Mechanistic study of the uptake/permeation of cell-penetrating peptides across a caco-2 monolayer and their stimulatory effect on epithelial insulin transport

Journal of Pharmaceutical Sciences

Volumn 102, Issue 11, 2013, Pages 3998-4008

  Kamei, Noriyasu ^a   Onuki, Yoshinori ^b   Takayama, Kozo ^b   Takeda Morishita, Mariko ^a  

^a KOBE GAKUIN UNIVERSITY   (Japan)

^b HOSHI UNIVERSITY   (Japan)

Author keywords

Caco 2 cells; Cell penetrating peptides (CPPs); Epithelial delivery permeability; Epithelial permeation; Insulin; Intestinal absorption; Oligoarginine; Oral drug delivery; Penetratin; Transcellular transport

Indexed keywords

ARGININE; CELL PENETRATING PEPTIDE; FLUORESCEIN; HUMAN INSULIN; LACTATE DEHYDROGENASE; OCTAARGININE; OCTAPEPTIDE; OLIGOPEPTIDE; PENETRATIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CHEMICAL PARAMETERS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG ABSORPTION; DRUG CLEARANCE; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; ELECTRIC RESISTANCE; ENERGY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; INTESTINE ABSORPTION; INTESTINE EPITHELIUM; LOW TEMPERATURE; MONOLAYER CULTURE; PROTEIN BINDING; TOXICITY TESTING; TRANSEPITHELIAL ELECTRICAL RESISTANCE;

CACO-2 CELLS; CELL-PENETRATING PEPTIDES (CPPS); EPITHELIAL DELIVERY/PERMEABILITY; EPITHELIAL PERMEATION; INSULIN; INTESTINAL ABSORPTION; OLIGOARGININE; ORAL DRUG DELIVERY; PENETRATIN; TRANSCELLULAR TRANSPORT;

CACO-2 CELLS; CARRIER PROTEINS; CELL-PENETRATING PEPTIDES; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; OLIGOPEPTIDES; PERMEABILITY; PHARMACEUTICAL VEHICLES;

EID: 84885844778     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.23708     Document Type: Article

References (49)

1. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF. 1999. In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science 285:1569-1572.
2. Astriab-Fisher A, Sergueev D, Fisher M, Shaw BR, Juliano RL. 2002. Conjugates of antisense oligonucleotides with the TAT and antennapedia cell-penetrating peptides: Effects on cellular uptake, binding to target sequences, and biologic actions. Pharm Res 19:744-754.
3. Torchilin VP, Levchenko TS. 2003. TAT-liposomes: A novel intracellular drug carrier. Curr Protein Pept Sci 4:133-140.
4. Marty C, Meylan C, Schott H, Ballmer-Hofer K, Schwendener RA. 2004. Enhanced heparan sulfate proteoglycan-mediated uptake of cell-penetrating peptide-modified liposomes. Cell Mol Life Sci 61:1785-1794.
5. Gupta B, Levchenko TS, Torchilin VP. 2005. Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv Drug Deliv Rev 57:637-651.
6. Futaki S. 2006. Oligoarginine vectors for intracellular delivery: Design and cellular-uptake mechanisms. Biopolymers 84:241-249.
7. Foerg C, Merkle HP. 2008. On the biomedical promise of cell penetrating peptides: Limits versus prospects. J Pharm Sci 97:144-162.
8. Heitz F, Morris MC, Divita G. 2009. Twenty years of cell-penetrating peptides: From molecular mechanisms to therapeutics. Br J Pharmacol 157:195-206.
9. Fonseca SB, Pereira MP, Kelley SO. 2009. Recent advances in the use of cell-penetrating peptides for medical and biological applications. Adv Drug Deliv Rev 61:953-964.
10. Vives E, Brodin P, Lebleu B. 1997. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272:16010-16017.
11. Mitchell DJ, Kim DT, Steinman L, Fathman CG, Rothbard JB. 2000. Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 56:318-325.
12. Futaki S, Suzuki T, Ohashi W, Yagami T, Tanaka S, Ueda K, Sugiura Y. 2001. Arginine-rich peptides: An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J Biol Chem 276:5836-5840.
13. Nakase I, Takeuchi T, Tanaka G, Futaki S. 2008. Methodological and cellular aspects that govern the internalization mechanisms of arginine-rich cell-penetrating peptides. Adv Drug Deliv Rev 60:598-607.
14. Derossi D, Joliot AH, Chassaing G, Prochiantz A. 1994. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 269:10444-10450.
15. Derossi D, Calvet S, Trembleau A, Brunissen A, Chassaing G, Prochiantz A. 1996. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J Biol Chem 271:18188-18193.
16. Morishita M, Kamei N, Ehara J, Isowa K, Takayama K. 2007. A novel approach using functional peptides for efficient intestinal absorption. J Control Release 118:177-184.
17. Kamei N, Morishita M, Eda Y, Ida N, Nishio R, Takayama K. 2008. Usefulness of cell-penetrating peptides to improve intestinal insulin absorption. J Control Release 132:21-25.
18. Kamei N, Morishita M, Takayama K. 2009. Importance of intermolecular interaction on the improvement of intestinal therapeutic peptide/protein absorption using cell-penetrating peptides. J Control Release 136:179-186.
19. Khafagy ES, Morishita M, Kamei N, Eda Y, Ikeno Y, Takayama K. 2009. Efficiency of cell-penetrating peptides on the nasal and intestinal absorption of therapeutic peptides and proteins. Int J Pharm 381:49-55.
20. Kamei N, Morishita M, Kanayama Y, Hasegawa K, Nishimura M, Hayashinaka E, Wada Y, Watanabe Y, Takayama K. 2010. Molecular imaging analysis of intestinal insulin absorption boosted by cell-penetrating peptides by using positron emission tomography. J Control Release 146:16-22.
21. Kamei N, Kikuchi S, Takeda-Morishita M, Terasawa Y, Yasuda A, Yamamoto S, Ida N, Nishio R, Takayama K. 2013. Determination of the optimal cell-penetrating peptide sequence for intestinal insulin delivery based on molecular orbital analysis with self-organization maps. J Pharm Sci 102:469-479.
22. Goldberg M, Gomez-Orellana I. 2003. Challenges for the oral delivery of macromolecules. Nat Rev Drug Discov 2:289-295.
23. Owens DR, Zinman B, Bolli G. 2003. Alternative routes of insulin delivery. Diabet Med 20:886-898.
24. Morishita M, Peppas NA. Is the oral route possible for peptide and protein drug delivery? 2006. Drug Discov Today 11:905-910.
25. Khafagy ES, Morishita M, Onuki Y, Takayama K. 2007. Current challenges in non-invasive insulin delivery systems: A comparative review. Adv Drug Deliv Rev 59:1521-1546.
26. Kamei N, Morishita M, Ehara J, Takayama K. 2008. Permeation characteristics of oligoarginine through intestinal epithelium and its usefulness for intestinal peptide drug delivery. J Control Release 131:94-99.
27. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B. 2003. Cell-penetrating peptides: A reevaluation of the mechanism of cellular uptake. J Biol Chem 278:585-590.
28. Drin G, Cottin S, Blanc E, Rees AR, Temsamani J. 2003. Studies on the internalization mechanism of cationic cell-penetrating peptides. J Biol Chem 278:31192-31201.
29. Fittipaldi A, Ferrari A, Zoppe M, Arcangeli C, Pellegrini V, Beltram F, Giacca M. 2003. Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J Biol Chem 278:34141-34149.
30. Wadia JS, Stan RV, Dowdy SF. 2004. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 10:310-315.
31. Nakase I, Niwa M, Takeuchi T, Sonomura K, Kawabata N, Koike Y, Takehashi M, Tanaka S, Ueda K, Simpson JC, Jones AT, Sugiura Y, Futaki S. 2004. Cellular uptake of arginine-rich peptides: Roles for macropinocytosis and actin rearrangement. Mol Ther 10:1011-1022.
32. Richard JP, Melikov K, Brooks H, Prevot P, Lebleu B, Chernomordik LV. 2005. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J Biol Chem 280:15300-15306.
33. Kaplan IM, Wadia JS, Dowdy SF. 2005. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J Control Release 102:247-253.
34. Duchardt F, Fotin-Mleczek M, Schwarz H, Fischer R, Brock R. 2007. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8:848-866.
35. Fretz MM, Penning NA, Al-Taei S, Futaki S, Takeuchi T, Nakase I, Storm G, Jones AT. 2007. Temperature-, concentration- and cholesterol-dependent translocation of L- and D-octa-arginine across the plasma and nuclear membrane of CD34 +leukaemia cells. Biochem J 403:335-342.
36. Jiao CY, Delaroche D, Burlina F, Alves ID, Chassaing G, Sagan S. 2009. Translocation and endocytosis for cell-penetrating peptide internalization. J Biol Chem 284:33957-33965.
37. Zaro JL, Rajapaksa TE, Okamoto CT, Shen WC. 2006. Membrane transduction of oligoarginine in HeLa cells is not mediated by macropinocytosis. Mol Pharm 3:181-186.
38. Ter-Avetisyan G, Tunnemann G, Nowak D, Nitschke M, Herrmann A, Drab M, Cardoso MC. 2009. Cell entry of arginine-rich peptides is independent of endocytosis. J Biol Chem 284:3370-3378.
39. Tunnemann G, Martin RM, Haupt S, Patsch C, Edenhofer F, Cardoso MC. 2006. Cargo-dependent mode of uptake and bioavailability of TAT-containing proteins and peptides in living cells. FASEB J 20:1775-1784.
40. Bai JP, Hsu MJ, Shier WT. 1995. Insulin-degrading enzyme in a human colon adenocarcinoma cell line (Caco-2). Pharm Res 12:513-517.
41. Bai JP, Chang LL. 1995. Transepithelial transport of insulin: I. Insulin degradation by insulin-degrading enzyme in small intestinal epithelium. Pharm Res 12:1171-1175.
42. Lim CJ, Norouziyan F, Shen WC. 2007. Accumulation of transferrin in Caco-2 cells: A possible mechanism of intestinal transferrin absorption. J Control Release 122:393-398.
43. Shah D, Shen WC. 1994. The establishment of polarity and enhanced transcytosis of transferrin receptors in enterocyte-like Caco-2 cells. J Drug Target 2:93-99.
44. Swanson JA, Watts C. 1995. Macropinocytosis. Trends Cell Biol 5:424-428.
45. Conner SD, Schmid SL. 2003. Regulated portals of entry into the cell. Nature 422:37-44.
46. Khalil IA, Kogure K, Akita H, Harashima H. 2006. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol Rev 58:32-45.
47. Falcone S, Cocucci E, Podini P, Kirchhausen T, Clementi E, Meldolesi J. 2006. Macropinocytosis: Regulated coordination of endocytic and exocytic membrane traffic events. J Cell Sci 119:4758-4769.
48. Console S, Marty C, Garcia-Echeverria C, Schwendener R, Ballmer-Hofer K. 2003. Antennapedia and HIV transactivator of transcription (TAT) "protein transduction domains" promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J Biol Chem 278:35109-35114.
49. Su Y, Mani R, Hong M. 2008. Asymmetric insertion of membrane proteins in lipid bilayers by solid-state NMR paramagnetic relaxation enhancement: A cell-penetrating peptide example. J Am Chem Soc 130:8856-8864.