Skip to main content

Advertisement

SpringerLink
Log in

High-density lipoprotein-mediated cardioprotection in heart failure

  • Published:
Heart Failure Reviews Aims and scope Submit manuscript

Abstract

The prevalence of heart failure (HF), including reduced ejection fraction (HFrEF) and preserved ejection fraction (HFpEF), has increased significantly worldwide. However, the prognosis and treatment of HF are still not good. Recent studies have demonstrated that high-density lipoprotein (HDL) plays an important role in cardiac repair during HF. The exact role and mechanism of HDL in the regulation of HF remain unexplained. Here, we discuss recent findings regarding HDL in the progression of HF, such as the regulation of excitation-contraction coupling, energy homeostasis, inflammation, neurohormone activation, and microvascular dysfunction. The effects of HDL on the regulation of cardiac-related cells, such as endothelial cells (ECs), cardiomyocytes (CMs), and on cardiac resident immune cell dysfunction in HF are also explained. An in-depth understanding of HDL function in the heart may provide new strategies for the prevention and treatment of HF.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Investigators A-H et al (2011) Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N Engl J Med 365(24):2255–2267

    Google Scholar 

  2. Christiansen MN, L.K, Jeppensen J, Torp-Pedersen C, Gislason G, Weeke P, Ramachandran VS (2016) Age-specific trends in incidence and prognosis of heart failure in Denmark. Circulation 134:A15936

    Google Scholar 

  3. Bauer A, Khalil M, Lüdemann M, Bauer J, Esmaeili A, de-Rosa R, Voelkel NF, Akintuerk H, Schranz D (2018) Creation of a restrictive atrial communication in heart failure with preserved and mid-range ejection fraction: effective palliation of left atrial hypertension and pulmonary congestion. Clin Res Cardiol 107(9):845–857

    PubMed  Google Scholar 

  4. Dwyer KH, Merz AA, Lewis EF, Claggett BL, Crousillat DR, Lau ES, Silverman MB, Peck J, Rivero J, Cheng S, Platz E (2018) Pulmonary congestion by lung ultrasound in ambulatory patients with heart failure with reduced or preserved ejection fraction and hypertension. J Card Fail 24(4):219–226

    PubMed  PubMed Central  Google Scholar 

  5. Schmederer Z, Rolim N, Bowen TS, Linke A, Wisloff U, Adams V, OptimEx study group (2018) Endothelial function is disturbed in a hypertensive diabetic animal model of HFpEF: moderate continuous vs. high intensity interval training. Int J Cardiol 273:147–154

    PubMed  Google Scholar 

  6. Amgalan D, Kitsis RN (2019) A mouse model for the most common form of heart failure. Nature 568(7752):324–325

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Otsuka K, Nakanishi K, Shimada K, Nakamura H, Inanami H, Nishioka H, Fujimoto K, Kasayuki N, Yoshiyama M (2018) Associations of sensitive cardiac troponin-I with left ventricular morphology, function and prognosis in end-stage renal disease patients with preserved ejection fraction. Heart Vessel 33(11):1334–1342

    Google Scholar 

  8. Kalogeropoulos AP et al (2019) Serial changes in left ventricular ejection fraction and outcomes in outpatients with heart failure and preserved ejection fraction. Am J Cardiol

  9. Wu KM et al (2019) High-density lipoprotein ameliorates palmitic acid-induced lipotoxicity and oxidative dysfunction in H9c2 cardiomyoblast cells via ROS suppression. Nutr Metab (Lond) 16:36

    Google Scholar 

  10. Schiattarella GG, Altamirano F, Tong D, French KM, Villalobos E, Kim SY, Luo X, Jiang N, May HI, Wang ZV, Hill TM, Mammen PPA, Huang J, Lee DI, Hahn VS, Sharma K, Kass DA, Lavandero S, Gillette TG, Hill JA (2019) Nitrosative stress drives heart failure with preserved ejection fraction. Nature 568(7752):351–356

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Kristensen SL, Mogensen UM, Jhund PS, Rørth R, Anand IS, Carson PE, Desai AS, Pitt B, Pfeffer MA, Solomon SD, Zile MR, Køber L, McMurray J (2019) N-terminal pro-B-type natriuretic peptide levels for risk prediction in patients with heart failure and preserved ejection fraction according to atrial fibrillation status. Circ Heart Fail 12(3):e005766

    CAS  PubMed  Google Scholar 

  12. Schnorbach J et al (2019) N-terminal pro brain natriuretic peptide eliminates the prognostic effect of atrial fibrillation in patients with chronic heart failure. ESC Heart Fail

  13. Patel VB, Zhong JC, Grant MB, Oudit GY (2016) Role of the ACE2/angiotensin 1-7 axis of the renin-angiotensin system in heart failure. Circ Res 118(8):1313–1326

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Hunter WG, RW MG 3rd, Kelly JP, Khouri MG, Craig DM, Haynes C, Felker GM, Hernandez AF, Velazquez EJ, Kraus WE, Shah SH (2019) High-density lipoprotein particle subfractions in heart failure with preserved or reduced ejection fraction. J Am Coll Cardiol 73(2):177–186

    PubMed  Google Scholar 

  15. Gombos T, Förhécz Z, Pozsonyi Z, Jánoskuti L, Prohászka Z, Karádi I (2017) Long-term survival and apolipoprotein A1 level in chronic heart failure: interaction with tumor necrosis factor alpha −308 G/A polymorphism. J Card Fail 23(2):113–120

    CAS  PubMed  Google Scholar 

  16. Zhao Q, Li J, Yang J, Li R (2017) Association of total cholesterol and HDL-C levels and outcome in coronary heart disease patients with heart failure. Medicine (Baltimore) 96(9):e6094

    CAS  Google Scholar 

  17. Chen SK et al (2019) Heart failure risk in systemic lupus erythematosus compared to diabetes mellitus and general medicaid patients. Semin Arthritis Rheum

  18. Lund A, Giil LM, Slettom G, Nygaard O, Heidecke H, Nordrehaug JE (2018) Antibodies to receptors are associated with biomarkers of inflammation and myocardial damage in heart failure. Int J Cardiol 250:253–259

    PubMed  Google Scholar 

  19. Perreault CL et al (1990) Abnormal intracellular calcium handling in acute and chronic heart failure: role in systolic and diastolic dysfunction. Eur Heart J 11(Suppl C):8–21

    CAS  PubMed  Google Scholar 

  20. Hiemstra, J.A., et al., Chronic low-intensity exercise attenuates cardiomyocyte contractile dysfunction and impaired adrenergic responsiveness in aortic-banded mini-swine. J Appl Physiol (1985), 2018. 124(4): p. 1034–1044

  21. Sadredini M, Danielsen TK, Aronsen JM, Manotheepan R, Hougen K, Sjaastad I, Stokke MK (2016) Beta-adrenoceptor stimulation reveals Ca2+ waves and sarcoplasmic reticulum Ca2+ depletion in left ventricular cardiomyocytes from post-infarction rats with and without heart failure. PLoS One 11(4):e0153887

    PubMed  PubMed Central  Google Scholar 

  22. Voors AA, Shah SJ, Bax JJ, Butler J, Gheorghiade M, Hernandez AF, Kitzman DW, McMurray J, Wirtz AB, Lanius V, van der Laan M, Solomon SD (2018) Rationale and design of the phase 2b clinical trials to study the effects of the partial adenosine A1-receptor agonist neladenoson bialanate in patients with chronic heart failure with reduced (PANTHEON) and preserved (PANACHE) ejection fraction. Eur J Heart Fail 20(11):1601–1610

    CAS  PubMed  Google Scholar 

  23. Mora MT et al (2018) Ca(2+) cycling impairment in heart failure is exacerbated by fibrosis: insights gained from mechanistic simulations. Front Physiol 9:1194

    PubMed  PubMed Central  Google Scholar 

  24. Wang Z, Cao Y, Yin Q, Han Y, Wang Y, Sun G, Zhu H, Xu M, Gu C (2018) Activation of AMPK alleviates cardiopulmonary bypass-induced cardiac injury via ameliorating acute cardiac glucose metabolic disorder. Cardiovasc Ther 36(6):e12482

    PubMed  Google Scholar 

  25. Santos-Gallego CG, Requena-Ibanez JA, San Antonio R, Ishikawa K, Watanabe S, Picatoste B, Flores E, Garcia-Ropero A, Sanz J, Hajjar RJ, Fuster V, Badimon JJ (2019) Empagliflozin ameliorates adverse left ventricular remodeling in nondiabetic heart failure by enhancing myocardial energetics. J Am Coll Cardiol 73(15):1931–1944

    CAS  PubMed  Google Scholar 

  26. Uchihashi M et al (2017) Cardiac-specific Bdh1 overexpression ameliorates oxidative stress and cardiac remodeling in pressure overload-induced heart failure. Circ Heart Fail 10(12)

  27. Okawa Y et al (2019) Ablation of cardiac TIGAR preserves myocardial energetics and cardiac function in the pressure overload heart failure model. Am J Physiol Heart Circ Physiol

  28. Helena Tuunanen EE, Naum A, Någren K, Hesse B, Airaksinen KEJ (2006) Free fatty acid depletion acutely decreases cardiac work and efficiency in cardiomyopathic heart failure. Circulation 114:2130–2137

    PubMed  Google Scholar 

  29. Sundstrom J et al (2004) Relations of plasma total TIMP-1 levels to cardiovascular risk factors and echocardiographic measures: the Framingham heart study. Eur Heart J 25(17):1509–1516

    CAS  PubMed  Google Scholar 

  30. Hulsmans M, Clauss S, Xiao L, Aguirre AD, King KR, Hanley A, Hucker WJ, Wülfers EM, Seemann G, Courties G, Iwamoto Y, Sun Y, Savol AJ, Sager HB, Lavine KJ, Fishbein GA, Capen DE, da Silva N, Miquerol L, Wakimoto H, Seidman CE, Seidman JG, Sadreyev RI, Naxerova K, Mitchell RN, Brown D, Libby P, Weissleder R, Swirski FK, Kohl P, Vinegoni C, Milan DJ, Ellinor PT, Nahrendorf M (2017) Macrophages facilitate electrical conduction in the heart. Cell 169(3):510–522 e20

    PubMed  PubMed Central  Google Scholar 

  31. Dick SA, Macklin JA, Nejat S, Momen A, Clemente-Casares X, Althagafi MG, Chen J, Kantores C, Hosseinzadeh S, Aronoff L, Wong A, Zaman R, Barbu I, Besla R, Lavine KJ, Razani B, Ginhoux F, Husain M, Cybulsky MI, Robbins CS, Epelman S (2019) Self-renewing resident cardiac macrophages limit adverse remodeling following myocardial infarction. Nat Immunol 20(1):29–39

    CAS  PubMed  Google Scholar 

  32. Sager HB, Hulsmans M, Lavine KJ, Moreira MB, Heidt T, Courties G, Sun Y, Iwamoto Y, Tricot B, Khan OF, Dahlman JE, Borodovsky A, Fitzgerald K, Anderson DG, Weissleder R, Libby P, Swirski FK, Nahrendorf M (2016) Proliferation and recruitment contribute to myocardial macrophage expansion in chronic heart failure. Circ Res 119(7):853–864

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Van der Borght K, S.C, Nindl V, Bouché A (2017) Myocardial infarction primes autoreactive T cells through activation of dendritic cells. Cell Rep 18(12):3005–3017

    PubMed  PubMed Central  Google Scholar 

  34. Paulus WJ, Tschope C (2013) A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 62(4):263–271

    PubMed  Google Scholar 

  35. Chami B, Barrie N, Cai X, Wang X, Paul M, Morton-Chandra R, Sharland A, Dennis JM, Freedman SB, Witting PK (2015) Serum amyloid a receptor blockade and incorporation into high-density lipoprotein modulates its pro-inflammatory and pro-thrombotic activities on vascular endothelial cells. Int J Mol Sci 16(5):11101–11124

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhang Q et al (2010) Essential role of HDL on endothelial progenitor cell proliferation with PI3K/Akt/cyclin D1 as the signal pathway. Exp Biol Med (Maywood) 235(9):1082–1092

    CAS  Google Scholar 

  37. Shih CM, Lin FY, Yeh JS, Lin YW, Loh SH, Tsao NW, Nakagami H, Morishita R, Sawamura T, Li CY, Lin CY, Huang CY (2019) Dysfunctional high density lipoprotein failed to rescue the function of oxidized low density lipoprotein-treated endothelial progenitor cells: a novel index for the prediction of HDL functionality. Transl Res 205:17–32

    CAS  PubMed  Google Scholar 

  38. Gordts SC, Muthuramu I, Nefyodova E, Jacobs F, van Craeyveld E, de Geest B (2013) Beneficial effects of selective HDL-raising gene transfer on survival, cardiac remodelling and cardiac function after myocardial infarction in mice. Gene Ther 20(11):1053–1061

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Li C et al (2019) Relationship of high-density lipoprotein-associated arylesterase activity to systolic heart failure in patients with and without type 2 diabetes. Sci Rep 9(1):5979

    PubMed  PubMed Central  Google Scholar 

  40. Griffiths K et al (2017) Type 2 diabetes in young females results in increased serum amyloid a and changes to features of high density lipoproteins in both HDL2 and HDL3. J Diabetes Res 2017:1314864

    PubMed  PubMed Central  Google Scholar 

  41. Chaudhary R et al (2018) HDL3-C is a marker of coronary artery disease severity and inflammation in patients on statin therapy. Cardiovasc Revasc Med

  42. Femlak M, Gluba-Brzózka A, Ciałkowska-Rysz A, Rysz J (2017) The role and function of HDL in patients with diabetes mellitus and the related cardiovascular risk. Lipids Health Dis 16(1):207

    PubMed  PubMed Central  Google Scholar 

  43. Biedzka-Sarek M, Metso J, Kateifides A, Meri T, Jokiranta TS, Muszyński A, Radziejewska-Lebrecht J, Zannis V, Skurnik M, Jauhiainen M (2011) Apolipoprotein A-I exerts bactericidal activity against Yersinia enterocolitica serotype O:3. J Biol Chem 286(44):38211–38219

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Esteve E, Castro A, Moreno JM, Vendrell J, Ricart W, Fernández-Real JM (2010) Circulating bactericidal/permeability-increasing protein (BPI) is associated with serum lipids and endothelial function. Thromb Haemost 103(4):780–787

    CAS  PubMed  Google Scholar 

  45. Rye PJBK-A (2017) HDL cholesterol concentration or HDL function: which matters? Eur Heart J 38(32):2487–2489

    PubMed  Google Scholar 

  46. Kim JB, Hama S, Hough G, Navab M, Fogelman AM, Maclellan WR, Horwich TB, Fonarow GC (2013) Heart failure is associated with impaired anti-inflammatory and antioxidant properties of high-density lipoproteins. Am J Cardiol 112(11):1770–1777

    CAS  PubMed  Google Scholar 

  47. Ossoli A et al (2019) Recombinant LCAT (lecithin:cholesterol acyltransferase) rescues defective HDL (high-density lipoprotein)-mediated endothelial protection in acute coronary syndrome. Arterioscler Thromb Vasc Biol 39(5):915–924

    CAS  PubMed  Google Scholar 

  48. Du XM et al (2015) HDL particle size is a critical determinant of ABCA1-mediated macrophage cellular cholesterol export. Circ Res 116(7):1133–1142

    CAS  PubMed  Google Scholar 

  49. Hunter WG, R.W.M, Kelly JP, Haynes C, Craig DM, Velazquez EJ, Kraus WE (2016) Circulating high-density lipoprotein particle profiles are independently associated with heart failure with preserved ejection fraction and predict adverse clinical outcomes. Circulation 134(1):12679

    Google Scholar 

  50. Potocnjak I et al (2017) Serum concentration of HDL particles predicts mortality in acute heart failure patients. Sci Rep 7:46642

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Perez L et al (2019) OxHDL controls LOX-1 expression and plasma membrane localization through a mechanism dependent on NOX/ROS/NF-kappaB pathway on endothelial cells. Lab Investig 99(3):421–437

    CAS  PubMed  Google Scholar 

  52. Wang M, Corsetti J, McNitt S, Rich DQ, Sparks CE, Moss AJ, Zareba W (2017) Inflammatory markers modify the risk of recurrent coronary events associated with apolipoprotein A-I in postinfarction patients. J Clin Lipidol 11(1):215–223

    PubMed  Google Scholar 

  53. Vanags LZ et al (2018) High-density lipoproteins and Apolipoprotein A-I improve stent biocompatibility. Arterioscler Thromb Vasc Biol 38(8):1691–1701

    CAS  PubMed  Google Scholar 

  54. Sirtori CR et al (2019) HDL therapy today: from atherosclerosis, to stent compatibility to heart failure. Ann Med:1–31

  55. Futh R et al (2009) Soluble P-selectin and matrix metalloproteinase 2 levels are elevated in patients with diastolic dysfunction independent of glucose metabolism disorder or coronary artery disease. Exp Clin Cardiol 14(3):e76–e79

    PubMed  PubMed Central  Google Scholar 

  56. Weschenfelder C, Marcadenti A, Stein AT, Gottschall CB (2017) Enlarged waist combined with elevated triglycerides (hypertriglyceridemic waist phenotype) and HDL-cholesterol in patients with heart failure. Sao Paulo Med J 135(1):50–56

    PubMed  Google Scholar 

  57. Seferovic JP, Claggett B, Seidelmann SB, Seely EW, Packer M, Zile MR, Rouleau JL, Swedberg K, Lefkowitz M, Shi VC, Desai AS, McMurray J, Solomon SD (2017) Effect of sacubitril/valsartan versus enalapril on glycaemic control in patients with heart failure and diabetes: a post-hoc analysis from the PARADIGM-HF trial. Lancet Diabetes Endocrinol 5(5):333–340

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Mishra M et al (2018) Reconstituted HDL (Milano) treatment efficaciously reverses heart failure with preserved ejection fraction in mice. Int J Mol Sci 19(11)

  59. Aboumsallem JP et al (2019) Effective treatment of diabetic cardiomyopathy and heart failure with reconstituted HDL (Milano) in mice. Int J Mol Sci 20(6)

  60. Jihe Li JS, Kurlansky P, Shehadeh LA (2018) Osteopontin RNA aptamer reverses heart failure and increases plasma HDL levels. Circulation 130:A18651

    Google Scholar 

  61. Benke K, Mátyás C, Sayour AA, Oláh A, Németh BT, Ruppert M, Szabó G, Kökény G, Horváth EM, Hartyánszky I, Szabolcs Z, Merkely B, Radovits T (2017) Pharmacological preconditioning with gemfibrozil preserves cardiac function after heart transplantation. Sci Rep 7(1):14232

    PubMed  PubMed Central  Google Scholar 

  62. Hammadah M, Kalogeropoulos AP, Georgiopoulou VV, Weber M, Wu Y, Hazen SL, Butler J, Tang WHW (2017) High-density lipoprotein-associated paraoxonase-1 activity for prediction of adverse outcomes in outpatients with chronic heart failure. Eur J Heart Fail 19(6):748–755

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Pradeep Natarajan AL (2018) Association of an HDL proteomic score with the presence of coronary atherosclerosis and future major adverse cardiovascular events. Circulation 138:A12724

    Google Scholar 

  64. Zhang Y, Chen A, Song L, Li M, Luo Z, Zhang W, Chen Y, He B (2016) Low-level vagus nerve stimulation reverses cardiac dysfunction and subcellular calcium handling in rats with post-myocardial infarction heart failure. Int Heart J 57(3):350–355

    CAS  PubMed  Google Scholar 

  65. Seidel T et al (2017) Sheet-like remodeling of the transverse tubular system in human heart failure impairs excitation-contraction coupling and functional recovery by mechanical unloading. Circulation 135(17):1632–1645

    PubMed  PubMed Central  Google Scholar 

  66. Sorsa T, Pollesello P, Solaro RJ (2004) The contractile apparatus as a target for drugs against heart failure: interaction of levosimendan, a calcium sensitiser, with cardiac troponin c. Mol Cell Biochem 266(1–2):87–107

    CAS  PubMed  Google Scholar 

  67. Yamagata K, Tanaka N, Suzuki K (2013) Epigallocatechin 3-gallate inhibits 7-ketocholesterol-induced monocyte-endothelial cell adhesion. Microvasc Res 88:25–31

    CAS  PubMed  Google Scholar 

  68. Yamagata K, Tanaka N, Matsufuji H, Chino M (2012) Beta-carotene reverses the IL-1beta-mediated reduction in paraoxonase-1 expression via induction of the CaMKKII pathway in human endothelial cells. Microvasc Res 84(3):297–305

    CAS  PubMed  Google Scholar 

  69. Keul P, M.M.G.J.v.B, Ghanem A, Müller FU, Baartscheer A (2016) Sphingosine-1-phosphate receptor 1 regulates cardiac function by modulating Ca2+ sensitivity and Na+/H+ exchange and mediates protection by ischemic preconditioning. Circulation 5:e003393

    Google Scholar 

  70. da Silva Ferreira T, Torres MR, Sanjuliani AF (2013) Dietary calcium intake is associated with adiposity, metabolic profile, inflammatory state and blood pressure, but not with erythrocyte intracellular calcium and endothelial function in healthy pre-menopausal women. Br J Nutr 110(6):1079–1088

    PubMed  Google Scholar 

  71. Nakajima H, Ishida T, Satomi-Kobayashi S, Mori K, Hara T, Sasaki N, Yasuda T, Toh R, Tanaka H, Kawai H, Hirata K (2013) Endothelial lipase modulates pressure overload-induced heart failure through alternative pathway for fatty acid uptake. Hypertension 61(5):1002–1007

    CAS  PubMed  Google Scholar 

  72. Umbarawan Y et al (2018) Myocardial fatty acid uptake through CD36 is indispensable for sufficient bioenergetic metabolism to prevent progression of pressure overload-induced heart failure. Sci Rep 8(1):12035

    PubMed  PubMed Central  Google Scholar 

  73. Djousse L et al (2013) Plasma free fatty acids and risk of heart failure: the cardiovascular health study. Circ Heart Fail 6(5):964–969

    CAS  PubMed  Google Scholar 

  74. Wang C et al (2019) Plin5 deficiency exacerbates pressure overload-induced cardiac hypertrophy and heart failure by enhancing myocardial fatty acid oxidation and oxidative stress. Free Radic Biol Med 141:372–382

    CAS  PubMed  Google Scholar 

  75. Fujii N et al (2004) Saturated glucose uptake capacity and impaired fatty acid oxidation in hypertensive hearts before development of heart failure. Am J Physiol Heart Circ Physiol 287(2):H760–H766

    CAS  PubMed  Google Scholar 

  76. Heywood SE et al (2017) High-density lipoprotein delivered after myocardial infarction increases cardiac glucose uptake and function in mice. Sci Transl Med 9(411)

  77. Stud, o.I.-T.H.C.L.S.P.N.H.F.i.H.P.T.L (2011) Low in-treatment HDL cholesterol levels strongly predict new heart failure in hypertensive patients: the LIFE study. Circulation 124(21):A8654

    Google Scholar 

  78. Zhou Q, Huang G, Yu X, Xu W (2018) A novel approach to estimate ROS origination by hyperbaric oxygen exposure, targeted probes and specific inhibitors. Cell Physiol Biochem 47(5):1800–1808

    CAS  PubMed  Google Scholar 

  79. Xie X, Zhao R, Shen GX (2012) Impact of cyanidin-3-glucoside on glycated LDL-induced NADPH oxidase activation, mitochondrial dysfunction and cell viability in cultured vascular endothelial cells. Int J Mol Sci 13(12):15867–15880

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Suetomi T, Willeford A, Brand CS, Cho Y, Ross RS, Miyamoto S, Brown JH (2018) Inflammation and NLRP3 inflammasome activation initiated in response to pressure overload by Ca(2+)/calmodulin-dependent protein kinase II delta signaling in cardiomyocytes are essential for adverse cardiac remodeling. Circulation 138(22):2530–2544

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Wilson AJ, Gill EK, Abudalo RA, Edgar KS, Watson CJ, Grieve DJ (2018) Reactive oxygen species signalling in the diabetic heart: emerging prospect for therapeutic targeting. Heart 104(4):293–299

    CAS  PubMed  Google Scholar 

  82. Galvani S et al (2015) HDL-bound sphingosine 1-phosphate acts as a biased agonist for the endothelial cell receptor S1P1 to limit vascular inflammation. Sci Signal 8(389):ra79

    PubMed  PubMed Central  Google Scholar 

  83. Durham KK, Chathely KM, Trigatti BL (2018) High-density lipoprotein protects cardiomyocytes against necrosis induced by oxygen and glucose deprivation through SR-B1, PI3K, and AKT1 and 2. Biochem J 475(7):1253–1265

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Yu W et al (2017) Glycation of paraoxonase 1 by high glucose instigates endoplasmic reticulum stress to induce endothelial dysfunction in vivo. Sci Rep 7:45827

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Muller C, Salvayre R, Nègre-Salvayre A, Vindis C (2011) HDLs inhibit endoplasmic reticulum stress and autophagic response induced by oxidized LDLs. Cell Death Differ 18(5):817–828

    CAS  PubMed  Google Scholar 

  86. Christian Besler KH, Makrides V, Riwanto M, Stein S, Verrey F, Lüscher TF, Landmesser U (2010) HDL stimulates endothelial CAT-1 expression and L-arginine uptake: a novel mechanism leading to endothelial-protective effects of HDL that is profoundly altered in patients with coronary disease. Circulation 122(21)

  87. Adams V, Besler C, Fischer T, Riwanto M, Noack F, Höllriegel R, Oberbach A, Jehmlich N, Völker U, Winzer EB, Lenk K, Hambrecht R, Schuler G, Linke A, Landmesser U, Erbs S (2013) Exercise training in patients with chronic heart failure promotes restoration of high-density lipoprotein functional properties. Circ Res 113(12):1345–1355

    CAS  PubMed  Google Scholar 

  88. Sulicka J, Surdacki A, Korkosz M, Mikołajczyk T, Strach M, Klimek E, Guzik T, Grodzicki T (2017) Endothelial dysfunction is independent of inflammation and altered CCR7 T cell expression in patients with ankylosing spondylitis. Clin Exp Rheumatol 35(5):844–849

    PubMed  Google Scholar 

  89. Clemente-Casares X, Hosseinzadeh S, Barbu I, Dick SA, Macklin JA, Wang Y, Momen A, Kantores C, Aronoff L, Farno M, Lucas TM, Avery J, Zarrin-Khat D, Elsaesser HJ, Razani B, Lavine KJ, Husain M, Brooks DG, Robbins CS, Cybulsky M, Epelman S (2017) A CD103(+) conventional dendritic cell surveillance system prevents development of overt heart failure during subclinical viral myocarditis. Immunity 47(5):974–989 e8

    CAS  PubMed  Google Scholar 

  90. Takahashi M (2019) Cell-specific roles of NLRP3 Inflammasome in myocardial infarction. J Cardiovasc Pharmacol 74(3):188–193

    CAS  PubMed  Google Scholar 

  91. Kobayashi M, Usui-Kawanishi F, Karasawa T, Kimura H, Watanabe S, Mise N, Kayama F, Kasahara T, Hasebe N, Takahashi M (2017) The cardiac glycoside ouabain activates NLRP3 inflammasomes and promotes cardiac inflammation and dysfunction. PLoS One 12(5):e0176676

    PubMed  PubMed Central  Google Scholar 

  92. Xi H, Zhang Y, Xu Y, Yang WY, Jiang X, Sha X, Cheng X, Wang J, Qin X, Yu J, Ji Y, Yang X, Wang H (2016) Caspase-1 inflammasome activation mediates homocysteine-induced pyrop-apoptosis in endothelial cells. Circ Res 118(10):1525–1539

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Suetomi T, Miyamoto S, Brown JH (2019) Inflammation in non-ischemic heart disease: initiation by cardiomyocyte CaMKII and NLRP3 inflammasome signaling. Am J Physiol Heart Circ Physiol

  94. Thacker SG, Zarzour A, Chen Y, Alcicek MS, Freeman LA, Sviridov DO, Demosky SJ Jr, Remaley AT (2016) High-density lipoprotein reduces inflammation from cholesterol crystals by inhibiting inflammasome activation. Immunology 149(3):306–319

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Gul I et al (2017) Prognostic role of soluble suppression of tumorigenicity-2 on cardiovascular mortality in outpatients with heart failure. Anatol J Cardiol 18(3):200–205

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Feng J, Zhang J, Jackson AO, Zhu X, Chen H, Chen W, Gui Q, Yin K (2017) Apolipoprotein A1 inhibits the TGF-beta1-induced endothelial-to-mesenchymal transition of human coronary artery endothelial cells. Cardiology 137(3):179–187

    CAS  PubMed  Google Scholar 

  97. Sampietro, F.B.M.P.F.S.M.P.A.E.F.F.B.T., Effect of heart failure induced by pacing on HDL levels and cellular cholesterol efflux in a model of minipig Eur Heart J, 2013. 34(1): p. P4212

  98. Curran NJLRLTHTKNHJE (2017) TRAK2, a novel regulator of ABCA1 expression, cholesterol efflux and HDL biogenesis. Eur Heart J 38(48):3579–3587

    PubMed  PubMed Central  Google Scholar 

  99. Anzures-Cabrera KKRMDDKEJNGSRUJ (2014) The effect of cholesteryl ester transfer protein inhibition on lipids, lipoproteins, and markers of HDL function after an acute coronary syndrome: the dal-ACUTE randomized trial. Eur Heart J 35(27):1792–1800

    PubMed  Google Scholar 

  100. Patel PJ, Khera AV, Wilensky RL, Rader DJ (2013) Anti-oxidative and cholesterol efflux capacities of high-density lipoprotein are reduced in ischaemic cardiomyopathy. Eur J Heart Fail 15(11):1215–1219

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Tzortzis HTIIPTKKS (2013) The association of elevated HDL levels (>70 mg/dl) with carotid atherosclerosis in middle-aged women with first diagnosed and untreated essential hypertension. Eur Heart J 34(1):P693

    Google Scholar 

  102. Miranda-Silva D, Gonçalves-Rodrigues P, Almeida-Coelho J, Hamdani N, Lima T, Conceição G, Sousa-Mendes C, Cláudia-Moura, González A, Díez J, Linke WA, Leite-Moreira A, Falcão-Pires I (2019) Characterization of biventricular alterations in myocardial (reverse) remodelling in aortic banding-induced chronic pressure overload. Sci Rep 9(1):2956

    PubMed  PubMed Central  Google Scholar 

  103. Lore Schrutka, M.K.D., ; Philipp Hohensinner, Patrick Sulzgruber, Impaired high-density lipoprotein anti-oxidative function is associated with outcome in patients with chronic heart failure J Am Heart Assoc, 2016. 5: p. e004169

    PubMed  PubMed Central  Google Scholar 

  104. Pang A et al (2015) Corin is down-regulated and exerts cardioprotective action via activating pro-atrial natriuretic peptide pathway in diabetic cardiomyopathy. Cardiovasc Diabetol 14:134

    PubMed  PubMed Central  Google Scholar 

  105. Ahmad S, Simmons T, Varagic J, Moniwa N, Chappell MC, Ferrario CM (2011) Chymase-dependent generation of angiotensin II from angiotensin-(1-12) in human atrial tissue. PLoS One 6(12):e28501

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Ranjana Tripathi DW, Sullivan R, Fan T-HM, Gladysheva IP (2016) Depressed corin levels indicate early systolic dysfunction before increases of atrial natriuretic peptide/B-type natriuretic peptide and heart failure development. Hypertension 67(2):362–367

    PubMed  Google Scholar 

  107. Tripathi R, Wang D, Sullivan R, Fan TH, Gladysheva IP, Reed GL (2016) Depressed corin levels indicate early systolic dysfunction before increases of atrial natriuretic peptide/B-type natriuretic peptide and heart failure development. Hypertension 67(2):362–367

    CAS  PubMed  Google Scholar 

  108. Backer JDSDDBSCJDMDBMKGD (2005) Plasma N-terminal pro-brain natriuretic peptide concentration predicts coronary events in men at work: a report from the BELSTRESS study. Eur Heart J 26(24):2644–2649

    PubMed  Google Scholar 

  109. Ferreira JP, Metra M, Mordi I, Gregson J, ter Maaten J, Tromp J, Anker SD, Dickstein K, Hillege HL, Ng LL, van Veldhuisen D, Lang CC, Voors AA, Zannad F (2019) Heart failure in the outpatient versus inpatient setting: findings from the BIOSTAT-CHF study. Eur J Heart Fail 21(1):112–120

    CAS  PubMed  Google Scholar 

  110. McMurray JJ et al (2014) Angiotensin-neprilysin inhibition versus enalapril in heart failure. N Engl J Med 371(11):993–1004

    PubMed  Google Scholar 

  111. Velazquez EJ, Morrow DA, DeVore A, Duffy CI, Ambrosy AP, McCague K, Rocha R, Braunwald E, PIONEER-HF Investigators (2019) Angiotensin-neprilysin inhibition in acute decompensated heart failure. N Engl J Med 380(6):539–548

    CAS  PubMed  Google Scholar 

  112. Packer M (2018) Leptin-aldosterone-neprilysin axis: identification of its distinctive role in the pathogenesis of the three phenotypes of heart failure in people with obesity. Circulation 137(15):1614–1631

    CAS  PubMed  Google Scholar 

  113. Quilliot D et al (2005) Myocardial collagen turnover in normotensive obese patients: relation to insulin resistance. Int J Obes 29(11):1321–1328

    CAS  Google Scholar 

  114. Packer M (2018) Derangements in adrenergic-adipokine signalling establish a neurohormonal basis for obesity-related heart failure with a preserved ejection fraction. Eur J Heart Fail 20(5):873–878

    CAS  PubMed  Google Scholar 

  115. Racca V, Castiglioni P, Panzarino C, Saresella M, Marventano I, Verde A, Oliva F, Ferratini M (2018) Differences in biochemical markers between heart-transplanted and left ventricular assist device implanted patients, during cardiac rehabilitation. Sci Rep 8(1):10816

    PubMed  PubMed Central  Google Scholar 

  116. Sandesara PB, O'Neal WT, Kelli HM, Samman-Tahhan A, Hammadah M, Quyyumi AA, Sperling LS (2018) The prognostic significance of diabetes and microvascular complications in patients with heart failure with preserved ejection fraction. Diabetes Care 41(1):150–155

    CAS  PubMed  Google Scholar 

  117. Munoz-Vega M et al (2018) Characterization of immortalized human dermal microvascular endothelial cells (HMEC-1) for the study of HDL functionality. Lipids Health Dis 17(1):44

    PubMed  PubMed Central  Google Scholar 

  118. Munoz-Vega M et al (2018) HDL-mediated lipid influx to endothelial cells contributes to regulating intercellular adhesion molecule (ICAM)-1 expression and eNOS phosphorylation. Int J Mol Sci 19(11)

  119. Giannessi D, Caselli C, del Ry S, Maltinti M, Pardini S, Turchi S, Cabiati M, Sampietro T, Abraham N, L’abbate A, Neglia D (2011) Adiponectin is associated with abnormal lipid profile and coronary microvascular dysfunction in patients with dilated cardiomyopathy without overt heart failure. Metabolism 60(2):227–233

    CAS  PubMed  Google Scholar 

  120. Hermans MP et al (2018) [HDL-C/apoA-I]: a multivessel cardiometabolic risk marker in women with T2DM. Diabetes Metab Res Rev 34(1)

  121. Jaana Rysä HL, Ilves M, Ruskoaho H (2005) Distinct upregulation of extracellular matrix genes in transition from hypertrophy to hypertensive heart failure. Hypertension 45:927–933

    PubMed  Google Scholar 

  122. Amin R et al (2017) Selective HDL-raising human Apo A-I gene therapy counteracts cardiac hypertrophy, reduces myocardial fibrosis, and improves cardiac function in mice with chronic pressure overload. Int J Mol Sci 18(9)

  123. Nishiga M, Horie T, Kuwabara Y, Nagao K, Baba O, Nakao T, Nishino T, Hakuno D, Nakashima Y, Nishi H, Nakazeki F, Ide Y, Koyama S, Kimura M, Hanada R, Nakamura T, Inada T, Hasegawa K, Conway SJ, Kita T, Kimura T, Ono K (2017) MicroRNA-33 controls adaptive fibrotic response in the remodeling heart by preserving lipid raft cholesterol. Circ Res 120(5):835–847

    CAS  PubMed  Google Scholar 

  124. Lin L, Gong H, Ge J, Jiang G, Zhou N, Li L, Ye Y, Zhang G, Ge J, Zou Y (2011) High density lipoprotein downregulates angiotensin II type 1 receptor and inhibits angiotensin II-induced cardiac hypertrophy. Biochem Biophys Res Commun 404(1):28–33

    CAS  PubMed  Google Scholar 

  125. Morin C, Rousseau E, Blier PU, Fortin S (2015) Effect of docosahexaenoic acid monoacylglyceride on systemic hypertension and cardiovascular dysfunction. Am J Physiol Heart Circ Physiol 309(1):H93–H102

    CAS  PubMed  Google Scholar 

  126. Givvimani S et al (2015) Hyperhomocysteinemia: a missing link to dysfunctional HDL via paraoxanase-1. Can J Physiol Pharmacol 93(9):755–763

    CAS  PubMed  Google Scholar 

  127. Potocnjak I et al (2016) Metrics of high-density lipoprotein function and hospital mortality in acute heart failure patients. PLoS One 11(6):e0157507

    PubMed  PubMed Central  Google Scholar 

  128. Yuhanna IS, Zhu Y, Cox BE, Hahner LD, Osborne-Lawrence S, Lu P, Marcel YL, Anderson RG, Mendelsohn ME, Hobbs HH, Shaul PW (2001) High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat Med 7(7):853–857

    CAS  PubMed  Google Scholar 

  129. Chen RZCYQXXGWMHLYQYYZZJBGHZ (2013) BMP7 counteracts TGF beta1 induced endothelial-to-mesenchymal transition in viral cardiomyopathy and its potential mechanism. Eur Heart J 34(1):P2964

    Google Scholar 

  130. Chen H et al (2019) Ghrelin attenuates myocardial fibrosis after acute myocardial infarction via inhibiting endothelial-to mesenchymal transition in rat model. Peptides 111:118–126

    CAS  PubMed  Google Scholar 

  131. Biolo A, Fisch M, Balog J, Chao T, Schulze PC, Ooi H, Siwik D, Colucci WS (2010) Episodes of acute heart failure syndrome are associated with increased levels of troponin and extracellular matrix markers. Circ Heart Fail 3(1):44–50

    CAS  PubMed  Google Scholar 

  132. Tsai TH et al (2019) Calcitriol attenuates doxorubicin-induced cardiac dysfunction and inhibits endothelial-to-mesenchymal transition in mice. Cells 8(8)

  133. Spillmann F et al (2015) High-density lipoproteins reduce endothelial-to-mesenchymal transition. Arterioscler Thromb Vasc Biol 35(8):1774–1777

    CAS  PubMed  Google Scholar 

  134. Li XA, Guo L, Dressman JL, Asmis R, Smart EJ (2005) A novel ligand-independent apoptotic pathway induced by scavenger receptor class B, type I and suppressed by endothelial nitric-oxide synthase and high density lipoprotein. J Biol Chem 280(19):19087–19096

    CAS  PubMed  Google Scholar 

  135. Pu DR, Liu L (2008) HDL slowing down endothelial progenitor cells senescence: a novel anti-atherogenic property of HDL. Med Hypotheses 70(2):338–342

    CAS  PubMed  Google Scholar 

  136. Shi Q, Hornsby PJ, Meng Q, Vandeberg JF, Vandeberg JL (2013) Longitudinal analysis of short-term high-fat diet on endothelial senescence in baboons. Am J Cardiovasc Dis 3(3):107–119

    PubMed  PubMed Central  Google Scholar 

  137. Katsuumi G, Shimizu I, Yoshida Y, Hayashi Y, Ikegami R, Suda M, Wakasugi T, Nakao M, Minamino T (2018) Catecholamine-induced senescence of endothelial cells and bone marrow cells promotes cardiac dysfunction in mice. Int Heart J 59(4):837–844

    CAS  PubMed  Google Scholar 

  138. Tardif DBNMTM-AMMYSGBNLJ-LDERJ-C (2013) High-density lipoprotein (HDL) mimetic peptide CER-522 induces regression of experimental left ventricular diastolic dysfunction. Eur Heart J 34(1):P2433

    Google Scholar 

  139. Trigatti KDaB (2018) Scavenger receptor class B type I is required for protection by high-density lipoprotein against doxorubicin-induced apoptosis in both mouse and human cardiomyocytes and cardiotoxicity in mice. Arterioscler Thromb Vasc Biol 34:A428

    Google Scholar 

  140. Adele Richart SEH, Henstridge DC, Alt K, Kiriazis H, Carey AL, Kammoun H, Begum H (2018) HDL modulates cardiac glucose metabolism and inflammation and improves cardiac function after myocardial ischemia reperfusion injury. Cardiology 134(1):A16760

    Google Scholar 

  141. Heidt T, Courties G, Dutta P, Sager HB, Sebas M, Iwamoto Y, Sun Y, da Silva N, Panizzi P, van der Laan A, Swirski FK, Weissleder R, Nahrendorf M (2014) Differential contribution of monocytes to heart macrophages in steady-state and after myocardial infarction. Circ Res 115(2):284–295

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Yadav R, Liu Y, Kwok S, Hama S, France M, Eatough R, Pemberton P, Schofield J, Siahmansur TJ, Malik R, Ammori BA, Issa B, Younis N, Donn R, Stevens A, Durrington P, Soran H (2015) Effect of extended-release niacin on high-density lipoprotein (HDL) functionality, lipoprotein metabolism, and mediators of vascular inflammation in statin-treated patients. J Am Heart Assoc 4(9):e001508

    PubMed  PubMed Central  Google Scholar 

  143. Tsuda S, Shinohara M, Oshita T, Nagao M, Tanaka N, Mori T, Hara T, Irino Y, Toh R, Ishida T, Hirata KI (2017) Novel mechanism of regulation of the 5-lipoxygenase/leukotriene B4 pathway by high-density lipoprotein in macrophages. Sci Rep 7(1):12989

    PubMed  PubMed Central  Google Scholar 

  144. De Nardo D et al (2014) High-density lipoprotein mediates anti-inflammatory reprogramming of macrophages via the transcriptional regulator ATF3. Nat Immunol 15(2):152–160

    PubMed  Google Scholar 

  145. Lameijer M, Binderup T, van Leent M, Senders ML, Fay F, Malkus J, Sanchez-Gaytan BL, Teunissen AJP, Karakatsanis N, Robson P, Zhou X, Ye Y, Wojtkiewicz G, Tang J, Seijkens TTP, Kroon J, Stroes ESG, Kjaer A, Ochando J, Reiner T, Pérez-Medina C, Calcagno C, Fisher EA, Zhang B, Temel RE, Swirski FK, Nahrendorf M, Fayad ZA, Lutgens E, Mulder WJM, Duivenvoorden R (2018) Efficacy and safety assessment of a TRAF6-targeted nanoimmunotherapy in atherosclerotic mice and non-human primates. Nat Biomed Eng 2(5):279–292

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Bansal SS, Ismahil MA, Goel M, Zhou G, Rokosh G, Hamid T, Prabhu SD (2019) Dysfunctional and proinflammatory regulatory T-lymphocytes are essential for adverse cardiac remodeling in ischemic cardiomyopathy. Circulation 139(2):206–221

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Ramos GC, van den Berg A, Nunes-Silva V, Weirather J, Peters L, Burkard M, Friedrich M, Pinnecker J, Abeßer M, Heinze KG, Schuh K, Beyersdorf N, Kerkau T, Demengeot J, Frantz S, Hofmann U (2017) Myocardial aging as a T-cell-mediated phenomenon. Proc Natl Acad Sci U S A 114(12):E2420–E2429

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Ahnstedt H et al (2018) Sex differences in adipose tissue CD8(+) T cells and regulatory T cells in middle-aged mice. Front Immunol 9:659

    PubMed  PubMed Central  Google Scholar 

  149. Westerterp M et al (2017) Cholesterol accumulation in dendritic cells links the Inflammasome to acquired immunity. Cell Metab 25(6):1294–1304 e6

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Tiniakou I et al (2015) High-density lipoprotein attenuates Th1 and th17 autoimmune responses by modulating dendritic cell maturation and function. J Immunol 194(10):4676–4687

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Wang SH et al (2012) HDL and ApoA-I inhibit antigen presentation-mediated T cell activation by disrupting lipid rafts in antigen presenting cells. Atherosclerosis 225(1):105–114

    CAS  PubMed  Google Scholar 

  152. Lekakis HTIIPTKKSTGPFHMA-NJ (2013) The association of elevated HDL levels (>70 mg/dl) with carotid atherosclerosis in middle-aged women with first diagnosed and untreated essential hypertension. Eur Heart J 34(1):P693

    Google Scholar 

  153. Prabhu Mathiyalagan YL, Sassi Y, Adamiak M, Ishikawa K, Zhong S, Kohlbrenner E, Yin X, Chepurko E, Agarwal N (2017) Modulation of N6-methyladenosine (m6A) by the Fat mass obesity-associated gene (FTO) regulates cardiac function. Circulation 136(1):A17407

    Google Scholar 

  154. Prabhu Mathiyalagan MA, Mayourian J, Sassi Y, Liang Y, Agarwal N, Jha D, Zhang S, Kohlbrenner E, Chepurko E, Chen J, Trivieri MG (2019) FTO-dependent n6-methyladenosine regulates cardiac function during remodeling and repair. Circulation 139:518–532

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research was supported by the National Natural Sciences Foundation of China (81970390, 81470569), the Innovation Foundation for Postgraduate of Hunan Province (CX2017B550, CX2016B490), Natural Science Foundation of Hunan Province, China (2018JJ2341), Science Foundation of the Health and Family Planning Commission in Hunan Province of China (B2019122), and the National College Students Innovation and Entrepreneurship Fund (201710555015, 201710555010).

Author information

Authors and Affiliations

  1. Center for Diabetic Systems Medicine, Guangxi Key Laboratory of Excellence, Guilin Medical University, Guilin, 541100, Guangxi, China

    Ampadu O. Jackson & Kai Yin

  2. International College, University of South China, Hengyang, Hunan Province, China

    Ampadu O. Jackson

  3. Functional Department, The First Affiliated Hospital of University of South China, Hengyang, 421001, Hunan, China

    Jun Meng

  4. Department of Cardiology, The First Affiliated Hospital of University of South China, Hengyang, Hunan Province, China

    Huifang Tang

  5. College of General Practitioners, The Second Affiliated Hospital of Guilin Medical University, Guilin, 541100, Guangxi, China

    Kai Yin

Authors
  1. Ampadu O. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huifang Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kai Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kai Yin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jackson, A., Meng, J., Tang, H. et al. High-density lipoprotein-mediated cardioprotection in heart failure. Heart Fail Rev 26, 767–780 (2021). https://doi.org/10.1007/s10741-020-09916-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10741-020-09916-0

Keywords

Search

Navigation