Dietary flaxseed enhances antioxidant defenses and is protective in a mouse model of lung ischemia-reperfusion injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 294, Issue 2, 2008, Pages

  Lee, James C ^a   Bhora, Faiz ^c   Sun, Jing ^a   Cheng, Guanjun ^a   Arguiri, Evguenia ^a   Solomides, Charalambos C ^d   Chatterjee, Shampa ^b   Christofidou Solomidou, Melpo ^a,e  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Ischemia reperfusion injury; Lignans, nuclear factor E2 related factor 2, heme oxygenase 1, phase II enzymes

Indexed keywords

HEME OXYGENASE 1; ISOPROSTANE DERIVATIVE; LIGNAN DERIVATIVE; MALONALDEHYDE; OMEGA 3 FATTY ACID; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTERIAL OXYGEN TENSION; ARTICLE; DETOXIFICATION; DIETARY INTAKE; ENDOTHELIUM CELL; EX VIVO STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; LINSEED; LIPID OXIDATION; LUNG ALVEOLUS MACROPHAGE; LUNG INJURY; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; RESPIRATORY BURST; UPREGULATION; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIOXIDANTS; CELL DEATH; CELLS, CULTURED; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; FLAX; FREE RADICAL SCAVENGERS; HYDROGEN PEROXIDE; LIGNANS; LUNG; MACROPHAGES, ALVEOLAR; MICE; OXIDATIVE STRESS; OXYGEN; PERFUSION; PHYTOTHERAPY; PLANT EXTRACTS; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; RESPIRATORY BURST;

EID: 39149101808     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00138.2007     Document Type: Article

References (51)

1. Appleton SD, Chretien ML, McLaughlin BE, Vreman HJ, Stevenson DK, Brien JF, Nakatsu K, Maurice DH, Marks GS. Selective inhibition of heme oxygenase, without inhibition of nitric oxide synthase or soluble guanylyl cyclase, by metalloporphyrins at low concentrations. Drug Metab Dispos 27: 1214-1219, 1999.
2. Chan K, Kan YW. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci USA 96: 12731-12736, 1999.
3. Chatterjee S, Levitan I, Wei Z, Fisher AB. KATP channels are an important component of the shear-sensing mechanism in the pulmonary microvasculature. Microcirculation 13: 633-644, 2006.
4. Chiu PY, Mak DH, Poon MK, Ko KM. In vivo antioxidant action of a lignan-enriched extract of Schisandra fruit and an anthraquinone- containing extract of Polygonum root in comparison with schisandrin B and emodin. Planta Med 68: 951-956, 2002.
5. Cho HY, Jedlicka AE, Reddy SPM, Kensler TW, Yamamoto M, Zhang LY, Kleeberger SR. Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol 26: 175-182, 2002.
6. Cho HY, Jedlicka AE, Reddy SPM, Zhang LY, Kensler TW, Kleeberger SR. Linkage analysis of susceptibility to hyperoxia. Nrf2 is a candidate gene. Am J Respir Cell Mol Biol 26: 42-51, 2002.
7. Choi AM, Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15: 9-19, 1996.
8. Christie JD, Carby M, Bag R, Corris P, Hertz M, Weill D. Report of the ISHLT Working Group on Primary Lung Graft Dysfunction part II: definition. A consensus statement of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 24: 1454-1459, 2005.
9. Christofidou-Solomidou M, AS, Wiewrodt RSC, Ng KAE, TS, SMA, VRM. PECAM-1-directed immunotargeting of catalase protects pulmonary endothelium against oxidative stress in mice. Am J Physiol Lung Cell Mol Physiol 285: L283-L292, 2003.
10. Christofidou-Solomidou M, Muzykantov VR. Antioxidant strategies in respiratory medicine. Treat Respir Med 5: 47-78, 2006.
11. Christofidou-Solomidou M, Scherpereel A, Wiewrodt R, Ng K, Sweitzer T, Arguiri E, Shuvaev V, Solomides CC, Albelda SM, Muzykantov VR. PECAM-directed delivery of catalase to endothelium protects against pulmonary vascular oxidative stress. Am J Physiol Lung Cell Mol Physiol 285: L283-L292, 2003.
12. Datla SR, Dusting GJ, Mori TA, Taylor CJ, Croft KD, Jiang F. Induction of heme oxygenase-1 in vivo suppresses NADPH oxidase derived oxidative stress. Hypertension 50: 636-642, 2007.
13. De Perrot M, Liu M, Waddell TK, Keshavjee S. Ischemia-reperfusion- induced lung injury. Am J Respir Crit Care Med 167: 490-511, 2003.
14. Eppinger MJ, Deeb GM, Bolling SF, Ward PA. Mediators of ischemia-reperfusion injury of rat lung. Am J Pathol 150: 1773-1784, 1997.
15. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11: 81-128, 1991.
16. Fisher AB, Arad I, Dodia C, Chander A, Feinstein SI. cAMP increases synthesis of surfactant-associated protein A by perfused rat lung. Am J Physiol Lung Cell Mol Physiol 260: L226-L233, 1991.
17. Gadek JE, DeMichele SJ, Karlstad MD, Pacht ER, Donahoe M, Albertson TE, Van Hoozen C, Wennberg AK, Nelson JL, Noursalehi M. Effect of enteral feeding with eicosapentaenoic acid, gamma-linolenic acid, and antioxidants in patients with acute respiratory distress syndrome. Enteral Nutrition in ARDS Study Group. Crit Care Med 27: 1409-1420, 1999.
18. Geuken E, Buis CI, Visser DS, Blokzijl H, Moshage H, Nemes B, Leuvenink HG, de Jong KP, Peeters PM, Slooff MJ, Porte RJ. Expression of heme oxygenase-1 in human livers before transplantation correlates with graft injury and function after transplantation. Am J Transplant 5: 1875-1885, 2005.
19. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501, 2000.
20. Halliwell B, Gutteridge JMC, Cross CE. Free radical, antioxidants and human disease: where are we now? Reactive oxygen species and human disease. J Lab Clin Med 119: 598-620, 1992.
21. Hu G, Cassano PA. Antioxidant nutrients and pulmonary function: the third national health and nutrition examination survey (NHANES III). Am J Epidemiol 151: 975-981, 2000.
22. Ikeda S, Kagaya M, Kobayashi K, Tohyama T, Kiso Y, Higuchi N, Yamashita K. Dietary sesame lignans decrease lipid peroxidation in rats fed docosahexaenoic acid. J Nutr Sci Vitaminol (Tokyo) 49: 270-276, 2003.
23. Ikeda T, Nishijima Y, Shibata H, Kiso Y, Ohnuki K, Fushiki T, Moritani T. Protective effect of sesamin administration on exercise-induced lipid peroxidation. Int J Sports Med 24: 530-534, 2003.
24. Kinniry P, Amrani Y, Vachani A, Solomides CC, Arguiri E, Workman A, Carter J, Christofidou-Solomidou M. Dietary flaxseed supplementation ameliorates inflammation and oxidative tissue damage in experimental models of acute lung injury in mice. J Nutr 136: 1545-1551, 2006.
25. 4-surfactant prevents hyperoxic and LPS-induced lung injury in mice. Pediatr Pulmonol 41: 916-928, 2006.
26. Kitts DD, Yuan YV, Wijewickreme AN, Thompson LU. Antioxidant activity of the flaxseed lignan secoisolariciresinol diglycoside and its mammalian lignan metabolites enterodiol and enterolactone. Mol Cell Biochem 202: 91-100, 1999.
27. Korzeniewski C, Callewaert DM. An enzyme-release assay for natural cytotoxicity. J Immunol Methods 64: 313-320, 1983.
28. Kris-Etherton PM, Harris WS, Appel LJ. Omega-3 fatty acids and cardiovascular disease: new recommendations from the American Heart Association. Arterioscler Thromb Vasc Biol 23: 151-152, 2003.
29. Kris-Etherton PM, Lichtenstein AH, Howard BV, Steinberg D, Witztum JL. Antioxidant vitamin supplements and cardiovascular disease. Circulation 110: 637-641, 2004.
30. Lee-Hilz YY, Boerboom AM, Westphal AH, Berkel WJ, Aarts JM, Rietjens IM. Pro-oxidant activity of flavonoids induces EpRE-mediated gene expression. Chem Res Toxicol 19: 1499-1505, 2006.
31. Leonard MO, Kieran NE, Howell K, Burne MJ, Varadarajan R, Dhakshinamoorthy S, Porter AG, O'Farrelly C, Rabb H, Taylor CT. Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. FASEB J 20: 2624-2626, 2006.
32. MacDonald-Wicks LK, Garg ML. Modulation of carbon tetrachloride-induced oxidative stress by dietary fat in rats. J Nutr Biochem 13: 87-95, 2002.
33. Matsuzaki I, Chatterjee S, Debolt K, Manevich Y, Zhang Q, Fisher AB. Membrane depolarization and NADPH oxidase activation in aortic endothelium during ischemia reflect altered mechanotransduction. Am J Physiol Heart Circ Physiol 288: H336-H343, 2005.
34. Metnitz PG, Bartens C, Fischer M, Fridrich P, Steltzer H, Druml W. Antioxidant status in patients with acute respiratory distress syndrome. Intensive Care Med 25: 180-185, 1999.
35. Nesbitt PD, Lam Y, Thompson LU. Human metabolism of mammalian lignan precursors in raw and processed flaxseed. Am J Clin Nutr 69: 549-555, 1999.
36. Pacht ER, DeMichele SJ, Nelson JL, Hart J, Wennberg AK, Gadek JE. Enteral nutrition with eicosapentaenoic acid, gamma-linolenic acid, and antioxidants reduces alveolar inflammatory mediators and protein influx in patients with acute respiratory distress syndrome. Crit Care Med 31: 491-500, 2003.
37. Pattanaik U, Prasad K. Oxygen free radicals and endotoxic shock: effect of flaxseed. J Cardiovasc Pharmacol Ther 3: 305-318, 1998.
38. Prasad K. Antioxidant activity of secoisolariciresinol diglucoside-derived metabolites, secoisolariciresinol, enterodiol, and enterolactone. Int J Angiol 9: 220-225, 2000.
39. Prasad K. Hydroxyl radical-scavenging property of secoisolariciresinol diglucoside (SDG) isolated from flax-seed. Mol Cell Biochem 168: 117-123, 1997.
40. Prasad K. Secoisolariciresinol diglucoside from flaxseed delays the development of type 2 diabetes in Zucker rat. J Lab Clin Med 138: 32-39, 2001.
41. Reeves PG, Nielsen FH, Fahey GC Jr. 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 123: 1939-1951, 1993.
42. Ritz SA, Wan J, Diaz-Sanchez D. Sulforaphane-stimulated phase II enzyme induction inhibits cytokine production by airway epithelial cells stimulated with diesel extract. Am J Physiol Lung Cell Mol Physiol 292: L33-L39, 2007.
43. Romieu I, Sienra-Monge JJ, Ramirez-Aguilar M, Tellez-Rojo MM, Moreno-Macias H, Reyes-Ruiz NI, del Rio-Navarro BE, Ruiz-Navarro MX, Hatch G, Slade R, Hernandez-Avila M. Antioxidant supplementation and lung functions among children with asthma exposed to high levels of air pollutants. Am J Respir Crit Care Med 166: 703-709, 2002.
44. Scapagnini G, Colombrita C, Amadio M, D'Agata V, Arcelli E, Sapienza M, Quattrone A, Calabrese V. Curcumin activates defensive genes and protects neurons against oxidative stress. Antioxid Redox Signal 8: 395-403, 2006.
45. Simopoulos AP. Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr 21: 495-505, 2002.
46. Struijs K, Vincken JP, Verhoef R, van Oostveen-van Casteren WH, Voragen AG, Gruppen H. The flavonoid herbacetin diglucoside as a constituent of the lignan macromolecule from flaxseed hulls. Phytochemistry 68: 1227-1235, 2007.
47. Tliba O, Tliba S, Da Huang C, Hoffman RK, DeLong P, Panettieri RA Jr, Amrani Y. Tumor necrosis factor alpha modulates airway smooth muscle function via the autocrine action of interferon beta. J Biol Chem 278: 50615-50623, 2003.
48. Ueda M, Fuchs S, Nakamura T, Schafer UF, Lehr CM, Menger MD, Schafers HJ. Reoxygenation results in cell death of human alveolar epithelial cells. J Heart Lung Transplant 23: 1198-1204, 2004.
49. Xue JY, Liu GT, Wei HL, Pan Y. Antioxidant activity of two dibenzocyclooctene lignans on the aged and ischemic brain in rats. Free Radic Biol Med 12: 127-135, 1992.
50. Yamashita K, Ollinger R, McDaid J, Sakahama H, Wang H, Tyagi S, Csizmadia E, Smith NR, Soares MP, Bach FH. Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs. FASEB J 20: 776-778, 2006.
51. ATP channel dependent. Am J Physiol Lung Cell Mol Physiol 289: L954-L961, 2005.