Altered transendothelial transport of hormones as a contributor to diabetes

Diabetes and Metabolism Journal

Volumn 38, Issue 2, 2014, Pages 92-99

  Yoon, Nanyoung ^a   Dang, Thanh Q ^a   Chasiotis, Helen ^a   Kelly, Scott P ^a   Sweeney, Gary ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

Adherens junctions; Adiponectin; Endocrine; Endothelial transport; Hormones; Insulin; Paracellular; Tight junctions; Transcellular

Indexed keywords

ADIPONECTIN; GLUCOCORTICOID;

CELL MEMBRANE PERMEABILITY; CELL TRANSPORT; DIABETES MELLITUS; DIABETIC RETINOPATHY; DRUG MECHANISM; ENDOTHELIAL DYSFUNCTION; HORMONE TRANSPORT; HUMAN; LIVER; NONHUMAN; PARACELLULAR TRANSPORT; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; REVIEW; SKELETAL MUSCLE; TIGHT JUNCTION; TRANSCELLULAR CELL MIGRATION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84901501716     PISSN: 22336079     EISSN: 22336087     Source Type: Journal    
DOI: 10.4093/dmj.2014.38.2.92     Document Type: Review

References (66)

1. Pries AR, Kuebler WM. Normal endothelium. Handb Exp Pharmacol 2006;176 Pt 1:1-40.
2. Goddard LM, Iruela-Arispe ML. Cellular and molecular regulation of vascular permeability. Thromb Haemost 2013;109: 407-15.
3. Chiu JD, Kolka CM, Richey JM, Harrison LN, Zuniga E, Kirkman EL, Bergman RN. Experimental hyperlipidemia dramatically reduces access of insulin to canine skeletal muscle. Obesity (Silver Spring) 2009;17:1486-92.
4. Kolka CM, Harrison LN, Lottati M, Chiu JD, Kirkman EL, Bergman RN. Diet-induced obesity prevents interstitial dispersion of insulin in skeletal muscle. Diabetes 2010;59:619-26.
5. Chiu JD, Richey JM, Harrison LN, Zuniga E, Kolka CM, Kirkman E, Ellmerer M, Bergman RN. 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 2008;57:828-35.
6. 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:E17-25.
7. Sjostrand M, Holmang A, Lonnroth P. Measurement of interstitial insulin in human muscle. Am J Physiol 1999;276:E151-4.
8. Herkner H, Klein N, Joukhadar C, Lackner E, Langenberger H, Frossard M, Bieglmayer C, Wagner O, Roden M, Muller M. Transcapillary insulin transfer in human skeletal muscle. Eur J Clin Invest 2003;33:141-6.
9. Bodenlenz M, Schaupp LA, Druml T, Sommer R, Wutte A, Schaller HC, Sinner F, Wach P, Pieber TR. Measurement of interstitial insulin in human adipose and muscle tissue under moderate hyperinsulinemia by means of direct interstitial access. Am J Physiol Endocrinol Metab 2005;289:E296-300.
10. Maggs DG, Jacob R, Rife F, Lange R, Leone P, During MJ, Tamborlane WV, Sherwin RS. Interstitial fluid concentrations of glycerol, glucose, and amino acids in human quadricep muscle and adipose tissue: evidence for significant lipolysis in skeletal muscle. J Clin Invest 1995;96:370-7.
11. 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 Physiol Endocrinol Metab 2011;301:E252-63.
12. Gunzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev 2013;93:525-69.
13. Gunzel D, Fromm M. Claudins and other tight junction proteins. Compr Physiol 2012;2:1819-52.
14. Kolka CM, Bergman RN. The barrier within: endothelial transport of hormones. Physiology (Bethesda) 2012;27:237-47.
15. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 2007;100:158-73.
16. Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 2007;100:174-90.
17. Kim SP, Ellmerer M, Van Citters GW, Bergman RN. Primacy of hepatic insulin resistance in the development of the metabolic syndrome induced by an isocaloric moderate-fat diet in the dog. Diabetes 2003;52:2453-60.
18. Kumar P, Shen Q, Pivetti CD, Lee ES, Wu MH, Yuan SY. Molecular mechanisms of endothelial hyperpermeability: implications in inflammation. Expert Rev Mol Med 2009;11:e19.
19. Miller NE, Michel CC, Nanjee MN, Olszewski WL, Miller IP, Hazell M, Olivecrona G, Sutton P, Humphreys SM, Frayn KN. Secretion of adipokines by human adipose tissue in vivo: partitioning between capillary and lymphatic transport. Am J Physiol Endocrinol Metab 2011;301:E659-67.
20. Schubert W, Frank PG, Woodman SE, Hyogo H, Cohen DE, Chow CW, Lisanti MP. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice: treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J Biol Chem 2002; 277:40091-8.
21. Miyawaki-Shimizu K, Predescu D, Shimizu J, Broman M, Predescu S, Malik AB. siRNA-induced caveolin-1 knockdown in mice increases lung vascular permeability via the junctional pathway. Am J Physiol Lung Cell Mol Physiol 2006;290:L405-13.
22. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 2001;276:38121-38.
23. Gory-Faure S, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P. Role of vascular endothelial-cadherin in vascular morphogenesis. Development 1999;126:2093-102.
24. Orsenigo F, Giampietro C, Ferrari A, Corada M, Galaup A, Sigismund S, Ristagno G, Maddaluno L, Koh GY, Franco D, Kurtcuoglu V, Poulikakos D, Baluk P, McDonald D, Grazia Lampugnani M, Dejana E. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 2012; 3:1208.
25. Ding H, Triggle CR. Endothelial dysfunction in diabetes: multiple targets for treatment. Pflugers Arch 2010;459:977-94.
26. Symons JD, Abel ED. Lipotoxicity contributes to endothelial dysfunction: a focus on the contribution from ceramide. Rev Endocr Metab Disord 2013;14:59-68.
27. Freidenberg GR, Suter S, Henry RR, Nolan J, Reichart D, Olefsky JM. Delayed onset of insulin activation of the insulin receptor kinase in vivo in human skeletal muscle. Diabetes 1994; 43:118-26.
28. Somwar R, Kim DY, Sweeney G, Huang C, Niu W, Lador C, Ramlal T, Klip A. GLUT4 translocation precedes the stimulation of glucose uptake by insulin in muscle cells: potential activation of GLUT4 via p38 mitogen-activated protein kinase. Biochem J 2001;359:639-49.
29. Barrett EJ, Rattigan S. Muscle perfusion: its measurement and role in metabolic regulation. Diabetes 2012;61:2661-8.
30. Kubota T, Kubota N, Kumagai H, Yamaguchi S, Kozono H, Takahashi T, Inoue M, Itoh S, Takamoto I, Sasako T, Kumagai K, Kawai T, Hashimoto S, Kobayashi T, Sato M, Tokuyama K, Nishimura S, Tsunoda M, Ide T, Murakami K, Yamazaki T, Ezaki O, Kawamura K, Masuda H, Moroi M, Sugi K, Oike Y, Shimokawa H, Yanagihara N, Tsutsui M, Terauchi Y, Tobe K, Nagai R, Kamata K, Inoue K, Kodama T, Ueki K, Kadowaki T. Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab 2011; 13:294-307.
31. Kolka CM, Bergman RN. The endothelium in diabetes: its role in insulin access and diabetic complications. Rev Endocr Metab Disord 2013;14:13-9.
32. Scheid MP, Sweeney G. The role of adiponectin signaling in metabolic syndrome and cancer. Rev Endocr Metab Disord. Epub 2013 Sep 10. http://dx.doi.org/10.1007/s11154-013-9265-5.
33. Liu Y, Sweeney G. Adiponectin action in skeletal muscle. Best Pract Res Clin Endocrinol Metab 2014;28:33-41.
34. Ye R, Scherer PE. Adiponectin, driver or passenger on the road to insulin sensitivity? Mol Metab 2013;2:133-41.
35. Park M, Sweeney G. Direct effects of adipokines on the heart: focus on adiponectin. Heart Fail Rev 2013;18:631-44.
36. Kubota N, Yano W, Kubota T, Yamauchi T, Itoh S, Kumagai H, Kozono H, Takamoto I, Okamoto S, Shiuchi T, Suzuki R, Satoh H, Tsuchida A, Moroi M, Sugi K, Noda T, Ebinuma H, Ueta Y, Kondo T, Araki E, Ezaki O, Nagai R, Tobe K, Terauchi Y, Ueki K, Minokoshi Y, Kadowaki T. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab 2007;6:55-68.
37. Neumeier M, Weigert J, Buettner R, Wanninger J, Schaffler A, Muller AM, Killian S, Sauerbruch S, Schlachetzki F, Steinbrecher A, Aslanidis C, Scholmerich J, Buechler C. Detection of adiponectin in cerebrospinal fluid in humans. Am J Physiol Endocrinol Metab 2007;293:E965-9.
38. Kusminski CM, McTernan PG, Schraw T, Kos K, O'Hare JP, Ahima R, Kumar S, Scherer PE. Adiponectin complexes in human cerebrospinal fluid: distinct complex distribution from serum. Diabetologia 2007;50:634-42.
39. Nielsen NB, Hojbjerre L, Sonne MP, Alibegovic AC, Vaag A, Dela F, Stallknecht B. Interstitial concentrations of adipokines in subcutaneous abdominal and femoral adipose tissue. Regul Pept 2009;155:39-45.
40. Hojbjerre L, Rosenzweig M, Dela F, Bruun JM, Stallknecht B. Acute exercise increases adipose tissue interstitial adiponectin concentration in healthy overweight and lean subjects. Eur J Endocrinol 2007;157:613-23.
41. Murdolo G, Hammarstedt A, Schmelz M, Jansson PA, Smith U. Acute hyperinsulinemia differentially regulates interstitial and circulating adiponectin oligomeric pattern in lean and insulin-resistant, obese individuals. J Clin Endocrinol Metab 2009; 94:4508-16.
42. Omran OM. Effects of thymoquinone on STZ-induced diabetic nephropathy: an immunohistochemical study. Ultrastruct Pathol 2014;38:26-33.
43. Shan CY, Yang JH, Kong Y, Wang XY, Zheng MY, Xu YG, Wang Y, Ren HZ, Chang BC, Chen LM. Alteration of the intestinal barrier and GLP2 secretion in Berberine-treated type 2 diabetic rats. J Endocrinol 2013;218:255-62.
44. Shin JY, Sohn J, Park KH. Chlorogenic acid decreases retinal vascular hyperpermeability in diabetic rat model. J Korean Med Sci 2013;28:608-13.
45. Bhattacharjee PS, Huq TS, Potter V, Young A, Davenport IR, Graves R, Mandal TK, Clement C, McFerrin HE, Muniruzzaman S, Ireland SK, Hill JM. High-glucose-induced endothelial cell injury is inhibited by a Peptide derived from human apolipoprotein E. PLoS One 2012;7:e52152.
46. Liu C, Wu J, Zou MH. Activation of AMP-activated protein kinase alleviates high-glucose-induced dysfunction of brain microvascular endothelial cell tight-junction dynamics. Free Radic Biol Med 2012;53:1213-21.
47. Rincon-Choles H, Vasylyeva TL, Pergola PE, Bhandari B, Bhandari K, Zhang JH, Wang W, Gorin Y, Barnes JL, Abboud HE. ZO-1 expression and phosphorylation in diabetic nephropathy. Diabetes 2006;55:894-900.
48. Antonetti DA, Barber AJ, Khin S, Lieth E, Tarbell JM, Gardner TW. Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content: vascular endothelial growth factor decreases occludin in retinal endothelial cells: Penn State Retina Research Group. Diabetes 1998;47: 1953-9.
49. Barber AJ, Antonetti DA, Gardner TW. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes: the Penn State Retina Research Group. Invest Ophthalmol Vis Sci 2000;41:3561-8.
50. Gow A, Southwood CM, Li JS, Pariali M, Riordan GP, Brodie SE, Danias J, Bronstein JM, Kachar B, Lazzarini RA. CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 1999;99:649-59.
51. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 2000;11:4131-42.
52. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 2002;156:1099-111.
53. Ben-Yosef T, Belyantseva IA, Saunders TL, Hughes ED, Kawamoto K, Van Itallie CM, Beyer LA, Halsey K, Gardner DJ, Wilcox ER, Rasmussen J, Anderson JM, Dolan DF, Forge A, Raphael Y, Camper SA, Friedman TB. Claudin 14 knockout mice, a model for autosomal recessive deafness DFNB29, are deaf due to cochlear hair cell degeneration. Hum Mol Genet 2003; 12:2049-61.
54. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, Furuse M, Tsukita S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 2003;161:653-60.
55. Miyamoto T, Morita K, Takemoto D, Takeuchi K, Kitano Y, Miyakawa T, Nakayama K, Okamura Y, Sasaki H, Miyachi Y, Furuse M, Tsukita S. Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice. J Cell Biol 2005;169:527-38.
56. Tamura A, Kitano Y, Hata M, Katsuno T, Moriwaki K, Sasaki H, Hayashi H, Suzuki Y, Noda T, Furuse M, Tsukita S, Tsukita S. Megaintestine in claudin-15-deficient mice. Gastroenterology 2008;134:523-34.
57. Nakano Y, Kim SH, Kim HM, Sanneman JD, Zhang Y, Smith RJ, Marcus DC, Wangemann P, Nessler RA, Banfi B. A claudin-9-based ion permeability barrier is essential for hearing. PLoS Genet 2009;5:e1000610.
58. Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, Furuse K, Sasaki H, Fujimura A, Imai M, Kusano E, Tsukita S, Furuse M. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci U S A 2010;107:8011-6.
59. Tatum R, Zhang Y, Salleng K, Lu Z, Lin JJ, Lu Q, Jeansonne BG, Ding L, Chen YH. Renal salt wasting and chronic dehydration in claudin-7-deficient mice. Am J Physiol Renal Physiol 2010;298:F24-34.
60. Will C, Breiderhoff T, Thumfart J, Stuiver M, Kopplin K, Sommer K, Gunzel D, Querfeld U, Meij IC, Shan Q, Bleich M, Willnow TE, Muller D. Targeted deletion of murine Cldn16 identifies extra- and intrarenal compensatory mechanisms of Ca2+ and Mg2+ wasting. Am J Physiol Renal Physiol 2010;298:F1152-61.
61. Hayashi D, Tamura A, Tanaka H, Yamazaki Y, Watanabe S, Suzuki K, Suzuki K, Sentani K, Yasui W, Rakugi H, Isaka Y, Tsukita S. Deficiency of claudin-18 causes paracellular H+ leakage, up-regulation of interleukin-1ß, and atrophic gastritis in mice. Gastroenterology 2012;142:292-304.
62. Fujita H, Hamazaki Y, Noda Y, Oshima M, Minato N. Claudin-4 deficiency results in urothelial hyperplasia and lethal hydronephrosis. PLoS One 2012;7:e52272.
63. Wada M, Tamura A, Takahashi N, Tsukita S. Loss of claudins 2 and 15 from mice causes defects in paracellular Na+ flow and nutrient transport in gut and leads to death from malnutrition. Gastroenterology 2013;144:369-80.
64. Gonzalez-Mariscal L, Hernandez S, Vega J. Inventions designed to enhance drug delivery across epithelial and endothelial cells through the paracellular pathway. Recent Pat Drug Deliv Formul 2008;2:145-76.
65. Deli MA. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim Biophys Acta 2009;1788:892-910.
66. Felinski EA, Antonetti DA. Glucocorticoid regulation of endothelial cell tight junction gene expression: novel treatments for diabetic retinopathy. Curr Eye Res 2005;30:949-57.