Dietary supplementation of ω-3 fatty acid-containing fish oil suppresses F2-isoprostanes but enhances inflammatory cytokine response in a mouse model of ovalbumin-induced allergic lung inflammation

Huiyong Yin; Wei Liu; Kasia Goleniewska; Ned A. Porter; Jason D. Morrow; R. Stokes Peebles Jr.

doi:10.1016/j.freeradbiomed.2009.05.033

Dietary supplementation of ω-3 fatty acid-containing fish oil suppresses F₂-isoprostanes but enhances inflammatory cytokine response in a mouse model of ovalbumin-induced allergic lung inflammation

Huiyong Yin
, Wei Liu
, Kasia Goleniewska
, Ned A. Porter
, Jason D. Morrow
, R. Stokes Peebles Jr.

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

54 Citations (Scopus)

Abstract

Epidemiological and clinical evidence has suggested that increased dietary intake of fish oil containing ω-3 fatty acids including eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) may be associated with a reduced risk of asthma. However, interventional studies on these effects have been equivocal and controversial. Free radical oxidation products of lipids and cyclooxygenases-derived prostaglandins are believed to play an important role in asthma, and fish oil supplementation may modulate the levels of these critical lipid mediators. We employed a murine model of allergic inflammation produced by sensitization to ovalbumin (OVA) to study the effects of fish oil supplementation on airway inflammation. Our studies demonstrated that ω-3 fatty acids were dose dependently incorporated into mouse lung tissue after dietary supplementation. We examined the oxidative stress status by measuring the levels of isoprostanes (IsoPs), the gold standard for oxidative stress in vivo. OVA challenge caused significant increase of F₂-IsoPs in mouse lung, suggesting an elevated level of oxidative stress. Compared to the control group, fish oil supplementation led to a significant reduction of F₂-IsoP (from arachidonic acid) with a concomitant increase of F₃-IsoPs (from EPA) and F₄-IsoPs (from DHA). Surprisingly, however, fish oil supplementation enhanced production of proinflammatory cytokine IL-5 and IL-13. Furthermore, fish oil supplementation suppressed the production of pulmonary protective PGE₂ in the bronchoalveolar lavage (BAL) while the level of urinary metabolites of the PGE₂ was increased. Our data suggest that augmented lung inflammation after fish oil supplementation may be due to the reduction of PGE₂ production in the lung and these dichotomous results bring into question the role of fish oil supplementation in the treatment of asthma. © 2009 Elsevier Inc. All rights reserved.

Original language	English
Pages (from-to)	622-628
Journal	Free Radical Biology and Medicine
Volume	47
Issue number	5
DOIs	https://doi.org/10.1016/j.freeradbiomed.2009.05.033
Publication status	Published - 1 Sept 2009
Externally published	Yes

Bibliographical note

Publication details (e.g. title, author(s), publication statuses and dates) are captured on an “AS IS” and “AS AVAILABLE” basis at the time of record harvesting from the data source. Suggestions for further amendments or supplementary information can be sent to [email protected].

Funding

This work is supported by a pilot grant from Center in Molecular Toxicology, Vanderbilt University (P30 ES00267), and NIH Grants DK48831, ES13125, and GM15431. We thank Drs. David Hachey, Wade Calcutt, and Mrs. Dawn Overstreet of the Mass Spectrometry Research Center of Vanderbilt University for their assistance with the MS analysis. The PGE-M analysis was carried out with the help of the Eicosanoid Core at Vanderbilt University. We gratefully acknowledge the discussion with Drs. Weisong Zhou and Ryszard Dworski at Vanderbilt University. This manuscript is dedicated to the memory of Dr. Jason Morrow.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Research Keywords

ω-3 Polyunsaturated fatty acids
Asthma
Fish oil
Free radicals
Isoprostanes
Lung inflammation
Mass spectrometry
Ovalbumin (OVA)
Prostaglandins

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Cite this

Yin, H., Liu, W., Goleniewska, K., Porter, N. A., Morrow, J. D., & Peebles Jr., R. S. (2009). Dietary supplementation of ω-3 fatty acid-containing fish oil suppresses F₂-isoprostanes but enhances inflammatory cytokine response in a mouse model of ovalbumin-induced allergic lung inflammation. Free Radical Biology and Medicine, 47(5), 622-628. https://doi.org/10.1016/j.freeradbiomed.2009.05.033

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title = "Dietary supplementation of ω-3 fatty acid-containing fish oil suppresses F2-isoprostanes but enhances inflammatory cytokine response in a mouse model of ovalbumin-induced allergic lung inflammation",

abstract = "Epidemiological and clinical evidence has suggested that increased dietary intake of fish oil containing ω-3 fatty acids including eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) may be associated with a reduced risk of asthma. However, interventional studies on these effects have been equivocal and controversial. Free radical oxidation products of lipids and cyclooxygenases-derived prostaglandins are believed to play an important role in asthma, and fish oil supplementation may modulate the levels of these critical lipid mediators. We employed a murine model of allergic inflammation produced by sensitization to ovalbumin (OVA) to study the effects of fish oil supplementation on airway inflammation. Our studies demonstrated that ω-3 fatty acids were dose dependently incorporated into mouse lung tissue after dietary supplementation. We examined the oxidative stress status by measuring the levels of isoprostanes (IsoPs), the gold standard for oxidative stress in vivo. OVA challenge caused significant increase of F2-IsoPs in mouse lung, suggesting an elevated level of oxidative stress. Compared to the control group, fish oil supplementation led to a significant reduction of F2-IsoP (from arachidonic acid) with a concomitant increase of F3-IsoPs (from EPA) and F4-IsoPs (from DHA). Surprisingly, however, fish oil supplementation enhanced production of proinflammatory cytokine IL-5 and IL-13. Furthermore, fish oil supplementation suppressed the production of pulmonary protective PGE2 in the bronchoalveolar lavage (BAL) while the level of urinary metabolites of the PGE2 was increased. Our data suggest that augmented lung inflammation after fish oil supplementation may be due to the reduction of PGE2 production in the lung and these dichotomous results bring into question the role of fish oil supplementation in the treatment of asthma. {\textcopyright} 2009 Elsevier Inc. All rights reserved.",

keywords = "ω-3 Polyunsaturated fatty acids, Asthma, Fish oil, Free radicals, Isoprostanes, Lung inflammation, Mass spectrometry, Ovalbumin (OVA), Prostaglandins",

author = "Huiyong Yin and Wei Liu and Kasia Goleniewska and Porter, \{Ned A.\} and Morrow, \{Jason D.\} and \{Peebles Jr.\}, \{R. Stokes\}",

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Yin, H, Liu, W, Goleniewska, K, Porter, NA, Morrow, JD & Peebles Jr., RS 2009, 'Dietary supplementation of ω-3 fatty acid-containing fish oil suppresses F₂-isoprostanes but enhances inflammatory cytokine response in a mouse model of ovalbumin-induced allergic lung inflammation', Free Radical Biology and Medicine, vol. 47, no. 5, pp. 622-628. https://doi.org/10.1016/j.freeradbiomed.2009.05.033

Dietary supplementation of ω-3 fatty acid-containing fish oil suppresses F₂-isoprostanes but enhances inflammatory cytokine response in a mouse model of ovalbumin-induced allergic lung inflammation. / Yin, Huiyong; Liu, Wei; Goleniewska, Kasia et al.
In: Free Radical Biology and Medicine, Vol. 47, No. 5, 01.09.2009, p. 622-628.

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

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AU - Yin, Huiyong

AU - Liu, Wei

AU - Goleniewska, Kasia

AU - Porter, Ned A.

AU - Morrow, Jason D.

AU - Peebles Jr., R. Stokes

N1 - Publication details (e.g. title, author(s), publication statuses and dates) are captured on an “AS IS” and “AS AVAILABLE” basis at the time of record harvesting from the data source. Suggestions for further amendments or supplementary information can be sent to [email protected].

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AB - Epidemiological and clinical evidence has suggested that increased dietary intake of fish oil containing ω-3 fatty acids including eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) may be associated with a reduced risk of asthma. However, interventional studies on these effects have been equivocal and controversial. Free radical oxidation products of lipids and cyclooxygenases-derived prostaglandins are believed to play an important role in asthma, and fish oil supplementation may modulate the levels of these critical lipid mediators. We employed a murine model of allergic inflammation produced by sensitization to ovalbumin (OVA) to study the effects of fish oil supplementation on airway inflammation. Our studies demonstrated that ω-3 fatty acids were dose dependently incorporated into mouse lung tissue after dietary supplementation. We examined the oxidative stress status by measuring the levels of isoprostanes (IsoPs), the gold standard for oxidative stress in vivo. OVA challenge caused significant increase of F2-IsoPs in mouse lung, suggesting an elevated level of oxidative stress. Compared to the control group, fish oil supplementation led to a significant reduction of F2-IsoP (from arachidonic acid) with a concomitant increase of F3-IsoPs (from EPA) and F4-IsoPs (from DHA). Surprisingly, however, fish oil supplementation enhanced production of proinflammatory cytokine IL-5 and IL-13. Furthermore, fish oil supplementation suppressed the production of pulmonary protective PGE2 in the bronchoalveolar lavage (BAL) while the level of urinary metabolites of the PGE2 was increased. Our data suggest that augmented lung inflammation after fish oil supplementation may be due to the reduction of PGE2 production in the lung and these dichotomous results bring into question the role of fish oil supplementation in the treatment of asthma. © 2009 Elsevier Inc. All rights reserved.

KW - ω-3 Polyunsaturated fatty acids

KW - Asthma

KW - Fish oil

KW - Free radicals

KW - Isoprostanes

KW - Lung inflammation

KW - Mass spectrometry

KW - Ovalbumin (OVA)

KW - Prostaglandins

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