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Maternal diet supplementation with high-docosahexaenoic-acid canola oil, along with arachidonic acid, promotes immune system development in allergy-prone BALB/c mouse offspring at 3 weeks of age

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A Correction to this article was published on 17 October 2023

This article has been updated

Abstract

Purpose

To study the effects of feeding docosahexaenoic acid (DHA, derived from novel canola oil), with same amount of arachidonic acid (ARA), supplemented diet to lactating dams on the immune system development of suckled offspring using a T helper type-2 (Th2)-dominant BALB/c mouse.

Methods

Dams received nutritionally complete control (no ARA or DHA) or DHA + ARA diet (1% DHA and 1% ARA of total fatty acids) from 5 days pre-parturition to the end of 3-week suckling period. After euthanization, relevant tissues were collected to study fatty acids, splenocyte phenotype and function (ex vivo cytokines with/without lipopolysaccharide (LPS, bacterial challenge) or phorbol myristate acetate + ionomycin (PMAi) stimulation).

Results

Feeding dams a DHA diet significantly increased the mammary gland milk phospholipid concentration of DHA and ARA. This resulted in 60% higher DHA levels in splenocyte phospholipids of the pups although ARA levels showed no difference. In dams fed DHA diet, significantly higher proportion of CD27+ cytotoxic T cell (CTL) and CXCR3+ CCR6- Th (enriched in Th1) were observed than control, but there were no differences in the splenocyte function upon PMAi (non-specific lymphocyte stimulant) stimulation. Pups from DHA-fed dams showed significantly higher IL-1β, IFN-γ and TNF-α (inflammatory cytokines) by LPS-stimulated splenocytes. This may be due to higher proportion of CD86+ macrophages and B cells (all p’s < 0.05) in these pups, which may influence T cell polarization.

Conclusion

Plant-based source of DHA in maternal diet resulted in higher ex vivo production of inflammatory cytokines by splenocytes due to change in their phenotype, and this can skew T cell towards Th1 response in a Th2-dominant BALB/c mouse.

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Data availability

The data underlying this article will be shared on reasonable request to the corresponding author.

Change history

Abbreviations

DHA:

Docosahexaenoic acid

ARA:

Arachidonic acid

ALA:

Alpha-linolenic acid

LA:

Linoleic acid

Th2:

T helper type-2

LCPUFA:

Long-chain polyunsaturated fatty acid

CD:

Cluster of differentiation

NK:

Natural killer

TNF-α:

Tumour necrosis factor-alpha

IFN-γ:

Interferon-gamma

IL:

Interleukin

CXCL1:

C-X-C motif ligand-1

CTLA-4:

Cytotoxic T lymphocyte-associated protein 4

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Acknowledgements

We would like to thank Nuseed for providing the DHA-enriched canola and DSM for providing the ARAsco oils used in preparing the animal diets. The authors would like to express gratitude towards help received from everyone involved in the completion of the project. Stephanie Tollenaar helped with animal care and handling. The summer students João Vitor Wagner and Alan Liang assistant with tissue collection, processing and laboratory procedures. Senior laboratory members Dr. Jessy Azarcoya and Dr. Marnie Newell provided technical assistance and analysis throughout the project.

Funding

This study was funded by Natural Sciences and Engineering Research Council discovery grant (NSERC RGPIN-2017-04746) to CJF and a grant from the Alberta Canola Producers Commission. DP has received scholarships from AGES ALES University of Alberta. DP has also received awards from GSS Government of Alberta and the 2020 Fisher Scientific Graduate Scholarship for scholarly achievements.

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Authors and Affiliations

  1. Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada

    Dhruvesh Patel, Jaqueline Munhoz, Susan Goruk, Caroline Richard & Catherine J. Field

  2. Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB, Canada

    Sue Tsai

Authors
  1. Dhruvesh Patel
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  2. Jaqueline Munhoz
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  3. Susan Goruk
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  4. Sue Tsai
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  5. Caroline Richard
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  6. Catherine J. Field
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Contributions

DP, SG, CR and CJF designed the study. DP, SG and JM conducted the research and analysed data. DP performed the statistical analysis and drafted the manuscript with the supervision of CJF, CR and ST. CJF has main responsibility for the final draft. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Catherine J. Field.

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Conflict of interest

The authors declare no competing interests in relation to the study.

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Patel, D., Munhoz, J., Goruk, S. et al. Maternal diet supplementation with high-docosahexaenoic-acid canola oil, along with arachidonic acid, promotes immune system development in allergy-prone BALB/c mouse offspring at 3 weeks of age. Eur J Nutr 62, 2399–2413 (2023). https://doi.org/10.1007/s00394-023-03160-6

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