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Omega-3 long-chain polyunsaturated fatty acids promote antibacterial and inflammation-resolving effects in Mycobacterium tuberculosis-infected C3HeB/FeJ mice, dependent on fatty acid status

Published online by Cambridge University Press:  05 April 2021

Arista Nienaber
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531
Mumin Ozturk
Affiliation:
International Centre for Genetic Engineering and Biotechnology (ICGEB), Cape Town-Component, University of Cape Town, Cape Town, Western Cape, South Africa, 7925 Institute of Infectious Diseases and Molecular Medicine (IDM), Division of Immunology and South African Medical Research Council (SAMRC) Immunology of Infectious Diseases, University of Cape Town, Cape Town, Western Cape, South Africa, 7925
Robin C. Dolman
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531
Renee Blaauw
Affiliation:
Division of Human Nutrition, Stellenbosch University, Tygerberg, Cape Town, Western Cape, South Africa, 7505
Lizelle Zandberg
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531
Simone King
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531
Melinda Britz
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531
Frank E.A. Hayford
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531 Department of Nutrition and Dietetics, University of Ghana, Accra, Ghana
Frank Brombacher
Affiliation:
International Centre for Genetic Engineering and Biotechnology (ICGEB), Cape Town-Component, University of Cape Town, Cape Town, Western Cape, South Africa, 7925 Institute of Infectious Diseases and Molecular Medicine (IDM), Division of Immunology and South African Medical Research Council (SAMRC) Immunology of Infectious Diseases, University of Cape Town, Cape Town, Western Cape, South Africa, 7925 Wellcome Centre for Infectious Diseases Research in Africa (CIDRI-Africa), Institute of Infectious Diseases and Molecular Medicine (IDM), University of Cape Town, Cape Town, Western Cape, South Africa, 7925
Du Toit Loots
Affiliation:
Human Metabolomics, Faculty of Natural and Agricultural Sciences, North-West University, Potchefstroom, North West, South Africa, 2531
Cornelius M. Smuts
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531
Suraj P. Parihar
Affiliation:
International Centre for Genetic Engineering and Biotechnology (ICGEB), Cape Town-Component, University of Cape Town, Cape Town, Western Cape, South Africa, 7925 Institute of Infectious Diseases and Molecular Medicine (IDM), Division of Immunology and South African Medical Research Council (SAMRC) Immunology of Infectious Diseases, University of Cape Town, Cape Town, Western Cape, South Africa, 7925 Wellcome Centre for Infectious Diseases Research in Africa (CIDRI-Africa), Institute of Infectious Diseases and Molecular Medicine (IDM), University of Cape Town, Cape Town, Western Cape, South Africa, 7925 Division of Medical Microbiology, Department of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, Western Cape, South Africa, 7925
Linda Malan
Affiliation:
Centre of Excellence for Nutrition, North-West University, Potchefstroom, North West, South Africa, 2531
Corresponding
E-mail address:
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Abstract

Non-resolving inflammation is characteristic of tuberculosis (TB). Given their inflammation-resolving properties, omega-3 long-chain polyunsaturated fatty acids (n-3 LCPUFA) may support TB treatment. This research aimed to investigate the effects of n-3 LCPUFA on clinical and inflammatory outcomes of Mycobacterium tuberculosis (Mtb)-infected C3HeB/FeJ mice with either normal or low n-3 PUFA status before infection. Using a two-by-two design, uninfected mice were conditioned on either an n-3 PUFA-sufficient (n-3FAS) or -deficient (n3FAD) diet for six weeks. One week post-infection, mice were randomised to either n-3 LCPUFA supplemented (n-3FAS/n-3+ and n3FAD/n3+) or continued on n-3FAS or n3FAD diets for three weeks. Mice were euthanised and fatty acid status, lung bacterial load and pathology, cytokine, lipid mediator, and immune cell phenotype analysed. n-3 LCPUFA supplementation in n-3FAS mice lowered lung bacterial loads (P=0·003), T cells (P=0·019), CD4+ T cells (P=0·014), IFN-γ (P<0·001) and promoted a pro-resolving lung lipid mediator profile. Compared with n-3FAS mice, the n-3FAD group had lower bacterial loads (P=0·037), significantly higher immune cell recruitment and a more pro-inflammatory lipid mediator profile, however, significantly lower lung IFN-γ, IL-1α, IL-1β, and IL-17, and supplementation in the n-3FAD group provided no beneficial effect on lung bacterial load or inflammation. Our study provides the first evidence that n-3 LCPUFA supplementation has antibacterial and inflammation-resolving benefits in TB when provided one week after infection in the context of a sufficient n-3 PUFA status. Whilst a low n-3 PUFA status may promote better bacterial control and lower lung inflammation not benefiting from n-3 LCPUFA supplementation.

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© The Authors 2021.
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Omega-3 long-chain polyunsaturated fatty acids promote antibacterial and inflammation-resolving effects in Mycobacterium tuberculosis-infected C3HeB/FeJ mice, dependent on fatty acid status
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Omega-3 long-chain polyunsaturated fatty acids promote antibacterial and inflammation-resolving effects in Mycobacterium tuberculosis-infected C3HeB/FeJ mice, dependent on fatty acid status
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Omega-3 long-chain polyunsaturated fatty acids promote antibacterial and inflammation-resolving effects in Mycobacterium tuberculosis-infected C3HeB/FeJ mice, dependent on fatty acid status
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