Safety, efficacy, and molecular mechanism of claudin-1-specific peptides to enhance blood-nerve-barrier permeability

Journal of Controlled Release

Volumn 185, Issue 1, 2014, Pages 88-98

  Sauer, Reine Solange ^a   Krug, Susanne M ^b   Hackel, Dagmar ^a,b   Staat, Christian ^c   Konasin, Natalia ^a   Yang, Shaobing ^a   Niedermirtl, Benedikt ^a   Bosten, Judith ^a   Günther, Ramona ^c   Dabrowski, Sebastian ^c   Doppler, Kathrin ^d   Sommer, Claudia ^d   Blasig, Ingolf E ^c   Brack, Alexander ^a   Rittner, Heike L ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^d UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

Biocompatibility; Drug delivery; In vitro test; In vivo test; Peptide; Peripheral nerve

Indexed keywords

BIOCOMPATIBILITY; BLOOD; BLOOD VESSELS; DRUG DELIVERY; RATS; SIGNAL TRANSDUCTION;

EXTRACELLULAR LOOPS; IN-VITRO TESTS; IN-VIVO TESTS; MECHANISM OF ACTION; MOLECULAR MECHANISM; MOTOR IMPAIRMENTS; PERIPHERAL NERVES; PROTEIN EXPRESSIONS;

PEPTIDES;

CLAUDIN 1; CLAUDIN 1 PEPTIDOMIMETIC; CLAUDIN 11; CLAUDIN 2; CLAUDIN 3; CLAUDIN 8; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; MORPHINE; PEPTIDOMIMETIC AGENT; TIGHT JUNCTION PROTEIN; TRANSCRIPTION FACTOR CDX2; TRICELLULIN; UNCLASSIFIED DRUG; NARCOTIC ANALGESIC AGENT; PEPTIDE;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOCOMPATIBILITY; BLOOD NERVE BARRIER; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG SAFETY; HOMEOBOX; HYDROPHILICITY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MACROMOLECULE; MALE; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NERVE INJURY; NONHUMAN; PAIN THRESHOLD; PEPTIDE SYNTHESIS; PERINEURIUM; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM; MOLECULAR GENETICS; PERMEABILITY; SCIATIC NERVE; TIGHT JUNCTION; WISTAR RAT;

AMINO ACID SEQUENCE; ANALGESIA; ANALGESICS, OPIOID; ANIMALS; CELL LINE; CLAUDIN-1; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PEPTIDES; PERIPHERAL NERVES; PERMEABILITY; RATS; RATS, WISTAR; SCIATIC NERVE; TIGHT JUNCTIONS;

EID: 84900474883     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.04.029     Document Type: Article

References (52)

1. D. Hackel, A. Brack, M. Fromm, and H.L. Rittner Modulation of tight junction proteins in the perineurium for regional pain control Ann. N. Y. Acad. Sci. 1257 2012 199 206
2. K.P. Pummi, H.J. Aho, M.K. Laato, J.T. Peltonen, and S.A. Peltonen Tight junction proteins and perineurial cells in neurofibromas J. Histochem. Cytochem. 54 2006 53 61
3. H.L. Rittner, S. Amasheh, R. Moshourab, D. Hackel, R.S. Yamdeu, S.A. Mousa, M. Fromm, C. Stein, and A. Brack Modulation of tight junction proteins in the perineurium to facilitate peripheral opioid analgesia Anesthesiology 116 2012 1323 1334
4. C. Tscheik, I.E. Blasig, and L. Winkler Trends in drug delivery through tissue barriers containing tight junctions Tissue Barriers 1 2013 e24565
5. D. Hackel, S.M. Krug, R.S. Sauer, S.A. Mousa, A. Bocker, D. Pflucke, E.J. Wrede, K. Kistner, T. Hoffmann, B. Niedermirtl, C. Sommer, L. Bloch, O. Huber, I.E. Blasig, S. Amasheh, P.W. Reeh, M. Fromm, A. Brack, and H.L. Rittner Transient opening of the perineurial barrier for analgesic drug delivery PNAS 109 2012 E2018 E2027
6. A.M. Binshtok, B.P. Bean, and C.J. Woolf Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers Nature 449 2007 607 610
7. D. Zwanziger, D. Hackel, C. Staat, A. Bocker, A. Brack, M. Beyermann, H. Rittner, and I.E. Blasig A peptidomimetic tight junction modulator to improve regional analgesia Mol. Pharm. 9 2012 1785 1794
8. S.M. Krug, M. Amasheh, I. Dittmann, I. Christoffel, M. Fromm, and S. Amasheh Sodium caprate as an enhancer of macromolecule permeation across tricellular tight junctions of intestinal cells Biomaterials 34 2013 275 282
9. R. Rosenthal, D. Gunzel, C. Finger, S.M. Krug, J.F. Richter, J.D. Schulzke, M. Fromm, and S. Amasheh The effect of chitosan on transcellular and paracellular mechanisms in the intestinal epithelial barrier Biomaterials 33 2012 2791 2800
10. G. Del Vecchio, C. Tscheik, K. Tenz, H.C. Helms, L. Winkler, R. Blasig, and I.E. Blasig Sodium caprate transiently opens claudin-5-containing barriers at tight junctions of epithelial and endothelial cells Mol. Pharm. 9 2012 2523 2533
11. R.J. Mrsny, G.T. Brown, K. Gerner-Smidt, A.G. Buret, J.B. Meddings, C. Quan, M. Koval, and A. Nusrat A key claudin extracellular loop domain is critical for epithelial barrier integrity Am. J. Pathol. 172 2008 905 915
12. E.A. Severson, M. Kwon, R.S. Hilgarth, C.A. Parkos, and A. Nusrat Glycogen synthase kinase 3 (GSK-3) influences epithelial barrier function by regulating occludin, claudin-1 and E-cadherin expression Biochem. Biophys. Res. Commun. 397 2010 592 597
13. W.C. Wang, J.J. Tsai, C.Y. Kuo, H.M. Chen, and S.H. Kao Non-proteolytic house dust mite allergen, Der p 2, upregulated expression of tight junction molecule claudin-2 associated with Akt/GSK-3beta/beta-catenin signaling pathway J. Cell Bioch. 112 2011 1544 1551
14. L. Zhang, F. Jouret, J. Rinehart, J. Sfakianos, I. Mellman, R.P. Lifton, L.H. Young, and M.J. Caplan AMP-activated protein kinase (AMPK) activation and glycogen synthase kinase-3beta (GSK-3beta) inhibition induce Ca2 +-independent deposition of tight junction components at the plasma membrane J. Biol. Chem. 286 2011 16879 16890
15. R. Lander, T. Nasr, S.D. Ochoa, K. Nordin, M.S. Prasad, and C. Labonne Interactions between Twist and other core epithelial-mesenchymal transition factors are controlled by GSK3-mediated phosphorylation Nat. Commun. 4 2013 1542
16. N. Miwa, M. Furuse, S. Tsukita, N. Niikawa, Y. Nakamura, and Y. Furukawa Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers Oncol. Res. 12 2001 469 476
17. O.M. Martinez-Estrada, A. Culleres, F.X. Soriano, H. Peinado, V. Bolos, F.O. Martinez, M. Reina, A. Cano, M. Fabre, and S. Vilaro The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells Biochem. J. 394 2006 449 457
18. T. Ohkubo, and M. Ozawa The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation J. Cell Sci. 117 2004 1675 1685
19. S.H. Ramirez, S. Fan, H. Dykstra, S. Rom, A. Mercer, N.L. Reichenbach, L. Gofman, and Y. Persidsky Inhibition of glycogen synthase kinase 3beta promotes tight junction stability in brain endothelial cells by half-life extension of occludin and claudin-5 PLoS One 8 2013 e55972
20. D. Zwanziger, C. Staat, A.V. Andjelkovic, and I.E. Blasig Claudin-derived peptides are internalized via specific endocytosis pathways Ann. N. Y. Acad. Sci. 1257 2012 29 37
21. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110
22. H.L. Rittner, D. Hackel, P. Voigt, S.A. Mousa, A. Stolz, D. Labuz, M. Schäfer, M. Schaefer, C. Stein, and A. Brack Mycobacteria attenuate nociceptive responses by formyl peptide receptor triggered opioid peptide release from neutrophils PLoS Pathog. 5 2009 e1000362
23. W. Puehler, C. Zöllner, A. Brack, M.A. Shaqura, H. Krause, M. Schafer, and C. Stein Rapid upregulation of mu opioid receptor mRNA in dorsal root ganglia in response to peripheral inflammation depends on neuronal conduction Neurosci 129 2004 473 479
24. D.K. Thotala, L. Geng, A.K. Dickey, D.E. Hallahan, and E.M. Yazlovitskaya A new class of molecular targeted radioprotectors: GSK-3beta inhibitors Int. J. Radiat. Oncol. Biol. Phys. 76 2010 557 565
25. I.E. Blasig, L. Winkler, B. Lassowski, S.L. Mueller, N. Zuleger, E. Krause, G. Krause, K. Gast, M. Kolbe, and J. Piontek On the self-association potential of transmembrane tight junction proteins Cell. Mol. Life Sci. 63 2006 505 514
26. C. Stein, A.H. Hassan, R. Przewlocki, C. Gramsch, K. Peter, and A. Herz Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation PNAS 87 1990 5935 5939
27. S. Peng, V.S. Rao, R.A. Adelman, and L.J. Rizzolo Claudin-19 and the barrier properties of the human retinal pigment epithelium Invest. Ophthalmol. Vis. Sci. 52 2011 1392 1403
28. S.M. Krug, S. Amasheh, J.F. Richter, S. Milatz, D. Gunzel, J.K. Westphal, O. Huber, J.D. Schulzke, and M. Fromm Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability Mol. Biol. Cell 20 2009 3713 3724
29. T.A. Brooks, B.T. Hawkins, J.D. Huber, R.D. Egleton, and T.P. Davis Chronic inflammatory pain leads to increased blood-brain barrier permeability and tight junction protein alterations Am. J. Physiol. Heart Circ. Physiol. 289 2005 H738 H743
30. C.M. Cereda, G.R. Tofoli, L.G. Maturana, A. Pierucci, L.A. Nunes, M. Franz-Montan, A.L. de Oliveira, S. Arana, D.R. de Araujo, and E. de Paula Local neurotoxicity and myotoxicity evaluation of cyclodextrin complexes of bupivacaine and ropivacaine Anesth. Analg. 115 2012 1234 1241
31. N. Üceyler, I. Kobsar, L. Biko, J. Ulzheimer, S.R. Levinson, R. Martini, and C. Sommer Heterozygous P0 deficiency protects mice from vincristine-induced polyneuropathy J. Neurosci. Res. 84 2006 37 46
32. A.A. Bhat, A. Sharma, J. Pope, M. Krishnan, M.K. Washington, A.B. Singh, and P. Dhawan Caudal homeobox protein Cdx-2 cooperates with Wnt pathway to regulate claudin-1 expression in colon cancer cells PLoS One 7 2012 e37174
33. S. Kucenas, N. Takada, H.C. Park, E. Woodruff, K. Broadie, and B. Appel CNS-derived glia ensheath peripheral nerves and mediate motor root development Nat. Neurosci. 11 2008 143 151
34. S. Pina-Oviedo, and C. Ortiz-Hidalgo The normal and neoplastic perineurium Adv. Anat. Pathol. 15 2008 147 164
35. H. Hirakawa, S. Okajima, T. Nagaoka, T. Takamatsu, and M. Oyamada Loss and recovery of the blood-nerve barrier in the rat sciatic nerve after crush injury are associated with expression of intercellular junctional proteins Exp. Cell Res. 284 2003 196 210
36. K.P. Pummi, A.M. Heape, R.A. Grenman, J.T. Peltonen, and S.A. Peltonen Tight junction proteins ZO-1, occludin, and claudins in developing and adult human perineurium J. Histochem. Cytochem. 52 2004 1037 1046
37. S. Poliak, S. Matlis, C. Ullmer, S.S. Scherer, and E. Peles Distinct claudins and associated PDZ proteins form different autotypic tight junctions in myelinating Schwann cells J. Cell Biol. 159 2002 361 372
38. G. Krause, L. Winkler, S.L. Mueller, R.F. Haseloff, J. Piontek, and I.E. Blasig Structure and function of claudins Biochim. Biophys. Acta 1778 2008 631 645
39. M. Furuse, M. Hata, K. Furuse, Y. Yoshida, A. Haratake, Y. Sugitani, T. Noda, A. Kubo, and S. Tsukita Claudin-based tight junctions are crucial for the mammalian epidermal barrier; a lesson from claudin-1-deficient mice J. Cell Biol. 156 2002 1099 1111
40. S. Hadj-Rabia, L. Baala, P. Vabres, D. Hamel-Teillac, E. Jacquemin, M. Fabre, S. Lyonnet, Y. De Prost, A. Munnich, M. Hadchouel, and A. Smahi Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease Gastroenterology 127 2004 1386 1390
41. T. Miyamoto, K. Morita, D. Takemoto, K. Takeuchi, Y. Kitano, T. Miyakawa, K. Nakayama, Y. Okamura, H. Sasaki, Y. Miyachi, M. Furuse, and S. Tsukita Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice J. Cell Biol. 169 2005 527 538
42. J. Hou, A. Renigunta, M. Konrad, A.S. Gomes, E.E. Schneeberger, D.L. Paul, S. Waldegger, and D.A. Goodenough Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex J. Clin. Invest. 118 2008 619 628
43. K. Umeda, T. Matsui, M. Nakayama, K. Furuse, H. Sasaki, M. Furuse, and S. Tsukita Establishment and characterization of cultured epithelial cells lacking expression of ZO-1 J. Biol. Chem. 279 2004 44785 44794
44. P.T. Ronaldson, K.M. Demarco, L. Sanchez-Covarrubias, C.M. Solinsky, and T.P. Davis Transforming growth factor-beta signaling alters substrate permeability and tight junction protein expression at the blood-brain barrier during inflammatory pain J. Cereb. Blood Flow Metab. 29 2009 1084 1098
45. S. Echeverry, X.Q. Shi, S. Rivest, and J. Zhang Peripheral nerve injury alters blood-spinal cord barrier functional and molecular integrity through a selective inflammatory pathway J. Neurosci. 31 2011 10819 10828
46. S. Beggs, X.J. Liu, C. Kwan, and M.W. Salter Peripheral nerve injury and TRPV1-expressing primary afferent C-fibers cause opening of the blood-brain barrier Mol. Pain. 6 2010 74
47. L. Winkler, C. Gehring, A. Wenzel, S.L. Muller, C. Piehl, G. Krause, I.E. Blasig, and J. Piontek Molecular determinants of the interaction between Clostridium perfringens enterotoxin fragments and claudin-3 J. Biol. Chem. 284 2009 18863 18872
48. H. Dyhre, L. Soderberg, S. Bjorkman, and C. Carlsson Local anesthetics in lipid-depot formulations - neurotoxicity in relation to duration of effect in a rat model Reg. Anesth. Pain Med. 31 2006 401 408
49. L. Soderberg, H. Dyhre, B. Roth, and S. Bjorkman Ultralong peripheral nerve block by lidocaine:prilocaine 1:1 mixture in a lipid depot formulation: comparison of in vitro, in vivo, and effect kinetics Anesthesiology 104 2006 110 121
50. C.M. Peters, D. Ririe, T.T. Houle, C.A. Aschenbrenner, and J.C. Eisenach Nociceptor-selective peripheral nerve block induces delayed mechanical hypersensitivity and neurotoxicity in rats Anesthesiology 120 4 2014 976 986
51. G.K. Harper, M.A. Stafford, and D.A. Hill Minimum volume of local anaesthetic required to surround each of the constituent nerves of the axillary brachial plexus, using ultrasound guidance: a pilot study Br. J. Anaesth. 104 2010 633 636
52. O. Sanchez-Ferras, B. Coutaud, T. Djavanbakht Samani, I. Tremblay, O. Souchkova, and N. Pilon Caudal-related homeobox (Cdx) protein-dependent integration of canonical Wnt signaling on paired-box 3 (Pax3) neural crest enhancer J. Biol. Chem. 287 2012 16623 16635