Approaches for enhancing oral bioavailability of peptides and proteins

International Journal of Pharmaceutics

Volumn 447, Issue 1-2, 2013, Pages 75-93

  Renukuntla, Jwala ^a   Vadlapudi, Aswani Dutt ^b   Patel, Ashaben ^b   Boddu, Sai H S ^c   Mitra, Ashim K ^b  

^a South College School of Pharmacy   (United States)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^c UNIVERSITY OF TOLEDO   (United States)

Author keywords

GI tract; Microparticles; Nanoparticles; Oral delivery; Peptides; Proteins

Indexed keywords

ACYLCARNITINE; BILE SALT; CELL PENETRATING PEPTIDE; CHELATING AGENT; CYCLODEXTRIN; ENZYME INHIBITOR; LIPOSOME; NANOPARTICLE; PEPTIDES AND PROTEINS; POLYMER; SURFACTANT;

ACTIVE TRANSPORT; CHEMICAL MODIFICATION; DERIVATIZATION; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; HYDROGEL; MACROMOLECULE; MOLECULAR WEIGHT; MUCOADHESION; PASSIVE TRANSPORT; PRIORITY JOURNAL; REVIEW; TRANSCYTOSIS;

ADMINISTRATION, ORAL; ANIMALS; BIOLOGICAL AVAILABILITY; CHEMISTRY, PHARMACEUTICAL; HUMANS; INTESTINAL ABSORPTION; PEPTIDES; PROTEINS;

EID: 84874945035     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2013.02.030     Document Type: Review

References (212)

1. A.J. Almeida, and E. Souto Solid lipid nanoparticles as a drug delivery system for peptides and proteins Adv. Drug Deliv. Rev. 59 2007 478 490
2. Z. Antosova, M. Mackova, V. Kral, and T. Macek Therapeutic application of peptides and proteins: parenteral forever? Trends Biotechnol. 27 2009 628 635
3. H. Arima, K. Yunomae, T. Morikawa, F. Hirayama, and K. Uekama Contribution of cholesterol and phospholipids to inhibitory effect of dimethyl-beta-cyclodextrin on efflux function of P-glycoprotein and multidrug resistance-associated protein 2 in vinblastine-resistant Caco-2 cell monolayers Pharm. Res. 21 2004 625 634
4. P. Artursson, T. Lindmark, S.S. Davis, and L. Illum Effect of chitosan on the permeability of monolayers of intestinal epithelial cells (Caco-2) Pharm. Res. 11 1994 1358 1361
5. P.F. Augustijns, T.P. Bradshaw, L.S. Gan, R.W. Hendren, and D.R. Thakker Evidence for a polarized efflux system in CACO-2 cells capable of modulating cyclosporin A transport Biochem. Biophys. Res. Commun. 197 1993 360 365
6. B.J. Aungst Absorption enhancers: applications and advances AAPS J. 14 2012 10 18
7. J.P. Bai, and G.L. Amidon Structural specificity of mucosal-cell transport and metabolism of peptide drugs: implication for oral peptide drug delivery Pharm. Res. 9 1992 969 978
8. J.P. Bai, L.L. Chang, and J.H. Guo Effects of polyacrylic polymers on the degradation of insulin and peptide drugs by chymotrypsin and trypsin J. Pharm. Pharmacol. 48 1996 17 21
9. Y. Bai, D.K. Ann, and W.C. Shen Recombinant granulocyte colony-stimulating factor-transferrin fusion protein as an oral myelopoietic agent Proc. Natl. Acad. Sci. U.S.A. 102 2005 7292 7296
10. A. Bernkop-Schnurch The use of inhibitory agents to overcome the enzymatic barrier to perorally administered therapeutic peptides and proteins J. Control. Release 52 1998 1 16
11. A. Bernkop-Schnurch, M.H. Hoffer, and K. Kafedjiiski Thiomers for oral delivery of hydrophilic macromolecular drugs Expert Opin. Drug Deliv. 1 2004 87 98
12. A. Bernkop-Schnurch, and M.E. Krajicek Mucoadhesive polymers as platforms for peroral peptide delivery and absorption: synthesis and evaluation of different chitosan-EDTA conjugates J. Control. Release 50 1998 215 223
13. A. Bernkop-Schnurch, A. Weithaler, K. Albrecht, and A. Greimel Thiomers: preparation and in vitro evaluation of a mucoadhesive nanoparticulate drug delivery system Int. J. Pharm. 317 2006 76 81
14. R.T. Borchardt Optimizing oral absorption of peptides using prodrug strategies J. Control. Release 62 1999 231 238
15. T.R. Borchardt, A. Jeffrey, T.J. Siahaan, S. Gangwar, and G.M. Pauletti Improvement of oral peptide bioavailability: Peptidomimetics and prodrug strategies Adv. Drug Deliv. Rev. 27 1997 235 256
16. M.E. Brewster, and T. Loftsson Cyclodextrins as pharmaceutical solubilizers Adv. Drug Deliv. Rev. 59 2007 645 666
17. N.D. Brown, D.L. Butler, and P.K. Chiang Stabilization of thymopentin and preservation of its pharmacological properties by 2-hydroxypropyl-beta- cyclodextrin J. Pharm. Pharmacol. 45 1993 666 667
18. A. Buda, C. Sands, and M.A. Jepson Use of fluorescence imaging to investigate the structure and function of intestinal M cells Adv. Drug Deliv. Rev. 57 2005 123 134
19. P.F. Builders, O.O. Kunle, L.C. Okpaku, M.I. Builders, A.A. Attama, and M.U. Adikwu Preparation and evaluation of mucinated sodium alginate microparticles for oral delivery of insulin Eur. J. Pharm. Biopharm. 70 2008 777 783
20. P.S. Burton, R.A. Conradi, A.R. Hilgers, and N.F. Ho Evidence for a polarized efflux system for peptides in the apical membrane of Caco-2 cells Biochem. Biophys. Res. Commun. 190 1993 760 766
21. P.S. Burton, R.A. Conradi, N.F. Ho, A.R. Hilgers, and R.T. Borchardt How structural features influence the biomembrane permeability of peptides J. Pharm. Sci. 85 1996 1336 1340
22. S.M. Catnach, P.D. Fairclough, and S.M. Hammond Intestinal absorption of peptide drugs: advances in our understanding and clinical implications Gut 35 1994 441 444
23. R. Challa, A. Ahuja, J. Ali, and R.K. Khar Cyclodextrins in drug delivery: an updated review AAPS Pharm. Sci. Tech. 6 2005 E329 E357
24. H. Checkoway, P. Boffetta, D.J. Mundt, and K.A. Mundt Critical review and synthesis of the epidemiologic evidence on formaldehyde exposure and risk of leukemia and other lymphohematopoietic malignancies Cancer Causes Control. 23 2012 1747 1766
25. Y. Chen, L. Yuan, L. Zhou, Z.H. Zhang, W. Cao, and Q. Wu Effect of cell-penetrating peptide-coated nanostructured lipid carriers on the oral absorption of tripterine Int. J. Nanomed. 7 2012 4581 4591
26. J. Cheng, B.A. Teply, S.Y. Jeong, C.H. Yim, D. Ho, I. Sherifi, S. Jon, O.C. Farokhzad, A. Khademhosseini, and R.S. Langer Magnetically responsive polymeric microparticles for oral delivery of protein drugs Pharm. Res. 23 2006 557 564
27. Y. Chien Oral drug delivery and delivery systems C. Y.W.; Novel Drug Delivery Systems 1992 Marcel Dekker Inc New York 139 196
28. M. Chittchang, A.K. Mitra, and T.P. Johnston Interplay of secondary structure and charge on the diffusion of a polypeptide through negatively charged aqueous pores Pharm. Res. 24 2007 502 511
29. M. Chittchang, N. Salamat-Miller, H.H. Alur, D.G. Vander Velde, A.K. Mitra, and T.P. Johnston Poly(L-lysine) as a model drug macromolecule with which to investigate secondary structure and microporous membrane transport, part 2: diffusion studies J. Pharm. Pharmacol. 54 2002 1497 1505
30. M.K. Chourasia, and S.K. Jain Pharmaceutical approaches to colon targeted drug delivery systems J. Pharm. Pharm. Sci. 6 2003 33 66
31. S. Clement, J.G. Still, G. Kosutic, and R.G. McAllister Oral insulin product hexyl-insulin monoconjugate 2 (HIM2) in type 1 diabetes mellitus: the glucose stabilization effects of HIM2 Diabetes Technol. Ther. 4 2002 459 466
32. R.A. Conradi, A.R. Hilgers, N.F. Ho, and P.S. Burton The influence of peptide structure on transport across Caco-2 cells Pharm. Res. 8 1991 1453 1460
33. E. Danforth Jr.; and R.O. Moore Intestinal absorption of insulin in the rat Endocrinology 65 1959 118 123
34. M.D. Del Curto, A. Maroni, L. Palugan, L. Zema, A. Gazzaniga, and M.E. Sangalli Oral delivery system for two-pulse colonic release of protein drugs and protease inhibitor/absorption enhancer compounds J. Pharm. Sci. 100 2011 3251 3259
35. L.C. DeVane Principles of pharmacokinetics and pharmacodynamics A.F. Schatzberg, C.B. Nemeroff, The American Psychiatric Publishing Textbook of Psychopharmacology third ed. 2004 American Psychiatric Pub Washington, DC 181 200
36. S.K. Dharma, P.H. Fishman, and G.A. Peyman A preliminary study of corneal penetration of 125I-labelled idoxuridine liposome Acta Ophthalmol. (Copenh.) 64 1986 298 301
37. A.N. Dodoo, S. Bansal, D.J. Barlow, F.C. Bennet, R.C. Hider, A.B. Lansley, M.J. Lawrence, and C. Marriott Systematic investigations of the influence of molecular structure on the transport of peptides across cultured alveolar cell monolayers Pharm. Res. 17 2000 7 14
38. A.H. Faraji, and P. Wipf Nanoparticles in cellular drug delivery Bioorg. Med. Chem. 17 2009 2950 2962
39. A. Fasano Modulation of intestinal permeability: an innovative method of oral drug delivery for the treatment of inherited and acquired human diseases Mol. Genet. Metab. 64 1998 12 18
40. G. Fetih, H. Fausia, N. Okada, T. Fujita, M. Attia, and A. Yamamoto Colon-specific delivery and enhanced colonic absorption of [Asu(1,7)]-eel calcitonin using chitosan capsules containing various additives in rats J. Drug Target 14 2006 165 172
41. J.A. Fix Oral controlled release technology for peptides: status and future prospects Pharm. Res. 13 1996 1760 1764
42. P. Fonte, F. Andrade, F. Araujo, C. Andrade, J. Neves, and B. Sarmento Chitosan-coated solid lipid nanoparticles for insulin delivery Methods Enzymol. 508 2012 295 314
43. S. Frokjaer, and D.E. Otzen Protein drug stability: a formulation challenge Nat. Rev. Drug Discov. 4 2005 298 306
44. H.H. Gangurde, S. Tamizharasi, C.M.Au; T. Sivakumar, and C.D. Upasani Approaches for peptides and proteins by colon specific delivery: Review Int. J. Pharm. Frontier Res. 1 2011 110 125
45. M. Garcia-Fuentes, C. Prego, D. Torres, and M.J. Alonso A comparative study of the potential of solid triglyceride nanostructures coated with chitosan or poly(ethylene glycol) as carriers for oral calcitonin delivery Eur. J. Pharm. Sci. 25 2005 133 143
46. A. Gazzaniga, P. Iamartino, G. Maffione, and M.E. Sangalli Oral delayed-release system for colonic specific delivery Int. J. Pharm. 108 1994 77 83
47. M. Gibaldi Biopharmaceutics and Clinical Pharmacokinetics fourth ed. 1991 Lea & Febiger Philadelphia
48. T. Gratieri, G.M. Gelfuso, E.M. Rocha, V.H. Sarmento, O. de Freitas, and R.F. Lopez A poloxamer/chitosan in situ forming gel with prolonged retention time for ocular delivery Eur. J. Pharm. Biopharm. 75 2010 186 193
49. D. Guggi, C.E. Kast, and A. Bernkop-Schnurch In vivo evaluation of an oral salmon calcitonin-delivery system based on a thiolated chitosan carrier matrix Pharm. Res. 20 2003 1989 1994
50. A. Gulbake, and S.K. Jain Chitosan: a potential polymer for colon-specific drug delivery system Expert Opin. Drug Deliv. 9 2012 713 729
51. J.H. Guo, and K.M. Cooklock The effects of backing materials and multilayered systems on the characteristics of bioadhesive buccal patches J. Pharm. Pharmacol. 48 1996 255 257
52. J. Haas, and C.M. Lehr Developments in the area of bioadhesive drug delivery systems Expert Opin. Biol. Ther. 2 2002 287 298
53. B. Haeberlin, T. Gengenbacher, A. Meinzer, and G. Fricker Cyclodextrins - Useful excipients for oral peptide administration? Int. J. Pharm. 137 1996 103 110
54. J.H. Hamman, G.M. Enslin, and A.F. Kotze Oral delivery of peptide drugs: barriers and developments BioDrugs 19 2005 165 177
55. M. Hashizume, T. Douen, M. Murakami, A. Yamamoto, K. Takada, and S. Muranishi Improvement of large intestinal absorption of insulin by chemical modification with palmitic acid in rats J. Pharm. Pharmacol. 44 1992 555 559
56. S. Hauptstein, and A. Bernkop-Schnurch Thiomers and thiomer-based nanoparticles in protein and DNA drug delivery Expert Opin. Drug Deliv. 9 2012 1069 1081
57. M. Hichens A comparison of thyrotropin-releasing hormone with analogs: influence of disposition upon pharmacology Drug Metab. Rev. 14 1983 77 98
58. P.W. Hsieh, C.F. Hung, and J.Y. Fang Current prodrug design for drug discovery Curr. Pharm. Des. 15 2009 2236 2250
59. M.A. Hurni, A.B. Noach, M.C. Blom-Roosemalen, A.G. de Boer, J.F. Nagelkerke, and D.D. Breimer Permeability enhancement in Caco-2 cell monolayers by sodium salicylate and sodium taurodihydrofusidate: assessment of effect-reversibility and imaging of transepithelial transport routes by confocal laser scanning microscopy J. Pharmacol. Exp. Ther. 267 1993 942 950
60. N. Hussain, P.U. Jani, and A.T. Florence Enhanced oral uptake of tomato lectin-conjugated nanoparticles in the rat Pharm. Res. 14 1997 613 618
61. H. Ichikawa, and N.A. Peppas Novel complexation hydrogels for oral peptide delivery: in vitro evaluation of their cytocompatibility and insulin-transport enhancing effects using Caco-2 cell monolayers J. Biomed. Mater. Res. A 67 2003 609 617
62. J. Iqbal, G. Shahnaz, S. Dunnhaupt, C. Muller, F. Hintzen, and A. Bernkop-Schnurch Preactivated thiomers as mucoadhesive polymers for drug delivery Biomaterials 33 2012 1528 1535
63. T. Irie, and K. Uekama Cyclodextrins in peptide and protein delivery Adv. Drug Deliv. Rev. 36 1999 101 123
64. U. Jaehde, R. Masereeuw, A.G. De Boer, G. Fricker, J.F. Nagelkerke, J. Vonderscher, and D.D. Breimer Quantification and visualization of the transport of octreotide, a somatostatin analogue, across monolayers of cerebrovascular endothelial cells Pharm. Res. 11 1994 442 448
65. S. Jain, V.V. Rathi, A.K. Jain, M. Das, and C. Godugu Folate-decorated PLGA nanoparticles as a rationally designed vehicle for the oral delivery of insulin Nanomedicine (Lond.) 7 2012 1311 1337
66. S. Jana, S. Mandlekar, and P. Marathe Prodrug design to improve pharmacokinetic and drug delivery properties: challenges to the discovery scientists Curr. Med. Chem. 17 2010 3874 3908
67. N. Jerry, Y. Anitha, C.P. Sharma, and P. Sony In vivo absorption studies of insulin from an oral delivery system Drug Deliv. 8 2001 19 23
68. Y. Jin, Y. Song, X. Zhu, D. Zhou, C. Chen, Z. Zhang, and Y. Huang Goblet cell-targeting nanoparticles for oral insulin delivery and the influence of mucus on insulin transport Biomaterials 33 2012 1573 1582
69. Jitendra, P.K. Sharma, S. Bansal, and A. Banik Noninvasive routes of proteins and peptides drug delivery Indian J. Pharm. Sci. 73 2011 367 375
70. L.R. Johnson Physiology of the Gastrointestinal Tract third ed. 1994 Raven Press New York
71. D.H. Jones, C.D. Partidos, M.W. Steward, and G.H. Farrar Oral delivery of poly(lactide-co-glycolide) encapsulated vaccines Behring Inst. Mitt. 1997 220 228
72. N. Kamei, M. Morishita, H. Chiba, N.J. Kavimandan, N.A. Peppas, and K. Takayama Complexation hydrogels for intestinal delivery of interferon beta and calcitonin J. Control. Release 134 2009 98 102
73. N. Kamei, M. Morishita, Y. Eda, N. Ida, R. Nishio, and K. Takayama Usefulness of cell-penetrating peptides to improve intestinal insulin absorption J. Control. Release 132 2008 21 25
74. N. Kamei, M. Morishita, and K. Takayama Importance of intermolecular interaction on the improvement of intestinal therapeutic peptide/protein absorption using cell-penetrating peptides J. Control. Release 136 2009 179 186
75. J.R. Kanwar, B.M. Long, and R.K. Kanwar The use of cyclodextrins nanoparticles for oral delivery Curr. Med. Chem. 18 2011 2079 2085
76. S. Katragadda, B. Budda, B.S. Anand, and A.K. Mitra Role of efflux pumps and metabolising enzymes in drug delivery Expert Opin. Drug Deliv. 2 2005 683 705
77. I.P. Kaur, A. Garg, A.K. Singla, and D. Aggarwal Vesicular systems in ocular drug delivery: an overview Int. J. Pharm. 269 2004 1 14
78. S. Khafagy el, and M. Morishita Oral biodrug delivery using cell-penetrating peptide Adv. Drug Deliv. Rev. 64 2012 531 539
79. S. Khafagy el, M. Morishita, K. Isowa, J. Imai, and K. Takayama Effect of cell-penetrating peptides on the nasal absorption of insulin J. Control. Release 133 2009 103 108
80. S. Khafagy el, M. Morishita, N. Kamei, Y. Eda, Y. Ikeno, and K. Takayama Efficiency of cell-penetrating peptides on the nasal and intestinal absorption of therapeutic peptides and proteins Int. J. Pharm. 381 2009 49 55
81. M. Kidron, H. Bar-On, E.M. Berry, and E. Ziv The absorption of insulin from various regions of the rat intestine Life Sci. 31 1982 2837 2841
82. B.Y. Kim, J.H. Jeong, K. Park, and J.D. Kim Bioadhesive interaction and hypoglycemic effect of insulin-loaded lectin-microparticle conjugates in oral insulin delivery system J. Control. Release 102 2005 525 538
83. M. Kipnes, P. Dandona, D. Tripathy, J.G. Still, and G. Kosutic Control of postprandial plasma glucose by an oral insulin product (HIM2) in patients with type 2 diabetes Diabetes Care 26 2003 421 426
84. M.A. Kisel, L.N. Kulik, I.S. Tsybovsky, A.P. Vlasov, M.S. Vorob'yov, E.A. Kholodova, and Z.V. Zabarovskaya Liposomes with phosphatidylethanol as a carrier for oral delivery of insulin: studies in the rat Int. J. Pharm. 216 2001 105 114
85. U.B. Kompella, and V.H. Lee Delivery systems for penetration enhancement of peptide and protein drugs: design considerations Adv. Drug Deliv. Rev. 46 2001 211 245
86. E. Koren, and V.P. Torchilin Cell-penetrating peptides: breaking through to the other side Trends Mol. Med. 18 2012 385 393
87. W. Kramer, G. Wess, A. Enhsen, E. Falk, A. Hoffmann, G. Neckermann, G. Schubert, and M. Urmann Modified bile acids as carriers for peptides and drugs J. Control. Release 46 1997 17 30
88. J. Kreuter Nanoparticles J. Kreuter, Colloidal Drug Delivery Systems 1994 M. Dekker New York 219 342
89. P. Kumar, and B. Mishra Colon targeted drug delivery systems - an overview Curr. Drug Deliv. 5 2008 186 198
90. D. Kurz, and T.A. Ciulla Novel approaches for retinal drug delivery Ophthalmol. Clin. North Am. 15 2002 405 410
91. K.C. Kwan Oral bioavailability and first-pass effects Drug Metab. Dispos. 25 1997 1329 1336
92. M.E. Lane, and O.I. Corrigan Paracellular and transcellular pathways facilitate insulin permeability in rat gut J. Pharm. Pharmacol. 58 2006 271 275
93. M. Laskowski Jr.; H.A. Haessler, R.P. Miech, R.J. Peanasky, and M. Laskowski Effect of trypsin inhibitor on passage of insulin across the intestinal barrier Science 127 1958 1115 1116
94. E.L. Lecluyse, S.C. Sutton, and J.A. Fix In vitro effects of long-chain acylcarnitines on the permeability, transepithelial electrical resistance and morphology of rat colonic mucosa J. Pharmacol. Exp. Ther. 265 1993 955 962
95. H. Lee, and T.G. Park Preparation and characterization of mono-PEGylated epidermal growth factor: evaluation of in vitro biologic activity Pharm. Res. 19 2002 845 851
96. H.J. Lee, and G.L. Amidon The effect of enzyme inhibitor and absorption site following [D-ala2, D-leu5]enkephalin oral administration in rats Biopharm. Drug Dispos. 23 2002 131 141
97. Y.H. Lee, and P.J. Sinko Oral delivery of salmon calcitonin Adv. Drug Deliv. Rev. 42 2000 225 238
98. A.L. Lehninger, D.L. Nelson, and M.M. Cox Lehninger Principles of Biochemistry fourth ed. 2005 W.H. Freeman New York
99. C.M. Lehr From sticky stuff to sweet receptors - achievements, limits and novel approaches to bioadhesion Eur. J. Drug Metab. Pharmacokinet. 21 1996 139 148
100. A. Leone-Bay, M. Sato, D. Paton, A.H. Hunt, D. Sarubbi, M. Carozza, J. Chou, J. McDonough, and R.A. Baughman Oral delivery of biologically active parathyroid hormone Pharm. Res. 18 2001 964 970
101. Z. Li, J. Chen, W. Sun, and Y. Xu Investigation of archaeosomes as carriers for oral delivery of peptides Biochem. Biophys. Res. Commun. 394 2010 412 417
102. J.F. Liang, and V.C. Yang Insulin-cell penetrating peptide hybrids with improved intestinal absorption efficiency Biochem. Biophys. Res. Commun. 335 2005 734 738
103. C.J. Lim, and W.C. Shen Comparison of monomeric and oligomeric transferrin as potential carrier in oral delivery of protein drugs J. Control. Release 106 2005 273 286
104. D.Z. Liu, E.L. LeCluyse, and D.R. Thakker Dodecylphosphocholine-mediated enhancement of paracellular permeability and cytotoxicity in Caco-2 cell monolayers J. Pharm. Sci. 88 1999 1161 1168
105. D.W. Loe, and F.J. Sharom Interaction of multidrug-resistant Chinese hamster ovary cells with the peptide ionophore gramicidin D Biochim. Biophys. Acta 1190 1994 72 84
106. T. Loftsson, and M.E. Brewster Pharmaceutical applications of cyclodextrins. 1. Drug solubilization and stabilization J. Pharm. Sci. 85 1996 1017 1025
107. M.A. Longer, H.S. Ch'ng, and J.R. Robinson Bioadhesive polymers as platforms for oral controlled drug delivery III: oral delivery of chlorothiazide using a bioadhesive polymer J. Pharm. Sci. 74 1985 406 411
108. A.M. Lowman, M. Morishita, M. Kajita, T. Nagai, and N.A. Peppas Oral delivery of insulin using pH-responsive complexation gels J. Pharm. Sci. 88 1999 933 937
109. K. Maculotti, E.M. Tira, M. Sonaggere, P. Perugini, B. Conti, T. Modena, and F. Pavanetto In vitro evaluation of chondroitin sulphate-chitosan microspheres as carrier for the delivery of proteins J. Microencapsul. 26 2009 535 543
110. R.I. Mahato, A.S. Narang, L. Thoma, and D.D. Miller Emerging trends in oral delivery of peptide and protein drugs Crit. Rev. Ther. Drug Carrier Syst. 20 2003 153 214
111. D.K. Malik, S. Baboota, A. Ahuja, S. Hasan, and J. Ali Recent advances in protein and peptide drug delivery systems Curr. Drug Deliv. 4 2007 141 151
112. A. Maroni, L. Zema, M.D. Del Curto, A. Foppoli, and A. Gazzaniga Oral colon delivery of insulin with the aid of functional adjuvants Adv. Drug Deliv. Rev. 64 2012 540 556
113. M. Marx Watching peptide drugs grow up Chem. Eng. News 83 2005 17 24
114. G. Millotti, G. Perera, C. Vigl, K. Pickl, F.M. Sinner, and A. Bernkop-Schnurch The use of chitosan-6-mercaptonicotinic acid nanoparticles for oral peptide drug delivery Drug Deliv. 18 2011 190 197
115. T. Mizuma, A. Koyanagi, and S. Awazu Intestinal transport and metabolism of glucose-conjugated kyotorphin and cyclic kyotorphin: metabolic degradation is crucial to intestinal absorption of peptide drugs Biochim. Biophys. Acta 1475 2000 90 98
116. J. Guo, C. Byrne, R. Darcy, and O.D. C.M. Mechanistic studies on the uptake and intracellular trafficking of novel cyclodextrin transfection complexes by intestinal epithelial cells Int. J. Pharm. 413 2011 174 183
117. V.J. Mohanraj, T.J. Barnes, and C.A. Prestidge Silica nanoparticle coated liposomes: a new type of hybrid nanocapsule for proteins Int. J. Pharm. 392 2010 285 293
118. M. Morishita, N. Kamei, J. Ehara, K. Isowa, and K. Takayama A novel approach using functional peptides for efficient intestinal absorption of insulin J. Control. Release 118 2007 177 184
119. M. Morishita, A.M. Lowman, K. Takayama, T. Nagai, and N.A. Peppas Elucidation of the mechanism of incorporation of insulin in controlled release systems based on complexation polymers J. Control. Release 81 2002 25 32
120. Y. Nakada, N. Awata, C. Nakamichi, and I. Sugimoto The effect of additives on the oral mucosal absorption of human calcitonin in rats J. Pharmacobiodyn. 11 1988 395 401
121. B.K. Nanjawade, F.V. Manvi, and A.S. Manjappa In situ-forming hydrogels for sustained ophthalmic drug delivery J. Control. Release 122 2007 119 134
122. C. Navarro, I. Gonzalez-Alvarez, M. Gonzalez-Alvarez, M. Manku, V. Merino, V.G. Casabo, and M. Bermejo Influence of polyunsaturated fatty acids on Cortisol transport through MDCK and MDCK-MDR1 cells as blood-brain barrier in vitro model Eur. J. Pharm. Sci. 42 2011 290 299
123. H. Newey, and D.H. Smyth The intestinal absorption of some dipeptides J. Physiol. 145 1959 48 56
124. D.T. O'Hagan, J.P. McGee, J. Holmgren, A.M. Mowat, A.M. Donachie, K.H. Mills, W. Gaisford, D. Rahman, and S.J. Challacombe Biodegradable microparticles for oral immunization Vaccine 11 1993 149 154
125. D.T. O'Hagan, D. Rahman, J.P. McGee, H. Jeffery, M.C. Davies, P. Williams, S.S. Davis, and S.J. Challacombe Biodegradable microparticles as controlled release antigen delivery systems Immunology 73 1991 239 242
126. D.H. Oh, K.H. Chun, S.O. Jeon, J.W. Kang, and S. Lee Enhanced transbuccal salmon calcitonin (sCT) delivery: effect of chemical enhancers and electrical assistance on in vitro sCT buccal permeation Eur. J. Pharm. Biopharm. 79 2011 357 363
127. J. Panyam, and V. Labhasetwar Biodegradable nanoparticles for drug and gene delivery to cells and tissue Adv. Drug Deliv. Rev. 55 2003 329 347
128. J.R. Pappenheimer, and K.Z. Reiss Contribution of solvent drag through intercellular junctions to absorption of nutrients by the small intestine of the rat J. Membr. Biol. 100 1987 123 136
129. K. Park, I.C. Kwon, and K. Park Oral protein delivery: Current status and future prospect React. Funct. Polym. 71 2011 280 287
130. G.B. Patel, B.J. Agnew, L. Deschatelets, L.P. Fleming, and G.D. Sprott In vitro assessment of archaeosome stability for developing oral delivery systems Int. J. Pharm. 194 2000 39 49
131. M. Patel, T. Shah, and A. Amin Therapeutic opportunities in colon-specific drug-delivery systems Crit. Rev. Ther. Drug Carrier Syst. 24 2007 147 202
132. M.M. Patel Cutting-edge technologies in colon-targeted drug delivery systems Expert Opin. Drug Deliv. 8 2011 1247 1258
133. G.M. Pauletti, F.W. Okumu, and R.T. Borchardt Effect of size and charge on the passive diffusion of peptides across Caco-2 cell monolayers via the paracellular pathway Pharm. Res. 14 1997 164 168
134. K.K. Peh, and C.F. Wong Polymeric films as vehicle for buccal delivery: swelling, mechanical, and bioadhesive properties J. Pharm. Pharm. Sci. 2 1999 53 61
135. N.A. Peppas, P. Bures, W. Leobandung, and H. Ichikawa Hydrogels in pharmaceutical formulations Eur. J. Pharm. Biopharm. 50 2000 27 46
136. G. Perera, M. Greindl, T.F. Palmberger, and A. Bernkop-Schnurch Insulin-loaded poly(acrylic acid)-cysteine nanoparticles: stability studies towards digestive enzymes of the intestine Drug Deliv. 16 2009 254 260
137. J.P. Rado, J. Marosi, L. Szende, L. Borbely, J. Tako, and J. Fischer The antidiuretic action of 1-deamino-8-D-arginine vasopressin (DDAVP) in man Int. J. Clin. Pharmacol. Biopharm. 13 1976 199 209
138. F. Rafii, W. Franklin, and C.E. Cerniglia Azoreductase activity of anaerobic bacteria isolated from human intestinal microflora Appl. Environ. Microbiol. 56 1990 2146 2151
139. J. Rautio, H. Kumpulainen, T. Heimbach, R. Oliyai, D. Oh, T. Jarvinen, and J. Savolainen Prodrugs: design and clinical applications Nat. Rev. Drug Discov. 7 2008 255 270
140. G. Repassy, and K. Lapis Ultrastructural characteristics, secretory and phagocytotic activity of Paneth cells Acta Morphol. Acad. Sci. Hung. 27 1979 21 24
141. C.D. Ridgley Jr.; and J.R. Wilkins 3rd. A comparison of median hearing thresholds from U.S. Navy and U.S. Army audiometric data bases Mil. Med. 156 1991 343 345
142. M. Roldo, E. Barbu, J.F. Brown, D.W. Laight, J.D. Smart, and J. Tsibouklis Azo compounds in colon-specific drug delivery Expert Opin. Drug Deliv. 4 2007 547 560
143. I. Rubinstein Oral insulin: deja vu? Nanomedicine (Lond.) 7 2012 631 632
144. G.J. Russell-Jones The potential use of receptor-mediated endocytosis for oral drug delivery Adv. Drug Deliv. Rev. 46 2001 59 73
145. G.J. Russell-Jones Use of targeting agents to increase uptake and localization of drugs to the intestinal epithelium J. Drug Target 12 2004 113 123
146. M. Saffran, G.S. Kumar, C. Savariar, J.C. Burnham, F. Williams, and D.C. Neckers A new approach to the oral administration of insulin and other peptide drugs Science 233 1986 1081 1084
147. N. Salamat-Miller, and T.P. Johnston Current strategies used to enhance the paracellular transport of therapeutic polypeptides across the intestinal epithelium Int. J. Pharm. 294 2005 201 216
148. B. Sarmento, S. Martins, D. Ferreira, and E.B. Souto Oral insulin delivery by means of solid lipid nanoparticles Int. J. Nanomed. 2 2007 743 749
149. R.J. Schilling, and A.K. Mitra Intestinal mucosal transport of insulin Int. J. Pharm. 62 1990 53 64
150. N.G. Schipper, K.M. Varum, and P. Artursson Chitosans as absorption enhancers for poorly absorbable drugs. 1 Influence of molecular weight and degree of acetylation on drug transport across human intestinal epithelial (Caco-2) cells Pharm. Res. 13 1996 1686 1692
151. N.G. Schipper, K.M. Varum, P. Stenberg, G. Ocklind, H. Lennernas, and P. Artursson Chitosans as absorption enhancers of poorly absorbable drugs. 3 Influence of mucus on absorption enhancement Eur. J. Pharm. Sci. 8 1999 335 343
152. S.R. Schwarze, A. Ho, A. Vocero-Akbani, and S.F. Dowdy In vivo protein transduction: delivery of a biologically active protein into the mouse Science 285 1999 1569 1572
153. S. Senel, and A.A. Hincal Drug permeation enhancement via buccal route: possibilities and limitations J. Control. Release 72 2001 133 144
154. N. Shah, T. Shah, and A. Amin Polysaccharides: a targeting strategy for colonic drug delivery Expert Opin. Drug Deliv. 8 2011 779 796
155. R. Shaikh, T.R. Raj Singh, M.J. Garland, A.D. Woolfson, and R.F. Donnelly Mucoadhesive drug delivery systems J. Pharm. Bioallied Sci. 3 2011 89 100
156. J. Shaji, and V. Patole Protein and Peptide drug delivery: oral approaches Indian J. Pharm. Sci. 70 2008 269 277
157. M. Shakweh, G. Ponchel, and E. Fattal Particle uptake by Peyer's patches: a pathway for drug and vaccine delivery Expert Opin. Drug Deliv. 1 2004 141 163
158. Z. Shao, Y. Li, T. Chermak, and A.K. Mitra Cyclodextrins as mucosal absorption promoters of insulin. II. Effects of beta-cyclodextrin derivatives on alpha-chymotryptic degradation and enteral absorption of insulin in rats Pharm. Res. 11 1994 1174 1179
159. F.J. Sharom, X. Yu, G. DiDiodato, and J.W. Chu Synthetic hydrophobic peptides are substrates for P-glycoprotein and stimulate drug transport Biochem. J. 320 1996 421 428
160. Sheppard, R.C.; 1981. Amino Acids, Peptides, and Proteins. Royal Society of Chemistry.
161. R.A. Siegel, and R. Langer Controlled release of polypeptides and other macromolecules Pharm. Res. 1 1984 2 10
162. R. Singh, and J.W. Lillard Jr. Nanoparticle-based targeted drug delivery Exp. Mol. Pathol. 86 2009 215 223
163. V. Sinha, A. Singh, R.V. Kumar, S. Singh, R. Kumria, and J. Bhinge Oral colon-specific drug delivery of protein and peptide drugs Crit. Rev. Ther. Drug Carrier Syst. 24 2007 63 92
164. V.R. Sinha, and R. Kumria Microbially triggered drug delivery to the colon Eur. J. Pharm. Sci. 18 2003 3 18
165. P. Sithigorngul, P. Burton, T. Nishihata, and L. Caldwell Effects of sodium salicylate on epithelial cells of the rectal mucosa of the rat: a light and electron microscopic study Life Sci. 33 1983 1025 1032
166. A. Sood, and R. Panchagnula Peroral route: an opportunity for protein and peptide drug delivery Chem. Rev. 101 2001 3275 3303
167. G.D. Sprott Structures of archaebacterial membrane lipids J. Bioenerg. Biomembr. 24 1992 555 566
168. G.D. Sprott, S. Sad, L.P. Fleming, C.J. Dicaire, G.B. Patel, and L. Krishnan Archaeosomes varying in lipid composition differ in receptor-mediated endocytosis and differentially adjuvant immune responses to entrapped antigen Archaea 1 2003 151 164
169. Stella, V.J.; 2007. Prodrug approaches to enhancing the oral delivery of poorly permeable drugs, in: Stella, V.J.; Borchardt, R.T.; Hageman, M.J.; Maag, H.; Oliyai, R.; Tilley, J.W.; SpringerLink (Online service) (Eds.), Prodrugs Challenges and Rewards Part 1. American Association of Pharmaceutical Scientists, New York, NY, pp. 37-82.
170. F.Y. Su, K.J. Lin, K. Sonaje, S.P. Wey, T.C. Yen, Y.C. Ho, N. Panda, E.Y. Chuang, B. Maiti, and H.W. Sung Protease inhibition and absorption enhancement by functional nanoparticles for effective oral insulin delivery Biomaterials 33 2012 2801 2811
171. E.S. Swenson, W.B. Milisen, and W. Curatolo Intestinal permeability enhancement: structure-activity and structure-toxicity relationships for nonylphenoxypolyoxyethylene surfactant permeability enhancers Pharm. Res. 11 1994 1501 1504
172. H. Takahashi, R.B. Kim, P.R. Perry, and G.R. Wilkinson Characterization of the hepatic canalicular membrane transport of a model oligopeptide: ditekiren J. Pharmacol. Exp. Ther. 281 1997 297 303
173. T. Tenma, E. Yodoya, S. Tashima, T. Fujita, M. Murakami, A. Yamamoto, and S. Muranishi Development of new lipophilic derivatives of tetragastrin: physicochemical characteristics and intestinal absorption of acyl-tetragastrin derivatives in rats Pharm. Res. 10 1993 1488 1492
174. M. Thanou, J.C. Verhoef, and H.E. Junginger Oral drug absorption enhancement by chitosan and its derivatives Adv. Drug Deliv. Rev. 52 2001 117 126
175. N. Thirawong, J. Thongborisute, H. Takeuchi, and P. Sriamornsak Improved intestinal absorption of calcitonin by mucoadhesive delivery of novel pectin-liposome nanocomplexes J. Control. Release 125 2008 236 245
176. D.T. Thwaites, B.H. Hirst, and N.L. Simmons Passive transepithelial absorption of thyrotropin-releasing hormone (TRH) via a paracellular route in cultured intestinal and renal epithelial cell lines Pharm. Res. 10 1993 674 681
177. M. Tomita, M. Shiga, M. Hayashi, and S. Awazu Enhancement of colonic drug absorption by the paracellular permeation route Pharm. Res. 5 1988 341 346
178. M. Torres-Lugo, M. Garcia, R. Record, and N.A. Peppas pH-Sensitive hydrogels as gastrointestinal tract absorption enhancers: transport mechanisms of salmon calcitonin and other model molecules using the Caco-2 cell model Biotechnol. Prog. 18 2002 612 616
179. G.J. Tortora, and S.R. Grabowski Principles of Anatomy and Physiology eighth ed. 1996 HarperCollins College New York, NY
180. E. Touitou, and A. Rubinstein Targeted enteral delivery of insulin to rats Int. J. Pharm. 30 1986 95 99
181. H. Tozaki, J. Komoike, C. Tada, T. Maruyama, A. Terabe, T. Suzuki, A. Yamamoto, and S. Muranishi Chitosan capsules for colon-specific drug delivery: improvement of insulin absorption from the rat colon J. Pharm. Sci. 86 1997 1016 1021
182. H. Tozaki, J. Nishioka, J. Komoike, N. Okada, T. Fujita, S. Muranishi, S.I. Kim, H. Terashima, and A. Yamamoto Enhanced absorption of insulin and (Asu(1,7))eel-calcitonin using novel azopolymer-coated pellets for colon-specific drug delivery J. Pharm. Sci. 90 2001 89 97
183. A. Trapani, V. Laquintana, N. Denora, A. Lopedota, A. Cutrignelli, M. Franco, G. Trapani, and G. Liso Eudragit RS 100 microparticles containing
184. R. Trehin, and H.P. Merkle Chances and pitfalls of cell penetrating peptides for cellular drug delivery Eur. J. Pharm. Biopharm. 58 2004 209 223
185. A. Tsuji, and I. Tamai Carrier-mediated intestinal transport of drugs Pharm. Res. 13 1996 963 977
186. A.D. Tuesca, C. Reiff, J.I. Joseph, and A.M. Lowman Synthesis, characterization and in vivo efficacy of PEGylated insulin for oral delivery with complexation hydrogels Pharm. Res. 26 2009 727 739
187. K. Ueda, A.M. Shimabuku, H. Konishi, Y. Fujii, S. Takebe, K. Nishi, M. Yoshida, T. Beppu, and T. Komano Functional expression of human P-glycoprotein in Schizosaccharomyces pombe FEBS Lett. 330 1993 279 282
188. A.D. Vadlapudi, R.K. Vadlapatla, D. Kwatra, R. Earla, S.K. Samanta, D. Pal, and A.K. Mitra Targeted lipid based drug conjugates: A novel strategy for drug delivery Int. J. Pharm. 434 2012 315 324
189. A.D. Vadlapudi, R.K. Vadlapatla, and A.K. Mitra Sodium dependent multivitamin transporter (SMVT): a potential target for drug delivery Curr. Drug Targets 13 2012 994 1003
190. K.M. Van de Graaff Anatomy and physiology of the gastrointestinal tract Pediatr. Infect. Dis. 5 1986 S11 S16
191. M.V. Varma, Y. Ashokraj, C.S. Dey, and R. Panchagnula P-glycoprotein inhibitors and their screening: a perspective from bioavailability enhancement Pharmacol. Res. 48 2003 347 359
192. I. Vavra, A. Machova, and I. Krejci Antidiuretic action of 1-deamino-(8-D-arginine)-vasopressin in unanesthetized rats J. Pharmacol. Exp. Ther. 188 1974 241 247
193. H. Vilhardt, and S. Lundin In vitro intestinal transport of vasopressin and its analogues Acta Physiol. Scand. 126 1986 601 607
194. K.V. Vinay Kumar, T. Sivakumar, and T. T. Mu Colon targeting drug delivery system: A review on recent approaches Int. J. Pharm. Biomed. Sci. 2 2011 11 19
195. E. Vives Present and future of cell-penetrating peptide mediated delivery systems: is the Trojan horse too wild to go only to Troy? J. Control. Release 109 2005 77 85
196. E. Walter, T. Kissel, and P. Raddatz Transport of peptidomimetic renin inhibitors across monolayers of a human intestinal cell line (Caco-2): evidence for self-enhancement of paracellular transport route Pharm. Res. 12 1995 1801 1805
197. J. Wang, D. Chow, H. Heiati, and W.C. Shen Reversible lipidization for the oral delivery of salmon calcitonin J. Control. Release 88 2003 369 380
198. J. Wang, D.J. Hogenkamp, M. Tran, W.Y. Li, R.F. Yoshimura, T.B. Johnstone, W.C. Shen, and K.W. Gee Reversible lipidization for the oral delivery of leu-enkephalin J. Drug Target 14 2006 127 136
199. X. Wang, J. Iqbal, D. Rahmat, and A. Bernkop-Schnurch Preactivated thiomers: permeation enhancing properties Int. J. Pharm. 438 2012 217 224
200. S. Watanabe, T. Takeuchi, and W.Y. Chey Mediation of trypsin inhibitor-induced pancreatic hypersecretion by secretin and cholecystokinin in rats Gastroenterology 102 1992 621 628
201. M. Werle, A. Makhlof, and H. Takeuchi Oral protein delivery: a patent review of academic and industrial approaches Recent Pat. Drug Deliv. Formul. 3 2009 94 104
202. A.C. Williams, and B.W. Barry Penetration enhancers Adv. Drug Deliv. Rev. 56 2004 603 618
203. S. Wroblewski, M. Berenson, P. Kopeckova, and J. Kopecek Biorecognition of HPMA copolymer-lectin conjugates as an indicator of differentiation of cell-surface glycoproteins in development, maturation, and diseases of human and rodent gastrointestinal tissues J. Biomed. Mater. Res. 51 2000 329 342
204. A. Yamamoto, E. Hayakawa, Y. Kato, A. Nishiura, and V.H. Lee A mechanistic study on enhancement of rectal permeability to insulin in the albino rabbit J. Pharmacol. Exp. Ther. 263 1992 25 31
205. A. Yamamoto, T. Taniguchi, K. Rikyuu, T. Tsuji, T. Fujita, M. Murakami, and S. Muranishi Effects of various protease inhibitors on the intestinal absorption and degradation of insulin in rats Pharm. Res. 11 1994 1496 1500
206. Yang, H.P.A., Nguyen, Vu Anh, Dong, Liang C., Wong, Patrick S. L., 1999. Peptide Formulation, in: States, U. (Ed.). Alza Corporation (Palo Alto, CA).
207. L. Yin, J. Ding, C. He, L. Cui, C. Tang, and C. Yin Drug permeability and mucoadhesion properties of thiolated trimethyl chitosan nanoparticles in oral insulin delivery Biomaterials 30 2009 5691 5700
208. H. Yuan, S.P. Jiang, Y.Z. Du, J. Miao, X.G. Zhang, and F.Q. Hu Strategic approaches for improving entrapment of hydrophilic peptide drugs by lipid nanoparticles Colloids Surf. B Biointerf. 70 2009 248 253
209. Yun, Y.; Cho, Y.W.; Park, K.; 2012. Nanoparticles for oral delivery: Targeted nanoparticles with peptidic ligands for oral protein delivery. Adv. Drug Deliv. Rev.
210. H. Zhang, I.A. Alsarra, and S.H. Neau An in vitro evaluation of a chitosan-containing multiparticulate system for macromolecule delivery to the colon Int. J. Pharm. 239 2002 197 205
211. L. Zhang, and G. Bulaj Converting peptides into drug leads by lipidation Curr. Med. Chem. 19 2012 1602 1618
212. M. Zorko, and U. Langel Cell-penetrating peptides: mechanism and kinetics of cargo delivery Adv. Drug Deliv. Rev. 57 2005 529 545