Macrophages transmit potent proangiogenic effects of oxLDL in vitro and in vivo involving HIF-1α Activation: A novel aspect of angiogenesis in atherosclerosis

Journal of Cardiovascular Translational Research

Volumn 6, Issue 4, 2013, Pages 558-569

  Hutter, Randolph ^a   Speidl, Walter S ^a   Valdiviezo, Carolina ^a   Sauter, Bernhard ^a   Corti, Roberto ^a   Fuster, Valentin ^a   Badimon, Juan J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Atherosclerosis; Inflammation; Lipids

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXIDIZED LOW DENSITY LIPOPROTEIN; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HYPERLIPIDEMIA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LOW FAT DIET; MACROPHAGE FUNCTION; MALE; MOLECULAR PATHOLOGY; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; THERAPY EFFECT;

ANIMALS; ATHEROSCLEROSIS; CELLS, CULTURED; COCULTURE TECHNIQUES; DIET, FAT-RESTRICTED; DISEASE MODELS, ANIMAL; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIPOPROTEINS, LDL; MACROPHAGES; MALE; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PARACRINE COMMUNICATION; RABBITS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ORYCTOLAGUS CUNICULUS;

EID: 84880512414     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-013-9469-9     Document Type: Article

References (45)

1. Burke, A. P.; Farb, A.; Malcom, G. T.; Liang, Y. H.; Smialek, J.; & Virmani, R. (1997). Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. The New England Journal of Medicine, 336(18), 1276-1282. doi: 10.1056/NEJM199705013361802.
2. Michel, J. B.; Virmani, R.; Arbustini, E.; & Pasterkamp, G. (2011). Intraplaque haemorrhages as the trigger of plaque vulnerability. European Heart Journal, 32(16), 1977-1985. doi: 10.1093/eurheartj/ehr054. 1985a, 1985b, 1985c.
3. Moreno, P. R.; Purushothaman, K. R.; Sirol, M.; Levy, A. P.; & Fuster, V. (2006). Neovascularization in human atherosclerosis. Circulation, 113(18), 2245-2252. doi: 10.1161/CIRCULATIONAHA.105.578955.
4. Moreno, P. R.; Sanz, J.; & Fuster, V. (2009). Promoting mechanisms of vascular health: circulating progenitor cells, angiogenesis, and reverse cholesterol transport. Journal of the American College of Cardiology, 53(25), 2315-2323. doi: 10.1016/j.jacc.2009.02.057.
5. Moulton, K. S.; Vakili, K.; Zurakowski, D.; Soliman, M.; Butterfield, C.; Sylvin, E.; et al. (2003). Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proceedings of the National Academy of Sciences of the United States of America, 100(8), 4736-4741. doi: 10.1073/pnas.0730843100.
6. Groszek, E.; & Grundy, S. M. (1980). The possible role of the arterial microcirculation in the pathogenesis of atherosclerosis. Journal of Chronic Diseases, 33(11-12), 679-684.
7. Hutter, R.; Valdiviezo, C.; Sauter, B. V.; Savontaus, M.; Chereshnev, I.; Carrick, F. E.; et al. (2004). Caspase-3 and tissue factor expression in lipid-rich plaque macrophages: evidence for apoptosis as link between inflammation and atherothrombosis. Circulation, 109(16), 2001-2008. doi: 10.1161/01.CIR.0000125526.91945.AE.
8. Palinski, W.; Rosenfeld, M. E.; Yla-Herttuala, S.; Gurtner, G. C.; Socher, S. S.; Butler, S. W.; et al. (1989). Low density lipoprotein undergoes oxidative modification in vivo. Proceedings of the National Academy of Sciences of the United States of America, 86(4), 1372-1376.
9. Parthasarathy, S.; Quinn, M. T.; Schwenke, D. C.; Carew, T. E.; & Steinberg, D. (1989). Oxidative modification of beta-very low density lipoprotein. Potential role in monocyte recruitment and foam cell formation. Arteriosclerosis, 9(3), 398-404.
10. Yla-Herttuala, S.; Palinski, W.; Rosenfeld, M. E.; Parthasarathy, S.; Carew, T. E.; Butler, S.; et al. (1989). Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. The Journal of Clinical Investigation, 84(4), 1086-1095. doi: 10.1172/JCI114271.
11. Vink, A.; Schoneveld, A. H.; Lamers, D.; Houben, A. J.; van der Groep, P.; van Diest, P. J.; et al. (2007). HIF-1 alpha expression is associated with an atheromatous inflammatory plaque phenotype and upregulated in activated macrophages. Atherosclerosis, 195(2), e69-75. doi: 10.1016/j.atherosclerosis. 2007.05.026.
12. Sluimer, J. C.; Gasc, J. M.; van Wanroij, J. L.; Kisters, N.; Groeneweg, M.; Sollewijn Gelpke, M. D.; et al. (2008). Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. Journal of the American College of Cardiology, 51(13), 1258-1265. doi: 10.1016/j.jacc.2007.12.025.
13. Kai, H.; Kuwahara, F.; Tokuda, K.; Shibata, R.; Kusaba, K.; Niiyama, H.; et al. (2002). Coexistence of hypercholesterolemia and hypertension impairs adventitial vascularization. Hypertension, 39(2 Pt 2), 455-459.
14. Karshovska, E.; Zernecke, A.; Sevilmis, G.; Millet, A.; Hristov, M.; Cohen, C. D.; et al. (2007). Expression of HIF-1alpha in injured arteries controls SDF-1alpha mediated neointima formation in apolipoprotein E deficient mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(12), 2540-2547. doi: 10.1161/ATVBAHA.107.151050.
15. Higashida, T.; Kanno, H.; Nakano, M.; Funakoshi, K.; & Yamamoto, I. (2008). Expression of hypoxia-inducible angiogenic proteins (hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and E26 transformation- specific-1) and plaque hemorrhage in human carotid atherosclerosis. Journal of Neurosurgery, 109(1), 83-91. doi: 10.3171/JNS/2008/109/7/0083.
16. Mayr, M.; Sidibe, A.; & Zampetaki, A. (2008). The paradox of hypoxic and oxidative stress in atherosclerosis. Journal of the American College of Cardiology, 51(13), 1266-1267. doi: 10.1016/j.jacc.2008.01.005.
17. Bosco, M. C.; Puppo, M.; Blengio, F.; Fraone, T.; Cappello, P.; Giovarelli, M.; et al. (2008). Monocytes and dendritic cells in a hypoxic environment: spotlights on chemotaxis and migration. Immunobiology, 213(9-10), 733-749. doi: 10.1016/j.imbio.2008.07.031.
18. Deguchi, J. O.; Yamazaki, H.; Aikawa, E.; & Aikawa, M. (2009). Chronic hypoxia activates the Akt and beta-catenin pathways in human macrophages. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(10), 1664-1670. doi: 10.1161/ATVBAHA.109.194043.
19. Elbarghati, L.; Murdoch, C.; & Lewis, C. E. (2008). Effects of hypoxia on transcription factor expression in human monocytes and macrophages. Immunobiology, 213(9-10), 899-908. doi: 10.1016/j.imbio.2008.07.016.
20. Poitz, D. M.; Augstein, A.; Weinert, S.; Braun-Dullaeus, R. C.; Strasser, R. H.; & Schmeisser, A. (2011). OxLDL and macrophage survival: essential and oxygen-independent involvement of the Hif-pathway. Basic Research in Cardiology, 106(5), 761-772. doi: 10.1007/s00395-011-0186-8.
21. Ribatti, D.; Levi-Schaffer, F.; & Kovanen, P. T. (2008). Inflammatory angiogenesis in atherogenesis - a double-edged sword. Annals of Medicine, 40(8), 606-621. doi: 10.1080/07853890802186913.
22. West, X. Z.; Malinin, N. L.; Merkulova, A. A.; Tischenko, M.; Kerr, B. A.; Borden, E. C.; et al. (2010). Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature, 467(7318), 972-976. doi: 10.1038/nature09421.
23. Yu, S.; Wong, S. L.; Lau, C. W.; Huang, Y.; & Yu, C. M. (2011). Oxidized LDL at low concentration promotes in-vitro angiogenesis and activates nitric oxide synthase through PI3K/Akt/eNOS pathway in human coronary artery endothelial cells. Biochemical and Biophysical Research Communications, 407(1), 44-48. doi: 10.1016/j.bbrc.2011.02.096.
24. Shatrov, V. A.; Sumbayev, V. V.; Zhou, J.; & Brune, B. (2003). Oxidized low-density lipoprotein (oxLDL) triggers hypoxia-inducible factor-1alpha (HIF-1alpha) accumulation via redox-dependent mechanisms. Blood, 101(12), 4847-4849. doi: 10.1182/blood-2002-09-2711.
25. Kessler J, Hahnel A, Wichmann H, Rot S, Kappler M, Bache M, Vordermark D (2010) HIF-1alpha inhibition by siRNA or chetomin in human malignant glioma cells: effects on hypoxic radioresistance and monitoring via CA9 expression. BMC cancer 10:605. doi: 10.1186/1471-2407-10-605
26. Bouvard, C.; De Arcangelis, A.; Dizier, B.; Galy-Fauroux, I.; Fischer, A. M.; Georges-Labouesse, E.; et al. (2012). Tie2-dependent knockout of alpha6 integrin subunit in mice reduces post-ischaemic angiogenesis. Cardiovascular Research. doi: 10.1093/cvr/cvs153.
27. Corti, R.; Osende, J. I.; Fallon, J. T.; Fuster, V.; Mizsei, G.; Jneid, H.; et al. (2004). The selective peroxisomal proliferator-activated receptor-gamma agonist has an additive effect on plaque regression in combination with simvastatin in experimental atherosclerosis: in vivo study by high-resolution magnetic resonance imaging. Journal of the American College of Cardiology, 43(3), 464-473. doi: 10.1016/j.jacc.2003.08.048.
28. Giannarelli, C.; Cimmino, G.; Connolly, T. M.; Ibanez, B.; Ruiz, J. M.; Alique, M.; et al. (2012). Synergistic effect of liver X receptor activation and simvastatin on plaque regression and stabilization: an magnetic resonance imaging study in a model of advanced atherosclerosis. European Heart Journal, 33(2), 264-273. doi: 10.1093/eurheartj/ehr136.
29. Lewis, C.; & Murdoch, C. (2005). Macrophage responses to hypoxia: implications for tumor progression and anti-cancer therapies. The American Journal of Pathology, 167(3), 627-635. doi: 10.1016/S0002-9440(10)62038-X.
30. Chavakis, E.; Dernbach, E.; Hermann, C.; Mondorf, U. F.; Zeiher, A. M.; & Dimmeler, S. (2001). Oxidized LDL inhibits vascular endothelial growth factor-induced endothelial cell migration by an inhibitory effect on the Akt/endothelial nitric oxide synthase pathway. Circulation, 103(16), 2102-2107.
31. Wu, Y.; Wang, Q.; Cheng, L.; Wang, J.; & Lu, G. (2009). Effect of oxidized low-density lipoprotein on survival and function of endothelial progenitor cell mediated by p38 signal pathway. Journal of Cardiovascular Pharmacology, 53(2), 151-156. doi: 10.1097/FJC.0b013e318197c637.
32. Haddad, P.; Dussault, S.; Groleau, J.; Turgeon, J.; Maingrette, F.; & Rivard, A. (2011). Nox2-derived reactive oxygen species contribute to hypercholesterolemia-induced inhibition of neovascularization: effects on endothelial progenitor cells and mature endothelial cells. Atherosclerosis, 217(2), 340-349. doi: 10.1016/j.atherosclerosis.2011.03.038.
33. Squadrito, M. L.; & De Palma, M. (2011). Macrophage regulation of tumor angiogenesis: implications for cancer therapy. Molecular Aspects of Medicine, 32(2), 123-145. doi: 10.1016/j.mam.2011.04.005.
34. Casazza, A.; Fu, X.; Johansson, I.; Capparuccia, L.; Andersson, F.; Giustacchini, A.; et al. (2011). Systemic and targeted delivery of semaphorin 3A inhibits tumor angiogenesis and progression in mouse tumor models. Arteriosclerosis, Thrombosis, and Vascular Biology, 31(4), 741-749. doi: 10.1161/ATVBAHA.110.211920.
35. Baer, C.; Squadrito, M. L.; Iruela-Arispe, M. L.; & De Palma, M. (2013). Reciprocal interactions between endothelial cells and macrophages in angiogenic vascular niches. Experimental Cell Research. doi: 10.1016/j.yexcr.2013.03.026.
36. Khaidakov, M.; Mitra, S.; Wang, X.; Ding, Z.; Bora, N.; Lyzogubov, V.; et al. (2012). Large impact of low concentration oxidized LDL on angiogenic potential of human endothelial cells: a microarray study. PloS One, 7(10), e47421. doi: 10.1371/journal.pone.0047421.
37. Norrby, K. (2006). In vivo models of angiogenesis. Journal of Cellular and Molecular Medicine, 10(3), 588-612.
38. Jeanpierre, E.; Le Tourneau, T.; Six, I.; Zawadzki, C.; Van Belle, E.; Ezekowitz, M. D.; et al. (2003). Dietary lipid lowering modifies plaque phenotype in rabbit atheroma after angioplasty: a potential role of tissue factor. Circulation, 108(14), 1740-1745. doi: 10.1161/01.CIR.0000089370.84709. 51.
39. Srimahachota, S.; Wunsuwan, R.; Siritantikorn, A.; Boonla, C.; Chaiwongkarjohn, S.; & Tosukhowong, P. (2010). Effects of lifestyle modification on oxidized LDL, reactive oxygen species production and endothelial cell viability in patients with coronary artery disease. Clinical Biochemistry, 43(10-11), 858-862. doi: 10.1016/j.clinbiochem.2010.04.056.
40. Tonstad, S.; Sundfor, T.; & Seljeflot, I. (2005). Effect of lifestyle changes on atherogenic lipids and endothelial cell adhesion molecules in young adults with familial premature coronary heart disease. The American Journal of Cardiology, 95(10), 1187-1191. doi: 10.1016/j.amjcard.2005.01.047.
41. Verhamme, P.; Quarck, R.; Hao, H.; Knaapen, M.; Dymarkowski, S.; Bernar, H.; et al. (2002). Dietary cholesterol withdrawal reduces vascular inflammation and induces coronary plaque stabilization in miniature pigs. Cardiovascular Research, 56(1), 135-144.
42. Inoue, T.; Hayashi, M.; Takayanagi, K.; & Morooka, S. (2002). Lipid-lowering therapy with fluvastatin inhibits oxidative modification of low density lipoprotein and improves vascular endothelial function in hypercholesterolemic patients. Atherosclerosis, 160(2), 369-376.
43. Inoue, T.; Yaguchi, I.; Uchida, T.; Kamishirado, H.; Nakahara, S.; Hayashi, T.; et al. (2002). Clinical significance of the antibody against oxidized low-density lipoprotein in acute myocardial infarction. Cardiology, 98(1-2), 13-17.
44. Shimada, K.; Mokuno, H.; Matsunaga, E.; Miyazaki, T.; Sumiyoshi, K.; Kume, A.; et al. (2004). Predictive value of circulating oxidized LDL for cardiac events in type 2 diabetic patients with coronary artery disease. Diabetes Care, 27(3), 843-844.
45. Shimada, K.; Mokuno, H.; Matsunaga, E.; Miyazaki, T.; Sumiyoshi, K.; Miyauchi, K.; et al. (2004). Circulating oxidized low-density lipoprotein is an independent predictor for cardiac event in patients with coronary artery disease. Atherosclerosis, 174(2), 343-347. doi: 10.1016/j.atherosclerosis.2004. 01.029.