Oral biodrug delivery using cell-penetrating peptide

Advanced Drug Delivery Reviews

Volumn 64, Issue 6, 2012, Pages 531-539

  Khafagy, El Sayed ^a   Morishita, Mariko ^b  

^a Suez Canal University   (Egypt)

^b HOSHI UNIVERSITY   (Japan)

Author keywords

Biodrugs; Cell penetrating peptides; Intestinal absorption; Molecular and biological factors; Non invasive; Oral delivery; Perspectives; Pharmaceutical strategy; Therapeutic peptides and proteins

Indexed keywords

BIODRUGS; BIOLOGICAL FACTORS; CELL-PENETRATING PEPTIDE; INTESTINAL ABSORPTION; NON-INVASIVE; ORAL DELIVERY; PERSPECTIVES; THERAPEUTIC PEPTIDES;

BIOCHEMISTRY; DRUG INTERACTIONS; DRUG PRODUCTS;

PEPTIDES;

ARGININE DERIVATIVE; CELL PENETRATING PEPTIDE; GALLIUM EDETATE GA 68; INSULIN; LACTATE DEHYDROGENASE; OLIGOARGININE; PENETRATIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

AREA UNDER THE CURVE; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG DISTRIBUTION; DRUG HALF LIFE; DRUG RESEARCH; ENTEROPATHY; HUMAN; INTESTINE ABSORPTION; INTESTINE EPITHELIUM; MEMBRANE PERMEABILITY; METHODOLOGY; MOLECULAR INTERACTION; NONHUMAN; ORAL DRUG ADMINISTRATION; PERMEABILITY BARRIER; PRIORITY JOURNAL; REVIEW;

ADMINISTRATION, ORAL; ANIMALS; BIOLOGICAL AVAILABILITY; CELL-PENETRATING PEPTIDES; DRUG DELIVERY SYSTEMS; DRUG DESIGN; HUMANS; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; PEPTIDES; PERMEABILITY; PROTEINS; TISSUE DISTRIBUTION;

EID: 84859720244     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2011.12.014     Document Type: Review

References (83)

1. Flower D.R. Advances in predicting and manipulating the immunogenicity of biotherapeutics and vaccines. BioDrugs 2009, 23:231-240.
2. Frokjaer S., Otez D.D. Protein drug stability: a formulation challenge. Nat. Rev. Drug Discov. 2005, 4:298-306.
3. Kumar T.R., Soppimath K., Nachaegari S.K. Novel delivery technologies for protein and peptide therapeutics. Curr. Pharm. Biotechnol. 2006, 7:261-276.
4. Cleland J.L., Daugherty A., Mrsny R. Emerging protein delivery methods. Curr. Opin. Biotechnol. 2001, 12:212-219.
5. Khafagy El-S., Morishita M., Onuki Y., Takayama K. Current challenges in noninvasive insulin delivery systems: a comparative review. Adv. Drug Deliv. Rev. 2007, 59:1521-1546.
6. Mustata G., Dinh S.M. Approaches to oral drug delivery for challenging molecules. Crit. Rev. Ther. Drug Carrier Syst. 2006, 23:111-1135.
7. Owens D.R. New horizons-alternative routes for insulin therapy. Nat. Rev. Drug Discov. 2002, 1:529-540.
8. Cefalu W.T. Concept, strategies, and feasibility of non-invasive insulin delivery. Diabetes Care 2004, 27:239-246.
9. Morishita M., Peppas N.A. Is the oral route possible for peptide and protein drug delivery?. Drug Discov. Today 2006, 11:905-910.
10. Goldberg M., Gomez-Orellana I. Challenges for the oral delivery of macromolecules. Nat. Rev. Drug Discov. 2003, 2:289-295.
11. Colombo P., Sonvico F., Colombo G., Bettini R. Novel platforms for oral drug delivery. Pharm. Res. 2009, 26:601-611.
12. Lane E.M., O'driscoll C.M., Corrigan O.I. Quantitative estimation of the effects of bile salts surfactant systems on insulin stability and permeability in the rat intestine using a mass balance model. J. Pharm. Pharmacol. 2005, 57:169-175.
13. Uchiyama T., Sugiyama T., Quan Y.S., Kotani A., Okada N., Fujita T., Muranishi S., Yamamoto A. Enhanced permeability of insulin across the rat intestinal membrane by various absorption enhancers: their intestinal mucosal toxicity and absorption enhancing mechanism of n-lauryl-β-d-maltopyranoside. J. Pharm. Pharmacol. 1999, 51:1241-1250.
14. 2EDTA and sodium glycocholate on intestinal absorption of insulin. Biol. Pharm. Bull. 1993, 16:68-72.
15. Salama N.N., Eddington N.D., Fasano A. Tight junction modulation and its relationship to drug delivery. Adv. Drug Deliv. Rev. 2006, 58:15-28.
16. Fasano A., Uzzau S. Modulation of intestinal tight junctions by zonula occludens toxin permits enteral administration of insulin and other macromolecules in an animal model. J. Clin. Invest. 1997, 99:1158-1164.
17. Agarwal V., Reddy I.K., Khan M.A. Polmethylacrylate microcapsules of insulin for oral delivery: preparation and in vitro dissolution stability in the presence of enzyme inhibitors. Int. J. Pharm. 2001, 225:31-39.
18. Agarwal V., Nazzal S., Reddy I.K., Khan M.A. Transport studies of insulin across rat jejunum in the presence of chicken and duck ovomucoid. J. Pharm. Pharmacol. 2001, 53:1131-1138.
19. Marschütz M.K., Caliceti P., Bernkop-Schnürch A. Design and in vivo evaluation of an oral delivery system for insulin. Pharm. Res. 2000, 17:468-1474.
20. Takeuchi H., Yamamoto H., Niwa T., Hino T., Kawashima Y. Enteral absorption of insulin in rats from mucoadhesive chitosan-coated liposomes. Pharm. Res. 1996, 13:896-901.
21. Bernkop-Schnürch A., Krajicek M.E. Mucoadhesive polymers as platforms for peroral peptide delivery and absorption: synthesis and evaluation of different chitosan-EDTA conjugates. J. Control. Release 2001, 50:215-223.
22. Lehr C.M. Lectin-mediated drug delivery: the second generation of bioadhesive. J. Control. Release 2000, 65:19-29.
23. Lowman A.M., Morishita M., Kajita M., Nagai T., Peppas N.A. Oral delivery of insulin using pH-responsive complexation gels. J. Pharm. Sci. 1999, 88:933-937.
24. Morishita M., Goto T., Nakamura K., Lowman A.M., Takayama K., Peppas N.A. Novel oral insulin delivery systems based on complexation polymer hydrogels: single and multiple administration studies in type 1 and 2 diabetic rats. J. Control. Release 2006, 110:587-594.
25. Watnasirichaikull S., Rades T., Tucker I.G., Davies N.M. In vitro release and oral bioactivity of insulin in diabetic rats using nanocapsules dispersed in biocompatible microemulsion. J. Pharm. Pharmacol. 2002, 54:473-480.
26. Kisel M.A., Kulik L.N., Tsybovsky I.S., Vlasov A.P., Vorob'yov M.S., Kholodova E.A., Zabarovskaya Z.V. Liposomes with phosphatidylethanol as a carrier for oral delivery of insulin: studies in the rat. Int. J. Pharm. 2001, 216:105-114.
27. Sajeesh S., Sharma C.P. Novel pH responsive polymethacrylic acid-chitosan-polyethylene glycol nanoparticles for oral peptide delivery. J. Biomed. Mater. Res. B. Appl. Biomater. 2005, 76:298-305.
28. Tozaki H., Nishioka J., Komoike J., Okada N., Fujita T., Muranishi S., Kim S.I., Terashima H., Yamamoto A. Enhanced absorption of insulin and (Asu1,7)eel-calcitonin using novel azopolymer-coated pellets for colon-specific drug delivery. J. Pharm. Sci. 2001, 90:89-97.
29. Sarciaux J.M., Acar L., Sado P.A. Using microemulsion formulation for oral drug delivery of therapeutic peptides. Int. J. Pharm. 1995, 120:127-136.
30. Hillery A.M., Jani P.U., Florence A.T. Comparative, quantitative study of lymphoid and non-lymphoid uptake of 60 nm particles. J. Drug Target. 1994, 2:151-156.
31. Xia C.Q., Wang J., Shen W.C. Hypoglycemic effect of insulin-transferrin conjugate in streptozotocin-induced diabetic rats. J. Pharmacol. Exp. Ther. 2000, 295:594-600.
32. Foged C., Nielsen H.M. Cell-penetrating peptides for drug delivery across membrane barriers. Expert Opin. Drug Deliv. 2008, 5:105-117.
33. Patel L.N., Zaro J.L., Shen W.C. Cell penetrating peptides: intracellular pathways and pharmaceutical perspectives. Pharm. Res. 2007, 24:1977-1992.
34. Futaki S. Arginine-rich peptides: potential for intracellular delivery of macromolecules and the mystery of the translocation mechanisms. Int. J. Pharm. 2002, 245:1-7.
35. Futaki S. Membrane-permeable arginine-rich peptides and the translocation mechanisms. Adv. Drug Deliv. Rev. 2005, 57:547-558.
36. Futaki S., Suzuki T., Ohashi W., Yagami T., Tanaka S., Ueda K., Sugiura Y. Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 2001, 276:5836-5840.
37. Nakase I., Takeuchi T., Tanaka G., Futaki S. Methodological and cellular aspects that govern the internalization mechanisms of arginine-rich cell-penetrating peptides. Adv. Drug Deliv. Rev. 2008, 60:598-607.
38. Vives E., Brodin P., Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 1997, 272:16010-16017.
39. Mitchell D.J., Kim D.T., Steinman L., Fathman C.G., Rothbard J.B. Polyarginine enters cells more efficiently than other polycationic homopolymers. J. Pept. Res. 2000, 56:318-325.
40. Derossi D., Joliot A.H., Chassaing G., Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 1994, 269:10444-10450.
41. Richard J.P., Melikov K., Vives E., Ramos C., Verbeure B., Gait M.J., Chernomordik L.V., Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 2003, 278:585-590.
42. Marty C., Meylan C., Schott H., Ballmer-Hofer K., Schwendener R.A. Enhanced heparan sulfate proteoglycan-mediated uptake of cell-penetrating peptide-modified liposomes. Cell. Mol. Life Sci. 2004, 61:1785-1794.
43. Tyagi M., Rusnati M., Presta M., Giacca M. Internalization of HIV-1 Tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 2001, 276:3254-3261.
44. Wadia J.S., Stan R.V., Dowdy S.F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 2004, 10:310-315.
45. Nakase I., Niwa M., Takeuchi T., Sonomura K., Kawabata N., Koike Y., Takehashi M., Tanaka S., Ueda K., Simpson J.C., Jones A.T., Sugiura Y., Futaki S. Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol. Ther. 2004, 10:1011-1022.
46. Khalil I.A., Kogure K., Futaki S., Harashima H. High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression. J. Biol. Chem. 2006, 281:3544-3551.
47. Kaplan I.M., Wadia J.S., Dowdy S.F. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J. Control. Release 2005, 102:247-253.
48. Swanson J.A., Watts C. Macropinocytosis. Trends Cell Biol. 1995, 5:424-428.
49. Falcone S., Cocucci E., Podini P., Kirchhausen T., Clementi E., Meldolesi J. Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events. J. Cell Sci. 2006, 119:4758-4769.
50. Massodi I., Bidwell G.L., Raucher D. Evaluation of cell penetrating peptides fused to elastin-like polypeptide for drug delivery. J. Control. Release 2005, 108:396-408.
51. Kleemann E., Neu M., Jekel N., Fink L., Schmehl T., Gessler T., Seeger W., Kissel T. Nano-carriers for DNA delivery to the lung based upon a TAT-derived peptide covalently coupled to PEG-PEI. J. Control. Release 2005, 109:299-316.
52. El-Andaloussi S., Guterstam P., Langel Ü. Assessing the delivery efficacy and internalization route of cell-penetrating peptides. Nat. Protoc. 2007, 2:2043-2047.
53. Torchilin V.P., Levchenko T.S., Rammohan R., Volodina N., Papahadjopoulos-Sternberg B., D'Souza G.G. Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome-DNA complexes. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:1972-1977.
54. Torchilin V.P. Multifunctional nanocarriers. Adv. Drug Deliv. Rev. 2006, 58:1532-1555.
55. Schwarze S.R., Ho A., Vocero-Akbani A., Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 1999, 285:1569-1572.
56. Liang J.F., Yang V.C. Insulin-cell penetrating peptide hybrids with improved intestinal absorption efficiency. Biochem. Biophys. Res. Commun. 2005, 335:734-738.
57. Kamei N., Morishita M., Ehara J., Takayama K. Permeation characteristics of oligoarginine through intestinal epithelium and its usefulness for intestinal peptide drug delivery. J. Control. Release 2008, 131:94-99.
58. Hawiger J. Noninvasive intracellular delivery of functional peptides and proteins. Curr. Opin. Chem. Biol. 1999, 3:89-94.
59. Morishita M., Kamei N., Ehara J., Isowa K., Takayama K. A novel approach using functional peptides for efficient intestinal absorption of insulin. J. Control. Release 2007, 118:177-184.
60. Kamei N., Morishita M., Eda Y., Ida N., Nishio R., Takayama K. Usefulness of cell-penetrating peptides to improve intestinal insulin absorption. J. Control. Release 2008, 132:21-25.
61. Khafagy El-S., Morishita M., Kamei N., Eda Y., Ikeno Y., Takayama K. Efficiency of cell-penetrating peptides on the nasal and intestinal absorption of therapeutic peptides and proteins. Int. J. Pharm. 2009, 381:49-55.
62. Jones S.W., Christison R., Bundell K., Voyce C.J., Brockbank S.M., Newham P., Lindsay M.A. Characterisation of cell-penetrating peptide-mediated peptide delivery. Br. J. Pharmacol. 2005, 145:1093-1102.
63. Ziegler A. Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv. Drug Deliv. Rev. 2008, 60:580-597.
64. Kamei N., Morishita M., Takayama K. Importance of intermolecular interaction on the improvement of intestinal therapeutic peptide/protein absorption using cell-penetrating peptides. J. Control. Release 2009, 136:179-186.
65. Joliot A., Prochiantz A. Hemoproteins as natural penetratin cargoes with signaling properties. Adv. Drug Deliv. Rev. 2008, 60:608-613.
66. Persson D., Thorén P.E., Lincoln P., Nordén B. Vesicle membrane interactions of penetratin analogues. Biochemistry 2004, 43:11045-11055.
67. Elmquist A., Langel Ü. In vitro uptake and stability study of pVEC and its all-D analog. Biol. Chem. 2003, 384:387-393.
68. Tugyl R., Uray K., Ivan D., Fellinger E., Perkins A., Hudecz F. Partial d-amino acid substitution: improved enzymatic stability and preserved Ab recognition of a MUC2 epitope peptide. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:413-418.
69. Khafagy El-S., Morishita M., Isowa K., Imai J., Takayama K. Effect of cell-penetrating peptides on the nasal absorption of insulin. J. Control. Release 2009, 133:103-108.
70. Suzuki R., Yamada Y., Harashima H. Efficient cytoplasmic protein delivery by means of a multifunctional envelope-type nano device. Biol. Pharm. Bull. 2007, 30:758-762.
71. Christiaens B., Grooten J., Reusens M., Joliot A., Goethals M., Vandekerckhove J., Prochiantz A., Rosseneu M. Membrane interaction and cellular internalization of penetratin peptides. Eur. J. Biochem. 2004, 271:1187-1197.
72. Brattwall C.E., Lincoln P., Nordén B. Orientation and conformation of cell-penetrating peptide penetratin in phospholipid vesicle membranes determined by polarized-light spectroscopy. J. Am. Chem. Soc. 2003, 125:14214-14215.
73. Järver P., Mäger I., Langel Ü. In vivo biodistribution and efficacy of peptide mediated delivery. Trends Pharmacol. Sci. 2010, 31:528-535.
74. Ohira T., Okuma T., Matsuoka T., Wada Y., Nakamura K., Watanabe Y., Inoue Y. FDG-microPET and diffusion-weighted MR image evaluation of early changes after radiofrequency ablation in implanted VX2 tumors in rabbits. Cardiovasc. Interv. Radiol. 2009, 32:114-120.
75. Okuma T., Matsuoka T., Okamura T., Wada Y., Yamamoto A., Oyama Y., Koyama K., Nakamura K., Watanabe Y., Inoue Y. 18F-FDG small-animal PET for monitoring the therapeutic effect of CT-guided radiofrequency ablation on implanted VX2 lung tumors in rabbits. J. Nucl. Med. 2006, 47:1351-1358.
76. Cui Y., Takamatsu H., Kakiuchi T., Ohba H., Kataoka Y., Yokoyama C., Onoe H., Watanabe Y., Hosoya T., Suzuki M., Noyori R., Tsukada H., Watanabe Y. Neuroprotection by a central nervous system-type prostacyclin receptor ligand demonstrated in monkeys subjected to middle cerebral artery occlusion and reperfusion: a positron emission tomography study. Stroke 2006, 37:2830-2836.
77. Sasabe T., Kobayashi M., Kondo Y., Onoe H., Matsubara S., Yamamoto S., Tsukada H., Onoe K., Watabe H., Iida H., Kogo M., Sano K., Hatanaka A., Sawada T., Watanabe Y. Activation of the anterior cingulate gyrus by 'Green Odor': a positron emission tomography study in the monkey. Chem. Senses 2003, 28:565-572.
78. Kobayashi M., Sasabe T., Takeda M., Kondo Y., Yoshikubo S., Imamura K., Onoe H., Sawada T., Watanabe Y. Functional anatomy of chemical senses in the alert monkey revealed by positron emission tomography. Eur. J. Neurosci. 2002, 16:975-980.
79. Kamei N., Morishita M., Kanayama Y., Hasegawa K., Nishimura M., Hayashinaka E., Wada Y., Watanabe Y., Takayama K. Molecular imaging analysis of intestinal insulin absorption boosted by cell-penetrating peptides by using positron emission tomography. J. Control. Release 2010, 146:16-22.
80. Duckworth W.C., Bennett R.G., Hamel F.G. Insulin degradation: progress and potential. Endocr. Rev. 1998, 19:608-624.
81. El-Andaloussi S., Järver P., Johansson H.J., Langel Ü. Cargo-dependent cytotoxicity and delivery efficacy of cell-penetrating peptides: a comparative study. Biochem. J. 2007, 407:285-292.
82. Saar K., Lindgren M., Hansen M., Eiriksdottir E., Jiang Y., Rosenthal-Aizman K., Sassian M., Langel Ü. Cell-penetrating peptides: a comparative membrane toxicity study. Anal. Biochem. 2005, 345:55-65.
83. Gonçalves E., Kitas E., Seelig J. Binding of oligoarginine to membrane lipids and heparan sulfate: structural and thermodynamic characterization of a cell-penetrating peptide. Biochemistry 2005, 44:2692-2702.