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Role of oxidative stress-related biomarkers in heart failure: galectin 3, α1-antitrypsin and LOX-1: new therapeutic perspective?

  • Valter LubranoEmail author
  • Silvana Balzan
Article

Abstract

Heart failure (HF) is considered one of the most common diseases and one of the major causes of death. The latest studies show that HF is associated with an increase in oxidative stress. The use of antioxidants as therapy is effective in animal models, but not in humans. In this review, we analyse some emerging markers related to oxidative stress, evaluating their possible use as therapeutic targets: galectin-3, a β galactoside associated with myocardial fibrosis, α1-antitrypsin, an antiprotease and lectin-like oxidized low-density-lipoprotein receptor-1, the major receptor for ox-LDL. The up-regulation of galectin-3 appears to be associated with HF, atrial fibrillation, dilated cardiomyopathy, fibrogenesis and mortality, while in other cases it seems that galectin-3 may be protective in ischaemia–reperfusion injury. Serum α1-antitrypsin protein levels may increase in the presence of high concentrations of serum proteases, which are over expressed during reperfusion. The overexpression of α1-antitrypsin or the exogenous α1-antitrypsin treatment exhibits an anti-oxidative stress role, evaluated by increased eNOS expression and by decreased MMP9 expression, implicated in HF. The cardiac lectin-like oxidized low-density-lipoprotein receptor-1 is activated by oxidative stress in ischaemia–reperfusion injury, inducing apoptosis in cardiomyocytes through the deleterious NF-kB pathway, while the administration of anti-lectin-like oxidized low-density-lipoprotein receptor-1 antibody suppresses apoptosis and reduces the extent of myocardial infarction. In conclusion, α1-antitrypsin and lectin-like oxidized low-density-lipoprotein receptor-1 seem to represent two good markers in HF and therapeutic targets, whereas galectin-3 does not.

Keywords

Biomarkers Oxidative stress Galectin-3 α1-Antitrypsin Lectin-like oxidized low-density-lipoprotein receptor-1 Heart failure 

Notes

Acknowledgements

The authors are grateful to Dr. Lucrecia Mota and Michael Minks for their English editing support.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

References

  1. 1.
    Palazzuoli A, Nuti R (2010) Heart failure: pathophysiology and clinical picture. Contrib Nephrol 164:1–10.  https://doi.org/10.1159/000313714 CrossRefPubMedGoogle Scholar
  2. 2.
    Lim S, Lam CS, Segers VF et al (2015) Cardiac endothelium-myocyte interaction: clinical opportunities for new heart failure therapies regardless of ejection fraction. Eur Heart J 36:2050–2060.  https://doi.org/10.1093/eurheartj/ehv132 CrossRefPubMedGoogle Scholar
  3. 3.
    Paulus WJ, Tschope C (2013) A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodelling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 62:263–267.  https://doi.org/10.1016/j.jacc.2013.02.092 CrossRefPubMedGoogle Scholar
  4. 4.
    Sun RR, Lu L, Liu M et al (2014) Biomarkers and heart disease. Eur Rev Med Pharmacol Sci 18:2927–2935PubMedGoogle Scholar
  5. 5.
    De Boer RA, Van der Velde AR, Mueller C et al (2014) Galectin-3: a modifiable risk factor in heart failure. Cardiovasc Drugs Ther 28:237–246.  https://doi.org/10.1007/s10557-014-6520-2 CrossRefPubMedGoogle Scholar
  6. 6.
    Lubrano V, Papa A, Pingitore A et al (2017) Alpha-1 protein evaluation to stratify heart failure patients. J Cardiovasc Med 18:774–776.  https://doi.org/10.2459/JCM.0000000000000016 CrossRefGoogle Scholar
  7. 7.
    Kataoka K, Hasegawa K, Sawamura T et al (2003) LOX-1 pathway affects the extent of myocardial ischemia-reperfusion injury. Biochem Biophys Res Commun 300:656–660.  https://doi.org/10.1016/s0006-291x(02)02905-4 CrossRefPubMedGoogle Scholar
  8. 8.
    Doughan AK, Harrison DG, Dikalov SI (2008) Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 102:488–496.  https://doi.org/10.1161/CIRCRESAHA.107.162800 CrossRefPubMedGoogle Scholar
  9. 9.
    Heymes C, Bendall JK, Ratajczak P et al (2003) Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 41:2164–2171.  https://doi.org/10.1016/s0735-1097(03)00471-6 CrossRefPubMedGoogle Scholar
  10. 10.
    Cappola TP, Kass DA, Nelson GS et al (2001) Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation 104:2407–2411.  https://doi.org/10.1161/hc4501.098928 CrossRefPubMedGoogle Scholar
  11. 11.
    Dhalla NS, Das PK, Sharma GP (1978) Subcellular basis of cardiac contractile failure. J Mol Cell Cardiol 10:363–385CrossRefGoogle Scholar
  12. 12.
    Dhalla NS, Temsah RM, Netticadan T (2000) Role of oxidative stress in cardiovascular diseases. J Hypertens 18:655–673.  https://doi.org/10.1097/00004872-200018060-00002 CrossRefPubMedGoogle Scholar
  13. 13.
    Blayney LM, Lai FA (2009) Ryanodine receptor-mediated arrhythmias and sudden cardiac death. Pharmacol Ther 123:151–177.  https://doi.org/10.1016/j.pharmthera.2009.03.006 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Mochizuki M, Yano M, Oda T et al (2007) Scavenging free radicals by low-dose carvedilol prevents redox-dependent Ca2+ leak via stabilization of ryanodine receptor in heart failure. J Am Coll Cardiol 49:1722–1732.  https://doi.org/10.1016/j.jacc.2007.01.064 CrossRefPubMedGoogle Scholar
  15. 15.
    Terentyev D, Györke I, Belevych AE et al (2008) Redox modification of ryanodine receptors contributes to sarcoplasmic reticulum Ca2+ leak in chronic heart failure. Circ Res 103:1466–1472.  https://doi.org/10.1161/CIRCRESAHA.108.184457 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Indo HP, Davidson M, Yen HC et al (2007) Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 7:106–118.  https://doi.org/10.1016/j.mito.2006.11.026 CrossRefPubMedGoogle Scholar
  17. 17.
    Hayashi D, Ohshima S, Isobe S et al (2013) Increased (99 m)Tc-sestamibi washout reflects impaired myocardial contractile and relaxation reserve during dobutamine stress due to mitochondrial dysfunction in dilated cardiomyopathy patients. J Am Coll Cardiol 61:2007–2017.  https://doi.org/10.1016/j.jacc.2013.01.074 CrossRefPubMedGoogle Scholar
  18. 18.
    Ahuja P, Wanagat J, Wang Z et al (2013) Divergent mitochondrial biogenesis responses in human cardiomyopathy. Circulation 127:1957–1967.  https://doi.org/10.1161/CIRCULATIONAHA.112.001219 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Redout EM, Wagner MJ, Zuidwijk MJ et al (2007) Right-ventricular failure is associated with increased mitochondrial complex II activity and production of reactive oxygen species. Cardiovasc Res 75:770–781.  https://doi.org/10.1016/j.cardiores.2007.05.012 CrossRefPubMedGoogle Scholar
  20. 20.
    Kubli DA, Gustafsson ÅB (2012) Mitochondria and mitophagy: the yin and yang of cell death control. Circ Res 111:1208–1221.  https://doi.org/10.1161/CIRCRESAHA.112.265819 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wang K, Klionsky DJ (2011) Mitochondria removal by autophagy. Autophagy 7:297–300.  https://doi.org/10.4161/auto.7.3.14502 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Piper HM, García-Dorado DM et al (1998) A fresh look at reperfusion injury. Cardiovasc Res 38:291–300.  https://doi.org/10.1016/s0008-6363(98)00033-9 CrossRefPubMedGoogle Scholar
  23. 23.
    Buja LM (2005) Myocardial ischemia and reperfusion injury. Cardiovasc Pathol 14:170–175.  https://doi.org/10.1016/j.carpath.2005.03.006 CrossRefPubMedGoogle Scholar
  24. 24.
    Bulluck H, Yellon DM, Hausenloy DJ (2016) Reducing myocardial infarct size: challenges and future opportunities. Heart 102:341–348.  https://doi.org/10.1136/heartjnl-2015-307855 CrossRefPubMedGoogle Scholar
  25. 25.
    Raedschelders K, Ansley DM, Chen DD (2012) The cellular and molecular origin of reactive oxygen species generation during myocardial ischemia and reperfusion. Pharmacol Ther 133:230–255.  https://doi.org/10.1016/j.pharmthera.2011.11.004 CrossRefPubMedGoogle Scholar
  26. 26.
    Khaper N, Singal PK (1997) Effects of after load-reducing drugs on pathogenesis of antioxidant changes and congestive heart failure in rats. J Am Coll Cardiol 9:856–861.  https://doi.org/10.1016/s0735-1097(96)00574-8 CrossRefGoogle Scholar
  27. 27.
    Khaper N, Kaur K, Li T et al (2003) Antioxidant enzyme gene expression in congestive heart failure following myocardial infarction. Mol Cell Biochem 251:9–15CrossRefGoogle Scholar
  28. 28.
    Adamy C, Mulder P, Khouzami L et al (2007) Neutral sphingomyelinase inhibition participates to the benefits of N-acetylcysteine treatment in post-myocardial infarction failing heart rats. J Mol Cell Cardiol 43:344–353.  https://doi.org/10.1016/j.yjmcc.2007.06.010 CrossRefPubMedGoogle Scholar
  29. 29.
    Townsend DM, Tew KD, Tapiero H (2003) The importance of glutathione in human disease. Biomed Pharmacother 57:145–155CrossRefGoogle Scholar
  30. 30.
    Minhas KM, Saraiva RM, Schuleri KH et al (2006) Xanthine oxidoreductase inhibition causes reverse remodeling in rats with dilated cardiomyopathy. Circ Res 98:271–279.  https://doi.org/10.1161/01.RES.0000200181.59551.71 CrossRefPubMedGoogle Scholar
  31. 31.
    Ukai T, Cheng CP, Tachibana H et al (2001) Allopurinol enhances the contractile response to dobutamine and exercise in dogs with pacing-induced heart failure. Circulation 103:750–755.  https://doi.org/10.1161/01.cir.103.5.750 CrossRefPubMedGoogle Scholar
  32. 32.
    Takimoto E, Champion HC, Li M et al (2005) Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodelling from chronic pressure load. J Clin Invest 115:1221–1231.  https://doi.org/10.1172/JCI21968 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Wang P, Chen H, Qin H et al (1998) Overexpression of human copper, zinc-superoxide dismutase (SOD1) prevents post ischemic injury. Proc Natl Acad Sci USA 95:4556–4560.  https://doi.org/10.1073/pnas.95.8.4556 CrossRefPubMedGoogle Scholar
  34. 34.
    Qin F, Lennon-Edwards S, Lancel S et al (2010) Cardiac-specific overexpression of catalase identifies hydrogen peroxide-dependent and -independent phases of myocardial remodelling and prevents the progression to overt heart failure in G(alpha)q-overexpressing transgenic mice. Circ Heart Fail 3:306–313.  https://doi.org/10.1161/CIRCHEARTFAILURE.109.864785 CrossRefPubMedGoogle Scholar
  35. 35.
    Hamblin M, Smith HM, Hill MF (2007) Dietary supplementation with vitamin E ameliorates cardiac failure in type I diabetic cardiomyopathy by suppressing myocardial generation of 8-iso-prostaglandin F2 alpha and oxidized glutathione. J Card Fail 13:884–892.  https://doi.org/10.1016/j.cardfail.2007.07.002 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Li W, Tang R, Ouyang S et al (2017) Folic acid prevents cardiac dysfunction and reduces myocardial fibrosis in a mouse model of high-fat diet-induced obesity. Nutr Metab 14:68.  https://doi.org/10.1186/s12986-017-0224-0 CrossRefGoogle Scholar
  37. 37.
    Cunnington C, Van Assche T, Shirodaria C et al (2012) Systemic and vascular oxidation limits the efficacy of oral tetrahydrobiopterin treatment in patients with coronary artery disease. Circulation 125:1356–1366.  https://doi.org/10.1161/CIRCULATIONAHA.111.038919 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Freudenberger RS, Schwarz RP, Brown J et al (2004) Rationale, design and organisation of an efficacy and safety study of oxypurinol added to standard therapy in patients with NYHA class III-IV congestive heart failure. Expert Opin Investig Drugs 13:1509–1516.  https://doi.org/10.1517/13543784.13.11.1509 CrossRefPubMedGoogle Scholar
  39. 39.
    Hare JM, Mangal B, Brown J et al (2008) Impact of oxypurinol in patients with symptomatic heart failure. J Am Coll Cardiol 51:2301–2309.  https://doi.org/10.1016/j.jacc.2008.01.068 CrossRefPubMedGoogle Scholar
  40. 40.
    Louzao-Martinez L, Vink A, Harakalova M et al (2016) Characteristic adaptations of the extracellular matrix in dilated cardiomyopathy. Int J Cardiol 220:634–646.  https://doi.org/10.1016/j.ijcard.2016.06.253 CrossRefPubMedGoogle Scholar
  41. 41.
    Al-Salam S, Hashmi S (2018) Myocardial ischemia reperfusion injury: apoptotic, inflammatory and oxidative stress. Role of galectin-3. Cell Physiol Biochem 50:1123–1139.  https://doi.org/10.1159/000494539 CrossRefPubMedGoogle Scholar
  42. 42.
    Ochieng J, Furtak V, Lukyanov P (2002) Extracellular functions of galectin-3. Glycoconj J 19:527–535.  https://doi.org/10.1023/B:GLYC.0000014082.99675.2f CrossRefPubMedGoogle Scholar
  43. 43.
    Akahani S, Nangia-Makker P, Inohara H et al (1997) Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res 57:5272–5276PubMedGoogle Scholar
  44. 44.
    Seetharaman J, Kanigsberg A, Slaaby R et al (1998) X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-A resolution. J Biol Chem 273:13047–13052.  https://doi.org/10.1074/jbc.273.21.13047 CrossRefPubMedGoogle Scholar
  45. 45.
    Bachhawat-Sikder K, Thomas CJ, Surolia A (2001) Thermodynamic analysis of the binding of galactose and poly-N-acetyllactosamine derivatives to human galectin-3. FEBS Lett 500:75–79.  https://doi.org/10.1016/s0014-5793(01)02586-8 CrossRefPubMedGoogle Scholar
  46. 46.
    Ochieng J, Fridman R, Nangia-Makker P et al (1994) Galectin-3 is a novel substrate for human matrix metalloproteinases-2 and -9. Biochemistry 33:14109–14114.  https://doi.org/10.1021/bi00251a020 CrossRefPubMedGoogle Scholar
  47. 47.
    Mey A, Leffler H, Hmama Z et al (1996) The animal lectin galectin-3 interacts with bacterial lipopolysaccharides via two independent sites. J Immunol 156:1572–1577PubMedGoogle Scholar
  48. 48.
    Ochieng J, Warfield P, Green-Jarvis B et al (1999) Galectin-3 regulates the adhesive interaction between breast carcinoma cells and elastin. J Cell Biochem 75:505–514CrossRefGoogle Scholar
  49. 49.
    Sciacchitano S, Lavra L, Morgante A et al (2018) One molecule for an alphabet of diseases, from A to Z. Int J Mol Sci 19(2):E379.  https://doi.org/10.3390/ijms19020379 CrossRefPubMedGoogle Scholar
  50. 50.
    Rabinovich GA, Toscano MA (2009) Turning “sweet” on immunity: galectin glycan interactions in immune tolerance and inflammation. Nat Rev Immunol 9:338–352.  https://doi.org/10.1038/nri2536 CrossRefPubMedGoogle Scholar
  51. 51.
    Arad U, Madar-Balakirski N, Angel-Korman A et al (2015) Galectin-3 is a sensor-regulator of toll-like receptor pathways in synovial fibroblasts. Cytokine 73:30–35.  https://doi.org/10.1016/j.cyto.2015.01.016 CrossRefPubMedGoogle Scholar
  52. 52.
    De Boer RA, Daniels LB, Maisel AS et al (2015) State of the art: newer biomarkers in heart failure. Eur J Heart Fail 17:559–569.  https://doi.org/10.1002/ejhf.273 CrossRefPubMedGoogle Scholar
  53. 53.
    Besler C, Lang D, Urban D et al (2017) Plasma and cardiac galectin-3 in patients with heart failure reflects both inflammation and fibrosis: implications for its use as a biomarker. Circ Heart Fail 10(1–9):e003804.  https://doi.org/10.1161/CIRCHEARTFAILURE.116.003804 CrossRefPubMedGoogle Scholar
  54. 54.
    Frunza O, Russo I, Saxena A et al (2016) Myocardial galectin-3 expression is associated with remodeling of the pressure-overloaded heart and may delay the hypertrophic response without affecting survival, dysfunction and cardiac fibrosis. Am J Pathol 186:1114–1127.  https://doi.org/10.1016/j.ajpath.2015.12.017 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Nguyen MN, Su Y, Vizi D et al (2018) Mechanisms responsible for increased circulating levels of galectin-3 in cardiomyopathy and heart failure. Sci Rep 8(8213):1–12.  https://doi.org/10.1038/s41598-018-26115-y CrossRefGoogle Scholar
  56. 56.
    Hernández-Romero D, Vílchez JA, Lahoz Á et al (2017) Galectin-3 as a marker of interstitial atrial remodelling involved in atrial fibrillation. Sci Rep 7:40378.  https://doi.org/10.1038/srep40378 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Jaquenod De Giusti C, Ure AE, Rivadeneyra L et al (2015) Macrophages and galectin 3 play critical roles in CVB3-induced murine acute myocarditis and chronic fibrosis. J Mol Cell Cardiol 85:58–70.  https://doi.org/10.1016/j.yjmcc.2015.05.010 CrossRefPubMedGoogle Scholar
  58. 58.
    Peacock WF (2003) Rapid optimization: strategies for optimal care of decompensated congestive heart failure patients in the emergency department. Rev Cardiovasc Med 3:41–48Google Scholar
  59. 59.
    Meijers WC, De Boer RA, Van Veldhuisen DJ et al (2015) Biomarkers and low risk in heart failure, data from COACH and TRIUMPH. Eur J Heart Fail 17:1271–1282.  https://doi.org/10.1002/ejhf.407 CrossRefPubMedGoogle Scholar
  60. 60.
    Meijers WC, Januzzi JL, Adourian AS et al (2014) Elevated plasma galectin-3 is associated with near-term rehospitalisation in heart failure: a pooled analysis of 3 clinical trials. Am Heart J 167:853–860.  https://doi.org/10.1016/j.ahj.2014.02.011 CrossRefPubMedGoogle Scholar
  61. 61.
    Martínez-Martínez E, Calvier L, Fernández-Celis A et al (2015) Galectin-3 blockade inhibits cardiac inflammation and fibrosis in experimental hyperaldosteronism and hypertension. Hypertension 66:767–775.  https://doi.org/10.1161/HYPERTENSIONAHA.115.05876 CrossRefPubMedGoogle Scholar
  62. 62.
    Calvier L, Martinez-Martinez E, Miana M et al (2015) The impact of galectin-3 inhibition on aldosterone-induced cardiac and renal injuries. JACC Heart Fail 3:59–67.  https://doi.org/10.1016/j.jchf.2014.08.002 CrossRefPubMedGoogle Scholar
  63. 63.
    Yu L, Ruifrok WP, Meissner M et al (2013) Genetic and pharmacological inhibition of galectin-3 prevents cardiac remodeling by interfering with myocardial fibrogenesis. Circ Heart Fail 6:107–117.  https://doi.org/10.1161/CIRCHEARTFAILURE.112.971168 CrossRefPubMedGoogle Scholar
  64. 64.
    Nguyen MN, Su Y, Kiriazis H et al (2018) Upregulated galectin-3 is not a critical disease mediator of cardiomyopathy induced by β2-adrenoceptor overexpression. Am J Physiol Heart Circ Physiol 314:1169–1178CrossRefGoogle Scholar
  65. 65.
    Grupper A, Nativi-Nicolau J, Maleszewski JJ et al (2016) Circulating galectin-3 levels are persistently elevated after heart transplantation and are associated with renal dysfunction. JACC Heart Fail 4:847–856.  https://doi.org/10.1016/j.jchf.2016.06.010 CrossRefPubMedGoogle Scholar
  66. 66.
    Jolly SR, Kane WJ, Bailie MB et al (1984) Canine myocardial reperfusion injury. Its reduction by the combined administration of superoxide dismutase and catalase. Circ Res 54:277–285.  https://doi.org/10.1161/01.res.54.3.277 CrossRefPubMedGoogle Scholar
  67. 67.
    Nakamura H, Nakamura K, Yodoi J (1997) Redox regulation of cellular activation. Annual Rev Immunol 15:351–369.  https://doi.org/10.1146/annurev.immunol.15.1.351 CrossRefGoogle Scholar
  68. 68.
    Ceconi C, Curello S, Cargnoni A et al (1988) The role of glutathione status in the protection against ischaemic and reperfusion damage: effects of N-acetyl cysteine. J Mol Cell Cardiol 20:5–13CrossRefGoogle Scholar
  69. 69.
    Singh A, Lee KJ, Lee CY et al (1989) Relation between myocardial glutathione content and extent of ischemia-reperfusion injury. Circulation 80:1795–1804.  https://doi.org/10.1161/01.cir.80.6.1795 CrossRefPubMedGoogle Scholar
  70. 70.
    Chen Z, Siu B, Ho YS et al (1998) Overexpression of MnSOD protects against myocardial ischemia/reperfusion injury in transgenic mice. J Mol Cell Cardiol 30:2281–2289.  https://doi.org/10.1006/jmcc.1998.0789 CrossRefPubMedGoogle Scholar
  71. 71.
    Woo YJ, Zhang JC, Vijayasarathy C et al (1998) Recombinant adenovirus-mediated cardiac gene transfer of superoxide dismutase and catalase attenuates post ischemic contractile dysfunction. Circulation 98:II255–II260PubMedGoogle Scholar
  72. 72.
    Matarrese P, Tinari N, Semeraro ML et al (2000) Galectin-3 overexpression protects from cell damage and death by influencing mitochondrial homeostasis. FEBS Lett 473:311–315.  https://doi.org/10.1016/s0014-5793(00)01547-7 CrossRefPubMedGoogle Scholar
  73. 73.
    Fernandes Bertocchi AP, Campanhole G, Wang PH et al (2008) A role for galectin-3 in renal tissue damage triggered by ischemia and reperfusion injury. Transpl Int 21:999–1007.  https://doi.org/10.1111/j.1432-2277.2008.00705.x CrossRefPubMedGoogle Scholar
  74. 74.
    Yamaoka A, Kuwabara I, Frigeri LG et al (1995) A human lectin, galectin-3 (epsilon bp/Mac-2), stimulates superoxide production by neutrophils. J Immunol 154:3479–3487PubMedGoogle Scholar
  75. 75.
    Dong R, Zhang M, Hu Q et al (2018) Galectin-3 as a novel biomarker for disease diagnosis and a target for therapy. Int J Mol Med 41:599–614.  https://doi.org/10.3892/ijmm.2017.3311 CrossRefPubMedGoogle Scholar
  76. 76.
    Berezin AE, Kremzer AA, Samura TA et al (2019) Altered signature of apoptotic endothelial cell-derived microvesicles predicts chronic heart failure phenotypes. Biomark Med 13:737–750.  https://doi.org/10.2217/bmm-2018-0449 CrossRefPubMedGoogle Scholar
  77. 77.
    Beltrami M, Ruocco G, Dastidar AG et al (2016) Additional value of Galectin-3 to BNP in acute heart failure patients with preserved ejection fraction. Clin Chim Acta 457:99–105.  https://doi.org/10.1016/j.cca.2016.04.007 CrossRefPubMedGoogle Scholar
  78. 78.
    Li M, Georgakopoulos D, Lu G et al (2005) p38 MAP kinase mediates inflammatory cytokine induction in cardiomyocytes and extracellular matrix remodeling in heart. Circulation 111:2494–2502.  https://doi.org/10.1161/01.CIR.0000165117.71483.0C CrossRefPubMedGoogle Scholar
  79. 79.
    Moore L, Fan D, Basu R et al (2012) Tissue inhibitor of metalloproteinases (TIMPs) in heart failure. Heart Fail Rev 17:693–706.  https://doi.org/10.1007/s10741-011-9266-y CrossRefPubMedGoogle Scholar
  80. 80.
    Lewis EC (2012) Expanding the clinical indications for α (1)-antitrypsin therapy. Mol Med 18:957–970.  https://doi.org/10.2119/molmed.2011.00196 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Abbate A, Van Tassell BW, Christopher S et al (2015) Effects of prolastin C (plasma-derived alpha-1 antitrypsin) on the acute inflammatory response in patients with ST-segment elevation myocardial infarction (from the VCU-alpha 1-RT pilot study). Am J Cardiol 115:8–12.  https://doi.org/10.1016/j.amjcard.2014.09.043 CrossRefPubMedGoogle Scholar
  82. 82.
    Duckers JM, Shale DJ, Stockley RA et al (2010) Cardiovascular and muscle skeletal co-morbidities in patients with alpha 1 antitrypsin deficiency. Respir Res 11:173.  https://doi.org/10.1186/1465-9921-11-1 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Forsyth KD, Talbot V, Beckman I (1994) Endothelial serpins-protectors of the vasculature? Clin Exp Immunol 95:277–282.  https://doi.org/10.1111/j.1365-2249.1994.tb06523.x CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Ortiz-Muñoz G, Houard X, Martín-Ventura JL et al (2009) HDL antielastase activity prevents smooth muscle cell anoikis, a potential new antiatherogenic property. FASEB J 23:3129–3139.  https://doi.org/10.1096/fj.08-127928 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Aldonyte R, Janssson L, Janciauskiene S (2004) Concentration-dependent effects of native and polymerised alpha1-antitrypsin on primary human monocytes, in vitro. BMC Cell Biol 5:1–11.  https://doi.org/10.1186/1471-2121-5-11 CrossRefGoogle Scholar
  86. 86.
    Laurent S, Cockcroft J, Van Bortel L et al (2006) Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 27:2588–2605.  https://doi.org/10.1093/eurheartj/ehl254 CrossRefPubMedGoogle Scholar
  87. 87.
    Willum-Hansen T, Staessen JA, Torp-Pedersen C et al (2006) Prognostic value of aortic pulse wave velocity as index of arterial stiffness in the general population. Circulation 113:664–670.  https://doi.org/10.1161/CIRCULATIONAHA.105.579342 CrossRefPubMedGoogle Scholar
  88. 88.
    Rana A, Goyal N, Ahlawat A et al (2014) Mechanisms involved in attenuated cardio-protective role of ischemic preconditioning in metabolic disorders. Perfusion 30:94–105.  https://doi.org/10.1177/0267659114536760 CrossRefPubMedGoogle Scholar
  89. 89.
    Feng Y, Hu L, Xu Q et al (2015) Cytoprotective role of alpha-1 antitrypsin in vascular endothelial cell under hypoxia/reoxygenation condition. J Cardiovasc Pharmacol 66:96–107.  https://doi.org/10.1097/FJC.0000000000000250 CrossRefPubMedGoogle Scholar
  90. 90.
    Bhatt LK, Veeranjaneyulu A (2014) Enhancement of matrix metalloproteinase 2 and 9 inhibitory action of minocycline by aspirin: an approach to attenuate outcome of acute myocardial infarction in diabetes. Arch Med Res 45:203–209.  https://doi.org/10.1016/j.arcmed.2014.01.008 CrossRefPubMedGoogle Scholar
  91. 91.
    Gilutz H, Siegel Y, Paran E et al (1983) Alpha1-antitrypsin in acute myocardial infarction. Br Heart J 49:26–29.  https://doi.org/10.1136/hrt.49.1.26 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Duranton J, Bieth GJ (2003) Inhibition of proteinase-3 by alpha1-antitrypsin in vitro predicts very fast inhibition in vivo. Am J Resp Cell Mol Biol 29:57–61.  https://doi.org/10.1165/rcmb.2002-0258OC CrossRefGoogle Scholar
  93. 93.
    Banfi C, Brioschi M, Barcella S et al (2008) Oxidized proteins in plasma of patients with heart failure: role in endothelial damage. Eur J Heart Fail 10:244–251.  https://doi.org/10.1016/j.ejheart.2008.01.016 CrossRefPubMedGoogle Scholar
  94. 94.
    Stockley RA (2014) Alpha1-antitrypsin review. Clin Chest Med 35:39–50.  https://doi.org/10.1016/j.ccm.2013.10.001 CrossRefPubMedGoogle Scholar
  95. 95.
    Abouzaki N, Christopher S, Benjamin CT et al (2018) Inhibiting the inflammatory injury after myocardial ischemia reperfusion with plasma-derived alpha-1 antitrypsin: a post hoc analysis of the VCU-α1RT Study. J Cardiovasc Pharmacol 71:375–379.  https://doi.org/10.1097/FJC.0000000000000583 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Aoyama T, Chen M, Fujiwara H et al (2000) LOX-1 mediates lysophosphatidylcholine induced oxidized LDL uptake in smooth muscle cells. FEBS Lett 467:217–220.  https://doi.org/10.1016/s0014-5793(00)01154-6 CrossRefPubMedGoogle Scholar
  97. 97.
    Chen M, Kakutani M, Minami M et al (2000) Increased expression of lectin-like oxidized low density lipoprotein receptor-1 in initial atherosclerotic lesions of Watanabe heritable hyperlipidemic rabbits. Arterioscler Thromb Vasc Biol 20:1107–1115CrossRefGoogle Scholar
  98. 98.
    Hu C, Dandapat A, Sun L et al (2008) Regulation of TGFbeta1-mediated collagen formation by LOX-1: studies based on forced overexpression of TGFbeta1 in wild-type and lox-1 knock-out mouse cardiac fibroblasts. J Biol Chem 283:10226–10331.  https://doi.org/10.1074/jbc.M708820200 CrossRefPubMedGoogle Scholar
  99. 99.
    Kataoka H, Kume N, Miyamoto S et al (1999) Expression of lectin-like oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation 99:3110–3117.  https://doi.org/10.1161/01.cir.99.24.3110 CrossRefPubMedGoogle Scholar
  100. 100.
    Lubrano V, Del Turco S, Nicolini G et al (2008) Circulating levels of lectin-like oxidized low-density lipoprotein Receptor-1 are associated with inflammatory markers. Lipids 43:945–950.  https://doi.org/10.1007/s11745-008-3227-9 CrossRefPubMedGoogle Scholar
  101. 101.
    Takaya T, Wada H, Morimoto T et al (2010) Left ventricular expression of lectin-like oxidized low-density lipoprotein receptor-1 in failing hearts. Circ J 74:723–729.  https://doi.org/10.1253/circj.cj-09-0488 CrossRefPubMedGoogle Scholar
  102. 102.
    Yokoyama C, Aoyama T, Ido T et al (2016) Deletion of LOX-1 protects against heart failure induced by doxorubicin. PLoS ONE 11:e0154994.  https://doi.org/10.1371/journal.pone.0154994 CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Iwai-Kanai E, Hasegawa K, Sawamura T et al (2001) Activation of lectin-like oxidized low-density lipoprotein receptor-1 induces apoptosis in cultured neonatal rat cardiac myocytes. Circulation 104:2948–2954.  https://doi.org/10.1161/hc4901.100381 CrossRefPubMedGoogle Scholar
  104. 104.
    Cleutjens JP, Kandala JC, Guarda E et al (1995) Regulation of collagen degradation in the rat myocardium after infarction. J Mol Cell Cardiol 27:1281–1289CrossRefGoogle Scholar
  105. 105.
    Hu C, Chen J, Dandapat A et al (2008) LOX-1 abrogation reduces myocardial ischemia-reperfusion injury in mice. J Mol Cell Cardiol 44:76–83.  https://doi.org/10.1016/j.yjmcc.2007.10.009 CrossRefPubMedGoogle Scholar
  106. 106.
    Li D, Williams V, Liu L et al (2002) LOX-1 inhibition in myocardial ischemia-reperfusion injury: modulation of MMP-1 and inflammation. Am J Physiol Heart Circ Physiol 283:1795–1801.  https://doi.org/10.1152/ajpheart.00382.2002 CrossRefGoogle Scholar
  107. 107.
    Besli F, Gullulu S, Sag S et al (2016) The relationship between serum lectin-like oxidized LDL receptor-1 levels and systolic heart failure. Acta Cardiol 71:185–190.  https://doi.org/10.2143/AC.71.2.3141848 CrossRefPubMedGoogle Scholar
  108. 108.
    Kobayashi N, Yoshida K, Nakano S et al (2006) Cardioprotective mechanisms of eplerenone on cardiac performance and remodeling in failing rat hearts. Hypertension 47:671–679.  https://doi.org/10.1161/01.HYP.0000203148.42892.7a CrossRefPubMedGoogle Scholar
  109. 109.
    Schlüter KD, Wolf A, Weber M et al (2017) Oxidized low-density lipoprotein (oxLDL) affects load-free cell shortening of cardiomyocytes in a pro-protein convertase subtilisin/kexin 9 (PCSK9)-dependent way. Basic Res Cardiol 112:63.  https://doi.org/10.1007/s00395-017-0650-1 CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Hu C, Dandapat A, Sun L et al (2008) Modulation of angiotensin II-mediated hypertension and cardiac remodeling by lectin-like oxidized low-density lipoprotein receptor-1 deletion. Hypertension 52:556–562.  https://doi.org/10.1161/HYPERTENSIONAHA.108.115287 CrossRefPubMedGoogle Scholar
  111. 111.
    Chen J, Li D, Schaefer R et al (2006) Cross-talk between dyslipidemia and renin-angiotensin system and the role of LOX-1 and MAPK in atherogenesis studies with the combined use of rosuvastatin and candesartan. Atherosclerosis 184:295–301.  https://doi.org/10.1016/j.atherosclerosis.2005.04.016 CrossRefPubMedGoogle Scholar
  112. 112.
    Chen K, Chen J, Liu Y et al (2005) Adhesion molecule expression in fibroblasts: alteration in fibroblast biology after transfection with LOX-1 plasmids. Hypertension 46:622–627.  https://doi.org/10.1161/01.HYP.0000179045.95915.b0 CrossRefPubMedGoogle Scholar
  113. 113.
    Zhang X, Dong S, Jia Q et al (2019) The MicroRNA in ventricular remodeling: the miR-30 family. Biosci Rep 2:39.  https://doi.org/10.1042/BSR20190788 CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Fondazione G. Monasterio, CNR-Regione ToscanaPisaItaly
  2. 2.Institute of Clinical PhisiologyCNRPisaItaly

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