Epithelial permeation and absorption mechanisms of biopharmaceuticals

Mucosal Delivery of Biopharmaceuticals: Biology, Challenges and Strategies

Volumn 9781461495246, Issue , 2014, Pages 99-122

  Nielsen, Hanne Morck ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Analysis; Complexes; Lipid based drug delivery systems; Paracellular transport; Particles; Pathway inhibitors; Permeability enhancers; Polymer based drug delivery systems; Tight junction modulators; Transcellular transport; Transcytosis

Indexed keywords

EID: 84930024302     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-9524-6_4     Document Type: Chapter

References (93)

1. Mullard A. 2012 FDA drug approvals. Nat Rev Drug Discov. 2013;12(2):87-90.
2. WangW. Oral protein drug delivery. J Drug Target. 1996;4(4):195-232.
3. Cone RA. Barrier properties of mucus. Adv Drug Deliv Rev. 2009;61(2):75-85.
4. Allen A, Hutton DA, Pearson JP, Sellers LA. Mucus glycoprotein structure, gel formation and gastrointestinal mucus function. Ciba Found Symp. 1984;109:137-56.
5. Kent M. Advanced Biology. Oxford: Oxford University Press; 2000.
6. Miller H, Zhang J, Kuolee R, Patel GB, ChenW. IntestinalMcells: the fallible sentinels?World J Gastroenterol. 2007;13(10):1477-86.
7. Yun Y, ChoYW, Park K. Nanoparticles for oral delivery: targeted nanoparticles with peptidic ligands for oral protein delivery. Adv Drug Deliv Rev. 2012;65(6):822-32.
8. Scheuch G, Kohlhaeufl MJ, Brand P, Siekmeier R. Clinical perspectives on pulmonary systemic and macromolecular delivery. Adv Drug Deliv Rev. 2006;58(9-10):996-1008.
9. Harris D, Robinson JR. Drug delivery via the mucous membranes of the oral cavity. J Pharm Sci. 1992;81(1):1-10.
10. Patton DL, Thwin SS, Meier A, Hooton TM, Stapleton AE, Eschenbach DA. Epithelial cell layer thickness and immune cell populations in the normal human vagina at different stages of the menstrual cycle. Am J Obstet Gynecol. 2000;183(4):967-73.
11. Sugano K, Kansy M, Artursson P, Avdeef A, Bendels S, Di L, Ecker GF, Faller B, Fischer H, Gerebtzoff G, Lennernaes H, Senner F. Coexistence of passive and carrier-mediated processes in drug transport. Nat Rev Drug Discov. 2010;9(8):597-614.
12. Pappenheimer JR. Physiological regulation of transepithelial impedance in the intestinal mucosa of rats and hamsters. J Membr Biol. 1987;100(2):137-48.
13. Rodgers LS, Fanning AS. Regulation of epithelial permeability by the actin cytoskeleton. Cytoskeleton (Hoboken). 2011;68(12):653-60.
14. Rubas W, Cromwell ME, Shahrokh Z, Villagran J, Nguyen TN, Wellton M, Nguyen TH, Mrsny RJ. Flux measurements across Caco-2 monolayers may predict transport in human large intestinal tissue. J Pharm Sci. 1996;85(2):165-9.
15. Rojanasakul Y, Wang LY, Bhat M, Glover DD, Malanga CJ, Ma JK the transport barrier of epithelia: a comparative study on membrane permeability and charge selectivity in the rabbit. Pharm Res. 1992;9(8):1029-34.
16. Powell DW. Barrier function of epithelia. Am J Physiol. 1981;241(4):G275-88.
17. Paulett iGM, Gangwar S, Knipp GT, Nerurkar MM, Okumu FW, Tamura K, Siahaan TJ, Borchardt RT. Structural requirements for intestinal absorption of peptide drugs. J Control Release. 1996;41(1-2):3-17.
18. Tang VW. Proteomic and bioinformatic analysis of epithelial tight junction reveals an unexpected cluster of synaptic molecules. Biol Direct. 2006;1:37.
19. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR. Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol. 2011;73:283-309.
20. Weber CR. Dynamic properties of the tight junction barrier. Ann N Y Acad Sci. 2012;1257: 77-84.
21. Lemmer HJ, Hamman JH. Paracellular drug absorption enhancement through tight junction modulation. Expert Opin Drug Deliv. 2013;10(1):103-14.
22. Matsuhisa K, Kondoh M, Takahashi A, Yagi K. Tight junction modulator and drug delivery. Expert Opin Drug Deliv. 2009;6(5):509-15.
23. Deli MA. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim Biophys Acta. 2009;1788(4):892-910.
24. Maher S, Brayden DJ, Feighery L, McClean S. Cracking the junction: update on the progress of gastrointestinal absorption enhancement in the delivery of poorly absorbed drugs. Crit Rev Ther Drug Carrier Syst. 2008;25(2):117-68.
25. Ivanov AI, Nusrat A, Parkos CA. Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. Bioessays. 2005;27(4):356-65.
26. Burton PS, Conradi RA, Hilgers AR. Mechanisms of peptide and protein absorption: (2) Transcellular mechanism of peptide and protein absorption: passive aspects. Adv Drug Deliv Rev. 1991;7(3):365-85.
27. Mahato RI, Narang AS, Thoma L, Miller DD. Emerging trends in oral delivery of peptide and protein drugs. Crit Rev Ther Drug Carrier Syst. 2003;20(2-3):153-214.
28. Nielsen CU, Steffansen B, Brodin B. Absorptive transporters. In: Steffansen B, Brodin B, Nielsen CU, editors. Molecular Biopharmaceutics. London: Pharmaceutical; 2010. pp. 193-212.
29. Nielsen CU, Brodin B, Jorgensen FS, Frokjaer S, Steffansen B. Human peptide transporters: therapeutic applications. Expert Opin Ther Pat. 2002;12(9):1329-50.
30. Dantzig AH. Oral absorption of β-lactam by intestinal peptide transport proteins. Adv Drug Deliv Rev. 1997;23(1-3):63-76.
31. WideraA, Kim KJ, Crandall ED, ShenWC.Transcytosis of GCSF-Transferrin across rat alveolar epithelial cell monolayers. Pharm Res. 2003;20(8):1231-8.
32. Shah D, Shen WC. Transcellular delivery of an insulin-Transferrin conjugate in enterocyte-like Caco-2 cells. J Pharm Sci. 1996;85(12):1306-11.
33. PetrusAK, Fairchild TJ, Doyle RP. Traveling the vitamin B12 pathway: oral delivery of protein and peptide drugs. Angew Chem Int Ed Engl. 2009;48(6):1022-8.
34. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature. 2003;422(6927):37-44.
35. Weisz OA, Rodriguez-Boulan E. Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci. 2009;122(Pt 23):4253-66.
36. Ben-Dov N, Korenstein R. Enhancement of cell membrane invaginations, vesiculation and uptake of macromolecules by protonation of the cell surface. PLoS One. 2012;7(4):e35204.
37. Ben-Dov N, Korenstein R. Actin-cytoskeleton rearrangement modulates proton-induced uptake. Exp Cell Res. 2013;319(7):946-54.
38. Abrami L, Liu S, Cosson P, Leppla SH, van der Goot FG. Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J Cell Biol. 2003;160(3): 321-8.
39. Mooren OL, Galletta BJ, Cooper JA. Roles for actin assembly in endocytosis. Annu Rev Biochem. 2012;81:661-86.
40. Sandvig K, van Deurs B. Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther. 2005;12(11):865-72.
41. Garred O, Rodal SK, van Deurs B, Sandvig K. Reconstitution of clathrin-independent endocytosis at the apical domain of permeabilized MDCK II cells: requirement for a Rho-family GTPase. Traffic. 2001;2(1):26-36.
42. Cohen AW, Hnasko R, Schubert W, Lisanti MP. Role of caveolae and caveolins in health and disease. Physiol Rev. 2004;84(4):1341-79.
43. Jones AT. Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med. 2007;11(4):670-84.
44. Tuma P, Hubbard AL. Transcytosis: crossing cellular barriers. Physiol Rev. 2003; 83(3):871-932.
45. Arbit E, Kidron M. Oral insulin: the rationale for this approach and current developments. J Diabetes Sci Technol. 2009;3(3):562-7.
46. Renukuntla J, Vadlapudi AD, Patel A, Boddu SH, Mitra AK. Approaches for enhancing oral bioavailability of peptides and proteins. Int J Pharm. 2013;447(1-2):75-93.
47. Li P, Nielsen HM, Mullertz A. Oral delivery of peptides and proteins using lipid-based drug delivery systems. Expert Opin Drug Deliv. 2012;9(10):1289-304.
48. van der Walle CF, Schmidt E. Modulation of the intestinal tight junctions using bacterial enterotoxins. In: van derWalle CF editor. Peptide and protein delivery. Oxford: Elsevier; 2011. pp. 195-219.
49. Hecht G, Pothoulakis C, LaMont JT, Madara JL. Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers. J Clin Invest. 1988;82(5):1516-24.
50. Just I, Fritz G, Aktories K, Giry M, Popoff MR, Boquet P, Hegenbarth S, von Eichel-Streiber C. Clostridium difficile toxin B acts on the GTP-binding protein Rho. J Biol Chem. 1994;269(14):10706-712.
51. Takahashi A, Kondoh M, Masuyama A, Fujii M, Mizuguchi H, HoriguchiY, WatanabeY. Role of C-Terminal regions of the C-Terminal fragment of Clostridium perfringens enterotoxin in its interaction with claudin-4. J Control Release. 2005;108(1):56-62.
52. Song KH, Fasano A, Eddington ND. Effect of the six-mer synthetic peptide (AT1002) fragment of zonula occludens toxin on the intestinal absorption of cyclosporin A. Int J Pharm. 2008;351(1-2):8-14.
53. Gonzalez-Mariscal L, Tapia R, Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim Biophys Acta. 2008;1778(3):729-56.
54. HiraseT, Kawashima S, Wong EY, UeyamaT, RikitakeY, Tsukita S, Yokoyama M, Staddon JM. Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCKdependent and-independent mechanisms. J Biol Chem. 2001;276(13):10423-31.
55. Aungst BJ. Absorption enhancers: applications and advances. AAPS J. 2012;14(1):10-8.
56. Shen L, Turner JR. Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell. 2005;16(9):3919-36.
57. Park K, Kwon IC, Park K. Oral protein delivery: current status and future prospect. React Funct Polym. 2011;71(3):280-87.
58. Maher S, Leonard TW, Jacobsen J, Brayden DJ. Safety and efficacy of sodium caprate in promoting oral drug absorption: from in vitro to the clinic. Adv Drug Deliv Rev. 2009;61(15):1427-49.
59. Hovgaard L, Brondsted H, Nielsen HM. Drug delivery studies in Caco-2 monolayers. II: Absorption enhancer effects of lysophosphatidylcholines. Int J Pharm. 1995;114(2):141-9.
60. Radwan MA, Aboul-Enein HY the effect of absorption enhancers on the initial degradation kinetics of insulin by alpha-chymotrypsin. Int J Pharm. 2001;217(1-2):111-20.
61. Sayani AP, ChienYW. Systemic delivery of peptides and proteins across absorptive mucosae. Crit Rev Ther Drug Carrier Syst. 1996;13(1-2):85-184.
62. Yoo HS, Choi HK, Park TG. Protein-fatty acid complex for enhanced loading and stability within biodegradable nanoparticles. J Pharm Sci. 2001;90(2):194-201.
63. Cui F, Shi K, Zhang L, Tao A, KawashimaY. Biodegradable nanoparticles loaded with insulinphospholipid complex for oral delivery: preparation, in vitro characterization and in vivo evaluation. J Control Release. 2006;114(2):242-50.
64. Sadeghi AM, Dorkoosh FA, Avadi MR, Weinhold M, Bayat A, Delie F, Gurny R, Larijani B, Rafiee-Tehrani M, Junginger HE. Permeation enhancer effect of chitosan and chitosan derivatives: comparison of formulations as soluble polymers and nanoparticulate systems on insulin absorption in Caco-2 cells. Eur J Pharm Biopharm. 2008;70(1):270-78.
65. Woitiski CB, Sarmento B, Carvalho RA, Neufeld RJ, Veiga F. Facilitated nanoscale delivery of insulin across intestinal membrane models. Int J Pharm. 2011;412(1-2):123-31.
66. Chen MC, Mi FL, Liao ZX, Hsiao CW, Sonaje K, Chung MF, Hsu LW, Sung HW. Recent advances in chitosan-based nanoparticles for oral delivery of macromolecules. Adv Drug Deliv Rev. 2012;65(6):865-79
67. Prego C, Garcia M, Torres D, Alonso MJ. Transmucosal macromolecular drug delivery. J Control Release. 2005;101(1-3):151-62.
68. Hu CS, Chiang CH, Hong PD, Yeh MK. Influence of charge on FITC-BSA-loaded chondroitin sulfate-chitosan nanoparticles upon cell uptake in human Caco-2 cell monolayers. Int J Nanomedicine. 2012;7:4861-72.
69. Foged C, Nielsen HM. Cell-penetrating peptides for drug delivery across membrane barriers. Expert Opin Drug Deliv. 2008;5(1):105-17.
70. Khafagy el-S, Morishita M, Kamei N, Eda Y, Ikeno Y, Takayama K. Efficiency of cellpenetrating peptides on the nasal and intestinal absorption of therapeutic peptides and proteins. Int J Pharm. 2009;381(1):49-55.
71. Khafagy el-S, Morishita M. Oral biodrug delivery using cell-penetrating peptide. Adv Drug Deliv Rev. 2012;64(6):531-9.
72. Trehin R, Krauss U, Beck-Sickinger AG, Merkle HP, Nielsen HM. Cellular uptake but low permeation of human calcitonin-derived cell penetrating peptides and Tat(47-57) through welldifferentiated epithelial models. Pharm Res. 2004;21(7):1248-56.
73. Li N, Li XR, Zhou YX, Li WJ, ZhaoY, Ma SJ, Li JW, Gao YJ, LiuY, Wang XL, Yin DD the use of polyion complex micelles to enhance the oral delivery of salmon calcitonin and transport mechanism across the intestinal epithelial barrier. Biomaterials. 2012;33(34):8881-92.
74. Du W, Fan Y, Zheng N, He B, Yuan L, Zhang H, Wang X, Wang J, Zhang X, Zhang Q. Transferrin receptor specific nanocarriers conjugated with functional 7peptide for oral drug delivery. Biomaterials. 2013;34(3):794-806.
75. He C, Yin L, Tang C, Yin C. Size-dependent absorption mechanism of polymeric nanoparticles for oral delivery of protein drugs. Biomaterials. 2012;33(33):8569-78.
76. Niu M, LuY, Hovgaard L, Guan P, TanY, Lian R, Qi J, WuW. Hypoglycemic activity and oral bioavailability of insulin-loaded liposomes containing bile salts in rats: the effect of cholate type, particle size and administered dose. Eur J Pharm Biopharm. 2012;81(2):265-72.
77. Barua S, Yoo JW, Kolhar P, Wakankar A, Gokarn YR, Mitragotri S. Particle shape enhances specificity of antibody-displaying nanoparticles. Proc Natl Acad Sci U S A. 2013;110(9): 3270-5.
78. Hussain N. Ligand-mediated tissue specific drug delivery. Adv Drug Deliv Rev. 2000;43(2-3):95-100.
79. Jin Y, Song Y, Zhu X, Zhou D, Chen C, Zhang Z, Huang Y. Goblet cell-Targeting nanoparticles for oral insulin delivery and the influence of mucus on insulin transport. Biomaterials. 2012;33(5):1573-82.
80. Rajapaksa TE, Stover-Hamer M, Fernandez X, Eckelhoefer HA, Lo DD. Claudin 4-Targeted protein incorporated into PLGA nanoparticles can mediate M cell targeted delivery. J Control Release. 2010;142(2):196-205.
81. Yoo MK, Kang SK, Choi JH, Park IK, Na HS, Lee HC, Kim EB, Lee NK, Nah JW, Choi YJ, Cho CS. Targeted delivery of chitosan nanoparticles to Peyer's patch using M cell-homing peptide selected by phage display technique. Biomaterials. 2010;31(30):7738-47.
82. Jepson MA, Clark MA, Hirst BH.Mcell targeting by lectins: a strategy for mucosal vaccination and drug delivery. Adv Drug Deliv Rev. 2004;56(4):511-25.
83. Monopoli MP, Aberg C, Salvati A, Dawson KA. Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol. 2012;7(12):779-86.
84. SalvatiA, PitekAS, MonopoliMP, Prapainop K, Bombelli FB, Hristov DR, Kelly PM, Aberg C, Mahon E, Dawson KA.Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat Nanotechnol. 2013;8(2):137-43.
85. Vogel U, Sandvig K, van Deurs B. Expression of caveolin-1 and polarized formation of invaginated caveolae in Caco-2 and MDCK II cells. J Cell Sci. 1998;111(Pt 6):825-32.
86. Al Soraj M, He L, Peynshaert K, Cousaert J, Vercauteren D, Braeckmans K, De Smedt SC, Jones AT. siRNA and pharmacological inhibition of endocytic pathways to characterize the differential role of macropinocytosis and the actin cytoskeleton on cellular uptake of dextran and cationic cell penetrating peptides octaarginine (R8) and HIV-Tat. J Control Release. 2012;161(1):132-41.
87. Berkowitz SA, Engen JR, Mazzeo JR, Jones GB. Analytical tools for characterizing biopharmaceuticals and the implications for biosimilars. Nat Rev Drug Discov. 2012;11(7):527-40.
88. Citi S. Protein kinase inhibitors prevent junction dissociation induced by low extracellular calcium in MDCK epithelial cells. J Cell Biol. 1992;117(1):169-78.
89. Fernandez D, Boix E, Pallares I, Aviles FX, Vendrell J. Structural and functional analysis of the complex between citrate and the zinc peptidase carboxypeptidase A. Enzyme Res. 2011;2011:128676.
90. Sung HW, Sonaje K, Liao ZX, Hsu LW, Chuang EY. pH-responsive nanoparticles shelled with chitosan for oral delivery of insulin: from mechanism to therapeutic applications. Acc Chem Res. 2012;45(4):619-29.
91. Su FY, Lin KJ, Sonaje K, Wey SP, Yen TC, Ho YC, Panda N, Chuang EY, Maiti B, Sung HW. Protease inhibition and absorption enhancement by functional nanoparticles for effective oral insulin delivery. Biomaterials. 2012;33(9):2801-11.
92. Krug SM, Amasheh M, Dittmann I, Christoffel I, Fromm M, Amasheh S. Sodium caprate as an enhancer of macromolecule permeation across tricellular tight junctions of intestinal cells. Biomaterials. 2013;34(1):275-82.
93. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol. 2007;8(8):603-12.