgG by the rat neonatal Fc receptor expressed in a rat kidney cell line: a system to study protein transport across epithelia,” Journal of Cell Science, vol. 113, part 7, pp. 1277–1285, 2000. View at Google Scholar · View at Scopus
  89. M. A. Wani, L. D. Haynes, J. Kim et al., “Familial hypercatabolic hypoproteinemia caused by deficiency of the neonatal Fc receptor, FcRn, due to a mutant β2-microglobulin gene,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 13, pp. 5084–5089, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. E. J. Israel, D. F. Wilsker, K. C. Hayes, D. Schoenfeld, and N. E. Simister, “Increased clearance of IgG in mice that lack β2-microglobulin: possible protective role of FcRn,” Immunology, vol. 89, no. 4, pp. 573–578, 1996. View at Google Scholar · View at Scopus
  91. R. P. Junghans and C. L. Anderson, “The protection receptor for IgG catabolism is the β2-microglobulin-containing neonatal intestinal transport receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 11, pp. 5512–5516, 1996. View at Google Scholar · View at Scopus
  92. C. Medesan, D. Matesoi, C. Radu, V. Ghetie, and E. S. Ward, “Delineation of the Amino Acid Residues Involved in Transcytosis and Catabolism of Mouse IgG1,” Journal of Immunology, vol. 158, no. 5, pp. 2211–2217, 1997. View at Google Scholar · View at Scopus
  93. C. Medesan, C. Radu, J. Kim, V. Ghetie, and E. S. Ward, “Localization of the site of the IgG molecule that regulates maternofetal transmission in mice,” European Journal of Immunology, vol. 26, no. 10, pp. 2533–2536, 1996. View at Publisher · View at Google Scholar · View at Scopus
  94. D. E. Vaughn, C. M. Milburn, D. M. Penny, W. L. Martin, J. L. Johnson, and P. J. Bjorkman, “Identification of critical IgG binding epitopes on the neonatal Fc receptor,” Journal of Molecular Biology, vol. 274, no. 4, pp. 597–607, 1997. View at Publisher · View at Google Scholar · View at Scopus
  95. W. Wang, P. Lu, Y. Fang et al., “Monoclonal antibodies with identical Fc sequences can bind to FcRn differentially with pharmacokinetic consequences,” Drug Metabolism and Disposition, vol. 39, no. 9, pp. 1469–1477, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. D. C. Roopenian, G. J. Christianson, T. J. Sproule et al., “The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs,” Journal of Immunology, vol. 170, no. 7, pp. 3528–3533, 2003. View at Google Scholar · View at Scopus
  97. K. J. Vincent and M. Zurini, “Current strategies in antibody engineering: Fc engineering and pH-dependent antigen binding, bispecific antibodies and antibody drug conjugates,” Biotechnology Journal, vol. 7, pp. 1444–1450, 2012. View at Publisher · View at Google Scholar
  98. W. F. Dall'Acqua, P. A. Kiener, and H. Wu, “Properties of Human IgG1s engineered for enhanced binding to the neonatal Fc Receptor (FcRn),” Journal of Biological Chemistry, vol. 281, no. 33, pp. 23514–23524, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. P. R. Hinton, J. M. Xiong, M. G. Johlfs, M. T. Tang, S. Keller, and N. Tsurushita, “An engineered human IgG1 antibody with longer serum half-life,” Journal of Immunology, vol. 176, no. 1, pp. 346–356, 2006. View at Google Scholar · View at Scopus
  100. J. E. Mikulska, “The neonatal receptor Fc gamma(FcRn)—structure and function,” Postepy Higieny i Medycyny Doswiadczalnej, vol. 55, no. 4, pp. 487–511, 2001. View at Google Scholar · View at Scopus
  101. R. J. Hansen and J. P. Balthasar, “Intravenous immunoglobulin mediates an increase in anti-platelet antibody clearance via the FcRn receptor,” Thrombosis and Haemostasis, vol. 88, no. 6, pp. 898–899, 2002. View at Google Scholar · View at Scopus
  102. A. J. Bitonti and J. A. Dumont, “Pulmonary administration of therapeutic proteins using an immunoglobulin transport pathway,” Advanced Drug Delivery Reviews, vol. 58, no. 9-10, pp. 1106–1118, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Deane, A. Sagare, K. Hamm et al., “IgG-assisted age-dependent clearance of Alzheimer's amyloid β peptide by the blood-brain barrier neonatal Fc receptor,” Journal of Neuroscience, vol. 25, no. 50, pp. 11495–11503, 2005. View at Publisher · View at Google Scholar · View at Scopus
  104. R. T. Peters, G. Toby, Q. Lu et al., “Biochemical and functional characterization of a recombinant monomeric Factor VIII-Fc fusion protein,” Journal of Thrombosis and Haemostasis, vol. 11, no. 1, pp. 132–141, 2013. View at Google Scholar
  105. J. T. Sockolosky, M. R. Tiffany, and F. C. Szoka, “Engineering neonatal Fc receptor-mediated recycling and transcytosis in recombinant proteins by short terminal peptide extensions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 16095–16100, 2012. View at Publisher · View at Google Scholar
  106. M. Yu, F. Du, H. Ise et al., “Preparation and characterization of a VEGF-Fc fusion protein matrix for enhancing HUVEC growth,” Biotechnology Letters, vol. 34, pp. 1765–1771, 2012. View at Publisher · View at Google Scholar
  107. M. J. Manco-Johnson, T. C. Abshire, A. D. Shapiro et al., “Prophylaxis versus episodic treatment to prevent joint disease in boys with severe hemophilia,” The New England Journal of Medicine, vol. 357, no. 6, pp. 535–544, 2007. View at Publisher · View at Google Scholar · View at Scopus