Probing the extracellular diffusion of antibodies in brain using in vivo integrative optical imaging and ex vivo fluorescence imaging

Journal of Controlled Release

Volumn 197, Issue , 2015, Pages 78-86

  Wolak, Daniel J ^a   Pizzo, Michelle E ^a   Thorne, Robert G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Antibody; Diffusion; Drug delivery; Extracellular space; Intracisternal; Intraparenchymal

Indexed keywords

BINDING ENERGY; BLOOD VESSELS; BODY FLUIDS; BRAIN; CEREBROSPINAL FLUID; DIFFUSION; DIFFUSION IN LIQUIDS; DRUG DELIVERY; ENZYME ACTIVITY; FLUORESCENCE; OPTICAL IMAGE STORAGE; TRANSPORT PROPERTIES;

CENTRAL NERVOUS SYSTEMS; CEREBRAL BLOOD VESSELS; EFFECTIVE DIFFUSION COEFFICIENTS; EXTRACELLULAR DIFFUSION; EXTRACELLULAR SPACE; INTRACISTERNAL; INTRAPARENCHYMAL; THERAPEUTIC ANTIBODIES;

ANTIBODIES;

FC RECEPTOR; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DIFFUSION COEFFICIENT; EX VIVO STUDY; EXTRACELLULAR SPACE; FEMALE; FLUORESCENCE IMAGING; GEOMETRY; IN VIVO STUDY; MICROENVIRONMENT; MOLECULAR SIZE; NEOCORTEX; NONHUMAN; RAT; ANIMAL; DIFFUSION; METABOLISM; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; DIFFUSION; EXTRACELLULAR SPACE; FEMALE; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; NEOCORTEX; OPTICAL IMAGING; RATS, SPRAGUE-DAWLEY; RECEPTORS, IGG;

EID: 84911425316     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.10.034     Document Type: Article

References (53)

1. W. Wang, E.Q. Wang, J.P. Balthasar, Monoclonal antibody pharmacokinetics and pharmacodynamics, Clin. Pharmacol. Ther. 84 (2008) 548-558.
2. G.L. Hortin, D. Sviridov, N.L. Anderson, High-abundance polypeptides of the human plasma proteome comprising the top 4 logs of polypeptide abundance, Clin. Chem. 54 (2008) 1608-1616.
3. H. Davson, M.B. Segal, Physiology of the CSF and Blood-Brain Barriers, CRC Press, Boca Raton, 1996.
4. S. Sandin, L.G. Ofverstedt, A.C. Wikstrom, O. Wrange, U. Skoglund, Structure and flexibility of individual immunoglobulin G molecules in solution, Structure 12 (2004) 409-415.
5. P. Holliger, P.J. Hudson, Engineered antibody fragments and the rise of single domains, Nat. Biotechnol. 23 (2005) 1126-1136.
6. E. Okun, M.P. Mattson, T.V. Arumugam, Involvement of Fc receptors in disorders of the central nervous system, Neruomol. Med. 12 (2010) 164-178.
7. H.A. Mohamed, D.R. Mosier, L.L. Zou, L. Siklos, M.E. Alexianu, J.I. Engelhardt, D.R. Beers, W.D. Le, S.H. Appel, Immunoglobulin Fc gamma receptor promotes immunoglobulin uptake, immunoglobulin-mediated calcium increase, and neurotransmitter release in motor neurons, J. Neurosci. Res. 69 (2002) 110-116.
8. M. Komine-Kobayashi, N. Chou, H. Mochizuki, A. Nakao, Y. Mizuno, T. Urabe, Dual role of Fcgamma receptor in transient focal cerebral ischemia in mice, Stroke 35 (2004) 958-963.
9. R.J.Y. Ho, M. Gibaldi, Biotechnology and Biopharmaceuticals: Transforming Proteins and Genes into Drugs, Second ed. Wiley-Blackwell, Hoboken, N.J., 2013
10. L.A. Lampson, Monoclonal antibodies in neuro-oncology: getting past the blood-brain barrier, MAbs 3 (2011) 153-160.
11. E.A. Neuwelt, P.A. Barnett, I. Hellstrom, K.E. Hellstrom, P. Beaumier, C.I. McCormick, R.M. Weigel, Delivery of melanoma-associated immunoglobulin monoclonal antibody and Fab fragments to normal brain utilizing osmotic blood-brain barrier disruption, Cancer Res. 48 (1988) 4725-4729.
12. R. Deane, A. Sagare, K. Hamm, M. Parisi, B. LaRue, H. Guo, Z. Wu, D.M. Holtzman, B.V. Zlokovic, IgG-assisted age-dependent clearance of Alzheimer's amyloid beta peptide by the blood-brain barrier neonatal Fc receptor, J. Neurosci. 25 (2005) 11495-11503.
13. D.R. Thakker, M.R. Weatherspoon, J. Harrison, T.E. Keene, D.S. Lane, W.F. Kaemmerer, G.R. Stewart, L.L. Shafer, Intracerebroventricular amyloid-beta antibodies reduce cerebral amyloid angiopathy and associatedmicro-hemorrhages in aged Tg2576mice, Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 4501-4506.
14. J. Moreth, C. Mavoungou, K. Schindowski, Passive anti-amyloid immunotherapy in Alzheimer's disease: what are the most promising targets? Immun. Ageing 10 (2013) 18.
15. M. Hammarlund-Udenaes, E.C.M.d. Lange, R.G. Thorne, Drug Delivery to the Brain: Physiological Concepts, Methodologies and Approaches, Springer, New York; Heidelberg, 2014.
16. Y.J. Yu, Y. Zhang, M. Kenrick, K. Hoyte, W. Luk, Y. Lu, J. Atwal, J.M. Elliott, S. Prabhu, R.J. Watts, M.S. Dennis, Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target, Sci. Transl. Med. 3 (2011) 84ra44.
17. D.J. Wolak, R.G. Thorne, Diffusion of macromolecules in the brain: implications for drug delivery, Mol. Pharm. 10 (2013) 1492-1504.
18. E. Sykova, C. Nicholson, Diffusion in brain extracellular space, Physiol. Rev. 88 (2008) 1277-1340.
19. R.G. Thorne, C. Nicholson, In vivo diffusion analysiswith quantum dots and dextrans predicts the width of brain extracellular space, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 5567-5572.
20. C. Nicholson, L. Tao, Hindered diffusion of high molecular weight compounds in brain extracellular microenvironment measured with integrative optical imaging, Biophys. J. 65 (1993) 2277-2290.
21. S. Hrabetova, J. Hrabe, C. Nicholson, Dead-space microdomains hinder extracellular diffusion in rat neocortex during ischemia, J. Neurosci. 23 (2003) 8351-8359.
22. R.G. Thorne, A. Lakkaraju, E. Rodriguez-Boulan, C. Nicholson, In vivo diffusion of lactoferrin in brain extracellular space is regulated by interactions with heparan sulfate, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 8416-8421.
23. R.G. Thorne, S. Hrabetova, C. Nicholson, Diffusion of epidermal growth factor in rat brain extracellular space measured by integrative optical imaging, J. Neurophysiol. 92 (2004) 3471-3481.
24. L.J. Harris, E. Skaletsky, A. McPherson, Crystallographic structure of an intact IgG1 monoclonal antibody, J. Mol. Biol. 275 (1998) 861-872.
25. S. Ryazantsev, V. Tischenko, C. Nguyen, V. Abramov, V. Zav'yalov, Three-dimensional structure of the human myeloma IgG2, PLoS One 8 (2013) e64076.
26. L. Tao, C. Nicholson, The three-dimensional point spread functions of a microscope objective in image and object space, J. Microsc. 178 (1995) 267-271.
27. L. Tao, C. Nicholson, Diffusion of albumins in rat cortical slices and relevance to volume transmission, Neuroscience 75 (1996) 839-847.
28. S.J. Cragg, C. Nicholson, J. Kume-Kick, L. Tao, M.E. Rice, Dopamine-mediated volume transmission inmidbrain is regulated by distinct extracellular geometry and uptake, J. Neurophysiol. 85 (2001) 1761-1771.
29. S. Prokopova-Kubinova, L. Vargova, L. Tao, K. Ulbrich, V. Subr, E. Sykova, C. Nicholson, Poly[N-(2-hydroxypropyl)methacrylamide] polymers diffuse in brain extracellular space with same tortuosity as small molecules, Biophys. J. 80 (2001) 542-548.
30. C.S. Patlak, J.D. Fenstermacher, Measurements of dog blood-brain transfer constants by ventriculocisternal perfusion, Am. J. Physiol. 229 (1975) 877-884.
31. C. Nicholson, Diffusion and related transport mechanisms in brain tissue, Rep. Prog. Phys. 64 (2001) 815-884.
32. J.J. Iliff, H. Lee, M. Yu, T. Feng, J. Logan, M. Nedergaard, H. Benveniste, Brain-wide pathway for waste clearance captured by contrast-enhanced MRI, J. Clin. Invest. 123 (2013) 1299-1309.
33. W.M. Deen, Hindered transport of large molecules in liquid-filled pores, AIChE J 33 (1987) 1409-1425.
34. J.G. van de Winkel, C.L. Anderson, Biology of human immunoglobulin G Fc receptors, J. Leukoc. Biol. 49 (1991) 511-524.
35. J. Fenstermacher, T. Kaye, Drug "diffusion" within the brain, Ann. N. Y. Acad. Sci. 531 (1988) 29-39.
36. M.A. Clauss, R.K. Jain, Interstitial transport of rabbit and sheep antibodies in normal and neoplastic tissues, Cancer Res. 50 (1990) 3487-3492.
37. W.M. Saltzman, M.L. Radomsky, K.J.Whaley, R.A. Cone, Antibody diffusion in human cervical mucus, Biophys. J. 66 (1994) 508-515.
38. L. Shi, M. Zeng, Y. Sun, B.M. Fu, Quantification of blood-brain barrier solute permeability and brain transport by multiphoton microscopy, J. Biomech. Eng. 136 (2014) 031005.
39. D. McLean, M.J. Cooke, Y. Wang, P. Fraser, P. St George-Hyslop, M.S. Shoichet, Targeting the amyloid-beta antibody in the brain tissue of a mouse model of Alzheimer's disease, J. Control. Release 159 (2012) 302-308.
40. Y. Wang, M.J. Cooke, Y. Lapitsky, R.G. Wylie, N. Sachewsky, D. Corbett, C.M. Morshead, M.S. Shoichet, Transport of epidermal growth factor in the stroke-injured brain, J. Control. Release 149 (2011) 225-235.
41. Y. Zhang, W.M. Pardridge, Mediated efflux of IgG molecules from brain to blood across the blood-brain barrier, J. Neuroimmunol. 114 (2001) 168-172.
42. C. O'Hear, J. Foote, Antibody buffering in the brain, J. Mol. Biol. 364 (2006) 1003-1009.
43. P.H. Strausbauch, E. Hurwitz, D. Givol, Interchain disulfide bonds of goat immunoglobulin G, Biochemistry 10 (1971) 2231-2237.
44. F. Xiao, C. Nicholson, J. Hrabe, S. Hrabetova, Diffusion of flexible random-coil dextran polymers measured in anisotropic brain extracellular space by integrative optical imaging, Biophys. J. 95 (2008) 1382-1392.
45. H.L. Gao, C.Y. Li, F.X. Ma, K. Wang, J.J. Xu, H.Y. Chen, X.H. Xia, A nanochannel array based device for determination of the isoelectric point of confined proteins, Phys. Chem. Chem. Phys. 14 (2012) 9460-9467.
46. J.F. Ghersi-Egea, W. Finnegan, J.L. Chen, J.D. Fenstermacher, Rapid distribution of intraventricularly administered sucrose into cerebrospinal fluid cisterns via subarachnoid velae in rat, Neuroscience 75 (1996) 1271-1288.
47. J.J. Iliff, M. Wang, Y. Liao, B.A. Plogg, W. Peng, G.A. Gundersen, H. Benveniste, G.E. Vates, R. Deane, S.A. Goldman, E.A. Nagelhus, M. Nedergaard, A paravascular pathway facilitates CSF fl ow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta, Sci. Transl. Med. 4 (2012) 147ra111.
48. R.G. Thorne, Primer on central nervous system structure/function and vasculature, ventricular system, and fluids of the brain, in: M. Hammarlund-Udenaes, E.C.M.d. Lange, R.G. Thorne (Eds.), Drug Delivery to the Brain: Physiological Concepts, Methodologies and Approaches, Springer, New York; Heidelberg, 2014, pp. 685-707.
49. R.D. Broadwell, M.V. Sofroniew, Serum proteins bypass the blood-brain fluid barriers for extracellular entry to the central nervous system, Exp. Neurol. 120 (1993) 245-263.
50. R.J. Ziegler, E.A. Salegio, J.C. Dodge, J. Bringas, C.M. Treleaven, S.D. Bercury, T.J. Tamsett, L. Shihabuddin, P. Hadaczek, M. Fiandaca, K. Bankiewicz, R.K. Scheule, Distribution of acid sphingomyelinase in rodent and non-human primate brain after intracerebroventricular infusion, Exp. Neurol. 231 (2011) 261-271.
51. G. Paxinos, K.B.J. Franklin, The Mouse Brain in Stereotaxic Coordinates, Compact, 2nd ed. Elsevier Academic Press, Amsterdam; Boston, 2004.
52. R.F. Martin, D.M. Bowden, Primate Brain Maps: Structure of the Macaque Brain, Elsevier, Amsterdam; New York, 2000, p. viii (160 pp.).
53. D.R. Groothuis, M.W. Vavra, K.E. Schlageter, E.W. Kang, A.C. Itskovich, S. Hertzler, C.V. Allen, H.L. Lipton, Efflux of drugs and solutes from brain: the interactive roles of diffusional transcapillary transport, bulk flow and capillary transporters, J. Cereb. Blood Flow Metab. 27 (2007) 43-56.