Induction of endoplasmic reticulum stress impairs insulin-stimulated vasomotor relaxation in rat aortic rings: Role of endothelin-1

Journal of Physiology and Pharmacology

Volumn 64, Issue 5, 2013, Pages 557-564

  Padilla, J ^a,b   Jenkins, N T ^c  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Endoplasmic reticulum stress; Endothelial function; Endothelin 1; Tunicamycin; Unfolded protein response; Vascular insulin resistance

Indexed keywords

ACETYLCHOLINE; ENDOTHELIN 1; ENDOTHELIN 1 RECEPTOR; ENDOTHELIN RECEPTOR; INSULIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TEZOSENTAN; TUNICAMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; FEMALE; IMMUNOBLOTTING; IN VITRO STUDY; NONHUMAN; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR RING; VASODILATATION; VASOMOTOR REFLEX;

ANIMALS; AORTA, THORACIC; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL CELLS; ENDOTHELIN-1; FEMALE; INSULIN; RATS; RATS, WISTAR; VASODILATION;

EID: 84888210043     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Muniyappa R, Sowers JR. Role of insulin resistance in endothelial dysfunction. Rev Endocr Metab Disord 2013; 14: 5-12.
2. Mather KJ, Steinberg HO, Baron AD. Insulin resistance in the vasculature. J Clin Invest 2013; 123: 1003-1004.
3. Bender SB, McGraw AP, Jaffe IZ, Sowers JR. Mineralocorticoid receptor-mediated vascular insulin resistance: an early contributor to diabetes-related vascular disease? Diabetes 2013; 62: 313-319.
4. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010; 140: 900-917.
5. Ni M, Lee AS. ER chaperones in mammalian development and human diseases. FEBS Lett 2007; 581: 3641-3651.
6. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 2007; 9: 2277-2293.
7. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74: 739-789.
8. Hummasti S, Hotamisligil GS. Endoplasmic reticulum stress and inflammation in obesity and diabetes. Circ Res 2010; 107: 579-591.
9. Eizirik DL, Cardozo AK, Cnop M. The role of endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008; 29: 42-61.
10. Hotamisligil GS. Endoplasmic reticulum stress and atherosclerosis. Nat Med 2010; 16: 396-399.
11. Cao SS, Kaufman RJ. Targeting endoplasmic reticulum stress in metabolic disease. Expert Opin Ther Targets 2013; 17: 437-448.
12. Flamment M, Hajduch E, Ferre P, Foufelle F. New insights into ER stress-induced insulin resistance. Trends Endocrinol Metab 2012; 23: 381-390.
13. Fu S, Watkins SM, Hotamisligil GS. The role of endoplasmic reticulum in hepatic lipid homeostasis and stress signaling. Cell Metab 2012; 15: 623-634.
14. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 2011; 29: 415-445.
15. Kaplon R, Chung E, Reese L, Cox-York K, Seals DR, Gentile CL. Activation of the unfolded protein response in vascular endothelial cells of nondiabetic obese adults. J Clin Endocrinol Metab 2013; 98: E1505-E1509.
16. Kawasaki N, Asada R, Saito A, Kanemoto S, Imaizumi K. Obesity-induced endoplasmic reticulum stress causes chronic inflammation in adipose tissue. Sci Rep 2012; 2: 799.
17. Pagliassotti MJ. Endoplasmic reticulum stress in nonalcoholic fatty liver disease. Annu Rev Nutr 2012; 32: 17-33.
18. Lastra G, Manrique C, McFarlane S, Sowers J. Cardiometabolic syndrome and chronic kidney disease. Curr Diab Rep 2006; 6: 207-212.
19. Boden G, Duan X, Homko C, et al. Increase in endplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 2008; 57: 2438-2444.
20. Bakker W, Eringa EC, Sipkema P, van Hinsbergh VWM. Endothelial dysfunction and diabetes: roles of hyperglycemia, impaired insulin signaling and obesity. Cell Tissue Res 2009; 335: 165-189.
21. Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res 2010; 107: 839-850.
22. Civelek M, Manduchi E, Riley RJ, Stoeckert CJ, Davies PF. Coronary artery endothelial transcriptome in vivo: identification of endoplasmic reticulum stress and enhanced reactive oxygen species by gene connectivity network analysis. Circ Cardiovasc Genet 2011; 4: 243-252.
23. Civelek M, Manduchi E, Riley RJ, Stoeckert CJ, Davies PF. Chronic endoplasmic reticulum stress activates unfolded protein reponse in arterial endothelium in regions of suceptibility to atherosclerosis. Circ Res 2009; 105: 453-461.
24. Davies PF, Civelek M. Endoplasmic reticulum stress, redox, and a proinflammatory environment in athero-susceptible endothelium in vivo at sites of complex hemodynamics shear stress. Antioxid Redox Signal 2011; 15: 1427-1432.
25. Gargalovic PS, Gharavi NM, Clark MJ, et al. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 2006; 26: 2490-2496.
26. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008; 454: 455-462.
27. Kassan M, Galan M, Partyka M, et al. Endoplasmic reticulum stress is involved in cardiac damage and vascular endothelial dysfunction in hypertensive mice. Arterioscler Thromb Vasc Biol 2012; 32: 1652-1661.
28. Hua Y, Kandadi MR, Zhu M, Ren J, Sreejayan N. Tauroursodeoxycholic acid attenuates lipid accumulation in endoplasmic reticulum-stressed macrophages. J Cardiovasc Pharmacol 2010; 55: 49-55.
29. Berger E, Haller D. Structure-function analysis of the tertiary bile acid TUDCA for the resolution of endoplasmic reticulum stress in intestinal epithelial cells. Biochem Biophys Res Commun 2011; 409: 610-615.
30. Li J, Wang JJ, Zhang SX. Preconditioning with endoplasmic reticulum stress mitigates retinal endothelial inflammation via activation of X-box binding protein 1. J Biol Chem 2011; 286: 4912-4921.
31. Chen Y, Wang JJ, Li J, et al. Activating transcriptional factor 4 mediates hyperglycemia-induced endothelial inflammation and retinal vascular leakage through activation of STAT3 in a mouse model of type 1 diabetes. Diabetologia 2012; 55: 2533-2545.
32. Ozcan L, Ergin AS, Lu A, et al. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab 2009; 9: 35-51.
33. Cacanyiova S, Dovinova I, Kristek F. The role of oxidative stress in acetylcholine-induced relaxation of endothelium-denuded arteries. J Physiol Pharmacol 2013; 64: 241-247.
34. Gourdin M, Ponchau O, Jamart J, De Kock M. Aging influences the effect of pre-hypoxic administration of clonidine, an alpha 2-adrenoceptor agonist, on post-hypoxic vasomotricity. J Physiol Pharmacol 2012; 63: 165-171.
35. Bauer V, Sotnikova R, Drabikova K. Effects of activated neutrophils on isolated rings of rat thoracic aorta. J Physiol Pharmacol 2011; 62: 513-520.
36. Bunker A, Arce-Esquivel AA, Rector RS, Booth FW, Ibdah JA, Laughlin MH. Physical activity maintains aortic endothelium dependent relaxation in the obese, type 2 diabetic OLETF rat. Am J Physiol Heart Circ Physiol 2010; 298: H1889-H1901.
37. Padilla J, Newcomer SC, Simmons GH, Kreutzer K V, Laughlin MH. Long-term exercise training does not alter brachial and femoral artery vasomotor function and endothelial phenotype in healthy pigs. Am J Physiol Heart Circ Physiol 2010; 299: H379-H385.
38. Padilla J, Jenkins NT, Lee S, et al. Vascular transcriptional alterations produced by juvenile obesity in Ossabaw swine. Physiol Genomics 2013; 45: 434-446.
39. Padilla J, Jenkins NT, Roberts MD, et al. Differential changes in vascular mRNA levels between rat iliac and renal arteries produced by cessation of voluntary running. Exp Physiol 2013; 98: 337-347.
40. Padilla J, Jenkins NT, Vieira-Potter VJ, Laughlin MH. Divergent phenotype of rat thoracic and abdominal perivascular adipose tissues. Am J Physiol Regul Integr Comp Physiol 2013; 304: R543-R552.
41. Mikus CR, Roseguini BT, Uptergrove GM, et al. Voluntary wheel running selectively augments insulin-stimulated vasodilation in arterioles from white skeletal muscle of insulin-resistant rats. Microcirculation 2012; 19: 729-738.
42. Pinhas-Hamiel O, Zeitler P. The global spread of type 2 diabetes mellitus in children and adolescents. J Pediatr 2005; 146: 693-700.
43. Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in U.S. children and adolescents, 2007-2008. JAMA 2010; 303: 242-249.
44. Misurski DA, Wu SQ, McNeill JR, Wilson TW, Gopalakrishnan V. Insulin-induced biphasic responses to rat mesenteric vascular bed: rol of endothelin. Hypertension 2001; 37: 1298-1302.
45. Martin JS, Padilla J, Jenkins NT, et al. Functional adaptations in the skeletal muscle microvasculature to endurance and interval sprint training in the type 2 diabetic OLETF rat. J Appl Physiol 2012; 113: 1223-1232.
46. Eringa EC, Stehouwer CD, Roos MH, Westerhof N, Sipkema P. Selective resistance to vasoactive effects of insulin in muscle resistance arteries of obese Zucker (fa/fa) rats. Am J Physiol Endocrinol Metab 2007; 293: E1134-E1139.
47. Galan M, Kassan M, Choi SK, et al. A novel role for epidermal growth factor receptor tyrosine kinase and its downstream endoplasmic reticulum stress in cardiac damage and microvascular dysfunction in type 1 diabetes mellitus. Hypertension 2012; 60: 71-80.
48. Zhou Q G, Fu XJ, Xu GY, et al. Vascular insulin resistance related to endoplasmic reticulum stress in aortas from a rat model of chronic kidney disease. Am J Physiol Heart Circ Physiol 2012; 303: H1154-H1165.
49. Zhao Y, Tian T, Huang T, et al. Subtilase cytotoxin activates MAP kinases through PERK and IRE1 branches of the unfolded protein response. Toxicol Sci 2011; 120: 79-86.
50. Chin TY, Lin HC, Kuo JP, Chueh SH. Dual effect of thapsigargin on cell death in porcine aortic smooth muscle cells. Am J Physiol Cell Physiol 2007; 292: C383-C395.
51. Pernow J, Shemyakin A, Bohm F. New perspectives on endothelin-1 in atherosclerosis and diabetes mellitus. Life Sci 2012; 91: 507-516.
52. Browatzki M, Schmidt J, Kubler W, Kranzhofer R. Endothelin-1 induces interleukin-6 release via activation of the transcription factor NF-kappaB in human vascular smooth muscle cells. Basic Res Cardiol 2000; 95: 98-105.
53. Dong F, Zhang X, Wold LE, Ren Q, Zhang Z, Ren J. Endothelin-1 enhances oxidative stress, cell proliferation and reduces apoptosis in human umbilical vein endothelial cells: role of ETB receptor, NADPH oxidase and caveolin-1. Br J Pharmacol 2005; 145: 323-333.
54. Jain A, Olovsson M, Burton GJ, Yung HW. Endothelin-1 induces endoplasmic reticulum stress by activating the PLC-IP(3) pathway: implications for placental pathophysiology in preeclampsia. Am J Pathol 2012; 180: 2309-2320.
55. Sheikh-Ali M, Sultan S, Alamir A, Hass M, Mooradian A. Hyperglycemia-induced endoplasmic reticulum stress in endothelial cells. Nutrition 2010; 26: 1146-1150.
56. Roy A, Kolattukudy PE. Monocyte chemotactic protein-induced protein (MCPIP) promotes inflammatory angiogenesis via sequential induction of oxidative stress, endoplasmic reticulum stress and autophagy. Cell Signal 2012; 24: 2123-2131.
57. Kharroubi I, Ladriere L, Cardozo AK, Dogusan Z, Cnop M, Eizirik DL. Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress. Endocrinology 2004; 145: 5087-5096.
58. Lu Y, Qian L, Zhang Q, et al. Palmitate induces apoptosis in mouse aortic endothelial cells and endothelial dysfunction in mice fed high-calorie and high-cholesterol diets. Life Sci 2013; 92: 1165-1173.