614
Views
22
CrossRef citations to date
0
Altmetric
Reviews

Receptor-mediated endocytosis of macromolecules and strategy to enhance their transport in alveolar epithelial cells

, PhD (Professor) , , MS (Assistant Professor) , , MS (Assistant Professor) & , PhD (Associate Professor)

Bibliography

  • Patton JS. Mechanisms of macromolecule absorption by the lungs. Adv Drug Deliv Rev 1996;19:3-36
  • Mehanna MM, Mohyeldin SM, Elgindy NA. Respirable nanocarriers as a promising strategy for antitubercular drug delivery. J Control Release 2014;187:183-97
  • Sung JC, Pulliam BL, Edwards DA. Nanoparticles for drug delivery to the lungs. Trends Biotechnol 2007;25(12):563-70
  • Baginski L, Tachon G, Falson F, et al. Reverse transcription polymerase chain reaction (RT-PCR) analysis of proteolytic enzymes in cultures of human respiratory epithelial cells. J Aerosol Med Pulm Drug Deliv 2011;24(2):89-101
  • Colthorpe P, Farr SJ, Taylor G, et al. The pharmacokinetics of pulmonary-delivered insulin: a comparison of intratracheal and aerosol administration to the rabbit. Pharm Res 1992;9(6):764-8
  • Paranjpe M, Müller-Goymann CC. Nanoparticle-mediated pulmonary drug delivery: a review. Int J Mol Sci 2014;15(4):5852-73
  • Ferkol T, Cohn LA, Phillips TE, et al. Targeted delivery of antiprotease to the epithelial surface of human tracheal xenografts. Am J Respir Crit Care Med 2003;167(10):1374-9
  • Codrons V, Vanderbist F, Ucakar B, et al. Impact of formulation and methods of pulmonary delivery on absorption of parathyroid hormone (1-34) from rat lungs. J Pharm Sci 2004;93(5):1241-52
  • Bosquillon C, Préat V, Vanbever R. Pulmonary delivery of growth hormone using dry powders and visualization of its local fate in rats. J Control Release 2004;96(2):233-44
  • Yamada K, Odomi M, Okada N, et al. Chitosan oligomers as potential and safe absorption enhancers for improving the pulmonary absorption of interferon-alpha in rats. J Pharm Sci 2005;94(11):2432-40
  • Sakagami M, Omidi Y, Campbell L, et al. Expression and transport functionality of FcRn within rat alveolar epithelium: a study in primary cell culture and in the isolated perfused lung. Pharm Res 2006;23(2):270-9
  • Nadkarni PP, Costanzo RM, Sakagami M. Pulmonary delivery of peptide YY for food intake suppression and reduced body weight gain in rats. Diabetes Obes Metab 2011;13(5):408-17
  • Baginski L, Tewes F, Buckley ST, et al. Investigations into the fate of inhaled salmon calcitonin at the respiratory epithelial barrier. Pharm Res 2012;29(1):332-41
  • Baginski L, Gobbo OL, Tewes F, et al. In vitro and in vivo characterisation of PEG-lipid-based micellar complexes of salmon calcitonin for pulmonary delivery. Pharm Res 2012;29(6):1425-34
  • John TA, Vogel SM, Minshall RD, et al. Evidence for the role of alveolar epithelial gp60 in active transalveolar albumin transport in the rat lung. J Physiol 2001;533(Pt 2):547-59
  • Yumoto R, Nishikawa H, Okamoto M, et al. Clathrin-mediated endocytosis of FITC-albumin in alveolar type II epithelial cell line RLE-6TN. Am J Physiol Lung Cell Mol Physiol 2006;290(5):L946-55
  • Buchäckert Y, Rummel S, Vohwinkel CU, et al. Megalin mediates transepithelial albumin clearance from the alveolar space of intact rabbit lungs. J Physiol 2012;590(Pt 20):5167-81
  • Yamahara H, Verroust P, Moestrup S, et al. Fate of insulin during transit across rat alveolar epithelial cell monolayers. Eur J Pharm Biopharm 1994;40:294-8
  • Bahhady R, Kim KJ, Borok Z, et al. Characterization of protein factor(s) in rat bronchoalveolar lavage fluid that enhance insulin transport via transcytosis across primary rat alveolar epithelial cell monolayers. Eur J Pharm Biopharm 2008;69:808-16
  • Ikehata M, Yumoto R, Kato Y, et al. Mechanism of insulin uptake in rat alveolar type II and type I-like epithelial cells. Biol Pharm Bull 2009;32(10):1765-9
  • Patton JS, Brain JD, Davies LA, et al. The particle has landed-characterizing the fate of inhaled pharmaceuticals. J Aerosol Med Pulm Drug Deliv 2010;23(Suppl 2):S71-87
  • Fehrenbach H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2001;2(1):33-46
  • Evans MJ, Cabral LJ, Stephens RJ, et al. Transformation of alveolar type 2 cells to type 1 cells following exposure to NO2. Exp Mol Pathol 1975;22(1):142-50
  • Uhal BD. Cell cycle kinetics in the alveolar epithelium. Am J Physiol 1997;272(6 Pt 1):L1031-45
  • Demling N, Ehrhardt C, Kasper M, et al. Promotion of cell adherence and spreading: a novel function of RAGE, the highly selective differentiation marker of human alveolar epithelial type I cells. Cell Tissue Res 2006;323(3):475-88
  • Endter S, Francombe D, Ehrhardt C, et al. RT-PCR analysis of ABC, SLC and SLCO drug transporters in human lung epithelial cell models. J Pharm Pharmacol 2009;61(5):583-91
  • Groneberg DA, Nickolaus M, Springer J, et al. Localization of the peptide transporter PEPT2 in the lung: implications for pulmonary oligopeptide uptake. Am J Pathol 2001;158(2):707-14
  • Groneberg DA, Eynott PR, Döring F, et al. Distribution and function of the peptide transporter PEPT2 in normal and cystic fibrosis human lung. Thorax 2002;57(1):55-60
  • Takano M, Horiuchi T, Sasaki Y, et al. Expression and function of PEPT2 during transdifferentiation of alveolar epithelial cells. Life Sci 2013;93(17):630-6
  • Takano M, Yumoto R, Murakami T. Expression and function of efflux drug transporters in the intestine. Pharmacol Ther 2006;109(1-2):137-61
  • Murakami T, Takano M. Intestinal efflux transporters and drug absorption. Expert Opin Drug Metab Toxicol 2008;4(7):923-39
  • Campbell L, Abulrob AN, Kandalaft LE, et al. Constitutive expression of p-glycoprotein in normal lung alveolar epithelium and functionality in primary alveolar epithelial cultures. J Pharmacol Exp Ther 2003;304(1):441-52
  • van der Deen M, de Vries EG, Timens W, et al. ATP-binding cassette (ABC) transporters in normal and pathological lung. Respir Res 2005;6:59
  • Endter S, Becker U, Daum N, et al. P-glycoprotein (MDR1) functional activity in human alveolar epithelial cell monolayers. Cell Tissue Res 2007;328(1):77-84
  • Cordon-Cardo C, O’Brien JP, Boccia J, et al. Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues. J Histochem Cytochem 1990;38(9):1277-87
  • Kim KJ, Malik AB. Protein transport across the lung epithelial barrier. Am J Physiol Lung Cell Mol Physiol 2003;284(2):L247-59
  • Nagai J, Takano M. GP60-mediated transport of albumin in endothelial and non-endothelial cells. In: Otagiri M, editor. Human serum albumin. Sojo University; Kumamoto, Japan: 2013. p. 122-35
  • Rennard SI, Basset G, Lecossier D, et al. Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution. J Appl Physiol 1986;60(2):532-8
  • Hastings RH, Folkesson HG, Matthay MA. Mechanisms of alveolar protein clearance in the intact lung. Am J Physiol Lung Cell Mol Physiol 2004;286(4):L679-89
  • Kim KJ, LeBon TR, Shinbane JS, et al. Asymmetric [14C]albumin transport across bullfrog alveolar epithelium. J Appl Physiol 1985;59(4):1290-7
  • Schnitzer JE, Carley WW, Palade GE. Albumin interacts specifically with a 60-kDa microvascular endothelial glycoprotein. Proc Natl Acad Sci USA 1988;85(18):6773-7
  • Schnitzer JE, Oh P. Albondin-mediated capillary permeability to albumin. Differential role of receptors in endothelial transcytosis and endocytosis of native and modified albumins. J Biol Chem 1994;269(8):6072-82
  • Tiruppathi C, Finnegan A, Malik AB. Isolation and characterization of a cell surface albumin-binding protein from vascular endothelial cells. Proc Natl Acad Sci USA 1996;93(1):250-4
  • Tiruppathi C, Song W, Bergenfeldt M, et al. Gp60 activation mediates albumin transcytosis in endothelial cells by tyrosine kinase-dependent pathway. J Biol Chem 1997;272(41):25968-75
  • Vogel SM, Minshall RD, Pilipović M, et al. Albumin uptake and transcytosis in endothelial cells in vivo induced by albumin-binding protein. Am J Physiol Lung Cell Mol Physiol 2001;281(6):L1512-22
  • Schnitzer JE, Oh P, Pinney E, et al. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 1994;127(5):1217-32
  • Hu G, Vogel SM, Schwartz DE, et al. Intercellular adhesion molecule-1-dependent neutrophil adhesion to endothelial cells induces caveolae-mediated pulmonary vascular hyperpermeability. Circ Res 2008;102(12):e120-31
  • Driscoll KE, Carter JM, Iype PT, et al. Establishment of immortalized alveolar type II epithelial cell lines from adult rats. In Vitro Cell Dev Biol Anim 1995;31(7):516-27
  • Lieber M, Smith B, Szakal A, et al. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int J Cancer 1976;17(1):62-70
  • Stearns RC, Paulauskis JD, Godleski JJ. Endocytosis of ultrafine particles by A549 cells. Am J Respir Cell Mol Biol 2001;24(2):108-15
  • Sporty JL, Horálková L, Ehrhardt C. In vitro cell culture models for the assessment of pulmonary drug disposition. Expert Opin Drug Metab Toxicol 2008;4(4):333-45
  • Ikehata M, Yumoto R, Nakamura K, et al. Comparison of albumin uptake in rat alveolar type II and type I-like epithelial cells in primary culture. Pharm Res 2008;25(4):913-22
  • Yumoto R, Suzuka S, Oda K, et al. Endocytic uptake of FITC-albumin by human alveolar epithelial cell line A549. Drug Metab Pharmacokinet 2012;27(3):336-43
  • Takano M, Yumoto R. Transport of proteins and peptides and its regulation in alveolar epithelial cells. Membrane 2011;36:145-53
  • Tagawa M, Yumoto R, Oda K, et al. Low-affinity transport of FITC-albumin in alveolar type II epithelial cell line RLE-6TN. Drug Metab Pharmacokinet 2008;23(5):318-27
  • Yumoto R, Suzuka S, Nishimoto S, et al. Enhancing effect of poly(amino acid)s on albumin uptake in human lung epithelial A549 cells. Drug Metab Pharmacokinet 2013;28:159-63
  • Nelson N, Harvey WR. Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol Rev 1999;79(2):361-85
  • Sasaki Y, Nagai J, Kitahara Y, et al. Expression of chloride channel, ClC-5, and its role in receptor-mediated endocytosis of albumin in OK cells. Biochem Biophys Res Commun 2001;282(1):212-18
  • Takano M, Koyama Y, Nishikawa H, et al. Segment-selective absorption of lysozyme in the intestine. Eur J Pharmacol 2004;502(1-2):149-55
  • Matsukawa Y, Yamahara H, Yamashita F, et al. Rates of protein transport across rat alveolar epithelial cell monolayers. J Drug Target 2000;7(5):335-42
  • Kim KJ, Matsukawa Y, Yamahara H, et al. Absorption of intact albumin across rat alveolar epithelial cell monolayers. Am J Physiol Lung Cell Mol Physiol 2003;284(3):L458-65
  • Farquhar MG, Saito A, Kerjaschki D, et al. The Heymann nephritis antigenic complex: megalin (gp330) and RAP. J Am Soc Nephrol 1995;6(1):35-47
  • Christensen EI, Birn H. Megalin and cubilin: synergistic endocytic receptors in renal proximal tubule. Am J Physiol Renal Physiol 2001;280(4):F562-73
  • Kozyraki R. Cubilin, a multifunctional epithelial receptor: an overview. J Mol Med (Berl) 2001;79(4):161-7
  • Hammad SM, Barth JL, Knaak C, et al. Megalin acts in concert with cubilin to mediate endocytosis of high density lipoproteins. J Biol Chem 2000;275(16):12003-8
  • Cui S, Verroust P, Moestrup S, et al. Megalin/gp330 mediates uptake of albumin in renal proximal tubule. Am J Physiol 1996;271:F900-7
  • Leheste JR, Rolinski B, Vorum H, et al. Megalin knockout mice as an animal model of low molecular weight proteinuria. Am J Pathol 1999;155(4):1361-70
  • Birn H, Fyfe JC, Jacobsen C, et al. Cubilin is an albumin binding protein important for renal tubular albumin reabsorption. J Clin Invest 2000;105(10):1353-61
  • Kolleck I, Wissel H, Guthmann F, et al. HDL-holoparticle uptake by alveolar type II cells: effect of vitamin E status. Am J Respir Cell Mol Biol 2002;27(1):57-63
  • John TA, Vogel SM, Tiruppathi C, et al. Quantitative analysis of albumin uptake and transport in the rat microvessel endothelial monolayer. Am J Physiol Lung Cell Mol Physiol 2003;284(1):L187-96
  • Greenwalt DE, Lipsky RH, Ockenhouse CF, et al. Membrane glycoprotein CD36: a review of its roles in adherence, signal transduction, and transfusion medicine. Blood 1992;80(5):1105-15
  • Baines RJ, Chana RS, Hall M, et al. CD36 mediates proximal tubular binding and uptake of albumin and is upregulated in proteinuric nephropathies. Am J Physiol Renal Physiol 2012;303(7):F1006-14
  • Tenten V, Menzel S, Kunter U, et al. Albumin is recycled from the primary urine by tubular transcytosis. J Am Soc Nephrol 2013;24(12):1966-80
  • Kim KJ, Fandy TE, Lee VHL, et al. Net absorption of IgG via FcRn-mediated transcytosis across rat alveolar epithelial cell monolayers. Am J Physiol Lung Cell Mol Physiol 2004;287(3):L616-22
  • Matthay MA, Folkesson HG, Clerici C. Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 2002;82(3):569-600
  • Ware LB, Matthay MA. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. Am J Respir Crit Care Med 2001;163(6):1376-83
  • Bachofen M, Weibel ER. Alterations of the gas exchange apparatus in adult respiratory insufficiency associated with septicemia. Am Rev Respir Dis 1977;116(4):589-615
  • Clark JG, Milberg JA, Steinberg KP, et al. Type III procollagen peptide in the adult respiratory distress syndrome. Association of increased peptide levels in bronchoalveolar lavage fluid with increased risk for death. Ann Intern Med 1995;122(1):17-23
  • Eckle T, Grenz A, Laucher S, et al. A2B adenosine receptor signaling attenuates acute lung injury by enhancing alveolar fluid clearance in mice. J Clin Invest 2008;118(10):3301-15
  • Kooijman EE, Kuzenko SR, Gong D, et al. Phosphatidylinositol 4,5-bisphosphate stimulates alveolar epithelial fluid clearance in male and female adult rats. Am J Physiol Lung Cell Mol Physiol 2011;301(5):L804-11
  • Pedersen LR, Müllertz KM, Amtorp O, et al. Enhanced alveolar fluid clearance following 72 h of continuous isoproterenol infusion in rats. Acta Physiol (Oxf) 2012;206(2):142-9
  • Saumon G, Martet G. Spermine increases the active and passive transport across the alveolar epithelium in situ: effect of thiol reagents. Pflugers Arch 2001;441(4):559-65
  • Kavimandan NJ, Losi E, Peppas NA. Novel delivery system based on complexation hydrogels as delivery vehicles for insulin-transferrin conjugates. Biomaterials 2006;27(20):3846-54
  • Shen Z, Zhang Q, Wei S, et al. Proteolytic enzymes as a limitation for pulmonary absorption of insulin: in vitro and in vivo investigations. Int J Pharm 1999;192(2):115-21
  • Park SH, Kwon JH, Lim SH, et al. Characterization of human insulin microcrystals and their absorption enhancement by protease inhibitors in rat lungs. Int J Pharm 2007;339(1-2):205-12
  • Widera A, Kim KJ, Crandall ED, et al. Transcytosis of GCSF-transferrin across rat alveolar epithelial cell monolayers. Pharm Res 2003;20(8):1231-8
  • Amet N, Wang W, Shen WC. Human growth hormone-transferrin fusion protein for oral delivery in hypophysectomized rats. J Control Release 2010;141(2):177-82
  • Wan JS, Persiani S, Shen WC. Transcellular processing of disulfide-and thioether-linked peroxidase-polylysine conjugates in cultured MDCK epithelial cells. J Cell Physiol 1990;145(1):9-15
  • Natsume H, Iwata S, Ohtake K, et al. Screening of cationic compounds as an absorption enhancer for nasal drug delivery. Int J Pharm 1999;185(1):1-12
  • Khalil IA, Kogure K, Futaki S, et al. High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression. J Biol Chem 2006;281(6):3544-51
  • Ramsay E, Hadgraft J, Birchall J, et al. Examination of the biophysical interaction between plasmid DNA and the polycations, polylysine and polyornithine, as a basis for their differential gene transfection in-vitro. Int J Pharm 2000;210(1-2):97-107
  • Agu RU, Ugwoke MI, Armand M, et al. The lung as a route for systemic delivery of therapeutic proteins and peptides. Respir Res 2001;2(4):198-209
  • de Galan BE, Simsek S, Tack CJ, et al. Efficacy and safety of inhaled insulin in the treatment of diabetes mellitus. Neth J Med 2006;64(9):319-25
  • Scheuch G, Kohlhaeufl MJ, Brand P, et al. Clinical perspectives on pulmonary systemic and macromolecular delivery. Adv Drug Deliv Rev 2006;58(9-10):996-1008
  • Owens DR. New horizons-alternative routes for insulin therapy. Nat Rev Drug Discov 2002;1(7):529-40
  • Owens DR, Zinman B, Bolli G. Alternative routes of insulin delivery. Diabet Med 2003;20(11):886-98
  • FDA News Release: FDA approves Afrezza to treat diabetes. Available from: www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm403122.htm
  • Wang Z, Zhang Q. Transport of proteins and peptides across human cultured alveolar A549 cell monolayer. Int J Pharm 2004;269(2):451-6
  • Bur M, Huwer H, Lehr CM, et al. Assessment of transport rates of proteins and peptides across primary human alveolar epithelial cell monolayers. Eur J Pharm Sci 2006;28(3):196-203
  • Kirchhausen T, Macia E, Pelish H. Use of Dynasore, the Small Molecule Inhibitor of Dynamin, in the Regulation of Endocytosis. Methods Enzymol 2008;438:77-93
  • Oda K, Yumoto R, Nagai J, et al. Mechanism underlying insulin uptake in alveolar epithelial cell line RLE-6TN. Eur J Pharmacol 2011;672(1-3):62-9
  • Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007;8(8):603-12
  • Di Guglielmo GM, Drake PG, Baass PC, et al. Insulin receptor internalization and signalling. Mol Cell Biochem 1998;182(1-2):59-63
  • Oda K, Yumoto R, Nagai J, et al. Enhancement effect of poly(amino acid)s on insulin uptake in alveolar epithelial cells. Drug Metab Pharmacokinet 2012;27(6):570-8
  • Dobbs LG, Pian MS, Maglio M, et al. Maintenance of the differentiated type II cell phenotype by culture with an apical air surface. Am J Physiol 1997;273(2 Pt 1):L347-54
  • Borok Z, Danto SI, Dimen LL, et al. Na+-K+-ATPase expression in alveolar epithelial cells: upregulation of active ion transport by KGF. Am J Physiol 1998;274(1 Pt 1):L149-58
  • Salomon JJ, Muchitsch VE, Gausterer JC, et al. The cell line NCl-H441 is a useful in vitro model for transport studies of human distal lung epithelial barrier. Mol Pharmaceutics 2014;11(3):995-1006
  • Kemp SJ, Thorley AJ, Gorelik J, et al. Immortalization of human alveolar epithelial cells to investigate nanoparticle uptake. Am J Respir Cell Mol Biol 2008;39(5):591-7
  • Horálková L, Radziwon A, Endter S, et al. Characterisation of the R3/1 cell line as an alveolar epithelial cell model for drug disposition studies. Eur J Pharm Sci 2009;36(4-5):444-50
  • van den Bogaard EH, Dailey LA, Thorley AJ, et al. Inflammatory response and barrier properties of a new alveolar type 1-like cell line (TT1). Pharm Res 2009;26(5):1172-80
  • Takano M, Yamamoto C, Sambuichi K, et al. Introduction of a single transporter gene ABCA3 directs RLE-6TN to more type II-like alveolar epithelial cells. Membrane 2013;38:246-53
  • Dobrinskikh E, Okamura K, Kopp JB, et al. Human podocytes perform polarized, caveolae-dependent albumin endocytosis. Am J Physiol Renal Physiol 2014;306(9):F941-51
  • Nagai M, Meerloo T, Takeda T, et al. The adaptor protein ARH escorts megalin to and through endosomes. Mol Biol Cell 2003;14(12):4984-96
  • Shah M, Baterina OYJr, Taupin V, et al. ARH directs megalin to the endocytic recycling compartment to regulate its proteolysis and gene expression. J Cell Biol 2013;202(1):113-27
  • Brewer PD, Habtemichael EN, Romenskaia I, et al. Insulin-regulated Glut4 translocation: membrane protein trafficking with six distinctive steps. J Biol Chem 2014;289(25):17280-98

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.