The possible mechanism for impaired angiogenesis after transient focal ischemia in type 2 diabetic GK rats: Different expressions of angiostatin and vascular endothelial growth factor

Biomedicine and Pharmacotherapy

Volumn 64, Issue 3, 2010, Pages 208-213

  Zhu, Meijia ^a   Bi, Xizhuang ^a   Jia, Qian ^b   Shangguan, Shina ^c  

^a SHANDONG UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c Affiliated Hospital of Shandong Medical College   (China)

Author keywords

Angiogenesis; Angiostatin; Diabetes mellitus; MMP 9; Vascular endothelial growth factor

Indexed keywords

ANGIOSTATIN; GELATINASE B; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; CAPILLARY DENSITY; CONTROLLED STUDY; GOTO KAKIZAKI RAT; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEOVASCULARIZATION (PATHOLOGY); NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; STROKE PATIENT; WESTERN BLOTTING; WISTAR RAT;

ANGIOSTATINS; ANIMALS; ANTIGENS, CD31; BLOOD GLUCOSE; CAPILLARIES; DIABETES MELLITUS, TYPE 2; GENE EXPRESSION REGULATION; ISCHEMIC ATTACK, TRANSIENT; MALE; MATRIX METALLOPROTEINASE 9; NEOVASCULARIZATION, PHYSIOLOGIC; RANDOM ALLOCATION; RATS; RATS, MUTANT STRAINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77949275179     PISSN: 07533322     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopha.2009.08.005     Document Type: Article

References (50)

1. Kaarisalo M.M., Räihä I., Sivenius J., et al. Diabetes worsens the outcome of acute ischemic stroke. Diabetes Res Clin Pract 69 3 (2005) 293-298
2. Taguchi Y., Takashima S., Sasahara E., et al. Morphological changes in capillaries in the ischemic brain in Wistar rats. Arch Histol Cytol 67 3 (2004) 253-261
3. Shibuya M. Vascular endothelial growth factor dependent and independent regulation of angiogenesis. BMB Rep 41 4 (2008) 278-286
4. Weihrauch D., Lohr N.L., Mraovic B., et al. Chronic Hyperglycemia Attenuates Coronary Collateral Development and Impairs Proliferative Properties of Myocardial Interstitial Fluid by Production of Angiostatin. Circulation 109 19 (2004) 2343-2348
5. Hueb W., Gersh B.J., Costa F., et al. Impact of Diabetes on Five-Year Outcomes of Patients With Multivessel Coronary Artery Disease. Ann Thorac Surg 83 1 (2007) 93-99
6. imura H., and Esumi H. Reciprocal regulation between nitric oxide and vascular endothelial growth factor in angiogenesis. Acta Biochim Pol 50 1 (2003) 49-59
7. Pepper M.S. Manipulating angiogenesis: from basic science to the bedside. Arterioscler Thromb Vasc Biol 17 4 (1997) 605-619
8. Sun Y., Jin K., Xie L., et al. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111 12 (2003) 1843-1851
9. Ferrara N., and Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 18 1 (1997) 4-25
10. Kovács Z., Ikezaki K., Samoto K., et al. VEGF and flt. Expression time kinetics in rat brain infarct. Stroke 27 10 (1996) 1865-1872
11. Hayashi T., Abe K., Suzuki H., et al. Rapid induction of vascular endothelial growth factor gene expression after transient middle cerebral artery occlusion in rats. Stroke 28 10 (1997) 2039-2044
12. Lennmyr F., Ata K.A., Funa K., et al. Expression of vascular endothelial growth factor (VEGF) and its receptors (Flt-1 and Flk-1) following permanent and transient occlusion of the middlecerebral artery in the rat. J Neuropathol Exp Neurol 57 9 (1998) 874-882
13. Li J., Brown L.F., Hibberd M.G., et al. VEGF, flk-1, and flt-1 expression in a rat myocardial infarction model of angiogenesis. Am J Physiol 270 (1996) 1803-1811
14. Banai S., Shweiki D., Pinson A., et al. Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: implications for coronary angiogenesis. Cardiovasc Res 28 8 (1994) 1176-1179
15. Cobbs C.S., Chen J., Greenberg D.A., et al. Vascular endothelial growth factor expression in transient focal cerebral ischemia in the rat. Neurosci Lett 249 2-3 (1998) 79-82
16. Mu D., Jiang X., Sheldon R.A., et al. Regulation of hypoxia-inducible factor 1alpha and induction of vascular endothelial growth factor in a rat neonatal stroke model. Neurobiol Dis 14 3 (2003) 524-534
17. Lennmyr F., Terént A., Syvänen A.C., et al. Vascular endothelial growth factor gene expression in middle cerebral artery occlusion in the rat. Acta Anaesthesiol Scand 49 4 (2005) 488-493
18. Marti H.J., Bernaudin M., Bellail A., et al. Hypoxia-Induced Vascular Endothelial Growth Factor Expression Precedes Neovascularization after Cerebral Ischemia. Am J Pathol 156 3 (2000) 965-976
19. Harrigan M.R., Ennis S.R., Masada T., et al. Intraventricular Infusion of Vascular Endothelial Growth Factor Promotes Cerebral Angiogenesis with Minimal Brain Edema. Neurosurgery 50 3 (2002) 589-598
20. O'Reilly M.S., Holmgren L., Shing Y., et al. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79 2 (1994) 315-328
21. O'Reilly M.S., Wiederschain D., Stetler-Stevenson W.G., et al. Regulation of angiostatin production by matrix metalloproteinase-2 in a model of concomitant resistance. J Biol Chem 274 41 (1999) 29568-29571
22. Chung A.W., Hsiang Y.N., Matzke L.A., et al. Reduced Expression of Vascular Endothelial Growth Factor Paralleled With the increased Angiostatin Expression Resulting From the Upregulated Activities of Matrix Metalloproteinase-2 and -9 in Human Type 2 Diabetic Arterial Vasculature. Circ Res 99 2 (2006) 140-148
23. Longa E.Z., Weinstein P.R., Carlson S., et al. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20 1 (1989) 84-91
24. Zhang Z.G., Zhang L., Jiang Q., et al. VEGF enhances angiogenesis and promotes blood-brain arrier leakage in the ischemic brain. J Clin Invest 106 7 (2000) 829-838
25. Zhang Z.G., Zhang L., Tsang W., et al. Dynamic platelet accumulation at the site of the occluded middle cerebral artery and in downstream microvessels is associated with loss of microvascular integrity after embolic middle cerebral artery occlusion. Brain Res 912 2 (2001) 181-194
26. Morris D.C., Yeich T., Khalighi M.M., et al. Microvascular structure after embolic focal cerebral ischemia in the rat. Brain Res 972 1-2 (2003) 31-37
27. Hazarika S., Dokun A.O., Li Y., et al. Impaired angiogenesis after hindlimb ischemia in type 2 diabetes mellitus: differential regulation of vascular endothelial growth factor receptor 1 and soluble vascular endothelial growth factor receptor 1. Circ Res 101 9 (2007) 948-956
28. Rivard A., Silver M., Chen D., et al. Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol 154 2 (1999) 355-363
29. Cornelius L.A., Nehring L.C., Harding E., et al. Matrix metalloproteinases generate angiostatin: effects on neovascularization. J Immunol 161 12 (1998) 6845-6852
30. Lai C.C., Wu W.C., Chen S.L., et al. Suppression of choroidal neovascularization by adeno-associated virus vector expressing angiostatin. Invest Ophthalmol Vis Sci 42 10 (2001) 2401-2407
31. Matsunaga T., Chilian W.M., and March K. Angiostatin is negatively associated with coronary collateral growth in patients with coronary artery disease. Am J Physiol Heart Circ Physiol 288 5 (2005) 2042-2046
32. Veitonmäki N., Cao R., Wu L.H., et al. Endothelial cell surface ATP synthase-triggered caspase-apoptotic pathway is essential for k1-5-induced antiangiogenesis. Cancer Res 64 10 (2004) 3679-3686
33. Chi S.L., and Pizzo S.V. Angiostatin is directly cytotoxic to tumor cells at low extracellular pH: a mechanism dependent on cell surface-associated ATP synthase. Cancer Res 66 2 (2006) 875-882
34. Wagner K.R., Kleinholz M., et al. Hyperglycemic versus normoglycemic stroke: topography of brain metabolites, intracellular pH, and infarct size. J Cereb Blood Flow Metab 12 2 (1992) 213-222
35. Sima J., Zhang S.X., Shao C., et al. The effect of angiostatin on vascular leakage and VEGF expression in rat retina. FEBS Lett 564 1-2 (2004) 19-23
36. Pepper M.S. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 21 7 (2001) 1104-1117
37. Azar D.T. Corneal angiogenic privilege: angiogenic and antiangiogenic factors in corneal avascularity, vasculogenesis, and wound healing (an American Ophthalmological Society thesis). Trans Am Ophthalmol Soc 104 (2006) 264-302
38. Claesson-Welsh L., Welsh M., Ito N., et al. Angiostatin induces endothelial cell apoptosis and activation of focal adhesion kinase independently of the integrin-binding motif RGD. Proc Natl Acad Sci U S A 95 10 (1998) 5579-5583
39. Kräling B.M., Wiederschain D.G., Boehm T., et al. The role of matrix metalloproteinase activity in the maturation of human capillary endothelial cells in vitro. J Cell Sci 112 (1999) 1599-1609
40. Death A.K., Fisher E.J., McGrath K.C., et al. High glucose alters matrix metalloproteinase expression in two key vascular cells: potential impact on atherosclerosis in diabetes. Atherosclerosis 168 2 (2003) 263-269
41. Romanic A.M., White R.F., Arleth A.J., et al. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29 5 (1998) 1020-1030
42. Tanaka H., Takai S., Jin D., et al. Inhibition of Matrix Metalloproteinase-9 Activity by Trandolapril after Middle Cerebral Artery Occlusion in Rats. Hypertens Res 30 5 (2007) 469-475
43. Montaner J., Alvarez-Sabin J., Molina C., et al. Matrix metalloproteinase expression after human cardioembolic stroke: temporal profile and relation to neurological impairment. Stroke 32 8 (2001) 1759-1766
44. Baynes J.W. Role of oxidative stress in development of complications in diabetes. Diabetes 40 4 (1991) 405-412
45. Giugliano D., Marfella R., Coppola L., et al. Vascular effects of acute hyperglycemia in humans are reversed by L-arginine. Evidence for reduced availability of nitric oxide during hyperglycemia. Circulation 95 7 (1997) 1783-1790
46. Evans J.L., Goldfine I.D., Maddux B.A., et al. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23 5 (2002) 599-622
47. Knipp B.S., Ailawadi G., Ford J.W., et al. Increased MMP-9 expression and activity by aortic smooth muscle cells after nitric oxide synthase inhibition is associated with increased nuclear factor-kappaB and activator protein-1 activity. J Surg Res 116 1 (2004) 70-80
48. Benbow U., and Brinckerhoff C.E. The AP-1 site and MMP gene regulation: what is all the fuss about?. Matrix Biol 15 8-9 (1997) 519-526
49. Sato H., Kita M., and Seiki M. v-Src activates the expression of 92-kDa type IV collagenase gene through the AP-1 site and the GT box homologous to retinoblastoma control elements. A mechanism regulating gene expression independent of that by inflammatory cytokines. J Biol Chem 268 31 (1993) 23460-23468
50. He Z., Opland D.M., Way K.J., et al. Regulation of Vascular Endothelial Growth Factor Expression and Vascularization in the Myocardium by Insulin Receptor and PI3K/Akt Pathways in Insulin Resistance and Ischemia. Arterioscler Thromb Vasc Biol 26 4 (2006) 787-793