Caveolin-1 phosphorylation regulates vascular endothelial insulin uptake and is impaired by insulin resistance in rats

Diabetologia

Volumn 58, Issue 6, 2015, Pages 1344-1353

  Wang, Hong ^a   Wang, Aileen X ^a   Aylor, Kevin ^a   Barrett, Eugene J ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

Caveolin 1; Endothelial cells; IL 6; Insulin uptake; TNF ; Tyrosine phosphorylation

Indexed keywords

CAV1 PROTEIN, RAT; CAVEOLIN 1; CSK TYROSINE-PROTEIN KINASE; INSULIN; INTERLEUKIN 6; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR; TYROSINE;

ANIMAL; CHEMISTRY; CYTOLOGY; ENDOTHELIUM CELL; FLUORESCENCE MICROSCOPY; INSULIN RESISTANCE; LIPID DIET; MALE; METABOLISM; PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; CAVEOLIN 1; DIET, HIGH-FAT; ENDOTHELIAL CELLS; INSULIN; INSULIN RESISTANCE; INTERLEUKIN-6; MALE; MICROSCOPY, FLUORESCENCE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE;

EID: 84939965994     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3546-3     Document Type: Article

References (54)

1. Yang YJ, Hope ID, Ader M, Bergman RN (1989) Insulin transport across capillaries is rate limiting for insulin action in dogs. J Clin Invest 84:1620–1628
2. Miles PD, Li S, Hart M et al (1998) Mechanisms of insulin resistance in experimental hyperinsulinemic dogs. J Clin Invest 101:202–211
3. Sjostrand M, Gudbjornsdottir S, Holmang A, Lonn L, Strindberg L, Lonnroth P (2002) Delayed transcapillary transport of insulin to muscle interstitial fluid in obese subjects. Diabetes 51:2742–2748
4. Simionescu M, Simionescu N, Palade GE (1974) Morphometric data on the endothelium of blood capillaries. J Cell Biol 60:128–152
5. Predescu D, Palade GE (1993) Plasmalemmal vesicles represent the large pore system of continuous microvascular endothelium. Am J Physiol 265:H725–H733
6. Pelkmans L, Zerial M (2005) Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436:128–133
7. Oh P, Borgstrom P, Witkiewicz H et al (2007) Live dynamic imaging of caveolae pumping targeted antibody rapidly and specifically across endothelium in the lung. Nat Biotechnol 25:327–337
8. Drab M, Verkade P, Elger M et al (2001) Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449–2452
9. Okamoto T, Schlegel A, Scherer PE, Lisanti MP (1998) Caveolins, a family of scaffolding proteins for organizing “preassembled signaling complexes” at the plasma membrane. J Biol Chem 273:5419–5422
10. Tiruppathi C, Song W, Bergenfeldt M, Sass P, Malik AB (1997) Gp60 activation mediates albumin transcytosis in endothelial cells by tyrosine kinase-dependent pathway. J Biol Chem 272:25968–25975
11. Aoki T, Nomura R, Fujimoto T (1999) Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 253:629–636
12. King GL, Johnson SM (1985) Receptor-mediated transport of insulin across endothelial cells. Science 227:1583–1586
13. Wang H, Liu Z, Li G, Barrett EJ (2006) The vascular endothelial cell mediates insulin transport into skeletal muscle. Am J Physiol Endocrinol Metab 291:E323–E332
14. Wang H, Wang AX, Barrett EJ (2011) Caveolin-1 is required for vascular endothelial insulin uptake. Am J Physiol Endocrinol Metab 300:E134–E144
15. Wang H, Wang AX, Liu Z, Barrett EJ (2008) Insulin signaling stimulates insulin transport by bovine aortic endothelial cells. Diabetes 57:540–547
16. Wang H, Wang AX, Aylor K, Barrett EJ (2013) Nitric oxide directly promotes vascular endothelial insulin transport. Diabetes 62:4030–4042
17. Zhang L, Wheatley CM, Richards SM, Barrett EJ, Clark MG, Rattigan S (2003) TNF-alpha acutely inhibits vascular effects of physiological but not high insulin or contraction. Am J Physiol Endocrinol Metab 285:E654–E660
18. Li G, Barrett EJ, Barrett MO, Cao W, Liu Z (2007) Tumor necrosis factor-alpha induces insulin resistance in endothelial cells via a p38 mitogen-activated protein kinase-dependent pathway. Endocrinology 148:3356–3363
19. Lee H, Volonte D, Galbiati F et al (2000) Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol Endocrinol 14:1750–1775
20. Kraegen EW, Clark PW, Jenkins AB, Daley EA, Chisholm DJ, Storlien LH (1991) Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes 40:1397–1403
21. Brons C, Jensen CB, Storgaard H et al (2009) Impact of short-term high-fat feeding on glucose and insulin metabolism in young healthy men. J Physiol 587:2387–2397
22. Wang H, Wang AX, Barrett EJ (2012) Insulin-induced endothelial cell cortical actin filament remodeling: a requirement for trans-endothelial insulin transport. Mol Endocrinol 26:1327–1338
23. Wang H, Wang AX, Liu Z, Chai W, Barrett EJ (2009) The trafficking/interaction of eNOS and caveolin-1 induced by insulin modulates endothelial nitric oxide production. Mol Endocrinol 23:1613–1623
24. del Pozo MA, Balasubramanian N, Alderson NB et al (2005) Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 7:901–908
25. Roskoski R Jr (2005) Src kinase regulation by phosphorylation and dephosphorylation. Biochem Biophys Res Commun 331:1–14
26. Xu W, Harrison SC, Eck MJ (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385:595–602
27. Schaffer L, Brand CL, Hansen BF et al (2008) A novel high-affinity peptide antagonist to the insulin receptor. Biochem Biophys Res Commun 376:380–383
28. Yi P, Park JS, Melton DA (2013) Betatrophin: a hormone that controls pancreatic beta cell proliferation. Cell 153:747–758
29. Genders AJ, Frison V, Abramson SR, Barrett EJ (2013) Endothelial cells actively concentrate insulin during its transendothelial transport. Microcirculation 20:434–439
30. Rotter V, Nagaev I, Smith U (2003) Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 278:45777–45784
31. Glenney JR Jr (1989) Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus. J Biol Chem 264:20163–20166
32. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68:673–682
33. Volonte D, Galbiati F, Pestell RG, Lisanti MP (2001) Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr(14)) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J Biol Chem 276:8094–8103
34. Kimura A, Mora S, Shigematsu S, Pessin JE, Saltiel AR (2002) The insulin receptor catalyzes the tyrosine phosphorylation of caveolin-1. J Biol Chem 277:30153–30158
35. Tao J, Malbon CC, Wang HY (2001) Insulin stimulates tyrosine phosphorylation and inactivation of protein-tyrosine phosphatase 1B in vivo. J Biol Chem 276:29520–29525
36. Dadke S, Chernoff J (2003) Protein-tyrosine phosphatase 1B mediates the effects of insulin on the actin cytoskeleton in immortalized fibroblasts. J Biol Chem 278:40607–40611
37. Chen Z, Bakhshi FR, Shajahan AN et al (2012) Nitric oxide-dependent Src activation and resultant caveolin-1 phosphorylation promote eNOS/caveolin-1 binding and eNOS inhibition. Mol Biol Cell 23:1388–1398
38. Montesano R, Roth J, Robert A, Orci L (1982) Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296:651–653
39. Pelkmans L, Fava E, Grabner H et al (2005) Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436:78–86
40. Minshall RD, Tiruppathi C, Vogel SM et al (2000) Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol 150:1057–1070
41. Herkner H, Klein N, Joukhadar C et al (2003) Transcapillary insulin transfer in human skeletal muscle. Eur J Clin Investig 33:141–146
42. 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
43. Bar RS, Boes M, Dake BL, Booth BA, Henley SA, Sandra A (1988) Insulin, insulin-like growth factors, and vascular endothelium. Am J Med 85:59–70
44. Li G, Barrett EJ, Wang H, Chai W, Liu Z (2005) Insulin at physiological concentrations selectively activates insulin but not insulin-like growth factor I (IGF-I) or insulin/IGF-I hybrid receptors in endothelial cells. Endocrinology 146:4690–4696
45. 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 Metab 301:E252–E263
46. Kolka CM, Bergman RN (2012) The barrier within: endothelial transport of hormones. Physiology (Bethesda) 27:237–247
47. Vicent D, Ilany J, Kondo T et al (2003) The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J Clin Invest 111:1373–1380
48. Kubota T, Kubota N, Kumagai H et al (2011) Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab 13:294–307
49. Shajahan AN, Timblin BK, Sandoval R, Tiruppathi C, Malik AB, Minshall RD (2004) Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells. J Biol Chem 279:20392–20400
50. Gottlieb-Abraham E, Shvartsman DE, Donaldson JC et al (2013) Src-mediated caveolin-1 phosphorylation affects the targeting of active Src to specific membrane sites. Mol Biol Cell 24:3881–3895
51. Schnitzer JE, Liu J, Oh P (1995) Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J Biol Chem 270:14399–14404
52. Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM (1994) Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci U S A 91:4854–4858
53. Klover PJ, Zimmers TA, Koniaris LG, Mooney RA (2003) Chronic exposure to interleukin-6 causes hepatic insulin resistance in mice. Diabetes 52:2784–2789
54. Kim F, Pham M, Maloney E et al (2008) Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler Thromb Vasc Biol 28:1982–1988