Transferrin receptor (TfR) trafficking determines brain uptake of TfR antibody affinity variants

Journal of Experimental Medicine

Volumn 211, Issue 2, 2014, Pages 233-244

  Bien Ly, Nga ^a   Yu, Y Joy ^a   Bumbaca, Daniela ^a   Elstrott, Justin ^a   Boswell, C Andrew ^a   Zhang, Yin ^a   Luk, Wilman ^a   Lu, Yanmei ^a   Dennis, Mark S ^a   Weimer, Robby M ^a   Chung, Inhee ^a   Watts, Ryan J ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIBODIES, BISPECIFIC; ANTIBODY AFFINITY; ASPARTIC ACID ENDOPEPTIDASES; BLOOD-BRAIN BARRIER; BRAIN; FEMALE; LYSOSOMES; MICE; MICE, INBRED C57BL; PROTEIN TRANSPORT; RECEPTORS, TRANSFERRIN; TRANSCYTOSIS;

EID: 84893754100     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20131660     Document Type: Article

References (25)

1. Atwal, J.K., Y. Chen, C. Chiu, D.L. Mortensen, W.J. Meilandt, Y. Liu, C.E. Heise, K. Hoyte, W. Luk, Y. Lu, et al. 2011. A therapeutic antibody targeting BACE1 inhibits amyloid-β production in vivo. Sci. Transl. Med. 3:84ra43. http://dx.doi.org/10.1126/scitranslmed.3002254
2. Bien-Ly, N., A.K. Gillespie, D. Walker, S.Y. Yoon, and Y. Huang. 2012. Reducing human apolipoprotein E levels attenuates age-dependent Aβ accumulation in mutant human amyloid precursor protein transgenic mice. J. Neurosci. 32:4803-4811. http://dx.doi.org/10.1523/JNEUROSCI.0033-12.2012
3. Boswell, C.A., D. Bumbaca, P.J. Fielder, and L.A. Khawli. 2012. Compartmental tissue distribution of antibody therapeutics: experimental approaches and interpretations. AAPS J. 14:612-618. http://dx.doi.org/10.1208/s12248-012-9374-1
4. Chizzonite, R., T. Truitt, F.J. Podlaski, A.G. Wolitzky, P.M. Quinn, P. Nunes, A.S. Stern, and M.K. Gately. 1991. IL-12: monoclonal antibodies specific for the 40-kDa subunit block receptor binding and biologic activity on activated human lymphoblasts. J. Immunol. 147:1548-1556.
5. Chung, I., R. Akita, R. Vandlen, D. Toomre, J. Schlessinger, and I. Mellman. 2010. Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature. 464:783-787. http://dx.doi.org/10.1038/nature08827
6. Couch, J.A., Y.J. Yu, Y. Zhang, J.M. Tarrant, R.N. Fuji, W.J. Meilandt, H. Solanoy, R.K. Tong, K. Hoyte, W. Luk, et al. 2013. Addressing safety liabilities of Tf R bispecific antibodies that cross the blood-brain barrier. Sci. Transl. Med. 5:183ra57. http://dx.doi.org/10.1126/scitranslmed.3005338
7. Dautry-Varsat, A., A. Ciechanover, and H.F. Lodish. 1983. pH and the recycling of transferrin during receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA. 80:2258-2262. http://dx.doi.org/10.1073/pnas.80.8.2258
8. Dufès, C., M. Al Robaian, and S. Somani. 2013. Transferrin and the transferrin receptor for the targeted delivery of therapeutic agents to the brain and cancer cells. Ther. Deliv. 4:629-640. http://dx.doi.org/10.4155/tde.13.21
9. Fishman, J.B., J.B. Rubin, J.V. Handrahan, J.R. Connor, and R.E. Fine. 1987. Receptor-mediated transcytosis of transferrin across the blood-brain barrier. J. Neurosci. Res. 18:299-304. http://dx.doi.org/10.1002/jnr.490180206
10. Gosk, S., C. Vermehren, G. Storm, and T. Moos. 2004. Targeting anti-transferrin receptor antibody (OX26) and OX26-conjugated liposomes to brain capillary endothelial cells using in situ perfusion. J. Cereb. Blood Flow Metab. 24:1193-1204. http://dx.doi.org/10.1097/01.WCB.0000135592.28823.47
11. Holtmaat, A., T. Bonhoeffer, D.K. Chow, J. Chuckowree, V. De Paola, S.B. Hofer, M. Hübener, T. Keck, G. Knott, W.C. Lee, et al. 2009. Long-term, highresolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4:1128-1144. http://dx.doi.org/10.1038/nprot.2009.89
12. Jefferies, W.A., M.R. Brandon, S.V. Hunt, A.F. Williams, K.C. Gatter, and D.Y. Mason. 1984. Transferrin receptor on endothelium of brain capillaries. Nature. 312:162-163. http://dx.doi.org/10.1038/312162a0
13. Jones, A.R., and E.V. Shusta. 2007. Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm. Res. 24:1759-1771. http://dx.doi.org/10.1007/s11095-007-9379-0
14. Kissel, K., S. Hamm, M. Schulz, A. Vecchi, C. Garlanda, and B. Engelhardt. 1998. Immunohistochemical localization of the murine transferrin receptor (Tf R) on blood-tissue barriers using a novel anti-Tf R monoclonal antibody. Histochem. Cell Biol. 110:63-72. http://dx.doi.org/10.1007/s004180050266
15. Manich, G., I. Cabezón, J. del Valle, J. Duran-Vilaregut, A. Camins, M. Pallàs, C. Pelegrí, and J. Vilaplana. 2013. Study of the transcytosis of an anti-transferrin receptor antibody with a Fab' cargo across the blood-brain barrier in mice. Eur. J. Pharm. Sci. 49:556-564. http://dx.doi.org/10.1016/j.ejps.2013.05.027
16. Matsui, T., T. Itoh, and M. Fukuda. 2011. Small GTPase Rab12 regulates constitutive degradation of transferrin receptor. Traffic. 12:1432-1443. http://dx.doi.org/10.1111/j.1600-0854.2011.01240.x
17. Moos, T., and E.H. Morgan. 2001. Restricted transport of anti-transferrin receptor antibody (OX26) through the blood-brain barrier in the rat. J. Neurochem. 79:119-129. http://dx.doi.org/10.1046/j.1471-4159.2001.00541.x
18. Paris-Robidas, S., V. Emond, C. Tremblay, D. Soulet, and F. Calon. 2011. In vivo labeling of brain capillary endothelial cells after intravenous injection of monoclonal antibodies targeting the transferrin receptor. Mol. Pharmacol. 80:32-39. http://dx.doi.org/10.1124/mol.111.071027
19. Predescu, S.A., D.N. Predescu, and A.B. Malik. 2007. Molecular determinants of endothelial transcytosis and their role in endothelial permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 293:L823-L842. http://dx.doi.org/10.1152/ajplung.00436.2006
20. Roberts, R.L., R.E. Fine, and A. Sandra. 1993. Receptor-mediated endocytosis of transferrin at the blood-brain barrier. J. Cell Sci. 104:521-532.
21. Rubin, L.L., and J.M. Staddon. 1999. The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 22:11-28. http://dx.doi.org/10.1146/annurev.neuro.22.1.11
22. Sheff, D., L. Pelletier, C.B. O'Connell, G. Warren, and I. Mellman. 2002. Transferrin receptor recycling in the absence of perinuclear recycling endosomes. J. Cell Biol. 156:797-804. http://dx.doi.org/10.1083/jcb.20111048
23. Traer, C.J., A.C. Rutherford, K.J. Palmer, T. Wassmer, J. Oakley, N. Attar, J.G. Carlton, J. Kremerskothen, D.J. Stephens, and P.J. Cullen. 2007. SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat. Cell Biol. 9:1370-1380. http://dx.doi.org/10.1038/ncb1656
24. Yu, Y.J., and R.J. Watts. 2013. Developing therapeutic antibodies for neurodegenerative disease. Neurotherapeutics. 10:459-472. http://dx.doi.org/10.1007/s13311-013-0187-4
25. Yu, Y.J., Y. Zhang, M. Kenrick, K. Hoyte, W. Luk, Y. Lu, J. Atwal, J.M. Elliott, S. Prabhu, R.J. Watts, and M.S. Dennis. 2011. Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target. Sci. Transl. Med. 3:84ra44. http://dx.doi.org/10.1126/scitranslmed.3002230