Targeting caveolae for vesicular drug transport

Journal of Controlled Release

Volumn 87, Issue 1-3, 2003, Pages 139-151

  Gumbleton, Mark ^a   Hollins, Andrew J ^a   Omidi, Yadollah ^a   Campbell, Lee ^a   Taylor, Glyn ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Caveolae; Lung; Targeting; Transcytosis; Transport

Indexed keywords

MONOCLONAL ANTIBODY;

BIOLOGY; CAVEOLA; CONFERENCE PAPER; DRUG ABSORPTION; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; INHALATIONAL DRUG ADMINISTRATION; LUNG; LUNG ALVEOLUS EPITHELIUM; MACROMOLECULE; MEMBRANE; NONHUMAN; PRIORITY JOURNAL;

EID: 0037458825     PISSN: 01683659     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-3659(02)00358-9     Document Type: Conference Paper

References (69)

1. Palade G.E. Fine structure of blood capillaries. J. Appl. Phys. 24:1953;1424.
2. Bruns R.R., Palade G.E. Studies on blood capillaries. I. General organization of blood capillaries in muscle. J. Cell Biol. 37:1968;244-276.
3. Yamada E. The fine structure of the gall bladder epithelium of the mouse. J. Biophys. Biochem. Cytol. 1:1955;445-458.
4. Glenney J.R. Tyrosine phosphorylation of a 22 kDa protein is correlated with transformation by Rous sarcoma virus. J. Biol. Chem. 264:1989;20163-29166.
5. Rothberg K.G., Heuser J.E., Donzell W.C., Ying Y.-S., Glenney J.R., Anderson R.G.W. Caveolin, a protein component of caveolae membrane coats. Cell. 68:1992;673-682.
6. Kurzchalia T.V., Dupree P., Parton R.G., Kelllner R., Virta H., Lehnert M., Simons K. VIP21, a 21 kDa membrane protein is an integral component of trans-Golgi network derived transport vesicles. J. Cell Biol. 118:1992;1003-1014.
7. Schlegel A., Volonte D., Engelman J.A., Galbiati F., Mehta P., Zhang X.-L., Scherer P.E., Lisanti M.P. Crowded little caves: structure and function of caveolae. Cell Signal. 10:1998;457-463.
8. Shaul P.W., Anderson R.G.W. Role of plasmalemmal vesicles in signal transduction. Am. J. Physiol. 275:1998;L843-L851.
9. Gumbleton M., Abulrob A.G., Campbell L. Caveolae: an alternative membrane transport compartment. Pharm. Res. 17:2000;1035-1048.
10. Gumbleton M. Caveolae-mediated membrane transport. Adv. Drug Deliv. Rev. 49:(3):2001;217-340.
11. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572.
12. Monier S., Parton R.G., Vogel F., Behlke J., Henske A., Kurzchalia T.V. VIP21-caveolin, a membrane protein constituent of caveolae coat, oligomerizes in vivo and in vitro. Mol. Biol. Cell. 6:1995;911-927.
13. Sargiacomo M., Scherer P.E., Tang Z.-L., Kubler E., Song K.S., Sanders M.C., Lisanti M.P. Oligomeric structure of caveolin: Implications for caveolae membrane organisation. Proc. Natl. Acad. Sci. USA. 92:1995;9407-9411.
14. Song K.S., Tang Z.-L., Li S., Lisanti M.P. Mutational analysis of the properties of caveolin-1. J. Biol. Chem. 272:1997;4398-4403.
15. Murata M., Peranen J., Schreiner R., Wieland F., Kurzchalia T.V., Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc. Natl. Acad. Sci. USA. 92:1995;10339-10343.
16. Monier S., Dietzen D.J., Hastings W.R., Lublin D.M., Kurzchalia T.V. Oligomerisation of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett. 388:1996;143-149.
17. Li S., Galbiati F., Volonte D., Sargiacomo M., Engelman J.A., Das K., Scherer P.E., Lisanti M.P. Mutational analysis of caveolin-induced vesicle formation. FEBS Lett. 434:1998;127-134.
18. Mora R., Bonilha V.L., Marmorstein A., Scherer P.E., Brown D., Lisanti M.P., Rodriguez-Boulan E. Caveolin-2 localises to the Golgi complex but redistributes to plasma membrane, caveolae and rafts when co-expressed with caveolin-1. J. Biol. Chem. 274:1999;25708-25717.
19. Scherer P.E., Lewis R.Y., Volonte D., Engelman J.A., Galbiati F., Couet J., Kohtz D.S., van Donselaar E., Lisanti M.P. Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in-vivo. J. Biol. Chem. 272:1997;29337-29346.
20. Scherer P.E., Lisanti M.P., Baldini G., Sargiacomo M., Mastick C.C., Lodish H.F. Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J. Cell. Biol. 127:1994;1233-1243.
21. Campbell L., Hollins A.J., Al-Eid A., Newman G.R., von Ruhland C., Gumbleton M. Caveolin-1 expression and caveolae biogenesis during cell transdifferentiation in lung alveolar epithelial primary cultures. Biochem. Biophys. Res. Commun. 262:1999;744-751.
22. Koleske A.J., Baltimore D., Lisanti M.P. Reduction of caveolin and caveolae in oncogenically transformed cells. Proc. Natl. Acad. Sci. USA. 92:1995;1381-1385.
23. Fra A.M., Williamson E., Simons K., Parton R.G. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Cell. Biol. 92:1995;8655-8659.
24. Li S., Song K.S., Koh S.S., Kikuchi A., Lisanti M.P. Baculovirus-based expression of mammalian caveolin in Sf21 insect cells. J. Biol. Chem. 271:1996;28647-28654.
25. Drab M., Verkade P., Elger M., Kasper L., John M., Lauterbach B., Menne J., Lindschau C., Mende F., Luft F.C., Schedl A., Haller H., Kurzchalia T.V. Loss of caveolae, vascular dysfunction and pulmonary defects in caveolin-1 gene disrupted mice. Science. 293:2001;2449-2452.
26. Razani B., Engelman J.A., Wang X.B., Schubert W., Zhang X.L., Marks C.B., Macaluso F., Russell R.G., Li M., Pestell R.G., Di Vizio D., Hou H., Kneitz B., Lagaud G., Christ G.J., Edelmann W., Lisanti M.P. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vacular abnormalities. J. Biol. Chem. 276:2001;38121-38138.
27. Razani B., Wang X.B., Engelman J.A., Lagaud G., Zhang X.L., Kneitz B., Hou H., Christ G.J., Edelmann W., Lisanti M.P. Caveolin-2-deficient mice show evidence of severe pulmonary dysfunction without disruption of caveolae. Mol. Cell. Biol. 22:2002;2329-2344.
28. McIntosh D.P., Schnitzer J.E. Caveolae require intact VAMP for targeted transport in vascular endothelium. Am. J. Physiol. 277:1999;H2222-H2232.
29. Sargiocomo M., Sudol M., Tang Z.-L., Lisanti M.P. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122:1993;789-807.
30. Chang W.J., Ying Y.-S., Rothberg K.G., Hooper N.M., Turner A.J., Gambliel H.A., De Gunzburg J., Mumby S.M., Gilman A.G., Anderson R.G.W. Purification and characterisation of smooth muscle cell caveolae. J. Cell Biol. 126:1994;127-138.
31. Brown D.A., Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical surface. Cell. 68:1992;533-544.
32. Smart E.J., Ying Y.-S., Conrad P.A., Anderson R.G.W. Caveolin moves from caveolae to Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127:1994;1185-1197.
33. Kurzchalia T.V., Hartmann E., Dupree P. Guilt by insolubility-does a protein's detergent insolubility reflect a caveolar location? Trends Cell Biol. 5:1995;187-189.
34. Song K.S., Li S., Okamoto T., Quilliam L.A., Sargiacomo M., Lisanti M.P. Co-purification and direct interaction of Ras with caveolin an integral membrane protein of caveolae microdomains. J. Biol. Chem. 271:1996;9690-9697.
35. Smart E.J., Ying Y.-S., Mineo C., Anderson R.G.W. A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc. Natl. Acad. Sci. USA. 92:1995;10104-10108.
36. Schnitzer J.E., Liu J., Oh P. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J. Biol. Chem. 24:1995;14399-14404.
37. 2+-ATPase and inositol triphosphate receptor. Proc. Natl. Acad. Sci. USA. 92:1995;1759-1763.
38. Schnitzer J.E., McIntosh D.P., Dvorak A.M., Liu J., Oh P. Separation of caveolae from associated microdomains of GPI-anchored proteins. Science. 269:1995;1435-1439.
39. Liu J., Oh P., Horner T., Rogers R.A., Schnitzer J.E. Organised endothelial cell surface signal transduction in caveolae distinct from glycosylphosphatidylinositol-anchored protein domains. J. Biol. Chem. 272:1997;7211-7222.
40. Oh P., Schnitzer J.E. Immunoisolation of caveolae with high affinity antibody binding to the oligomeric caveolin cage. J. Biol Chem. 274:1999;23144-23154.
41. Stan R.-V., Roberts W.G., Predescu D., Ihida K., Saucan L., Ghitescu L., Palade G.E. Immunoisolation and partial characterisation of endothelial plasmalemmal vesicles (caveolae). Mol. Biol. Cell. 8:1997;595-605.
42. Anderson R.G.W., Kamen B.A., Rothberg K.G., Lacey S.W. Potocytosis, sequestration and transport of small molecules by caveolae. Science. 255:1992;410-411.
43. Smart E.J., Mineo C., Anderson R.G.W. Clustered folate receptors deliver 5-methyltetrahydrofolate to cytoplasm of MA104 cells. J. Cell Biol. 134:1996;1169-1177.
44. Smart E.J., Ying Y.S., Donzell W.C., Anderson R.G.W. A role for caveolin in the transport of cholesterol from endoplasmic reticulum to plasma membrane. J. Biol. Chem. 271:1996;29427-29435.
45. Uittenbogaard A., Ying S., Smart E.J. Characterization of a cytosolic heat shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J. Biol. Chem. 273:1998;6525-6532.
46. Fielding C.J., Fielding P.E. Caveolae and intracellular trafficking of cholesterol. Adv. Drug Deliv. Rev. 49:2001;251-265.
47. Pelkmans L., Kartenbeck J., Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:2001;473-483.
48. Orlandi P.A., Fishman P.H. Filipin-dependent inhibition of cholera toxin, evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141:1998;905-916.
49. Schmid S.L., Sorkin A.D. Meeting report from Euresco/EMBL membrane dynamics in endocytosis. 6-11th October in Tomar Portugal. Traffic. 3:2002;77-85.
50. Predescu D., Horvat R., Predescu S., Palade G. Transcytosis in the continuous endothelium of the myocardial microvasculature is inhibited by N-ethylmaleimide. Proc. Natl. Acad. Sci. USA. 91:1994;3014-3018.
51. Predescu D., Palade G. Plasmalemmal vesicles represent the large pore system of continuous microvascular endothelium. Am. J. Physiol. 265:1993;H725-H733.
52. Predescu S., Predescu D., Palade G. Plasmalemmal vesicles function as transcytotic carriers for small proteins in the continuous endothelium. Am. J. Physiol. 272:1997;H937-H949.
53. Schnitzer J.E., Oh P., Pinney E., Allard J. Fillipin-sensitive caveolae-mediated transport in endothelium, reduced transcytosis, scavenger endocytosis and capillary permeability of select macromolecules. J. Cell. Biol. 127:1994;1217-1232.
54. Schnitzer J.E., Allard J., Oh P. NEM inhibits transcytosis, endocytosis, and capillary permeability, implication of caveolae fusion in endothelia. Am. J. Physiol. 268:1995;H48-H55.
55. Schnitzer J.E., Oh P. Albondin-mediated capillary permeability to albumin, differentiation role of receptors in endothelial transcytosis and endocytosis of native and modified albumins. J. Cell Biol. 269:1994;6072-6082.
56. Schnitzer J.E. Caveolae: from basic trafficking mechanisms to targeting transcytosis for tissue-specific drug and gene delivery. Adv. Drug Deliv. Rev. 49:2001;265-280.
57. Gumbleton M. Caveolae as potential macromolecule trafficking compartments within alveolar epithelium. Adv. Drug Deliv. Rev. 49:2001;281-300.
58. Schubert W., Frank P.G., Chow C.-W., Lisanti M.P. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J. Biol. Chem. 276:2001;48619-48622.
59. Thomsen P., Roepstorff K., Stahlhut M., van Deurs B. Caveolae are highly immobile plasma membrane microdomains which are not involved in constituitive endocytic trafficking. Mol. Biol. Cell. 13:2002;238-250.
60. Campbell L., Hollins A.J., Al-Eid A., Newman G.R., von Ruhland C., Gumbleton M. Caveolin-1 expression and caveolae biogenesis during cell transdifferentiation in lung alveolar epithelial primary cultures. Biochem. Biophys. Res. Commun. 262:1999;744-751.
61. Hastings R.H., Folkesson H.G., Petersen V., Ciriales R., Matthay M.A. Cellular uptake of albumin from lungs of anesthetised rabbits. Am. J. Physiol. 269:1995;L453-L462.
62. Hastings R.H., Wright J.R., Albertine K.H., Ciriales R., Matthay M.A. Effect of endocytosis inhibitors on alveolar clearance of albumin, immunoglobulin G and SP-A in rabbits. Am. J. Physiol. 266:1994;L544-L552.
63. John T.A., Vogel S.M., Minshall R.D., Ridge K., Tiruppathi C., Malik A.B. Evidence for the role of alveolar epithelial gp60 in active transalveolar albumin transport in the rat lung. J. Physiol. 533:2001;547-559.
64. Matsukawa Y., Yamahara H., Yamashita F., Lee V.H.L., Crandall E.D., Kim K.J. Rates of protein transport across rat alveolar epithelial cell monolayers. J. Drug Target. 7:2000;335-342.
65. Kim K.J., Rattan V., Oh P., Schnitzer J.E., Kalra V.K., Crandall E.D. Specific albumin-binding protein in alveolar epithelial cell monolayers (abstract). Am. J. Respir. Crit. Care Med. 151:1995;A190.
66. Effros R.M., Mason G.M. Measurements of pulmonary epithelial permeability in vivo. Am. Rev. Respir. Dis. 127:1983;S59-S65.
67. Cabral-Marques H.M., Hadgraft J., Kellaway I.W., Taylor G. Studies of cyclodextrin inclusion complexes IV The pulmonary absorption of salbutamol from a complex with 2-hydroxy-propyl β-cyclodextrin in rabbits. Int. J. Pharm. 77:1991;303-307.
68. Taylor G., Colthorpe P., Farr S.J. Pulmonary absorption of proteins, influence of deposition site and competitive elimination processes. Proc. Respir. Drug Deliv. IV:1994;25-37.
69. McIntosh D.P., Tan X.-Y., Oh P., Schnitzer J.E. Targeting endothelium and its dynamic caveolae for tissue specific transcytosis in vivo: A pathway to overcome cell barriers to drug and gene delivery. Proc. Natl. Acad. Sci. USA. 99:2002;1196-2001.