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Docosahexaenoic acid slows inflammation resolution and impairs the quality of healed skin tissue

Docosahexaenoic acid slows inflammation resolution and impairs the quality of healed skin tissue
Docosahexaenoic acid slows inflammation resolution and impairs the quality of healed skin tissue
There is no consensus on the effects of omega-3 (ω-3) fatty acids (FA) on cutaneous repair. To solve this problem, we used 2 different approaches: 1) FAT-1 transgenic mice, capable of producing endogenous ω-3 FA; 2) wild-type (WT) mice orally supplemented with DHA-enriched fish oil. FAT-1 mice had higher systemic (serum) and local (skin tissue) ω-3 FA levels, mainly docosahexaenoic acid (DHA), in comparison to WT mice. FAT-1 mice had increased myeloperoxidase (MPO) activity and content of CXCL-1 and CXCL-2, and reduced IL-10 in the skin wound tissue three days after the wound induction. Inflammation was maintained by an elevated TNF-α concentration and presence of inflammatory cells and edema. Neutrophils and macrophages isolated from FAT-1 mice, also produced increased TNF-α and reduced IL-10 levels. In these mice, the wound closure was delayed, with a wound area 6-fold bigger in relation with WT group, on the last day of analysis (14 days post-wounding). This was associated with poor orientation of collagen fibers and structural aspects in repaired tissue. Similarly, DHA group had a delay during late inflammatory phase. This group had increased TNF-α content and CD45+F4/80+ cells at the 3rd day after skin wounding and increased concentrations of important metabolites derived from ω-3, like 18-HEPE and reduced concentrations of those from ω-6 FA. In conclusion, elevated DHA content, achieved in both FAT-1 and DHA groups, slowed inflammation resolution and impaired the quality of healed skin tissue.
2345-2360
Candreva, Thamiris
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Kühl, Carolina M.C.
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Burger, Beatriz
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dos Anjos, Mariah B.P.
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Torsoni, Márcio A.
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Consonni, Sílvio R.
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Crisma, Amanda R.
a1beda0c-360d-45ea-8965-8dd507d7cdcb
Fisk, Helena
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Calder, Philip
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de Mato, Felipe C.P.
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Sernaglia, Erica M.
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Vinolo, Marco A.R.
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Rodrigues, Hosana G.
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Candreva, Thamiris
b97d98d9-d4a6-498a-8e2d-8df83ee4e267
Kühl, Carolina M.C.
239b8b0a-f7a1-4dc8-a741-c205c0ba0db5
Burger, Beatriz
a193f3d2-b83e-4a8e-89f6-bd662d402e10
dos Anjos, Mariah B.P.
5a09182c-21d3-4d8f-90bf-4fca767bb0bf
Torsoni, Márcio A.
5dbdb79e-18e0-4844-bcb7-966b65bd352e
Consonni, Sílvio R.
15e67477-0958-4f23-a30e-a6f38f9c0b69
Crisma, Amanda R.
a1beda0c-360d-45ea-8965-8dd507d7cdcb
Fisk, Helena
2483d346-75dd-41b3-a481-10f8bb39cd9f
Calder, Philip
1797e54f-378e-4dcb-80a4-3e30018f07a6
de Mato, Felipe C.P.
60c182fe-73fe-4d08-9d33-06e97de7cd78
Sernaglia, Erica M.
91432d1e-dc4a-44ae-8089-0e911d40e83b
Vinolo, Marco A.R.
a27391c3-d908-40ba-bd6b-443a10c028dd
Rodrigues, Hosana G.
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Candreva, Thamiris, Kühl, Carolina M.C., Burger, Beatriz, dos Anjos, Mariah B.P., Torsoni, Márcio A., Consonni, Sílvio R., Crisma, Amanda R., Fisk, Helena, Calder, Philip, de Mato, Felipe C.P., Sernaglia, Erica M., Vinolo, Marco A.R. and Rodrigues, Hosana G. (2019) Docosahexaenoic acid slows inflammation resolution and impairs the quality of healed skin tissue. Clinical Sciences, 133 (22), 2345-2360, [CS20190753]. (doi:10.1042/CS20190753).

Record type: Article

Abstract

There is no consensus on the effects of omega-3 (ω-3) fatty acids (FA) on cutaneous repair. To solve this problem, we used 2 different approaches: 1) FAT-1 transgenic mice, capable of producing endogenous ω-3 FA; 2) wild-type (WT) mice orally supplemented with DHA-enriched fish oil. FAT-1 mice had higher systemic (serum) and local (skin tissue) ω-3 FA levels, mainly docosahexaenoic acid (DHA), in comparison to WT mice. FAT-1 mice had increased myeloperoxidase (MPO) activity and content of CXCL-1 and CXCL-2, and reduced IL-10 in the skin wound tissue three days after the wound induction. Inflammation was maintained by an elevated TNF-α concentration and presence of inflammatory cells and edema. Neutrophils and macrophages isolated from FAT-1 mice, also produced increased TNF-α and reduced IL-10 levels. In these mice, the wound closure was delayed, with a wound area 6-fold bigger in relation with WT group, on the last day of analysis (14 days post-wounding). This was associated with poor orientation of collagen fibers and structural aspects in repaired tissue. Similarly, DHA group had a delay during late inflammatory phase. This group had increased TNF-α content and CD45+F4/80+ cells at the 3rd day after skin wounding and increased concentrations of important metabolites derived from ω-3, like 18-HEPE and reduced concentrations of those from ω-6 FA. In conclusion, elevated DHA content, achieved in both FAT-1 and DHA groups, slowed inflammation resolution and impaired the quality of healed skin tissue.

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Accepted/In Press date: 13 November 2019
e-pub ahead of print date: 13 November 2019
Published date: 29 November 2019

Identifiers

Local EPrints ID: 435904
URI: http://eprints.soton.ac.uk/id/eprint/435904
PURE UUID: eff44aaf-0d1f-42ae-bb4b-e14579340d8f
ORCID for Helena Fisk: ORCID iD orcid.org/0000-0002-9534-3246
ORCID for Philip Calder: ORCID iD orcid.org/0000-0002-6038-710X

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Date deposited: 22 Nov 2019 17:30
Last modified: 26 Nov 2021 02:59

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Contributors

Author: Thamiris Candreva
Author: Carolina M.C. Kühl
Author: Beatriz Burger
Author: Mariah B.P. dos Anjos
Author: Márcio A. Torsoni
Author: Sílvio R. Consonni
Author: Amanda R. Crisma
Author: Helena Fisk ORCID iD
Author: Philip Calder ORCID iD
Author: Felipe C.P. de Mato
Author: Erica M. Sernaglia
Author: Marco A.R. Vinolo
Author: Hosana G. Rodrigues

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