Multiplexed evaluation of serum and CSF pharmacokinetics of brain-targeting single-domain antibodies using a NanoLC-SRM-ILIS method

Molecular Pharmaceutics

Volumn 10, Issue 5, 2013, Pages 1542-1556

  Haqqani, Arsalan S ^a   Caram Salas, Nadia ^a   Ding, Wen ^a   Brunette, Eric ^a   Delaney, Christie E ^a   Baumann, Ewa ^a   Boileau, Eve ^a   Stanimirovic, Danica ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

blood brain barrier; CSF; drug delivery; mass spectrometry; MRM; pharmacokinetics; single domain antibodies; SRM

Indexed keywords

FC44 ANTIBODY; FC5 ANTIBODY; NANOBODY; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN CELL; BRAIN ENDOTHELIAL CELL; CEREBROSPINAL FLUID; CONTROLLED STUDY; DRUG CEREBROSPINAL FLUID LEVEL; ENDOTHELIUM CELL; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; IN VITRO STUDY; ISOTOPE LABELING; LIMIT OF DETECTION; LIMIT OF QUANTITATION; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PHAGE DISPLAY; PLASMA HALF LIFE; PRIORITY JOURNAL; TREATMENT DURATION; ANIMAL; BLOOD; BRAIN; CELL CULTURE; DRUG DELIVERY SYSTEM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOASSAY; IMMUNOLOGY; MASS SPECTROMETRY; METABOLISM; NANOTECHNOLOGY; PROCEDURES; PROTEIN TRANSPORT; RAT; TISSUE DISTRIBUTION; WISTAR RAT;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DRUG DELIVERY SYSTEMS; ENDOTHELIAL CELLS; HUMANS; IMMUNOASSAY; MALE; MASS SPECTROMETRY; NANOTECHNOLOGY; PROTEIN TRANSPORT; RATS; RATS, WISTAR; SINGLE-DOMAIN ANTIBODIES; TISSUE DISTRIBUTION;

EID: 84877255599     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp3004995     Document Type: Article

References (54)

1. Neuwelt, E. A.; Bauer, B.; Fahlke, C.; Fricker, G.; Iadecola, C.; Janigro, D.; Leybaert, L.; Molnar, Z.; O'Donnell, M. E.; Povlishock, J. T.; Saunders, N. R.; Sharp, F.; Stanimirovic, D.; Watts, R. J.; Drewes, L. R. Engaging neuroscience to advance translational research in brain barrier biology Nat. Rev. Neurosci. 2011, 12, 169-182
2. Pardridge, W. M. Drug and gene delivery to the brain: the vascular route Neuron 2002, 36, 555-558
3. Pardridge, W. M.; Buciak, J. L.; Friden, P. M. Selective transport of an anti-transferrin receptor antibody through the blood-brain barrier in vivo J. Pharmacol. Exp. Ther. 1991, 259, 66-70
4. Yu, Y. J.; Zhang, Y.; Kenrick, M.; Hoyte, K.; Luk, W.; Lu, Y.; Atwal, J.; Elliott, J. M.; Prabhu, S.; Watts, R. J.; Dennis, M. S. Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target Sci. Transl. Med. 2011, 3, 84ra44
5. Boado, R. J.; Hui, E. K.; Lu, J. Z.; Zhou, Q. H.; Pardridge, W. M. Selective targeting of a TNFR decoy receptor pharmaceutical to the primate brain as a receptor-specific IgG fusion protein J. Biotechnol. 2010, 146, 84-91
6. Ohshima-Hosoyama, S.; Hosoyama, T.; Nelon, L. D.; Keller, C. IGF-1 receptor inhibition by picropodophyllin in medulloblastoma Biochem. Biophys. Res. Commun. 2010, 399, 727-732
7. Demeule, M.; Currie, J. C.; Bertrand, Y.; Che, C.; Nguyen, T.; Regina, A.; Gabathuler, R.; Castaigne, J. P.; Beliveau, R. Involvement of the low-density lipoprotein receptor-related protein in the transcytosis of the brain delivery vector angiopep-2 J. Neurochem. 2008, 106, 1534-1544
8. Gabathuler, R. Development of new peptide vectors for the transport of therapeutic across the blood-brain barrier Ther. Delivery 2010, 1, 571-586
9. Gonzalez, A. M.; Leadbeater, W. E.; Burg, M.; Sims, K.; Terasaki, T.; Johanson, C. E.; Stopa, E. G.; Eliceiri, B. P.; Baird, A. Targeting choroid plexus epithelia and ventricular ependyma for drug delivery to the central nervous system BMC Neurosci. 2011, 12, 4
10. Muruganandam, A.; Tanha, J.; Narang, S.; Stanimirovic, D. Selection of phage-displayed llama single-domain antibodies that transmigrate across human blood-brain barrier endothelium FASEB J. 2002, 16, 240-242
11. Tanha, J.; Muruganandam, A.; Stanimirovic, D. Phage display technology for identifying specific antigens on brain endothelial cells Methods Mol. Med. 2003, 89, 435-449
12. Tanha, J.; Dubuc, G.; Hirama, T.; Narang, S. A.; MacKenzie, C. R. Selection by phage display of llama conventional V(H) fragments with heavy chain antibody V(H)H properties J. Immunol. Methods 2002, 263, 97-109
13. Hamers-Casterman, C.; Atarhouch, T.; Muyldermans, S.; Robinson, G.; Hamers, C.; Songa, E. B.; Bendahman, N.; Hamers, R. Naturally occurring antibodies devoid of light chains Nature 1993, 363, 446-448
14. Abulrob, A.; Sprong, H.; Van Bergen en, H. P.; Stanimirovic, D. The blood-brain barrier transmigrating single domain antibody: mechanisms of transport and antigenic epitopes in human brain endothelial cells J. Neurochem. 2005, 95, 1201-1214
15. Kondrat, r. w.; McClusky, g. a.; Cooks, R. G. Multiple reaction monitoring in mass spectrometry/mass spectrometry for direct analysis of complex mixtures Anal. Chem. 1978, 50, 2017-2021
16. Gergov, M.; Ojanpera, I.; Vuori, E. Simultaneous screening for 238 drugs in blood by liquid chromatography-ion spray tandem mass spectrometry with multiple-reaction monitoring J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 2003, 795, 41-53
17. Ackermann, B. L.; Berna, M. J. Coupling immunoaffinity techniques with MS for quantitative analysis of low-abundance protein biomarkers Expert Rev. Proteomics 2007, 4, 175-186
18. Barnidge, D. R.; Goodmanson, M. K.; Klee, G. G.; Muddiman, D. C. Absolute quantification of the model biomarker prostate-specific antigen in serum by LC-Ms/MS using protein cleavage and isotope dilution mass spectrometry J. Proteome Res. 2004, 3, 644-652
19. Kamiie, J.; Ohtsuki, S.; Iwase, R.; Ohmine, K.; Katsukura, Y.; Yanai, K.; Sekine, Y.; Uchida, Y.; Ito, S.; Terasaki, T. Quantitative atlas of membrane transporter proteins: development and application of a highly sensitive simultaneous LC/MS/MS method combined with novel in-silico peptide selection criteria Pharm. Res. 2008, 25, 1469-1483
20. Kirkpatrick, D. S.; Gerber, S. A.; Gygi, S. P. The absolute quantification strategy: a general procedure for the quantification of proteins and post-translational modifications Methods 2005, 35, 265-273
21. Kuhn, E.; Wu, J.; Karl, J.; Liao, H.; Zolg, W.; Guild, B. Quantification of C-reactive protein in the serum of patients with rheumatoid arthritis using multiple reaction monitoring mass spectrometry and 13C-labeled peptide standards Proteomics 2004, 4, 1175-1186
22. Zhang, F.; Bartels, M. J.; Stott, W. T. Quantitation of human glutathione S-transferases in complex matrices by liquid chromatography/tandem mass spectrometry with signature peptides Rapid Commun. Mass Spectrom. 2004, 18, 491-498
23. Shen, D. D.; Artru, A. A.; Adkison, K. K. Principles and applicability of CSF sampling for the assessment of CNS drug delivery and pharmacodynamics Adv. Drug Delivery Rev. 2004, 56, 1825-1857
24. Lin, J. H. CSF as a surrogate for assessing CNS exposure: an industrial perspective Curr. Drug Metab. 2008, 9, 46-59
25. Bell, A.; Wang, Z. J.; Arbabi-Ghahroudi, M.; Chang, T. A.; Durocher, Y.; Trojahn, U.; Baardsnes, J.; Jaramillo, M. L.; Li, S.; Baral, T. N.; O'Connor-McCourt, M.; MacKenzie, R.; Zhang, J. Differential tumor-targeting abilities of three single-domain antibody formats Cancer Lett. 2010, 289, 81-90
26. Iqbal, U.; Trojahn, U.; Albaghdadi, H.; Zhang, J.; O'Connor-McCourt, M.; Stanimirovic, D.; Tomanek, B.; Sutherland, G.; Abulrob, A. Kinetic analysis of novel mono- and multivalent VHH-fragments and their application for molecular imaging of brain tumours Br. J. Pharmacol. 2010, 160, 1016-1028
27. McCafferty, J.; Griffiths, A. D.; Winter, G.; Chiswell, D. J. Phage antibodies: filamentous phage displaying antibody variable domains Nature 1990, 348, 552-554
28. Hussack, G.; Arbabi-Ghahroudi, M.; van Faassen, H.; Songer, J. G.; Ng, K. K.; MacKenzie, R.; Tanha, J. Neutralization of Clostridium difficile toxin A with single-domain antibodies targeting the cell receptor binding domain J. Biol. Chem. 2011, 286, 8961-8976
29. Zhang, J.; Tanha, J.; Hirama, T.; Khieu, N. H.; To, R.; Tong-Sevinc, H.; Stone, E.; Brisson, J. R.; MacKenzie, C. R. Pentamerization of single-domain antibodies from phage libraries: a novel strategy for the rapid generation of high-avidity antibody reagents J. Mol. Biol. 2004, 335, 49-56
30. Haqqani, A. S.; Kelly, J. F.; Stanimirovic, D. B. Quantitative protein profiling by mass spectrometry using label-free proteomics Methods Mol. Biol. 2008, 439, 241-256
31. Caljon, G.; Caveliers, V.; Lahoutte, T.; Stijlemans, B.; Ghassabeh, G. H.; Van Den, A. J.; Smolders, I.; De Baetselier, P.; Michotte, Y.; Muyldermans, S.; Magez, S.; Clinckers, R. Using microdialysis to analyse the passage of monovalent nanobodies through the blood-brain barrier Br. J. Pharmacol. 2012, 165, 2341-2353
32. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 1996, 68, 850-858
33. Garberg, P.; Ball, M.; Borg, N.; Cecchelli, R.; Fenart, L.; Hurst, R. D.; Lindmark, T.; Mabondzo, A.; Nilsson, J. E.; Raub, T. J.; Stanimirovic, D.; Terasaki, T.; Oberg, J. O.; Osterberg, T. In vitro models for the blood-brain barrier Toxicol. In Vitro 2005, 19, 299-334
34. Iqbal, U.; Abulrob, A.; Stanimirovic, D. B. Integrated platform for brain imaging and drug delivery across the blood-brain barrier Methods Mol. Biol. 2011, 686, 465-481
35. Nirogi, R.; Kandikere, V.; Mudigonda, K.; Bhyrapuneni, G.; Muddana, N.; Saralaya, R.; Benade, V. A simple and rapid method to collect the cerebrospinal fluid of rats and its application for the assessment of drug penetration into the central nervous system J. Neurosci. Methods 2009, 178, 116-119
36. Christenson, R. H.; Behlmer, P.; Howard, J. F., Jr.; Winfield, J. B.; Silverman, L. M. Interpretation of cerebrospinal fluid protein assays in various neurologic diseases Clin. Chem. 1983, 29, 1028-1030
37. Domanski, D.; Percy, A. J.; Yang, J.; Chambers, A. G.; Hill, J. S.; Freue, G. V.; Borchers, C. H. MRM-based multiplexed quantitation of 67 putative cardiovascular disease biomarkers in human plasma Proteomics 2012, 12, 1222-1243
38. Kuzyk, M. A.; Smith, D.; Yang, J.; Cross, T. J.; Jackson, A. M.; Hardie, D. B.; Anderson, N. L.; Borchers, C. H. Multiple reaction monitoring-based, multiplexed, absolute quantitation of 45 proteins in human plasma Mol. Cell Proteomics 2009, 8, 1860-1877
39. Hagman, C.; Ricke, D.; Ewert, S.; Bek, S.; Falchetto, R.; Bitsch, F. Absolute quantification of monoclonal antibodies in biofluids by liquid chromatography-tandem mass spectrometry Anal. Chem. 2008, 80, 1290-1296
40. Hoofnagle, A. N.; Becker, J. O.; Wener, M. H.; Heinecke, J. W. Quantification of thyroglobulin, a low-abundance serum protein, by immunoaffinity peptide enrichment and tandem mass spectrometry Clin. Chem. 2008, 54, 1796-1804
41. Lindqvist, A.; Jansson, B.; Hammarlund-Udenaes, M. Quantitative analysis of the opioid peptide DAMGO in rat plasma and microdialysis samples using liquid chromatography-tandem mass spectrometry J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 2012, 900, 11-17
42. Chen, F.; Hori, T.; Ohashi, N.; Baine, A. M.; Eckman, C. B.; Nguyen, J. H. Occludin is regulated by epidermal growth factor receptor activation in brain endothelial cells and brains of mice with acute liver failure Hepatology 2011, 53, 1294-1305
43. Abbott, N. J. Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology Neurochem. Int. 2004, 45, 545-552
44. De Lange, E. C.; Danhof, M. Considerations in the use of cerebrospinal fluid pharmacokinetics to predict brain target concentrations in the clinical setting: implications of the barriers between blood and brain Clin. Pharmacokinet. 2002, 41, 691-703
45. Nau, R.; Sorgel, F.; Eiffert, H. Penetration of drugs through the blood-cerebrospinal fluid/blood-brain barrier for treatment of central nervous system infections Clin. Microbiol. Rev. 2010, 23, 858-883
46. Deane, R.; Sagare, A.; Hamm, K.; Parisi, M.; LaRue, B.; Guo, H.; Wu, Z.; Holtzman, D. M.; Zlokovic, B. V. IgG-assisted age-dependent clearance of Alzheimer's amyloid beta peptide by the blood-brain barrier neonatal Fc receptor J. Neurosci. 2005, 25, 11495-11503
47. Schlachetzki, F.; Zhu, C.; Pardridge, W. M. Expression of the neonatal Fc receptor (FcRn) at the blood-brain barrier J. Neurochem. 2002, 81, 203-206
48. Abuqayyas, L.; Balthasar, J. P. Investigation of the role of FcgammaR and FcRn in mAb distribution to the brain Mol. Pharmaceutics 2012, 10.1021/mp300214k
49. Styren, S. D.; Mufson, E. J.; Styren, G. C.; Civin, W. H.; Rogers, J. Epidermal growth factor receptor expression in demented and aged human brain Brain Res. 1990, 512, 347-352
50. Thorne, R. G.; Nicholson, C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 5567-5572
51. Groothuis, D. R.; Vavra, M. W.; Schlageter, K. E.; Kang, E. W.; Itskovich, A. C.; Hertzler, S.; Allen, C. V.; Lipton, H. L. Efflux of drugs and solutes from brain: the interactive roles of diffusional transcapillary transport, bulk flow and capillary transporters J. Cereb. Blood Flow Metab. 2007, 27, 43-56
52. Thorne, R. G.; Hrabetova, S.; Nicholson, C. Diffusion of epidermal growth factor in rat brain extracellular space measured by integrative optical imaging J. Neurophysiol. 2004, 92, 3471-3481
53. Iliff, J. J.; Wang, M.; Liao, Y.; Plogg, B. A.; Peng, W.; Gundersen, G. A.; Benveniste, H.; Vates, G. E.; Deane, R.; Goldman, S. A.; Nagelhus, E. A.; Nedergaard, M. A Paravascular Pathway Facilitates CSF Flow Through the Brain Parenchyma and the Clearance of Interstitial Solutes, Including Amyloid beta Sci. Transl. Med. 2012, 4, 147ra111
54. Szentistvanyi, I.; Patlak, C. S.; Ellis, R. A.; Cserr, H. F. Drainage of interstitial fluid from different regions of rat brain Am. J. Physiol. 1984, 246, F835-F844