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Buttermilk: an important source of lipid soluble forms of choline that influences the immune system development in Sprague–Dawley rat offspring

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A Correction to this article was published on 17 October 2023

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Abstract

Purpose

To determine the effect of feeding buttermilk-derived choline metabolites on the immune system development in Sprague–Dawley rat pups.

Methods

Sprague–Dawley dams were randomized to one of the three diets containing 1.7 g/kg choline: 1-Control (100% free choline (FC)), 2-Buttermilk (BM, 37% phosphatidylcholine (PC), 34% sphingomyelin (SM), 17% glycerophosphocholine (GPC), 7% FC, 5% phosphocholine), and 3-Placebo (PB, 50% PC, 25% FC, 25% GPC) until the end of the lactation period. At weaning, pups continued on the same diet as their mom. Cell phenotypes and cytokine production by mitogen-stimulated splenocytes isolated from 3- and 10-week-old pups were measured.

Results

At 3 weeks, BM-pups had a higher proportion of cytotoxic T cells (CTL; CD3 + CD8 +) while both BM- and PB-pups had an increased proportion of cells expressing CD28 + , CD86 + and CD27 + (all p > 0.05). Following ConA stimulation, splenocytes from BM- and PB-pups produced more TNF-α and IFN-γ and after LPS stimulation produced more IL-10 and TNF-α (all p > 0.05). Starting at week 6 of age, BM-pups had a higher body weight. At 10 weeks, both the BM- and PB-pups had a higher proportion of CTL expressing CD27 + . After ConA stimulation, splenocytes from BM- and PB-pups produced more IL-2, IFN-γ and IL-6 and more IL-10 after LPS stimulation (all p > 0.05).

Conclusion

The proportion of lipid soluble forms of choline in the diet during lactation and weaning periods influence the immune system development in rat offspring.

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Abbreviations

AA:

Arachidonic acid

ALA:

α-Linolenic acid

APC:

Antigen presenting cells

BM:

Buttermilk diet

ConA:

Concanavalin A

CTL:

Cytotoxic T cells

CTLA-4:

Cytotoxic T lymphocyte associated protein 4

DHA:

Docosahexaenoic acid

DPA:

Docosapentaenoic acid

FC:

Free choline

GALT:

Gut-associated lymphoid tissue

GPC:

Glycerophosphocholine

IFN-γ:

Interferon-gamma

Ig:

Immunoglobulin

IL:

Interleukin

LPS:

Lipopolysaccharide

MFGM:

Milk fat globule membrane

MUFA:

Monounsaturated fatty acid

n:

Omega

OVA:

Ovalbumin

PB:

Placebo diet

PC:

Phosphatidylcholine

Pcho:

Phosphocholine

PRRs:

Pattern recognition receptors

PUFA:

Polyunsaturated fatty acid

SFA:

Saturated fatty acid

SM:

Sphingomyelin

TCR:

T cell receptor

TLR4:

Toll-like receptor 4

TNF-α:

Tumor necrosis factor-alpha

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Acknowledgements

The authors would like to acknowledge the technical assistance of Emily Wadge, Reid Steele, Nicole Coursen and Marnie Newell. We express our gratitude to the undergraduate students that worked on the project.

Funding

This study was supported by a Dairy Farmers of Canada grant and Discovery grants from the Natural Sciences and Engineering Research Council of Canada. JAB is recipient of a PhD CONACYT (Consejo Nacional de Ciencia y Tecnología) scholarship from Mexico.

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Authors and Affiliations

  1. Department of Agricultural, Food and Nutritional Science, Center for Health Research Innovation, University of Alberta, 4-002G Li Ka Shing, Edmonton, AB, T6G 2E1, Canada

    Jessy Azarcoya-Barrera, Catherine J. Field, Susan Goruk, Alexander Makarowski, Jonathan M. Curtis, René L. Jacobs & Caroline Richard

  2. STELA Dairy Research Center, Institute of Nutrition and Functional Foods (INAF), Université Laval, Québec, Canada

    Yves Pouliot

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  1. Jessy Azarcoya-Barrera
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Contributions

CR, CJF, RLJ, YP and JMC designed and obtained funding for this study. SG, AM and JAB conducted research and analyzed data. JAB performed the statistical analysis and wrote the manuscript under the supervision of CR and RLJ. CR and CJF have primary responsibility for final content. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Caroline Richard.

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Azarcoya-Barrera, J., Field, C.J., Goruk, S. et al. Buttermilk: an important source of lipid soluble forms of choline that influences the immune system development in Sprague–Dawley rat offspring. Eur J Nutr 60, 2807–2818 (2021). https://doi.org/10.1007/s00394-020-02462-3

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