Pharmacological inhibition of galectin-3 protects against hypertensive nephropathy

American Journal of Physiology - Renal Physiology

Volumn 308, Issue 5, 2015, Pages F500-F509

  Frenay, Anne Roos S ^a   Yu, Lili ^a,b   van der Velde, A Rogier ^a   Vreeswijk Baudoin, Inge ^a   López Andrés, Natalia ^c   van Goor, Harry ^a   Silljé, Herman H ^a   Ruifrok, Willem P ^a   de Boer, Rudolf A ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b HARBIN MEDICAL UNIVERSITY   (China)

^c Red de Investigación en Servicios de Salud en Enfermedades Crónicas   (Spain)

Author keywords

Chronic kidney disease; Fibrosis; Galectin 3; Hypertension; Renin angiotensin system; TGR(mREN)27

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CREATININE; CYTOKINE; DESMIN; GALECTIN 3; KIDNEY INJURY MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN; N ACETYLLACTOSAMINE SYNTHASE; AMINOSUGAR; N-ACETYLLACTOSAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CYTOKINE RELEASE; EXTRACELLULAR MATRIX; GLOMERULOSCLEROSIS; HEART FUNCTION; HEMODYNAMICS; KIDNEY INJURY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEINURIA; RAT; RENOVASCULAR HYPERTENSION; SYSTOLIC BLOOD PRESSURE; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPLICATION; DRUG SCREENING; HYPERTENSION; KIDNEY DISEASES; SPRAGUE DAWLEY RAT;

AMINO SUGARS; ANIMALS; DRUG EVALUATION, PRECLINICAL; GALECTIN 3; HYPERTENSION; KIDNEY DISEASES; MALE; RATS, SPRAGUE-DAWLEY;

EID: 84924044033     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00461.2014     Document Type: Article

References (58)

1. Ahmad N, Gabius HJ, Sabesan S, Oscarson S, Brewer CF. Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin- 3, and the carbohydrate recognition domain of galectin-3. Glycobiology 14: 817-825, 2004.
2. Becker GJ, Hewitson TD. The role of tubulointerstitial injury in chronic renal failure. Curr Opin Nephrol Hypertens 9: 133-138, 2000.
3. Blixt O, Collins BE, van den Nieuwenhof IM, Crocker PR, Paulson JC. Sialoside specificity of the siglec family assessed using novel multivalent probes: identification of potent inhibitors of myelin-associated glycoprotein. J Biol Chem 278: 31007-31019, 2003.
4. Bolbrinker J, Markovic S, Wehland M, Melenhorst WB, van Goor H, Kreutz R. Expression and response to angiotensin-converting enzyme inhibition of matrix metalloproteinases 2 and 9 in renal glomerular damage in young transgenic rats with renin-dependent hypertension. J Pharmacol Exp Ther 316: 8-16, 2006.
5. Brouwers FP, de Boer RA, van der Harst P, Struck J, de Jong PE, de Zeeuw D, Gans RO, Gansevoort RT, Hillege HL, van Gilst WH, Bakker SJ. Influence of age on the prognostic value of mid-regional pro-adrenomedullin in the general population. Heart 98: 1348-1353, 2012.
6. Carome MA, Striker LJ, Peten EP, Moore J, Yang CW, Stetler- Stevenson WG, Striker GE. Human glomeruli express TIMP-1 mRNA and TIMP-2 protein and mRNA. Am J Physiol Renal Fluid Electrolyte Physiol 264: F923-F929, 1993.
7. Dang Z, MacKinnon A, Marson LP, Sethi T. Tubular atrophy and interstitial fibrosis after renal transplantation is dependent on galectin-3. Transplantation 93: 477-484, 2012.
8. Demotte N, Wieers G, Van Der Smissen P, Moser M, Schmidt C, Thielemans K, Squifflet JL, Weynand B, Carrasco J, Lurquin C, Courtoy PJ, van der Bruggen P. A galectin-3 ligand corrects the impaired function of human CD4 and CD8 tumor-infiltrating lymphocytes and favors tumor rejection in mice. Cancer Res 70: 7476-7488, 2010.
9. El-Nahas AM. Plasticity of kidney cells: role in kidney remodeling and scarring. Kidney Int 64: 1553-1563, 2003.
10. Gestwicki JE, Cairo CW, Strong LE, Oetjen KA, Kiessling LL. Influencing receptor-ligand binding mechanisms with multivalent ligand architecture. J Am Chem Soc 124: 14922-14933, 2002.
11. Goletz S, Hanisch FG, Karsten U. Novel αGalNAc containing glycans on cytokeratins are recognized invitro by galectins with type II carbohydrate recognition domains. J Cell Sci 110: 1585-1596, 1997.
12. Granger JP. An emerging role for inflammatory cytokines in hypertension. Am J Physiol Heart Circ Physiol 290: H923-H924, 2006.
13. Hall JE, Crook ED, Jones DW, Wofford MR, Dubbert PM. Mechanisms of obesity-associated cardiovascular and renal disease. Am J Med Sci 324: 127-137, 2002.
14. Hamming I, Navis G, Kocks MJ, van Goor H. ACE inhibition has adverse renal effects during dietary sodium restriction in proteinuric and healthy rats. J Pathol 209: 129-139, 2006.
15. Hartner A, Klanke B, Cordasic N, Amann K, Schmieder RE, Veelken R, Hilgers KF. Statin treatment reduces glomerular inflammation and podocyte damage in rat deoxycorticosterone-acetate-salt hypertension. J Hypertens 27: 376-385, 2009.
16. 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.
17. Hillege HL, Girbes AR, de Kam PJ, Boomsma F, de Zeeuw D, Charlesworth A, Hampton JR, van Veldhuisen DJ. Renal function, neurohormonal activation, and survival in patients with chronic heart failure. Circulation 102: 203-210, 2000.
18. Iacobini C, Menini S, Oddi G, Ricci C, Amadio L, Pricci F, Olivieri A, Sorcini M, Di Mario U, Pesce C, Pugliese G. Galectin-3/AGE-receptor 3 knockout mice show accelerated AGE-induced glomerular injury: evidence for a protective role of galectin-3 as an AGE receptor. FASEB J 18: 1773-1775, 2004.
19. Iacobini C, Oddi G, Menini S, Amadio L, Ricci C, Di Pippo C, Sorcini M, Pricci F, Pugliese F, Pugliese G. Development of age-dependent glomerular lesions in galectin-3/AGE-receptor-3 knockout mice. Am J Physiol Renal Physiol 289: F611-F621, 2005.
20. Ibsen H, Wachtell K, Olsen MH, Borch-Johnsen K, Lindholm LH, Mogensen CE, Dahlof B. Albuminuria and cardiovascular risk in hypertensive patients with left ventricular hypertrophy: the LIFE Study. Kidney Int Suppl: S56-S58, 2004.
21. Iimura O, Takahashi H, Yashiro T, Madoiwa S, Sakata Y, Asano Y, Kusano E. Effect of ureteral obstruction on matrix metalloproteinase-2 in rat renal cortex. Clin Exp Nephrol 8: 223-229, 2004.
22. Jafar TH, Stark PC, Schmid CH, Landa M, Maschio G, de Jong PE, de Zeeuw D, Shahinfar S, Toto R, Levey AS; AIPRD Study Group. Progression of chronic kidney disease: the role of blood pressure control, proteinuria, and angiotensin-converting enzyme inhibition: a patient-level meta-analysis. Ann Intern Med 139: 244-252, 2003.
23. Klahr S, Levey AS, Beck GJ, Caggiula AW, Hunsicker L, Kusek JW, Striker G. The effects of dietary protein restriction and blood-pressure control on the progression of chronic renal disease. Modification of Diet in Renal Disease Study Group. N Engl J Med 330: 877-884, 1994.
24. Kolatsi-Joannou M, Price KL, Winyard PJ, Long DA. Modified citrus pectin reduces galectin-3 expression and disease severity in experimental acute kidney injury. PLos One 6: e18683, 2011.
25. Kuipers I, van der Harst P, Kuipers F, van Genne L, Goris M, Lehtonen JY, van Veldhuisen DJ, van Gilst WH, de Boer RA. Activation of liver X receptor-α reduces activation of the renal and cardiac renin-angiotensin-aldosterone system. Lab Invest 90: 630-636, 2010.
26. Liu HY, Huang ZL, Yang GH, Lu WQ, Yu NR. Inhibitory effect of modified citrus pectin on liver metastases in a mouse colon cancer model. World J Gastroenterol 14: 7386-7391, 2008.
27. 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.
28. Lopez-Andres N, Rossignol P, Iraqi W, Fay R, Nuee J, Ghio S, Cleland JG, Zannad F, Lacolley P. Association of galectin-3 and fibrosis markers with long-term cardiovascular outcomes in patients with heart failure, left ventricular dysfunction, and dyssynchrony: insights from the CARE-HF (Cardiac Resynchronization in Heart Failure) trial. Eur J Heart Fail 14: 74-81, 2012.
29. Lu B, Tigchelaar W, Ruifrok WP, van Gilst WH, de Boer RA, Sillje HH. DHRS7c, a novel cardiomyocyte-expressed gene that is downregulated by adrenergic stimulation and in heart failure. Eur J Heart Fail 14: 5-13, 2012.
30. Martinez-Martinez E, Jurado-Lopez R, Valero-Munoz M, Bartolome MV, Ballesteros S, Luaces M, Briones AM, Lopez-Andres N, Miana M, Cachofeiro V. Leptin induces cardiac fibrosis through galectin-3, mTOR and oxidative stress: potential role in obesity. J Hypertens 32: 1104-1114, 2014.
31. Meguid El Nahas A, Bello AK. Chronic kidney disease: the global challenge. Lancet 365: 331-340, 2005.
32. Mifsud S, Kelly DJ, Qi W, Zhang Y, Pollock CA, Wilkinson-Berka JL, Gilbert RE. Intervention with tranilast attenuates renal pathology and albuminuria in advanced experimental diabetic nephropathy. Nephron Physiol 95: p83-91, 2003.
33. Muntner P, Hamm LL, Kusek JW, Chen J, Whelton PK, He J. The prevalence of nontraditional risk factors for coronary heart disease in patients with chronic kidney disease. Ann Intern Med 140: 9-17, 2004.
34. Ochieng J, Furtak V, Lukyanov P. Extracellular functions of galectin-3. Glycoconj J 19: 527-535, 2004.
35. Okamura DM, Pasichnyk K, Lopez-Guisa JM, Collins S, Hsu DK, Liu FT, Eddy AA. Galectin-3 preserves renal tubules and modulates extracellular matrix remodeling in progressive fibrosis. Am J Physiol Renal Physiol 300: F245-F253, 2011.
36. O'Seaghdha CM, Hwang SJ, Ho JE, Vasan RS, Levy D, Fox CS. Elevated galectin-3 precedes the development of CKD. J Am Soc Nephrol 24: 1470-1477, 2013.
37. Pacher P, Nagayama T, Mukhopadhyay P, Batkai S, Kass DA. Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat Protoc 3: 1422-1434, 2008.
38. Pang J, Rhodes DH, Pini M, Akasheh RT, Castellanos KJ, Cabay RJ, Cooper D, Perretti M, Fantuzzi G. Increased adiposity, dysregulated glucose metabolism and systemic inflammation in galectin-3 KO mice. PLos One 8: e57915, 2013.
39. Park JK, Theuer S, Kirsch T, Lindschau C, Klinge U, Heuser A, Plehm R, Todiras M, Carmeliet P, Haller H, Luft FC, Muller DN, Fiebeler A. Growth arrest specific protein 6 participates in DOCAinduced target-organ damage. Hypertension 54: 359-364, 2009.
40. Pejnovic N, Pantic J, Jovanovic I, Radosavljevic G, Milovanovic M, Nikolic I, Zdravkovic N, Djukic A, Arsenijevic N, Lukic M. Galectin-3 deficiency accelerates high-fat diet induced obesity and amplifies inflammation in adipose tissue and pancreatic islets. Diabetes 62: 1932-1944, 2013.
41. Peterson JC, Adler S, Burkart JM, Greene T, Hebert LA, Hunsicker LG, King AJ, Klahr S, Massry SG, Seifter JL. Blood pressure control, proteinuria, and the progression of renal disease. The Modification of Diet in Renal Disease Study. Ann Intern Med 123: 754-762, 1995.
42. Rabinovich GA. Galectins: an evolutionarily conserved family of animal lectins with multifunctional properties; a trip from the gene to clinical therapy. Cell Death Differ 6: 711-721, 1999.
43. Ruifrok WP, Qian C, Sillje HH, van Goor H, van Veldhuisen DJ, van Gilst WH, de Boer RA. Heart failure-associated anemia: bone marrow dysfunction and response to erythropoietin. J Mol Med 89: 377-387, 2011.
44. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-β1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 112: 1486-1494, 2003.
45. Sharma AK, Mauer SM, Kim Y, Michael AF. Altered expression of matrix metalloproteinase-2, TIMP, and TIMP-2 in obstructive nephropathy. J Lab Clin Med 125: 754-761, 1995.
46. Sharma K, Ziyadeh FN. The emerging role of transforming growth factor-beta in kidney diseases. Am J Physiol Renal Fluid Electrolyte Physiol 266: F829-F842, 1994.
47. Sharma UC, Pokharel S, van Brakel TJ, van Berlo JH, Cleutjens JP, Schroen B, Andre 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.
48. Shlipak MG, Fried LF, Crump C, Bleyer AJ, Manolio TA, Tracy RP, Furberg CD, Psaty BM. Elevations of inflammatory and procoagulant biomarkers in elderly persons with renal insufficiency. Circulation 107: 87-92, 2003.
49. Smilde TD, Damman K, van der Harst P, Navis G, Westenbrink BD, Voors AA, Boomsma F, van Veldhuisen DJ, Hillege HL. Differential associations between renal function and "modifiable" risk factors in patients with chronic heart failure. Clin Res Cardiol 98: 121-129, 2009.
50. Smith GL, Lichtman JH, Bracken MB, Shlipak MG, Phillips CO, DiCapua P, Krumholz HM. Renal impairment and outcomes in heart failure: systematic review and meta-analysis. J Am Coll Cardiol 47: 1987-1996, 2006.
51. Taniguchi T, Asano Y, Akamata K, Noda S, Masui Y, Yamada D, Takahashi T, Ichimura Y, Toyama T, Tamaki Z, Tada Y, Sugaya M, Kadono T, Sato S. Serum levels of galectin-3: possible association with fibrosis, aberrant angiogenesis, and immune activation in patients with systemic sclerosis. J Rheumatol 39: 539-544, 2012.
52. Tejler J, Leffler H, Nilsson UJ. Synthesis of O-galactosyl aldoximes as potent LacNAc-mimetic galectin-3 inhibitors. Bioorg Med Chem Lett 15: 2343-2345, 2005.
53. Ulrich P, Cerami A. Protein glycation, diabetes, and aging. Recent Prog Horm Res 56: 1-21, 2001.
54. Witte K, Schnecko A, Schmidt T, Voll C, Kranzlin B, Lemmer B. Cardiovascular risk, renal hypertensive damage, and effects of amlodipine treatment in transgenic TGR(mREN2)27 rats. Gen Pharmacol 33: 423- 430, 1999.
55. Yang RY, Hsu DK, Liu FT. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci USA 93: 6737-6742, 1996.
56. Yang RY, Rabinovich GA, Liu FT. Galectins: structure, function and therapeutic potential. Expert Rev Mol Med 10: e17, 2008.
57. 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.
58. Zuberi RI, Hsu DK, Kalayci O, Chen HY, Sheldon HK, Yu L, Apgar JR, Kawakami T, Lilly CM, Liu FT. Critical role for galectin-3 in airway inflammation and bronchial hyperresponsiveness in a murine model of asthma. Am J Pathol 165: 2045-2053, 2004.