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Original Article

Coadministration of Adenoviral Vascular Endothelial Growth Factor and Angiopoietin-1 Enhances Vascularization and Reduces Ventricular Remodeling in the Infarcted Myocardium of Type 1 Diabetic Rats

  1. Samson Mathews Samuel1,2,
  2. Yuzo Akita1,
  3. Debayon Paul1,
  4. Mahesh Thirunavukkarasu1,
  5. Lijun Zhan1,
  6. Perumana R. Sudhakaran2,
  7. Chuanfu Li3 and
  8. Nilanjana Maulik1
  1. 1Molecular Cardiology and Angiogenesis Laboratory, Department of Surgery, University of Connecticut Health Center, Farmington, Connecticut;
  2. 2Department of Biochemistry, University of Kerala, Trivandrum, Kerala, India;
  3. 3Department of Surgery, East Tennessee State University, Johnson City, Tennessee.
  1. Corresponding author: Nilanjana Maulik, nmaulik{at}neuron.uchc.edu.
  1. S.M.S. and Y.A. contributed equally to this work.

Diabetes 2010 Jan; 59(1): 51-60. https://doi.org/10.2337/db09-0336
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  • FIG. 1.
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    FIG. 1.

    A: Representative micrographs showing the in vivo transfection efficiency of Ad.LacZ in the nondiabetic sham-operated groups. Robust infection of the myocardium as assessed by β-galactosidase staining in the viable cardiac muscle surrounding the sites of gene transfer can be seen in the Ad.LacZ-transfected myocardium. B: Expression of VEGF as assessed by immunohistochemical staining. C: Expression of Ang-1 as assessed by immunohistochemical staining. The decrease in the expression of VEGF and Ang-1 is evident in the diabetic DS and DLZMI groups compared with the respective nondiabetic CS and CLZMI groups. Increase in the expression of VEGF and Ang-1 can be seen in the groups that received the combination gene therapy (CVAMI and DVAMI) compared with their respective (CLZMI and DLZMI) Ad.LacZ-treated groups. (−) represents representative micrographs showing the sections in which primary antibody was not added to verify the specificity of the staining protocol. CS, nondiabetic control sham; DS, diabetic sham; CLZMI, nondiabetic control animals that received Ad.LacZ injections; DLZMI, diabetic animals that received Ad.LacZ injections; CVAMI, nondiabetic control animals that received combination gene therapy; and DVAMI, diabetic animals that received combination gene therapy. (A high-quality color digital representation of this figure is available in the online issue.)

  • FIG. 2.
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    FIG. 2.

    Effect of combination gene therapy on myocardial fibrosis 7 and 30 days after gene therapy. A: Representative images show myocardial infarct and fibrosis after 7 days of MI and combination gene therapy. B: Representative images show myocardial infarct and fibrosis after 30 days of MI and combination gene therapy. There is no evident fibrosis in the CS and DS groups. A thinner infarct and significant fibrosis is evident in the CLZMI and DLZMI groups. Combination gene therapy in the CVAMI and DVAMI groups resulted in a thicker infarct containing islands of viable cardiac tissue. CS, nondiabetic control sham; DS, diabetic sham; CLZMI, nondiabetic control animals that received Ad.LacZ injections; DLZMI, diabetic animals that received Ad.LacZ injections; CVAMI, nondiabetic control animals that received combination gene therapy; and DVAMI, diabetic animals that received combination gene therapy. (A high-quality color digital representation of this figure is available in the online issue.)

  • FIG. 3.
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    FIG. 3.

    Effect of combination gene therapy on capillary and arteriolar density 7 days after the intervention. Representative images (A) and graphical representation (B) of capillary density analysis among the different groups (counts/mm2). Representative images (C) and graphical representation (D) of arteriolar density analysis among the different groups (counts/mm2). There was a significant increase in the capillary and arteriolar density in the CVAMI and DVAMI groups compared with the CLZMI and DLZMI groups, respectively. CS (black solid bar), nondiabetic control sham; DS (gray solid bar), diabetic sham; CLZMI (white bar), nondiabetic control animals that received Ad.LacZ injections; DLZMI (diagonal brick bar), diabetic animals that received Ad.LacZ injections; CVAMI (wave bar), nondiabetic control animals that received combination gene therapy; and DVAMI (wide upward diagonal bar), diabetic animals that received combination gene therapy. Values are presented as mean ± SEM. *P ≤ 0.05 when DS is compared with CS, #P ≤ 0.05 compared with CLZMI, †P ≤ 0.05 when DVAMI is compared with DLZMI. (A high-quality color digital representation of this figure is available in the online issue.)

  • FIG. 4.
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    FIG. 4.

    Effect of combination gene therapy on the expression of VEGF, Flk-1, Ang-1, Tie-2, and survivin 4 days after the intervention. A: Representative Western blots of VEGF, Flk-1, Ang-1, Tie-2, and survivin comparing CS and DS groups. B: Bar graphs show the quantitative difference in expression of VEGF, Flk-1, Ang-1, Tie-2, and survivin between the CS and DS groups. C: Representative Western blots for VEGF, Flk-1, Ang-1, Tie-2, and survivin comparing the CLZMI, DLZMI, CVAMI, and DVAMI groups, 4 days after the therapy. D: Bar graphs show the quantitative difference in expression of VEGF, Flk-1, Ang-1, Tie-2, and survivin among the CLZMI, DLZMI, CVAMI, and DVAMI groups. There was a significant increase in the expression of these proteins in the CVAMI and DVAMI groups compared with the CLZMI and DLZMI groups, respectively. Glyceraldehyde-3-phosphate dehydrogenase was used as a loading control. CS (black solid bars), nondiabetic control sham; DS (gray solid bars), diabetic sham; CLZMI (white bar), nondiabetic control animals that received Ad.LacZ injections; DLZMI (diagonal brick bar), diabetic animals that received Ad.LacZ injections; CVAMI (wave bar), nondiabetic control animals that received combination gene therapy; and DVAMI (wide upward diagonal bar), diabetic animals that received combination gene therapy. Values given as mean ± SEM. *P ≤ 0.05 when DS is compared with CS, #P ≤ 0.05 compared with CLZMI, †P ≤ 0.05 when DVAMI is compared with DLZMI.

  • FIG. 5.
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    FIG. 5.

    Effect of combination gene therapy on phosphorylation of MK2 (Western blot) and DNA binding activity of NFκB (electrophoretic mobility shift assay [EMSA]). A: Representative Western blots for p-MK2 comparing CS and DS groups, 2 and 4 days after the surgery. B: Graphical representation of p-MK2 in the CS and DS groups, 2 and 4 days after the therapy. C: Representative Western blots for p-MK2 comparing CLZMI, DLZMI, CVAMI, and DVAMI groups, 2 and 4 days after the therapy. D: Graphical representation of p-MK2 in the CLZMI, DLZMI, CVAMI, and DVAMI groups, 2 and 4 days after the therapy. The gene therapy significantly increased the levels of p-MK2, 2 and 4 days after the therapy. E: EMSA analysis reveals increased DNA binding activity of NFκB in the CVAMI and DVAMI groups compared with the CLZMI and DLZMI groups, respectively. CS (black solid bars), nondiabetic control sham; DS (gray solid bars), diabetic sham; CLZMI (white bar), nondiabetic control animals that received Ad.LacZ injections; DLZMI (diagonal brick bar), diabetic animals that received Ad.LacZ injections; CVAMI (wave bar), nondiabetic control animals that received combination gene therapy; and DVAMI (wide upward diagonal bar), diabetic animals that received combination gene therapy. Values given as mean ± SEM. *P ≤ 0.05 when DS is compared with CS, #P ≤ 0.05 compared with CLZMI, †P ≤ 0.05 when DVAMI is compared with DLZMI.

  • FIG. 6.
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    FIG. 6.

    Effect of combination gene therapy on left ventricular myocardial functions (echocardiography). A: Representative echocardiograph pictures of parasternal short axis images after 30 days of surgery and therapy. Bar graphs represent LVIDs in systole (in mm) (B), % ejection fraction (C), % fractional shortening (D), and heart rate in beats/min (E). There was a significant increase in the myocardial functions in the CVAMI and DVAMI groups compared with the CLZMI and DLZMI groups, respectively. CS (black solid bars), nondiabetic control sham; DS (gray solid bars), diabetic sham; CLZMI (white bar), nondiabetic control animals that received Ad.LacZ injections; DLZMI (diagonal brick bar), diabetic animals that received Ad.LacZ injections; CVAMI (wave bar), nondiabetic control animals that received combination gene therapy; and DVAMI (wide upward diagonal bar), diabetic animals that received combination gene therapy. Values given as mean ± SEM. *P ≤ 0.05 when DS is compared with CS, #P ≤ 0.05 compared with CLZMI, †P ≤ 0.05 when DVAMI is compared with DLZMI.

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Coadministration of Adenoviral Vascular Endothelial Growth Factor and Angiopoietin-1 Enhances Vascularization and Reduces Ventricular Remodeling in the Infarcted Myocardium of Type 1 Diabetic Rats
Samson Mathews Samuel, Yuzo Akita, Debayon Paul, Mahesh Thirunavukkarasu, Lijun Zhan, Perumana R. Sudhakaran, Chuanfu Li, Nilanjana Maulik
Diabetes Jan 2010, 59 (1) 51-60; DOI: 10.2337/db09-0336

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Coadministration of Adenoviral Vascular Endothelial Growth Factor and Angiopoietin-1 Enhances Vascularization and Reduces Ventricular Remodeling in the Infarcted Myocardium of Type 1 Diabetic Rats
Samson Mathews Samuel, Yuzo Akita, Debayon Paul, Mahesh Thirunavukkarasu, Lijun Zhan, Perumana R. Sudhakaran, Chuanfu Li, Nilanjana Maulik
Diabetes Jan 2010, 59 (1) 51-60; DOI: 10.2337/db09-0336
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