1,943
Views
1
CrossRef citations to date
0
Altmetric
Review

In vitro studies of the renin-angiotensin system in human adipose tissue/adipocytes and possible relationship to SARS-CoV-2: a scoping review

, &
Article: 2194034 | Received 27 Sep 2022, Accepted 02 Jan 2023, Published online: 27 Mar 2023

References

  • Muñoz-Durango N, Fuentes CA, Castillo AE, et al. Role of the renin-angiotensin-aldosterone system beyond blood pressure regulation: molecular and cellular mechanisms involved in end-organ damage during arterial hypertension. Int J Mol Sci. 2016;17(7):797.
  • Schmieder RE, Hilgers KF, Schlaich MP, et al. Renin-angiotensin system and cardiovascular risk. Lancet. 2007;369(9568):1208–20.
  • Ferrario CM, Varagic J. The ANG-(1–7)/ace2/mas axis in the regulation of nephron function. Am J Physiol Renal Physiol. 2010;298(6):F1297.
  • Cassis LA. Local adipose tissue renin-angiotensin system. Curr Hypertens Rep. 2008;10(2):93.
  • Kalupahana NS, Moustaid-Moussa N. The adipose tissue renin-angiotensin system and metabolic disorders: a review of molecular mechanisms. Crit Rev Biochem Mol Biol. 2012;47(4):379.
  • Blüher M. Adipose tissue dysfunction contributes to obesity related metabolic diseases. Best Pract Res Clin Endocrinol Metab. 2013;27(2):163–177.
  • World Health Organization. Summary table of SARS cases by country, 1 November 2002-7 August 2003. Available from: https://www.who.int/csr/sars/country/en/country2003_08_15.pdf.
  • Worldometer. Total deaths of novel coronavirus (2019-nCov). [cited 2021 Jul 30]. Available from: https://www.worldometers.info/coronavirus/coronavirus-death-toll/
  • Ryan PM, Caplice NM. Is adipose tissue a reservoir for viral spread, immune activation, and cytokine amplification in coronavirus disease 2019? Obesity. 2020;28(7):1191.
  • Martínez-Colón GJ, Ratnasiri K, Chen H, et al. SARS-CoV-2 infection drives an inflammatory response in human adipose tissue through infection of adipocytes and macrophages. Sci Transl Med. 2022 Dec 7;14(674):eabm9151. DOI:10.1126/scitranslmed.abm9151.
  • Oudit GY, Penninger JM. Recombinant human angiotensin-converting enzyme 2 as a new renin-angiotensin system peptidase for heart failure therapy. Curr Heart Fail Rep. 2011;8(3):176–183.
  • Zhong J, Guo D, Chen CB, et al. Prevention of angiotensin II – mediated renal oxidative stress, inflammation, and fibrosis by angiotensin-converting enzyme 2. Hypertension. 2011;57(2):314–322. DOI:10.1161/HYPERTENSIONAHA.110.164244
  • Arksey H, O’malley L. Scoping studies: towards a methodological framework. Int J Soc Res Methodol. 2005;8(1):19–32.
  • Tricco AC, Lillie E, Zarin W, et al. PRISMA extension for scoping reviews (PRISMA-Scr): checklist and explanation. Ann Intern Med. 2018;169(7):467–473.
  • Munn Z, Peters MD, Stern C, et al. Systematic review or scoping review? Guidance for authors when choosing between the systematic or scoping review approach. BMC Med Res Methodol. 2018;18:1–7.
  • Lefebvre C, Glanville J, Briscoe S, et al. Chapter 4: searching for and selecting studies. In: Higgins J, Thomas J, Chandler J, Cumpston M, Li T, Page M Welch V, editors. Cochrane Handbook for Systematic Reviews of Interventions version 6.2 (updated February 2021). Cochrane; 2021. Available from: www.training.cochrane.org/handbook
  • Han T, Kang J, Li G, et al. Analysis of 2019-nCov receptor ACE2 expression in different tissues and its significance study. Ann Transl Med. 2020;8(17):1077.
  • Kerslake R, Hall M, Randeva H, et al. Co-expression of peripheral olfactory receptors with SARS-CoV-2 infection mediators: potential implications beyond loss of smell as a COVID-19 symptom. Int J of Mol Med. 2020;46(3):949–956.
  • Li MY, Li L, Zhang Y, et al. Expression of the SARS-CoV-2 cell receptor gene ACE2 in a wide variety of human tissues. Infect Dis Poverty. 2020;9(02):23–29.
  • Liu H, Xin J, Cai S, et al. Mendelian randomization analysis provides causality of smoking on the expression of ACE2, a putative SARS-CoV-2 receptor. Elife. 2021;10:e64188.
  • Kristem L, Recamonde-Mendoza M, Cigerza G, et al. Roux-en-Y Gastric bypass downregulates angiotensin-converting enzyme 2 (ACE2) gene expression in subcutaneous white adipose tissue: a putative protective mechanism against severe COVID-19. Obes Surg. 2021;31(6):2831–2834.
  • Li L, Spranger L, Soll D, et al. Metabolic impact of weight loss induced reduction of adipose ACE-2 – Potential implication in COVID-19 infections? Metabolism. 2020;113:154401.
  • Favre G, Legueult K, Pradier C, et al. Visceral fat is associated to the severity of COVID-19. Metabolism. 2021;115:154440.
  • Couselo-Seijas M, Almengló C, Agra-Bermejo RM, et al. Higher ACE2 expression levels in epicardial cells than subcutaneous stromal cells from patients with cardiovascular disease: diabetes and obesity as possible enhancer. Eur J Clin Invest. 2021;51(5):e13463.
  • Desterke C, Griscelli F, Imeri J, et al. Molecular investigation of adequate sources of mesenchymal stem cells for cell therapy of COVID-19 associated organ failure. Stem Cells Transl Med. 2021;10(4):568–571.
  • de Ligt M, Hesselink M, Jorgensen J, et al. The angiotensin II type 1 receptor blocker valsartan in the battle against COVID-19. Obesity. 2021;29(9):1423–1426.
  • MacKay DL, Tesar PJ, Liang LN, et al. Characterizing medullary and human mesenchymal stem cell-derived adipocytes. J of Cell Physiol. 2006;207(3):722–728.
  • Fain JN, Nesbit AS, Sudlow FF, et al. Release in vitro of adipsin, vascular cell adhesion molecule 1, angiotensin 1-converting enzyme, and soluble tumor necrosis factor receptor 2 by human omental adipose tissue as well as by the nonfat cells and adipocytes. Metabolism. 2007;56(11):1583–1590.
  • Fain JN, Buehrer B, Bahouth SW, et al. Comparison of messenger RNA distribution for 60 proteins in fat cells vs the nonfat cells of human omental adipose tissue. Metabolism. 2008;57(7):1005–1015.
  • Achard V, Boullu-Ciocca S, Desbriere R, et al. Renin receptor expression in human adipose tissue. Am J Physiol Regul Integr Cop Physiol. 2007;292:274–282.
  • Schling P. Expression of angiotensin II receptors type 1 and type 2 in human preadipose cells during differentiation. Horm Metab Res. 2002;34(11–12):709–715.
  • Sysoeva VY, Ageeva LV, Tyurin-Kuzmin PA, et al. Local angiotensin II promotes adipogenic differentiation of human adipose tissue mesenchymal stem cells through type 2 angiotensin receptor. Stem Cell Res. 2017;25:115–122.
  • Than A, Xu S, Li R, et al. Angiotensin type 2 receptor activation promotes browning of white adipose tissue and brown adipogenesis. Sigl Transduct Target Ther. 2017;2:17022.
  • Engeli S, Janke J, Gorzelniak K, et al. Regulation of the nitric oxide system in human adipose tissue. J Lipid Res. 2004;45(9):1640–1648.
  • Brücher R, Cifuentes M, Acuña MJ, et al. Larger anti-adipogenic effect of angiotensin II on omental preadipose cells of obese humans. Obesity. 2007;15(7):1643–1646.
  • Janke J, Engeli S, Gorzelniak K, et al. Mature adipocytes inhibit in vitro differentiation of human preadipocytes via angiotensin type 1 receptors. Diabetes. 2002;51(6):1699–1707. 10.2337/diabetes.51.6.1699.
  • Dünner N, Quezada C, Berndt FA, et al. Angiotensin II signaling in human preadipose cells: participation of ERK1,2-dependent modulation of Akt. PLoS ONE. 2013;8(10):e375440.
  • Fuentes P, Acuña MJ, Cifuentes M, et al. The anti-adipogenic effect of angiotensin II on human preadipose cells involves ERK1,2 activation and PPARG phosphorylation. J Endocrinol. 2010;206(1):75–83.
  • Janke J, Schupp M, Engeli S, et al. Angiotensin type 1 receptor antagonists induce human in-vitro adipogenesis through peroxisome proliferator-activated receptor-gamma activation. J Hypertens. 2006;24(9):1809–1816.
  • Ye ZW, Wu XM, Jiang JG. Expression changes of angiotensin II pathways and bioactive mediators during human preadipocytes-visceral differentiation. Metabolism. 2009;58(9):1288–1296.
  • Than A, Leow MK, Chen P. Control of adipogenesis by the autocrine interplays between angiotensin 1-7/mas receptor and angiotensin II/AT1 receptor signaling pathways. J Biol Chem. 2013;288(22):15520–15531.
  • Sarzani R, Marcucci P, Salvi F, et al. Angiotensin II stimulates and atrial natriuretic peptide inhibits human visceral adipocyte growth. Int J Obes. 2008;32(2):259–267.
  • Song K, Wang Z, Li W, et al. In vitro culture, determination, and directed differentiation of adult adipose-derived stem cells towards cardiomyocyte-like cells induced by angiotensin II. Appl Biochem Biotechnol. 2013;170(2):459–470.
  • Gaafar T, Shawky S, Attia W, et al. The role of angiotensin II in cardiomyogenic differentiation of human adipose tissue-derived mesenchymal stem cells. Comp Clin Pathol. 2015;24:879–885.
  • Goossens GH, Bizzarri A, Venteclef N, et al. Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation. 2011;124(1):67–76.
  • Harte A, McTernan P, Chetty R, et al. Insulin-mediated upregulation of the renin angiotensin system in human subcutaneous adipocytes is reduced by rosiglitazone. Circulation. 2005;111:1954–1961.
  • Menikdiwela KR, Ramalingam L, Allen L, et al. Angiotensin II increases endoplasmic reticulum stress in adipose tissue and adipocytes. Sci Rep. 2019;9(1):8481.
  • Skurk T, van Harmelen V, Hauner H. Angiotensin II stimulates the release of interleukin-6 and interleukin-8 from cultured human adipocytes by activation of NF-kappaB. Arterioscler Thromb Vasc Biol. 2004;24(7):1199–1203.
  • Polonis K, Becari C, Chahal CA, et al. Chronic intermittent hypoxia triggers a senescence-like phenotype in human white preadipocytes. Sci Rep. 2020;10:6846.
  • Skurk T, Lee YM, Hauner H. Angiotensin II and its metabolites stimulate PAI-1 protein release from human adipocytes in primary culture. Hypertension. 2001;37:1336–1340.
  • Skurk T, van Harmelen V, Blum WF, et al. Angiotensin II promotes leptin production in cultured human fat cells by an ERK1/2-dependent pathway. Obes Res. 2005;13(6):969–973.
  • Li Y, Zuo L, Zhu W, et al. Telmisartan attenuates the inflamed mesenteric adipose tissue in spontaneous colitis by mechanisms involving regulation of neurotensin/microRNA-155. Biochem Pharmacol. 2015;93(4):461–469.
  • Boccara F, Auclair M, Cohen A, et al. HIV protease inhibitors activate the adipocyte renin angiotensin system. Antivir Ther. 2009;15(3):363–375.
  • Blumensatt M, Fahlbusch P, Hilgers R, et al. Secretory products from epicardial adipose tissue from patients with type 2 diabetes impair mitochondrial β-oxidation in cardiomyocytes via activation of the cardiac renin-angiotensin system and induction of miR-208a. Basic Res Cardiol. 2017;112(1):2.
  • Rasha F, Kahathuduwa C, Ramlingam L, et al. Combined effects of eicosapentaenoic acid and adipocyte renin-angiotensin system inhibition on breast cancer cell inflammation and migration. Cancers (Basel). 2020;12(1):220.
  • Rasha F, Ramalingam L, Menikdiwela K, et al. Renin angiotensin system inhibition attenuates adipocyte-breast cancer cell interactions. Exp Cell Res. 2020;394(1):112114.
  • de Oliveira M, De Sibio MT, Mathias LS, et al. Irisin modulates genes associated with severe coronavirus disease (COVID-19) outcome in human subcutaneous adipocytes cell culture. Mol Cell Endocrinol. 2020;15(515):110917.
  • Patel VB, Mori J, McLean BA, et al. ACE2 deficiency worsens epicardial adipose tissue inflammation and cardiac dysfunction in response to diet-induced obesity. Diabetes. 2016;65(1):85–95. DOI:10.2337/db15-0399
  • Pinheiro TDA, Barcala-Jorge AS, Andrade JM, et al. Obesity and malnutrition similarly alter the renin-angiotensin system and inflammation in mice and human adipose. J Nutr Biochem. 2017;48:74–82.
  • Serazin V, Dos Santos E, Morot M, et al. Human adipose angiotensinogen gene expression and secretion are stimulated by cyclic AMP via increased DNA cyclic AMP responsive element binding activity. Endocrine. 2004;25(2):97–104.
  • Prat-Larquemin L, Oppert JM, Clément K, et al. Adipose angiotensinogen secretion, blood pressure, and AGT M235T polymorphism in obese patients. Obes Res. 2004;12(3):556–561.
  • Sarzani R, Bordicchia M, Marcucci P, et al. Angiotensinogen promoter variants influence gene expression in human kidney and visceral adipose tissue. J Hum Hypertens. 2010;24:213–219.
  • Park S, Lu KT, Liu X, et al. Allele-specific expression of angiotensinogen in human subcutaneous adipose tissue. Hypertension. 2013;62:41–47.
  • Gorzelniak K, Engeli S, Janke J, et al. Hormonal regulation of the human adipose-tissue-renin-angiotensin system: relationship to obesity and hypertension. J Hypertens. 2002;20(5):965–973.
  • Malinowski M, Deja MA, Golba KS, et al. Perivascular tissue of internal thoracic artery releases potent nitric oxide and prostacyclin-independent anticontractile factor. Eur J Cardiothorac Surg. 2008;33(2):225–231.
  • Ehrhart-Bornstein M, Lamounier-Zepter V, Schraven A, et al. Human adipocytes secrete mineralocorticoid-releasing factors. Proc Natl Acad Sci, USA. 2003;100(24):14211–14216.
  • Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181(2):271–280.e8.
  • Lighter J, Phillips M, Hochman S, et al. Obesity in patients younger than 60 years is a risk factor for Covid-19 hospital admission. Clin Infects Dis. 2020;71(15):896–897.
  • Engeli S, Böhnke J, Gorzelniak K, et al. Weight loss and the renin-angiotensin-aldosterone system. Hypertension. 2005;45(3):356–362.
  • Al-Benna S. Association of high level gene expression of ACE2 in adipose tissue with mortality of COVID-19 infection in obese patients. Obes Med. 2020;19:100283.
  • Williams B, Zhang Y. Hypertension, renin-angiotensin-aldosterone system inhibition, and COVID-19. Lancet. 2020;395(10238):1671–1673.
  • Ferrario CM, Ahmad S, Groban L. Mechanisms by which angiotensin-receptor blockers increase ACE2 levels. Nat Rev Cardiol. 2020;17(6):378.
  • Vaduganathan M, Vardeny O, Michel T, et al. Renin–angiotensin–aldosterone system inhibitors in patients with Covid-19. N Engl J Med. 2020;382(17):2441–2448.
  • Klöting N, Blüher M. Adipocyte dysfunction, inflammation and metabolic syndrome. Rev Endocr Metab Disord. 2014;15(4):277–287.
  • Bartelt A, Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol. 2014;10(1):24–36.
  • Hanssen MJ, van der Lans AA, Brans B, et al. Short-term cold acclimation recruits brown adipose tissue in obese humans. Diabetes. 2016;65(5):1179–1189.
  • Qiu Y, Sun L, Hu X, et al. Compromised browning plasticity of primary subcutaneous adipocytes derived from overweight Chinese adults. Diabetol Metab Syndr. 2020;12(1):1–11.
  • Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res. 2007;100(9):1249–1260.
  • Cai L, Johnstone BH, Cook TG, et al. IFATS collection: human adipose tissue‐derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells. 2009;27(1):230–237.
  • Bai X, Alt E. Myocardial regeneration potential of adipose tissue-derived stem cells. Biochem Biophys Res Commun. 2010;401(3):321–326.
  • Hotamisligil GS. Foundations of immunometabolism and implications for metabolic health and disease. Immunity. 2017;47(3):406–420.
  • Guilherme A, Virbasius JV, Puri V, et al. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Reviews Mol Cell Biol. 2008;9(5):367–377.