Glucose attenuates hypoxia-induced changes in endothelial cell growth by inhibiting HIF-1α expression

Diabetes and Vascular Disease Research

Volumn 11, Issue 4, 2014, Pages 270-280

  Gao, Wei ^a   Ferguson, Gail ^a   Connell, Paul ^a,b   Walshe, Tony ^a   O'Brien, Colm ^b   Redmond, Eileen M ^c   Cahill, Paul A ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Diabetes; Endothelial; HIF 1 ; Hyperglycaemia; Hypoxia

Indexed keywords

CASPASE 3; CYCLINE; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROTEIN BCL XL;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL GROWTH; CELL HYPOXIA; CELL PROLIFERATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENDOTHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE SILENCING; HYPERGLYCEMIA; HYPOXIA RESPONSE ELEMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; TRANSACTIVATION;

EID: 84905671721     PISSN: 14791641     EISSN: 17528984     Source Type: Journal    
DOI: 10.1177/1479164114533356     Document Type: Article

References (53)

1. Chong ZZ and Maiese K. Mammalian target of rapamycin signaling in diabetic cardiovascular disease. Cardiovasc Diabetol 2012; 11: 45
2. Peterson LR, McKenzie CR and Schaffer JE. Diabetic cardiovascular disease: getting to the heart of the matter. J Cardiovasc Transl Res 2012; 5: 436-445
3. Nathan DM, Cleary PA, Backlund J-YC, et al. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 2005; 353: 2643-2653
4. Molnar GD, Taylor WF and Langworthy A. On measuring the adequacy of diabetes regulation: comparison of continuously monitored blood glucose patterns with values at selected time points. Diabetologia 1974; 10: 139-143
5. Nath B and Szabo G. Hypoxia and hypoxia inducible factors: diverse roles in liver diseases. Hepatology 2012; 55: 622-633
6. Semenza GL. Hypoxia-inducible factor 1 and cardiovascular disease. Annu Rev Physiol 2014; 76: 39-56
7. Walshe TE and D'Amore PA. The role of hypoxia in vascular injury and repair. Annu Rev Pathol 2008; 3: 615-643
8. Kim Y-W and Byzova TV. Oxidative stress in angiogenesis and vascular disease. Blood 2014; 123: 625-631
9. Dotsch J, Knerr I, Rascher W, et al. Does defective hypoxia signalling cause type 2 diabetes? Eur J Endocrinol 2006; 154: 781-782
10. Gunton JE, Kulkarni RN, Yim S, et al. Loss of ARNT/ HIF1beta mediates altered gene expression and pancreaticislet dysfunction in human type 2 diabetes. Cell 2005; 122: 337-349
11. Xiao H, Gu Z, Wang G, et al. The possible mechanisms underlying the impairment of HIF-1a pathway signaling in hyperglycemia and the beneficial effects of certain therapies. Int J Med Sci 2013; 10: 1412-1421
12. Airley RE and Mobasheri A. Hypoxic regulation of glucose transport, anaerobic metabolism and angiogenesis in cancer: novel pathways and targets for anticancer therapeutics. Chemotherapy 2007; 53: 233-256
13. Gao W, Ferguson G, Connell P, et al. High glucose concentrations alter hypoxia-induced control of vascular smooth muscle cell growth via a HIF-1alpha-dependent pathway. J Mol Cell Cardiol 2007; 42: 609-619
14. Baracca A, Sgarbi G, Padula A, et al. Glucose plays a main role in human fibroblasts adaptation to hypoxia. Int J Biochem Cell Biol 2013; 45: 1356-1365
15. Colombo A, Guha S, Mackle JN, et al. Cyclic strain amplitude dictates the growth response of vascular smooth muscle cells in vitro: role in in-stent restenosis and inhibition with a sirolimus drug-eluting stent. Biomech Model Mechanobiol 2013; 12: 671-683
16. Sweeney C, Morrow D, Birney YA, et al. Notch 1 and 3 receptor signaling modulates vascular smooth muscle cell growth, apoptosis, and migration via a CBF-1/RBP-Jk dependent pathway. FASEB J 2004; 18: 1421-1423
17. Romero-Calvo I, Ocon B, Martinez-Moya P, et al. Reversible Ponceau staining as a loading control alternative to actin in Western blots. Anal Biochem 2010; 401: 318-320
18. Bruick RK. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci USA 2000; 97: 9082-9087
19. Willard AL and Herman IM. Vascular complications and diabetes: current therapies and future challenges. J Ophthalmol 2012; 2012: 209538 (14 pp.)
20. Pop-Busui R, Sima A and Stevens M. Diabetic neuropathy and oxidative stress. Diabetes Metab Res Rev 2006; 22: 257-273
21. Hashmi S and Al-Salam S. Hypoxia-inducible factor-1 alpha in the heart: a double agent? Cardiol Rev 2012; 20: 268-273
22. Malmberg K, Norhammar A, Wedel H, et al. Glycometabolic state at admission: important risk marker of mortality in conventionally treated patients with diabetes mellitus and acute myocardial infarction: long-term results from the Diabetes and Insulin-Glucose Infusion in Acute Myocardial Infarction (DIGAMI) study. Circulation 1999; 99: 2626-2632
23. Xue W, Cai L, Tan Y, et al. Cardiac-specific overexpression of HIF-1{alpha} prevents deterioration of glycolytic pathway and cardiac remodeling in streptozotocin-induced diabetic mice. Am J Pathol 2010; 177: 97-105
24. Cioffi CL, Liu XQ, Kosinski PA, et al. Differential regulation of HIF-1 alpha prolyl-4-hydroxylase genes by hypoxia in human cardiovascular cells. Biochem Biophys Res Commun 2003; 303: 947-953
25. Catrina S-B, Botusan IR, Rantanen A, et al. Hypoxiainducible factor-1alpha and hypoxia-inducible factor-2alpha are expressed in kaposi sarcoma and modulated by insulinlike growth factor-I. Clin Cancer Res 2006; 12: 4506-4514
26. Connell P, Walshe T, Ferguson G, et al. Elevated glucose attenuates agonist- and flow-stimulated endothelial nitric oxide synthase activity in microvascular retinal endothelial cells. Endothelium 2007; 14: 17-24
27. Hempel A, Maasch C, Heintze U, et al. High glucose concentrations increase endothelial cell permeability via activation of protein kinase C alpha. Circ Res 1997; 81: 363-371
28. Joshi M, Kotha SR, Malireddy S, et al. Conundrum of pathogenesis of diabetic cardiomyopathy: role of vascular endothelial dysfunction, reactive oxygen species, and mitochondria. Mol Cell Biochem 2013; 386: 233-249
29. Pant R, Marok R and Klein LW. Pathophysiology of coronary vascular remodeling: relationship with traditional risk factors for coronary artery disease. Cardiol Rev 2014; 22: 13-16
30. Sena CM, Pereira AM and Seica R. Endothelial dysfunction - a major mediator of diabetic vascular disease. Biochim Biophys Acta 2013; 1832: 2216-2231
31. Piga R, Naito Y, Kokura S, et al. Short-term high glucose exposure induces monocyte-endothelial cells adhesion and transmigration by increasing VCAM-1 and MCP-1 expression in human aortic endothelial cells. Atherosclerosis 2007; 193: 328-334
32. Chakravarthy U, Hayes RG, Stitt AW, et al. Constitutive nitric oxide synthase expression in retinal vascular endothelial cells is suppressed by high glucose and advanced glycation end products. Diabetes 1998; 47: 945-952
33. Hamuro M, Polan J, Natarajan M, et al. High glucose induced nuclear factor kappa B mediated inhibition of endothelial cell migration. Atherosclerosis 2002; 162: 277-287
34. Curcio F and Ceriello A. Decreased cultured endothelial cell proliferation in high glucose medium is reversed by antioxidants: new insights on the pathophysiological mechanisms of diabetic vascular complications. In Vitro Cell Dev Biol 1992; 28A: 787-790
35. Merchan JR, Kovacs K, Railsback JW, et al. Antiangiogenic activity of 2-deoxy-d-glucose. PLoS One 2010; 5: e13699
36. Martin A, Komada MR and Sane DC. Abnormal angiogenesis in diabetes mellitus. Med Res Rev 2003; 23: 117-145
37. Fisher SA, Langille BL and Srivastava D. Apoptosis during cardiovascular development. Circ Res 2010; 87: 856-864
38. Gao C, Sun W, Christofidou-Solomidou M, et al. PECAM-1 functions as a specific and potent inhibitor of mitochondrialdependent apoptosis. Blood 2003; 102: 169-179
39. Chavakis E and Dimmeler S. Regulation of endothelial cell survival and apoptosis during angiogenesis. Arterioscler Thromb Vasc Biol 2002; 22: 887-893
40. Ackermann EJ, Taylor JK, Narayana R, et al. The role of antiapoptotic Bcl-2 family members in endothelial apoptosis elucidated with antisense oligonucleotides. J Biol Chem 1999; 274: 11245-11252
41. Norhammar A, Malmberg K, Diderholm E, et al. Diabetes mellitus: the major risk factor in unstable coronary artery disease even after consideration of the extent of coronary artery disease and benefits of revascularization. J Am Coll Cardiol 2004; 43: 585-591
42. Staab A, Loffler J, Said HM, et al. Modulation of glucose metabolism inhibits hypoxic accumulation of hypoxiainducible factor-1alpha (HIF-1alpha). Strahlenther Onkol 2007; 183: 366-373
43. Catrina S-B, Okamoto K, Pereira T, et al. Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 2004; 53: 3226-3232
44. Lim JI, Spee C and Hinton DR. A comparison of hypoxiainducible factor-a in surgically excised neovascular membranes of patients with diabetes compared with idiopathic epiretinal membranes in nondiabetic patients. Retina 2010; 30: 1472-1478
45. Bento CF and Pereira P. Regulation of hypoxia-inducible factor 1 and the loss of the cellular response to hypoxia in diabetes. Diabetologia 2011; 54: 1946-1956
46. Capla JM, Grogan RH, Callaghan MJ, et al. Diabetes impairs endothelial progenitor cell-mediated blood vessel formation in response to hypoxia. Plast Reconstr Surg 2007; 119: 59-70.
47. Kajiwara H, Luo Z, Belanger AJ, et al. A hypoxic inducible factor-1 alpha hybrid enhances collateral development and reduces vascular leakage in diabetic rats. J Gene Med 2009; 11: 390-400
48. Thangarajah H, Yao D, Chang EI, et al. The molecular basis for impaired hypoxia-induced VEGF expression in diabetic tissues. Proc Natl Acad Sci USA 2009; 106: 13505-13510
49. Baynes JW and Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 1999; 48: 1-9
50. Zou A-P and Cowley AW. Reactive oxygen species and molecular regulation of renal oxygenation. Acta Physiol Scand 2003; 179: 233-241
51. Olson N and Van der Vliet A. Interactions between nitric oxide and hypoxia-inducible factor signaling pathways in inflammatory disease. Nitric Oxide 2011; 25: 125-137
52. Bullock JJ, Mehta SL, Lin Y, et al. Hyperglycemia-enhanced ischemic brain damage in mutant manganese SOD mice is associated with suppression of HIF-1alpha. Neurosci Lett 2009; 456: 89-92
53. Kimura H, Weisz A, Kurashima Y, et al. Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood 2000; 95: 189-197.