Advances in dual regulation of atherosclerotic pathways by perivascular adipose tissue

Main Article Content

Kou Haixin
Chang Xindi
Guo Shuaijie
Zhang Yifan
Liu Ping

Abstract

Atherosclerosis (AS) is formed due to complex interactions between vascular cells and inflammatory factors. During the development of AS, perivascular inflammatory factors are closely associated with perivascular adipose tissue (PVAT), which regulates the development of AS through the secretion of different factors, and the brown adipose tissue it contains may have a positive regulatory effect on AS. Therefore, activating PVAT and browning it may be a new target for the treatment of cardiovascular diseases such as AS. A variety of Chinese herbal medicine active ingredients and compounds have been found to promote adipose tissue browning. In this paper, we review the pathways of PVAT dual regulation of AS and the progress of adipose tissue browning research.

Article Details

Section
Review Article

References

Kim HW, Shi H, Winkler MA, Lee R, Weintraub NL. Perivascular adipose tissue and vascular perturbation/atherosclerosis. Arterioscler Thromb Vasc Biol. 2020;40(11):2569-76.

Nosalski R, Guzik TJ. Perivascular adipose tissue inflammation in vascular disease. Br J Pharmacol. 2017;174(20):3496-513.

Mu WJ, Yang LJ, Song SS, Tang Y. Research progress of different adipose tissues and atherosclerosis. Chinese Bulletin of Life Sciences. 2021;33(2):166-75. (in Chinese)

Withers SB, Forman R, Meza-Perez S, Sorobetea D, Sitnik K, Hopwood T, et al. Eosinophils are key regulators of perivascular adipose tissue and vascular functionality. Sci Rep. 2017;7:44571.

Xia N, Horke S, Habermeier A, Closs EI, Reifenberg G, Gericke A, et al. Uncoupling of endothelial nitric oxide synthase in perivascular adipose tissue of diet-induced obese mice. Arterioscler Thromb Vasc Biol. 2016;36(1):78-85.

Liu XN. The role of perivascular adipose tissue in the repair of injured endothelium in diabetic rats [Dissertation]. Beijing: Peking Union Medical College; 2017. (in Chinese)

Potor L, Nagy P, Méhes G, Hendrik Z, Jeney V, Pethő D, et al. Hydrogen sulfide abrogates hemoglobin-lipid interaction in atherosclerotic lesion. Oxid Med Cell Longev. 2018;2018:3812568.

Du CK, Lin XJ, Xu WJ, Zheng FJ, Cai JY, Yang JC, et al. Sulfhydrated sirtuin-1 increasing its deacetylation activity is an essential epigenetics mechanism of anti-atherogenesis by hydrogen sulfide. Antioxid Redox Signal. 2019;30(2):184-97.

Xu MX, Liu WX, Liang YT, Zhao DC. Recent research of H2S and autophagy in cardiovascular diseases. China Journal of Modern Medicine. 2020;30(21):34-8. (in Chinese)

Guo J, Bian Y, Bai R, Li H, Fu M, Xiao C. Globular adiponectin attenuates myocardial ischemia/reperfusion injury by upregulating endoplasmic reticulum Ca2+-ATPase activity and inhibiting endoplasmic reticulum stress. J Cardiovasc Pharmacol. 2013;62(2):143-53.

Srikakulapu P, Upadhye A, Rosenfeld SM, Marshall MA, McSkimming C, Hickman AW, et al. Perivascular adipose tissue harbors atheroprotective IgM-producing B cells. Front Physiol. 2017;8:719.

Konaniah ES, Kuhel DG, Basford JE, Weintraub NL, Hui DY. Deficiency of LRP1 in mature adipocytes promotes diet-induced inflammation and atherosclerosis-brief report. Arterioscler Thromb Vasc Biol. 2017;37(6):1046-9.

Leandro A, Queiroz M, Azul L, Seiça R, Sena CM. Omentin: a novel therapeutic approach for the treatment of endothelial dysfunction in type 2 diabetes. Free Radic Biol Med. 2021;162:233-42.

Kumar RK, Kaiser LM, Rockwell CE, Watts SW. Interleukin-10 does not contribute to the anti-contractile nature of PVAT in health. Vascul Pharmacol. 2021;138:106838.

Xiong WH. Investigation on the function of perivascular adipose tissue in atherogenesis [dissertation]. Hunan: University of South China; 2019. (in Chinese)

Adachi Y, Ueda K, Nomura S, Ito K, Katoh M, Katagiri M, et al. Beiging of perivascular adipose tissue regulates its inflammation and vascular remodeling. Nat Commun. 2022;13(1):5117.

Zhou Y, Li H, Xia N. The interplay between adipose tissue and vasculature: role of oxidative stress in obesity. Front Cardiovasc Med. 2021;8:650214.

Dakroub A, Nasser SA, Kobeissy F, Yassine HM, Orekhov A, Sharifi-Rad J, et al. Visfatin: an emerging adipocytokine bridging the gap in the evolution of cardiovascular diseases. J Cell Physiol. 2021;236(9):6282-96.

Bermudez B, Dahl TB, Medina I, Groeneweg M, Holm S, Montserrat-de la Paz S, et al. Leukocyte overexpression of intracellular NAMPT attenuates atherosclerosis by regulating PPARγ-dependent monocyte differentiation and function. Arterioscler Thromb Vasc Biol. 2017;37(6):1157-67.

Dong Z, Li R, Liu XF, Zhang H, Wang F, Gao RL, et al. Research on serum level of visfatin increases the vulnerability of atherosclerotic plaque by up-regulating ADAMTS-4 expression in macrophages. Journal of China-Japan Friendship Hospital. 2023;37(3):131-5. (in Chinese)

Wu W, Li J, Zhao M, Liu X. HIF-1α mediates visfatin-induced CTGF expression in vascular endothelial cells. Cell Mol Biol (Noisy-le-grand). 2017;63(4):28-32.

Cai QQ, Luo TT. Advances in the study of the relationship between visfatin and atherosclerotic lesions. Practical Geriatrics. 2020;34(5):499-501. (in Chinese)

Kiernan K, MacIver NJ. The role of the adipokine leptin in immune cell function in health and disease. Front Immunol. 2021;11:622468.

Antoniades C, Tousoulis D, Vavlukis M, Fleming I, Duncker DJ, Eringa E, et al. Perivascular adipose tissue as a source of therapeutic targets and clinical biomarkers: a clinical consensus statement from the European Society of Cardiology Working Group on Coronary Pathophysiology and Micro-circulation. Eur Heart J. 2023;44(38):3827-44.

Tran KV, Fitzgibbons T, Min SY, DeSouza T, Corvera S. Distinct adipocyte progenitor cells are associated with regional phenotypes of perivascular aortic fat in mice. Mol Metab. 2018;9:199-206.

Sidossis L, Kajimura S. Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J Clin Invest. 2015;125(2):478-86.

Pei Y, Otieno D, Gu I, Lee SO, Parks JS, Schimmel K, et al. Effect of quercetin on nonshivering thermogenesis of brown adipose tissue in high-fat diet-induced obese mice. J Nutr Biochem. 2021;88:108532.

Qiao Y, Zhang JC, Liu Y, Ma LQ, Mao T, Sun XL. Mechanism research of effective ingredients of Ginseng Radix et Rhizoma and Chuanxiong Rhizoma on regulating white adipose browning by PPARγ/PGC-1α/UCP1 pathway. Chinese Traditional and Herbal Drugs. 2022;53(2):478-83. (in Chinese)

Wang SW, Hu YQ, Wang R, Zhang YF, Xue MZ, Wang YQ, et al. Effect and mechanism of total saponins from panax japonicus on white adipose tissue browning/brown adipose tissue activation in high-fat diet-induced mice. Chinese Journal of Experimental Traditional Medical Formulae. 2024;30(2):71-8. (in Chinese)

Qi G, Zhou Y, Zhang X, Yu J, Li X, Cao X, et al. Cordycepin promotes browning of white adipose tissue through an AMP-activated protein kinase (AMPK)-dependent pathway. Acta Pharm Sin B. 2019;9(1):135-43.

Ma L, Zhao ZW, Guo XM, Li J, Xu L, Mei WJ, et al. Tanshinone IIA and its derivative activate thermogenesis in adipocytes and induce “beiging” of white adipose tissue. Mol Cell Endocrinol. 2022;544:111557.

Zhang YQ, Zhang ZZ, Zhang YW, Wu LM, Gao L, Yao R, et al. Baicalin promotes the activation of brown and white adipose tissue through AMPK/PGC1α pathway. Eur J Pharmacol. 2022;922:174913.

Liu XH, Li GS, Li XY, Gao ZN, Huang L, Liu YL. Berberine inhibits TGF-β1 pathway to induce browning of visceral white adipose tissue to improve lipid-induced insulin resistance in type 2 diabetic hamsters. Modern Journal of Integrated Traditional Chinese and Western Medicine. 2021;30(7):694-9. (in Chinese)

Nan WS. Irisin promoting human adipocyte beiging through PI3K-AKT signal pathway [dissertation]. Shandong: Shandong University; 2024. (in Chinese)

Ding J, Zhao J, Wan MM, Su X, Gao G, Xu JY, et al. Effect and mechanism of Zexie decoction in promoting white adipose tissue browning/brown adipose tissue activation based on GLP-1R/cAMP/PKA/CREB pathway. China Journal of Chinese Materia Medica. 2023;48(21):5851-62. (in Chinese)

Zhang XQ, Xu WH, Xiao XX, Ding JF, Jiang Y, Tu J. Molecular mechanism of Gegen Qinlian decoction in promoting differentiation of brown adipose tissue to improve glucose and lipid metabolism disorders in diabetic rats. China Journal of Chinese Materia Medica. 2021;46(17):4462-70. (in Chinese)

Zhang LF. Dingxin recipe III promotes white adipose tissue browning in obese mice through the AMPK/SIRT1 pathway [dissertation]. Guangdong: Southern Medical University; 2023. (in Chinese)

He XL, Li XZ, Xu DW, Li Y, Yang ZX. Electroacupuncture intervention improves lipid metabolism and promotes browning of white adipose tissue by activating AMPK/Sirt1 pathway and up-regulating Nrg4 content in middleaged and aged obese rats. Acupuncture Research. 2023;48(8):764-72. (in Chinese)