Cell-Penetrating Peptides as Carriers for Oral Delivery of Biopharmaceuticals

Basic and Clinical Pharmacology and Toxicology

Volumn 118, Issue 2, 2016, Pages 99-106

  Kristensen, Mie ^a   Nielsen, Hanne Mørck ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PENETRATING PEPTIDE; DRUG; DRUG CARRIER; EXENDIN 4; GASTRIN; GLUCAGON LIKE PEPTIDE 1; GLYCOSAMINOGLYCAN; INSULIN; INTERLEUKIN 6; PARATHYROID HORMONE; PARATHYROID HORMONE[1-34]; PENETRATIN; POLYARGININE; SIALIC ACID DERIVATIVE; TRANSACTIVATOR PROTEIN; DRUG DOSAGE FORM;

ARTICLE; COMPLEX FORMATION; DRUG DELIVERY SYSTEM; DRUG FORMULATION; ENDOCYTOSIS; ENZYMATIC DEGRADATION; HUMAN; INTESTINE; METABOLIC STABILITY; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; TRANSCYTOSIS; CHEMISTRY; DRUG ADMINISTRATION ROUTE; DRUG DOSAGE FORM; METABOLISM; PROCEDURES;

CELL-PENETRATING PEPTIDES; DOSAGE FORMS; DRUG ADMINISTRATION ROUTES; DRUG DELIVERY SYSTEMS; HUMANS;

EID: 84983201990     PISSN: 17427835     EISSN: 17427843     Source Type: Journal    
DOI: 10.1111/bcpt.12515     Document Type: Article

References (53)

1. Hamman JH, Enslin GM, Kotzé AF. Oral delivery of peptide drugs: barriers and developments. BioDrugs 2005;19:165-77.
2. Frankel A, Pabo C. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988;8:1189-93.
3. Lindgren M, Hällbrink M, Prochiantz A, Langel U. Cell-penetrating peptides. Trends Pharmacol Sci 2000;21:99-103.
4. Milletti F. Cell-penetrating peptides: classes, origin, and current landscape. Drug Discov Today 2012;17:850-60.
5. Lindgren M, Rosenthal-Aizman K, Saar K, Eiríksdóttir E, Jiang Y, Sassian M et al. Overcoming methotrexate resistance in breast cancer tumour cells by the use of a new cell-penetrating peptide. Biochem Pharmacol 2006;71:416-25.
6. Stewart KM, Horton KL, Kelley SO. Cell-penetrating peptides as delivery vehicles for biology and medicine. Org Biomol Chem 2008;6:2242-55.
7. Margus H, Padari K, Pooga M. Cell-penetrating peptides as versatile vehicles for oligonucleotide delivery. Mol Ther 2012;20:525-33.
8. Morris MC, Depollier J, Mery J, Heitz F, Divita G. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat Biotechnol 2001;19:1173-6.
9. Khafagy E-S, Morishita M. Oral biodrug delivery using cell-penetrating peptide. Adv Drug Deliv Rev 2012;64:531-9.
10. McConnell EL, Fadda HM, Basit AW. Gut instincts: explorations in intestinal physiology and drug delivery. Int J Pharm 2008;364:213-26.
11. Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014;14:141-53.
12. Boegh M, Nielsen HM. Mucus as a barrier to drug delivery - understanding and mimicking the barrier properties. Basic Clin Pharmacol Toxicol 2015;116:179-86.
13. Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001;2:285-93.
14. Tuma PL, Hubbard AL. Transcytosis: crossing cellular barriers. Physiol Rev 2003;83:871-932.
15. Kristensen M, Foged C, Berthelsen J, Nielsen HM. Peptide-enhanced oral delivery of therapeutic peptides and proteins. J Drug Deliv Sci Technol 2013;23:365-73.
16. Ziegler A, Seelig J. Binding and clustering of glycosaminoglycans: a common property of mono- and multivalent cell-penetrating compounds. Biophys J 2008;94:2142-9.
17. Rydberg HA, Matson M, Amand HL, Esbjörner EK, Nordén B. Effects of tryptophan content and backbone spacing on the uptake efficiency of cell-penetrating peptides. Biochemistry 2012;51:5531-9.
18. Bechara C, Pallerla M, Zaltsman Y, Burlina F, Alves ID, Lequin O et al. Tryptophan within basic peptide sequences triggers glycosaminoglycan-dependent endocytosis. Biochemistry 2013;27:1-12.
19. Liang JF, Yang VC. Insulin-cell penetrating peptide hybrids with improved intestinal absorption efficiency. Biochem Biophys Res Commun 2000;335:734-8.
20. 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;118:177-84.
21. Caldinelli L, Albani D, Pollegioni L. One single method to produce native and Tat-fused recombinant human α-synuclein in Escherichia coli. BMC Biotechnol 2013;13:32.
22. Kristensen M, de Groot AM, Berthelsen J, Franzyk H, Sijts A, Nielsen HM. Conjugation of cell-penetrating peptides to parathyroid hormone affects its structure, potency, and transepithelial permeation. Bioconjug Chem 2015;26:477-88.
23. Kristensen M, Franzyk H, Klausen MT, Iversen A, Bahnsen JS, Skyggebjerg RB et al. Penetratin-mediated transepithelial insulin permeation: importance of cationic residues and pH for complexation and permeation. AAPS J 2015;17:1200-9.
24. Rosenberg AS. Effects of protein aggregates: an immunologic perspective. AAPS J 2006;8:501-7.
25. 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;132:21-5.
26. Nielsen EJB, Yoshida S, Kamei N, Iwamae R, Khafagy E-S, Olsen J et al. In vivo proof of concept of oral insulin delivery based on a co-administration strategy with the cell-penetrating peptide penetratin. J Control Release 2014;189:19-24.
27. Khafagy E-S, Morishita M, Ida N, Nishio R, Isowa K, Takayama K. Structural requirements of penetratin absorption enhancement efficiency for insulin delivery. J Control Release 2010;143:302-10.
28. Kamei N, Kikuchi S, Takeda-morishita M, Terasawa Y, Yasuda A, Yamamoto S et al. Determination of the optimal cell-penetrating peptide sequence for intestinal insulin delivery based on molecular orbital analysis with self-organizing maps. J Pharm Sci 2013;102:469-79.
29. Mitchell DJ, Kim DT, Steinman L, Fathman CG, Rothbard JB. Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 2000;56:318-25.
30. Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 1994;269:10444-50.
31. Khafagy E-S, Kamei N, Nielsen EJB, Nishio R, Takeda-Morishita M. One-month subchronic toxicity study of cell-penetrating peptides for insulin nasal delivery in rats. Eur J Pharm Biopharm 2013;85:736-43.
32. Khafagy E-S, Morishita M, Takayama K. The role of intermolecular interactions with penetratin and its analogue on the enhancement of absorption of nasal therapeutic peptides. Int J Pharm 2010;388:209-12.
33. Khafagy E-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.
34. Horne WS, Gellman SH. Foldamers with heterogeneous backbones. Acc Chem Res 2008;41:1399-408.
35. Rennert R, Wespe C, Beck-Sickinger AG, Neundorf I. Developing novel hCT derived cell-penetrating peptides with improved metabolic stability. Biochim Biophys Acta 2006;1758:347-54.
36. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ et al. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J Biol Chem 2003;278:585-90.
37. El-Andaloussi S, Holm T, Langel U. Cell-penetrating peptides: mechanisms and applications. Curr Pharm Des 2005;11:3597-611.
38. Cleal K, He L, Watson PD, Jones AT. Endocytosis, intracellular traffic and fate of cell penetrating peptide based conjugates and nanoparticles. Curr Pharm Des 2013;19:2878-94.
39. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003;422:37-44.
40. Clayton AHA, Atcliffe BW, Howlett GJ, Sawyer WH. Conformation and orientation of penetratin in phospholipid membranes. J Pept Sci 2006;12:233-8.
41. Sakai N, Takeuchi T, Futaki S, Matile S. Direct observation of anion-mediated translocation of fluorescent oligoarginine carriers into and across bulk liquid and anionic bilayer membranes. ChemBioChem 2005;6:114-22.
42. Zhu X, Shan W, Zhang P, Jin Y, Guan S, Fan T et al. Penetratin derivative-based nanocomplexes for enhanced intestinal insulin delivery. Mol Pharm 2014;11:317-28.
43. Kosuge M, Takeuchi T, Nakase I, Jones AT, Futaki S. Cellular internalization and distribution of arginine-rich peptides as a function of extracellular peptide concentration, serum, and plasma membrane associated proteoglycans. Bioconjug Chem 2008;19:656-64.
44. Tünnemann G, Martin RM, Haupt S, Patsch C, Edenhofer F, Cardoso MC. Cargo-dependent mode of uptake and bioavailability of Tat-containing proteins and peptides in living cells. FASEB J 2006;20:1775-84.
45. Hirose H, Takeuchi T, Osakada H, Pujals S, Katayama S, Nakase I et al. Transient focal membrane deformation induced by arginine-rich peptides leads to their direct penetration into cells. Mol Ther 2012;20:1-10.
46. Zhang X, Wan L, Pooyan S, Su Y, Gardner CR, Leibowitz MJ et al. Quantitative assessment of the cell penetrating properties of RI-Tat-9: evidence for a cell type-specific barrier at the plasma membrane of epithelial cells. Mol Pharm 2004;1:145-55.
47. Jones AT, Sayers EJ. Cell entry of cell penetrating peptides: tales of tails wagging dogs. J Control Release 2012;161:582-91.
48. Verdurmen WPR, Thanos M, Ruttekolk IR, Gulbins E, Brock R. Cationic cell-penetrating peptides induce ceramide formation via acid sphingomyelinase: implications for uptake. J Control Release 2010;147:171-9.
49. Herce HD, Garcia AE, Cardoso MC. Fundamental molecular mechanism for the cellular uptake of guanidinium-rich molecules. J Am Chem Soc 2014;136:17459-67.
50. Alves ID, Bechara C, Walrant A, Zaltsman Y, Jiao CY, Sagan S. Relationships between membrane binding, affinity and cell internalization efficacy of a cell-penetrating peptide: penetratin as a case study. PLoS ONE 2011;6:e24096.
51. Lukyanenko V, Malyukova I, Hubbard A, Delannoy M, Boedeker E, Zhu C et al. Enterohemorrhagic Escherichia coli infection stimulates Shiga toxin 1 macropinocytosis and transcytosis across intestinal epithelial cells. Am J Cell Physiol 2011;301:1140-9.
52. Luzio JP, Pryor PR, Bright NA. Lysosomes: fusion and function. Nat Rev Mol Cell Biol 2007;8:622-32.
53. Taverner A, Dondi R, Almansour K, Laurent F, Owens S-E, Eggleston IM et al. Enhanced paracellular transport of insulin can be achieved via transient induction of myosin light chain phosphorylation. J Control Release 2015;210:189-97.