Cardiac-deleterious role of galectin-3 in chronic Angiotensin II-induced hypertension

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 311, Issue 5, 2016, Pages H1287-H1296

  González, Germán E ^a,b   Rhaleb, N E ^a,c   D’Ambrosio, Martin A ^a   Nakagawa, Pablo ^a   Liao, Tang Dong ^a   Peterson, Edward L ^a   Leung, Pablo ^a   Dai, Xiangguo ^a   Janic, Branislava ^a   Liu, Yun He ^a   Yang, Xiao Ping ^a   Carretero, Oscar A ^a  

^a HENRY FORD HOSPITAL   (United States)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin II; Fibrosis; Galectin 3; Hypertension; Inflammation; Interleukin 6; Macrophages

Indexed keywords

ANGIOTENSIN II; CD4 ANTIGEN; CHLORDANE; GALECTIN 3; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1; CD68 PROTEIN, MOUSE; CYTOKINE; DIFFERENTIATION ANTIGEN; ICAM1 PROTEIN, MOUSE; LEUKOCYTE ANTIGEN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE DELETION; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; HEREDITARY HYPERTENSION; INNATE IMMUNITY; LUNG WEIGHT; MALE; MOUSE; NONHUMAN; PLETHYSMOGRAPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SPLENIC T CELL; SYSTOLIC BLOOD PRESSURE; WESTERN BLOTTING; ANIMAL; BLOOD PRESSURE; C57BL MOUSE; CARDIAC MUSCLE; CARDIOMEGALY; CHEMICALLY INDUCED; COMPLICATION; DIAGNOSTIC IMAGING; DISEASE MODEL; ECHOCARDIOGRAPHY; FIBROSIS; GENETICS; HEART LEFT VENTRICLE FUNCTION; HYPERTENSION; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANGIOTENSIN II; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BLOOD PRESSURE; BLOTTING, WESTERN; CARDIOMEGALY; CYTOKINES; DISEASE MODELS, ANIMAL; ECHOCARDIOGRAPHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROSIS; FLOW CYTOMETRY; GALECTIN 3; HYPERTENSION; INTERCELLULAR ADHESION MOLECULE-1; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; PLETHYSMOGRAPHY; T-LYMPHOCYTES, REGULATORY; VASCULAR CELL ADHESION MOLECULE-1; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT;

EID: 84994627883     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00096.2016     Document Type: Article

References (52)

1. Arangalage D, Nguyen V, Robert T, Melissopoulou M, Mathieu T, Estellat C, Codogno I, Huart V, Duval X, Cimadevilla C, Vahanian A, Dehoux M, Messika-Zeitoun D. Determinants and prognostic value of galectin-3 in patients with aortic valve stenosis. Heart 102: 862–868, 2016.
2. Barhoumi T, Kasal DA, Li MW, Shbat L, Laurant P, Neves MF, Paradis P, Schiffrin EL. T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 57: 469–476, 2011.
3. Bozcali E, Polat V, Aciksari G, Opan S, Bayrak I˙ H, Paker N, Karakaya O. Serum concentrations of galectin-3 in patients with cardiac syndrome X. Atherosclerosis 237: 259–263, 2014.
4. Brands MW, Banes-Berceli AK, Inscho EW, Al-Azawi H, Allen AJ, Labazi H. Interleukin 6 knockout prevents angiotensin II hypertension: role of renal vasoconstriction and Janus kinase 2/signal transducer and activator of transcription 3 activation. Hypertension 56: 879–884, 2010.
5. Calvier L, Miana M, Reboul P, Cachofeiro V, Martinez-Martinez E, de Boer RA, Poirier F, Lacolley P, Zannad F, Rossignol P, Lopez-Andres N. Galectin-3 mediates aldosterone-induced vascular fibrosis. Arterioscler Thromb Vasc Biol 33: 67–75, 2013.
6. Chen C, Duckworth CA, Zhao Q, Pritchard DM, Rhodes JM, Yu LG. Increased circulation of galectin-3 in cancer induces secretion of metastasis- promoting cytokines from blood vascular endothelium. Clin Cancer Res 19: 1693–1704, 2013.
7. Cingolani OH, Yang XP, Liu YH, Villanueva M, Rhaleb NE, Carretero OA. Reduction of cardiac fibrosis decreases systolic performance without affecting diastolic function in hypertensive rats. Hypertension 43: 1067–1073, 2004.
8. Cummings RD, Liu FT. Galectins. In: Essentials of Glycobiology, edited by Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2009, p. 475–488.
9. de Boer RA, Lok DJ, Jaarsma T, van der Meer P, Voors AA, Hillege HL, van Veldhuisen DJ. Predictive value of plasma galectin-3 levels in heart failure with reduced and preserved ejection fraction. Ann Med 43: 60–68, 2011.
10. de Boer RA, Yu L, van Veldhuisen DJ. Galectin-3 in cardiac remodeling and heart failure. Curr Heart Fail Rep 7: 1–8, 2010.
11. Falcone C, Lucibello S, Mazzucchelli I, Bozzini S, D’Angelo A, Schirinzi S, Totaro R, Falcone R, Bondesan M, Pelissero G. Galectin-3 plasma levels and coronary artery disease: a new possible biomarker of acute coronary syndrome. Int J Immunopathol Pharmacol 24: 905–913, 2011.
12. Fenster BE, Lasalvia L, Schroeder JD, Smyser J, Silveira LJ, Buckner JK, Brown KK. Galectin-3 levels are associated with right ventricular functional and morphologic changes in pulmonary arterial hypertension. Heart Vessels 31: 939–946, 2016.
13. Fermino ML, Dias FC, Lopes CD, Souza MA, Cruz AK, Liu FT, Chammas R, Roque-Barreira MC, Rabinovich GA, Bernardes ES. Galectin-3 negatively regulates the frequency and function of CD4_CD25_Foxp3_ regulatory T cells and influences the course of Leishmania major infection. Eur J Immunol 43: 1806–1817, 2013.
14. Gonzalez GE, Cassaglia P, Noli Truant S, Fernandez MM, Wilensky L, Volberg V, Malchiodi EL, Morales C, Gelpi RJ. Galectin-3 is essential for early wound healing and ventricular remodeling after myocardial infarction in mice. Int J Cardiol 176: 1423–1425, 2014.
15. Gonzalez GE, Rhaleb NE, D’Ambrosio MA, Nakagawa P, Liu Y, Leung P, Dai X, Yang XP, Peterson EL, Carretero OA. Deletion of interleukin-6 prevents cardiac inflammation, fibrosis and dysfunction without affecting blood pressure in angiotensin II-high salt-induced hypertension. J Hypertens 33: 144–152, 2015.
16. Gonzalez GE, Rhaleb NE, Nakagawa P, Liao TD, Liu Y, Leung P, Dai X, Yang XP, Carretero OA. N-acetyl-seryl-aspartyl-lysyl-proline reduces cardiac collagen cross-linking and inflammation in angiotensin II-induced hypertensive rats. Clin Sci (Lond) 126: 85–94, 2014.
17. Greene AS, Rieder MJ. Measurement of vascular density. Methods Mol Med 51: 489–496, 2001.
18. Hansen-Smith FM, Watson L, Lu DY, Goldstein I. Griffonia simplicifolia I: fluorescent tracer for microcirculatory vessels in nonperfused thin muscles and sectioned muscle. Microvasc Res 36: 199–215, 1988.
19. Henderson NC, MacKinnon AC, Farnworth SL, Kipari T, Haslett C, Iredale JP, Liu FT, Hughes J, Sethi T. Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. Am J Pathol 172: 288–298, 2008.
20. Hsu DK, Yang RY, Pan Z, Yu L, Salomon DR, Fung-Leung WP, Liu FT. Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am J Pathol 156: 1073–1083, 2000.
21. Jiang HR, Al RZ, Mensah-Brown E, Shahin A, Xu D, Goodyear CS, Fukada SY, Liu FT, Liew FY, Lukic ML. Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J Immunol 182: 1167–1173, 2009.
22. Kim H, Lee J, Hyun JW, Park JW, Joo HG, Shin T. Expression and immunohistochemical localization of galectin-3 in various mouse tissues. Cell Biol Int 31: 655–662, 2007.
23. Kvakan H, Kleinewietfeld M, Qadri F, Park JK, Fischer R, Schwarz I, Rahn HP, Plehm R, Wellner M, Elitok S, Gratze P, Dechend R, Luft FC, Muller DN. Regulatory T cells ameliorate angiotensin II-induced cardiac damage. Circulation 119: 2904–2912, 2009.
24. Lee DL, Sturgis LC, Labazi H, Osborne JB Jr, Fleming C, Pollock JS, Manhiani M, Imig JD, Brands MW. Angiotensin II hypertension is attenuated in interleukin-6 knockout mice. Am J Physiol Heart Circ Physiol 290: H935–H940, 2006.
25. Liao TD, Yang XP, D’Ambrosio M, Zhang Y, Rhaleb NE, Carretero OA. N-acetyl-seryl-aspartyl-lysyl-proline attenuates renal injury and dysfunction in hypertensive rats with reduced renal mass: Council for High Blood Pressure Research. Hypertension 55: 459–467, 2010.
26. Liu YH, D’Ambrosio M, Liao TD, Peng H, Rhaleb NE, Sharma U, Andre S, Gabius HJ, Carretero OA. N-acetyl-seryl-aspartyl-lysyl-proline prevents cardiac remodeling and dysfunction induced by galectin-3, a mammalian adhesion/growth-regulatory lectin. Am J Physiol Heart Circ Physiol 296: H404–H412, 2009.
27. Liu YH, D’Ambrosio MA, Liao TD, Peng HM, Rhaleb NE, Sharma U, Carretero OA. Ac-SDKP prevents cardiac fibrosis and dysfunction induced by galectin-3: role of TGF-β/Smad3 signaling pathway (Abstract). FASEB J 23: 362, 2009.
28. Liu YH, Xu J, Yang XP, Yang F, Shesely E, Carretero OA. Effect of ACE inhibitors and angiotensin II type 1 receptor antagonists on endothelial NO synthase knockout mice with heart failure. Hypertension 39: 375–381, 2002.
29. Liu YH, Yang XP, Sharov VG, Nass O, Sabbah HN, Peterson E, Carretero OA. Effects of angiotensin-converting enzyme inhibitors and angiotensin II type 1 receptor antagonists in rats with heart failure. Role of kinins and angiotensin II type 2 receptors. J Clin Invest 99: 1926–1935, 1997.
30. Lok DJ, van der Meer P, de la Porte PW, Lipsic E, Van Wijngaarden J, Hillege HL, van Veldhuisen DJ. Prognostic value of galectin-3, a novel marker of fibrosis, in patients with chronic heart failure: data from the DEAL-HF study. Clin Res Cardiol 99: 323–328, 2010.
31. Martínez-Martínez E, Calvier L, Fernández-Celis A, Rousseau E, Jurado-López R, Rossoni LV, Jaisser F, Zannad F, Rossignol P, Cachofeiro V, López-Andrés N. Galectin-3 blockade inhibits cardiac inflammation and fibrosis in experimental hyperaldosteronism and hypertension. Hypertension 66: 767–775, 2015.
32. Matrougui K, Zakaria AE, Kassan M, Choi S, Nair D, Gonzalez- Villalobos RA, Chentoufi AA, Kadowitz P, Belmadani S, Partyka M. Natural regulatory T cells control coronary arteriolar endothelial dysfunction in hypertensive mice. Am J Pathol 178: 434–441, 2011.
33. Mayr A, Klug G, Mair J, Streil K, Harrasser B, Feistritzer HJ, Jaschke W, Schocke M, Pachinger O, Metzler B. Galectin-3: relation to infarct scar and left ventricular function after myocardial infarction. Int J Cardiol 163: 335–337, 2013.
34. Melendez GC, McLarty JL, Levick SP, Du Y, Janicki JS, Brower GL. Interleukin 6 mediates myocardial fibrosis, concentric hypertrophy, and diastolic dysfunction in rats. Hypertension 56: 225–231, 2010.
35. Nakagawa P, Liu Y, Liao TD, Chen X, Gonzalez GE, Bobbitt KR, Smolarek D, Peterson EL, Kedl R, Yang XP, Rhaleb NE, Carretero OA. Treatment with N-acetyl-seryl-aspartyl-lysyl-proline prevents experimental autoimmune myocarditis in rats. Am J Physiol Heart Circ Physiol 303: H1114–H1127, 2012.
36. Peeters AC, Netea MG, Janssen MC, Kullberg BJ, van der Meer JW, Thien T. Pro-inflammatory cytokines in patients with essential hypertension. Eur J Clin Invest 31: 31–36, 2001.
37. Peng H, Yang XP, Carretero OA, Nakagawa P, D’Ambrosio M, Leung P, Xu J, Peterson EL, Gonzalez GE, Harding P, Rhaleb NE. Angiotensin II-induced dilated cardiomyopathy in Balb/c but not C57BL/6J mice. Exp Physiol 96: 756–764, 2011.
38. Rabinovich GA, Toscano MA. Turning “sweet” on immunity: galectinglycan interactions in immune tolerance and inflammation. Nat Rev Immunol 9: 338–352, 2009.
39. Rakusan K. Changes in the myocardial oxygen tension caused by changes in several oxygen determinants, with special consideration of the diffusion distance. In: Oxygen in the Heart Muscle. Springfield, IL: Thomas, 1971, p. 66–71.
40. Sahn DJ, DeMaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58: 1072–1083, 1978.
41. Sano H, Hsu DK, Apgar JR, Yu L, Sharma BB, Kuwabara I, Izui S, Liu FT. Critical role of galectin-3 in phagocytosis by macrophages. J Clin Invest 112: 389–397, 2003.
42. Sharma U, Rhaleb NE, Pokharel S, Harding P, Rasoul S, Peng H, Carretero OA. Novel anti-inflammatory mechanisms of N-acetyl-Ser- Asp-Lys-Pro in hypertension-induced target organ damage. Am J Physiol Heart Circ Physiol 294: H1226–H1232, 2008.
43. Sharma UC, Pokharel S, van Brakel TJ, van Berlo JH, Cleutjens JP, Schroen B, Andr S, Crijns HJ, Gabius HJ, Maessen J, Pinto YM. Galectin-3 marks activated macrophages in failure-prone hypertrophied hearts and contributes to cardiac dysfunction. Circulation 110: 3121–3128, 2004.
44. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11: 762–774, 2011.
45. Sun Y, Carretero OA, Xu J, Rhaleb NE, Yang JJ, Pagano PJ, Yang XP. Deletion of inducible nitric oxide synthase provides cardioprotection in mice with 2-kidney, 1-clip hypertension. Hypertension 53: 49–56, 2009.
46. Tummala PE, Chen XL, Sundell CL, Laursen JB, Hammes CP, Alexander RW, Harrison DG, Medford RM. Angiotensin II induces vascular cell adhesion molecule expression in rat vasculature. A potential link between the renin-angiotensin system and atherosclerosis. Circulation 100: 1223–1229, 1999.
47. Vergaro G, Del Franco A, Giannoni A, Prontera C, Ripoli A, Barison A, Masci PG, Aquaro GD, Cohen Solal A, Padeletti L, Passino C, Emdin M. Galectin-3 and myocardial fibrosis in nonischemic dilated cardiomyopathy. Int J Cardiol 184: 96–100, 2015.
48. Vergaro G, Prud’homme M, Fazal L, Merval R, Passino C, Emdin M, Samuel JL, Cohen Solal A, Delcayre C. Inhibition of galectin-3 pathway prevents isoproterenol-induced left ventricular dysfunction and fibrosis in mice. Hypertension 67: 606–612, 2016.
49. Wang D, Carretero OA, Yang XY, Rhaleb NE, Liu YH, Liao TD, Yang XP. N-acetyl-seryl-aspartyl-lysyl-proline stimulates angiogenesis in vitro and in vivo. Am J Physiol Heart Circ Physiol 287: H2099–H2105, 2004.
50. Yang XP, Liu YH, Rhaleb NE, Kurihara N, Kim HE, Carretero OA. Echocardiographic assessment of cardiac function in conscious and anesthetized mice. Am J Physiol Heart Circ Physiol 277: H1967–H1974, 1999.
51. Yu L, Ruifrok WP, Meissner M, Bos EM, van Goor H, Sanjabi B, van der Harst P, Pitt B, Goldstein IJ, Koerts JA, van Veldhuisen DJ, Bank RA, van Gilst WH, Sillje HH, de Boer RA. Genetic and pharmacological inhibition of galectin-3 prevents cardiac remodeling by interfering with myocardial fibrogenesis. Circ Heart Fail 6: 107–117, 2013.
52. Zhang W, Wang W, Yu H, Zhang Y, Dai Y, Ning C, Tao L, Sun H, Kellems RE, Blackburn MR, Xia Y. Interleukin 6 underlies angiotensin II-induced hypertension and chronic renal damage. Hypertension 59: 136–144, 2012.