Dietary ω-3 fatty acids protect against vasculopathy in a transgenic mouse model of sickle cell disease

Haematologica

Volumn 100, Issue 7, 2015, Pages 870-880

  Kalish, Brian T ^a   Matte, Alessandro ^b   Andolfo, Immacolata ^c   Iolascon, Achille ^c   Weinberg, Olga ^a   Ghigo, Alessandra ^d   Cimino, James ^d   Siciliano, Angela ^b   Hirsch, Emilio ^d   Federti, Enrica ^b   Puder, Mark ^a   Brugnara, Carlo ^a   De Franceschi, Lucia ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF VERONA   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTATE AMINOTRANSFERASE; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOKINE; ENDOTHELIN 1; HEME OXYGENASE 1; OMEGA 3 FATTY ACID; PEROXIREDOXIN 2; VASCULAR CELL ADHESION MOLECULE 1; ANTIINFLAMMATORY AGENT; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIETARY INTAKE; DISEASE ASSOCIATION; DOWN REGULATION; ECHOCARDIOGRAPHY; ENDOTHELIAL DYSFUNCTION; ERYTHROCYTE MEMBRANE; HEART LEFT VENTRICLE OUTFLOW TRACT; HEMATOLOGICAL PARAMETERS; HISTOLOGY; HYPOXIA; IMMUNOBLOTTING; LIPID COMPOSITION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REOXYGENATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SICKLE CELL ANEMIA; UPREGULATION; VASCULAR DISEASE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BLOOD VESSEL; DIET THERAPY; DIETARY SUPPLEMENT; DISEASE MODEL; DRUG EFFECTS; HUMAN; METABOLISM; NEUTROPHIL; PATHOLOGY; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM;

ANEMIA, SICKLE CELL; ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD VESSELS; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; ENDOTHELIUM, VASCULAR; ERYTHROCYTE MEMBRANE; FATTY ACIDS, OMEGA-3; HUMANS; HYPOXIA; MICE; MICE, TRANSGENIC; NEUTROPHILS; OXYGEN;

EID: 84936098682     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2015.124586     Document Type: Article

References (61)

1. Bunn HF. Pathogenesis and treatment of sickle cell disease. N Engl J Med. 1997;337(11):762-769.
2. Sparkenbaugh E, Pawlinski R. Interplay between coagulation and vascular inflammation in sickle cell disease. Br J Haematol. 2013;162(1):3-14.
3. De Franceschi L, Cappellini MD, Olivieri O. Thrombosis and sickle cell disease. Semin Thromb Hemost. 2011;37(3):226-236.
4. Hebbel RP, Vercellotti G, Nath KA. A systems biology consideration of the vasculopathy of sickle cell anemia: the need for multi-modality chemo-prophylaxsis. Cardiovasc Hematol Disord Drug Targets. 2009;9(4):271-292.
5. Massaro M, Scoditti E, Carluccio MA, De Caterina R. Basic mechanisms behind the effects of n-3 fatty acids on cardiovascular disease. Prostaglandins Leukot Essent Fatty Acids. 2008;79(3-5):109-115.
6. Calder PC. Omega-3 fatty acids and inflammatory processes. Nutrients. 2010;2(3):355-374.
7. Rangel-Huerta OD, Aguilera CM, Mesa MD, Gil A. Omega-3 long-chain polyunsaturated fatty acids supplementation on inflammatory biomakers: a systematic review of randomised clinical trials. Br J Nutr. 2012;107 (Suppl 2):S159-170.
8. Wachira JK, Larson MK, Harris WS. n-3 Fatty acids affect haemostasis but do not increase the risk of bleeding: clinical observations and mechanistic insights. Br J Nutr. 2014;111(9):1652-1662.
9. Chen J, Shearer GC, Chen Q, et al. Omega-3 fatty acids prevent pressure overloadinduced cardiac fibrosis through activation of cyclic GMP/protein kinase G signaling in cardiac fibroblasts. Circulation. 2011;123(6):584-593.
10. Ren H, Ghebremeskel K, Okpala I, et al. Abnormality of erythrocyte membrane n-3 long chain polyunsaturated fatty acids in sickle cell haemoglobin C (HbSC) disease is not as remarkable as in sickle cell anaemia (HbSS). Prostaglandins Leukot Essent Fatty Acids. 2006;74(1):1-6.
11. Ren H, Obike I, Okpala I, et al. Steady-state haemoglobin level in sickle cell anaemia increases with an increase in erythrocyte membrane n-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2005;72(6):415-421.
12. Okpala I, Ibegbulam O, Duru A, et al. Pilot study of omega-3 fatty acid supplements in sickle cell disease. APMIS. 2011;119(7):442-448.
13. Daak AA, Ghebremeskel K, Hassan Z, et al. Effect of omega-3 (n-3) fatty acid supplementation in patients with sickle cell anemia: randomized, double-blind, placebocontrolled trial. Am J Clin Nutr. 2013;97(1):37-44.
14. Tomer A, Kasey S, Connor WE, et al. Reduction of pain episodes and prothrombotic activity in sickle cell disease by dietary n-3 fatty acids. Thromb Haemost. 2001; 85(6):966-974.
15. Simopoulos AP. Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr. 1991;54(3):438-463.
16. Vinchi F, De Franceschi L, Ghigo A, et al. Hemopexin therapy improves cardiovascular function by preventing heme-induced endothelial toxicity in mouse models of hemolytic diseases. Circulation. 2013;127(12):1317-1329.
17. Wu LC, Sun CW, Ryan TM, et al. Correction of sickle cell disease by homologous recombination in embryonic stem cells. Blood. 2006;108(4):1183-1188.
18. Reeves PG, Nielsen FH, Fahey GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993;123(11):1939-1951.
19. de Franceschi L, Baron A, Scarpa A, et al. Inhaled nitric oxide protects transgenic SAD mice from sickle cell disease-specific lung injury induced by hypoxia/reoxygenation. Blood. 2003;102(3):1087-1096.
20. Stocker JW, De Franceschi L, McNaughton-Smith GA, et al. ICA-17043, a novel Gardos channel blocker, prevents sickled red blood cell dehydration in vitro and in vivo in SAD mice. Blood. 2003;101(6):2412-2418.
21. De Franceschi L, Saadane N, Trudel M, et al. Treatment with oral clotrimazole blocks Ca(2+)-activated K+ transport and reverses erythrocyte dehydration in transgenic SAD mice. A model for therapy of sickle cell disease. J Clin Invest. 1994;93(4):1670-1676.
22. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226(1):497-509.
23. Siciliano A, Malpeli G, Platt OS, et al. Abnormal modulation of cell protective systems in response to ischemic/reperfusion injury is important in the development of mouse sickle cell hepatopathy. Haematologica. 2011;96(1):24-32.
24. Andolfo I, Alper SL, De Franceschi L, et al. Multiple clinical forms of dehydrated hereditary stomatocytosis arise from mutations in PIEZO 1. Blood. 2013;121(19):3925-3935.
25. De Franceschi L, Platt OS, Malpeli G, et al. Protective effects of phosphodiesterase-4 (PDE-4) inhibition in the early phase of pulmonary arterial hypertension in transgenic sickle cell mice. FASEB J. 2008;22(6):1849-1860.
26. de Franceschi L, Malpeli G, Scarpa A, et al. Protective effects of S-nitrosoalbumin on lung injury induced by hypoxia-reoxygenation in mouse model of sickle cell disease. Am J Physiol Lung Cell Mol Physiol. 2006;291(3):457-465.
27. Kaul DK, Hebbel RP. Hypoxia/reoxygenation causes inflammatory response in transgenic sickle mice but not in normal mice. J Clin Invest. 2000;106(3):411-420.
28. Sabaa N, de Franceschi L, Bonnin P, et al. Endothelin receptor antagonism prevents hypoxia-induced mortality and morbidity in a mouse model of sickle-cell disease. J Clin Invest. 2008;118(5):1924-1933.
29. Osborn L, Hession C, Tizard R, et al. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell. 1989;59(6):1203-1211.
30. Belcher JD, Mahaseth H, Welch TE, et al. Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice. J Clin Invest. 2006;116(3):808-816.
31. Sharma S, Chhibber S, Mohan H, Sharma S. Dietary supplementation with omega-3 polyunsaturated fatty acids ameliorates acute pneumonia induced by Klebsiella pneumoniae in BALB/c mice. Can J Microbiol. 2013;59(7):503-510.
32. Umar S, Nadadur RD, Li J, et al. Intralipid prevents and rescues fatal pulmonary arterial hypertension and right ventricular failure in rats. Hypertension. 2011;58(3):512-518.
33. Berger MM, Rozendal CS, Schieber C, et al. The effect of endothelin-1 on alveolar fluid clearance and pulmonary edema formation in the rat. Anest Analg. 2009;108(1):225-231.
34. Rybicki AC, Benjamin LJ. Increased levels of endothelin-1 in plasma of sickle cell anemia patients. Blood. 1998;92(7):2594-2596.
35. Kitagawa T, Yokoyama Y, Kokuryo T, Nagino M. Protective effects of branchedchain amino acids on hepatic ischemiareperfusion-induced liver injury in rats: a direct attenuation of Küpffer cell activation. Am J Physiol Gastrointest Liver Physiol. 2013;304(4):346-355.
36. Shetty S, Lalor PF, Adams DH. Lymphocyte recruitment to the liver: molecular insights into the pathogenesis of liver injury and hepatitis. Toxicology. 2008;254(3):136-146.
37. Volpes R, Van Den Oord JJ, Desmet VJ. Vascular adhesion molecules in acute and chronic liver inflammation. Hepatology. 1992;15(2):269-275.
38. Vercellotti GM, Khan FB, Nguyen J, et al. Hferritin ferroxidase induces cytoprotective pathways and inhibits microvascular stasis in transgenic sickle mice. Front Pharmacol. 2014;5:79.
39. Billett HH, Fabry ME, Nagel RL. Hemoglobin distribution width: a rapid assessment of dense red cells in the steady state and during painful crisis in sickle cell anemia. J Lab Clin Med. 1988;112(3):339-344.
40. Chihara J, Yamamoto T, Kurachi D, Nakajima S. Soluble ICAM-1 in sputum of patients with bronchial asthma. Lancet. 1994;343(8905):1108.
41. Shibahara S, Muller RM, Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem. 1987;262(27):12889-12892.
42. Chen SW, Park SW, Kim M, et al. Human heat shock protein 27 overexpressing mice are protected against hepatic ischemia and reperfusion injury. Transplantation. 2009;87 (10):1478-1487.
43. Hafez T, Moussa M, Nesim I, et al. The effect of intraportal prostaglandin E1 on adhesion molecule expression, inflammatory modulator function, and histology in canine hepatic ischemia/reperfusion injury. J Surg Res. 2007;138(1):88-99.
44. De Caterina R. n-3 fatty acids in cardiovascular disease. N Engl J Med. 2011;364(25): 2439-2450.
45. Wang Q, Liang X, Wang L, et al. Effect of omega-3 fatty acids supplementation on endothelial function: a meta-analysis of randomized controlled trials. Atherosclerosis. 2012;221(2):536-543.
46. Sampaio AL, Rae GA, Henriques MG. Participation of endogenous endothelins in delayed eosinophil and neutrophil recruitment in mouse pleurisy. Inflamm Res. 2000;49(4):170-176.
47. Scorletti E, Bhatia L, McCormick KG, et al. Effects of purified eicosapentaenoic and docosahexaenoic acids in non-alcoholic fatty liver disease: results from the *WELCOME study. Hepatology. 2014;60(4):1211-1221.
48. Xin W, Wei W, Li X. Effect of fish oil supplementation on fasting vascular endothelial function in humans: a meta-analysis of randomized controlled trials. PloS One. 2012;7(9):46028.
49. Hatzipantelis ES, Pana ZD, Gombakis N, et al. Endothelial activation and inflammation biomarkers in children and adolescents with sickle cell disease. Int J Hematol. 2013;98(2):158-163.
50. Belcher JD, Mahaseth H, Welch TE, et al. Critical role of endothelial cell activation in hypoxia-induced vasoocclusion in transgenic sickle mice. Am J Physiol Heart Circ Physiol. 2005;288(6):H2715-2725.
51. Ott J, Hiesgen C, Mayer K. Lipids in critical care medicine. Prostaglandins Leukot Essent Fatty Acids. 2011;85(5):267-273.
52. Kato GJ, Martyr S, Blackwelder WC, et al. Levels of soluble endothelium-derived adhesion molecules in patients with sickle cell disease are associated with pulmonary hypertension, organ dysfunction, and mortality. Br J Haematol. 2005;130(6):943-953.
53. Elmariah H, Garrett ME, De Castro LM, et al. Factors associated with survival in a contemporary adult sickle cell disease cohort. Am J Hematol. 2014;89(5):530-535.
54. Desai AA, Patel AR, Ahmad H, et al. Mechanistic insights and characterization of sickle cell disease-associated cardiomyopathy. Circ Cardiovasc Imaging. 2014;7(3):430-437.
55. Junqueira FP, Fernandes JL, Cunha GM, et al. Right and left ventricular function and myocardial scarring in adult patients with sickle cell disease: a comprehensive magnetic resonance assessment of hepatic and myocardial iron overload. J Cardiovasc Magn Reson. 2013;15:83.
56. Dimitrow PP, Undas A, Wolkow P, Tracz W, Dubiel JS. Enhanced oxidative stress in hypertrophic cardiomyopathy. Pharmacol Rep. 2009;61(3):491-495.
57. Wang Q, Zheng X, Cheng Y, et al. Resolvin D1 stimulates alveolar fluid clearance through alveolar epithelial sodium channel, Na,K-ATPase via ALX/cAMP/PI3K pathway in lipopolysaccharide-induced acute lung injury. J Immunol. 2014;192(8):3765-3777.
58. El Kebir D, Gjorstrup P, Filep JG. Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation. Proc Nat Acad Sci USA. 2012;109(37):14983-14988.
59. Wandersee NJ HM, Maciaszek JL, Larson MC, et al. Dietary supplememntation with Docosahexanoic acid (DHA) improves RBC flexibility and reduces cold hypersensitivity in mice with sickle cell disease. ASH; 2012; 2012:2116.
60. Setty BN, Chen D, Stuart MJ. Sickle red blood cells stimulate endothelial cell production of eicosanoids and diacylglycerol. J Lab Clin Med. 1996;128(3):313-321.
61. Ha T, Li Y, Hua F, Ma J, Gao X, Kelley J, et al. Reduced cardiac hypertrophy in toll-like receptor 4-deficient mice following pressure overload. Cardiovasc Res. 2005;68(2):224-234.