ROLE OF PERIVASCULAR ADIPOSE TISSUE IN THE DEVELOPMENT OF ATHEROSCLEROTIC AND NONATHEROSCLEROTIC DISEASES
https://doi.org/10.15789/1563-0625-2019-4-633-642
Abstract
Perivascular adipose tissue surrounds most large blood vessels and plays an important role in vascular homeostasis. Recent studies have shown that perivascular adipose tissue effects vasodilation and vasoconstriction, which indicates that the perivascular adipose tissue regulates tone and diameter of the vessels. Adipocytokines and chemokines, secreted from the perivascular adipose tissue, apparently have direct access to the adjacent arterial wall by diffusion, or through vasa vasorum. The present data indicate that perivascular adipose tissue plays an important role in atherosclerosis, hypertension. Recently, some studies were performed that examined the role of perivascular adipose tissue in non-atherosclerotic vascular diseases, such as neointimal formation, aortic aneurysm, arterial stiffness and vasculitis. The present review will discuss a role of perivascular adipose tissue in pathogenesis of atherosclerosis, hypertension and non-atherosclerotic vascular diseases.
About the Authors
E. G. Uchasova
Federal State Research Institute for Complex Issues of Cardiovascular Diseases
Russian Federation
Russian Federation
PhD (Medicine), Senior Research Associate, Laboratory of Homeostasis Research
650002, Russian Federation, Kemerovo, Sosnovy bvld, 6
Phone: 7 (3842) 64-05-53
O V Gruzdeva
Federal State Research Institute for Complex Issues of Cardiovascular Diseases;
Kemerovo State Medical University
PhD, MD (Medicine), Head, Laboratory of Homeostasis Research; Associate Professor, Department of Pathological Physiology
650002, Russian Federation, Kemerovo, Sosnovy bvld, 6
Yu A Dyleva
Federal State Research Institute for Complex Issues of Cardiovascular Diseases
PhD (Medicine), |Senior Research Associate, Laboratory of Homeostasis Research
650002, Russian Federation, Kemerovo, Sosnovy bvld, 6
E V Belik
Federal State Research Institute for Complex Issues of Cardiovascular Diseases
Junior Research Associate, Laboratory of Homeostasis Research
650002, Russian Federation, Kemerovo, Sosnovy bvld, 6
References
1. Vardulaki K.A., Walker N.M., Day N.E., Duffy S.W., Ashton H.A., Scott R.A. Quantifying the risks of hypertension, age, sex and smoking in patients with abdominal aortic aneurysm. Br. J. Surg., 2000, Vol. 87. pp. 195- 200.
2. Schroeter M.R., Eschholz N., Herzberg S., Jerchel I., Leifheit-Nestler M., Czepluch F.S., Chalikias G., Konstantinides S., Schäfer K. Leptin dependent and leptin independent paracrine effects of perivascular adipose tissue on neointima formation significance. Arterioscler. Thromb. Vasc. Biol., 2013, Vol. 33, pp. 980-987.
3. Gruzdeva O.V., Akbasheva O.E., Dyleva Yu.A., Antonova L.V., Matveeva V.G., Uchasova E.G., Fanaskova E.V., Karetnikova V.N., Ivanov S.V., Barbarash O.L. Adipokine and cytokine profiles of epicardial and subcutaneous adipose tissue in patients with coronary heart disease. Byulleten eksperimentalnoy biologii i meditsiny = Bulletin of Experimental Biology and Medicine, 2017, Vol. 163, no. 5, pp. 560-563. (In Russ.)
4. Somoza B., Guzmán R., Cano V., Merino B., Ramos P., Díez-Fernández C. Fernández-Alfonso M.S., Ruiz-Gayo M. Induction of cardiac uncoupling protein-2 expression and adenosine 5-monophosphate-activated proteinkinase phosphorylation during early states of diet-induced obesity in mice. Endocrinology, 2007, Vol. 148, pp. 924-931.
5. Verhagen S.N., Visseren F.L. Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis, 2011, Vol. 214, pp. 3-10.
6. Ott A.V., Chumakova G.A., Veselovskaya N.G. Resistance to leptin in development of different obesity phenotypes. Rossiyskiy kardiologicheskiy zhurnal = Russian Journal of Cardiology, 2016, Vol. 4, no. 132 .pp. 14-18. (In Russ.)
7. Wang P., Xu T.Y., Guan Y.F., Su D.F., Fan G.R., Miao C.Y. Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. Cardiovasc. Res., 2009, Vol. 81, pp. 370-380.
8. Takaoka M., Suzuki H., Shioda S., Sekikawa, K., Saito Y., Nagai R., Sata M. Endovascular injury induces rapid phenotypic changes in perivascular adipose tissue. Arterioscler. Thromb. Vasc. Biol., 2010, Vol. 30, pp. 1576- 1582.
9. Antonopoulos A.S., Sanna F., Sabharwal N., Thomas S., Oikonomou E.K., Herdman L. Detecting human coronary inflammation by imaging perivascular fat. Sci. Transl. Med., 2017, Vol. 9, eaal2658. doi: 10.1126/scitranslmed.aal2658.
10. Tanaka K., Sata M. Roles of Perivascular adipose tissue in the pathogenesis of atherosclerosis. Front. Physiol., Vol. 9, p. 3.
11. Wenzel U.O., Bode M., Köhl J., Ehmke H. A pathogenic role of complement in arterial hypertension and hypertensive end organ damage. Am. J. Physiol. Heart Circ. Physiol., 2017, Vol. 312, no. 3, pp. 349-354.
12. Bourlier V., Zakaroff-Girard A., Miranville A., de Barros S., Maumus M., Sengenes C. Remodeling phenotype of human subcutaneous adipose tissue macrophages. Circulation, 2008, Vol. 11, pp. 806-815.
13. Withers S.B., Agabiti-Rosei C., Livingstone D.M., Little M.C., Aslam R., Malik R.A. Heagerty A.M. Arterioscler. Thromb. Vasc. Biol., 2011, Vol. 31, no. 4, pp. 908-913.
14. Tchkonia T., Lenburg M., Thomou T., Giorgadze N., Frampton G., Pirtskhalava T., Cartwright A., Cartwright M., Flanagan J., Karagiannides I., Gerry N., Forse R.A., Tchoukalova Y., Jensen M.D., Pothoulakis C., Kirkland J.L. Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am. J. Physiol. Endocrinol. Metab., 2007, Vol. 292, pp. 298-307.
15. Britton K.A., Wang N., Palmisano J., Corsini E., Schlett C.L., Hoffmann U. Thoracic periaortic and visceral adipose tissue and their cross-sectional associations with measures of vascular function. Obesity (Silver Spring), 2013, Vol. 21, no. 7, pp. 1496-1503.
16. Thanassoulis G., Massaro J.M., Corsini E., Rogers I., Schlett C.L., Meigs J.B., Hoffmann U., O’Donnell C.J., Fox C.S. Periaortic adipose tissue and aortic dimensions in the Framingham Heart Study. J. Am. Heart Assoc., 2012, Vol. 1, e000885. doi:10.1161/JAHA.112.000885.
17. Yilmaz H., Gerdan V., Kozaci D., Solmaz D., Akar S., Can G., Gulcu A., Goktay Y., Sari I., Birlik M., Akkoc N., Onen F. Ghrelin and adipokines as circulating markers of disease activity in patients with Takayasu arteritis. Arthritis Res. Ther., 2012, Vol. 14, p. 272.
18. Brown N.K., Zhou Z., Zhang J., Zeng R., Wu J., Eitzman D.T., Chen Y.E., Chang L. Perivascular adipose tissue in vascular function and disease. Arterioscler. Thromb. Vasc. Biol., 2014, Vol. 34, no. 8, pp. 1621-1630.
19. Zhang L.N., Wilson D.W., Cunha V.D., Sullivan M.E., Vergona R., Rutledge J.C., Wang Y.X. Endothelial NO synthase deficiency promotes smooth muscle progenitor cells in association with upregulation of stromal cell derived factor-1a in a mouse model of carotid artery ligation. Arterioscler. Thromb. Vasc. Biol., 2006, Vol. 26, pp. 765-772.
20. Tian Z., Miyata K., Tazume H., Sakaguchi H., Kadomatsu T., Horio E., Komohara Y., Araki K., Hirata Y., Tabata M., Takanashi S., Takeya M., Hao H., Shimabukuro M., Sata M., Kawasuji M., Oike Y. Perivascular adipose tissue-secreted angiopoietin-like protein 2 (Angptl2) accelerates neointimal hyperplasia after endovascular injury. J. Mol. Cell. Cardiol., 2013, Vol. 57, pp. 1-12.
21. Cai X., Lin Y., Hauschka P.V., Grottkau B.E. Adipose stem cells originate from perivascular cells. Biol. Cell, 2011, Vol. 103, pp. 435-447.
22. van Dam A.D., Boon M.R., Berbée J.F.P., Rensen P.C.N., van Harmelen V. Targeting white, brown and perivascular adipose tissue in atherosclerosis development. Eur. J. Pharmacol., 2017, Vol. 816, pp. 82-92.
23. Chang L., Villacorta L., Li R., Hamblin M., Xu W., Dou C., Zhang J., Wu J., Zeng R., Chen Y.E. Loss of perivascular adipose tissue on peroxisome proliferator-activated receptor-gamma deletion in smooth muscle cells impairs intravascular thermoregulation and enhances atherosclerosis. Circulation, 2012, Vol. 126, pp. 1067-1078.
24. Vardulaki K.A., Walker N.M., Day N.E., Duffy S.W., Ashton H.A., Scott R.A. Quantifying the risks of hypertension, age, sex and smoking in patients with abdominal aortic aneurysm. Br. J. Surg., 2000, Vol. 87. pp. 195- 200.
25. Chatterjee T.K., Stoll L.L., Denning G.M., Harrelson A., Blomkalns A.L., Idelman G., Rothenberg F.G., Neltner B., Romig-Martin S.A., Dickson E.W., Rudich S., Weintraub N.L. Proinflammatory phenotype of perivascular adipocytes: Influence of high-fat feeding. Circ. Res., 2009, Vol. 104, pp. 541-549.
26. Verhagen S.N., Visseren F.L. Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis, 2011, Vol. 214, pp. 3-10.
27. Chen J.Y., Tsai P.J., Tai H.C., Tsai R.L., Chang Y.T., Wang M.C., Chiou Y.W., Yeh M.L., Tang M.J., Lam C.F., Shiesh S.C., Li Y.H., Tsai W.C., Chou C.H., Lin L.J., Wu H.L., Tsai Y.S. Increased aortic stiffness and attenuated lysyl oxidase activity in obesity significance. Arterioscler. Thromb. Vasc. Biol., 2013, Vol. 33, pp. 839-846.
28. Wang P., Xu T.Y., Guan Y.F., Su D.F., Fan G.R., Miao C.Y. Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. Cardiovasc. Res., 2009, Vol. 81, pp. 370-380.
29. Chen Y.C., Huang, A.L., Kyaw T.S., Bobik A., Peter K. Atherosclerotic plaque rupture: identifying the straw that breaks the camel’s back. Arterioscler. Thromb. Vasc. Biol., 2016, Vol. 36, pp. 63-72.
30. Wenzel U.O., Bode M., Köhl J., Ehmke H. A pathogenic role of complement in arterial hypertension and hypertensive end organ damage. Am. J. Physiol. Heart Circ. Physiol., 2017, Vol. 312, no. 3, pp. 349-354.
31. Cronin O., Walker P. J., Golledge J. The association of obesity with abdominal aortic aneurysm presence and growth. Atherosclerosis, 2013, Vol. 226, pp. 321-327.
32. Withers S.B., Agabiti-Rosei C., Livingstone D.M., Little M.C., Aslam R., Malik R.A. Heagerty A.M. Arterioscler. Thromb. Vasc. Biol., 2011, Vol. 31, no. 4, pp. 908-913.
33. Du B., Ouyang A., Eng J.S., Fleenor B.S. Aortic perivascular adiposederived interleukin-6 contributes to arterial stiffness in low-density lipoprotein receptor deficient mice. Am. J. Physiol. Heart Circ. Physiol., 2015, Vol. 308, pp. 1382-1390.
34. Yilmaz H., Gerdan V., Kozaci D., Solmaz D., Akar S., Can G., Gulcu A., Goktay Y., Sari I., Birlik M., Akkoc N., Onen F. Ghrelin and adipokines as circulating markers of disease activity in patients with Takayasu arteritis. Arthritis Res. Ther., 2012, Vol. 14, p. 272.
35. Zhang L.N., Wilson D.W., Cunha V.D., Sullivan M.E., Vergona R., Rutledge J.C., Wang Y.X. Endothelial NO synthase deficiency promotes smooth muscle progenitor cells in association with upregulation of stromal cell derived factor-1a in a mouse model of carotid artery ligation. Arterioscler. Thromb. Vasc. Biol., 2006, Vol. 26, pp. 765-772.
36. Fernández-Alfonso M.S., Somoza B., Tsvetkov D., Kuczmanski A., Dashwood M., Gil-Ortega M. Role of perivascular adipose tissue in health and disease. Compr. Physiol., 2018, Vol. 8, pp. 23-59.
37. Fitzgibbons T.P., Czech M.P. Epicardial and perivascular adipose tissues and their influence on cardiovascular disease: basic mechanisms and clinical associations. J. Am. Heart Assoc., 2014, Vol. 3, e000582. doi: 10.1161/JAHA.113.000582.
38. Fleenor B.S., Eng J.S., Sindler A.L., Pham B.T., Kloor J.D., Seals D.R. Superoxide signaling in perivascular adipose tissue promotes age-related artery stiffness. Aging Cell, 2014, Vol. 13, pp. 576-578.
39. Folkesson M., Vorkapic E., Gulbins E., Japtok L., Kleuser B., Welander M., Länne T., Wågsäter D. Inflammatory cells, ceramides, and expression of proteases in perivascular adipose tissue adjacent to human abdominal aortic aneurysms. J. Vasc. Surg., 2017, Vol. 65, pp. 1171-1179.
40. Gálvez-Prieto B., Somoza B., Gil-Ortega M., García-Prieto C.F., de Las Heras A.I., González M.C., Arribas S., Aranguez I., Bolbrinker J., Kreutz R., Ruiz-Gayo M., Fernández-Alfonso M.S. Anticontractile effect of perivascular adipose tissue and leptin are reduced in hypertension. Front. Pharmacol., 2012, Vol. 3, p. 103.
41. Gao Y.J., Takemori K., Su L.Y., An W.S., Lu C., Sharma A.M., Lee R.M. Perivascular adipose tissue promotes vasoconstriction: the role of superoxide anion. Cardiovasc. Res., 2006, Vol. 71, pp. 363-373.
42. Gil-Ortega M., Condezo-Hoyos L., García-Prieto C.F., Arribas S.M., González M.C., Aranguez I., Ruiz-Gayo M., Somoza B., Fernández-Alfonso M.S. Imbalance between pro and anti-oxidant mechanisms in perivascular adipose tissue aggravates long-term high-fat diet-derived endothelial dysfunction. PLoS ONE, 2014, Vol. 9, no. 4, e95312. doi: 10.1371/journal.pone.0095312.
43. Goel S.A., Guo L.W., Liu B., Kent K.C. Mechanisms of post-intervention arterial remodelling. Cardiovasc. Res., 2012, Vol. 96, pp. 363-371.
44. Gotway M.B., Araoz P.A., Macedo T.A., Stanson A.W., Higgins C.B., Ring E.J., Dawn S.K., Webb W.R., Leung J.W., Reddy G.P. Imaging findings in Takayasu’s arteritis. Am. J. Roentgenol., 2005, Vol. 184, pp. 1945-1950.
45. Gruzdeva O., Uchasova E., Dyleva Y., Borodkina D., Akbasheva O., Belik E., Karetnikova V., Brel N., Kokov A., Kashtalap V., Barbarash O. Relationships between epicardial adipose tissue thickness and adipo-fibrokine indicator profiles post-myocardial infarction. Cardiovasc. Diabetol., 2018, Vol. 17, p. 40.
46. Hansson G.K., Hermansson A. The immune system in atherosclerosis. Nat. Immunol., 2011, Vol. 12, pp. 204-212.
47. Horimatsu T., Kim H.W., Weintraub N.L. The role of perivascular adipose tissue in non-atherosclerotic vascular disease. Front. Physiol., 2017, Vol. 8, p. 969.
48. Kitzman D.W., Herrington D.M., Brubaker P.H., Moore J.B., Eggebeen J., Haykowsky M.J. Carotid arterial stiffness and its relationship to exercise intolerance in older patients with heart failure and preserved ejection fraction. Hypertension, 2013, Vol. 61, pp. 112-119.
49. Knudson J.D., Payne G.A., Borbouse L., Tune J.D. Leptin and mechanisms of endothelial dysfunction and cardiovascular disease. Curr. Hypertens. Rep., 2008, Vol. 10, pp. 434-439.
50. Kuivaniemi H., Ryer E.J., Elmore J.R., Tromp G. Understanding the pathogenesis of abdominal aortic aneurysms. Expert Rev. Cardiovasc. Ther., 2015, Vol. 13, pp. 975-987.
51. Lederle F.A., Johnson G.R., Wilson S.E., Ballard D.J., Jordan W.D. Jr., Blebea J., Littooy F.N., Freischlag J.A., Bandyk D., Rapp J.H., Salam A.A. Rupture rate of large abdominal aortic aneurysms in patients refusing or unfit for elective repair. JAMA, 2002, Vol. 287, pp. 2968-2972.
52. Lee M.H., Chen S.J., Tsao C.M., Wu C.C. Perivascular adipose tissue inhibits endothelial function of rat aortas via caveolin-1. PLoS ONE, 2014, Vol. 9, e99947. doi:10.1371/journal.pone.0099947.
53. Li H., Wang Y.P., Zhang L.N., Tian G. Perivascular adipose tissue derived leptin promotes vascular smooth muscle cell phenotypic switching via p38 mitogen-activated protein kinase in metabolic syndrome rats. Exp. Biol. Med., 2014, Vol. 239, pp. 954-965.
54. Lohn M., Dubrovska G., Lauterbach B., Luft F.C., Gollasch M., Sharma A.M., Periadventitial fat releases a vascular relaxing factor. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol., 2002, Vol. 16, pp. 1057-1063.
55. Matsuda M., Shimomura I., Sata M., Arita Y., Nishida M., Maeda N. Kumada M., Okamoto Y., Nagaretani H., Nishizawa H., Kishida K., Komuro R., Ouchi N., Kihara S., Nagai R., Funahashi T., Matsuzawa Y. Role of adiponectin in preventing vascular stenosis the missing link of adipovascular axis. J. Biol. Chem., 2002, Vol. 277, pp. 37487-37491.
56. Mauro C.R., Ilonzo G., Nguyen B.T., Yu P., Tao M., Gao I., Seidman M.A., Nguyen L.L., Ozaki C.K. Attenuated adiposopathy in perivascular adipose tissue compared with subcutaneous human adipose tissue. Am. J. Surg., 2013, Vol. 206, pp. 241-244.
57. Miao C.Y., Li Z.Y. The role of perivascular adipose tissue in vascular smooth muscle cell growth. Br. J. Pharmacol., 2012, Vol. 165, pp. 643-658.
58. Padilla J., Jenkins N.T., Vieira-Potter V.J., Laughlin M.H. Divergent phenotype of rat thoracic and abdominal perivascular adipose tissues. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2013, Vol. 304, pp. 543-552.
59. Payne G.A., Bohlen H.G., Dincer U.D., Borbouse L., Tune J.D. Periadventitial adipose tissue impairs coronary endothelial function via PKC beta-dependent phosphorylation of nitric oxide synthase. Am. J. Physiol. Heart. Circ. Physiol., 2009, Vol. 297, pp. 460-465.
60. Rajsheker S., Manka D., Blomkalns, A.L., Chatterjee T.K., Stoll L.L., Weintraub N.L. Crosstalk between perivascular adipose tissue and blood vessels. Curr. Opin. Pharmacol., 2010, Vol. 10, pp. 191-196.
61. Richards B.L., March L., Gabriel S.E. Epidemiology of large-vessel vasculidities. Best Pract. Res. Clin. Rheumatol., 2010, Vol. 24, pp. 871-883.
62. Rossi C., Santini E., Chiarugi M., Salvati A., Comassi M., Vitolo E., Solini A. The complex P2X7 receptor/inflammasome in perivascular fat tissue of heavy smokers. Eur. J. Clin. Invest., 2014, Vol. 44, pp. 295-302.
63. Rudic R.D., Shesely E. G., Maeda N., Smithies O., Segal S.S., Sessa W.C. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J. Clin. Invest., 1998, Vol. 101, pp. 731-736.
64. Sahin A.S., Bariskaner H., Gökbel H., Okudan N. The dual effects of leptin on aortic rings with and without endothelium isolated from streptozotocin-induced diabetic rats. Methods Find. Exp. Clin. Pharmacol., 2009, Vol. 31, pp. 325-329.
65. Schnabel R., Larson M.G., Dupuis J., Lunetta K.L., Lipinska I., Meigs J.B., Yin X., Rong J., Vita J.A., Newton-Cheh C., Levy D., Keaney J.F. Jr, Vasan R.S., Mitchell G.F., Benjamin E.J. Relations of inflammatory biomarkers and common genetic variants with arterial stiffness and wave reflection. Hypertension, 2008,Vol. 51, pp. 1651-1657.
66. Schroeter M.R., Eschholz N., Herzberg S., Jerchel I., Leifheit-Nestler M., Czepluch F.S., Chalikias G., Konstantinides S., Schäfer K. Leptin dependent and leptin independent paracrine effects of perivascular adipose tissue on neointima formation significance. Arterioscler. Thromb. Vasc. Biol., 2013, Vol. 33, pp. 980-987.
67. Somoza B., Guzmán R., Cano V., Merino B., Ramos P., Díez-Fernández C. Fernández-Alfonso M.S., Ruiz-Gayo M. Induction of cardiac uncoupling protein-2 expression and adenosine 5-monophosphate-activated proteinkinase phosphorylation during early states of diet-induced obesity in mice. Endocrinology, 2007, Vol. 148, pp. 924-931.
68. Takaoka M., Suzuki H., Shioda S., Sekikawa, K., Saito Y., Nagai R., Sata M. Endovascular injury induces rapid phenotypic changes in perivascular adipose tissue. Arterioscler. Thromb. Vasc. Biol., 2010, Vol. 30, pp. 1576- 1582.
69. Tanaka K., Sata M. Roles of Perivascular adipose tissue in the pathogenesis of atherosclerosis. Front. Physiol., Vol. 9, p. 3.
70. Tchkonia T., Lenburg M., Thomou T., Giorgadze N., Frampton G., Pirtskhalava T., Cartwright A., Cartwright M., Flanagan J., Karagiannides I., Gerry N., Forse R.A., Tchoukalova Y., Jensen M.D., Pothoulakis C., Kirkland J.L. Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am. J. Physiol. Endocrinol. Metab., 2007, Vol. 292, pp. 298-307.
71. Thanassoulis G., Massaro J.M., Corsini E., Rogers I., Schlett C.L., Meigs J.B., Hoffmann U., O’Donnell C.J., Fox C.S. Periaortic adipose tissue and aortic dimensions in the Framingham Heart Study. J. Am. Heart Assoc., 2012, Vol. 1, e000885. doi:10.1161/JAHA.112.000885.
72. Tian Z., Miyata K., Tazume H., Sakaguchi H., Kadomatsu T., Horio E., Komohara Y., Araki K., Hirata Y., Tabata M., Takanashi S., Takeya M., Hao H., Shimabukuro M., Sata M., Kawasuji M., Oike Y. Perivascular adipose tissue-secreted angiopoietin-like protein 2 (Angptl2) accelerates neointimal hyperplasia after endovascular injury. J. Mol. Cell. Cardiol., 2013, Vol. 57, pp. 1-12.
73. van Dam A.D., Boon M.R., Berbée J.F.P., Rensen P.C.N., van Harmelen V. Targeting white, brown and perivascular adipose tissue in atherosclerosis development. Eur. J. Pharmacol., 2017, Vol. 816, pp. 82-92.
74. Vardulaki K.A., Walker N.M., Day N.E., Duffy S.W., Ashton H.A., Scott R.A. Quantifying the risks of hypertension, age, sex and smoking in patients with abdominal aortic aneurysm. Br. J. Surg., 2000, Vol. 87. pp. 195- 200.
75. Verhagen S.N., Visseren F.L. Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis, 2011, Vol. 214, pp. 3-10.
76. Wang P., Xu T.Y., Guan Y.F., Su D.F., Fan G.R., Miao C.Y. Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. Cardiovasc. Res., 2009, Vol. 81, pp. 370-380.
77. Wenzel U.O., Bode M., Köhl J., Ehmke H. A pathogenic role of complement in arterial hypertension and hypertensive end organ damage. Am. J. Physiol. Heart Circ. Physiol., 2017, Vol. 312, no. 3, pp. 349-354.
78. Withers S.B., Agabiti-Rosei C., Livingstone D.M., Little M.C., Aslam R., Malik R.A. Heagerty A.M. Arterioscler. Thromb. Vasc. Biol., 2011, Vol. 31, no. 4, pp. 908-913.
79. Yilmaz H., Gerdan V., Kozaci D., Solmaz D., Akar S., Can G., Gulcu A., Goktay Y., Sari I., Birlik M., Akkoc N., Onen F. Ghrelin and adipokines as circulating markers of disease activity in patients with Takayasu arteritis. Arthritis Res. Ther., 2012, Vol. 14, p. 272.
80. Zhang L.N., Wilson D.W., Cunha V.D., Sullivan M.E., Vergona R., Rutledge J.C., Wang Y.X. Endothelial NO synthase deficiency promotes smooth muscle progenitor cells in association with upregulation of stromal cell derived factor-1a in a mouse model of carotid artery ligation. Arterioscler. Thromb. Vasc. Biol., 2006, Vol. 26, pp. 765-772.
Review
For citations:
Uchasova E.G., Gruzdeva O.V., Dyleva Yu.A., Belik E.V. ROLE OF PERIVASCULAR ADIPOSE TISSUE IN THE DEVELOPMENT OF ATHEROSCLEROTIC AND NONATHEROSCLEROTIC DISEASES. Medical Immunology (Russia). 2019;21(4):633-642. (In Russ.) https://doi.org/10.15789/1563-0625-2019-4-633-642
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