Angiogenesis inhibitor, endostar, prevents vasa vasorum neovascularization in a swine atherosclerosis model

Journal of Atherosclerosis and Thrombosis

Volumn 22, Issue 10, 2015, Pages 1100-1112

  Xu, Xiaoming ^a   Mao, Wei ^a   Chai, Yueyang ^b   Dai, Jin ^a   Chen, Qian ^b   Wang, Lihui ^b   Zhuang, Qin ^b   Pan, Yongming ^b   Chen, Minli ^b   Ni, Guibao ^a   Huang, Zhaoquan ^a  

^a Zhejiang Traditional Chinese Medical Hospital   (China)

^b ZHEJIANG CHINESE MEDICAL UNIVERSITY   (China)

Author keywords

Atherosclerosis; Endostar; Neovascularization; Swine; Vasa vasorum

Indexed keywords

C REACTIVE PROTEIN; CATENIN; INTERLEUKIN 6; RECOMBINANT ENDOSTATIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; ANGIOGENESIS INHIBITOR; ENDOSTAR PROTEIN; ENDOSTATIN; RECOMBINANT PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL WALL THICKNESS; ARTICLE; ATHEROSCLEROSIS; BLOOD ANALYSIS; BODY WEIGHT; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; HISTOLOGY; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LIPID BLOOD LEVEL; MALE; NONHUMAN; PROTEIN EXPRESSION; VASA VASORUM NEOVASCULARIZATION; WEIGHT GAIN; WESTERN BLOTTING; ABDOMINAL AORTA; ANIMAL; DISEASE MODEL; DRUG EFFECTS; MINIPIG; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; PIG; VASA VASORUM;

ANGIOGENESIS INHIBITORS; ANIMALS; AORTA, ABDOMINAL; ATHEROSCLEROSIS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENDOSTATINS; IMMUNOHISTOCHEMISTRY; MALE; NEOVASCULARIZATION, PATHOLOGIC; RECOMBINANT PROTEINS; SWINE; SWINE, MINIATURE; VASA VASORUM;

EID: 84943229266     PISSN: 13403478     EISSN: 18803873     Source Type: Journal    
DOI: 10.5551/jat.26906     Document Type: Article

References (58)

1. Weber C, Noels H: Atherosclerosis: current pathogenesis and therapeutic options. Nat Med, 2011; 17: 1410-1422
2. Erbel C, Sato K, Meyer FB, Kopecky SL, Frye RL, Goronzy JJ, Weyand CM: Functional profile of activated dendritic cells in unstable atherosclerotic plaque. Basic Res Cardiol, 2007; 102: 123-132
3. Ross R: Atherosclerosis--an inflammatory disease. N Engl J Med, 1999; 340: 115-126
4. Zhang C: The role of inflammatory cytokines in endothelial dysfunction. Basic Res Cardiol, 2008; 103: 398-406
5. Sirol M, Moreno PR, Purushothaman KR, Vucic E, Amirbekian V, Weinmann HJ, Muntner P, Fuster V, Fayad ZA: Increased neovascularization in advanced lipid-rich atherosclerotic lesions detected by gadofluorine-M-enhanced MRI: implications for plaque vulnerability. Circ Cardiovasc Imaging, 2009; 2: 391-396
6. Winter PM, Caruthers SD, Zhang H, Williams TA, Wickline SA, Lanza GM: Antiangiogenic synergism of integrin-targeted fumagillin nanoparticles and atorvastatin in atherosclerosis. JACC Cardiovasc Imaging, 2008; 1: 624-634
7. Langheinrich AC, Michniewicz A, Sedding DG, Walker G, Beighley PE, Rau WS, Bohle RM, Ritman EL: Correlation of vasa vasorum neovascularization and plaque progression in aortas of apolipoprotein E(-/-)/low-density lipoprotein(-/-) double knockout mice. Arterioscler Thromb Vasc Biol, 2006; 26: 347-352
8. Eriksson EE: Intravital microscopy on atherosclerosis in apolipoprotein e-deficient mice establishes microvessels as major entry pathways for leukocytes to advanced lesions. Circulation, 2011; 124: 2129-2138
9. Jeziorska M, Woolley DE: Neovascularization in early atherosclerotic lesions of human carotid arteries: its potential contribution to plaque development. Hum Pathol, 1999; 30: 919-925
10. Moreno PR, Purushothaman KR, Fuster V, Echeverri D, Truszczynska H, Sharma SK, Badimon JJ, O’Connor WN: Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation, 2004; 110: 2032-2038
11. O’Brien KD, McDonald TO, Chait A, Allen MD, Alpers CE: Neovascular expression of E-selectin, intercellular adhesion molecule-1, and vascular cell adhesion molecule-1 in human atherosclerosis and their relation to intimal leukocyte content. Circulation, 1996; 93: 672-682
12. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK, Farb A, Guerrero LJ, Hayase M, Kutys R, Narula J, Finn AV, Virmani R: Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med, 2003; 349: 2316-2325
13. Moulton KS: Angiogenesis in atherosclerosis: gathering evidence beyond speculation. Curr Opin Lipidol, 2006; 17: 548-555
14. Gossl M, Herrmann J, Tang H, Versari D, Galili O, Mannheim D, Rajkumar SV, Lerman LO, Lerman A: Prevention of vasa vasorum neovascularization attenuates early neointima formation in experimental hypercholesterolemia. Basic Res Cardiol, 2009; 104: 695-706
15. Winter PM, Morawski AM, Caruthers SD, Fuhrhop RW, Zhang H, Williams TA, Allen JS, Lacy EK, Robertson JD, Lanza GM, Wickline SA: Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. Circulation, 2003; 108: 2270-2274
16. Wilson SH, Herrmann J, Lerman LO, Holmes DR Jr, Napoli C, Ritman EL, Lerman A: Simvastatin preserves the structure of coronary adventitial vasa vasorum in experimental hypercholesterolemia independent of lipid lowering. Circulation, 2002; 105: 415-418
17. Herrmann J, Best PJ, Ritman EL, Holmes DR, Lerman LO, Lerman A: Chronic endothelin receptor antagonism prevents coronary vasa vasorum neovascularization in experimental hypercholesterolemia. J Am Coll Cardiol, 2002; 39: 1555-1561
18. Lu N, Ling Y, Gao Y, Chen Y, Mu R, Qi Q, Liu W, Zhang H, Gu H, Wang S, Yang Y, Guo Q: Endostar suppresses invasion through downregulating the expression of matrix metalloproteinase-2/9 in MDA-MB-435 human breast cancer cells. Exp Biol Med (Maywood), 2008; 233: 1013-1020
19. Ma X, Yao Y, Yuan D, Liu H, Wang S, Zhou C, Song Y: Recombinant human endostatin endostar suppresses angiogenesis and lymphangiogenesis of malignant pleural effusion in mice. PloS one, 2012; 7: e53449
20. Jia H, Kling J: China offers alternative gateway for experimental drugs. Nat Biotechnol, 2006; 24: 117-118
21. Wang TB, Wei XQ, Lin WH, Shi HP, Dong WG: The inhibition of Endostar on the angiogenesis and growth of gastrointestinal stromal tumor xenograft. Clin Exp Med, 2012; 12: 89-95
22. Zhou JF, Bai CM, Wang YZ, Li XY, Cheng YJ, Chen SC: Endostar combined with chemotherapy for treatment of metastatic colorectal and gastric cancer: a pilot study. Chin Med J (Engl), 2011; 124: 4299-4303
23. Mao W, Kong J, Dai J, Huang ZQ, Wang DZ, Ni GB, Chen ML: Evaluation of recombinant endostatin in the treatment of atherosclerotic plaques and neovascularization in rabbits. J Zhejiang Univ Sci B, 2010; 11: 599-607
24. Busnelli M, Froio A, Bacci ML, Giunti M, Cerrito MG, Giovannoni R, Forni M, Gentilini F, Scagliarini A, Deleo G, Benatti C, Leone BE, Biasi GM, Lavitrano M: Pathogenetic role of hypercholesterolemia in a novel preclinical model of vascular injury in pigs. Atherosclerosis, 2009; 207: 384-390
25. Guarda E, Katwa LC, Campbell SE, Tanner MA, Webel RM, Laughlin H, Jenkins S, Myers PR: Extracellular matrix collagen synthesis and degradation following coronary balloon angioplasty. J Mol Cell Cardiol, 1996; 28: 699-706
26. de Groot E, van Leuven SI, Duivenvoorden R, Meuwese MC, Akdim F, Bots ML, Kastelein JJ: Measurement of carotid intima-media thickness to assess progression and regression of atherosclerosis. Nat Clin Pract Cardiovasc Med, 2008; 5: 280-288
27. Kleinbongard P, Heusch G, Schulz R: TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther, 2010; 127: 295-314
28. Fleiner M, Kummer M, Mirlacher M, Sauter G, Cathomas G, Krapf R, Biedermann BC: Arterial neovascularization and inflammation in vulnerable patients: early and late signs of symptomatic atherosclerosis. Circulation, 2004; 110: 2843-2850
29. Kumamoto M, Nakashima Y, Sueishi K: Intimal neovascularization in human coronary atherosclerosis: its origin and pathophysiological significance. Hum Pathol, 1995; 26: 450-456
30. Moreno PR, Purushothaman KR, Sirol M, Levy AP, Fuster V: Neovascularization in human atherosclerosis. Circulation, 2006; 113: 2245-2252
31. Herrmann J, Lerman LO, Rodriguez-Porcel M, Holmes DR Jr, Richardson DM, Ritman EL, Lerman A: Coronary vasa vasorum neovascularization precedes epicardial endothelial dysfunction in experimental hypercholesterolemia. Cardiovasc Res, 2001; 51: 762-766
32. Ritman EL, Lerman A: The dynamic vasa vasorum. Cardiovasc Res, 2007; 75: 649-658
33. Mehta JL, Chen J, Hermonat PL, Romeo F, Novelli G: Lectin-like, oxidized low-density lipoprotein receptor-1 (LOX-1): a critical player in the development of atherosclerosis and related disorders. Cardiovasc Res, 2006; 69: 36-45
34. Sluimer JC, Gasc JM, van Wanroij JL, Kisters N, Groeneweg M, Sollewijn Gelpke MD, Cleutjens JP, van den Akker LH, Corvol P, Wouters BG, Daemen MJ, Bijnens AP: Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol, 2008; 51: 1258-1265
35. Kolodgie FD, Burke AP, Nakazawa G, Cheng Q, Xu X, Virmani R: Free cholesterol in atherosclerotic plaques: where does it come from? Curr Opin Lipidol, 2007; 18: 500-507
36. Moos MP, John N, Grabner R, Nossmann S, Gunther B, Vollandt R, Funk CD, Kaiser B, Habenicht AJ: The lamina adventitia is the major site of immune cell accumulation in standard chow-fed apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol, 2005; 25: 2386-2391
37. Xiangdong L, Yuanwu L, Hua Z, Liming R, Qiuyan L, Ning L: Animal models for the atherosclerosis research: a review. Protein Cell, 2011; 2: 189-201
38. Rademakers T, Douma K, Hackeng TM, Post MJ, Sluimer JC, Daemen MJ, Biessen EA, Heeneman S, van Zandvoort MA: Plaque-associated vasa vasorum in aged apolipoprotein E-deficient mice exhibit proatherogenic functional features in vivo. Arterioscler Thromb Vasc Biol, 2013; 33: 249-256
39. Moulton KS, Vakili K, Zurakowski D, Soliman M, Butterfield C, Sylvin E, Lo KM, Gillies S, Javaherian K, Folkman J: Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci U S A, 2003; 100: 4736-4741
40. Tanabe K, Maeshima Y, Ichinose K, Kitayama H, Takazawa Y, Hirokoshi K, Kinomura M, Sugiyama H, Makino H: Endostatin peptide, an inhibitor of angiogenesis, prevents the progression of peritoneal sclerosis in a mouse experimental model. Kidney Int, 2007; 71: 227-238
41. Matsuno H, Yudoh K, Uzuki M, Nakazawa F, Sawai T, Yamaguchi N, Olsen BR, Kimura T: Treatment with the angiogenesis inhibitor endostatin: a novel therapy in rheumatoid arthritis. J Rheumatol, 2002; 29: 890-895
42. Del Porto F, Lagana B, Lai S, Nofroni I, Tinti F, Vitale M, Podesta E, Mitterhofer AP, D’Amelio R: Response to antitumour necrosis factor alpha blockade is associated with reduction of carotid intima-media thickness in patients with active rheumatoid arthritis. Rheumatology (Oxford), 2007; 46: 1111-1115
43. Branen L, Hovgaard L, Nitulescu M, Bengtsson E, Nilsson J, Jovinge S: Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol, 2004; 24: 2137-2142
44. Ridker PM, Hennekens CH, Buring JE, Rifai N: C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med, 2000; 342: 836-843
45. Duh EJ, Yang HS, Haller JA, De Juan E, Humayun MS, Gehlbach P, Melia M, Pieramici D, Harlan JB, Campochiaro PA, Zack DJ: Vitreous levels of pigment epithelium-derived factor and vascular endothelial growth factor: implications for ocular angiogenesis. Am J Ophthalmol, 2004; 137: 668-674
46. Pedram A, Razandi M, Aitkenhead M, Hughes CC, Levin ER: Integration of the non-genomic and genomic actions of estrogen. Membrane-initiated signaling by steroid to transcription and cell biology. J Biol Chem, 2002; 277: 50768-50775
47. Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD: Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med, 2001; 7: 425-429
48. Tang X, Yang Y, Yuan H, You J, Burkatovskaya M, Amar S: Novel transcriptional regulation of VEGF in inflammatory processes. J Cell Mol Med, 2013; 17: 386-397
49. Lucerna M, Zernecke A, de Nooijer R, de Jager SC, Bot I, van der Lans C, Kholova I, Liehn EA, van Berkel TJ, Yla-Herttuala S, Weber C, Biessen EA: Vascular endothelial growth factor-A induces plaque expansion in ApoE knockout mice by promoting de novo leukocyte recruitment. Blood, 2007; 109: 122-129
50. Sluimer JC, Kolodgie FD, Bijnens AP, Maxfield K, Pacheco E, Kutys B, Duimel H, Frederik PM, van Hinsbergh VW, Virmani R, Daemen MJ: Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. J Am Coll Cardiol, 2009; 53: 1517-1527
51. Rao TP, Kuhl M: An updated overview on Wnt signaling pathways: a prelude for more. Circ Res, 2010; 106: 1798-1806
52. Dejana E: The role of wnt signaling in physiological and pathological angiogenesis. Circ Res, 2010; 107: 943-952
53. Xu X, Mao W, Chen Q, Zhuang Q, Wang L, Dai J, Wang H, Huang Z: Endostar, a modified recombinant human endostatin, suppresses angiogenesis through inhibition of Wnt/beta-catenin signaling pathway. PloS one, 2014; 9: e107463
54. Feinstein SB: Contrast ultrasound imaging of the carotid artery vasa vasorum and atherosclerotic plaque neovascularization. J Am Coll Cardiol, 2006; 48: 236-243
55. Kerwin WS, Oikawa M, Yuan C, Jarvik GP, Hatsukami TS: MR imaging of adventitial vasa vasorum in carotid atherosclerosis. Magn Reson Med, 2008; 59: 507-514
56. Elice F, Rodeghiero F: Side effects of anti-angiogenic drugs. Thromb Res, 2012; 129 Suppl 1: S50-53
57. Elice F, Rodeghiero F, Falanga A, Rickles FR: Thrombosis associated with angiogenesis inhibitors. Best Pract Res Clin Haematol, 2009; 22: 115-128
58. Winter PM, Neubauer AM, Caruthers SD, Harris TD, Robertson JD, Williams TA, Schmieder AH, Hu G, Allen JS, Lacy EK, Zhang H, Wickline SA, Lanza GM: Endothelial alpha(v)beta3 integrin-targeted fumagillin nanoparticles inhibit angiogenesis in atherosclerosis. Arterioscler Thromb Vasc Biol, 2006; 26: 2103-2109