Clathrin-dependent entry and vesicle-mediated exocytosis define insulin transcytosis across microvascular endothelial cells

Molecular Biology of the Cell

Volumn 26, Issue 4, 2015, Pages 740-750

  Azizi, Paymon M ^a,b,c   Zyla, Roman E ^b   Guan, Sha ^a,b,c   Wang, Changsen ^b   Liu, Jun ^c   Bolz, Steffen Sebastian ^b   Heit, Bryan ^d   Klip, Amira ^a,c   Lee, Warren L ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; CLATHRIN; DYNAMIN; INSULIN;

ARTICLE; CAPILLARY ENDOTHELIAL CELL; CELL ASSAY; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; GENE SILENCING; HORMONE TRANSPORT; HUMAN; HUMAN CELL; INSULIN BINDING; INSULIN DEGRADATION; LYSOSOME; MOLECULAR STABILITY; MUSCLE CELL; PRIORITY JOURNAL; QUANTITATIVE ASSAY; TRANSCYTOSIS; CAPILLARY PERMEABILITY; CAVEOLA; CELL LINE; ENDOTHELIUM CELL; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

CAPILLARY PERMEABILITY; CAVEOLAE; CAVEOLIN 1; CELL LINE; CLATHRIN; DYNAMINS; ENDOCYTOSIS; ENDOTHELIAL CELLS; EXOCYTOSIS; HUMANS; INSULIN; LYSOSOMES; TRANSCYTOSIS;

EID: 84922789726     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-08-1307     Document Type: Article

References (40)

1. Aird WC (2007a). Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 100, 158-173.
2. Aird WC (2007b). Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 100, 174-190.
3. Armstrong SM, Khajoee V, Wang C, Wang T, Tigdi J, Yin J, Kuebler WM, Gillrie M, Davis SP, Ho M, et al. (2012). Co-regulation of transcellular and paracellular leak across microvascular endothelium by dynamin and Rac. Am J Pathol 180, 1308-1323.
4. Barrett EJ, Wang H, Upchurch CT, Liu Z (2011). Insulin regulates its own delivery to skeletal muscle by feed-forward actions on the vasculature. Am J Physiol Endocrinol Metabol 301, E252-E263.
5. Becherer U, Pasche M, Nofal S, Hof D, Matti U, Rettig J (2007). Quantifying exocytosis by combination of membrane capacitance measurements and total internal reflection fluorescence microscopy in chromaffin cells. PLoS One 2, e505.
6. Bolte S, Cordelieres FP (2006). A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224, 213-232.
7. Bonadonna RC, Saccomani MP, Del Prato S, Bonora E, DeFronzo RA, Cobelli C (1998). Role of tissue-specific blood flow and tissue recruitment in insulin-mediated glucose uptake of human skeletal muscle. Circulation 98, 234-241.
8. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000). Rab7: a key to lysosome biogenesis. Mol Biol Cell 11, 467-480.
9. Chiu JD, Richey JM, Harrison LN, Zuniga E, Kolka CM, Kirkman E, Ellmerer M, Bergman RN (2008). Direct administration of insulin into skeletal muscle reveals that the transport of insulin across the capillary endothelium limits the time course of insulin to activate glucose disposal. Diabetes 57, 828-835.
10. Craig LE, Spelman JP, Strandberg JD, Zink MC (1998). Endothelial cells from diverse tissues exhibit differences in growth and morphology. Microvasc Res 55, 65-76.
11. Crocker JC, Grier DG (1995). Methods of digital video microscopy for colloidal studies. J Colloid Interface Sci 179, 298-310.
12. Duckworth WC, Bennett RG, Hamel FG (1998). Insulin degradation: progress and potential. Endocr Rev 19, 608-624.
13. Dutta D, Williamson CD, Cole NB, Donaldson JG (2012). Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis. PLoS One 7, e45799.
14. Eggleston EM, Jahn LA, Barrett EJ (2007). Hyperinsulinemia rapidly increases human muscle microvascular perfusion but fails to increase muscle insulin clearance: evidence that a saturable process mediates muscle insulin uptake. Diabetes 56, 2958-2963.
15. Ghitescu L, Fixman A, Simionescu M, Simionescu N (1986). Specific binding sites for albumin restricted to plasmalemmal vesicles of continuous capillary endothelium: receptor-mediated transcytosis. J Cell Biol 102, 1304-1311.
16. Hammons GT, Jarett L (1980). Lysosomal degradation of receptor-bound 125I-labeled insulin by rat adipocytes: its characterization and dissociation from the short-term biologic effects of insulin. Diabetes 29, 475-486.
17. Herkner H, Klein N, Joukhadar C, Lackner E, Langenberger H, Frossard M, Bieglmayer C, Wagner O, Roden M, Muller M (2003). Transcapillary insulin transfer in human skeletal muscle. Eur J Clin Invest 33, 141-146.
18. Hernandez JL, Coll T, Ciudad CJ (2004). A highly efficient electroporation method for the transfection of endothelial cells. Angiogenesis 7, 235-241.
19. King GL, Johnson SM (1985). Receptor-mediated transport of insulin across endothelial cells. Science 227, 1583-1586.
20. Kolka CM, Bergman RN (2013). The endothelium in diabetes: its role in insulin access and diabetic complications. Rev Endocr Metab Disord 14, 13-19.
21. Kumar S, West DC, Ager A (1987). Heterogeneity in endothelial cells from large vessels and microvessels. Differentiation 36, 57-70.
22. Majumdar S, Genders AJ, Inyard AC, Frison V, Barrett EJ (2012). Insulin entry into muscle involves a saturable process in the vascular endothelium. Diabetologia 55, 450-456.
23. McCluskey A, Daniel JA, Hadzic G, Chau N, Clayton EL, Mariana A, Whiting A, Gorgani NN, Lloyd J, Quan A, et al. (2013). Building a better dynasore: the dyngo compounds potently inhibit dynamin and endocytosis. Traffic 14, 1272-1289.
24. Ponder BA, Wilkinson MM (1983). Organ-related differences in binding of Dolichos biflorus agglutinin to vascular endothelium. Dev Biol 96, 535-541.
25. Porter JC, Hall A (2009). Epithelial ICAM-1 and ICAM-2 regulate the egression of human T cells across the bronchial epithelium. FASEB J 23, 492-502.
26. Reglero-Real N, Alvarez-Varela A, Cernuda-Morollon E, Feito J, Marcos-Ramiro B, Fernandez-Martin L, Gomez-Lechon MJ, Muntane J, Sandoval P, Majano PL, et al. (2014). Apicobasal polarity controls lymphocyte adhesion to hepatic epithelial cells. Cell Rep 8, 1879-1893.
27. Richey JM (2013). The vascular endothelium, a benign restrictive barrier? NO! Role of nitric oxide in regulating insulin action. Diabetes 62, 4006-4008.
28. Schubert W, Frank PG, Razani B, Park DS, Chow CW, Lisanti MP (2001). Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem 276, 48619-48622.
29. Shimada Y, Maruya M, Iwashita S, Ohno-Iwashita Y (2002). The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur J Biochem 269, 6195-6203.
30. Steil GM, Ader M, Moore DM, Rebrin K, Bergman RN (1996). Transendothelial insulin transport is not saturable in vivo. No evidence for a receptor-mediated process. J Clin Invest 97, 1497-1503.
31. Tuma P, Hubbard AL (2003). Transcytosis: crossing cellular barriers. Physiol Rev 83, 871-932.
32. van Dam EM, Stoorvogel W (2002). Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol Biol Cell 13, 169-182.
33. Vicent D, Ilany J, Kondo T, Naruse K, Fisher SJ, Kisanuki YY, Bursell S, Yanagisawa M, King GL, Kahn CR (2003). The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J Clin Invest 111, 1373-1380.
34. von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, Robertson MJ, MacGregor KA, Tomilin N, Pechstein A, Chau N, et al. (2011). Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146, 471-484.
35. Wang H, Liu Z, Li G, Barrett EJ (2006). The vascular endothelial cell mediates insulin transport into skeletal muscle. Am J Physiol Endocrinol Metabol 291, E323-E332.
36. Wang H, Wang AX, Aylor K, Barrett EJ (2013). Nitric oxide directly promotes vascular endothelial insulin transport. Diabetes 62, 4030-4042.
37. Wang H, Wang AX, Barrett EJ (2011). Caveolin-1 is required for vascular endothelial insulin uptake. Am J Physiol Endocrinol Metabol 300, E134-E144.
38. Williams TM, Lisanti MP (2004). The caveolin proteins. Genome Biol 5, 214.
39. Wu NZ, Baldwin AL (1992). Transient venular permeability increase and endothelial gap formation induced by histamine. Am J Physiol 262, H1238-H1247.
40. Yang YJ, Hope ID, Ader M, Bergman RN (1994). Importance of transcapillary insulin transport to dynamics of insulin action after intravenous glucose. Am J Physiol 266, E17-E25.