Glycaemic variability affects ischaemia-induced angiogenesis in diabetic mice

Clinical Science

Volumn 121, Issue 12, 2011, Pages 555-564

  Biscetti, Federico ^a   Pitocco, Dario ^a   Straface, Giuseppe ^b   Zaccardi, Francesco ^a   De Cristofaro, Raimondo ^c   Rizzo, Paola ^a   Lancellotti, Stefano ^c   Arena, Vincenzo ^c   Stigliano, Egidio ^c   Musella, Tittania ^a   Ghirlanda, Giovanni ^a   Flex, Andrea ^a  

^a FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

Author keywords

Angiogenesis; Diabetes complication; Endothelial nitric oxide synthase; Glycaemic variability; Vascular endothelial growth factor

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; INSULIN GLARGINE; PROTEIN KINASE B; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; GLUCOSE BLOOD LEVEL; GLYCEMIC VARIABILITY; HINDLIMB; HISTOLOGY; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; INSULIN TREATMENT; LASER DOPPLER FLOWMETRY; LEG BLOOD FLOW; LIMB ISCHEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STREPTOZOCIN DIABETES; TREATMENT OUTCOME; VASCULARIZATION; WESTERN BLOTTING;

ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC ANGIOPATHIES; HYPERGLYCEMIA; ISCHEMIA; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80052405477     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20110043     Document Type: Article

References (37)

1. Stamler, J., Vaccaro, O., Neaton, J. D. and Wentworth, D. (1993) Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the multiple risk factor intervention trial. Diabetes Care 16, 434-444.
2. Panzram, G. (1987) Mortality and survival in type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 30, 123-131.
3. Kaushik, S., Wang, J. J.,Wong, T. Y., Flood, V., Barclay, A., Brand-Miller, J. and Mitchell, P. (2009) Glycemic index, retinal vascular caliber, and stroke mortality. Stroke 40, 206-212.
4. Mukamal, K. J., Nesto, R. W., Cohen, M. C., Muller, J. E., Maclure, M., Sherwood, J. B. and Mittleman, M. A. (2001) Impact of diabetes on long-term survival after acute myocardial infarction: comparability of risk with prior myocardial infarction. Diabetes Care 24, 1422-1427.
5. Monnier, L., Mas, E., Ginet, C., Michel, F., Villon, L., Cristol, J. P. and Colette, C. (2006) Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA, J. Am. Med. Assoc. 295, 1681-1687.
6. Kilpatrick, E. S., Rigby, A. S. and Atkin, S. L. (2008) A1C variability and the risk of microvascular complications in type 1 diabetes: data from the diabetes control and complications trial. Diabetes Care 31, 2198-2202.
7. Levitzky, Y. S., Pencina, M. J., D'Agostino, R. B., Meigs, J. B., Murabito, J. M., Vasan, R. S. and Fox, C. S. (2008) Impact of impaired fasting glucose on cardiovascular disease: the Framingham Heart Study. J. Am. Coll. Cardiol. 51, 264-270.
8. Coutinho, M., Gerstein, H. C., Wang, Y. and Yusuf, S. (1999) The relationship between glucose and incident cardiovascular events. A metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years. Diabetes Care 22, 233-240.
9. Zaccardi, F., Pitocco, D. and Ghirlanda, G. (2009) Glycemic risk factors of diabetic vascular complications: the role of glycemic variability. Diabetes Metab. Res. Rev. 25, 199-207.
10. Diabetes Control and Complications Trial (1995) The relationship of glycemic exposure (HbA1c) to the risk of development and progression of retinopathy in the diabetes control and complications trial. Diabetes 44, 968-983.
11. Risso, A., Mercuri, F., Quagliaro, L., Damante, G. and Ceriello, A. (2001) Intermittent high glucose enhances apoptosis in human umbilical vein endothelial cells in culture. Am. J. Physiol. Endocrinol. Metab. 281, E924-E930.
12. Quagliaro, L., Piconi, L., Assaloni, R., Martinelli, L.,Motz, E. and Ceriello, A. (2003) Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes 52, 2795-2804.
13. Ceriello, A., Esposito, K., Piconi, L., Ihnat, M. A., Thorpe, J. E., Testa, R., Boemi, M. and Giugliano, D. (2008) Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes 57, 1349-1354.
14. Martin, A., Komada, M. R. and Sane, D. C. (2003) Abnormal angiogenesis in diabetes mellitus. Med. Res. Rev. 23, 117-145.
15. Rivard, A., Silver, M., Chen, D., Kearney, M., Magner, M., Annex, B., Peters, K. and Isner, J. M. (1999) Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am. J. Pathol. 154, 355-363.
16. Brownlee, M. (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813-820.
17. Goldberg, I. J., Hu, Y., Noh, H. L., Wei, J., Huggins, L. A., Rackmill, M. G., Hamai, H., Reid, B. N., Blaner, W. S. and Huang, L. S. (2008) Decreased lipoprotein clearance is responsible for increased cholesterol in LDL receptor knockout mice with streptozotocin-induced diabetes. Diabetes 57, 1674-1682.
18. Service, F. J., Molnar, G. D., Rosevear, J. W., Ackerman, E., Gatewood, L. C. and Taylor, W. F. (1970) Mean amplitude of glycemic excursions, a measure of diabetic instability. Diabetes 19, 644-655.
19. McDonnell, C. M., Donath, S. M., Vidmar, S. I., Werther, G. A. and Cameron, F. J. (2005) A novel approach to continuous glucose analysis utilizing glycemic variation. Diabetes Technol. Ther. 7, 253-263.
20. Biscetti, F., Straface, G., De Cristofaro, R., Lancellotti, S., Rizzo, P., Arena, V., Stigliano, E., Pecorini, G., Egashira, K., De Angelis, G. et al. (2010) High-mobility group box-1 protein promotes angiogenesis after peripheral ischemia in diabetic mice through a VEGF-dependent mechanism. Diabetes 59, 1496-1505.
21. Ciulla, M. M., Acquistapace, G., Toffetti, L., Paliotti, R., Ferrero, S., Magrini, F. and Braidotti, P. (2009) Ki67 cytoplasmic expression: observations in normal tissue from heart atrial appendages of healthy rats. Cell Cycle 8, 2125.
22. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S. A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
23. Nathan, D. M., Kuenen, J., Borg, R., Zheng, H., Schoenfeld, D. and Heine, R. J. (2008) Translating the A1C assay into estimated average glucose values. Diabetes Care 31, 1473-1478.
24. Olsson, A. K., Dimberg, A., Kreuger, J. and Claesson-Welsh, L. (2006) VEGF receptor signalling: in control of vascular function. Nat. Rev. Mol. Cell Biol. 7, 359-371.
25. Roguin, A., Nitecki, S., Rubinstein, I., Nevo, E., Avivi, A., Levy, N. S., Abassi, Z. A., Sabo, E., Lache, O., Frank, M. et al. (2003) Vascular endothelial growth factor (VEGF) fails to improve blood flow and to promote collateralization in a diabetic mouse ischemic hindlimb model. Cardiovasc. Diabetol. 2, 18.
26. Horvath, E. M., Benko, R., Kiss, L., Muranyi, M., Pek, T., Fekete, K., Barany, T., Somlai, A., Csordas, A. and Szabo, C. (2009) Rapid 'glycaemic swings' induce nitrosative stress, activate poly(ADP-ribose) polymerase and impair endothelial function in a rat model of diabetes mellitus. Diabetologia 52, 952-961.
27. Loomans, C. J., de Koning, E. J., Staal, F. J., Rookmaaker, M. B., Verseyden, C., de Boer, H. C., Verhaar, M. C., Braam, B., Rabelink, T. J. and van Zonneveld, A. J. (2004) Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53, 195-199.
28. Yan, S. F., Ramasamy, R., Naka, Y. and Schmidt, A. M. (2003) Glycation, inflammation and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ. Res. 93, 1159-1169.
29. Zaccardi, F., Pitocco, D. and Ghirlanda, G. (2009) A rat model of glycaemic variability. Diabetologia 52, 1689-1690.
30. Loges, S., Roncal, C. and Carmeliet, P. (2009) Development of targeted angiogenic medicine. J. Thromb. Haemostasis 7, 21-33.
31. Di Stefano, R., Felice, F. and Balbarini, A. (2009) Angiogenesis as risk factor for plaque vulnerability. Curr. Pharm. Des. 15, 1095-1106.
32. Blanes, M. G., Oubaha, M., Rautureau, Y. and Gratton, J. P. (2007) Phosphorylation of tyrosine 801 of vascular endothelial growth factor receptor-2 is necessary for Akt-dependent endothelial nitric-oxide synthase activation and nitric oxide release from endothelial cells. J. Biol. Chem. 282, 10660-10669.
33. Felaco, M., Grilli, A., De Lutiis, M. A., Patruno, A., Libertini, N., Taccardi, A. A., Di Napoli, P., Di Giulio, C., Barbacane, R. and Conti, P. (2001) Endothelial nitric oxide synthase (eNOS) expression and localization in healthy and diabetic rat hearts. Ann. Clin. Lab. Sci. 31, 179-186.
34. Zdychova, J. and Komers, R. (2005) Emerging role of Akt kinase/protein kinase B signaling in pathophysiology of diabetes and its complications. Physiol. Res. 54, 1-16.
35. Preis, S. R., Hwang, S. J., Coady, S., Pencina, M. J., D'Agostino, Sr, R. B., Savage, P. J., Levy, D. and Fox, C. S. (2009) Trends in all-cause and cardiovascular disease mortality among women and men with and without diabetes mellitus in the Framingham Heart Study, 1950 to 2005. Circulation 119, 1728-1735.
36. Giardino, I., Edelstein, D. and Brownlee, M. (1996) BCL-2 expression or antioxidants prevent hyperglycemia-induced formation of intracellular advanced glycation endproducts in bovine endothelial cells. J. Clin. Invest. 97, 1422-1428.
37. Gao, L. and Mann, G. E. (2009) Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signalling. Cardiovasc. Res. 82, 9-20.