Enhanced brain delivery of the opioid peptide damgo in glutathione pegylated liposomes: A microdialysis study

Molecular Pharmaceutics

Volumn 10, Issue 5, 2013, Pages 1533-1541

  Lindqvist, Annika ^a   Rip, Jaap ^b   Gaillard, Pieter J ^b   Björkman, Sven ^a   Hammarlund Udenaes, Margareta ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b To BBB Technologies BV   (Netherlands)

Author keywords

antinociception; blood brain barrier; drug delivery; liposomes; microdialysis; nanocarrier; opioid peptide; pharmacokinetics

Indexed keywords

ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; GLUTATHIONE POLYETHYLENE GLYCOL LIPOSOME; LIPOSOME; MACROGOL DERIVATIVE; UNCLASSIFIED DRUG; GLUTATHIONE; NARCOTIC ANALGESIC AGENT;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BLOOD SAMPLING; BRAIN; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG DISPOSITION; DRUG DISTRIBUTION; DRUG EXPOSURE; DRUG FORMULATION; DRUG HALF LIFE; DRUG INFUSION; IN VITRO STUDY; IN VIVO STUDY; INTERSTITIAL FLUID; LIPOSOMAL DELIVERY; LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY TANDEM MASS SPECTROMETRY; LOADING DRUG DOSE; MALE; MAXIMUM PLASMA CONCENTRATION; MICRODIALYSIS; NANOENCAPSULATION; NONHUMAN; PRIORITY JOURNAL; RAT; STEADY STATE; TANDEM MASS SPECTROMETRY; ANIMAL; DRUG DELIVERY SYSTEM; HALF LIFE TIME; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; SPRAGUE DAWLEY RAT;

ANALGESICS, OPIOID; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; DRUG DELIVERY SYSTEMS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; GLUTATHIONE; HALF-LIFE; INFUSIONS, INTRAVENOUS; LIPOSOMES; MALE; MICRODIALYSIS; POLYETHYLENE GLYCOLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84877256284     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300272a     Document Type: Article

References (53)

1. Gabathuler, R. Approaches to transport therapeutic drugs across the blood-brain barrier to treat brain diseases Neurobiol. Dis. 2009, 37 (1) 48-57
2. Brasnjevic, I.; Steinbusch, H. W.; Schmitz, C.; Martinez-Martinez, P. Delivery of peptide and protein drugs over the blood-brain barrier Prog. Neurobiol. 2009, 87 (4) 212-51
3. Lawrence, S. Billion dollar babies - biotech drugs as blockbusters Nat. Biotechnol. 2007, 25 (4) 380-2
4. Banks, W. A. Delivery of peptides to the brain: emphasis on therapeutic development Biopolymers 2008, 90 (5) 589-94
5. Begley, D. J. Delivery of therapeutic agents to the central nervous system: the problems and the possibilities Pharmacol. Ther. 2004, 104 (1) 29-45
6. de Boer, A. G.; Gaillard, P. J. Drug targeting to the brain Annu. Rev. Pharmacol. Toxicol. 2007, 47, 323-55
7. Brightman, M. W.; Reese, T. S. Junctions between intimately apposed cell membranes in the vertebrate brain J. Cell Biol. 1969, 40 (3) 648-77
8. Abbott, N. J.; Patabendige, A. A.; Dolman, D. E.; Yusof, S. R.; Begley, D. J. Structure and function of the blood-brain barrier Neurobiol. Dis. 2010, 37 (1) 13-25
9. Torchilin, V. P. Recent advances with liposomes as pharmaceutical carriers Nat. Rev. Drug Discovery 2005, 4 (2) 145-60
10. Lichota, J.; Skjorringe, T.; Thomsen, L. B.; Moos, T. Macromolecular drug transport into the brain using targeted therapy J. Neurochem. 2010, 113 (1) 1-13
11. Zhang, X.; Liu, L.; Ma, K.; Rao, Y.; Zhao, Q.; Li, F. Analytical methods for brain targeted delivery system in vivo: perspectives on imaging modalities and microdialysis J. Pharm. Biomed. Anal. 2012, 59, 1-12
12. van Rooy, I.; Cakir-Tascioglu, S.; Hennink, W. E.; Storm, G.; Schiffelers, R. M.; Mastrobattista, E. In vivo methods to study uptake of nanoparticles into the brain Pharm. Res. 2011, 28 (3) 456-71
13. Chaurasia, C. S.; Muller, M.; Bashaw, E. D.; Benfeldt, E.; Bolinder, J.; Bullock, R.; Bungay, P. M.; DeLange, E. C.; Derendorf, H.; Elmquist, W. F.; Hammarlund-Udenaes, M.; Joukhadar, C.; Kellogg, D. L., Jr.; Lunte, C. E.; Nordstrom, C. H.; Rollema, H.; Sawchuk, R. J.; Cheung, B. W.; Shah, V. P.; Stahle, L.; Ungerstedt, U.; Welty, D. F.; Yeo, H. AAPS-FDA workshop white paper: microdialysis principles, application and regulatory perspectives Pharm. Res. 2007, 24 (5) 1014-25
14. Gaillard, P. Crossing barriers from blood-to-brain and academia-to-industry Ther. Delivery 2010, 1 (4) 495-500
15. Gaillard, P. J.; Visser, C. C.; Appeldoorn, C. C. M.; Rip, J. Enhanced brain drug delivery: safely crossing the blood-brain barrier Drug Discovery Today: Technol. 2012, 9 (2) e155-60
16. Perez, A. T.; Domenech, G. H.; Frankel, C.; Vogel, C. L. Pegylated liposomal doxorubicin (Doxil) for metastatic breast cancer: the Cancer Research Network, Inc., experience Cancer Invest. 2002, 20 (Suppl. 2) 22-9
17. Sundar, S.; Chakravarty, J.; Agarwal, D.; Rai, M.; Murray, H. W. Single-dose liposomal amphotericin B for visceral leishmaniasis in India N. Engl. J. Med. 2010, 362 (6) 504-12
18. Kannan, R.; Kuhlenkamp, J. F.; Jeandidier, E.; Trinh, H.; Ookhtens, M.; Kaplowitz, N. Evidence for carrier-mediated transport of glutathione across the blood-brain barrier in the rat J. Clin. Invest. 1990, 85 (6) 2009-13
19. Kannan, R.; Chakrabarti, R.; Tang, D.; Kim, K. J.; Kaplowitz, N. GSH transport in human cerebrovascular endothelial cells and human astrocytes: evidence for luminal localization of Na+-dependent GSH transport in HCEC Brain Res. 2000, 852 (2) 374-82
20. Zlokovic, B. V.; Mackic, J. B.; McComb, J. G.; Weiss, M. H.; Kaplowitz, N.; Kannan, R. Evidence for transcapillary transport of reduced glutathione in vascular perfused guinea-pig brain Biochem. Biophys. Res. Commun. 1994, 201 (1) 402-8
21. van Tellingen, O.; Brandsma, D.; Boogerd, W.; Appeldoorn, C.; Manca, F.; Rip, J.; Dorland, R.; van Kregten, J.; Gaillard, P. GSH-conjugation improves efficacy of doxil against intracranial xenografts Neuro-Oncology 2010, 12 (Suppl. 3) iii34
22. Gaillard, P.; Appeldoorn, C.; Rip, J.; Dorland, R.; van der Pol, S.; Kooij, G.; de Vries, E. H.; Reijerkerk, A. Enhanced brain delivery of liposomal methylprednisolone improved therapeutic efficacy in a model of neuroinflammation J. Controlled Release 2012, 10.1016/j.jconrel.2012.06.022
23. George, S. R.; Fan, T.; Xie, Z.; Tse, R.; Tam, V.; Varghese, G.; O'Dowd, B. F. Oligomerization of mu- and delta-opioid receptors. Generation of novel functional properties J. Biol. Chem. 2000, 275 (34) 26128-35
24. Handa, B. K.; Land, A. C.; Lord, J. A.; Morgan, B. A.; Rance, M. J.; Smith, C. F. Analogues of beta-LPH61-64 possessing selective agonist activity at mu-opiate receptors Eur. J. Pharmacol. 1981, 70 (4) 531-40
25. Fiori, A.; Cardelli, P.; Negri, L.; Savi, M. R.; Strom, R.; Erspamer, V. Deltorphin transport across the blood-brain barrier Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (17) 9469-74
26. Al-Khrasani, M.; Spetea, M.; Friedmann, T.; Riba, P.; Kiraly, K.; Schmidhammer, H.; Furst, S. DAMGO and 6beta-glycine substituted 14-O-methyloxymorphone but not morphine show peripheral, preemptive antinociception after systemic administration in a mouse visceral pain model and high intrinsic efficacy in the isolated rat vas deferens Brain Res. Bull. 2007, 74 (5) 369-75
27. Hammarlund-Udenaes, M.; Friden, M.; Syvanen, S.; Gupta, A. On the rate and extent of drug delivery to the brain Pharm. Res. 2008, 25 (8) 1737-50
28. Gupta, A.; Chatelain, P.; Massingham, R.; Jonsson, E. N.; Hammarlund-Udenaes, M. Brain distribution of cetirizine enantiomers: comparison of three different tissue-to-plasma partition coefficients: K(p), K(p,u), and K(p,uu) Drug Metab. Dispos. 2006, 34 (2) 318-23
29. Janssen, P. A.; Niemegeers, C. J.; Dony, J. G. The inhibitory effect of fentanyl and other morphine-like analgesics on the warm water induced tail withdrawl reflex in rats Arzneim. Forsch. 1963, 13, 502-7
30. Bouw, M. R.; Hammarlund-Udenaes, M. Methodological aspects of the use of a calibrator in in vivo microdialysis-further development of the retrodialysis method Pharm. Res. 1998, 15 (11) 1673-9
31. Wang, Y.; Wong, S. L.; Sawchuk, R. J. Microdialysis calibration using retrodialysis and zero-net flux: application to a study of the distribution of zidovudine to rabbit cerebrospinal fluid and thalamus Pharm. Res. 1993, 10 (10) 1411-9
32. 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, 11-7
33. Mao, J.; Price, D. D.; Lu, J.; Mayer, D. J. Antinociceptive tolerance to the mu-opioid agonist DAMGO is dose-dependently reduced by MK-801 in rats Neurosci. Lett. 1998, 250 (3) 193-6
34. Ekblom, M.; Hammarlund-Udenaes, M.; Paalzow, L. Modeling of tolerance development and rebound effect during different intravenous administrations of morphine to rats J. Pharmacol. Exp. Ther. 1993, 266 (1) 244-52
35. Gardmark, M.; Ekblom, M.; Bouw, R.; Hammarlund-Udenaes, M. Quantification of effect delay and acute tolerance development to morphine in the rat J. Pharmacol. Exp. Ther. 1993, 267 (3) 1061-7
36. Chen, C.; Pollack, G. M. Development of a capillary zone electrophoresis assay to examine the disposition of [D-pen2,5]enkephalin in rats J. Chromatogr., B: Biomed. Appl. 1996, 681 (2) 363-73
37. Chen, C.; Pollack, G. M. Blood-brain disposition and antinociceptive effects of -D-penicillamine2,5-enkephalin in the mouse J. Pharmacol. Exp. Ther. 1997, 283 (3) 1151-9
38. Yang, J. Z.; Chen, W.; Borchardt, R. T. In vitro stability and in vivo pharmacokinetic studies of a model opioid peptide, H-Tyr-D-Ala-Gly-Phe-D-Leu-OH (DADLE), and its cyclic prodrugs J. Pharmacol. Exp. Ther. 2002, 303 (2) 840-8
39. Van Dorpe, S.; Adriaens, A.; Polis, I.; Peremans, K.; Van Bocxlaer, J.; De Spiegeleer, B. Analytical characterization and comparison of the blood-brain barrier permeability of eight opioid peptides Peptides 2010, 31 (7) 1390-9
40. Szeto, H. H.; Lovelace, J. L.; Fridland, G.; Soong, Y.; Fasolo, J.; Wu, D.; Desiderio, D. M.; Schiller, P. W. In vivo pharmacokinetics of selective mu-opioid peptide agonists J. Pharmacol. Exp. Ther. 2001, 298 (1) 57-61
41. Fleck, C. Determination of the glomerular filtration rate (GFR): methodological problems, age-dependence, consequences of various surgical interventions, and the influence of different drugs and toxic substances Physiol. Res. 1999, 48 (4) 267-79
42. Chen, C.; Pollack, G. M. Extensive biliary excretion of the model opioid peptide [D-PEN2,5] enkephalin in rats Pharm. Res. 1997, 14 (3) 345-50
43. Blume, G.; Cevc, G. Liposomes for the sustained drug release in vivo Biochim. Biophys. Acta 1990, 1029 (1) 91-7
44. Klibanov, A. L.; Maruyama, K.; Torchilin, V. P.; Huang, L. Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes FEBS Lett. 1990, 268 (1) 235-7
45. Witt, K. A.; Huber, J. D.; Egleton, R. D.; Roberts, M. J.; Bentley, M. D.; Guo, L.; Wei, H.; Yamamura, H. I.; Davis, T. P. Pharmacodynamic and pharmacokinetic characterization of poly(ethylene glycol) conjugation to met-enkephalin analog [D-Pen2, D-Pen5]-enkephalin (DPDPE) J. Pharmacol. Exp. Ther. 2001, 298 (2) 848-56
46. Dagenais, C.; Graff, C. L.; Pollack, G. M. Variable modulation of opioid brain uptake by P-glycoprotein in mice Biochem. Pharmacol. 2004, 67 (2) 269-76
47. Oude Elferink, R. P.; Zadina, J. MDR1 P-glycoprotein transports endogenous opioid peptides Peptides 2001, 22 (12) 2015-20
48. Sarkadi, B.; Muller, M.; Homolya, L.; Hollo, Z.; Seprodi, J.; Germann, U. A.; Gottesman, M. M.; Price, E. M.; Boucher, R. C. Interaction of bioactive hydrophobic peptides with the human multidrug transporter FASEB J. 1994, 8 (10) 766-70
49. Syvanen, S.; Xie, R.; Sahin, S.; Hammarlund-Udenaes, M. Pharmacokinetic consequences of active drug efflux at the blood-brain barrier Pharm. Res. 2006, 23 (4) 705-17
50. Ying, X.; Wen, H.; Yao, H. J.; Zhang, Y.; Tian, W.; Zhang, L.; Ju, R. J.; Wang, X. X.; Yu, Y.; Lu, W. L. Pharmacokinetics and tissue distribution of dual-targeting daunorubicin liposomes in mice Pharmacology 2011, 87 (1-2) 105-14
51. Afergan, E.; Epstein, H.; Dahan, R.; Koroukhov, N.; Rohekar, K.; Danenberg, H. D.; Golomb, G. Delivery of serotonin to the brain by monocytes following phagocytosis of liposomes J. Controlled Release 2008, 132 (2) 84-90
52. Ulbrich, K.; Hekmatara, T.; Herbert, E.; Kreuter, J. Transferrin- and transferrin-receptor-antibody-modified nanoparticles enable drug delivery across the blood-brain barrier (BBB) Eur. J. Pharm. Biopharm. 2009, 71 (2) 251-6
53. Kannan, R.; Mittur, A.; Bao, Y.; Tsuruo, T.; Kaplowitz, N. GSH transport in immortalized mouse brain endothelial cells: evidence for apical localization of a sodium-dependent GSH transporter J. Neurochem. 1999, 73 (1) 390-9