Insulin exits skeletal muscle capillaries by fluid-phase transport

Journal of Clinical Investigation

Volumn 128, Issue 2, 2018, Pages 699-714

  Williams, Ian M ^a   Valenzuela, Francisco A ^b   Kahl, Steven D ^b   Ramkrishna, Doraiswami ^c   Mezo, Adam R ^b   Young, Jamey D ^a,d,e   Sam Wells, K ^a,e   Wasserman, David H ^a,e  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c PURDUE UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEXA FLUOR 647; FLUORESCENT DYE; INSULIN; INSULIN RECEPTOR; UNCLASSIFIED DRUG; GLUCOSE; INSR PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; PROTEIN BINDING; RHODAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CAPILLARY ENDOTHELIUM; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; IMAGE ANALYSIS; IN VIVO STUDY; INSULIN BLOOD LEVEL; INSULIN METABOLISM; INTERSTITIUM; INTRAVITAL MICROSCOPY; LEARNING ALGORITHM; LIQUID; MALE; MATHEMATICAL MODEL; MOUSE; MUSCLE CAPILLARY; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; ANIMAL; C57BL MOUSE; CAPILLARY; CHEMISTRY; DIABETES MELLITUS; GLUCOSE CLAMP TECHNIQUE; HUMAN; HYPERINSULINISM; IMAGE PROCESSING; KINETICS; METABOLISM; THEORETICAL MODEL; TRANSPORT AT THE CELLULAR LEVEL; VASCULARIZATION;

ANIMALS; ANTIGENS, CD; BIOLOGICAL TRANSPORT; CAPILLARIES; DIABETES MELLITUS; GLUCOSE; GLUCOSE CLAMP TECHNIQUE; HUMANS; HYPERINSULINISM; IMAGE PROCESSING, COMPUTER-ASSISTED; INSULIN; INTRAVITAL MICROSCOPY; KINETICS; MALE; MICE; MICE, INBRED C57BL; MODELS, THEORETICAL; MUSCLE, SKELETAL; PROTEIN BINDING; RECEPTOR, INSULIN; RHODAMINES;

EID: 85041472379     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI94053     Document Type: Article

References (49)

1. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. PhysiolRev. 2006;86(1):279–367.
2. Kolka CM, Bergman RN. The barrier within: endothelial transport of hormones. Physiology (Bethesda). 2012;27(4):237–247.
3. Barrett EJ, Wang H, Upchurch CT, Liu Z. Insulin regulates its own delivery to skeletal muscle by feed-forward actions on the vasculature. Am J PhysiolEndocrinolMetab. 2011;301(2):E252–E263.
4. Meijer RI, Gray SM, Aylor KW, Barrett EJ. Pathways for insulin access to the brain: the role of the microvascular endothelial cell. Am J Physiol Heart Circ Physiol. 2016;311(5):H1132–H1138.
5. Yang YJ, Hope ID, Ader M, Bergman RN. Insulin transport across capillaries is rate limiting for insulin action in dogs. J Clin Invest. 1989;84(5):1620–1628.
6. Broussard JL, et al. Insulin access to skeletal muscle is impaired during the early stages of diet-induced obesity. Obesity (Silver Spring). 2016;24(9):1922–1928.
7. Kubota T, et al. Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. CellMetab. 2011;13(3):294–307.
8. Sjöstrand M, Gudbjörnsdottir S, Holmäng A, Lönn L, Strindberg L, Lönnroth P. Delayed transcapillary transport of insulin to muscle interstitial fluid in obese subjects. Diabetes. 2002;51(9):2742–2748.
9. King GL, Johnson SM. Receptor-mediated transport of insulin across endothelial cells. Science. 1985;227(4694):1583–1586.
10. Majumdar S, Genders AJ, Inyard AC, Frison V, Barrett EJ. Insulin entry into muscle involves a saturable process in the vascular endothelium. Diabetologia. 2012;55(2):450–456.
11. Wang H, Liu Z, Li G, Barrett EJ. The vascular endothelial cell mediates insulin transport into skeletal muscle. Am J Physiol Endocrinol Metab. 2006;291(2):E323–E332.
12. Steil GM, Ader M, Moore DM, Rebrin K, Bergman RN. Transendothelial insulin transport is not saturable in vivo. No evidence for a receptor-mediated process. J Clin Invest. 1996;97(6):1497–1503.
13. Vicent D, et al. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J Clin Invest. 2003;111(9):1373–1380.
14. Konishi M, et al. Endothelial insulin receptors differentially control insulin signaling kinetics in peripheral tissues and brain of mice. Proc Natl Acad Sci U S A. 2017;114(40):E8478–E8487.
15. Albelda SM, et al. Permeability characteristics of cultured endothelial cell monolayers. J Appl Physiol. 1988;64(1):308–322.
16. Durr E, et al. Direct proteomic mapping of the lung microvascular endothelial cell surface in vivo and in cell culture. Nat Biotechnol. 2004;22(8):985–992.
17. Hentz NG, Richardson JM, Sportsman JR, Daijo J, Sittampalam GS. Synthesis and characterization of insulin-fluorescein derivatives for bioanalytical applications. AnalChem. 1997;69(24):4994–5000.
18. Chen AK, Cheng Z, Behlke MA, Tsourkas A. Assessing the sensitivity of commercially available fluorophores to the intracellular environment. AnalChem. 2008;80(19):7437–7444.
19. Berlier JE, et al. Quantitative comparison of long-wavelength Alexa Fluor dyes to Cy dyes: fluorescence of the dyes and their bioconjugates. J Histochem Cytochem. 2003;51(12):1699–1712.
20. Bagher P, Segal SS. The mouse cremaster muscle preparation for intravital imaging of the microcirculation. J Vis Exp. 2011;52(52):2874.
21. Poole DC, Musch TI, Kindig CA. In vivo microvascular structural and functional consequences of muscle length changes. Am J Physiol. 1997;272(5 pt 2):H2107–H2114.
22. Lee JF, et al. Balance of S1P1 and S1P2 signaling regulates peripheral microvascular permeability in rat cremaster muscle vasculature. Am J Physiol Heart Circ Physiol. 2009;296(1):H33–H42.
23. Magidson V, Khodjakov A. Circumventing photodamage in live-cell microscopy. Methods Cell Biol. 2013;114:545–560.
24. Otsu N. A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern. 1979;9(1):62–66.
25. Huxley VH, Curry FE, Adamson RH. Quantitative fluorescence microscopy on single capillaries: alpha-lactalbumin transport. Am J Physiol. 1987;252(1 pt 2):H188–H197.
26. Baxter LT, Jain RK. Transport of fluid and macromolecules in tumors. I. Role of interstitial pressure and convection. Microvasc Res. 1989;37(1):77–104.
27. Schäffer L, et al. A novel high-affinity peptide antagonist to the insulin receptor. Biochem Bio-phys Res Commun. 2008;376(2):380–383.
28. Lieu ZZ, Gleeson PA. Endosome-to-Golgi transport pathways in physiological processes. Histol Histopathol. 2011;26(3):395–408.
29. Sjöstrand M, Holmäng A, Lönnroth P. Measurement of interstitial insulin in human muscle. Am J Physiol. 1999;276(1 pt 1):E151–E154.
30. Yang YJ, Hope ID, Ader M, Bergman RN. Importance of transcapillary insulin transport to dynamics of insulin action after intravenous glucose. Am J Physiol. 1994;266(1 pt 1):E17–E25.
31. Lee WL, Klip A. Endothelial transcytosis of insulin: does it contribute to insulin resistance? Physiology (Bethesda). 2016;31(5):336–345.
32. Bendayan M, Rasio EA. Transport of insulin and albumin by the microvascular endothelium of the rete mirabile. JCellSci. 1996;109(pt 7):1857–1864.
33. Wang H, Wang AX, Barrett EJ. Caveolin-1 is required for vascular endothelial insulin uptake. Am J Physiol Endocrinol Metab. 2011;300(1):E134–E144.
34. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res. 2007;100(2):158–173.
35. Azizi PM, et al. Clathrin-dependent entry and vesicle-mediated exocytosis define insulin transcytosis across microvascular endothelial cells. MolBiolCell. 2015;26(4):740–750.
36. Laakso M, Edelman SV, Brechtel G, Baron AD. Decreased effect of insulin to stimulate skeletal muscle blood flow in obese man. A novel mechanism for insulin resistance. J Clin Invest. 1990;85(6):1844–1852.
37. Rattigan S, Clark MG, Barrett EJ. Hemody-namic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes. 1997;46(9):1381–1388.
38. Vincent MA, et al. Skeletal muscle microvascular recruitment by physiological hyperinsulinemia precedes increases in total blood flow. Diabetes. 2002;51(1):42–48.
39. Liu F, Kohn WD, Mayer JP. Site-specific fluo-rescein labeling of human insulin. J Pept Sci. 2012;18(5):336–341.
40. Kohn WD, et al. pI-shifted insulin analogs with extended in vivo time action and favorable receptor selectivity. Peptides. 2007;28(4):935–948.
41. Ayala JE, et al. Hyperinsulinemic-euglycemic clamps in conscious, unrestrained mice. J Vis Exp. 2011;(57):3188.
42. Ayala JE, et al. Standard operating procedures for describing and performing metabolic tests of glucose homeostasis in mice. Dis Model Mech. 2010;3(9–10):525–534.
43. Kraegen EW, James DE, Jenkins AB, Chisholm DJ. Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am J Physiol. 1985;248(3 pt 1):E353–E362.
44. Morgan CR, Lazarow A. Immunoassay of pancreatic and plasma insulin following alloxan injection of rats. Diabetes. 1965;14(10):669–671.
45. Williams IM, Otero YF, Bracy DP, Wasserman DH, Biaggioni I, Arnold AC. Chronic angioten-sin-(1-7) improves insulin sensitivity in high-fat fed mice independent of blood pressure. Hypertension. 2016;67(5):983–991.
46. Steele R, Wall JS, De Bodo RC, Altszuler N. Measurement of size and turnover rate of body glucose pool by the isotope dilution method. Am J Physiol. 1956;187(1):15–24.
47. Crank J. The Mathematics Of Diffusion. Oxford, United Kingdom: Oxford University Press; 1975.
48. Baatz H, Steinbauer M, Harris AG, Krombach F. Kinetics of white blood cell staining by intravascular administration of rhodamine 6G. Int J Microcirc Clin Exp. 1995;15(2):85–91.
49. Mempel TR, Scimone ML, Mora JR, von Andrian UH. In vivo imaging of leukocyte trafficking in blood vessels and tissues. Curr Opin Immunol. 2004;16(4):406–417.