A potential role for insulin resistance in experimental pulmonary hypertension

European Respiratory Journal

Volumn 41, Issue 4, 2013, Pages 861-871

  West, James ^a   Niswender, Kevin D ^a   Johnson, Jennifer A ^a   Pugh, Meredith E ^a   Gleaves, Linda ^a   Fessel, Joshua P ^a   Hemnes, Anna R ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Dexamethasone; Glucocorticoid; Homeostatic model assessment of insulin resistance; Insulin resistance; Mouse model; Pulmonary hypertension

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CCAAT ENHANCER BINDING PROTEIN DELTA; DEXAMETHASONE; DOXYCYCLINE; GLUCOCORTICOID RECEPTOR; I KAPPA B KINASE BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; CELL DIFFERENTIATION; CONTROLLED STUDY; ENERGY BALANCE; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; IMMUNOCYTOCHEMISTRY; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTOLIC BLOOD PRESSURE; WEIGHT GAIN;

ANIMALS; BODY COMPOSITION; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; CELL LINE; DEXAMETHASONE; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; HUMANS; HYPERTENSION, PULMONARY; INSULIN RESISTANCE; MALE; MICE; MICE, TRANSGENIC; MUTATION; PHENOTYPE; PROTEIN TRANSPORT; RATS; RECEPTORS, GLUCOCORTICOID;

EID: 84875862818     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00030312     Document Type: Article

References (56)

1. Farber HW, Loscalzo J. Pulmonary arterial hypertension. N Engl J Med 2004; 351: 1655-1665.
2. Simonneau G, Robbins IM, Beghetti M, et al. Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol 2009; 54: Suppl. 1, S43-S54.
3. Humbert M, Sitbon O, Chaouat A, et al. Survival in patients with idiopathic, familial, and anorexigen-associated pulmonary arterial hypertension in the modern management era. Circulation 2010; 122: 156-163.
4. Pugh ME, Robbins IM, Rice TW, et al. Unrecognized glucose intolerance is common in pulmonary arterial hypertension. J Heart Lung Transplant 2011; 30: 904-911.
5. Zamanian RT, Hansmann G, Snook S, et al. Insulin resistance in pulmonary arterial hypertension. Eur Respir J 2009; 33: 318-324.
6. Xu W, Koeck T, Lara AR, et al. Alterations of cellular bioenergetics in pulmonary artery endothelial cells. Proc Natl Acad Sci USA 2007; 104: 1342-1347.
7. Heresi GA, Aytekin M, Newman J, et al. Plasma levels of highdensity lipoprotein cholesterol and outcomes in pulmonary arterial hypertension. Am J Respir Crit Care Med 2010; 182: 661-668.
8. Austin ED, Phillips JA, Cogan JD, et al. Truncating and missense BMPR2 mutations differentially affect the severity of heritable pulmonary arterial hypertension. Respir Res 2009; 10: 87.
9. Machado RD, Eickelberg O, Elliott CG, et al. Genetics and genomics of pulmonary arterial hypertension. J Am Coll Cardiol 2009; 54: Suppl. 1, S32-S42.
10. Dewachter L, Adnot S, Guignabert C, et al. Bone morphogenetic protein signalling in heritable versus idiopathic pulmonary hypertension. Eur Respir J 2009; 34: 1100-1110.
11. Aldred MA, Comhair SA, Varella-Garcia M, et al. Somatic chromosome abnormalities in the lungs of patients with pulmonary arterial hypertension. Am J Respir Crit Care Med 2010; 182: 1153-1160.
12. Schleinitz D, Kloting N, Bottcher Y, et al. Genetic and evolutionary analyses of the human bone morphogenetic protein receptor 2 (BMPR2) in the pathophysiology of obesity. PLoS One 2011; 6: e16155.
13. Syed AA, Halpin CG, Irving JA, et al. A common intron 2 polymorphism of the glucocorticoid receptor gene is associated with insulin resistance in men. Clin Endocrinol (Oxf) 2008; 68: 879-884.
14. Syed AA, Redfern CP, Weaver JU. In vivo and in vitro glucocorticoid sensitivity in obese people with cushingoid appearance. Obesity (Silver Spring) 2008; 16: 2374-2378.
15. Walker BR. Abnormal glucocorticoid activity in subjects with risk factors for cardiovascular disease. Endocr Res 1996; 22: 701-708.
16. Donn R, Berry A, Stevens A, et al. Use of gene expression profiling to identify a novel glucocorticoid sensitivity determining gene, BMPRII. FASEB J 2007; 21: 402-414.
17. Hayashi K, Yamaguchi T, Yano S, et al. BMP/Wnt antagonists are upregulated by dexamethasone in osteoblasts and reversed by alendronate and PTH: potential therapeutic targets for glucocorticoidinduced osteoporosis. BiochemBiophys Res Commun 2009; 379: 261-266.
18. Luppen CA, Chandler RL, Noh T, et al. BMP-2 vs. BMP-4 expression and activity in glucocorticoid-arrested MC3T3-E1 osteoblasts: Smad signaling, not alkaline phosphatase activity, predicts rescue of mineralization. Growth Factors 2008; 26: 226-237.
19. Moral-Sanz J, Menendez C, Moreno L, et al. Pulmonary arterial dysfunction in insulin resistant obese Zucker rats. Respir Res 2011; 12: 51.
20. Hansmann G, de Jesus Perez VA, Alastalo TP, et al. An antiproliferative BMP-2/PPARgamma/apoE axis in human and murine SMCs and its role in pulmonary hypertension. J Clin Invest 2008; 118: 1846-1857.
21. Hansmann G, Wagner RA, Schellong S, et al. Pulmonary arterial hypertension is linked to insulin resistance and reversed by peroxisome proliferator-activated receptor-gamma activation. Circulation 2007; 115: 1275-1284.
22. West J, Fagan K, Steudel W, et al. Pulmonary hypertension in transgenic mice expressing a dominant-negative BMPRII gene in smooth muscle. Circ Res 2004; 94: 1109-1114.
23. West J, Harral J, Lane K, et al. Mice expressing BMPR2R899X transgene in smooth muscle develop pulmonary vascular lesions. Am J Physiol Lung Cell Mol Physiol 2008; 295: L744-755.
24. Yasuda T, Tada Y, Tanabe N, et al. Rho-kinase inhibition alleviates pulmonary hypertension in transgenic mice expressing a dominant-negative type II bone morphogenetic protein receptor gene. Am J Physiol Lung Cell Mol Physiol 2011; 301: L667-L674.
25. Johnson JA, Hemnes AR, Perrien DS, et al. Cytoskeletal defects in Bmpr2-associated pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 2012; 302: L474-L484.
26. Mather K. Surrogate measures of insulin resistance: of rats, mice, and men. Am J Physiol Endocrinol Metab 2009; 296: E398-E399.
27. Spurney CF, Knoblach S, Pistilli EE, et al. Dystrophin-deficient cardiomyopathy in mouse: expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul Disord 2008; 18: 371-381.
28. Tanaka N, Dalton N, Mao L, et al. Transthoracic echocardiography in models of cardiac disease in themouse. Circulation 1996; 94: 1109-1117.
29. Postic C, Shiota M, Niswender KD, et al. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J Biol Chem 1999; 274: 305-315.
30. Lane K, Talati M, Austin E, et al. Oxidative injury is a common consequence of BMPR2 mutations. Pulm Circ 2011; 1: 72-83.
31. Majka S, Hagen M, Blackwell T, et al. Physiologic and molecular consequences of endothelial Bmpr2 Mutation. Respir Res 2011; 12: 84.
32. Pan DA, Lillioja S, Kriketos AD, et al. Skeletal muscle triglyceride levels are inversely related to insulin action.Diabetes 1997; 46: 983-988.
33. Krssak M, Falk Petersen K, Dresner A, et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 1999; 42: 113-116.
34. Samuel VT, Petersen KF, Shulman GI. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 2010; 375: 2267-2277.
35. Vessby B. Dietary fat and insulin action in humans. Br J Nutr 2000; 83: Suppl. 1, S91-s96.
36. Fryer LG, Kruszynska YT. Insulin resistance in high fat fed rats. Role of glucose transporters, membrane lipids, and triglyceride stores. Ann N Y Acad Sci 1993; 683: 91-97.
37. Mendelson CR, ed. Endocrinology of the Lung. 1st Edn. New York, Humana Press, 2000.
38. Robbins IM, Newman JH, Johnson RF, et al. Association of the metabolic syndrome with pulmonary venous hypertension. Chest 2009; 136: 31-36.
39. Pugh ME, Hemnes AR. Metabolic and hormonal derangements in pulmonary hypertension: from mouse to man. Int J Clin Pract Suppl 2010; 168: 5-13.
40. Austin ED, Menon S, Hemnes AR, et al. Idiopathic and heritable PAH perturb common molecular pathways, correlated with increased MSX1 expression. Pulm Circ 2011; 1: 389-398.
41. Newman JH, Wheeler L, Lane KB. Mutation in the gene for bone morphogenetic protein receptor II as a cause of primary pulmonary hypertension in a large kindred. N Engl J Med 2001; 345: 319-324.
42. Archer SL, Gomberg-MaitlandM,MaitlandML, et al.Mitochondrial metabolism, redox signaling, and fusion: a mitochondria-ROS-HIF-1alpha-Kv1.5 O2-sensing pathway at the intersection of pulmonary hypertension and cancer. Am J Physiol Heart Circ Physiol 2008; 294: H570-H578.
43. Sutendra G, Dromparis P, Wright P, et al. The role of nogo and the mitochondria-endoplasmic reticulum unit in pulmonary hypertension. Sci Transl Med 2011; 3: 88ra55.
44. Sutendra G, Bonnet S, Rochefort G, et al. Fatty acid oxidation and malonyl-CoA decarboxylase in the vascular remodeling of pulmonary hypertension. Sci Transl Med 2010; 2: 44ra58.
45. Machado RD, Rudarakanchana N, Atkinson C, et al. Functional interaction between BMPR-II and Tctex-1, a light chain of Dynein, is isoform-specific and disrupted by mutations underlying primary pulmonary hypertension. Hum Mol Genet 2003; 12: 3277-3286.
46. Foletta VC, Lim MA, Soosairajah J, et al. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J Cell Biol 2003; 162: 1089-1098.
47. Wong WK, Knowles JA, Morse JH. Bone morphogenetic protein receptor type II C-terminus interacts with c-Src: implication for a role in pulmonary arterial hypertension. Am J Respir Cell Mol Biol 2005; 33: 438-446.
48. Ruegg J, Holsboer F, Turck C, et al. Cofilin 1 is revealed as an inhibitor of glucocorticoid receptor by analysis of hormoneresistant cells. Mol Cell Biol 2004; 24: 9371-9382.
49. van Raalte DH, Ouwens DM, Diamant M. Novel insights into glucocorticoid-mediated diabetogenic effects: towards expansion of therapeutic options? Eur J Clin Invest 2009; 39: 81-93.
50. Price LC, Montani D, Tcherakian C, et al. Dexamethasone reverses monocrotaline-induced pulmonary arterial hypertension in rats. Eur Respir J 2011; 37: 813-822.
51. Berglund ED, Li CY, Poffenberger G, et al. Glucose metabolism in vivo in four commonly used inbred mouse strains. Diabetes 2008; 57: 1790-1799.
52. Haluzik M, Colombo C, Gavrilova O, et al. Genetic background (C57BL/6J versus FVB/N) strongly influences the severity of diabetes and insulin resistance in ob/ob mice. Endocrinology 2004; 145: 3258-3264.
53. Barros RP, Gustafsson JA. Estrogen receptors and the metabolic network. Cell Metab 2011; 14: 289-299.
54. Zitzmann M. Testosterone deficiency, insulin resistance and the metabolic syndrome. Nat Rev Endocrinol 2009; 5: 673-681.
55. Winzell MS, Ahren B. The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 2004; 53: Suppl. 3, S215-219.
56. Buettner R, Scholmerich J, Bollheimer LC. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 2007; 15: 798-808.