Melittin as a permeability enhancer II: In vitro investigations in human mucus secreting intestinal monolayers and rat colonic mucosae

Pharmaceutical Research

Volumn 24, Issue 7, 2007, Pages 1346-1356

  Maher, Sam ^a,b   Feighery, Linda ^c   Brayden, David J ^c   McClean, Siobhán ^a,b  

^a DUBLIN INSTITUTE OF TECHNOLOGY   (Ireland)

^b National Institute for Cellular Biotechnology   (Ireland)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Absorption enhancer; Gastrointestinal permeability models; Melittin; Oral peptide delivery; Ussing chambers

Indexed keywords

CALMODULIN; CARBON 14; ENZYME INHIBITOR; MANNITOL; MELITTIN; MOLECULAR MARKER; PENETRATION ENHANCING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CELL LINE; COLON MUCOSA; CONTROLLED STUDY; CYTOTOXICITY; DRUG PENETRATION; DRUG POTENTIATION; DRUG STABILITY; ELECTRIC RESISTANCE; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE ABSORPTION; INTESTINE EPITHELIUM CELL; INTESTINE SECRETION; IONIZATION CHAMBER; MONOLAYER CULTURE; MUCOUS CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SHORT CIRCUIT CURRENT; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CACO-2 CELLS; CALMODULIN; CELL SURVIVAL; COLON; DIFFUSION CHAMBERS, CULTURE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG STABILITY; ELECTRIC IMPEDANCE; HEMOLYSIS; HT29 CELLS; HUMANS; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; MALE; MANNITOL; MELITTEN; MEMBRANE POTENTIALS; MUCUS; PERMEABILITY; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; SHEEP; SULFONAMIDES; TRITIUM;

EID: 34249872197     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-007-9246-z     Document Type: Article

References (56)

1. C. A. Lipinski, F. Lombardo, B. W. Dominy, and P. J. Feeney. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 46:3-26 (2001).
2. J. Miyoshi and Y. Takai. Molecular perspective on tight-junction assembly and epithelial polarity. Adv. Drug Deliv. Rev. 57:815-855 (2005).
3. R. J. Mrsny. Modification of epithelial tight junction integrity to enhance transmucosal absorption. Crit. Rev. Ther. Drug Carr. Syst. 22:331-418 (2005).
4. N. A. Motlekar, K. S. Srivenugopal, M. S. Wachtel, and B. B. Youan. Oral delivery of low-molecular-weight heparin using sodium caprate as absorption enhancer reaches therapeutic levels. J. Drug Target. 13:573-583 (2005).
5. T. Lindmark, N. Schipper, L. Lazorova, A. G. de Boer, and P. Artursson. Absorption enhancement in intestinal epithelial Caco-2 monolayers by sodium caprate: assessment of molecular weight dependence and demonstration of transport routes. J. Drug Target. 5:215-223 (1998).
6. Y. Kato, H. Onishi, and Y. Machida. Application of chitin and chitosan derivatives in the pharmaceutical field. Curr. Pharm. Biotechnol. 4:303-309 (2003).
7. T. W. Leonard, J. Lynch, M. J. McKenna, and D. J. Brayden. Promoting absorption of drugs in humans using medium-chain fatty acid-based solid dosage forms: GIPET. Expert. Opin. Drug Deliv. 3:685-692 (2006).
8. M. T. Tosteson, S. J. Holmes, M. Razin, and D. C. Tosteson. Melittin lysis of red cells. J. Membr. Biol. 87:35-44 (1985).
9. G. L. Lee and W. N. Hait. Inhibition of growth of C6 astrocytoma cells by inhibitors of calmodulin. Life Sci. 36:347-354 (1985).
10. J. Cuppoletti, B. V. Chernyak, P. Huang, and D. H. Malinowska. Structure-function relationships in the interaction of amphipathic helical polypeptides with the gastric H/K ATPase. Ann. N. Y. Acad. Sci. 671:443-445 (1992).
11. J. Cuppoletti and D. H. Malinowska. Interaction of polypeptides with the gastric (H+ + K+)ATPase: melittin, synthetic analogs, and a potential intracellular regulatory protein. Mol. Cell. Biochem. 114:57-63 (1992).
12. S. S. Saini, A. K. Chopra, and J. W. Peterson. Melittin activates endogenous phospholipase D during cytolysis of human monocytic leukemia cells. Toxicon 37:1605-1619 (1999).
13. K. Koumanov, A. Momchilova, and C. Wolf. Bimodal regulatory effect of melittin and phospholipase A2-activating protein on human type II secretory phospholipase A2. Cell Biol. Int. 27:871-877 (2003).
14. K. R. Gravitt, N. E. Ward, and C. A. O'Brian. Inhibition of protein kinase C by melittin: antagonism of binding interactions between melittin and the catalytic domain by active-site binding of MgATP. Biochem. Pharmacol. 47:425-427 (1994).
15. L. Yang, T. A. Harroun, T. M. Weiss, L. Ding, and H. W. Huang. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81:1475-1485 (2001).
16. Y. Shai. Mode of action of membrane active antimicrobial peptides. Biopolymers 66:236-248 (2002).
17. P. M. Hwang and H. J. Vogel. Structure-function relationships of antimicrobial peptides. Biochem. Cell. Biol. 76:235-246 (1998).
18. P. Liu, P. Davis, H. Liu, and T. R. Krishnan. Evaluation of cytotoxicity and absorption enhancing effects of melittin-a novel absorption enhancer. Eur. J. Pharm. Biopharm. 48:85-87 (1999).
19. S. Maher, L. Feighery, D. Brayden, and S. McClean. Melittin as a permeability enhancer I: investigation of its mechanism of action in polarized Caco-2 cells. Pharm. Res. in press:(2006).
20. S. Maher and S. McClean. Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro. Biochem. Pharmacol. 71:1289-1298 (2006).
21. T. Lindmark, Y. Kimura, and P. Artursson. Absorption enhancement through intracellular regulation of tight junction permeability by medium chain fatty acids in Caco-2 cells. J. Pharmacol. Exp. Ther. 284:362-369 (1998).
22. C. Hilgendorf, H. Spahn-Langguth, C. G. Regardh, E. Lipka, G. L. Amidon, and P. Langguth. Caco-2 versus Caco-2/HT29-MTX co-cultured cell lines: permeabilities via diffusion, inside- and outside-directed carrier-mediated transport. J. Pharm. Sci. 89:63-75 (2000).
23. I. J. Hidalgo, T. J. Raub, and R. T. Borchardt. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96:736-749 (1989).
24. A. R. Hilgers, R. A. Conradi, and P. S. Burton. Caco-2 cell monolayers as a model for drug transport across the intestinal mucosa. Pharm. Res. 7:902-910 (1990).
25. I. Behrens, A. I. Pena, M. J. Alonso, and T. Kissel. Comparative uptake studies of bioadhesive and non-bioadhesive nanoparticles in human intestinal cell lines and rats: the effect of mucus on particle adsorption and transport. Pharm. Res. 19:1185-1193 (2002).
26. S. Keely, A. Rullay, C. Wilson, A. Carmichael, S. Carrington, A. Corfield, D. M. Haddleton, and D. J. Brayden. In vitro and ex vivo intestinal tissue models to measure mucoadhesion of poly (methacrylate) and N-trimethylated chitosan polymers. Pharm. Res. 22:38-49 (2005).
27. S. B. Suddarth. Acetylcysteine, a new and effective mucolytic agent. Bull. Geisinger. 15:65-69 (1963).
28. S. Soans, L. M. Galindo, and F. U. Garcia. Mucin stain on frozen sections: a rapid 3-minute method. Arch. Pathol. Lab. Med. 123:378-380 (1999).
29. S. McClean, E. Prosser, E. Meehan, D. O'Malley, N. Clarke, Z. Ramtoola, and D. Brayden. Binding and uptake of biodegradable poly-DL-lactide micro- and nanoparticles in intestinal epithelia. Eur. J. Pharm. Sci. 6:153-163 (1998).
30. A. W. Cuthbert and H. S. Margolius. Kinins stimulate net chloride secretion by the rat colon. Br. J. Pharmacol. 75:587-598 (1982).
31. K. E. Barrett and S. J. Keely. Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects. Annu. Rev. Physiol. 62:535-572 (2000).
32. E. K. Anderberg, C. Nystrom, and P. Artursson. Epithelial transport of drugs in cell culture. VII: effects of pharmaceutical surfactant excipients and bile acids on transepithelial permeability in monolayers of human intestinal epithelial (Caco-2) cells. J. Pharm. Sci. 81:879-887 (1992).
33. P. Artursson, A. L. Ungell, and J. E. Lofroth. Selective paracellular permeability in two models of intestinal absorption: cultured monolayers of human intestinal epithelial cells and rat intestinal segments. Pharm. Res. 10:1123-1129 (1993).
34. W. I. Lencer, G. Cheung, G. R. Strohmeier, M. G. Currie, A. J. Ouellette, M. E. Selsted, and J. L. Madara. Induction of epithelial chloride secretion by channel-forming cryptdins 2 and 3. Proc. Natl. Acad. Sci. U S A 94:8585-8589 (1997).
35. T. Sawai, N. Usui, J. Dwaihy, R. A. Drongowski, A. Abe, A. G. Coran, and C. M. Harmon. The effect of phospholipase A2 on bacterial translocation in a cell culture model. Pediatr. Surg. Int. 16:262-266 (2000).
36. P. Isenring and B. Forbush, 3rd. Ion and bumetanide binding by the Na-K-Cl cotransporter. Importance of transmembrane domains. J. Biol. Chem. 272:24556-24562 (1997).
37. A. Fasano, C. Fiorentini, G. Donelli, S. Uzzau, J. B. Kaper, K. Margaretten, X. Ding, S. Guandalini, L. Comstock, and S. E. Goldblum. Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro. J. Clin. Invest. 96:710-720 (1995).
38. T. Borbiev, A. D. Verin, S. Shi, F. Liu, and J. G. Garcia. Regulation of endothelial cell barrier function by calcium/calmodulin-dependent protein kinase II. Am. J. Physiol., Lung Cell. Mol. Physiol. 280:L983-990 (2001).
39. R. Hertle, R. Mrsny, and D. J. Fitzgerald. Dual-function vaccine for Pseudomonas aeruginosa: characterization of chimeric exotoxin A-pilin protein. Infect. Immun. 69:6962-6969 (2001).
40. M. E. Fernandez Miyakawa, V. Pistone Creydt, F. A. Uzal, B. A. McClane, and C. Ibarra. Clostridium perfringens enterotoxin damages the human intestine in vitro. Infect. Immun. 73:8407-8410 (2005).
41. A. P. Soler, R. D. Miller, K. V. Laughlin, N. Z. Carp, D. M. Klurfeld, and J. M. Mullin. Increased tight junctional permeability is associated with the development of colon cancer. Carcinogenesis 20:1425-1431 (1999).
42. T. Y. Ma, N. T. Hoa, D. D. Tran, V. Bui, A. Pedram, S. Mills, and M. Merryfield. Cytochalasin B modulation of Caco-2 tight junction barrier: role of myosin light chain kinase. Am. J. Physiol.: Gasterointest. Liver Physiol. 279:G875-G885 (2000).
43. A. Fasano, B. Baudry, D. W. Pumplin, S. S. Wasserman, B. D. Tall, J. M. Ketley, and J. B. Kaper. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc. Natl. Acad. Sci. U S A 88:5242-5246 (1991).
44. A. Fasano and S. Uzzau. Modulation of intestinal tight junctions by Zonula occludens toxin permits enteral administration of insulin and other macromolecules in an animal model. J. Clin. Invest. 99:1158-1164 (1997).
45. M. J. Cano-Cebrian, T. Zornoza, L. Granero, and A. Polache. Intestinal absorption enhancement via the paracellular route by fatty acids, chitosans and others: a target for drug delivery. Cur. Drug. Del. 9-22 (2005).
46. A. F. Kotze, H. L. Luessen, B. J. de Leeuw, A. G. de Boer, J. C. Verhoef, and H. E. Junginger. Comparison of the effect of different chitosan salts and N-trimethyl chitosan chloride on the permeability of intestinal epithelial cells (Caco-2). J. Control. Release 51:35-46 (1998).
47. A. F. Kotze, M. M. Thanou, H. L. Luebetaen, A. G. de Boer, J. C. Verhoef, and H. E. Junginger. Enhancement of paracellular drug transport with highly quaternized N-trimethyl chitosan chloride in neutral environments: in vitro evaluation in intestinal epithelial cells (Caco-2). J. Pharm. Sci. 88:253-257 (1999).
48. E. K. Anderberg and P. Artursson. Epithelial transport of drugs in cell culture. VIII: effects of sodium dodecyl sulfate on cell membrane and tight junction permeability in human intestinal epithelial (Caco-2) cells. J. Pharm. Sci. 82:392-398 (1993).
49. G. Schultheiss, R. Ribeiro, and M. Diener. Fatty acids inhibit anion secretion in rat colon: apical and basolateral action sites. Pflugers Arch. 442:603-613 (2001).
50. M. Diener and W. Rummel. Phospholipase A2 and mediation of the activation of short-circuit current in the rat colonic mucosa. Naunyn-Schmiedebergs Arch. Pharmacol. 343:652-658 (1991).
51. R. F. Steiner, L. Marshall, and D. Needleman. The interaction of melittin with calmodulin and its tryptic fragments. Arch. Biochem. Biophys. 246:286-300 (1986).
52. W. B. Gratzer and A. J. Baines. Calmodulin, Elsevier, 1988.
53. M. Hayashi, T. Sakai, Y. Hasegawa, T. Nishikawahara, H. Tomioka, A. Iida, N. Shimizu, M. Tomita, and S. Awazu. Physiological mechanism for enhancement of paracellular drug transport. J. Control. Release 62:141-148 (1999).
54. L. Liu, H. Yan, A. Ni, X. Cheng, and B. He. Interaction of calmodulin with synthetic deletion peptides of melittin. Int. J. Pept. Protein Res. 43:107-112 (1994).
55. M. Itakura and T. Iio. Static and kinetic studies of calmodulin and melittin complex. J. Biochem. (Tokyo) 112:183-191 (1992).
56. A. A. Sakr and W. A. -A. Habib. Oral formulation for treatment of bacteria-induced diseases of the colon. In U. S. P. Office (ed.), Vol. 5,958,873 (U. S. P. Office, ed), USA, 1997.