Analytical characterization and comparison of the blood-brain barrier permeability of eight opioid peptides

Peptides

Volumn 31, Issue 7, 2010, Pages 1390-1399

  Van Dorpe, Sylvia ^a   Adriaens, Antita ^a   Polis, Ingeborgh ^a   Peremans, Kathelijne ^a   Van Bocxlaer, Jan ^a   De Spiegeleer, Bart ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Blood brain barrier; Metabolism; Opioid receptor; Peptides

Indexed keywords

DERMORPHIN; OPIATE PEPTIDE; PEPTIDE DERIVATIVE; PROTEIN CTAP; PROTEIN CTOP; PROTEIN DAMGO; PROTEIN EM 1; PROTEIN EM 2; PROTEIN TAPP; PROTEIN TAPS; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG HALF LIFE; DRUG STABILITY; DRUG TRANSPORT; MALE; MEMBRANE PERMEABILITY; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; KINETICS; MALE; MICE; OPIOID PEPTIDES; PERMEABILITY;

EID: 77952545323     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.peptides.2010.03.029     Document Type: Article

References (103)

1. Abbott N.J., Patabendige A.A.K., Dolman D.E.M., Yusof S.R., and Begley D.J. Structure and function of the blood-brain barrier. Neurobiology of Disease 37 (2010) 13-25
2. Abbruscato T.J., Thomas S.A., Hruby V.J., and Davis T.P. Blood-brain barrier permeability and bioavailability of a highly potent and mu-selective opioid receptor antagonist, CTAP: comparison with morphine. Journal of Pharmacology and Experimental Therapeutics 280 (1997) 402-409
3. Adessi C., and Soto C. Converting a peptide into a drug: strategies to improve stability and bioavailability. Current Medicinal Chemistry 9 (2002) 963-978
4. Banach T., Zurowski D., Gil K., Weilsbrodt N.W., Rosenfeld G., and Thor P.J. Peripheral mechanisms of intestinal dysmotility in the morphine tolerant and dependent rats. Journal of Physiology and Pharmacology 57 (2006) 73-82
5. Banks W.A. Delivery of peptides to the brain: emphasis on therapeutic development. Biopolymers 90 (2008) 589-594
6. Banks W.A., and Kastin A.J. Peptide-transport systems for opiates across the blood-brain-barrier. American Journal of Physiology 259 (1990) E1-E10
7. Banks W.A., and Kastin A.J. Peptides and the blood-brain-barrier-lipophilicity as a predictor of permeability. Brain Research Bulletin 15 (1985) 287-292
8. Banks W.A., Kastin A.J., and Conn P.M. Quantifying carrier-mediated transport of peptides from the brain to the blood. Methods in enzymology (1989), Academic Press p. 652-660
9. 125I]N-Tyr-delta sleep-inducing peptide crosses the blood-brain barrier by a non-competitive mechanism. Brain Research 301 (1984) 201-207
10. Banks W.A., Kastin A.J., and Ehrensing C.A. Endogenous peptide Tyr-Pro-Trp-Gly-NH2 (TYR-W-MIF-1) is transported from the brain to the blood by peptide-transport system-1. Journal of Neuroscience Research 35 (1993) 690-695
11. Banks W.A., Kastin A.J., Michals E.A., and Barrera C.M. Stereospecific transport of Tyr-MIF-1 across the blood-brain barrier by peptide transport system-1. Brain Research Bulletin 25 (1990) 589-592
12. Begley D.J. ABC transporters and the blood-brain barrier. Current Pharmaceutical Design 10 (2004) 1295-1312
13. Bell K.M., and Traynor J.R. Dynorphin A(1-8): stability and implications for in vitro opioid activity. Canadian Journal of Physiology and Pharmacology 76 (1998) 325-333
14. Belyaev N.A., Kolesanova E.F., Baronets V.Y., Terebilina N.N., and Panchenko L.F. Enkephalin metabolism in rat brain after bestatin administration. Peptide Science-Present and Future (1999) 689-690
15. Bickel U., Yoshikawa T., and Pardridge W.M. Delivery of peptides and proteins through the blood-brain barrier. Advanced Drug Delivery Reviews 46 (2001) 247-279
16. Bonner G.G., Davis P., Stropova D., Ferguson R., Yamamura H.I., Porreca F., et al. Opioid peptides: simultaneous delta agonism and mu antagonism in somatostatin analogues. Peptides 18 (1997) 93-100
17. Brasnjevic I., Steinbusch H.W.M., Schmitz C., Martinez-Martinez P., and European NanoBioPharmaceutics R. Delivery of peptide and protein drugs over the blood-brain barrier. Progress in Neurobiology 87 (2009) 212-251
18. Broccardo M., Erspamer V., Falconierierspamer G., Improta G., Linari G., Melchiorri P., et al. Pharmacological data on dermorphins, a new class of potent opioid-peptides from amphibian skin. British Journal of Pharmacology 73 (1981) 625-631
19. Brownson E.A., Abbruscato T.J., Gillespie T.J., Hruby V.J., and Davis T.P. Effect of peptidases at the blood-brain-barrier on the permeability of enkephalin. Journal of Pharmacology and Experimental Therapeutics 270 (1994) 675-680
20. Brugos B., and Hochhaus G. Metabolism of dynorphin A(1-13). Pharmazie 59 (2004) 339-343
21. Capasso A. Bioactivity of new mu and delta opioid peptides. Medicinal Chemistry 3 (2007) 480-487
22. Champion H.C., and Kadowitz P.J. d-[Ala(2)]endomorphin 2 and endomorphin 2 have nitric oxide-dependent vasodilator activity in rats. American Journal of Physiology. Heart and Circulatory Physiology 274 (1998) H1690-H1697
23. Chen W.Q., Yang J.Z., Andersen R., Nielsen L.H., and Borchardt R.T. Evaluation of the permeation characteristics of a model opioid peptide, H-Tyr-d-Ala-Gly-Phe-d-Leu-OH (DADLE), and its cyclic prodrugs across the blood-brain barrier using an in situ perfused rat brain model. Journal of Pharmacology and Experimental Therapeutics 303 (2002) 849-857
24. Churchill L., Bausback H.H., Gerritsen M.E., and Ward P.E. Metabolism of opioid peptides by cerebral microvascular aminopeptidase M. Biochimica et Biophysica Acta (BBA): General Subjects 923 (1987) 35-41
25. de Boer A.G., van der Sandt I.C.J., and Gaillard P.J. The role of drug transporters at the blood-brain barrier. Annual Review of Pharmacology and Toxicology 43 (2003) 629-656
26. Deguchi Y., Miyakawa Y., Sakurada S., Naito Y., Morimoto K., Ohtsuki S., et al. Blood-brain barrier transport of a novel mu(1)-specific opioid peptide, H-Tyr-d-Arg-Phe-beta-Ala-OH (TAPA). Journal of Neurochemistry 84 (2003) 1154-1161
27. Dhanda S., Singh J., and Singh H. Hydrolysis of various bioactive peptides by goat brain dipeptidylpeptidase-III homologue. Cell Biochemistry and Function 26 (2008) 339-345
28. Egleton R.D., Abbruscato T.J., Thomas S.A., and Davis T.P. Transport of opioid peptides into the central nervous system. Journal of Pharmaceutical Sciences 87 (1998) 1433-1439
29. Egleton R.D., and Davis T.P. Transport of the delta-opioid receptor agonist [d-penicillamine(2,5)] enkephalin across the blood-brain barrier involves transcytosis. Journal of Pharmaceutical Sciences 88 (1999) 392-397
30. Ferro E.S., Carreno F.R., Goni C., Garrido P.A.G., Guimaraes A.O., Castro L.M., et al. The intracellular distribution and secretion of endopeptidases 24.15 (EC 3.4.24.15) and 24.16 (EC 3.4.24.16). Protein and Peptide Letters 11 (2004) 415-421
31. Fichna J., Do-Rego J.C., Chung N.N., Costentin J., Schiller P.W., and Janecka A. [Dmt(1), d-1-Nal(3)]morphiceptin, a novel opioid peptide analog with high analgesic activity. Peptides 29 (2008) 633-638
32. Fiori A., Cardelli P., Negri L., Savi M.R., Strom R., and Erspamer V. Deltorphin transport across the blood-brain barrier. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 9469-9474
33. Ganapathy V., and Miyauchi S. Transport systems for opioid peptides in mammalian tissues. AAPS Journal 7 (2005) E852-E856
34. Gerebtzoff G., Li-Blatter X., Fischer H., Frentzel A., and Seelig A. Halogenation of drugs enhances membrane binding and permeation. Chembiochem 5 (2004) 676-684
35. Gil J., Larrinaga G., Meana J.J., Rodriguez-Puertas R., Irazusta J., and Casis L. Regional and subcellular distribution of soluble aminopeptidase in the human and the rat brain: a comparative study. Neuropeptides 35 (2001) 276-284
36. Gray R.A., Vandervelde D.G., Burke C.J., Manning M.C., Middaugh C.R., and Borchardt R.T. Delta-sleep-inducing peptide-solution conformational studies of a membrane-permeable peptide. Biochemistry 33 (1994) 1323-1331
37. Gromovykh P.S., Guzevatykh L.S., Shevchenko K.V., Andreeva L.A., Alfeeva L.Y., Shevchenko V.P., et al. Synthesis, pharmacokinetics, and metabolism of the C-terminal tripeptide of dermorphin and its diastereomer. Russian Journal of Bioorganic Chemistry 33 (2007) 537-543
38. 2 (CTOP) in mice. European Journal of Pharmacology 150 (1988) 355-360
39. Gutierrez E.G., Banks W.A., and Kastin A.J. Murine tumor-necrosis-factor-alpha is transported from blood to brain in the mouse. Journal of Neuroimmunology 47 (1993) 169-176
40. Gutkowska J., and Schiller P.W. Renal effects of TAPP, a highly selective mu-opioid agonist. British Journal of Pharmacology 119 (1996) 239-244
41. Hau V.S., Huber J.D., Campos C.R., Lipkowski A.W., Misicka A., and Davis T.P. Effect of guanidino modification and proline substitution on the in vitro stability and blood-brain barrier permeability of endomorphin II. Journal of Pharmaceutical Sciences 91 (2002) 2140-2149
42. Henriksen G., and Willoch F. Imaging of opioid receptors in the central nervous system. Brain 131 (2008) 1171-1196
43. Hirning L.D., Mosberg H.I., Hurst R., Hruby V.J., Burks T.F., and Porreca F. Studies in vitro with ICI 174, 864, [d-Pen2, d-Pen5]-enkephalin (DPDPE) and [d-Ala2, NMePhe4, Gly-ol]-enkephalin (DAGO). Neuropeptides 5 (1985) 383-386
44. Holzer P. Opioid receptors in the gastrointestinal tract. Regulatory Peptides 155 (2009) 11-17
45. Hui K.S., Saito M., and Hui M. A novel neuron-specific aminopeptidase in rat brain synaptosomes-its identification, purification, and characterization. Journal of Biological Chemistry 273 (1998) 31053-31060
46. Inbar P., Li C.Q., Takayama S.A., Bautista M.R., and Yang J. Oligo(ethylene glycol) derivatives of thioflavin T as inhibitors of protein-amyloid interactions. Chembiochem 7 (2006) 1563-1566
47. Ioja E., Toth G., Benyhe S., Tourwe D., Peter A., Tomboly C., et al. Opioid receptor binding characteristics and structure-activity studies of novel tetrapeptides in the TIPP (Tyr-Tic-Phe-Phe) series. Neurosignals 14 (2005) 317-328
48. Janecka A., Fichna J., and Janecki T. Opioid receptors and their ligands. Current Topics in Medicinal Chemistry 4 (2004) 1-17
49. Janecka A., Staniszewska R., and Fichna J. Endomorphin analogs. Current Medicinal Chemistry 14 (2007) 3201-3208
50. Janecka A., Staniszewska R., Gach K., and Fichna J. Enzymatic degradation of endomorphins. Peptides 29 (2008) 2066-2073
51. Jilek A., and Kreil G. D-Amino acids in animal peptides. Monatshefte Fur Chemie 139 (2008) 1-5
52. Kastin A.J., and Akerstrom V. Entry of exendin-4 into brain is rapid but may be limited at high doses. International Journal of Obesity 27 (2003) 313-318
53. Kastin A.J., Akerstrom V., and Pan W.H. Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. Journal of Molecular Neuroscience 18 (2002) 7-14
54. Kastin A.J., Fasold M.B., Smith R.R., Horner K.A., and Zadina J.E. Saturable brain-to-blood transport of endomorphins. Experimental Brain Research 139 (2001) 70-75
55. Kastin A.J., Pan W.H., Maness L.M., and Banks W.A. Peptides crossing the blood-brain barrier: some unusual observations. Brain Research 848 (1999) 96-100
56. Kniesel U., and Wolburg H. Tight junctions of the blood-brain barrier. Cellular and Molecular Neurobiology 20 (2000) 57-76
57. Koda Y., Del Borgo M., Wessling S.T., Lazarus L.H., Okada Y., Toth I., et al. Synthesis and in vitro evaluation of a library of modified endomorphin 1 peptides. Bioorganic & Medicinal Chemistry 16 (2008) 6286-6296
58. Koide S., Onishi H., Katayama M., and Yamagami S. Metabolic profile of opioid-peptides differs in the hippocampus and striatum of seizure-susceptible e1 mice. Neurochemical Research 20 (1995) 279-283
59. Krondahl E., Von Euler-Chelpin H., Orzechowski A., Ekstrom G., and Lennernas H. Investigations of the in-vitro metabolism of three opioid tetrapeptides by pancreatic and intestinal enzymes. Journal of Pharmacy and Pharmacology 52 (2000) 785-795
60. Krondahl E., von Euler-Chelpin H., Orzechowski A., Ekström G., and Lennernäs H. In vitro metabolism of opioid tetrapeptide agonists in various tissues and subcellular fractions from rats. Peptides 22 (2001) 613-621
61. Kusuhara H., and Sugiyama Y. Efflux transport systems at the blood-brain barrier and blood CSF barrier. Drug Transport(ers) and the Diseased Brain 1277 (2005) 111-122
62. Larrinaga G., Gil J., Meana J.J., Ruiz F., Callado L.F., and Irazusta J. Aminopeptidase activity in the postmortem brain of human heroin addicts. Neurochemistry International 46 (2005) 213-219
63. Leslie F.M., and Goldstein A. Degradation of dynorphin-(1-13) by membrane-bound rat-brain enzymes. Neuropeptides 2 (1982) 185-196
64. Li Q., Min J.K., Ahn Y.H., Namm J.H., Kim E.M., Lui R., et al. Styryl-based compounds as potential in vivo imaging agents for beta-amyloid plaques. Chembiochem 8 (2007) 1679-1687
65. Liu H.M., Zhang B.Z., Liu X.F., Wang C.L., Ni J.M., and Wang R. Endomorphin-1 analogs with enhanced metabolic stability and systemic analgesic activity: design, synthesis, and pharmacological characterization. Bioorganic & Medicinal Chemistry 15 (2007) 1694-1702
66. Lowery J.J., Yeomans L., Keyari C.M., Davis P., Porreca F., Knapp B.I., et al. Glycosylation improves the central effects of DAMGO. Chemical Biology & Drug Design 69 (2007) 41-47
67. Maness L.M., Banks W.A., Zadina J.E., and Kastin A.J. Periventricular penetration and disappearance of ICV Tyr-MIF-1, DAMGO, tyrosine, and albumin. Peptides 17 (1996) 247-250
68. Martin W.R., Eades C.G., Thompson J.A., Huppler R.E., and Gilbert P.E. Effects of morphine-like and nalorphine-like drugs in nondependent and morphine-dependent chronic spinal dog. Journal of Pharmacology and Experimental Therapeutics 197 (1976) 517-532
69. Melchiorri P., and Negri L. The dermorphin peptide family. General Pharmacology 27 (1996) 1099-1107
70. Minnis J.G., Patierno S., Kohlmeier S.E., Brecha N.C., Tonini M., and Sternini C. Ligand-induced mu opioid receptor endocytosis and recycling in enteric neurons. Neuroscience 119 (2003) 33-42
71. Misra A., Ganesh S., Shahiwala A., and Shah S.P. Drug delivery to the central nervous system: a review. Journal of Pharmacy and Pharmaceutical Sciences 6 (2003) 252-273
72. Mollereau C., and Mouledous L. Tissue distribution of the opioid receptor-like (ORL1) receptor. Peptides 21 (2000) 907-917
73. Mosnaim A.D., Puente J., Tse R., and Wolf M.E. In vitro human brain methionine-enkephalin metabolism. FASEB Journal 19 (2005) A509-A510
74. Negri L., Lattanzi R., Tabacco F., Scolaro B., and Rocchi R. Glycodermorphins: opioid peptides with potent and prolonged analgesic activity and enhanced blood-brain barrier penetration. British Journal of Pharmacology 124 (1998) 1516-1522
75. Okada Y., Fukumizu A., Takahashi M., Shimizu Y., Tsuda Y., Yokoi T., et al. Synthesis of stereoisomeric analogues of endomorphin-2, H-Tyr-Pro-Phe-Phe-NH2, and examination of their opioid receptor binding activities and solution conformation. Biochemical and Biophysical Research Communications 276 (2000) 7-11
76. Pan W.H., Tu H., and Kastin A.J. Differential BBB interactions of three ingestive peptides: obestatin, ghrelin, and adiponectin. Peptides 27 (2006) 911-916
77. Patlak C.S., Blasberg R.G., and Fenstermacher J.D. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Journal of Cerebral Blood Flow and Metabolism 3 (1983) 1-7
78. Pelton J.T., Kazmierski W., Gulya K., Yamamura H.I., and Hruby V.J. Design and synthesis of conformationally constrained somatostatin analogs with high potency and specificity for mu-opioid receptors. Journal of Medicinal Chemistry 29 (1986) 2370-2375
79. Pinto A., Hoffmanns U., Ott M., Fricker G., and Metzler-Nolte N. Modification with organometallic compounds improves crossing of the blood-brain barrier of [Leu(5)]-enkephalin derivatives in an in vitro model system. Chembiochem 10 (2009) 1852-1860
80. Prokai L., Kim H.S., Zharikova A., Roboz J., Ma L., Deng L., et al. Electrospray ionization mass spectrometric and liquid chromatographic mass spectrometric studies on the metabolism of synthetic dynorphin A peptides in brain tissue in vitro and in vivo. Journal of Chromatography A 800 (1998) 59-68
81. Sakurada C., Sakurada S., Hayashi T., Katsuyama S., Tan-No K., and Sakurada T. Degradation of endomorphin-2 at the supraspinal level in mice is initiated by dipeptidyl peptidase IV: an in vitro and in vivo study. Biochemical Pharmacology 66 (2003) 653-661
82. Sasaki Y., Matsui M., Taguchi M., Suzuki K., Sakurada S., Sato T., et al. d-Arg2-dermorphin tetrapeptide analogs: a potent and long-lasting analgesic activity after subcutaneous administration. Biochemical and Biophysical Research Communications 120 (1984) 214-218
83. Sato T., Sakurada S., Sakurada T., Furuta S., Chaki K., Kisara K., et al. Opioid activities of d-Arg2-substituted tetrapeptides. Journal of Pharmacology and Experimental Therapeutics 242 (1987) 654-659
84. Schiller P.W. Opioid peptide-derived analgesics. AAPS Journal 7 (2005) E560-E565
85. Shane R., Wilk S., and Bodnar R.J. Modulation of endomorphin-2-induced analgesia by dipeptidyl peptidase IV. Brain Research 815 (1999) 278-286
86. Shinada T., Ishida T., Hayashi K.I., Yoshida Y., Shigeri Y., and Ohfune Y. Synthesis of leucine-enkephalin analogs containing alpha-amino squaric acid. Tetrahedron Letters 48 (2007) 7614-7617
87. Somogyvari-Vigh A., Kastin A.J., Liao J., Zadina J.E., and Pan W.H. Endomorphins exit the brain by a saturable efflux system at the basolateral surface of cerebral endothelial cells. Experimental Brain Research 156 (2004) 224-230
88. 2 with [mu]-opioid receptor in rat brain and CHO-[mu]/1 cell line. Peptides 19 (1998) 1091-1098
89. Szeto H.H., Lovelace J.L., Fridland G., Soong Y., Fasolo J., Wu D.L., et al. In vivo pharmacokinetics of selective mu-opioid peptide agonists. Journal of Pharmacology and Experimental Therapeutics 298 (2001) 57-61
90. Taylor E.M. The impact of efflux transporters in the brain on the development of drugs for CNS disorders. Clinical Pharmacokinetics 41 (2002) 81-92
91. Toth G., Keresztes A., Szucs M., Forro E., and Fulop F. Endomorphin analogs with alicyclic beta-amino acids. Proceedings of the 5th Joint Meeting on Medicinal Chemistry (2007) 47-50
92. Triguero D., Buciak J., and Pardridge W.M. Capillary depletion method for quantification of blood-brain-barrier transport of circulating peptides and plasma-proteins. Journal of Neurochemistry 54 (1990) 1882-1888
93. Vaccarino A.L., Olson G.A., Olson R.D., and Kastin A.J. Endogenous opiates: 1998[small star, filled]. Peptides 20 (1999) 1527-1574
94. Vanhoof G., Goossens F., Demeester I., Hendriks D., and Scharpe S. Proline motifs in peptides and their biological processing. FASEB Journal 9 (1995) 736-744
95. Vergote V., Bodé S., Peremans K., Vanbree H., Baert B., Slegers G., et al. Analysis of iodinated peptides by LC-DAD/ESI ion trap mass spectrometry. Journal of Chromatography B 850 (2007) 213-220
96. Vermeire A., and Remon J.P. Stability and compatibility of morphine. International Journal of Pharmaceutics 187 (1999) 17-51
97. 3H]Tyr--Arg2-Phe-Sar4 at opioid receptors. European Journal of Pharmacology 473 (2003) 127-134
98. Weltrowska G., Lemieux C., Chung N.N., and Schiller P.W. Cyclic enkephalin analogs containing various para-substituted phenylalanine derivatives in place of Tyr(1) are potent opioid agonists. Journal of Peptide Research 65 (2005) 36-41
99. Wilson J.F., Anderson S., Snook G., and Llewellyn K.D. Quantification of the permeability of the blood-CSF barrier to [alpha]-MSH in the rat. Peptides; 5 (1984) 681-685
100. Witt K.A., and Davis T.P. CNS drug delivery: opioid peptides and the blood-brain barrier. AAPS Journal 8 (2006) E76-E88
101. Yu Y., Shao X., Wang C.L., Liu H.M., Cui Y., Fan Y.Z., et al. In vitro and in vivo characterization of opioid activities of endomorphins analogs with novel constrained C-terminus: evidence for the important role of proper spatial disposition of the third aromatic ring. Peptides 28 (2007) 859-870
102. Zadina J.E., Hackler L., Ge L.J., and Kastin A.J. A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386 (1997) 499-502
103. Zieleniak A., Rodziewicz-Motowidlo S., Rusak L., Chung N.N., Czaplewski C., Witkowska E., et al. Deltorphin analogs restricted via a urea bridge: structure and opioid activity. Journal of Peptide Science 14 (2008) 830-837